Journal of Asia-Paci Fic Entomology: Dale G. Bottrell, Kenneth G. Schoenly

Author's personal copy
Journal of Asia-Pacific Entomology 15 (2012) 122–140
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Journal of Asia-Pacific Entomology

journal homepage: www.elsevier.com/locate/jape
Invited Review
Resurrecting the ghost of green revolutions past: The brown planthopper as a

recurring threat to high-yielding rice production in tropical Asia
Dale G. Bottrell a,⁎, Kenneth G. Schoenly b
a
Department of Entomology, University of Maryland, College Park, Maryland 20742, USA
b
Department of Biological Sciences, California State University, Stanislaus, Turlock, CA 95382, USA
a r t i c l e i n f o a b s t r a c t
Article history: The brown planthopper (BPH), Nilaparvata lugens (Stål), which periodically erupted in tropical Asian rice be-
Received 17 June 2011 fore the 1960s, became a major threat after farmers adopted green revolution technologies in the 1960s.
Revised 16 September 2011 Management and policy changes in the 1980s and 1990s emphasized non-insecticidal tactics to avert BPH
Accepted 17 September 2011
outbreaks. However, insecticides have resurfaced as the primary means for controlling rice insect pests and
Available online 01 October 2011
tropical Asian countries have recently experienced planthopper outbreaks in record numbers. Our review
Keywords:
of factors that have contributed to the outbreaks points to insecticides as the most tangible outbreak factor
Insect outbreaks primarily because of their harmful effects on natural enemies. BPH resistance to insecticides and especially
Intra- and inter-population variation imidacloprid has increased the probability of outbreaks as farmers have applied increasing quantities of in-
Tropical pest management secticide in an attempt to combat resistant populations. Similarly, heavy use of nitrogen fertilizer, especially
Agricultural landscapes on hybrid rice, has increased the potential for outbreaks. Other factors triggering outbreaks are less documen-
Moran effect ted, but we discuss the possibility that the high outbreak synchrony in geographically separated populations
Metapopulation of BPH may suggest a “Moran effect” such as climate that promotes an environment favoring above-average
increases in BPH populations. Also, we hypothesize that BPH functions as a metapopulation and, as such, pe-
riodic outbreaks could be a natural phenomenon requiring resupply of planthoppers into vacant areas to en-
sure genetic linkage among subpopulations. We conclude with a series of recommendations for research and
policy changes aimed at better understanding the cause of BPH outbreaks and for developing sustainable
management practices to prevent future outbreaks.
© Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection
Society, 2011. Published by Elsevier B.V. All rights reserved.
Contents
Background to problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123

Green revolution transforms Asian rice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123
BPH impedes the green revolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123
IPM heralded as the solution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 124
The BPH problem resurfaces . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125
Aims of review . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 125
The insecticide-induced outbreak paradigm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 126
Impact on natural enemies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 126
Insecticide-induced hormesis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 126
Insecticide resistance magnifies the problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 126
Do insecticides speed up BPH's adaptation to resistant rice? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
Synthesis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
Does nitrogen fertilizer provoke BPH outbreaks? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
Concerns with fertilizer use on hybrid rice . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 127
Impact of resistant cultivars on BPH . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 128
Mechanisms of resistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 128
Screening for BPH resistance . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129
Questions about the validity of the BPH biotype concept. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129
⁎ Corresponding author. Tel.: + 1 301 513 9548; fax: +1 301 314 9290.
E-mail addresses: bottrell@umd.edu (D.G. Bottrell), kgschoenly@biology.csustan.edu (K.G. Schoenly).
1226-8615/$ – see front matter © Korean Society of Applied Entomology, Taiwan Entomological Society and Malaysian Plant Protection Society, 2011. Published by Elsevier B.V. All
rights reserved.
doi:10.1016/j.aspen.2011.09.004
D.G. Bottrell, K.G. Schoenly / Journal of Asia-Pacific Entomology 15 (2012) 122–140 123
Achieving greater durability in BPH-resistant rice. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129

Integrating plant resistance and biological control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130
Effects of regional and local landscape patterns on BPH . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 130
Synchronous or asynchronous planting? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 131
Role of non-rice vegetation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 131
Implications of the looming water crisis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132
Are BPH outbreaks the ecological consequence of natural large-scale changes in the environment?. . . . . . . . . . . . . . . . . . . . . . . . 132
Climate change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 132
Could sunspot-related UV-radiation produce a Moran effect? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
Discussion, conclusions, and recommendations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
The insecticide-induced outbreak paradigm . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
Recommendation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
Fertilizer inputs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 133
Recommendation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134
BPH migratory cycles and metapopulation dynamics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134
Recommendation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134
Resistant cultivars and BPH biotypes. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 134
Recommendation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
Asian landscapes and climate change . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
Recommendation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
An Asian-wide multidisciplinary, multi-agency approach . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
Recommendation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 135
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 136
Background to problem treatments to the rice (Kenmore et al., 1987). In the Philippine prov-
ince of Nueva Ecija, a major irrigated rice area of Southeast Asia,
Green revolution transforms Asian rice Litsinger (2008) found that farmers treated high-yielding rice (seed-
beds and main crop) 1–10 times (average of 1.4–3.2) per crop using
Beginning in the 1960s, the production of rice (Oryza sativa L.) in 40 different insecticides (comprising 64 distinct brands). National ag-
tropical Asia evolved from a low-yielding traditional system that used ricultural research and education systems (NARES) and chemical
rice landraces developed by farmers and produced with nominal artifi- companies inspired by the green revolution recommended insecti-
cial inputs to a high-yielding scheme founded on genetically improved cides to rice farmers as a means to boost crop yield and avert cata-
cultivars, synthetic fertilizers, and synthetic pesticides. IR8 developed strophic pest losses. Insect epidemics, which, ironically, the
by the International Rice Research Institute (IRRI) and introduced into insecticides often triggered, reinforced the farmers’ fear of insect
the Philippines in 1966 was the first high-yielding rice cultivar for trop- pests and the need to apply the chemicals (Heong et al., 1994;
ical farmers. In favorable growing environments, IR8 produ- Bandong et al., 2002; Litsinger, 2008). The farmers continued to
ced ≈ 10 t ha−1 (harvested grain) compared to≈ 1 t ha−1 for treat the rice routinely even after breeders had incorporated insect
traditional rice (De Datta et al., 1968). IR8 quickly spread throughout resistance into the high-yielding cultivars (Heinrichs, 1992; Litsinger,
tropical Asia and contributed significantly in elevating rice production 2009). Some governments provided insecticides at low costs to en-
in areas that faced rice shortages (Conway and Toenniessen, 1999). sure that farmers would regularly treat their rice crops (Kenmore,
“Green revolution” technologies (IR8 and later improved cultivars, 1991; Gallagher et al., 2009). In Indonesia, for example, 1986 govern-
controlled irrigation, synthetic fertilizers, and pesticides) quickly dis- ment subsidies for pesticides amounted to $179 million (1995 U.S.
placed traditional rice farming methods in many areas (Jennings, dollars), which was about 0.17% of the country's GDP and 0.8%
1974). In the Philippines, N40% of the riceland was planted with im- of the total government expenditure (World Bank data cited in
proved cultivars within 3 years after the release of IR8 in 1966 Gallagher et al., 2009). From 1976 to 1987, Indonesian government
(Huke and Huke, 1990). Philippine rice production attributable to expenditure on pesticides totaled nearly $1.5 billion (1995 U.S. dol-
the new technologies increased an average of 12.4% annually from lars) (World Bank data cited in Gallagher et al., 2009). Yet, few
1967–1968 to 1971–1972 (Jennings, 1974). The new rice cultivars farmers were trained to use insecticides properly. Rice farmers in
reached harvest maturity relatively quickly (105–110 days for later the Philippines surveyed by Heong et al. (1995a) applied some 80%
improved varieties from the Philippines, Bangladesh, and India) com- of the insecticide sprays at the wrong pest or when pests were not a
pared to the traditional cultivars (160–200 days) (De Datta, 1981). problem. Because of poor application equipment, N75% of an insecti-
This meant that farmers with irrigation systems could yearly harvest cide's active ingredient ended up in the rice fields’ water instead of
two and sometimes three crops from the same rice paddy. Monocul- the intended target area (Heong et al., 1995a). Despite the farmers’
tures of the new high-yielding cultivars appeared year round in many belief that insecticides were essential to protect rice yield, numerous
irrigated areas. Artificial fertilizers and insecticides became trade- evaluations showed that the insecticides were rarely necessary
mark features of the high-yielding system. Without fertilizers, the ge- for profitable rice farming (Waibel, 1986; Pingali and Roger, 1995;
netically improved cultivars yielded no better than the traditional Matteson, 2000).
cultivars (De Datta et al., 1968). Farmers perceived chemical insecti-
cides as insurance to protect investments in fertilizers and other in- BPH impedes the green revolution
puts. Insecticide use spiraled in the high-yielding production
systems as illustrated in several Philippine provinces. In the decade An unanticipated problem arising with the rice green revolution was
before the availability of IR8 in 1966, about 60% of Philippine farmers the recurring outbreaks of the brown planthopper (BPH), Nilaparvata
were using some insecticides; by the late 1970s, nearly 70% of farmers lugens (Stål) (Hemiptera: Delphacidae). This insect develops on culti-
planting high-yielding rice cultivars routinely applied insecticidal vated rice, several species of wild Oryza (Pathak and Heinrichs, 1982;
124 D.G. Bottrell, K.G. Schoenly / Journal of Asia-Pacific Entomology 15 (2012) 122–140
Claridge et al., 1985; Romena and Heinrichs, 1989), and the weed Leer- to BPH while acknowledging that the pest had the capacity to adapt
sia hexandra Swartz (Heinrichs and Medrano, 1984; Claridge et al., to the resistant cultivars (IRRI, 1979). IR26, the first high-yielding
1985). Diagnostic markers and genetic distance analysis using RAPD- rice cultivar with BPH resistance released by IRRI in l974, was suc-
PCR revealed the possibility of sibling species in the BPH complex be- cessful only for ≤3 years. In the laboratory, Pathak and Heinrichs
tween rice-caught and Leersia-caught populations (Latif et al., 2008). (1982) discovered that BPH populations could adapt to IR-26 in 7–
BPH feeds by inserting its stylets into the vascular tissue of plant leaf 10 generations.
blades and leaf sheaths and ingesting the sap (Sōgawa, 1982). Popula-
tions concentrate at the base of the plant and reach maximum density IPM heralded as the solution
after canopy closure (Reissig et al., 1986). Heavy infestations can
cause the complete drying and wilting of rice plants, a condition The IRRI (1979) conferees highlighted integrated pest manage-
known as “hopperburn” (Bae and Pathak, 1970). The pest also transmits ment (IPM) as a management strategy to help prevent BPH outbreaks.
the plant pathogens ragged stunt virus and grassy stunt virus (Ling, A term introduced by the Council on Environmental Quality (CEQ,
1972; IRRI, 1983; Hibino et al., 1985; Cabauatan et al., 2009). BPH may 1972) from the earlier term integrated pest control (Stern et al.,
complete some 12 generations per year in the tropics (Dyck et al., 1959), IPM uses different methods to prevent pest populations from
1979) but only ≤3 generations in temperate areas (Kuno, 1979; Perfect reaching damaging levels. Rather than relying on a single method of
and Cook, 1994). The northern geographical limit of winter breeding for pest control, IPM combines pest-resistant cultivars, fertilizer manage-
the species is around the Red River Delta of Vietnam (Kisimoto, 1976). It ment, agronomic practices that conserve and increase the effects of
occurs throughout the year in the Asian tropics and subtropics and ex- predators and other naturally occurring biological control agents,
pands its range northward when rice becomes available in temperate and, when needed, prudent use of pesticides based on need rather
areas of China, India, Japan, and Korea (Perfect and Cook, 1994). Migra- than prophylactic treatment.
tion aided by weather frontal systems ensures that some members of a In 1980, with technical assistance from the Food and Agriculture
migrating population will reach distances of several hundred kilome- Organization of the United Nations (FAO), countries of tropical Asia
ters (Kisimoto, 1976, 1979; Kisimoto and Rosenberg, 1994; Turner et launched a major rice IPM program to increase economically and en-
al., 1999; Zhu et al., 2000b; Otuka, 2009). However, BPH does not sur- vironmentally sound pest management practices (Gallagher et al.,
vive the winter in temperate areas. Infestations of BPH in the temperate 1994, 2009; Matteson et al., 1994; Pontius et al., 2001). From 1980
environments originate from yearly migrations from tropical Asia and to 1989, the program emphasized pest surveillance, host-plant resis-
China (Cheng et al., 1979; Kisimoto, 1979; Kisimoto and Rosenberg, tance, judicious use of pesticides, natural enemies of pests, and field
1994; Perfect and Cook, 1994; Zhu et al., 2000b; Otuka, 2009; Watanabe demonstrations that gave farmers first-hand experience with IPM
et al., 2009). During autumn, return migrations (north-to-south) of BPH practices and ecological concepts. Each component had a working
populations have been studied over China and India (Riley et al., 1991, group led by designated NARES. The governments of India, the Philip-
1995). Such return migrations may help explain how long-distance mi- pines, and Indonesia declared national IPM policies in the mid-1980s.
grants are maintained in southern overwintering populations. Indonesian officials banned 57 pesticides known to cause BPH out-
According to references cited by Dyck and Thomas (1979), Heinrichs breaks and also stopped pesticide subsidies. The policy shift to curb
(1994), and Mochida and Okada (1979), planthopper outbreaks oc- pesticides saved the Indonesian government more than $100 million
curred in rice hundreds of years before the green revolution started in per year (1995 U.S. dollars) and reduced pesticide imports by two-
the 1960s. Outbreaks reputedly occurred in Korea around AD 18 (Paik thirds (World Bank data cited in Gallagher et al., 2009). The approxi-
and Paik, 1977; Dyck and Thomas, 1979) and in Japan as early as AD mate cost of the FAO program in Indonesia between 1985 and 1988
697 or 701 (Miyashita, 1963; Grist and Lever, 1969; Konishi and Ito, was US$650,000 (P.E. Kenmore, personal communication 31 Jan.
1973; Dyck and Thomas, 1979). After the discovery of whale oil as an in- 2011).
secticide in 1670, followed by the use of slaked lime and bittern The FAO-IPM program emphasized intense on-farm training in
(Konishi and Ito, 1973), leafhoppers (Hemiptera: Cicadellidae) and farmer field schools (FFS) to make rice farmers proficient at imple-
planthoppers reputedly surged in Japan (Miyashita, 1963). Confirming menting IPM with minimal technical assistance. From 1980 to 2002,
such early reports as BPH outbreaks presents taxonomic problems, as the IPM program trained farmers in 13 countries (Bangladesh, Cam-
the species N. lugens was not described until 1854 (Dupo and Barrion, bodia, China, India, Indonesia, Laos, Malaysia, Myanmar, Nepal, the
2009). However, Fiji, Japan, Korea, Solomon Islands, Taiwan, and per- Philippines, Sri Lanka, Thailand, and Vietnam). Data from Malaysia
haps other countries had confirmed BPH outbreaks before 1966, the and Myanmar are not available, but N2 million rice farmers in the
year that IR8 was introduced (Dyck and Thomas, 1979; Kenmore, other 11 countries were FFS-trained from 1989 to 2000 (Pontius et
1980). Before the green revolution, the most notable outbreaks were al., 2001). According to van den Berg and Jiggins (2007), the number
in temperate areas, notably Japan and Korea. Outbreaks in the tropics of FFS-trained farmers represented only 1–5% of all farmer house-
were generally localized and occurred infrequently (Dyck and Thomas, holds in those countries. Six of the countries that participated in the
1979; Kenmore, 1980). FAO program (Bangladesh, China, India, Indonesia, the Philippines,
In 1977, in response to the threat that BPH outbreaks presented to and Vietnam) accounted for more than 90% of all FFS graduates
the new high-yielding tropical rice, IRRI (1979) convened an interna- (van den Berg and Jiggins, 2007). Farmers trained in IPM reduced in-
tional conference to review the problem and to identify priority re- secticide use by 50–80% while sustaining or increasing rice yield
search and education programs leading toward better management (Matteson, 2000). The greatest impact was in Indonesia, where
of the pest. The conferees concluded that Intensification of rice crop- some 1.5 million farmers received IPM training (Oka, 2003). The
ping and its associated technologies had brought significant changes IPM training combined with the pesticide policies led to a 75% reduc-
to the rice landscape, which encouraged BPH outbreaks, especially tion in insecticide use on rice of the IPM-trained farmers in the prov-
in irrigated areas where farmers planted 2 or 3 rice crops per year. ince of Java (Gallagher et al., 1994).
The continuous succession of monocultures over large areas provided In 1991, IRRI launched a complementary pesticide-reduction pro-
abundant BPH habitat that enabled the populations to reproduce gram called farmer participatory research (FPR) to resolve the
nearly year round, and the heavy use of nitrogen fertilizer likely in- farmers’ misperceptions about the need to control leaffolders (Lepi-
creased the pest's reproductive potential (Dyck et al., 1979). Frequent doptera: Pyralidae). Studies at IRRI indicated that leaffolders rarely
use of insecticides exacerbated the problem by killing natural ene- reduce rice yield if left untreated (Graf et al., 1992; De Kraker,
mies that regulated BPH's populations. The conferees emphasized 1996); yet rice farmers perceived that these insects would cause
the importance of developing rice cultivars with genetic resistance heavy yield losses if not controlled (Heong et al., 1994; Heong and
Escalada, 1997). Surveys indicated that most insecticide applications Aims of review
during the first 30–40 days of rice planting were aimed at leaffolders
(Heong and Escalada, 1997). In FPR experiments, during the first 30– A widely shared view of rice insect management specialists is that
40 days after planting, participating farmers applied insecticidal the BPH poses a significant threat to tropical rice only after its natural
sprays as they normally would have (usually 1–3 times) to most of enemies have been disrupted by insecticidal treatments. In other
their crop but they left a portion (≈100 m 2) of each field untreated. words, the BPH will remain at non-damaging levels unless insecticides
At harvest, the farmer determined yields from both portions of the unleash it from natural control. That was the prevailing view in 1977
field and then compared results with neighboring farmers who had when IRRI (1979) held the first major international conference on
conducted similar experiments. Participating farmers often quickly planthoppers. The same view persisted three decades later when IRRI
realized economic benefits when stopping the early treatments and held the second major international conference on planthoppers in
became ambassadors in spreading the "no-spray" message to other 2008 (Heong and Hardy, 2009). We will critically examine the rationale
farmers. In some areas, government agencies initiated complementa- and limitations to the “insecticide-induced outbreak paradigm,” which
ry media campaigns using radio, TV, printed materials, and other advocates that BPH outbreaks are triggered by insecticides. Then we
methods of communication to encourage more farmers to stop will assess other factors that might contribute to BPH outbreaks. Our re-
early-season use of rice insecticides. The FPR programs in several lo- view of the extensive literature on this topic includes papers, books, and
cations of Southeast Asia eliminated 50–80% of the insecticide use book chapters published through early 2011.
on rice without yield loss (Heong and Escalada, 1997). The greatest Although our assessment is restricted to outbreaks of the BPH,
impact was in the Mekong Delta of Vietnam. Surveys showed that outbreaks of two other species of rice planthoppers, the whitebacked
from 1992 to 1997, Delta farmers reduced the average number of in- planthopper (WBPH), Sogatella furcifera (Horváth), and the small
secticide sprays per rice crop from 3.1 to 1.0 (Huan et al., 1999). brown planthopper (SBPH), Laodelphax striatellus (Fallén), have also
Throughout the Delta, the FPR programs decreased insecticide use intensified in many areas of Asia in recent years (Heong and Hardy,
by ≈50% on some 2 million rice farms (Escalada et al., 1999). 2009). BPH and the two other delphacids occur sympatrically in
some areas (Dupo and Barrion, 2009) and may co-occur in the same
rice field in a given cropping season. Like BPH, WBPH and SBPH
The BPH problem resurfaces have periodically reached outbreak levels in rice for decades, but re-
curring outbreaks became increasingly common in the past decade.
The FAO-IPM and IRRI-FPR programs and complementary efforts In some areas of China, all three species have caused serious yield
of the participating Asian countries, various national and multination- losses every year since the early 2000s (Cheng, 2009). SBPH and
al donor agencies, and nongovernmental organizations contributed WBPH have primarily infested hybrid rice, SBPH and BPH have pri-
significantly in promoting natural biological control and other non- marily infested Japonica rice (O. sativa japonica), and all three species
chemical methods, reducing insecticides, and lessening risks of have infested Indica rice (O. sativa indica) in China (Cheng, 2009).
planthopper outbreaks (Kenmore, 1991; Gallagher et al., 1994, WBPH occurs widely in rice areas of Asia (Dupo and Barrion, 2009).
2009; Heong and Escalada, 1997; Matteson, 2000; Heong and As with the BPH, the northern limit of the winter breeding area for
Hardy, 2009). However, the efforts were not sustainable. This was the WBPH is around the Red River Delta of Vietnam (Kisimoto,
the conclusion reached at a major international conference on rice 1976). Like the BPH, the WBPH makes long migratory flights and an-
planthoppers at IRRI in 2008 (Heong and Hardy, 2009). The conferees nually colonizes in the temperate areas of Japan, Korea, and most
reported that chemical control had resurfaced as a primary tactic for areas of China (Kisimoto, 1976; Turner et al., 1999; Otuka, 2009). Dur-
controlling rice insects and since 2003 Asian countries have seen ing the period 1998–2007, WBPH damaged more hectares of rice in
planthopper outbreaks equal to or worse than those of the 1970s China than the brown planthopper (Catindig et al., 2009). WBPH
(Heong and Hardy, 2009). The resurrection of chemical control is il- has become the most predominant insect pest in areas planted with
lustrated by data from Vietnam's Mekong Delta (Escalada et al., Indica hybrid rice in China (Sōgawa et al., 2009). The SBPH, which at-
2009). The FAO-FFS, initiated in 1992, had trained an estimated tacks rice and also wheat (Triticum spp.) and sugarcane (Saccharum offi-
410,000 Mekong Delta farmers by 1997. Delta rice farmers neither cinarum L.), occurs mainly in temperate rice areas (Dupo and Barrion,
trained in the FFS nor exposed to the IRRI-FPR media campaign to re- 2009). In China, this pest is becoming increasingly damaging and re-
duce insecticides applied insecticide sprays about 2.1 times per rice search has confirmed high levels of insecticidal resistance in its popula-
crop. Farmers exposed to the media campaign alone sprayed about tions (e.g., Gao et al., 2008).
1.2 times and those exposed to both the media campaign and FFS Besides directly damaging rice plants, WBPH and SBPH transmit rice
training sprayed about 0.5 times. However, starting in 2005, insecti- diseases. WBPH vectors the southern rice black streak dwarf virus
cide use intensified and by 2007 the level of use had surpassed the (SRBSDV) discovered in 2001 in Guangdong province, China and de-
level that preceded the FFS and FPR-media campaigns (Escalada et scribed by Zhou et al. (2008) and Zhang et al. (2008). Il-R. Choi reported
al., 2009). The chemical industry now conducts major mass media that SRBSDV had also been found in Japan (Kyushu island) (Sept. 24,
campaigns to promote insecticidal control in rice throughout Viet- 2010 Ricehoppers, IRRI-ADB, 2011). SBPH vectors the virus diseases
nam's Mekong Delta. rice stripe virus (RSV) and rice black streaked dwarf virus (RBSDV).
Bangladesh, Cambodia, China, India, Indonesia, Japan, Korea, Laos, China has experienced serious RSV epidemics in recent years (Wang et
Malaysia, the Philippines, Thailand, and Vietnam have recorded major al., 2008a). In western Japan, according to information by local plant
BPH outbreaks in recent years (Heong and Hardy, 2009). Reports of protection offices (Otuka, 2009), the proportion of RSV viruliferous
difficulty controlling BPH because of insecticide resistance are in- adults of L. striatellus has recently shown a gradual increase to 6–16%.
creasingly common (Gorman et al., 2008; Wang et al., 2008b; All three planthopper species are r-strategists with short life cy-
Matsumura et al., 2009; Heong et al., 2011; IRRI-ADB, 2011). BPH out- cles, rapid reproductive rates, and high migratory potential (Cheng,
breaks in China in 2005–2007, which affected 6.6–9.4 million ha of 2009; Heong, 2009). They normally reside at low densities but their
rice (Catindig et al., 2009), exceeded those ever recorded (Cheng, populations can exhibit explosive increases and cause devastating
2009). The outbreak area of 2005–2007 amounted to ≈ 23–30% of economic impacts. The prevailing view is that outbreaks of all three
China's ≈ 29.2 million ha of rice (IRRI, 2011b). By comparison, BPH species are primarily triggered by insecticide use (Heong and Hardy,
outbreaks in 1998–2000 affected only 2.2–3.5 million ha of rice 2009). The blog Ricehoppers maintained by IRRI-ADB (2011) is a
(Catindig et al., 2009) or ≈ 7–11% of China's total rice area valuable source for information on the status of the three species in
(≈31.2 million ha) (IRRI, 2011b). Asian rice.
The insecticide-induced outbreak paradigm increase via hormesis (Hardin et al., 1995; Cohen, 2006; Dutcher,
2007). Chelliah et al. (1980) showed that sublethal doses of methyl
Impact on natural enemies parathion and decamethrin applied topically to 5th instar BPH nymphs
increased reproduction in BPH adults that developed from the nymphs.
The seminal research of Kenmore (1980) and Kenmore et al. Sublethal doses of some insecticides increase fecundity in BPH females
(1984) in the Philippines clearly demonstrated the ability of natural by stimulating changes in rice plant nutrients (Wu et al., 2001, 2003;
enemies to regulate the population density of BPH in tropical rice Yin et al., 2008). Yin et al. (2008) found that insecticide-induced repro-
not treated with insecticides. Although BPH populations can reach ductive stimulation varied among rice cultivars, insecticides, and the in-
relatively high densities even on BPH-resistant cultivars in low-pesti- secticides’ application rates. Sublethal applications of the insecticide
cide (molluscicide only) fields when predators are abundant (e.g., deltamethrin resulted in significantly more brachypterous (flightless)
Schoenly et al., 2010), predation primarily by spiders and the insects BPH adults when compared to sublethal applications of imidacloprid
Microvelia douglasi atrolineata Bergroth (Hemiptera: Veliidae) and or triazophos. The highest BPH reproductive rate occurred on plants
Cyrtorhinus lividipennis (Reuter) (Hemiptera: Miridae) appears to treated with triazophos. Treatments of all insecticides evaluated
prevent BPH outbreaks in tropical rice (e.g., Kenmore, 1980; (deltamethrin, imidacloprid, triazophos, and a synthetic pyrethroid)
Heinrichs and Mochida, 1984; Kenmore et al., 1984; Nakasuji and on both BPH susceptible (TN1) and resistant (Xieyou 963) rice culti-
Dyck, 1984; Sahu et al., 1996; Settle et al., 1996; Fagan et al., 1998; vars increased soluble sugar levels in 3rd- and 5th-instar nymphs
Sigsgaard, 2007; Dupo and Barrion, 2009). Less intensively studied and adults developing from nymphs that had fed on insecticide-trea-
is the role of parasitoids in regulating BPH density under field condi- ted rice plants. Also, adults developing from nymphs that fed on
tions, although significant levels of parasitism of BPH eggs have been treated plants had significantly more crude fat than adults develop-
observed (e.g., Chiu, 1979; Kenmore, 1980; Kenmore et al., 1984; ing from nymphs that fed on untreated plants. Reproductive stimu-
Fowler et al., 1991; Claridge et al., 2001; Dupo and Barrion, 2009; lation attributed to insecticide treatment was more pronounced on
Gurr et al., 2011). Parasitism by many of the BPH parasitoids is usually BPH-susceptible cultivars.
insufficient to cause significant BPH mortality (Greathead, 1983). The results of Yin et al. (2008) indicate that sublethal insecticide
However, habitat manipulation of non-rice vegetation seems to applications could theoretically increase BPH's capacity for migration
have potential in increasing the effects of some parasitoids, especially because the planthoppers would acquire more fat and sugar, which
mymarid wasps (Gurr et al., 2011). Important egg parasitoids of BPH provide fuel for flight, when feeding on insecticide-treated rice plants
may include mymarid (e.g., Anagrus spp., Gonatocerus spp.), tricho- than when feeding on untreated rice plants. Litsinger (2008) found
grammatid (Oligosita spp. and Paracentrobia spp.), and eulophid (Tet- that, to save time and money, Philippine rice farmers often apply in-
rastichus spp.) wasps (Sahad, 1984; Fowler et al., 1991; Claridge et al., secticides in wide sweeps (wetting only a subset of leaves) and
2002; Dupo and Barrion, 2009; Gurr et al., 2011). A range of parasit- apply sprays at rates lower than recommended by insecticide manu-
oids, including strepsipterans, dryinid wasps, pipunculid flies, and facturers. Moreover, because BPH populations build up at the base of
other taxa (Claridge et al., 2002; Dupo and Barrion, 2009), attack the rice plant over time, the closed canopy can shield them from
BPH nymphs and adults. spray droplets (Reissig et al., 1986). The results of Yin et al. (2008)
Although insecticide applications to rice do not always trigger BPH suggest that farmer applications of sublethal rates of certain insecti-
outbreaks (e.g., Heinrichs et al., 1982a, 1982b), they often disrupt the cides could enhance both BPH's reproductive and migratory capacity
actions of BPH's natural enemies either by direct killing action or by and theoretically increase the threat of BPH outbreaks even if the in-
disrupting food chains (e.g., Chelliah and Heinrichs, 1980; Heinrichs secticides did not harm natural enemies.
et al., 1982a; Heinrichs et al., 1982b; Reissig et al., 1982; Heinrichs
and Mochida, 1984; Song et al., 1984; Cohen et al., 1994; Schoenly Insecticide resistance magnifies the problem
et al., 1996; Cuong et al., 1997; Fagan et al., 1998; Heong and
Schoenly, 1998). Wide-scale outbreaks of BPH in tropical Asian rice Genetic resistance to the organochlorine compound BHC appeared
in the 1970s and 1980s (IRRI, 1979; Heinrichs et al., 1982a; Shepard in BPH populations in Japan in 1967 some 15 years after the insecti-
et al., 1991) were attributed to the insecticidal destruction of natural cide was first used on the country's rice (Miyata, 1989). Researchers
enemies (Matteson, 2000). The BPH's ascendancy following insecti- detected resistance to malathion and diazinon (organophosphorus
cide use was commonly called “pest resurgence” (e.g., Chelliah and compounds) in BPH populations on IRRI's experimental farm in the
Heinrichs, 1980; Heinrichs et al., 1982a,b; Reissig et al., 1982; Hein- Philippines in the late-1960s and 1970s (Heinrichs, 1979, 1994) and
richs and Mochida, 1984). Smith and van den Bosch (1967) originally resistance to organophosphorus and carbamate insecticides in Tai-
used the term pest resurgence to describe the rapid numerical re- wan in the 1970s (Miyata, 1989). By the early 1990s, numerous
bound of a pest following use of an insecticide aimed at that specific Asian countries had reported BPH resistance to organochlorine, or-
pest. In many areas of Asia, farmers use insecticides specifically to ganophosphorus, carbamate, and pyrethroid insecticides (e.g., Nagata
control BPH even when its population density is low. More often, et al., 1979; Kilin et al., 1981; Miyata, 1989; Hirai, 1993; Heinrichs,
however, in the tropics except during BPH outbreaks insecticides 1994). Until recently, the reports of resistance in BPH populations
are directed at leaffolders or other pests (Heong et al., 1994; Litsinger, were mostly from temperate areas. Wide-scale use of neonicotinyl
2008) and not BPH. Smith (1970) proposed the term “secondary pest compounds (mainly imidacloprid) has magnified the resistance prob-
outbreak” to describe the increase of a nontarget secondary pest from lem in both tropical and temperate areas (Matsumura et al., 2009;
its normal sub-injurious level to pest status following insecticidal Heong et al., 2011; IRRI-ADB, 2011). By 2008, laboratory assays had
control of a target pest. Normally, a secondary pest does not attain in- confirmed imidacloprid resistance in BPH populations in China,
jurious levels because of effective natural enemies or other regulatory India, Japan, Indonesia, Malaysia, Taiwan, Thailand, and Vietnam
factors; it erupts only when insecticides or other factors cause ecolog- (Gorman et al., 2008; Matsumura et al., 2009). Rice farmers in several
ical disruption. Insecticides have caused both resurgence and second- countries have reported reduced efficacy using imidacloprid to con-
ary outbreaks of BPH. trol BPH (Gorman et al., 2008). BPH resistance to imidacloprid has
created especially difficult problems for Chinese rice farmers
Insecticide-induced hormesis (Cheng, 2009).
From 1996 to 2006, Wang et al. (2008b) assayed 42 field samples
Insecticides not only increase the likelihood of pest outbreaks by dis- of BPH from eight Chinese provinces for resistance to imidacloprid.
rupting the actions of natural enemies but also may promote pest Most of the BPH populations remained susceptible to imidacloprid
from 1996 to 2003 except in Guilin (Guangxi Zhuang Autonomous unlikely that insecticides have been wholly responsible for outbreaks
Region) where minor resistance was detected in 1997. However, by in the tropics, as we will discuss.
2005 high to extremely-high resistance levels appeared in BPH popu-
lations from numerous locations. Within only a 2-year period, a pop- Does nitrogen fertilizer provoke BPH outbreaks?
ulation from Nanning (Guangxi Zhuang Autonomous Region)
increased in resistance by N200-fold. In other areas, especially in Nitrogen is the most limiting nutrient for rice in tropical Asian soils
southeast China, BPH developed N800-fold resistance to imidacloprid. (Bouldin, 1986; Kundu and Ladha, 1995). As a rule, 1 kg of nitrogen is
To control the imidacloprid-resistant populations, farmers increased required to produce 15–20 kg of grain. Naturally available nitrogen
the application rate of imidacloprid from 15 g (a.i.) ha −1 to ≈ 60– from biological fixation (e.g., Ladha et al., 1993) and mineralization of
120 g (a.i.) ha −1. In many rice-growing areas, farmers sprayed during soil nitrogen (e.g., Bouldin, 1986; Kundu and Ladha, 1995) is sufficient
every BPH generation to prevent outbreaks of the pest (Wang et al., to attain harvest yields of 2–3.5 t ha−1. Farmers expecting a higher
2008b). Imidacloprid's long residual activity and high efficacy make yield must apply additional nitrogen. Before the availability of IR8 and
it the preferred insecticide for controlling BPH in many areas later high-yielding cultivars, tropical rice farmers did not regularly
(Denholm and Rowland, 1992; Wang et al., 2008b). Trends suggest apply fertilizers because the traditional cultivars usually produced less
that continued heavy use of the insecticide will exacerbate the prob- than 2–3 t ha−1. However, large amounts of fertilizer were necessary
lem of genetic resistance in BPH populations in China and other coun- to achieve successful yield from the improved cultivars (De Datta et
tries (Heong et al., 2011). al., 1968; De Datta, 1981). In China, for example, the yield of rice in-
Because BPH migrates long distances, it seems that resistance to insec- creased from 4.13 to 6.26 t ha−1 in the past 25 years (2006 data from
ticides should be slowed by the regular influx of immigrants from areas of China's ministry of agriculture, Cheng, 2009). During this same period,
low insecticide use (Zhuang et al., 2004). However, in China imidacloprid total chemical fertilizer and nitrogen use increased from 12.69 and
has been used intensively on a large scale to control BPH in both the em- 9.34 million tons to 47.66 and 22.29 million tons, respectively (Cheng,
igrating area and the immigrating area (Liu et al., 2003; Cheng, 2009). 2009). Farmers in China now apply an average of 180 kg N ha−1 to
Imidacloprid has also been used intensively in southeastern Asian coun- rice (Lu et al., 2007), compared to ≥100 kg N ha−1 that tropical farmers
tries (Gorman et al., 2008; Wang et al., 2008b) where BPH populations in Asia apply to high-yielding rice cultivars (Saleque et al., 2004).
develop on rice year round and are the major source for northbound mi- Nitrogen-enriched plants can significantly enhance the size, perfor-
gration to China in the following year (Kisimoto, 1979; Perfect and Cook, mance, and abundance of herbivorous insects (Awmack and Leather,
1994; Matsumura et al., 2009). Therefore, once resistance to imidacloprid 2002). In 1970, Sōgawa showed that rice plants fertilized with high
evolves, the resistant BPH migrants may quickly spread the imidacloprid- levels of nitrogen will attract more BPH than nitrogen-poor plants and
resistance alleles long distances (Wang et al., 2008b). also improve the insect's survival and reproduction. Since then, field
Insecticide resistance can aggravate the problem of resurgence and studies have repeatedly demonstrated that BPH populations respond
secondary outbreaks of BPH because farmers must use increasing quan- positively to nitrogen fertilization (e.g., Cheng, 1971; Dyck et al., 1979;
tities of insecticide to combat the resistant population. Furthermore, as Heinrichs and Medrano, 1985; Lu and Heong, 2009) and also have im-
discussed, Yin et al. (2008) showed that imidacloprid foliar applications plicated nitrogen fertilizer as a cause for BPH outbreaks in high-yielding
to rice could increase lipids and soluble sugar in BPH nymphs and adults systems (Mochida and Dyck, 1977; Dyck et al., 1979; Kenmore, 1980; Lu
feeding on the plants. BPH populations that survived imidacloprid ap- et al., 2005; Lu and Heong, 2009). Increased plant nitrogen accelerates
plications could theoretically migrate above-average distances and BPH feeding and honeydew-excretion (Sōgawa, 1970; Cheng, 1971),
therefore serve as an especially important conduit in the spread of imi- survival (Lu and Heong, 2009), fecundity (Visarto et al., 2001; Lu and
dacloprid-resistance alleles into new areas. Heong, 2009), and population growth (Cheng, 1971; Visarto et al.,
2001; Lu and Heong, 2009) and the tendency for BPH outbreaks (Uhm
et al., 1985; Lu and Heong, 2009). Although not substantiated in the
Do insecticides speed up BPH's adaptation to resistant rice?
field, laboratory results of Lu et al. (2005) suggested that BPH's toler-
ance to adverse environmental stresses increases when nitrogen is ap-
Gallagher et al. (1994) and Heinrichs (1992) proposed that insecti-
plied to rice. Survival of nymphs, fecundity, and egg hatchability were
cides could accelerate the rate at which BPH adapts to resistant rice cul-
significantly higher in BPH populations on nitrogen-rich rice plants
tivars. Their hypothesis assumed that insecticidal applications to BPH-
than nitrogen-poor rice plants. Also, feeding on the nitrogen-rich plants
resistant plants would significantly disrupt the regulatory effects of
allowed female adults to survive longer in the absence of food.
BPH's natural enemies. When natural enemies are abundant, insecti-
Although nitrogen-rich rice plants can boost BPH's reproductive
cides would kill a significant portion of a BPH population and therefore
and growth capability, the populations often remain small in insecti-
reduce the population's exposure to the host-plant resistance mecha-
cide-free rice receiving high levels of nitrogen (Lu and Heong, 2009).
nism. With fewer natural enemies following an insecticide application,
On the other hand, Schoenly et al. (2010) recorded relatively high
the level of plant selection pressure on the BPH populations would the-
BPH densities in low-pesticide (molluscicide only) fields of BPH-resis-
oretically increase, thereby speeding up BPH's adaptation to the resis-
tant rice when high levels of nitrogen (120 kg ha −1) were applied.
tant rice. The argument advanced by Gallagher et al. (1994) and
Natural enemies, especially when combined with BPH-resistant culti-
Heinrichs (1992) makes intuitive sense but we are unaware if it has
vars (e.g., Cuong et al., 1997), seem to be essential in preventing BPH
been tested in controlled field experiments.
outbreaks in tropical rice heavily fertilized with nitrogen.
Synthesis Concerns with fertilizer use on hybrid rice
Our review of the extensive literature suggests that insecticides Hybrid rice produced by crossing two inbred lines is occupying sig-
are the single most tangible human-controlled input responsible for nificantly more Asian riceland. Hybrid rice now accounts for ≈ 60% of
BPH outbreaks. The literature since the start of the green revolution the rice planted in China (IRRI, 2011c). Although hybrid seeds may
in the 1960s, much of which we have cited, provides many persuasive cost two times more than non-hybrid seeds, farmer profits can be sub-
examples of the insecticides’ negative effects on BPH. The two largest stantially higher because the hybrids yield 16–20% more than their in-
international conferences on rice planthoppers to date (IRRI, 1979; bred parents (IRRI, 2006). Larger planthopper populations and
Heong and Hardy, 2009) singled out heavy use of insecticide as the frequent outbreaks in farmers’ fields have been reported for the hybrid
primary driving force behind BPH outbreaks. However, it is highly rice (Mew et al., 1988; Sōgawa et al., 2003). The hybrids’ dense canopy,
resulting from more vigorous vegetative growth, apparently makes Plant breeders are especially interested in transgenic rice plants
them more attractive to migrating or dispersing insects (Cohen et al., expressing snowdrop lectin, Galanthus nivalis agglutinin (GNA), to
2003). The hybrid plants have greater nitrogen uptake and nitrogen control planthoppers. Transgenic plants with GNA have exhibited re-
use efficiency (defined as grain yield per unit nitrogen fertilizer applied) sistance to BPH (Nagadhara et al., 2003) and WBPH (Nagadhara et al.,
than their inbred parent lines (Virmani, 1994; Yang et al., 1999). The in- 2004) and also green leafhoppers (Nephotettix sp.) (Nagadhara et al.,
creased nitrogen uptake and use efficiency in the hybrids could result in 2003). Of the available transgenic rice plants, GNA plants are the clos-
more available nitrogen for BPH and other pests (Cohen et al., 2003). est to commercialization (Malone et al., 2008).
Furthermore, the hybrids’ complete lack or low level of genetic resis-
tance to planthoppers makes them more susceptible to the insects. Mechanisms of resistance
The main hybrid rice cultivars in China are susceptible to WBPH, and
only about 12% of the newly developed varieties showed any BPH resis- Researchers do not clearly understand what natural mechanisms in
tance in field tests (Chen et al., 2005). rice plants confer resistance to BPH and how these mechanisms relate
to identified resistance genes (Chen, 2009; Horgan, 2009; Seo et al.,
Impact of resistant cultivars on BPH 2009). How the major resistance genes or quantitative trait loci
(QTLs) function is uncertain (e.g., Horgan, 2009). It has been generally
Developing improved rice cultivars with insect and disease resis- accepted that host selection by planthoppers is due to phloem chemis-
tance is an important objective of rice breeding (Khush, 1971, 1979, try and likely involves the lack of particular feeding stimulants (Cook
1984; Bonman et al., 1992; Park et al., 2007; Jena and Mackill, 2008; and Denno, 1994). Silicic and oxalic acids deter BPH feeding on resistant
Brar et al., 2009). High-yielding cultivars with resistance to BPH, rice (Yoshihara et al., 1979a, 1979b, 1980). Phenolic acids in resistant
other insects, and diseases (Brar et al., 2009) have contributed signif- varieties appear to be related to the inability of BPH to find and ingest
icantly in elevating rice yield throughout tropical Asia. IRRI is the phloem (Fisk, 1980). On the other hand, BPH is more likely to reject
world's primary rice breeding center and has supplied thousands of rice varieties with low levels of essential amino acids in the phloem
improved breeding lines to rice producing countries. An estimated (Sōgawa, 1982). Shigematsu et al. (1982) found that sterols acted as
50% of the world rice area is planted to IRRI-bred varieties or their sucking inhibitors for BPH whereas asparagine stimulated sucking.
progenies (IRRI, 2011a). However, the results of studies in Korea suggest that BPH can thrive
IRRI started a program to breed rice for resistance to BPH soon on resistant rice with Bph1 or bph2 genes despite its difficulty ingesting
after Pathak et al. (1969) identified sources of rice resistance to the the phloem sap of resistant plants (Seo et al., 2009). The results of Du et
insect in 1967. Many countries in Asia have started similar programs. al. (2009) reveal that the BPH-resistance gene Bph14 is a member of the
The first two resistance genes were designated as Bph1 and bph2 CC-NB-LRR disease resistance gene family that mediates resistance
(Athwal et al., 1971). Twenty-one genes for BPH resistance have through direct or indirect recognition of pathogen-associated molecular
now been identified from cultivated and wild species of Oryza (Park patterns or pathogen effectors (Jones and Dangl, 2006; Takken and
et al., 2007; Jena and Mackill, 2008; Brar et al., 2009). Producing rice Tameling, 2009). Bph14 confers resistance to BPH at seedling and matu-
with durable resistance to BPH is a major challenge because of the rity stages of the rice plant. It carries a unique LRR domain that might
pest's history of adapting to resistant cultivars (Brar et al., 2009; Horgan, function in recognizing the BPH invasion and activating the defense re-
2009). The pest adapted to IR26, the first high-yielding cultivar with BPH sponse. Bph14 is predominantly expressed in vascular bundles, the site
resistance (with Bph1 gene), within 2 or 3 years after being released to of BPH feeding. Expression of Bph14 activates the salicylic acid signaling
farmers. Other BPH-resistant cultivars have remained viable for only a pathway and induces callose deposition in phloem cells and trypsin in-
relatively short time (e.g., Heinrichs, 1988, 1992). Although some hibitor production after planthopper infestation, thereby reducing the
BPH-resistant cultivars and notably IR36 and IR64 have shown greater feeding, growth rate, and longevity of BPH.
durability (e.g., Cohen et al., 1997; Alam and Cohen, 1998; Brar et al., Studies of inter-specific interactions suggest that BPH's response
2009), BPH is still a nemesis of plant breeders. to rice and vice versa may be affected by the presence of other species
Fifteen of the BPH-resistance genes have been mapped to chromo- of organisms. Cheng et al. (2001), for example, found that the level of
somal location and 8 have been linked with molecular markers (Brar resistance to BPH in a rice plant can decline if WBPH previously
et al., 2009). Resistance to BPH may be due either to major (qualita- infested the plant, although the mechanisms were not determined.
tive) or minor (quantitative) traits. Recent advances in BPH genomics Several genes have been linked to induced defenses in rice. OsBi1 is
(Noda, 2009), marker-assisted selection (Jena and Mackill, 2008; Brar a BPH-inducible gene implicated in the resistance of rice plants to
et al., 2009), genetics of host-plant resistance to BPH (Fujita et al., BPH (Wang et al., 2004). Whether other insects of rice also induce
2009), and rice genomics (Jena and Mackill, 2008; Brar et al., 2009) OsBi1 is not known. Bph14, discussed above, mediates disease resis-
offer new opportunities for rice breeders. The breeders can now iden- tance through direct or indirect recognition of pathogen-associated
tify and map precisely the genes for BPH resistance (Gramene, 2011). molecular patterns or pathogen effectors (Jones and Dangl, 2006;
Marker-assisted selection techniques can help breeders develop rice Takken and Tameling, 2009). As noted, OsBi1 is also a BPH-inducible
cultivars with two or more genes for resistance pyramided into a sin- gene that reduces the performance of BPH (Du et al., 2009). The inter-
gle plant, therefore theoretically achieving greater durability (Brar et acting effects of BPH and plant diseases on rice with the Bph14 gene
al., 2009). Breeders can use DNA profiles and genetic linkage maps to are not known.
evaluate the genomes of wild species for new and useful resistance The presence of mutualistic yeast-like endosymbionts (YLS) may
genes (Tanksley and McCouch, 1997). Numerous species of wild increase the complexity of the interactions between BPH and rice.
Oryza are genetically resistant to BPH and other insects (e.g., Jung- The intracellular endosymbionts reside in BPH's fat bodies (Chen et
Tsung et al., 1986; Romena and Heinrichs, 1989) and are a valuable al., 1981) and appear to play a role in providing protein through the
resource for plant breeders seeking resistance sources for improved recycling of uric acid stored in the fat bodies (Sasaki et al., 1996).
rice cultivars. Uric acid content in planthoppers decreases when nitrogen is unavail-
In addition to the natural sources of BPH resistance in O. sativa and able (Sasaki et al., 1996). YLS also synthesize ergosterol-5,7,24 (28)-
its wild relatives, scientists have identified numerous BPH toxins from trienol, which is a precursor of cholesterol and the molting hormone
non-rice sources that have potential in transgenic rice plants engi- ecdysone (Wetzel et al., 1992). If BPH depends on the YLS for securing
neered specifically to resist BPH. To our knowledge, no varieties of essential amino acids as Lu et al. (2004) suggested, variation in YLS in
transgenic rice are currently grown commercially although several the BPH populations might partially explain the variation in
engineered varieties have been approved for commercialization. planthopper performance on different rice varieties (Chen, 2009).
Researchers have also detected bacterial endosymbionts in BPH. for nymphal development (Horgan, 2009). When cultivars have dif-
Tang et al. (2010) identified 18 operational taxonomic units of bacte- ferent levels of resistance, nymphs will disperse between plants, the
ria representing four phyla (Proteobacteria, Firmicutes, Actinobacteria, degree of movement (activity) being negatively correlated with feed-
and Bacteroidetes) in BPH populations but did not determine their ing. Although movement between plants may appear to simulate field
function. In other species of insects, the bacterial endosymbionts responses, it is largely governed by “push–pull” dynamics in the ex-
may function as obligate nutritional mutualists, facultative mutualists perimental seedboxes (Horgan, 2009). The outcome is influenced by
that protect against natural enemies or stress, and reproductive ma- peculiarity, combinations, and relative positions of the plants in a par-
nipulators that enhance productivity of infected female lines ticular seedbox and would not be expected to remain constant be-
(Moran et al., 2008). The discovery by Tang et al. (2010) that the fre- tween successive tests (Horgan, 2009).
quencies of bacterial infections differed among the three populations
investigated (designated as BPH biotypes 1, 2, and 3) raises more Questions about the validity of the BPH biotype concept
questions about how microbial endosymbionts may affect the intra-
and inter-population variation in BPH's response to different rice Many have questioned the validity of the BPH biotype concept and
cultivars. have pointed to flaws in rice breeding objectives that target specific
BPH regional biotypes (e.g., Claridge and Den Hollander, 1980,
Screening for BPH resistance 1983; Sōgawa, 1981; Claridge et al., 1984; Denno and Roderick,
1990; Gallagher et al., 1994; Hare, 1994; Heinrichs, 1994; Roderick,
Breeders at IRRI and at other rice breeding centers in Asia have in- 1994). Considerable evidence indicates that IRRI's biotype models
corporated BPH-resistance sources in rice aimed at designated BPH bio- do not mirror the genetic variation found in natural field populations
types (Brar et al., 2009). In the greenhouse, IRRI has screened as many of BPH. Individual populations of BPH are heavily influenced by and
as 44,335 accessions for biotype 1 (15.4% resistant); 10,553 for biotype adapted to local host-plant associations. Within a 200-kilometer radi-
2 (1.9% resistant); and 13,021 for biotype 3 (1.8% resistant) (Jackson, us in Sri Lanka, for example, Claridge et al. (1982) detected substan-
1997). [IRRI has also screened thousands of accessions for resistance tial variation in response to resistant cultivars among BPH
to the WBPH, green leafhoppers, Nephotettix spp., yellow stem borer, populations inhabiting traditional and modern rice cultivars and
Scirpophaga incertulas (Walker), and striped stem borer, Chilo suppres- wild Oryza species. The BPH populations appear to contain abundant
salis (Walker) (Jackson, 1997).] The screening methods use greenhouse polygenic variation for host associated traits (Sezer and Butlin, 1998).
populations of designated BPH biotypes that vary in their virulence to Claridge et al. (1984) showed that morphological and fecundity
cultivars with different plant resistance genes (Gallagher et al., 1994). differences between BPH biotypes are largely lost after one genera-
Biotype numbers correspond to the rice genes for resistance. Popula- tion on a common rice cultivar. The differences among designated
tions of a particular biotype are maintained in the greenhouse. For ex- biotypes appear to be mostly environmentally induced and may be
ample, cultures of BPH maintained on the rice variety Mudgo with the because of nutritional differences across cultivars. Studies reviewed
Bph1 gene and on the variety ASD7 with the bph2 gene are designated by Roderick (1994) indicate that there is minimal genetic difference
respectively biotype 1 and biotype 2 (Pathak and Saxena, 1980). Bio- among the BPH biotypes, and short periods of selection can alter
type 1 is susceptible to all BPH-resistance genes. Biotype 2 is virulent their survival and performance. Furthermore, there is not a one-to-
to the Bph1 gene but susceptible to the other genes, biotype 3 is virulent one correspondence between a single gene in a BPH biotype and
only to bph2, and biotype 4 is virulent to both Bph1 and bph2 but not any single gene for resistance in the rice host (Roderick, 1994).
Bph3 or Bph4 (Khush, 1984). On the other hand, the critics have yet to establish practical cost-
The conventional method for evaluating rice for BPH resistance is effective alternatives that rice breeders can use when evaluating
the standard seedbox-screening test (SSST) (Heinrichs et al., 1985; breeding lines for resistance that is best tailored for the genetic vari-
IRRI, 1996). Some rice breeding centers have modified the screening ation found in natural field populations of BPH. The breeders obvious-
protocols slightly (e.g., Kaneda et al., 1981), but the fundamental pro- ly want to release rice breeding lines and cultivars with BPH
cedures developed at IRRI in the 1970s (Heinrichs et al., 1985; IRRI, resistance that provides the best defenses against natural popula-
1996) are still used to screen rice germplasm for resistance (Brar et tions. Although they have relied on the seedbox-screening test, they
al., 2009; Horgan, 2009). Test plants are sown in rows in a seedbox recognize its limitations and in the future will likely rely increasingly
(≈60 × 40 × 10 cm). A susceptible check and resistant variety are on DNA markers for evaluating rice breeding material for BPH-resis-
also sown in rows in the same box. Seven days after sowing, seedlings tance genes. Marker-assisted selection can be used to determine the
are thinned to about 20 plants per row and infested with 2nd instar presence or absence of BPH-resistance genes in plant breeding mate-
BPH nymphs (≈ 8 per seedling) of a designated biotype (Horgan, rial (Jena and Mackill, 2008; Brar et al., 2009).
2009). When susceptible checks are killed (usually after about
1 week), plants are rated for damage on a 0–9 scale, where 0–3 is Achieving greater durability in BPH-resistant rice
classified as resistant, 4–6 as moderately resistant, and 7–9 as suscep-
tible (Velusamy et al., 1986). The modified seedbox-screening test Evolutionary models predict that the less a control tactic such as
(MSST) has also been used at some rice breeding centers. Investiga- plant resistance challenges a pest, the longer it will take for the pest
tors using the MSST infest rice seedlings 20 days after sowing with to adapt to the tactic (Gould, 1988, 1991). Management strategies
four 2nd instar BPH nymphs per plant. Plants are evaluated when sus- that integrate natural enemies and other tactics alongside plant resis-
ceptible checks are killed, using the SSST rating scale to identify rela- tance would theoretically reduce the rate at which BPH adapts to re-
tive levels of BPH resistance. With the MSST, F1 BPH nymphs cause sistant rice. Rotating different cultivars between planting seasons,
mortality of the susceptible check as the original nymphs have had planting multiple resistant lines within the same field, combining dif-
time to mature and reproduce in the seedboxes (Horgan, 2009). ferent resistance genes with the same cultivar, and other schemes
The screening methods offer the planthoppers a choice among used singularly or in combination may have potential in slowing
plants (the accession of unknown resistance, resistant check, and sus- BPH's adaptation to resistant rice (e.g., Hare, 1994). Breeding for
ceptible check) before initiating feeding (SSST and MSST) or oviposi- moderate or polygenic resistance to BPH may be a better strategy
tion (MSST) responses (Horgan, 2009). However, the SSST, which is for achieving durable resistance than a strategy that seeks high resis-
more widely used, only evaluates nymphal feeding responses. The tance from a single major gene (e.g., Heinrichs, 1986; Bosque-Pérez
MSST improves on the SSST by allowing nymphs to develop to adults, and Buddenhagen, 1992; Alam and Cohen, 1998; Xu et al., 2002).
when they can oviposit, presumably in response to cultivar suitability QTLs were found to confer durable BPH resistance in IR64 (Alam
and Cohen, 1998) and Teqing (Xu et al., 2002) and therefore would cultivar may enhance the beneficial effects. Sōgawa (1982) showed
seem to offer considerable potential increasing the durability of resis- that rice cultivars resistant to the BPH reduce the insect's growth
tant cultivars. rate and stimulate increased probing and movement on plants. Both
Plant pathologists have demonstrated that some diseases of small the reduced growth rate and increased activity may affect natural
grains may be less severe in crop mixtures (multiline cultivars and cul- enemy response. By keeping the planthopper populations small, the
tivar mixtures) than in pure stands (e.g., Mundt, 2002). In field studies resistant plants prevent some predators from exhibiting a strong nu-
in China, rice blast disease caused by the fungus Pyricularia oryzae was merical response in resistant rice (Stapely et al., 1979; Kenmore et al.,
94% less severe in mixtures of rice than in pure stands (Zhu et al., 1984; Döbel and Denno, 1994). Simultaneously, the resistant plants
2000a). Disease-susceptible rice varieties planted in mixtures with re- increase BPH's risk of being eaten by visually responsive lycosid spi-
sistant varieties had 89% greater yield than when planted alone. Mixing ders that react to moving prey (Kenmore et al., 1984). Kartohardjono
rice varieties may be an effective alternative to fungicides and may also and Heinrichs (1984) found that lycosid spiders captured more prey
reduce the dependence on high levels of plant disease resistance (Zhu et on resistant than susceptible cultivars. Senguttuvan and Gopalan
al., 2000a). As Mundt (2002) discussed, cultivar mixtures are more use- (1990) reported that the predator C. lividipennis is more effective
ful under some conditions than others, and experimental methodology against the BPH on resistant cultivars than susceptible cultivars,
(especially problems of scale) may be crucial in evaluating the potential which they attributed to greater BPH activity on resistant plants.
efficacy of mixtures on disease. In the Mekong Delta, Vietnam, Cuong et al. (1997) tallied the
Mixing a BPH-resistant cultivar with a susceptible cultivar may also populations of BPH, whitebacked planthopper, green leafhoppers, he-
have promise; mixing the two together would theoretically slow the mipteran and spider predators, and rice yield on rice cultivars suscep-
rate at which the pest adapts to the resistant cultivar (Atsatt and tible, moderately resistant, and highly resistant to the BPH under
O'Dowd, 1976; Gould, 1986). This is because in a homogenous planting insecticide-treated and insecticide-free conditions. BPH outbreaks
of only resistant plants all members of a pest population will be exposed and hopperburned plants occurred only in plots of the insecticide-
to the resistance factor. By contrast, in a random mixture of 50% resis- treated susceptible cultivars. Rice yield in insecticide-free plots was
tant plants and 50% susceptible plants, only half of the pest population lower in the BPH-susceptible cultivars than in the resistant cultivars
will be exposed to resistant plants. Of course, this assumes that equal only in 1 of 4 seasons. In plots of a moderately resistant cultivar and
numbers of pests initially colonize the resistant and susceptible culti- a highly resistant cultivar, populations of the three pests and preda-
vars, which may or may not be the case. tors were generally similar. Furthermore, rice yield did not differ
We did not find published information from field studies that under either the insecticide-treated or insecticide-free conditions. In
compared the effects of random mixtures (two or more rice cultivars) insecticide-free plots, predator–BPH ratios were generally higher on
versus pure stands (one rice cultivar) on BPH population develop- resistant cultivars than susceptible cultivars. The results of Cuong et
ment or plant damage. In greenhouse studies, Weerapat et al. al. (1997) suggest that susceptible cultivars left untreated will not
(1977) found that BPH caused less damage to a susceptible variety necessarily incur BPH damage even if adjacent rice is experiencing
(RD7) when it was mixed with a resistant variety (RD9). The re- BPH outbreaks. They also suggest that moderate and high levels of re-
searchers infested seedling plants (two leaf stage) with large num- sistance were not incompatible with biological control of BPH, white-
bers of 1st instar BPH nymphs and recorded plant damage 10 days backed planthopper, or green leafhopper. However, not all insect
later. When the two varieties were isolated from one another in ho- resistant cultivars are necessarily equally attractive or more attractive
mogeneous plantings, 100% of the RD7 plants were BPH damaged to natural enemies than non-resistant cultivars. Luo et al. (2006), for
while none of the RD9 plants were damaged. In a mixture of 50% example, found that the BPH parasitoid Anagrus nilaparvatae (Pang et
RD7 plants and 50% RD9 plants, only 18% of the RD7 plants were dam- Wang) was less attracted to JA-treated resistant (IR26 and IR64) than
aged. Weerapat et al. (1977) did not speculate why mixing the sus- JA-treated susceptible rice cultivars (TN1, B97-59, XS63) in laboratory
ceptible and resistant varieties provided protection to the and field tests.
susceptible variety. A number of factors could have contributed. In To our knowledge, there have been no comprehensive field as-
natural settings in the wild or in agricultural polycultures, neighbor- sessments to compare arthropod community structure in BPH-resis-
ing plants sometimes act as natural pest repellents, mask the herbi- tant and BPH-susceptible rice. Given that Philippine and Indonesian
vores’ preferred host plants, or reduce the time herbivores remain irrigated fields, for example, have more than 640 and 760 taxa of
on their host plants (e.g., Pimentel, 1961; Tahvanainen and Root, macroinvertebrates, respectively (Cohen et al., 1994; Settle et al.,
1972; Root, 1973; Andow, 1991; Barbosa et al., 2009). 1996), and that Indian irrigated rice supports at least 92 and 84 taxa
The most urgent challenge in achieving durability is to convince of spiders and hymenopteran parasitoids, respectively (Beevi et al.,
farmers to stop using insecticides to control BPH on rice that is resis- 2000; Sebastian et al., 2005), the lack of community-level assess-
tant to the pest. Breeding efforts aimed at boosting the rice's genetic ments is not surprising.
defenses against the BPH are a poor investment if farmers continue The ideal form of plant resistance may be when the resistant cul-
to apply insecticides to the resistant plants (Gallagher et al., 1994). tivars suppressed the pests and simultaneously benefited natural en-
Chemical control of BPH on resistant rice is an unnecessary invest- emies. A high level of pest resistance may not be necessary, since the
ment for farmers, is potentially harmful to humans and the environ- partial resistance would be potentiated by actions of natural enemies.
ment, and, according to Gallagher et al. (1994) and Heinrichs Cultivars with partial resistance would put less selective pressure on
(1992), could speed up BPH's adaptation to the resistant plants. the BPH and would theoretically delay its adaptation to the resistant
rice. However, the simulation models of Gould et al. (1991) and Johnson
Integrating plant resistance and biological control and Gould (1992) suggest that natural enemies could actually acceler-
ate the rate at which some insect pests adapt to resistant plants. Deter-
Even if natural enemies are protected from insecticides and crop- mining optimal strategies for combining plant resistance and biological
ping practices are favorable for their increase, they will not perform control in BPH management requires much more research.
satisfactorily on inhospitable plants (e.g., Hare, 1992; Bottrell et al.,
1998). Results of several studies indicate that different rice cultivars Effects of regional and local landscape patterns on BPH
can differentially affect BPH's natural enemies (e.g., Kartohardjono
and Heinrichs, 1984; Senguttuvan and Gopalan, 1990; Rapusas et Agricultural landscapes function as a mosaic patchwork of habitats
al., 1996). One cultivar may discourage or even cancel the potentially that include the dominant crop, other crops, fallow fields, wild vege-
beneficial effects of a natural enemy. On the other hand, a different tation, and, often, aquatic systems. Both wild and cultivated plants
neighboring a crop field may affect pests and vectors, natural ene- metapopulation model that incorporated both natural enemy and pest
mies, and other biological components of the agroecosystem (e.g., population movements, Ives and Settle (1997) found that asynchronous
Bunce et al., 1993; Pickett and Bugg, 1998; Landis et al., 2000; New, crops with predators migrating between fields lowered pest densities
2005). In the Mekong Delta, Vietnam, Wilby et al. (2006) analyzed more than synchronous crops without migrating predators. Moreover,
plant–arthropod relationships in a rice-dominated landscape along they found that pest populations will be reduced if predators move
two 10-km long transects and found a complicated (and sometimes into fields early and exploit alternate prey. In other human-managed
confounding) association between landscape heterogeneity (vegeta- ecosystems, heterogeneous landscapes are less prone to insect pest out-
tion and crop richness, rice, and uncultivated cover) and arthropod breaks than homogeneous landscapes (e.g., Su et al., 1996; Cappuccino
diversity. In habitat-by-habitat comparisons, Wilby et al. (2006) et al., 1998; Jactel et al., 2002). Theoretical and empirical studies suggest
found that maturing rice (near the flowering or ripening stages) sup- that heterogeneous landscapes allow mobile generalists—characteristic
ported greater arthropod diversity than rice in other stages (seedling, of the arthropod predators and many insect parasitoids that frequent
tillering, stubble, and ratoon). The maturing rice also supported rice in tropical Asia—to increase rapidly in response to increasing pest
greater arthropod diversity than other crop species (e.g., vegetables, abundance (i.e., “birdfeeder effect”) and play key roles in stabilizing
flowers, and fruits), especially if the other crops received high pesti- food webs (Kondoh, 2003; McCann et al., 2005; Eveleigh et al., 2007).
cide inputs. Wilby et al. (2006) hypothesized that natural enemy di- In agroecosystems, birdfeeder effects can be triggered by farmer inter-
versity and effectiveness may be maintained even in regions of ventions that encourage pest outbreaks. For example, in farmers’ fields
expanding rice monoculture if pesticide and fertilizer inputs are low at Zaragoza, Philippines, deltamethrin sprays triggered outbreaks in
and there is no large-scale synchronous fallow. three delphacid planthoppers: BPH, WBPH, and Tagosodes pusanus (Dis-
tant). During the 21-day spray interval, predator populations plum-
Synchronous or asynchronous planting? meted, then rebounded in the sprayed plot, eventually outnumbering
predators in the unsprayed plot (Schoenly et al., 1996). At this site,
The debate about which large-scale cropping pattern—synchro- rice farmers have been forced to adopt the asynchronous planting sys-
nous or asynchronous planting—maintains lower pest densities year tem due to the uneven availability of irrigation water (Loevinsohn et
round in tropical rice landscapes has raged for decades (e.g., Dyck et al., 1993).
al., 1979; Oka, 1988; Loevinsohn et al., 1993; Way and Heong, 1994; Asynchronous cropping offers the advantage of creating continu-
Settle et al., 1996; Ives and Settle, 1997; Schoenly et al., 2010). Histor- ous refuges for migrating arthropods. However, its deployment over
ically, policy makers have recommended wide-scale synchronous large areas results in less efficient use of irrigation water (Loevinsohn
planting to deprive rice pests food and refuges into which they et al., 1993; Litsinger, 2008) and it may increase problems with rice
could invade after planting. Synchronous cropping, which creates a rats, Rattus argentiventer (Robinson and Kloss), (Lam, 1983; Stenseth
rice-free fallow lasting 1–3 months (usually between the dry and et al., 2003) and tungro virus (Wada and Nik, 1992; Cabunagan et al.,
wet seasons), is widespread due to the need to conserve water in 2001). Furthermore, the asynchronous system may increase certain
the dry season; whereas, asynchronous cropping creates a heteroge- mosquito-borne diseases (Mogi and Miyagi, 1990) by extending pro-
neous mixture of cultivated and temporarily unused fields and is duction of vector mosquitoes that prefer newly planted or harvested
common where irrigation systems are less efficient or have slower fields with short or sparse vegetation (Heathcote, 1970; Chandler
water delivery rates (Litsinger, 2008). Fallowing reportedly disrupts and Highton, 1975).
insect pest life cycles (Dyck et al., 1979; Oka, 1988; Loevinsohn et
al., 1993) and reduces leafhopper-transmitted disease (Wada and Role of non-rice vegetation
Nik, 1992; Cabunagan et al., 2001). Synchronous cropping allegedly
promotes rapid population buildup of the BPH and green leafhopper To what degree wild habitats and non-rice crops affect the dynamics
N. virescens (Distant) in post-fallow, wet-season crops (Widiarta et of BPH and its natural enemies in nearby rice fields is poorly understood
al., 1990). Synchronous cropping may produce more frequent and in- at both the local spatial scale and across the broader landscape. In some
tense pest outbreaks and smaller and less diverse predator popula- landscapes, boundaries between habitat patches (i.e., ecotones) provide
tions than asynchronous crops (Sawada et al., 1992; Wada and Nik, population refuges and optional routes for species movements and also
1992; Settle et al., 1996). Therefore, if the fallow between cropping buffer wind and water erosion (Wiens et al., 1985; Meffe and Carroll,
seasons is prolonged and dry, it could deplete natural enemy popula- 1994). The elevated earthen mounds (bunds or levees) that surround
tions and reduce their effectiveness in controlling pests in subsequent fields of irrigated and rainfed rice may be important habitat for both
(post-fallow) crops. harmful species (e.g., weeds and rats) and beneficial organisms includ-
Schoenly et al. (2010) tested the impact of small-scale, synchronous ing natural enemies important in controlling BPH and other pests. In Sri
fallows on rice invertebrate faunas at two sites on Luzon Island, Philip- Lanka, Bambaradeniya et al. (2004) recorded 82 species of weeds in rice
pines. Invertebrates were sampled in the same fields over two cropping field bunds; 36 species were exclusive to the bunds. Some arthropods
seasons interrupted by a 6-week wet fallow at IRRI in Southern Luzon concentrate on the bunds when rice is flooded and re-enter fields
and a 12-week dry fallow at Zaragoza in Central Luzon. Except for when irrigation ceases or the rice canopy closes. Pardosa spp. and Aty-
significantly larger populations of green leafhoppers, N. virescens and pena (= Callitrichia) formosana (Oi), spiders that are dominant preda-
N. nigropictus (Stål), in post-fallow crops, as Widiarta et al. (1990) tors of BPH during the first 35 days after rice transplanting (Sahu et
recorded in wet-season crops, small-scale synchronous fallowing com- al., 1996; Sigsgaard et al., 1999), commonly transverse flooded rice
bined with molluscicide-only pesticide inputs and pest-resistant varie- fields. In the Philippines, colonies of the ant Solenopsis geminata (Fabri-
ties did not induce pest outbreaks or notably diminish populations of cius) infest bunds of irrigated and rainfed fields in large numbers and
natural enemies when embedded in asynchronous cropping on larger, prey on immature hemipterans (including planthoppers), lepidop-
regional scales (Schoenly et al., 2010). terans, and the golden apple snail, Pomacea canaliculata (Lamarck)
It might appear that the original metapopulation model of Levins (Way et al., 1998; Way and Heong, 2009). Vegetation bordering rice
(1969) and later versions (e.g., Hanski, 1991) provide theoretical sup- fields (e.g., on bunds or levees, along irrigation canals or roadsides, in
port for the synchronous rice cropping system. This is because the per- uncultivated fields, or in cultivated fields of crops other than rice) may
sistence of a metapopulation requires asynchronous dynamics of local provide important refugia for BPH's natural enemies. For example, the
genetically connected populations (Hanski, 1999). However, the Levins egg parasitoids Anagrus spp. and Oligosita spp. of rice leafhoppers and
(1969) and subsequent metapopulation models ignored the role of nat- planthoppers live in nearby Echinochloa- and Leptochloa-rich habitats,
ural enemies in mitigating pest outbreaks (Jervis, 1997). In their respectively, and move rapidly into newly planted rice (Yu et al.,
1996). Fallow fields harbor rice invertebrates that live in soil crevices spp.) and human malaria (Pao-Ling, 1984; Roger and Bhuiyan,
and remain there or move to non-rice habitats (Arida and Heong, 1990). Because of the looming water crisis, periodic drying of irrigat-
1994). Nearby water sources (irrigation canals, drainage ditches, rivers, ed rice fields may be increasingly necessary even in areas where some
and streams) harbor aquatic taxa that recolonize rice fields and influ- yield loss might be expected (Bouman, 2001; Bouman et al., 2007).
ence species richness (Roger, 1996) and also the management of dis- Although the changes may reduce problems with certain mosquitoes,
ease vectors (Mogi and Miyagi, 1990) especially during the wet they could disrupt the natural control of BPH and other pests. The
season. Although habitats surrounding rice potentially affect the rice water of irrigated rice in tropical Asia is rich in species diversity
field biota, it is not clear how and to what extent immigrants and espe- and, as discussed, includes aquatic predators important in regulating
cially predators and parasitoids from the non-rice habitats stabilize BPH populations.
pest-natural enemy dynamics in rice fields. Understanding the link in
the rice and non-rice habitats may be the key in pinpointing causes of Are BPH outbreaks the ecological consequence of natural
BPH outbreaks at local and regional scales. large-scale changes in the environment?
Isolating the rice crop in time may be highly effective in altering
the dynamics of a pest population (Kiritani, 1979; Litsinger, 1994). It is tempting to conclude that human-controlled inputs such as
For example, a rice cultivar that reaches harvest maturity in 100– insecticides or insecticides in combination with nitrogen fertilizer,
130 days would provide much less time for a vegetative pest like for example, have been totally responsible for the synchronous BPH
BPH to develop than a cultivar that reaches harvest maturity in outbreaks in tropical rice observed across many areas of Asia, shortly
180 days. Delaying the sowing and transplanting dates by 2 wks after the beginning of the green revolution and again more recently.
(May to June) in China's Yangtze Delta reduced densities of BPH im- However, less-tangible natural governing factors may have created
migrants by 70% and also reduced infection rates of rice stripe virus an environment favoring an above-average increase in the pest's
by 50% (Cheng, 2009). Similarly, planting rice at later dates in south- populations independent of the human inputs. The high overall out-
ern Japan reduced densities of SBPH, another vector of rice stripe break synchrony in the geographically separated populations of BPH
virus (Okamoto et al., 1967). Although synchronous fallowing re- could indicate that a ”Moran effect” (Moran, 1953) such as climate
portedly disrupts insect life cycles (Dyck et al., 1979; Oka, 1988; has played a role. Moran (1953) predicted that if population synchro-
Loevinsohn et al., 1993), a prolonged and dry fallow may deplete ny was driven by an environmental variable such as climate, autocor-
natural enemy populations and allow pest populations to build up relation in population fluctuations would equal the autocorrelation in
unchecked in the post-fallow crop. However, Schoenly et al. environmental noise. His prediction assumed the same linear density
(2010) found that synchronous fallowing on small-scales (several regulation on a logarithmic scale in all of the affected populations and
adjacent fields) embedded within a larger asynchronously planted that the correlation in the fluctuations between two geographically
landscape did not disrupt the effectiveness of natural enemies. separated populations would always be the same, irrespective of ini-
This was because the mixture of cultivated and temporarily unused tial population sizes. Spatial correlations in ecological variables
fields ensured between-field and between-season exchanges of rice caused by, for instance, similar climates, were initially suggested to
invertebrate populations. Low-pesticide (molluscicide only) inputs be synchronizing agents for the fluctuations in size of spatially segre-
and pest-resistant rice varieties were compatible with this practice gated populations. The Moran effect can potentially play an important
(Schoenly et al., 2010). role in driving synchrony in a wide variety of ecological phenomena
Intercropping (or polycropping) may also impact pest population regardless of scale (Koenig, 2002). In such an environment conducive
dynamics. For example, in Fujian Province, China, Lin et al. (2011) for more rapid BPH increases, natural enemies and BPH-resistant cul-
recorded 49–55% fewer planthoppers (BPH, WBPH) in rice plots inter- tivars would be expected to have less effect in regulating the BPH's
cropped with chili pepper, Capsicum sp., ginger, Zingiber officinale Roscoe, density, and natural enemy destructive insecticides would therefore
sticky maize, Zea mays L., and peanut, Arachis hypogaea L., than in rice be expected to have an above-average negative impact.
plots planted as monocultures. The authors hypothesized that the non-
rice crops could have masked the chemical and visual cues planthoppers Climate change
use to locate rice, reducing the crop's apparency to pests. The researchers
did not determine how rice yield or natural enemies were affected by the Predictions are that climate change will have adverse impacts on
intercropping. rice production through the interactive and combined effects of
high temperature and humidity, drought, salinity, and submergence
Implications of the looming water crisis (IPCC., 2007; Wassmann et al., 2009). How such abiotic stresses will
affect BPH, other pest populations, and their natural enemies and al-
Worldwide, irrigated lowland rice receives some 34–43% of the ternate prey is uncertain although limited research has provided
world's total irrigation water, or 24–30% of the world's total freshwa- some insights. In laboratory studies, survivorship of BPH eggs and
ter withdrawals (Bouman et al., 2007). Increasing water scarcity adults was lower at temperatures ≥35 °C than at 25–30 °C (Bae et
threatens the sustainability, production, and ecosystem services of al., 1987; Heong et al., 1995b). Moreover, higher temperatures affect-
rice fields and is forcing farmers and scientists to innovate more effi- ed BPH instars and populations differently (Heong et al., 1995b), per-
cient water management practices. Conventional production of irri- haps due to differential mortality rates of their intracellular symbiotes
gated rice, which evolved centuries ago, involves continuous (Bae, 1995). In the past half-century in Japan, the major rice pest
flooding of the paddies from planting to nearing harvest maturity. fauna has shifted from stem borers (1945–1965), to delphacids and
However, evidence has shown that periodic drainage of the rice fields cicadellids (1965–1995), and, more recently, to rice bugs (various
may not reduce yield and in fact may bolster yield (Singh et al., 1996; species of the families Miridae, Coreidae, Alydidae, and Pentatomi-
Guerra et al., 1998). Moreover, some studies suggest that rice yield dae) and migrant populations of delphacids including BPH and
may decline in continuously flooded intensive rice monocultures be- WBPH (Kiritani, 2006). From 1961 to 2000, the mean surface temper-
cause of reduced soil fertility (e.g., Dawe et al., 2000). Long-term ex- ature rose by 1.0 °C in Japan. Kiritani (2006) predicted that global
periments in Southeast Asia indicate that periodic drainage of rice warming could favor natural enemies (except for spiders) by increas-
fields can counter the detrimental effects of soil infertility (Dawe et ing the number of generations more than it would their prey species.
al., 2000). In China, periodic drainage reduced the volume of irriga- However, other studies have suggested that species-specific re-
tion water by 40–70% with no apparent loss in rice yield (Guerra et sponses to rising temperatures could trigger range dissociations be-
al., 1998) and also reduced larval mosquitoes (Anopheles and Culex tween pest and natural enemy populations by shifting their
phenologies, distributional ranges, or migration patterns (Peters, for migration. This is because the survivors seem to secure more ener-
1991; Heong et al., 1995b; Song et al., 1995; Song and Heong, 1997; gy and become heavier when feeding on the imidacloprid-treated
Kiritani, 2006). plants. Planthopper populations that survive imidacloprid treatment
Evaluating the responses to large-scale effects such as climate re- could theoretically migrate above-average distances and therefore
quires insights into the spatial scaling of effects on local population dy- serve as an especially important conduit in spreading imidacloprid-
namics. Testing the hypothesis that climate may have produced a resistance alleles into new areas.
Moran effect on BPH populations in recent years is difficult due to the Although insecticides appear to be the most predictable driving
sketchy published database on historical outbreaks in the tropics. Data force behind BPH outbreaks, it is doubtful that they are solely respon-
systematically recorded at representative locations for long periods of sible for outbreaks. A major gap in the insecticide-induced paradigm
time is necessary. Shu et al. (2011) studied the relationship between relates to the periodic outbreaks recorded in temperate and tropical
ENSO events (La Niña and El Niño) and outbreaks of BPH in the middle areas before the start of the green revolution. BPH outbreaks that pur-
and lower reaches of Yangtze River during the period of 1957–2009. portedly occurred in Korea as far back as AD 18 (Paik and Paik, 1977;
They found no apparent relationship in La Niña years and outbreaks. Dyck and Thomas, 1979) and in Japan as early as AD 697 or 701
However, BPH outbreaks occurred mainly in EI Niño years and 3 years (Miyashita, 1963; Grist and Lever, 1969; Konishi and Ito, 1973; Dyck
after an El Niño year. More analyses similar to those in the Shu et al. and Thomas, 1979) are taxonomically contestable because the BPH
(2011) study are needed before conclusions can be drawn about the im- was not described as a separate species until 1854 (Dupo and Barrion,
pact of large-scale events such as ENSO phenomena. 2009). Insecticides derived from naturally occurring ingredients (e.g.,
whale oil, slaked lime) were used on some Asian rice long before the
Could sunspot-related UV-radiation produce a Moran effect? green revolution (Kenmore, 1980). Nevertheless, before the 1960s
the BPH was considered a major rice pest only in Japan and
Long-term variation in the activity of sunspots has been correlated Korea (Paik and Paik, 1977; Dyck and Thomas, 1979; Kenmore, 1980;
with population fluctuations of some herbivores. Paik and Paik Heinrichs, 1994). For certain, BPH populations regularly made long-
(1977) reported that five major outbreaks of BPH and WBPH between distance migratory flights from tropical Asia northward before
1912 and 1976 in Korea correlated closely with low sunspot activity. modern insecticides were widely used on tropical rice. The recurring
They concluded that in years of low numbers of sunspots, outbreaks pre-1960s migrations of BPH into Japan and Korea suggest that signifi-
of the planthoppers would be expected. However, they did not spec- cant numbers of macropters (migratory forms) developed from more
ulate on the cause and effect relations. On the other hand, Shu et al. southerly tropical sources. Because of the infrequent pre-1960s use of
(2011), in the study in the middle and lower reaches of Yangtze insecticides in the tropics, factors other than insecticides likely triggered
River discussed above, detected no apparent relationship in sunspot the movement of northerly-bound macropterous populations.
activity and BPH outbreaks although their study spanned a shorter
time interval than the Paik and Paik (1977) study. Recommendation
Low sunspot activity leads to a thinner ozone layer and thus Collaborators from both tropical and temperate areas should de-
higher surface ultraviolet-B radiation (UV-B). UV-B is a potent elicitor sign and implement large-scale coordinated experiments in represen-
of a variety of changes in the chemistry, morphology, and physiology tative areas to determine if outbreaks and major migrations of BPH
of plants and animals. Common signals, such as jasmonic acid play (and also WBPH and SBPH) are exclusively insecticide-induced. The
important roles in the mechanisms by which plants respond to possibility of a Moran effect (Moran, 1953) related to climate events
UV-B and to damage by herbivores. Foggo et al. (2007) found that or sunspots needs to be considered alongside the effects of insecti-
the effects of UV-B may mediate the trophic links between cabbage, cides. The overarching need is to determine if the complete with-
Brassica oleracea L., its diamondback moth pest, Plutella xylostella L., drawal of insecticides from tropical rice would be sufficient by itself
and the pest's parasitoid Cotesia plutellae Kurdjumov (Foggo et al., to eliminate significant outbreaks and reduce production of macrop-
2007). We do not suggest that sunspot-related UV-radiation would elicit ters making migratory flights.
a similar tritrophic interaction in rice, and we recognize that the correla-
tion in sunspots and planthopper outbreaks reported by Paik and Paik Fertilizer inputs
(1977) may have been coincidental. However, analyses of sunspot-
related factors similar to those of Paik and Paik (1977) and Shu et al. Beginning with the green revolution of the 1960s, the continuous
(2011) in different Asian countries might prove instructive. succession of genetically improved rice monocultures in tropical Asia
enabled BPH populations to reproduce nearly year round. Heavy use
Discussion, conclusions, and recommendations of nitrogen fertilizer has increased the pest's reproductive potential in
rice. Planthoppers often remain at low densities in rice receiving high
The insecticide-induced outbreak paradigm levels of nitrogen if insecticides are not applied (e.g., Lu and Heong,
2009). Although abundant nitrogen may push populations to relatively
A compelling argument can be made to support the paradigm that high densities even in fields of BPH-resistant rice not treated with insec-
BPH outbreaks are primarily and regularly insecticidally induced on ticides (Schoenly et al., 2010), natural enemies, especially when com-
high-yielding rice cultivars in the tropics. Insecticides do not always bined with BPH-resistant cultivars (Cuong et al., 1997), usually keep
trigger BPH outbreaks in the treated fields, but frequent applications the populations below outbreak numbers in nitrogen-rich, non-hybrid
increase the likelihood because of their harmful effects on natural en- rice. However, the nitrogen-rich hybrid rice plants seem to create favor-
emies. BPH resistance to insecticides intensifies the probability of out- able conditions for BPH outbreaks in areas with large plantings of the
breaks; once significant levels of resistance emerge, farmers must hybrids (e.g., Cheng, 2009). The complete lack or low level of genetic re-
apply increasing quantities of insecticide to combat the resistant pop- sistance to planthoppers increases their susceptibility to outbreaks
ulation. The wide-scale use of imidacloprid and related compounds (Chen et al., 2005).
since the early 1990s has magnified the problem of insecticide resis- Studies in many areas indicate that rice farmers apply nitrogen fer-
tance in BPH populations in both tropical and temperate areas tilizer at rates higher than recommended. Although nitrogen fertilizer
(Matsumura et al., 2009; Heong et al., 2011). Rice farmers in several is necessary for high yield, overuse increases the likelihood of planthop-
countries have reported reduced efficacy using imidacloprid to con- per problems, contaminates the environment, and wastes money. In the
trol BPH. Furthermore, the results of Yin et al. (2008) suggest that face of increasing rice fertilizer prices, the need to focus on careful nutri-
sublethal applications of the insecticide could increase BPH's capacity ent management is greater than ever (Fischer, 1998).
Recommendation level. If BPH exists as a metapopulation, then migrations would be

Planthopper specialists should collaborate with fertilizer special- expected to repopulate areas that have experienced extinction. This
ists (and other relevant disciplines) in deriving optimal nutrient man- being the case, periodic outbreaks in source areas might be a neces-
agement practices to recommend to farmers who use high nitrogen sary natural phenomenon to ensure that sufficient numbers of
inputs to grow hybrid and non-hybrid rice. The goal should be to de- planthoppers enter migratory flights.
velop practices that minimize nitrogen inputs while simultaneously
sustaining profitable yield. Recommendation
A comprehensive Asian-wide multidisciplinary, multi-institutional
BPH migratory cycles and metapopulation dynamics coordinated effort should be launched to determine the specific triggers
leading up to planthopper migration, the resources in the habitat and
At any given time, a significant fraction of a BPH population may be climatic effects that govern these events, and the spatial scale dynamics
flightless brachypters (Kisimoto, 1965). The production of (migratory) and genetic interrelations of different subpopulations.
macropters seems to be positively density dependent, and crowding
forces individuals into microhabitats that would not otherwise be occu- Resistant cultivars and BPH biotypes
pied under low-density conditions (Denno and Roderick, 1990; Denno
et al., 1994). Applications of insecticides that unleashed BPH popula- A high percentage of the improved rice cultivars in Asia now contain
tions from their natural enemies would be expected to provoke such a genes for BPH resistance, and rice breeders continue to develop breed-
density dependent response. Under insecticide-induced outbreaks, ing lines and cultivars with resistance (Brar et al., 2009). As discussed,
large numbers of BPH would be expected to emigrate, some reaching the natural mechanisms that make the plants resistant to BPH are not
long distances. As discussed, the factors that triggered outbreaks before well understood. Clarifying how the mechanisms that confer BPH resis-
the green revolution are unclear. Were the outbreaks due to extreme tance are related to major genes or QTLs would benefit future breeding
weather events such as abnormally dry or wet periods that favored and plant resistance deployment strategies and also provide a better
the BPH but depressed its natural enemies? Another relevant issue is understanding of inter-population and inter-specific interactions on
the frequency and duration of the outbreaks. Periodic outbreaks that rice plants (Chen, 2009; Horgan, 2009; Seo et al., 2009). Studies of
lasted for short periods might indicate that the BPH was reacting to ex- inter-specific interactions suggest that BPH's response to rice and vice
treme weather or that these are merely natural phenomena triggered versa may be affected by the presence of other species of organisms.
by overcrowding, etc. Sustained synchronous outbreaks in different As discussed, Cheng et al. (2001) found that the level of resistance to
geographical areas might point to a Moran effect as discussed. Unfortu- BPH in a rice plant can decline if WBPH previously infested the plant, al-
nately, gaps in historical BPH population records since the 1960s would though the mechanisms are unknown. As also discussed, OsBi1 is an in-
probably preclude a reliable assessment except in certain locations. ducible gene implicated in the resistance to BPH (Wang et al., 2004).
Another question concerning pre-1960s BPH dynamics pertains to Whether other species of rice insects also induce OsBi1 is not known.
the migration of populations into the temperate areas of Asia. Did the The BPH-resistant gene Bph14, as discussed, mediates disease resistance
pre-1960s migrants originate only from outbreak sources (cultivated through direct or indirect recognition of pathogen-associated molecular
O. sativa or wild Oryza host plants) in the tropics or were small persis- patterns or pathogen effectors (Jones and Dangl, 2006; Takken and
tent pulses of immigrants from non-outbreak tropical sources suffi- Tameling, 2009). The interacting effects of BPH and plant diseases on
cient to fuel the BPH problem in temperate areas? Scientists have a rice with the Bph14 gene are not known.
good understanding of the intercountry migratory flight patterns of The presence of mutualistic yeast-like endosymbionts may further
BPH (Turner et al., 1999; Otuka, 2009; Watanabe et al., 2009), al- increase the complexity of the interactions between BPH and rice. The
though the specific conditions that produce macropters in the popu- YLS appear to play a role in providing protein through the recycling of
lations and activate migrations are not well understood. As uric acid stored in the fat bodies (Sasaki et al., 1996) and synthesizing
discussed, the production of migratory forms seems to be positively ergosterol-5,7,24 (28)-trienol, which is a precursor of cholesterol and
density dependent, and crowding forces individuals into microhabi- the molting hormone ecdysone (Wetzel et al., 1992). Variation in YLS
tats that they would not otherwise occupy under low-density condi- in the BPH populations might partially explain the variation in
tions. Unfortunately, factors other than insecticides that may trigger planthopper performance on different rice varieties (Chen, 2009).
density dependent responses that lead up to crowding and migration The discovery by Tang et al. (2010) that the frequencies of bacterial
have not been well documented. infections differed among the three populations investigated (desig-
The northern limit of the winter breeding area for BPH popula- nated as BPH biotypes 1, 2, and 3) raises more questions about how
tions is around the Red River Delta of Vietnam (Kisimoto, 1976). microbial endosymbionts may affect the intra- and inter-population
The genetic analysis by Mun et al. (1999) indicated that populations variation in BPH's response to different rice cultivars.
south of the Red River Delta experienced regular mixing but were dis- Devising deployment strategies that extend the life of the resistant
tinct from populations to the north, which contribute to yearly migra- cultivars offers many untried opportunities. Pyramiding two or more
tions to temperate areas of Japan, Korea, and most areas of China BPH-resistance genes into a single plant (Brar et al., 2009), planting
(Kisimoto, 1976; Otuka, 2009). The genetic connectivity within sub- multiple resistant lines within the same field, mixing pest-resistant
populations of each of the two geographical populations suggests cultivars with pest-susceptible cultivars, ecological engineering strat-
that BPH functions as a larger metapopulation. The theoretical pest egies that increase and conserve natural enemies (e.g., Gurr et al.,
model of Ives and Settle (1997) assumed that the insect functions in 2004; Gurr, 2009), seeking more “natural enemy” friendly rice varie-
this manner. In the metapopulation scenario as originally described ties, and other deployment strategies might reduce BPH pressure on
by Levins (1969), a group of genetically connected subpopulations rice and prolong the life of resistant cultivars. However, any of these
will occupy spatially discrete areas. One subpopulation may go ex- efforts are a poor investment if farmers continue to apply insecticides
tinct but other subpopulations will remain to supply individuals to the resistant plants. Any deployment strategy aimed at extending
that disperse and repopulate empty patches. How long a subpopula- the life of resistant cultivars must have a companion effort to stop un-
tion survives in a given area depends on the relationship in the rate necessary insecticide use on rice.
of extinction and the rate in which immigrants repopulate it. Hanski An important need is the development of new evaluation methods
(1991) showed that persistence of a metapopulation in a variable en- and conceptual guidelines that plant breeders can use when evaluat-
vironment requires asynchronous dynamics of local populations, dis- ing rice for BPH resistance and releasing breeding lines and new cul-
persal among them, and an optimal density at the local population tivars tailored for the genetic variation found in natural populations
of BPH. Breeders will likely rely increasingly on DNA markers to eval- An Asian-wide multidisciplinary, multi-agency approach
uate rice for BPH resistance (Jena and Mackill, 2008; Brar et al., 2009).
Evaluating novel resistance mechanisms such as natural enemy at- The seminal work of Kenmore (1980) and Kenmore et al. (1984)
tractiveness will require entirely new methods. It is important that clearly showed that BPH in the Asian tropics normally resides at low
entomologists and breeders find common ground to resolve their dif- densities but always has the potential to erupt into outbreak num-
ferences on the concept of BPH biotypes. Beginning with the seminal bers. Once the outbreaks start, little can be done to stop them. Past ef-
discovery of Claridge et al. (1984), evidence suggests that the differ- forts to avert outbreaks have not been sustainable. The current
ences between BPH biotypes are to a great extent environmentally in- unilateral use of insecticides to remedy the situation is futile and
duced perhaps because of nutritional differences between the rice will only perpetuate recurring outbreaks—that much is clear. Other
cultivars on which they develop. Considerable evidence has shown factors contributing to the outbreaks are less clear.
that IRRI's biotype models do not mirror the genetic variation found The planthopper problem is so complex and so widespread geo-
in field populations of BPH. graphically that no one institution can begin to understand the total-
ity of factors leading up to outbreaks and migrations or to devise a
Recommendation management strategy for all situations. Considerable research is
Entomologists and breeders need to collaborate in establishing needed, ranging from the basic molecular level to the international
concepts and evaluation methods to ensure that rice breeding lines landscape level, and new and coordinated surveillance and forecast-
and cultivars are released in new areas only after they have been eval- ing methods will be required to understand and predict outbreaks
uated for resistance that reflects the genetic variation in the natural and migrations between countries.
BPH populations targeted. They also need to collaborate in devising The most important immediate need is for all of the affected coun-
evaluation and deployment strategies explicitly aimed at extending tries to take coordinated actions on large spatial scales to reverse the
the longevity of BPH-resistant cultivars. pesticide-use treadmill. Unless this is done, the chemical industry will
continue to dictate crop protection practices to farmers, unnecessary
insecticide use will proliferate, and planthopper outbreaks will recur.
Asian landscapes and climate change Educational programs to increase the farmers’ awareness of the futil-
ity of the unilateral chemical control are needed to counter the chem-
Climate change, diminished water resources, loss of wild habitat, ical companies’ influence. However, deriving the best approach to
and other changes in the future could have profound effects on the farmer training and participation in the future poses some complex
Asian landscape. Future research will need to address a number of is- questions. For example, why did farmers that had profited from the
sues regarding how best to manage rice in the background of these IPM training or FPR participation resume their former insecticide-
changes. How climate change will affect planthoppers and other rice use patterns? Was the chemical industry's marketing campaign solely
pests is not clear. Because individual pest species do not experience responsible for the change? Would the farmers have resumed their
climate change in isolation from other species, whole community former insecticide-use patterns even if not influenced by the chemical
studies over multiple years will be necessary to understand the ef- marketing campaigns perhaps because they perceived that the crops
fects of changing climate in different Asian environments. Shrinking eventually deteriorated when not treated? Or did the lack of re-
irrigation water will certainly force farmers in many areas to adopt ir- sources in the affected countries prevent national plant protection
rigation practices that include periodic drying of the irrigated rice services and pesticide regulatory agencies from sustaining the IPM
fields. As discussed, in tropical irrigated rice of Asia, a number of pred- and FPR efforts initiated in the 1980s and 1990s?
ators that attack BPH and other rice pests are aquatic (e.g., Kenmore,
1980; Kenmore et al., 1984; Nakasuji and Dyck, 1984; Reissig et al.,
1986; Almazan and Heong, 1992; Settle et al., 1996; Schoenly et al., Recommendation
1998; Dupo and Barrion, 2009). Therefore, research is needed to ex- A comprehensive Asian-wide multidisciplinary, multi-institutional
amine how changes in irrigation contribute to planthopper outbreaks coordinated effort is necessary to develop a planthopper management
and what measures might be available to mitigate the negative ef- strategy that achieves long-term sustainability. The management strat-
fects. Shrinking water sources will also force farmers that now prac- egy should evolve under an umbrella of cooperative efforts between the
tice asynchronous cropping in many areas to shift to more water- affected tropical and temperate countries and all relevant disciplines
efficient synchronous cropping. Research is needed to determine and agencies. The strategy obviously must include provisions for
how this change in planting scheme and how different intercropping addressing the prevailing pesticide problem and implementing educa-
manipulations (e.g., rice with maize, ginger, peanut, chili pepper, etc.) tional programs and legislation to stop unnecessary and environmen-
will affect planthoppers. Additional research is required to determine tally unsound use of insecticides on rice.
the link in rice and nearby wild habitat. Wild vegetation surrounding
rice fields may harbor certain pests such as rats that negatively affect
the rice crop or provide breeding habitat for arthropod vectors of Acknowledgments
human disease. On the other hand, wild vegetation may provide im-
portant caches for many species of natural enemies including those We are grateful to Jiaan Cheng, Michael B. Cohen, Kong Luen Heong,
critical in controlling BPH and other rice pests. Peter E. Kenmore, James A. Litsinger, Kazushige Sōgawa, Yoo-Han Song,
and an anonymous reviewer for commenting on drafts of this article; to
Recommendation Gene Hettel, Lea Delos Reyes, and Mila Ramos of the International Rice
Collaborators of the relevant disciplines should reassess pest man- Research Institute, Deborah Childers and Julie Reuben of the California
agement practices at both local and regional levels to deal with the State University, Stanislaus, and the University of Maryland University
new combinations of stresses that changes in climate and other fac- Libraries for providing valuable assistance in securing published materi-
tors will impose, especially in irrigated rice where water supplies al used in the review; and to Shuqi He for translating main points of the
are becoming increasingly scarce. Future assessments of rice pest Shu et al. (2011) article from Chinese to English. We dedicate this re-
management need to be coordinated with human disease and vector view to the late Robert F. Denno, renowned ecologist and international-
management practices (Service, 1989; Roger and Bhuiyan, 1990) to ly respected scientist extraordinaire whose exceptional contributions
determine how such overlapping deployments affect planthopper on delphacids will forever stand out in the chronicles of planthopper
dynamics. ecology and management.
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Journal of Asia-Paciﬁc Entomology 15 (2012) 122–140

Contents lists available at SciVerse ScienceDirect

Journal of Asia-Paciﬁc Entomology

Resurrecting the ghost of green revolutions past: The brown planthopper as a

Background to problem . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 123

Achieving greater durability in BPH-resistant rice. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 129

Synthesis Concerns with fertilizer use on hybrid rice

Recommendation level. If BPH exists as a metapopulation, then migrations would be

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