- Email: [email protected]
Rice water weevil (Coleoptera: Curculionidae) in mainland China: Invasion, spread and control
ARTICLE IN PRESS
Crop Protection 24 (2005) 695–702 www.elsevier.com/locate/cropro
Review
Rice water weevil (Coleoptera: Curculionidae) in mainland China: Invasion, spread and control Hong Chena,, Zhongmei Chenb, Yongshu Zhoub a
Department of Biology, State University of New York-Buffalo, 109 Cook Hall, Buffalo, NY 14260, USA b Plant Quarantine Institute, Beijing 100029, China Received 26 March 2004; received in revised form 29 November 2004; accepted 1 December 2004
Abstract The rice water weevil, Lissorhoptrus oryzophilus Kuschel, is the most important species among invasive insects in China. The parthenogenic weevil, first detected in Tanghai County of Hebei Province in 1988, has become one of the major rice pests in China with yield loss of 10–80%. Since then, the pest has expanded its range of infestation at a rate of 10–30 km/year. This pest has been found in eleven provinces and two large municipal areas infesting over 400,000 ha by late 2003. Quarantine measures did not effectively limit the spread of rice water weevil due to its parthenogenesis, flying, swimming and hitchhiking on human transportation. The weevil’s life history, population dynamics, host–plant relationships and mode of establishment have been studied at a number of locations. Currently, the pest is managed by integration of insecticides, water management, delayed transplanting, blacklight trapping, application of Beauveria bassiana and Metarhizium anisopliae spores and rice cultivars with tolerance to the rice water weevil. r 2005 Elsevier Ltd. All rights reserved. Keywords: Lissorhoptrus oryzophilus; Invasive species; Insect pest; Distribution; Quarantine; Control
Contents 1. 2.
3.
4.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1. Economical and ecological impacts of the rice water weevil in mainland China Invasion and spread of the rice water weevil in mainland China . . . . . . . . . . . . . . . 2.1. Invasion and spread . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Potential distribution in mainland China . . . . . . . . . . . . . . . . . . . . . . . . . . . Host plants and life history of the rice water weevil in mainland China . . . . . . . . . . 3.1. Host plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Phenology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Quarantine and control of the rice water weevil in mainland China . . . . . . . . . . . . . 4.1. Quarantine and isolation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Insecticidal control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Cultural practices for control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4. Physical control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5. Biological control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.6. Tolerant rice cultivars . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Corresponding author. Tel.: +1 716 645 2363x123; fax: +1 716 645 2975.
E-mail address: [email protected] (H. Chen). 0261-2194/$ - see front matter r 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2004.12.005
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
696 696 697 697 698 698 698 699 699 699 699 699 700 700 700
ARTICLE IN PRESS 696
H. Chen et al. / Crop Protection 24 (2005) 695–702
5. Future research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 700 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 700 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 700
1. Introduction The rice water weevil, Lissorhoptrus oryzophilus Kuschel, is endemic to the southern United States, where the beetle reproduces sexually and feeds on gramineous and cyperaceous weeds as its native hosts. The weevil’s damage to introduced rice was reported in Georgia in the early 1880s (Webb, 1914; Isely and Schwardt, 1934). For over 100 years, this weevil has been the most destructive insect pest of rice since its host shift to rice in North America (Webb, 1914; Zhou, 1987; Sun et al., 1996). In the late 1950s, a parthenogenic population of L. oryzophilus was found in northern California (Lange and Grigarick, 1959). From there the parthenogenic rice water weevil was carried across the Pacific into Asia in the mid-1970s (Japan Plant Protection Association, 1986). Webb (1914) and Isely and Schwardt (1934) summarized early studies on taxonomy, life cycle, host plants, economic importance and control of the rice water weevil in the United States. Insecticides remain the most effective means of controlling the rice water weevil (Stout et al., 2002a). Since the withdrawal of carbofuran, the four insecticides, fipronil, lambda-cyhalothrin, zetacypermethrin and diflubenzuron, have been registered for use against the rice water weevil. Fipronil, which will be dropped from the United States market after 2004, is used to treat rice seeds and kills the larvae (Bernhardt, 1999; Way and Wallace, 1999b; Stout et al., 2000), lambda-cyhalothrin, zetacypermethrin and diflubenzuron are applied as post-flood sprays for the adults, and diflubenzuron targets the eggs (Way and Wallace, 1999a; Stout et al., 2000). Recently, cultural control strategies, such as timing of planting (Barbour et al., 1993; Thompson et al., 1994a; Wu and Wilson, 1997; Stout et al., 2002c) and water management (Thompson et al., 1994b; Rice et al., 1999; Stout et al., 2002b; Zou et al., 2004), have been applied against the rice water weevil. Studies on integrated population management of the rice water weevil included weevil–host interaction (Thompson and Quisenberry, 1995; Wu and Wilson, 1997; Tindall and Stout, 2003; Tindall et al., 2004), rice plant resistance (N’Guessan and Quisenberry, 1994; N’Guessan et al., 1994a; Stout et al., 2001) and tolerance to the weevil (N’Guessan et al., 1994b; Stout et al., 2002b). The invasion of parthenogenic L. oryzophilus, which presumably ‘‘hitchhiked’’ across the Pacific into Asia from California, was first reported in Aichi Prefecture, Japan in 1976 (Japan Plant Protection Association, 1986). Ten years later, the rice water weevil spread
2000 km throughout the Japanese Archipelago (Iwata, 1979; Japan Plant Protection Association, 1986; Matsui, 1987). In Aichi the weevil was univoltine and the overwintered adults immigrated into rice paddies during May and June when daytime temperature exceeding 20 1C. By late July the eggs and larvae were found in paddies (Japan Plant Protection Association, 1986; Matsui, 1987). In southern Japan the weevil was bivoltine with very low larval densities on late-planting rice seedlings (Matsui, 1987). Larvae in both seedling nursery boxes and paddies were controlled with Carbosulfan and Cartap granules. Cultural control, such as transplanting of mature seedlings with higher tolerance to the pest and drainage for 15 days in paddies was also used against the rice water weevils. Among 150 rice varieties grown in Japan, a few of them showed high tolerance to the weevil (Japan Plant Protection Association, 1986; Matsui, 1987). In 1988, the parthenogenic rice water weevil was recorded in mainland China and the Korean peninsula, whereas the initial occurrence of rice water weevil in Taiwan was reported Taoyuan County in March 1990 (Sun et al., 1996). In Korea the weevil was primarily univoltine and a partial secondgeneration occured in some years (Li, 1993; Sun et al. 1996). Direction and speed of the weevil’s dispersal in Korea were affected by wind, mountain and ground transportation (Uhm et al., 1989). Quarantine measures to contain the rice water weevil were not successful in the early stage of rice water weevil invasion into eastern Asia. At this time, primary control of the pest in eastern Asia is focused on insecticide applications (Zhang, 1989; Li, 1993; Sun et al., 1996; Ministry of Agriculture, 2003). The range of rice water weevil infestation is expanding, and its spread into other rice producing regions is highly probable if this trend continues, posing a global threat to rice production (Stout et al., 2002a). 1.1. Economical and ecological impacts of the rice water weevil in mainland China Among some dozen exotic insect pests causing significant economic impacts in mainland China since the late 1970s (Xie et al., 2000), the rice water weevil draws the most attention and effort, because rice is the most important crop in China. The total area for rice production in China exceeds 33.3 million ha annually, from which the total annual rice production ranged from 171 million to 191 million tons in the past decade, accounting for about 35% of the world’s total (General Station of Plant Protection, 1988; IRRI, 2004). In 1986, the Chinese Ministry of Agriculture listed the rice water
ARTICLE IN PRESS H. Chen et al. / Crop Protection 24 (2005) 695–702
weevil as a quarantine pest before the initial detection of the weevil in China (Zhou, 1987). According to the plant quarantine and protection regulations, the Chinese central and provincial governments allotted millions of dollars (in RMB yuan) and set up special teams to study and practice quarantine and management of the rice water weevil soon after its discovery, initially trying to eliminate the pest. Despite these efforts, the range of rice water weevil continues to expand in mainland China. The rice water weevil was recognized as an important invasive pest immediately after its discovery in mainland China because of the severe rice yield losses. The adults feed on the upper leaf surfaces producing longitudinal scars. Larval feeding on roots causes stunted growth, yellowing of the leaves (chlorosis) and plants that are easily uprooted, resulting in few tillers and low grain yield. In mainland China yield losses typically exceeded 10% in the established paddies, but approached over 80% in newly infested areas (Guo, 1996; Sun et al., 1996). As a newly introduced pest, the rice water weevil did not conform to the Practical System of Integrated Rice Pest Management that was established in the early 1990s to control over 385 rice insect pests nationwide (General Station of Plant Protection, 1988; Du, 1991; Zhang, 1995). The invasion of rice water weevil poses a tremendous challenge for rice production, particularly in the area of integrating the rice water weevil control into existing rice IPM programs.
2. Invasion and spread of the rice water weevil in mainland China
697
Yuhuan County, Zhejiang Province. A follow-up survey in the same year revealed that the pest had spread to 15,300 ha of paddies in Yuhuan, Wenling, Leqing, Yongjia and Tongtou Counties of Zhejiang Province (Shang and Zhai, 1997). It was assumed that the rice water weevil reached Zhejiang Province by ship from Taiwan (Sun et al., 1996). Finally, in July 1993 rice water weevil was found in Ji’an County, Jilin Province. The invasive rice water weevil appear to have flownover or hitchhiked on human transports across a distance of 500 m from North Korea (Li, 1997). Yearly surveys, conducted after an initial discovery, showed that the rate of rice water weevil expansion ranged from 10 to 30 km/year in mainland China (Li and Cui, 1996; Sun et al., 1996). The weevils from Hebei were found reaching the suburbs of Tianjin and Beijing Cities in 1990, and Dongying of Shandong Province in 1992 (Sun et al., 1996). The rice water weevil in Zhejiang dispersed southward rapidly and entered the northern region of Fujian Province in 1996 (Wang et al., 2001; Chen et al., 2002). In May 2001 the pest was found in south-central region of Anhui Province and was detected to spread southward (Fang et al., 2003). Wind, temperature and human transportation played an important role in the range and speed of weevil dispersal in China (Sun et al., 1996; Zhai et al., 1999). By late 2003, the rice water weevil had been reported in the eleven provinces of Jilin, Liaoning, Hebei, Shandong, Shanxi, Jiangsu, Zhejiang, Anhui, Fujian, Guangdong, Guangxi and Hunan, and in the two large cities of Tianjin and Beijing (Fig. 1) (Zhang, 2003). Over
2.1. Invasion and spread The rice water weevil entry into mainland China was made through four speculated routes (Guo, 1996; Li and Cui, 1996; Shang and Zhai, 1997; Sun et al., 1996; He et al., 1997; Li, 1997). First, in May 1988 the Tanghai County farmers in Hebei Province reported infestations of a weevil causing heavy rice yield loss beginning in 1986. Compared with the specimens of rice water weevils from Japan, the weevils and larvae collected in China were identified to be the parthenogenic L. oryzophilus in the same year. This identification was confirmed by scanning electronic microscopy (Chen, 1989, 1991). A 1989 survey showed that the rice water weevil infested 42,700 ha of paddies in Luannan, Tanghai, Leting, Fengnan and Luan Counties of Hebei Province. It appeared that the larvae of rice water weevil entered these areas by infested rice seedlings from Japan (Sun et al., 1996). Second, in July 1991 rice water weevil was trapped by a blacklight in Dandong City, Liaoning Province. This invasion appeared to be aided by wind from North Korea (Li and Cui, 1996; He et al., 1997). Third, in May 1993 rice water weevil was detected in
N
↑
Jilin Liaoning Hebei Beijing Tianjing Shanxi Shandong Jiangsu Anhui Zhejiang Hunan Fujian
600 km Guangxi
Guangdong
Fig. 1. Occurrence of the rice water weevil in mainland China. The circles indicate the sites where the weevil was found. The weevil was also reported from the provinces of Shanxi, Jiangsu, Hunan, Guangdong and Guangxi without detailed locations (Zhang, 2003). The dotted line indicates the northwestern boundary of the pest’s potential distribution (from Mao et al., 1997).
ARTICLE IN PRESS H. Chen et al. / Crop Protection 24 (2005) 695–702
698
400,000 ha of paddies have been infested by the pest in mainland China. 2.2. Potential distribution in mainland China Mao et al. (1997) tested the effects of low humidity (5–35% RH) and low temperature (10 to 10 1C) on mortalities of newly emerged and overwintering populations of rice water weevil. The mortalities increased as temperature or relative humidity dropped, indicating that the weevils had limited tolerances to drought and cold. The computer software CLIMEX predicted the weevil’s potential distribution in mainland China (Fig. 1). The movement of rice water weevil was blocked further north by cold winter stress in Helongjiang and Jilin Provinces and to the west at high elevation in Sichuan and Yunnan Provinces. It is hypothesized that, dry summer and cold winter stress stopped the weevil’s spread within Inter-Mongolia Region and Gansu Province in northwestern China.
families in Tanghai and Luannan Counties, Hebei Province (Table 1). Of these host plants, 15 species in 5 families support L. oryzophilus larvae (Sun et al., 1996). Liu et al. (1998) observed that the adults of rice water weevil fed on corn seedling leaves in Ji’an County of Jilin Province, but emigrated into adjacent paddies after rice was transplanted. Although the rice water weevil has a wide range of host plants, the pest feeds primarily on rice plant under paddy conditions (Sun et al., 1996; Liu et al. 1998).
JI’an, Jilin 41˚10’ N
overwintered adults eggs larvae pupae
Tanghai, Hebei 39˚20’ N
Leqing, Zhejiang 28˚10’ N 1st-generation adults
3. Host plants and life history of the rice water weevil in mainland China
2nd-generation adults
Mar.
3.1. Host plants Field and laboratory studies have shown that adults of the rice water weevil feed on 64 plant species in 10
Apr.
May.
Jun.
Jul.
Aug.
Sep.
Oct.
Fig. 2. Life cycles of rice water weevil in three locations in mainland China (compiled from Shang and Zhai, 1997; Sun et al., 1996; Li, 1997; Zhai, 1998).
Table 1 Host plants of the rice water weevil in Tanghai and Luannan Counties, Hebei Province (from Sun et al., 1996) Family
Species
Alismateae Araceae Butomaceae Commelinaceae Cyperaceae
Alisma orientale (Sam.) Juzepcz.a, Sagittaria sagittifolia L. Acorus calamus L.a Butomus umbellatus L. Commelina communis L. Carex onoei Franch. et Sav., C. tangiana Ohwi, Cyperus difformis L., C. glomeratus L., Eleocharis valleculosa Ohwia, Juncellu serotinus (Rottb.) C. B. Clarke, Pycreus sanguinolentus (Vahl) Ness, Scirpus planiculmis Fr. Schmidta, S. tabernaemontani Gmel, S. triqueter L.a Iris ensata Thunb Aeluropus littoralis var. sinensis Debeaux, Agropyron cristatum (L.) Gaertn., Agrostis stolonifera L., Alopecurus aequalis Sobol., Aneurolepidium chinense (Trin.) Kitag., Arthraxon hispidus (Thunb.) Makino, Beckmannia syzigachne (Steud.) Fernald, Calamagrostis pseudophragmites (Hall. f.) Koel, Chloris virgata Swartz, Coix lacrymajobi L., Digitaria adscendens (H. B. K.) Henr., D. sanguinalis (L.) Scop.a, Diplachne fusca (L.) Beauv.a, Echinochloa crusgalli (L.) Beauv.a, E. crusgalli var. cruspavonis (H. B. K.) Hitch.a, Eleusine indica (L.) Gaertner, Eragrostis autumnalis Keng, E. cilianensis (All.) Link, Eriochloa villosa (Thunb.) Kunth, Hierochloe odorata (L.) Beauv., Imperata cylindrica (L.) Beauv. var. major Hubb., Leersia japonica (Makino) Keng f.a, Miscanthus sacchariflorus (Maxim.) Benth. Et Hook. f., Oryza sativa L.a, Panicum miliaceum L., Parapholis incurva (L.) C. E. Hubb., Pennisetum alopecuroides (L.) Spreng., Phragmitas communis Triniusa, Phyllostachys bambusoides Sieb. & Zucc., Poa annua L., Puccinellia chinampoensis Ohwia, Roegneria kamoji Ohwi, Saccharum sinensis Roxb., Setaria italica (L.) Beauv., S. lutescens (Weigel) Hubb., S. viridis (L.) Beauv., Sorghum vulgare Pers., Spartina anglica C. E. Hubb., Themeda triandra Forsk. var. japonica (Willd.) Makino, Zea mays L., Zizania aquatica L.a Juncus bufonius L., J. effusus L., J. gracillimus (Buch.) V. Krecz. et Gontsh. Potamogeton distinctus A. Bennett Typha angustata Bory et Chaub, T. minima Funka, T. orientalis Presl
Iridaceae Gramineae
Juncaceae Potamogetonaceae Typhaceae a
Larval hosts.
ARTICLE IN PRESS H. Chen et al. / Crop Protection 24 (2005) 695–702
699
3.2. Phenology
4.2. Insecticidal control
The rice water weevil in northern Chinese provinces of Jilin, Liaoning, Hebei and Shandong is univoltine (Fig. 2) (Sun et al., 1996; Li, 1997). On the other hand, a partial second-generation emerges from early September to early October in the double-cropping rice region of Zhejiang Province in southeastern China (Fig. 2) (Shang and Zhai, 1997; Zhai, 1998). Adults of rice water weevil prefer woods, meadows and river bunds adjacent to paddy as overwintering sites (Shang and Zhai, 1997; Sun et al., 1996; He et al., 1997; Zheng et al., 1997; Ding, 2002). In Tanghai County of Hebei Province, 99% of the adults overwinter within 3 cm of the surface soil (Sun et al., 1996). Further north, in Dangdong of Liaoning Province, 70% of the weevil adults inhabit the soil layer of 4–6 cm deep during the winter (He et al., 1997). In early spring, the overwintered adults began to be active, and later immigrate into the nearby seedling beds and paddies where they feed and oviposit.
Insecticides provide the most effective means of controlling the weevil in China as they do in the United States and Japan (Stout et al., 2002a; Matsui, 1987). Since the first recorded infestation of rice water weevil in mainland China in 1988, more than 60 insecticides have been evaluated for control (Shang and Zhai, 1997; Sun et al., 1996; He et al., 1997; Wang and Liu, 1997; Zheng et al., 1997; Yang et al., 1998). Economic thresholds and insecticide application measures have been set up for different developmental stages and habits, such as the overwintering site, seedling bed and paddy (Ministry of Agriculture, 2003). In addition, pest alerts for insecticide application were generated by the predictive models, related to meteorological data, oogenesis and degeneration/regeneration of indirect flight muscle, to forecast the periods of developmental stages, and migratory flight of rice water weevil (Li and Ye, 1998; Li, 1999; Gu et al., 2003; Zhai, 1998). Insecticides have been recommended for management of overwintered adults in overwintering sites, seedling beds and paddies. Applications of isocarbophos, malathion, esfenvalerate, cypermethrin or etofenprox were used when densities of the weevil exceeded economic thresholds (Sun et al., 1996; Yang et al., 1998; Ministry of Agriculture, 2003). Granular formulations of carbofuran or isofenphosmethyl, applied to flooded paddies, were used to manage the larvae (Sun et al., 1996; Ministry of Agriculture, 2003). Due to the lower density of second-generation weevils in southern China, they were controlled by the insecticides that targeted other rice pests (Shang and Zhai, 1997).
4. Quarantine and control of the rice water weevil in mainland China 4.1. Quarantine and isolation The Chinese central and local governments made enormous efforts to block the weevil spread during the period of invasion and initial establishment. Once the rice water weevil was detected in a location, surveys were launched to map the infested area. Because the pest can survive in stored rice grain, rice straw and grass over one month (Sun et al., 1996; Shang et al., 2003), transport of host materials such as rice seeds, seedlings and plants were forbidden from areas under quarantine. Materials and goods infested by the pest had to be fumigated by sulfuryl fluoride, aluminum phosphide or methyl bromide before transported from weevil infested areas (Sun et al., 1996; Sun and Zheng, 1998; Zheng et al., 1998). Vehicles leaving a quarantine area were subjected to an application of 5% esfenvalerate (v:v ¼ 1:2000) or 20% Xin Xing Dao Le Fen (a mixture of malathion and fenvalerate) (1:1000) to kill weevils (Sun et al., 1996; Ministry of Agriculture, 2003). The isolation effort for the rice water weevil has not been successful in mainland China. By flight alone, the range of rice water weevil infestation expanded 10–20 km/year after 1988 (Sun et al., 1996). Irrigation systems, rivers and occasional hitchhiking on human transportation dispersed the weevil (Sun et al., 1996). All of these factors greatly reduce the efficacy of quarantine and isolation measures.
4.3. Cultural practices for control Although weevil management still depends heavily on insecticides, appropriate cultural practices can also contribute to pest management. Seedling nurture without flood is commonly used (Sun et al., 1996). In Zhejiang Province, exposure of leaf-sheaths of rice seedlings by field drainage, resulted in an obvious suppression of oviposition and a great reduction in net fecundity of the pest when the exposure lasted over 16 days during the early and mid-oviposition stages (Jiang and Cheng, 2003). Delayed transplanting of 3–4 weeks was also effective, because older rice plants were more tolerant to injury (Sun et al., 1996; Ministry of Agriculture, 2003). In paddies, intermittent flooding with a drainage period up to 20 days was applied to reduce oviposition because female adults lay eggs only under flooded conditions. However, this intermittentflooding method should not be used in regions with a hot and dry growing season, where rice plants can be damaged by lack of water (Sun et al., 1996). In northern China, ploughing paddies in late autumn dramatically
ARTICLE IN PRESS 700
H. Chen et al. / Crop Protection 24 (2005) 695–702
increased mortality of the overwintering adults in the soil by up to 75%, because cold winter temperature killed the adults on the ground and in the upper layer of soil (Sun et al., 1996). 4.4. Physical control Blacklight trapping was effective in controlling migrating overwintered weevils (Sun et al., 1996; Ministry of Agriculture, 2003). Weevil capture per trap per night reached several kilograms in Tanghai County, Hebei Province, in late 1980s before a chemical control program was initiated (Sun et al., 1996). In Tongcheng of Anhui Province in 2001 and 2002, over 98% of total blacklight captures occurred during April 14 and May 14 when the overwintered adults immigrated into paddies (Fang et al., 2003). 4.5. Biological control The white muscardine fungus, Beauveria bassiana, was sprayed at a rate of 150,000 1010 spores/ha to control the overwintered adults during their migrating period (Ministry of Agriculture, 2003). Although B. bassiana took two weeks after application to show control effect, the infection rate was over 60% in weevil populations (Sun et al., 1996). In Zhejinag Province Metarhizium anisopliae was also used to control weevils at pre-oviposition stage. However, the infection rate of M. anisopliae in newly emerged adults was very low (Chai et al., 2000; Chen et al., 2000). No effective predators and parasites for weevil control are known in the infested areas in China (Yu et al., 2003).
States. Those weeds grown adjacent to paddies could serve as refugia where rice water weevil populations may persist and from where they may threaten paddies. On the other hand, the more preferred weeds can be used as trap plants near paddies. For biological control, it is necessary to conduct more studies on the weevil’s natural enemies such as predators, parasites and microbial pathogens in China. More research is needed to integrate weevil control into the current rice IPM programs. International cooperation should be initiated to reduce the possibility of the weevil spread across borders and aid the newly infested countries in weevil management. Origin and spread pattern of rice water weevils may be tracked by DNA fingerprinting. Phylogeny of the parthenogenic weevil populations and their relationship with the sexually reproducing populations in North America are important for understanding weevil biology and control. These can be addressed using genetic markers and population genetic methods in the future. More importantly, as Stout et al. (2002a) suggested, the greatest need is for the development of rice lines with high resistance to the rice water weevil, using both traditional breeding and genetic engineering methods, in various parts of the world.
Acknowledgements We thank Dr. G. Zhou (SUNY-Buffalo) for the map preparation using the ArcViews GIS. Three anonymous reviewers provided constructive comments and suggestions. We also want to acknowledge Dr. K. C. Kim (Penn State) for working on our manuscript.
4.6. Tolerant rice cultivars References In Tanghai County of Hebei Province Cultivar Zhonghua 8 and indica rice cultivars were less preferred by the weevil while Cultivars Xiangdao and Jigeng 8 were susceptible to the injury by the weevil (Sun et al., 1996). Tian et al. (2003) evaluated rice cultivars grown in Liaoning Province for resistance to the rice water weevil and found that few of the cultivars showed tolerance to the pest.
5. Future research Research is needed to refine thresholds for insecticide applications and efficacy, and monitoring methods for the weevil in different infested areas. Some chemicals registered in the United States should be tested for their efficacies against the rice water weevil in China. Investigation on host preference of the rice water weevil in China may reveal more preferred weeds over rice plant as Tindall and Stout (2003) found in the United
Barbour, J.D., Muegge, M.A., Trahan, G.B., Bollich, P.A., 1993. Effect of planting date on rice water weevil: numbers of feeding scars, eggs, and larvae. LA. Rice Res. Station Annu. Res. Rep. 85, 556–558. Bernhardt, J.L., 1999. Control of rice water weevil with Icon, 1998. Arthropod Manage. Tests 24, 271. Chai, Y., Chen, Z., Feng, H., Pan, L., 2000. Bioassay of Metarhizium anisopliae on the rice water weevil. Chin. J. Biol. Control 16, 22–25 (in Chinese, with English abstract). Chen, H., 1989. Scanning electron microscopy of the female adult of the rice water weevil, Lissorhoptrus oryzophilus. Plant Quarantine 3, 177–179 (in Chinese). Chen, H., 1991. Larval cephalic characteristics of Leptinotarsa decemlineata, Sitophilus granarius and Lissorhoptrus oryzophilus. Plant Quarantine 5, 6–10 (in Chinese). Chen, Z., Feng, H., Shi, L., Liu, Y., Pan, L., Wang, G., 2000. Evaluation of Metarhizium anisopliae for control of rice water weevil in the field. Chin. J. Biol. Control 16, 53–55 (in Chinese, with English abstract). Chen, J., Zhou, L., Lin, S., 2002. Occurrence and control of rice water weevil in Fujian. Plant Quarantine 16, 312–313 (in Chinese). Ding, Y., 2002. Occurrence and control of rice water weevil in Anshan, Jilin. Plant Prot. 28, 57 (in Chinese).
ARTICLE IN PRESS H. Chen et al. / Crop Protection 24 (2005) 695–702 Du, Z., 1991. Integrated Management of Rice Pests in China. China Agric. Press, Beijing (in Chinese). Fang, H., Fang, X., Chen, C., Li, Q., Feng, J., Li, B., 2003. Occurrence of rice water weevil in south-central Anhui. Plant Quarantine 17, 215–217 (in Chinese). General Station of Plant Protection, 1988. The Development in Integrated Control of Rice Diseases and Insect Pests in China. Zhejiang Science & Technology Press, Hangzhou (in Chinese). Gu, Y., Lin, Y., Li, B., Li, Y., 2003. Prediction of occurrence period of rice water weevil by simplified temperature summation. Plant Prot. 29, 43–45 (in Chinese). Guo, S., 1996. Risk analysis and quarantine measures on rice water weevil in Hebei. Plant Quarantine 10, 288–290 (in Chinese). He, N., Li, T., Jia, J., 1997. Occurrence and control of rice water weevil in Liaoning Province. Plant Quarantine 11 (Suppl.), 30–37 (in Chinese). IRRI, 2004. http://www.riceweb.org. Isely, D., Schwardt, H.H., 1934. The rice water weevil. Bull. Arkansas Agric. Exp. Stn. 299, 1–44. Iwata, T., 1979. Invasion of the rice water weevil, Lissorhoptrus oryzae, into Japan, spread of its distribution and abstract of the research experiments conducted in Japan. Jpn. Pestic. Inf. 36, 14–21. Japan Plant Protection Association, 1986. Control of the Rice Water Weevil in Japan (in Japanese). Jiang, M., Cheng, J., 2003. Effects of starvation and absence of free water on the oviposition of overwintered adult rice water weevil. Int. J. Pest Manage. 49, 89–94. Lange, W.H., Grigarick, A.A., 1959. Rice water weevil, beetle pest in rice growing areas of southern states discovered in California. Calif. Agric. 13 (8), 10–11. Li, H., 1993. Life cycle of rice water weevil in central North Korea. Plant Quarantine 7, 115 (in Chinese). Li, T., 1997. The rice water weevil in Ji’an. Plant Quarantine 11, 373 (in Chinese). Li, X., 1999. Use meteorological data to forecast the life cycle of the first-generation rice water weevil. Plant Quarantine 13, 277–278 (in Chinese). Li, J., Cui, S., 1996. Spread of rice water weevil in the areas adjacent to North Korea. Plant Quarantine 10, 242 (in Chinese). Li, X., Ye, K., 1998. Prediction of migratory flight and oviposition of overwintered adult of rice water weevil by meteorological data. Plant Quarantine 12, 330–332 (in Chinese). Liu, Y., Kang, R., Zheng, L., 1998. Rice water weevil feeding on corn. Plant Quarantine 12, 379 (in Chinese). Mao, Z., Sun, R., Dou, X., Chen, H., Zhou, M., Gui, G., Wu, C., 1997. Effects of low humidity and temperature on the mortality of rice water weevil and its potential distribution in China. Plant Quarantine 11 (Suppl.), 26–29 (in Chinese). Matsui, M., 1987. Expansion of distribution area of the rice water weevil and methods of controlling the insect pest in Japan. Jpn. Agric. Res. Q. 20, 166–173. Ministry of Agriculture, 2003. A Guide to the Rice Water Weevil Control (in Chinese). N’Guessan, F.K., Quisenberry, S.S., 1994. Screening selected rice lines for resistance to the rice water weevil (Coleoptera: Curculionidae). Environ. Entomol. 23, 665–675. N’Guessan, F.K., Quisenberry, S.S., Linscombe, S.D., 1994a. Investigation of antixenosis and antibiosis as mechanism of resistance in rice to the rice weevil (Coleoptera: Curculionidae). J. Entomol. Sci. 29, 259–263. N’Guessan, F.K., Quisenberry, S.S., Thompson, R.A., Linscombe, S.D., 1994b. Assessment of Louisiana rice breeding lines for tolerance to the rice water weevil (Coleoptera: Curculionidae). J. Econ. Entomol. 87, 476–481.
701
Rice, W.C., Croughan, T.P., Ring, D.R., Muegge, M.A., Stout, M.J., 1999. Delayed flood for management of rice water weevil (Coleoptera: Curculionidae). Environ. Entomol. 28, 1130–1135. Shang, H., Zhai, B., 1997. The spread of rice water weevil in southern China. In: Yang, X. (Ed.), Advance in Entomology. Forestry Press, Beijing, China, pp. 105–110 (in Chinese). Shang, H., Cheng, J., Jiang, M., Tang, Q., Gu, Y., 2003. Survival of adult rice water weevils during harvesting and storage of the first season rice crop in Zhejiang. Acta Entomol. Sinica 46, 190–195 (in Chinese, with English abstract). Stout, M.J., Rice, W.C., Riggio, R.M., Ring, D.R., 2000. The effects of four insecticides on the population dynamics of the rice water weevil, Lissorhoptrus oryzophilus Kuschel. J. Entomol. Sci. 35, 48–61. Stout, M.J., Rice, W.C., Linscombs, S.D., Bollich, P.K., 2001. Identification of rice cultivars resistant to Lissorhoptrus oryzophilus (Coleoptera: Curculinidae), and their use in an integrated management program. J. Econ. Entomol. 94, 963–970. Stout, M.J., Rice, W.C., Ring, D.R., 2002a. Integrated management of the rice water weevil. LA. Agric. 45, 20–21. Stout, M.J., Rice, W.C., Ring, D.R., 2002b. The influence of plant age on tolerance of rice to injury by the rice water weevil, Lissorhoptrus oryzophilus (Coleoptera: Curculinidae). Bull. Entomol. Res. 92, 177–184. Stout, M.J., Riggio, R.M., Li, Z., Roberts, R., 2002c. Flooding influences ovipositional and feeding behavior of the rice water weevil (Coleoptera: Curculinidae). J. Econ. Entomol. 95, 715–721. Sun, B., Zheng, X., 1998. Fumigation of rice water weevil by methyl bromide. Plant Quarantine 12, 214–215 (in Chinese). Sun, R., Mao, Z., Dai, D., Xiao, L., Chen, H., Wang, C., 1996. The Rice Water Weevil. China Agric. Press, Beijing (in Chinese). Thompson, R.A., Quisenberry, S.S., 1995. Rice plant density effect on rice water weevil (Coleoptera: Curculionidae) infestation. Environ. Entomol. 24, 19–23. Thompson, R.A., Quisenberry, S.S., N’Guessan, F.K., Heagler, A.M., Giesler, G., 1994a. Planting date as a potential cultural method for managing the rice water weevil (Coleoptera: Curculionidae) in water-seeded rice in southwest Louisiana. J. Econ. Entomol. 87, 1318–1324. Thompson, R.A., Quisenberry, S.S., Trahan, G.B., Heagler, A.M., Giesler, G., 1994b. Water management as a cultural control tactic for the rice water weevil (Coleoptera: Curculionidae) in southwest Louisiana. J. Econ. Entomol. 87, 223–230. Tian, C., Yu, F., Liu, Z., Su, F., 2003. Evaluation of Rice Germplasm Material T03 for resistance to rice water weevil. Liaoning Agric. Sci. 5, 5–7 (in Chinese). Tindall, K.V., Stout, M.J., 2003. Use of commen weeds of rice as hosts for the rice water weevil (Coleoptera: Curculionidae). Environ. Entomol. 32, 1227–1233. Tindall, K.V., Stout, M.J., Williams, B.J., 2004. Effects of the presence of Barnyardgrass on rice water weevil (Coleoptera: Curculionidae) and rice stink bug (Hemiptera: Pentatomidae) populations on rice. Environ. Entomol. 33, 720–726. Uhm, K.B., Lee, Y.I., Kim, Y.H., Choi, K.M., Yon, K.S., 1989. Studies on the future dispersion of the rice water weevil, Lissorhoptrus oryzophilus, in Korea. Res. Rep. Rural Develop. Adm. (Suweon) 31, 23–28 (in Korean). Wang, J., Liu, D., 1997. Potential establishment analysis and quarantine of rice water weevil in Jilin. Province. Plant Quarantine 11 (Suppl.), 38–40 (in Chinese). Wang, Y., Bao, Y., Hua, Y., 2001. Occurrence and control of quarantine pests in Changnan, Zhejiang. Plant Quarantine 15, 303–304 (in Chinese). Way, M.O., Wallace, R.G., 1999a. Control of rice water weevil with Fury 1.5EC, Dimilin 2L, Icon 6.2FS and Karate Z in a dry-planted delayed flood culture, 1998. Arthropod Manag. Tests 24, 277–278.
ARTICLE IN PRESS 702
H. Chen et al. / Crop Protection 24 (2005) 695–702
Way, M.O., Wallace, R.G., 1999b. Control of rice water weevil with Icon 6.2FS applied to dry or pre-germinated seed in a waterplanted delayed flood culture, 1998. Arthropod Manag. Tests 24, 279. Webb, J.L., 1914. Notes on the rice water weevil (Lissorhoptrus simplex Say). J. Econ. Entomol. 7, 432–438. Wu, G.W., Wilson, L.T., 1997. Growth and yield response of rice to rice water weevil injury. Environ. Entomol. 26, 1191–1201. Xie, Y., Li, Z., Gregg, W., Li, D., 2000. Invasive species in China—an overview. Biodivers. Conserv. 10, 1317–1341. Yang, W., Zhang, X., Zhang, J., 1998. Elimination and control of rice water weevil in Beijing. Plant Quarantine 12, 277–279 (in Chinese). Yu, F., Li, Z., Liu, P., Su, F., Tian, C., 2003. Research advances in biocontrol of rice water weevil. Liaoning Agric. Sci. 6, 19–20 (in Chinese). Zhai, B., 1998. Ovarian and flight muscle development of rice water weevil, Lissorhoptrus oryzophilus Kuschel. Plant Quarantine 12, 141–144 (in Chinese).
Zhai, P., Zheng, X., Shang, H., Cheng, J., 1999. Influence of wind on takeoff of rice water weevils. China Agric. Meteorol. 20, 24–28 (in Chinese). Zhang, R., 2003. China Invasive Pest Alert. (http://www.biotech.org.cn (in Chinese). Zhang, W., 1995. Agricultural Entomology. China Agric. Press, Beijing (in Chinese). Zhang, Z., 1989. Occurrence of rice water weevil in North Korea. Plant Prot. 15, 49–50 (in Chinese). Zheng, X., Zhai, B., Wu, J., 1997. Life history and control of rice water weevil in Southeastern coast of Zhejiang Province. Plant Quarantine 11 (Suppl.), 41–44 (in Chinese). Zheng, Z., Meng, D., Sun, R., Sun, B., Wang, H., 1998. Fumigation of rice water weevil by aluminum phosphide. J. Hebei Agric. Univ. 21, 35 (in Chinese). Zhou, Y., 1987. The rice water weevil, a pest with quarantine significance to China. World Agric. 10, 35–36 (in Chinese). Zou, L., Stout, M.J., Ring, D.R., 2004. Density–yield relationships for rice water weevil on rice for different varieties and under different water management regimes. Crop Prot. 23, 543–550.
Crop Protection 24 (2005) 695–702 www.elsevier.com/locate/cropro
Review
Rice water weevil (Coleoptera: Curculionidae) in mainland China: Invasion, spread and control Hong Chena,, Zhongmei Chenb, Yongshu Zhoub a
Department of Biology, State University of New York-Buffalo, 109 Cook Hall, Buffalo, NY 14260, USA b Plant Quarantine Institute, Beijing 100029, China Received 26 March 2004; received in revised form 29 November 2004; accepted 1 December 2004
Abstract The rice water weevil, Lissorhoptrus oryzophilus Kuschel, is the most important species among invasive insects in China. The parthenogenic weevil, first detected in Tanghai County of Hebei Province in 1988, has become one of the major rice pests in China with yield loss of 10–80%. Since then, the pest has expanded its range of infestation at a rate of 10–30 km/year. This pest has been found in eleven provinces and two large municipal areas infesting over 400,000 ha by late 2003. Quarantine measures did not effectively limit the spread of rice water weevil due to its parthenogenesis, flying, swimming and hitchhiking on human transportation. The weevil’s life history, population dynamics, host–plant relationships and mode of establishment have been studied at a number of locations. Currently, the pest is managed by integration of insecticides, water management, delayed transplanting, blacklight trapping, application of Beauveria bassiana and Metarhizium anisopliae spores and rice cultivars with tolerance to the rice water weevil. r 2005 Elsevier Ltd. All rights reserved. Keywords: Lissorhoptrus oryzophilus; Invasive species; Insect pest; Distribution; Quarantine; Control
Contents 1. 2.
3.
4.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1.1. Economical and ecological impacts of the rice water weevil in mainland China Invasion and spread of the rice water weevil in mainland China . . . . . . . . . . . . . . . 2.1. Invasion and spread . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Potential distribution in mainland China . . . . . . . . . . . . . . . . . . . . . . . . . . . Host plants and life history of the rice water weevil in mainland China . . . . . . . . . . 3.1. Host plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Phenology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Quarantine and control of the rice water weevil in mainland China . . . . . . . . . . . . . 4.1. Quarantine and isolation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Insecticidal control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.3. Cultural practices for control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.4. Physical control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.5. Biological control . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.6. Tolerant rice cultivars . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Corresponding author. Tel.: +1 716 645 2363x123; fax: +1 716 645 2975.
E-mail address: [email protected] (H. Chen). 0261-2194/$ - see front matter r 2005 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2004.12.005
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
. . . . . . . . . . . . . . .
696 696 697 697 698 698 698 699 699 699 699 699 700 700 700
ARTICLE IN PRESS 696
H. Chen et al. / Crop Protection 24 (2005) 695–702
5. Future research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 700 Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 700 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 700
1. Introduction The rice water weevil, Lissorhoptrus oryzophilus Kuschel, is endemic to the southern United States, where the beetle reproduces sexually and feeds on gramineous and cyperaceous weeds as its native hosts. The weevil’s damage to introduced rice was reported in Georgia in the early 1880s (Webb, 1914; Isely and Schwardt, 1934). For over 100 years, this weevil has been the most destructive insect pest of rice since its host shift to rice in North America (Webb, 1914; Zhou, 1987; Sun et al., 1996). In the late 1950s, a parthenogenic population of L. oryzophilus was found in northern California (Lange and Grigarick, 1959). From there the parthenogenic rice water weevil was carried across the Pacific into Asia in the mid-1970s (Japan Plant Protection Association, 1986). Webb (1914) and Isely and Schwardt (1934) summarized early studies on taxonomy, life cycle, host plants, economic importance and control of the rice water weevil in the United States. Insecticides remain the most effective means of controlling the rice water weevil (Stout et al., 2002a). Since the withdrawal of carbofuran, the four insecticides, fipronil, lambda-cyhalothrin, zetacypermethrin and diflubenzuron, have been registered for use against the rice water weevil. Fipronil, which will be dropped from the United States market after 2004, is used to treat rice seeds and kills the larvae (Bernhardt, 1999; Way and Wallace, 1999b; Stout et al., 2000), lambda-cyhalothrin, zetacypermethrin and diflubenzuron are applied as post-flood sprays for the adults, and diflubenzuron targets the eggs (Way and Wallace, 1999a; Stout et al., 2000). Recently, cultural control strategies, such as timing of planting (Barbour et al., 1993; Thompson et al., 1994a; Wu and Wilson, 1997; Stout et al., 2002c) and water management (Thompson et al., 1994b; Rice et al., 1999; Stout et al., 2002b; Zou et al., 2004), have been applied against the rice water weevil. Studies on integrated population management of the rice water weevil included weevil–host interaction (Thompson and Quisenberry, 1995; Wu and Wilson, 1997; Tindall and Stout, 2003; Tindall et al., 2004), rice plant resistance (N’Guessan and Quisenberry, 1994; N’Guessan et al., 1994a; Stout et al., 2001) and tolerance to the weevil (N’Guessan et al., 1994b; Stout et al., 2002b). The invasion of parthenogenic L. oryzophilus, which presumably ‘‘hitchhiked’’ across the Pacific into Asia from California, was first reported in Aichi Prefecture, Japan in 1976 (Japan Plant Protection Association, 1986). Ten years later, the rice water weevil spread
2000 km throughout the Japanese Archipelago (Iwata, 1979; Japan Plant Protection Association, 1986; Matsui, 1987). In Aichi the weevil was univoltine and the overwintered adults immigrated into rice paddies during May and June when daytime temperature exceeding 20 1C. By late July the eggs and larvae were found in paddies (Japan Plant Protection Association, 1986; Matsui, 1987). In southern Japan the weevil was bivoltine with very low larval densities on late-planting rice seedlings (Matsui, 1987). Larvae in both seedling nursery boxes and paddies were controlled with Carbosulfan and Cartap granules. Cultural control, such as transplanting of mature seedlings with higher tolerance to the pest and drainage for 15 days in paddies was also used against the rice water weevils. Among 150 rice varieties grown in Japan, a few of them showed high tolerance to the weevil (Japan Plant Protection Association, 1986; Matsui, 1987). In 1988, the parthenogenic rice water weevil was recorded in mainland China and the Korean peninsula, whereas the initial occurrence of rice water weevil in Taiwan was reported Taoyuan County in March 1990 (Sun et al., 1996). In Korea the weevil was primarily univoltine and a partial secondgeneration occured in some years (Li, 1993; Sun et al. 1996). Direction and speed of the weevil’s dispersal in Korea were affected by wind, mountain and ground transportation (Uhm et al., 1989). Quarantine measures to contain the rice water weevil were not successful in the early stage of rice water weevil invasion into eastern Asia. At this time, primary control of the pest in eastern Asia is focused on insecticide applications (Zhang, 1989; Li, 1993; Sun et al., 1996; Ministry of Agriculture, 2003). The range of rice water weevil infestation is expanding, and its spread into other rice producing regions is highly probable if this trend continues, posing a global threat to rice production (Stout et al., 2002a). 1.1. Economical and ecological impacts of the rice water weevil in mainland China Among some dozen exotic insect pests causing significant economic impacts in mainland China since the late 1970s (Xie et al., 2000), the rice water weevil draws the most attention and effort, because rice is the most important crop in China. The total area for rice production in China exceeds 33.3 million ha annually, from which the total annual rice production ranged from 171 million to 191 million tons in the past decade, accounting for about 35% of the world’s total (General Station of Plant Protection, 1988; IRRI, 2004). In 1986, the Chinese Ministry of Agriculture listed the rice water
ARTICLE IN PRESS H. Chen et al. / Crop Protection 24 (2005) 695–702
weevil as a quarantine pest before the initial detection of the weevil in China (Zhou, 1987). According to the plant quarantine and protection regulations, the Chinese central and provincial governments allotted millions of dollars (in RMB yuan) and set up special teams to study and practice quarantine and management of the rice water weevil soon after its discovery, initially trying to eliminate the pest. Despite these efforts, the range of rice water weevil continues to expand in mainland China. The rice water weevil was recognized as an important invasive pest immediately after its discovery in mainland China because of the severe rice yield losses. The adults feed on the upper leaf surfaces producing longitudinal scars. Larval feeding on roots causes stunted growth, yellowing of the leaves (chlorosis) and plants that are easily uprooted, resulting in few tillers and low grain yield. In mainland China yield losses typically exceeded 10% in the established paddies, but approached over 80% in newly infested areas (Guo, 1996; Sun et al., 1996). As a newly introduced pest, the rice water weevil did not conform to the Practical System of Integrated Rice Pest Management that was established in the early 1990s to control over 385 rice insect pests nationwide (General Station of Plant Protection, 1988; Du, 1991; Zhang, 1995). The invasion of rice water weevil poses a tremendous challenge for rice production, particularly in the area of integrating the rice water weevil control into existing rice IPM programs.
2. Invasion and spread of the rice water weevil in mainland China
697
Yuhuan County, Zhejiang Province. A follow-up survey in the same year revealed that the pest had spread to 15,300 ha of paddies in Yuhuan, Wenling, Leqing, Yongjia and Tongtou Counties of Zhejiang Province (Shang and Zhai, 1997). It was assumed that the rice water weevil reached Zhejiang Province by ship from Taiwan (Sun et al., 1996). Finally, in July 1993 rice water weevil was found in Ji’an County, Jilin Province. The invasive rice water weevil appear to have flownover or hitchhiked on human transports across a distance of 500 m from North Korea (Li, 1997). Yearly surveys, conducted after an initial discovery, showed that the rate of rice water weevil expansion ranged from 10 to 30 km/year in mainland China (Li and Cui, 1996; Sun et al., 1996). The weevils from Hebei were found reaching the suburbs of Tianjin and Beijing Cities in 1990, and Dongying of Shandong Province in 1992 (Sun et al., 1996). The rice water weevil in Zhejiang dispersed southward rapidly and entered the northern region of Fujian Province in 1996 (Wang et al., 2001; Chen et al., 2002). In May 2001 the pest was found in south-central region of Anhui Province and was detected to spread southward (Fang et al., 2003). Wind, temperature and human transportation played an important role in the range and speed of weevil dispersal in China (Sun et al., 1996; Zhai et al., 1999). By late 2003, the rice water weevil had been reported in the eleven provinces of Jilin, Liaoning, Hebei, Shandong, Shanxi, Jiangsu, Zhejiang, Anhui, Fujian, Guangdong, Guangxi and Hunan, and in the two large cities of Tianjin and Beijing (Fig. 1) (Zhang, 2003). Over
2.1. Invasion and spread The rice water weevil entry into mainland China was made through four speculated routes (Guo, 1996; Li and Cui, 1996; Shang and Zhai, 1997; Sun et al., 1996; He et al., 1997; Li, 1997). First, in May 1988 the Tanghai County farmers in Hebei Province reported infestations of a weevil causing heavy rice yield loss beginning in 1986. Compared with the specimens of rice water weevils from Japan, the weevils and larvae collected in China were identified to be the parthenogenic L. oryzophilus in the same year. This identification was confirmed by scanning electronic microscopy (Chen, 1989, 1991). A 1989 survey showed that the rice water weevil infested 42,700 ha of paddies in Luannan, Tanghai, Leting, Fengnan and Luan Counties of Hebei Province. It appeared that the larvae of rice water weevil entered these areas by infested rice seedlings from Japan (Sun et al., 1996). Second, in July 1991 rice water weevil was trapped by a blacklight in Dandong City, Liaoning Province. This invasion appeared to be aided by wind from North Korea (Li and Cui, 1996; He et al., 1997). Third, in May 1993 rice water weevil was detected in
N
↑
Jilin Liaoning Hebei Beijing Tianjing Shanxi Shandong Jiangsu Anhui Zhejiang Hunan Fujian
600 km Guangxi
Guangdong
Fig. 1. Occurrence of the rice water weevil in mainland China. The circles indicate the sites where the weevil was found. The weevil was also reported from the provinces of Shanxi, Jiangsu, Hunan, Guangdong and Guangxi without detailed locations (Zhang, 2003). The dotted line indicates the northwestern boundary of the pest’s potential distribution (from Mao et al., 1997).
ARTICLE IN PRESS H. Chen et al. / Crop Protection 24 (2005) 695–702
698
400,000 ha of paddies have been infested by the pest in mainland China. 2.2. Potential distribution in mainland China Mao et al. (1997) tested the effects of low humidity (5–35% RH) and low temperature (10 to 10 1C) on mortalities of newly emerged and overwintering populations of rice water weevil. The mortalities increased as temperature or relative humidity dropped, indicating that the weevils had limited tolerances to drought and cold. The computer software CLIMEX predicted the weevil’s potential distribution in mainland China (Fig. 1). The movement of rice water weevil was blocked further north by cold winter stress in Helongjiang and Jilin Provinces and to the west at high elevation in Sichuan and Yunnan Provinces. It is hypothesized that, dry summer and cold winter stress stopped the weevil’s spread within Inter-Mongolia Region and Gansu Province in northwestern China.
families in Tanghai and Luannan Counties, Hebei Province (Table 1). Of these host plants, 15 species in 5 families support L. oryzophilus larvae (Sun et al., 1996). Liu et al. (1998) observed that the adults of rice water weevil fed on corn seedling leaves in Ji’an County of Jilin Province, but emigrated into adjacent paddies after rice was transplanted. Although the rice water weevil has a wide range of host plants, the pest feeds primarily on rice plant under paddy conditions (Sun et al., 1996; Liu et al. 1998).
JI’an, Jilin 41˚10’ N
overwintered adults eggs larvae pupae
Tanghai, Hebei 39˚20’ N
Leqing, Zhejiang 28˚10’ N 1st-generation adults
3. Host plants and life history of the rice water weevil in mainland China
2nd-generation adults
Mar.
3.1. Host plants Field and laboratory studies have shown that adults of the rice water weevil feed on 64 plant species in 10
Apr.
May.
Jun.
Jul.
Aug.
Sep.
Oct.
Fig. 2. Life cycles of rice water weevil in three locations in mainland China (compiled from Shang and Zhai, 1997; Sun et al., 1996; Li, 1997; Zhai, 1998).
Table 1 Host plants of the rice water weevil in Tanghai and Luannan Counties, Hebei Province (from Sun et al., 1996) Family
Species
Alismateae Araceae Butomaceae Commelinaceae Cyperaceae
Alisma orientale (Sam.) Juzepcz.a, Sagittaria sagittifolia L. Acorus calamus L.a Butomus umbellatus L. Commelina communis L. Carex onoei Franch. et Sav., C. tangiana Ohwi, Cyperus difformis L., C. glomeratus L., Eleocharis valleculosa Ohwia, Juncellu serotinus (Rottb.) C. B. Clarke, Pycreus sanguinolentus (Vahl) Ness, Scirpus planiculmis Fr. Schmidta, S. tabernaemontani Gmel, S. triqueter L.a Iris ensata Thunb Aeluropus littoralis var. sinensis Debeaux, Agropyron cristatum (L.) Gaertn., Agrostis stolonifera L., Alopecurus aequalis Sobol., Aneurolepidium chinense (Trin.) Kitag., Arthraxon hispidus (Thunb.) Makino, Beckmannia syzigachne (Steud.) Fernald, Calamagrostis pseudophragmites (Hall. f.) Koel, Chloris virgata Swartz, Coix lacrymajobi L., Digitaria adscendens (H. B. K.) Henr., D. sanguinalis (L.) Scop.a, Diplachne fusca (L.) Beauv.a, Echinochloa crusgalli (L.) Beauv.a, E. crusgalli var. cruspavonis (H. B. K.) Hitch.a, Eleusine indica (L.) Gaertner, Eragrostis autumnalis Keng, E. cilianensis (All.) Link, Eriochloa villosa (Thunb.) Kunth, Hierochloe odorata (L.) Beauv., Imperata cylindrica (L.) Beauv. var. major Hubb., Leersia japonica (Makino) Keng f.a, Miscanthus sacchariflorus (Maxim.) Benth. Et Hook. f., Oryza sativa L.a, Panicum miliaceum L., Parapholis incurva (L.) C. E. Hubb., Pennisetum alopecuroides (L.) Spreng., Phragmitas communis Triniusa, Phyllostachys bambusoides Sieb. & Zucc., Poa annua L., Puccinellia chinampoensis Ohwia, Roegneria kamoji Ohwi, Saccharum sinensis Roxb., Setaria italica (L.) Beauv., S. lutescens (Weigel) Hubb., S. viridis (L.) Beauv., Sorghum vulgare Pers., Spartina anglica C. E. Hubb., Themeda triandra Forsk. var. japonica (Willd.) Makino, Zea mays L., Zizania aquatica L.a Juncus bufonius L., J. effusus L., J. gracillimus (Buch.) V. Krecz. et Gontsh. Potamogeton distinctus A. Bennett Typha angustata Bory et Chaub, T. minima Funka, T. orientalis Presl
Iridaceae Gramineae
Juncaceae Potamogetonaceae Typhaceae a
Larval hosts.
ARTICLE IN PRESS H. Chen et al. / Crop Protection 24 (2005) 695–702
699
3.2. Phenology
4.2. Insecticidal control
The rice water weevil in northern Chinese provinces of Jilin, Liaoning, Hebei and Shandong is univoltine (Fig. 2) (Sun et al., 1996; Li, 1997). On the other hand, a partial second-generation emerges from early September to early October in the double-cropping rice region of Zhejiang Province in southeastern China (Fig. 2) (Shang and Zhai, 1997; Zhai, 1998). Adults of rice water weevil prefer woods, meadows and river bunds adjacent to paddy as overwintering sites (Shang and Zhai, 1997; Sun et al., 1996; He et al., 1997; Zheng et al., 1997; Ding, 2002). In Tanghai County of Hebei Province, 99% of the adults overwinter within 3 cm of the surface soil (Sun et al., 1996). Further north, in Dangdong of Liaoning Province, 70% of the weevil adults inhabit the soil layer of 4–6 cm deep during the winter (He et al., 1997). In early spring, the overwintered adults began to be active, and later immigrate into the nearby seedling beds and paddies where they feed and oviposit.
Insecticides provide the most effective means of controlling the weevil in China as they do in the United States and Japan (Stout et al., 2002a; Matsui, 1987). Since the first recorded infestation of rice water weevil in mainland China in 1988, more than 60 insecticides have been evaluated for control (Shang and Zhai, 1997; Sun et al., 1996; He et al., 1997; Wang and Liu, 1997; Zheng et al., 1997; Yang et al., 1998). Economic thresholds and insecticide application measures have been set up for different developmental stages and habits, such as the overwintering site, seedling bed and paddy (Ministry of Agriculture, 2003). In addition, pest alerts for insecticide application were generated by the predictive models, related to meteorological data, oogenesis and degeneration/regeneration of indirect flight muscle, to forecast the periods of developmental stages, and migratory flight of rice water weevil (Li and Ye, 1998; Li, 1999; Gu et al., 2003; Zhai, 1998). Insecticides have been recommended for management of overwintered adults in overwintering sites, seedling beds and paddies. Applications of isocarbophos, malathion, esfenvalerate, cypermethrin or etofenprox were used when densities of the weevil exceeded economic thresholds (Sun et al., 1996; Yang et al., 1998; Ministry of Agriculture, 2003). Granular formulations of carbofuran or isofenphosmethyl, applied to flooded paddies, were used to manage the larvae (Sun et al., 1996; Ministry of Agriculture, 2003). Due to the lower density of second-generation weevils in southern China, they were controlled by the insecticides that targeted other rice pests (Shang and Zhai, 1997).
4. Quarantine and control of the rice water weevil in mainland China 4.1. Quarantine and isolation The Chinese central and local governments made enormous efforts to block the weevil spread during the period of invasion and initial establishment. Once the rice water weevil was detected in a location, surveys were launched to map the infested area. Because the pest can survive in stored rice grain, rice straw and grass over one month (Sun et al., 1996; Shang et al., 2003), transport of host materials such as rice seeds, seedlings and plants were forbidden from areas under quarantine. Materials and goods infested by the pest had to be fumigated by sulfuryl fluoride, aluminum phosphide or methyl bromide before transported from weevil infested areas (Sun et al., 1996; Sun and Zheng, 1998; Zheng et al., 1998). Vehicles leaving a quarantine area were subjected to an application of 5% esfenvalerate (v:v ¼ 1:2000) or 20% Xin Xing Dao Le Fen (a mixture of malathion and fenvalerate) (1:1000) to kill weevils (Sun et al., 1996; Ministry of Agriculture, 2003). The isolation effort for the rice water weevil has not been successful in mainland China. By flight alone, the range of rice water weevil infestation expanded 10–20 km/year after 1988 (Sun et al., 1996). Irrigation systems, rivers and occasional hitchhiking on human transportation dispersed the weevil (Sun et al., 1996). All of these factors greatly reduce the efficacy of quarantine and isolation measures.
4.3. Cultural practices for control Although weevil management still depends heavily on insecticides, appropriate cultural practices can also contribute to pest management. Seedling nurture without flood is commonly used (Sun et al., 1996). In Zhejiang Province, exposure of leaf-sheaths of rice seedlings by field drainage, resulted in an obvious suppression of oviposition and a great reduction in net fecundity of the pest when the exposure lasted over 16 days during the early and mid-oviposition stages (Jiang and Cheng, 2003). Delayed transplanting of 3–4 weeks was also effective, because older rice plants were more tolerant to injury (Sun et al., 1996; Ministry of Agriculture, 2003). In paddies, intermittent flooding with a drainage period up to 20 days was applied to reduce oviposition because female adults lay eggs only under flooded conditions. However, this intermittentflooding method should not be used in regions with a hot and dry growing season, where rice plants can be damaged by lack of water (Sun et al., 1996). In northern China, ploughing paddies in late autumn dramatically
ARTICLE IN PRESS 700
H. Chen et al. / Crop Protection 24 (2005) 695–702
increased mortality of the overwintering adults in the soil by up to 75%, because cold winter temperature killed the adults on the ground and in the upper layer of soil (Sun et al., 1996). 4.4. Physical control Blacklight trapping was effective in controlling migrating overwintered weevils (Sun et al., 1996; Ministry of Agriculture, 2003). Weevil capture per trap per night reached several kilograms in Tanghai County, Hebei Province, in late 1980s before a chemical control program was initiated (Sun et al., 1996). In Tongcheng of Anhui Province in 2001 and 2002, over 98% of total blacklight captures occurred during April 14 and May 14 when the overwintered adults immigrated into paddies (Fang et al., 2003). 4.5. Biological control The white muscardine fungus, Beauveria bassiana, was sprayed at a rate of 150,000 1010 spores/ha to control the overwintered adults during their migrating period (Ministry of Agriculture, 2003). Although B. bassiana took two weeks after application to show control effect, the infection rate was over 60% in weevil populations (Sun et al., 1996). In Zhejinag Province Metarhizium anisopliae was also used to control weevils at pre-oviposition stage. However, the infection rate of M. anisopliae in newly emerged adults was very low (Chai et al., 2000; Chen et al., 2000). No effective predators and parasites for weevil control are known in the infested areas in China (Yu et al., 2003).
States. Those weeds grown adjacent to paddies could serve as refugia where rice water weevil populations may persist and from where they may threaten paddies. On the other hand, the more preferred weeds can be used as trap plants near paddies. For biological control, it is necessary to conduct more studies on the weevil’s natural enemies such as predators, parasites and microbial pathogens in China. More research is needed to integrate weevil control into the current rice IPM programs. International cooperation should be initiated to reduce the possibility of the weevil spread across borders and aid the newly infested countries in weevil management. Origin and spread pattern of rice water weevils may be tracked by DNA fingerprinting. Phylogeny of the parthenogenic weevil populations and their relationship with the sexually reproducing populations in North America are important for understanding weevil biology and control. These can be addressed using genetic markers and population genetic methods in the future. More importantly, as Stout et al. (2002a) suggested, the greatest need is for the development of rice lines with high resistance to the rice water weevil, using both traditional breeding and genetic engineering methods, in various parts of the world.
Acknowledgements We thank Dr. G. Zhou (SUNY-Buffalo) for the map preparation using the ArcViews GIS. Three anonymous reviewers provided constructive comments and suggestions. We also want to acknowledge Dr. K. C. Kim (Penn State) for working on our manuscript.
4.6. Tolerant rice cultivars References In Tanghai County of Hebei Province Cultivar Zhonghua 8 and indica rice cultivars were less preferred by the weevil while Cultivars Xiangdao and Jigeng 8 were susceptible to the injury by the weevil (Sun et al., 1996). Tian et al. (2003) evaluated rice cultivars grown in Liaoning Province for resistance to the rice water weevil and found that few of the cultivars showed tolerance to the pest.
5. Future research Research is needed to refine thresholds for insecticide applications and efficacy, and monitoring methods for the weevil in different infested areas. Some chemicals registered in the United States should be tested for their efficacies against the rice water weevil in China. Investigation on host preference of the rice water weevil in China may reveal more preferred weeds over rice plant as Tindall and Stout (2003) found in the United
Barbour, J.D., Muegge, M.A., Trahan, G.B., Bollich, P.A., 1993. Effect of planting date on rice water weevil: numbers of feeding scars, eggs, and larvae. LA. Rice Res. Station Annu. Res. Rep. 85, 556–558. Bernhardt, J.L., 1999. Control of rice water weevil with Icon, 1998. Arthropod Manage. Tests 24, 271. Chai, Y., Chen, Z., Feng, H., Pan, L., 2000. Bioassay of Metarhizium anisopliae on the rice water weevil. Chin. J. Biol. Control 16, 22–25 (in Chinese, with English abstract). Chen, H., 1989. Scanning electron microscopy of the female adult of the rice water weevil, Lissorhoptrus oryzophilus. Plant Quarantine 3, 177–179 (in Chinese). Chen, H., 1991. Larval cephalic characteristics of Leptinotarsa decemlineata, Sitophilus granarius and Lissorhoptrus oryzophilus. Plant Quarantine 5, 6–10 (in Chinese). Chen, Z., Feng, H., Shi, L., Liu, Y., Pan, L., Wang, G., 2000. Evaluation of Metarhizium anisopliae for control of rice water weevil in the field. Chin. J. Biol. Control 16, 53–55 (in Chinese, with English abstract). Chen, J., Zhou, L., Lin, S., 2002. Occurrence and control of rice water weevil in Fujian. Plant Quarantine 16, 312–313 (in Chinese). Ding, Y., 2002. Occurrence and control of rice water weevil in Anshan, Jilin. Plant Prot. 28, 57 (in Chinese).
ARTICLE IN PRESS H. Chen et al. / Crop Protection 24 (2005) 695–702 Du, Z., 1991. Integrated Management of Rice Pests in China. China Agric. Press, Beijing (in Chinese). Fang, H., Fang, X., Chen, C., Li, Q., Feng, J., Li, B., 2003. Occurrence of rice water weevil in south-central Anhui. Plant Quarantine 17, 215–217 (in Chinese). General Station of Plant Protection, 1988. The Development in Integrated Control of Rice Diseases and Insect Pests in China. Zhejiang Science & Technology Press, Hangzhou (in Chinese). Gu, Y., Lin, Y., Li, B., Li, Y., 2003. Prediction of occurrence period of rice water weevil by simplified temperature summation. Plant Prot. 29, 43–45 (in Chinese). Guo, S., 1996. Risk analysis and quarantine measures on rice water weevil in Hebei. Plant Quarantine 10, 288–290 (in Chinese). He, N., Li, T., Jia, J., 1997. Occurrence and control of rice water weevil in Liaoning Province. Plant Quarantine 11 (Suppl.), 30–37 (in Chinese). IRRI, 2004. http://www.riceweb.org. Isely, D., Schwardt, H.H., 1934. The rice water weevil. Bull. Arkansas Agric. Exp. Stn. 299, 1–44. Iwata, T., 1979. Invasion of the rice water weevil, Lissorhoptrus oryzae, into Japan, spread of its distribution and abstract of the research experiments conducted in Japan. Jpn. Pestic. Inf. 36, 14–21. Japan Plant Protection Association, 1986. Control of the Rice Water Weevil in Japan (in Japanese). Jiang, M., Cheng, J., 2003. Effects of starvation and absence of free water on the oviposition of overwintered adult rice water weevil. Int. J. Pest Manage. 49, 89–94. Lange, W.H., Grigarick, A.A., 1959. Rice water weevil, beetle pest in rice growing areas of southern states discovered in California. Calif. Agric. 13 (8), 10–11. Li, H., 1993. Life cycle of rice water weevil in central North Korea. Plant Quarantine 7, 115 (in Chinese). Li, T., 1997. The rice water weevil in Ji’an. Plant Quarantine 11, 373 (in Chinese). Li, X., 1999. Use meteorological data to forecast the life cycle of the first-generation rice water weevil. Plant Quarantine 13, 277–278 (in Chinese). Li, J., Cui, S., 1996. Spread of rice water weevil in the areas adjacent to North Korea. Plant Quarantine 10, 242 (in Chinese). Li, X., Ye, K., 1998. Prediction of migratory flight and oviposition of overwintered adult of rice water weevil by meteorological data. Plant Quarantine 12, 330–332 (in Chinese). Liu, Y., Kang, R., Zheng, L., 1998. Rice water weevil feeding on corn. Plant Quarantine 12, 379 (in Chinese). Mao, Z., Sun, R., Dou, X., Chen, H., Zhou, M., Gui, G., Wu, C., 1997. Effects of low humidity and temperature on the mortality of rice water weevil and its potential distribution in China. Plant Quarantine 11 (Suppl.), 26–29 (in Chinese). Matsui, M., 1987. Expansion of distribution area of the rice water weevil and methods of controlling the insect pest in Japan. Jpn. Agric. Res. Q. 20, 166–173. Ministry of Agriculture, 2003. A Guide to the Rice Water Weevil Control (in Chinese). N’Guessan, F.K., Quisenberry, S.S., 1994. Screening selected rice lines for resistance to the rice water weevil (Coleoptera: Curculionidae). Environ. Entomol. 23, 665–675. N’Guessan, F.K., Quisenberry, S.S., Linscombe, S.D., 1994a. Investigation of antixenosis and antibiosis as mechanism of resistance in rice to the rice weevil (Coleoptera: Curculionidae). J. Entomol. Sci. 29, 259–263. N’Guessan, F.K., Quisenberry, S.S., Thompson, R.A., Linscombe, S.D., 1994b. Assessment of Louisiana rice breeding lines for tolerance to the rice water weevil (Coleoptera: Curculionidae). J. Econ. Entomol. 87, 476–481.
701
Rice, W.C., Croughan, T.P., Ring, D.R., Muegge, M.A., Stout, M.J., 1999. Delayed flood for management of rice water weevil (Coleoptera: Curculionidae). Environ. Entomol. 28, 1130–1135. Shang, H., Zhai, B., 1997. The spread of rice water weevil in southern China. In: Yang, X. (Ed.), Advance in Entomology. Forestry Press, Beijing, China, pp. 105–110 (in Chinese). Shang, H., Cheng, J., Jiang, M., Tang, Q., Gu, Y., 2003. Survival of adult rice water weevils during harvesting and storage of the first season rice crop in Zhejiang. Acta Entomol. Sinica 46, 190–195 (in Chinese, with English abstract). Stout, M.J., Rice, W.C., Riggio, R.M., Ring, D.R., 2000. The effects of four insecticides on the population dynamics of the rice water weevil, Lissorhoptrus oryzophilus Kuschel. J. Entomol. Sci. 35, 48–61. Stout, M.J., Rice, W.C., Linscombs, S.D., Bollich, P.K., 2001. Identification of rice cultivars resistant to Lissorhoptrus oryzophilus (Coleoptera: Curculinidae), and their use in an integrated management program. J. Econ. Entomol. 94, 963–970. Stout, M.J., Rice, W.C., Ring, D.R., 2002a. Integrated management of the rice water weevil. LA. Agric. 45, 20–21. Stout, M.J., Rice, W.C., Ring, D.R., 2002b. The influence of plant age on tolerance of rice to injury by the rice water weevil, Lissorhoptrus oryzophilus (Coleoptera: Curculinidae). Bull. Entomol. Res. 92, 177–184. Stout, M.J., Riggio, R.M., Li, Z., Roberts, R., 2002c. Flooding influences ovipositional and feeding behavior of the rice water weevil (Coleoptera: Curculinidae). J. Econ. Entomol. 95, 715–721. Sun, B., Zheng, X., 1998. Fumigation of rice water weevil by methyl bromide. Plant Quarantine 12, 214–215 (in Chinese). Sun, R., Mao, Z., Dai, D., Xiao, L., Chen, H., Wang, C., 1996. The Rice Water Weevil. China Agric. Press, Beijing (in Chinese). Thompson, R.A., Quisenberry, S.S., 1995. Rice plant density effect on rice water weevil (Coleoptera: Curculionidae) infestation. Environ. Entomol. 24, 19–23. Thompson, R.A., Quisenberry, S.S., N’Guessan, F.K., Heagler, A.M., Giesler, G., 1994a. Planting date as a potential cultural method for managing the rice water weevil (Coleoptera: Curculionidae) in water-seeded rice in southwest Louisiana. J. Econ. Entomol. 87, 1318–1324. Thompson, R.A., Quisenberry, S.S., Trahan, G.B., Heagler, A.M., Giesler, G., 1994b. Water management as a cultural control tactic for the rice water weevil (Coleoptera: Curculionidae) in southwest Louisiana. J. Econ. Entomol. 87, 223–230. Tian, C., Yu, F., Liu, Z., Su, F., 2003. Evaluation of Rice Germplasm Material T03 for resistance to rice water weevil. Liaoning Agric. Sci. 5, 5–7 (in Chinese). Tindall, K.V., Stout, M.J., 2003. Use of commen weeds of rice as hosts for the rice water weevil (Coleoptera: Curculionidae). Environ. Entomol. 32, 1227–1233. Tindall, K.V., Stout, M.J., Williams, B.J., 2004. Effects of the presence of Barnyardgrass on rice water weevil (Coleoptera: Curculionidae) and rice stink bug (Hemiptera: Pentatomidae) populations on rice. Environ. Entomol. 33, 720–726. Uhm, K.B., Lee, Y.I., Kim, Y.H., Choi, K.M., Yon, K.S., 1989. Studies on the future dispersion of the rice water weevil, Lissorhoptrus oryzophilus, in Korea. Res. Rep. Rural Develop. Adm. (Suweon) 31, 23–28 (in Korean). Wang, J., Liu, D., 1997. Potential establishment analysis and quarantine of rice water weevil in Jilin. Province. Plant Quarantine 11 (Suppl.), 38–40 (in Chinese). Wang, Y., Bao, Y., Hua, Y., 2001. Occurrence and control of quarantine pests in Changnan, Zhejiang. Plant Quarantine 15, 303–304 (in Chinese). Way, M.O., Wallace, R.G., 1999a. Control of rice water weevil with Fury 1.5EC, Dimilin 2L, Icon 6.2FS and Karate Z in a dry-planted delayed flood culture, 1998. Arthropod Manag. Tests 24, 277–278.
ARTICLE IN PRESS 702
H. Chen et al. / Crop Protection 24 (2005) 695–702
Way, M.O., Wallace, R.G., 1999b. Control of rice water weevil with Icon 6.2FS applied to dry or pre-germinated seed in a waterplanted delayed flood culture, 1998. Arthropod Manag. Tests 24, 279. Webb, J.L., 1914. Notes on the rice water weevil (Lissorhoptrus simplex Say). J. Econ. Entomol. 7, 432–438. Wu, G.W., Wilson, L.T., 1997. Growth and yield response of rice to rice water weevil injury. Environ. Entomol. 26, 1191–1201. Xie, Y., Li, Z., Gregg, W., Li, D., 2000. Invasive species in China—an overview. Biodivers. Conserv. 10, 1317–1341. Yang, W., Zhang, X., Zhang, J., 1998. Elimination and control of rice water weevil in Beijing. Plant Quarantine 12, 277–279 (in Chinese). Yu, F., Li, Z., Liu, P., Su, F., Tian, C., 2003. Research advances in biocontrol of rice water weevil. Liaoning Agric. Sci. 6, 19–20 (in Chinese). Zhai, B., 1998. Ovarian and flight muscle development of rice water weevil, Lissorhoptrus oryzophilus Kuschel. Plant Quarantine 12, 141–144 (in Chinese).
Zhai, P., Zheng, X., Shang, H., Cheng, J., 1999. Influence of wind on takeoff of rice water weevils. China Agric. Meteorol. 20, 24–28 (in Chinese). Zhang, R., 2003. China Invasive Pest Alert. (http://www.biotech.org.cn (in Chinese). Zhang, W., 1995. Agricultural Entomology. China Agric. Press, Beijing (in Chinese). Zhang, Z., 1989. Occurrence of rice water weevil in North Korea. Plant Prot. 15, 49–50 (in Chinese). Zheng, X., Zhai, B., Wu, J., 1997. Life history and control of rice water weevil in Southeastern coast of Zhejiang Province. Plant Quarantine 11 (Suppl.), 41–44 (in Chinese). Zheng, Z., Meng, D., Sun, R., Sun, B., Wang, H., 1998. Fumigation of rice water weevil by aluminum phosphide. J. Hebei Agric. Univ. 21, 35 (in Chinese). Zhou, Y., 1987. The rice water weevil, a pest with quarantine significance to China. World Agric. 10, 35–36 (in Chinese). Zou, L., Stout, M.J., Ring, D.R., 2004. Density–yield relationships for rice water weevil on rice for different varieties and under different water management regimes. Crop Prot. 23, 543–550.