Analysis of the Huge Immigration of Sogatella furcifera (Hemiptera: Delphacidae) to Southern China in the Spring of 2012

Analysis of the Huge Immigration of Sogatella furcifera (Hemiptera: Delphacidae) to Southern... Abstract Sogatella furcifera (Horváth) is a migratory rice pest that periodically erupts across Asia, and early immigration is an important cause of its outbreak. The early immigration of S. furcifera into southern China shows evident annual fluctuations. In the spring of 2012, the huge size of the immigrant population and the large number of immigration peaks were at levels rarely seen prior to that year. However, little research has been done on the entire process of round-trip migration to clarify the development of the population, the long-distance migration and the final eruption. In this study, the light-trap data for S. furcifera in southern China and Vietnam in 2011–2016 were collected, and the trajectory modeling showed that the early immigrants to southern China came from the northern and central Vietnam, Laos, and northeastern Thailand. Analysis of the development of the population, the migration process and meteorological factors revealed the reasons for the huge size of the early immigration: 1) the expansion of the source area could be seen as a precondition; 2) the large size of the returned population in the last autumn and the warm temperature of southern Vietnam and Laos in the last winter increased the initial populations; 3) the sustained strong southwest winds were conducive to the northward migration of the population during the major immigration period in early May. Therefore, the large-scale immigration of S. furcifera to southern China in the spring of 2012 resulted from the combined effects of several factors involved in the process of round-trip migration. Introduction Many insects in nature have migratory characteristics (Holland et al. 2006). Migratory insects undertake regular long-distance movements in groups from one habitat to another during certain periods of their lives (Hugh and Drake 2007, Chapman et al. 2010). Examples include the monarch butterfly (Danaus plexippus), desert locusts (Schistocerca gregaria), and the armyworm (Mythimna separate (Walker)) (Bartel et al. 2011, Homberg 2015). At present, many major agricultural pests have been identified as migratory insects. For example, the rice planthoppers of whitebacked planthoppers (WBPH, Sogatella furcifera (Horváth)) and brown planthoppers (Nilaparvata lugens (Stål)) are migratory. Rice, as the staple food eaten by more than half of the global population, suffers heavy losses from the insects. The periodic eruption of rice planthoppers in Asia can result in heavy losses of rice production, and the insects are hard to control. Before the 1960s, S. furcifera and N. lugens were secondary pests of rice; they occasionally occurred in China and Southeast Asian countries, and the affected areas were not very large (Cheng et al. 1979, the National Cooperated Research Group of Brown Planthoppers 1980, Deng 1981). In the 1970s and 1980s, Southeast Asian countries promoted high-yield rice varieties, adopted dense-planting cultivation measures and abused wide-spectrum insecticides. The living environment of rice planthoppers was greatly improved, and populations erupted to make the insects the number-one pest for rice in Asia (the National Cooperated Research Group of Brown Planthoppers 1980, 1981). In the 1990s, N. lugens’ population was effectively controlled by promoting large-scale high-yield indica hybrid rice that is resistant to planthoppers. S. furcifera became the dominant species in many areas (Pender 1994; Riley et al. 1994; Crummay and Atkinson 1997; Zhai 2011). In 2012, the early immigration population of S. furcifera was at an unprecedented level in southern China; outbreaks occurred in many rice fields. Therefore, the resource areas, migratory patterns and huge immigration of S. furcifera have been hot topics in research and challenges under the background of the current cropping systems and climate. Chinese researchers ascertained the basic migratory pattern and biological and ecological characteristics of WBPH by national coordinated research in the late 1970s and early 1980s. S. furcifera cannot overwinter in most rice fields in China; only a few overwintering sites are distributed in ratooning rice, original seedlings and rice stubble in Hainan and the southern parts of Guangdong, Guangxi, and Yunnan. The main overwintering source areas are in the warm Indo-China Peninsula (Luo et al. 2013). A northward migration of S. furcifera from the Indo-China Peninsula to southern China occurs by southwest windborne airflow every spring and summer, and progeny of the migrant populations in southern China expand the distribution northward to the middle and lower Yangtze Valley Plain. In autumn, the populations return to overwintering areas in the South (the National Coordinated Research Group for White Back Planthoppers 1981). Outbreaks of S. furcifera populations are often associated with rice varieties, cultivation systems, meteorological conditions, early immigration, resistance to pesticides and others. Rice varieties, cultivation systems, and resistance to pesticides change relatively slowly among these factors. However, meteorological factors are more changeable and difficult to control (Furuno et al. 2005, Bao et al. 2007, Wu et al. 2015). The occurrence of S. furcifera depends largely on the size of the early migrant population, which is affected not only by the population cardinal number but also by weather conditions (Syobu et al. 2012). The year 2012 was the most serious year of S. furcifera occurrence area and degree in China. Large-scale immigration occurred in various rice regions at the same time in early May in southern China. During this period, peaks of light-trap catches were observed at many monitoring sites in southern China, and the number of light-trap catches was more than 10,000 in a single day at Zhaoping, Yongfu, and Wan’an site. The large size of the immigrant population and the many immigration peaks were rarely seen before this year. Therefore, an exploration of S. furcifera immigration dynamics in the spring of 2012 would help us to clarify the pattern of migration, and study of the meteorological background during the large immigration period would help reveal the mechanism of outbreak development. Although some studies have been done on the occurrence of S. furcifera in 2012, most of these have focused on the local situation or one factor in immigration (Chen et al. 2012, Ma et al. 2013, Wang et al. 2017). The causes of the great S. furcifera immigration are still not explained at the macroscale, and thus this study was conducted to investigate the entire immigration process of 2012 from the aspects of the source area, the migration process, and the weather background. The study seeks to answer the following three questions: 1) Where were the source areas of S. furcifera in the early season in southern China in recent years? 2) How did the meteorological factors affect the outbreak of the early immigrant population? 3) How did the returned populations of the last autumn and the overwintering populations affect the scale of immigration in the next spring? Materials and Methods Meteorological Data Data on meteorological factors were provided by the European Center for Medium-Range Weather Forecasts (ECMWF) (http://www.ecmwf.int). Wind data in 2012 were recorded daily at 00:00, 06:00, 12:00, and 18:00 (UTC) with a spatial horizontal resolution of 0.75°. Climate data including wind and surface temperature were monthly means of daily means from 1987 to 2016, and the spatial resolution was 0.75°. The climatic mean could represent longer-lasting mean states calculated over a 30-yr period (from 1987 to 2016). Light-Trapped S. furcifera in Southern China and Vietnam Daily light-trap data from 2011 to 2016 from 20 sites in Southern China were collected by the National Agriculture Technology Extension and Service Center in China. The 20 monitoring sites were distributed in four provinces, eight in Guangxi Province (Longzhou, Bobai, Xingbin, Yizhou, Zhaoping, Babuqu, Yongfu, and Quanzhou), seven in Guangdong Province (Gaozhou, Yangchun, Kaiping, Zijin, Wengyuan, Meixian, and Qujiang), three in the southern part of Hunan Province (Hongjiang, Shaodong, and Youxian), and two in southern Jiangxi Province (Dayu and Wan’an). The daily data of S. furcifera in Vietnam were provided by the Plant Protection Bureau of Ministry of Agriculture and Rural Development. Light-trap monitors were placed at three sites in northern and central Vietnam (Hai Hau, Nam Dan, and Thang Binh). At each experimental site in China, a 20 W black light lamp (Jiaduo Brand, Industry and Trade Co. Ltd, Henan Province) was placed in a major rice field. In China, these lamps were turned on from 19:00 h to 07:00 h (Beijing Time) the next morning every day. In Vietnam, black light traps were turned on from 18:00 h to 06:00 h (Ho Chi Minh Time) daily. The number of light-trap catches of S. furcifera was recorded daily. In this study, early immigration of S. furcifera was the focus of our research. In southern China, the initial immigrants often appear in March, and the immigrant population increases in April and May. Thus, only the daily light-trap data of S. furcifera in spring (March–May) were considered, including southern China and Vietnam. In addition, an abrupt increase in the daily count data was defined as the beginning of a peak period, and an abrupt decrease defined as the end. The date of the peak value in the period was regarded as the peak day. The number of light-trap catches exceeding 50 in March, exceeding 100 in April, or exceeding 500 in May were the peak values, the dates of which were identified as peak days. Trajectory Analysis Probable source and landing areas of migratory S. furcifera were defined by constructing backward and forward trajectories using the HYSPLIT model, which was developed by the National Oceanic and Atmospheric Administration (NOAA) in the United States and Australian Bureau of Meteorology (Lu et al. 2013). The trajectory simulations used the following assumptions: 1) S. furcifera mostly take-off at dusk and partly at dawn (Cheng et al. 1979, Riley et al. 1991, Hu et al. 2014). 2) S. furcifera flies downwind (Ohkubo and Kisimoto 1971, Riley et al. 1991, Chapman et al. 2010, Hu et al. 2017). 3) The low-temperature threshold is 16.5°C for S. furcifera flight (Riley et al. 1991, 1994; Otuka et al. 2005). 4) Migrant flights are concentrated at a height of 800–1,500 m in spring and autumn (Deng 1981, Riley et al. 1991, Furuno et al. 2005). 5) The maximum flight time of S. furcifera is 36 h. (Zhang et al. 1992, Wang and Zhai 2004). 6) S. furcifera landed in the period that the light-trapped lamps were on. Moreover, all these endpoints of backward/forward trajectories should satisfy the following two requirements: 1) The source or landing areas were located in rice planting areas (Diao et al. 2012). 2) The source areas must have sufficient long-winged adults that can fly away. During the peak days of light-trap catches in spring in Southern China, backward trajectories from light-trap locations were set every 1 h during peak periods (from 19:00 to 05:00 (UTC + 8 h) of the next day) and terminated at the take-off time of S. furcifera (about 18:00) at 3 initial heights above mean sea level: 1,000, 1,200, and 1,500 m (Hu et al. 2014, Zhang et al. 2016, Wu et al. 2017b). Dawn take-off was not considered as its number is much lower than that at dusk (Riley et al. 1991, Hu et al. 2017). A total of 30 trajectories (10 h × 3 heights) were calculated for each location on a peak day, and the total run time (flight duration) of each trajectory was 36 h. The backward endpoints were considered likely source areas. The forward trajectories analysis of autumn returning across southern China set heights at 800, 1,000, and 1,200 m, and started every 24 h with a starting time of 19:00 (UTC + 8 h). The flight duration was also 36 h. The endpoints of forward trajectories were viewed as possible landing areas. Date Processing According to the rice cultivation system and occurrence of S. furcifera in the early season (the National Coordinated Research Group for White Back Planthoppers in China 1981), the distribution area of S. furcifera in southern China and Vietnam was divided into six areas (Fig. 1). Area I was located south of 23°N and west of 106.5°E, Area II was located south of 23°N and east of 106.5°E, Area III was located between 23°N–27.5°N and west of 108°E, Area IV was located between 23°N–27.5°N and 108°E–113°E, Area V was located between 23°N–27.5°N and 113°E–117°E, and Area VI was located between 23°N–27.5°N and east of 117°E. The probability of a source area was calculated from the number of endpoints in each area using Visual FoxPro and ArcGIS. The darker regions indicated denser endpoints, meaning that the probability that migrants land there is larger. Fig. 1. View largeDownload slide Location of light-trap sites of S. furcifera in Southern China and Vietnam. Red circles represent light-trap sites in southern China, and blue triangles represent light-trap sites in Vietnam. HJ-Hongjiang, SD-Shaodong, YX-Youxian, WA-Wan’an, QZ-Quanzhou, DY-Dayu, YF-Yongfu, QJ-Qujiang, YZ-Yizhou, WY-Wengyuan, BBQ-Babuqu, MX-Meixian, ZP-Zhaoping, XB-Xingbin, ZJ-Zijin, LZ-Longzhou, KP-Kaiping, YC-Yangchun, BB-Bobai, GZ-Gaozhou. Fig. 1. View largeDownload slide Location of light-trap sites of S. furcifera in Southern China and Vietnam. Red circles represent light-trap sites in southern China, and blue triangles represent light-trap sites in Vietnam. HJ-Hongjiang, SD-Shaodong, YX-Youxian, WA-Wan’an, QZ-Quanzhou, DY-Dayu, YF-Yongfu, QJ-Qujiang, YZ-Yizhou, WY-Wengyuan, BBQ-Babuqu, MX-Meixian, ZP-Zhaoping, XB-Xingbin, ZJ-Zijin, LZ-Longzhou, KP-Kaiping, YC-Yangchun, BB-Bobai, GZ-Gaozhou. Results Early Immigration of S. furcifera Into Southern China in 2011–2016 The accumulative light-trap catches of S. furcifera from March to May at each of 20 sites in southern China during 2011–2016 showed that the early immigration in 2012 was huge, greater than in other years (Fig. 2). The immigrating catches at most observation sites in 2012 were over 5,000. Numbers of immigration peaks of S. furcifera were recorded in each month from March to May in 2011–2016 at the 20 sites in southern China (Table 1), and the annual fluctuations vary greatly among these years. The greatest immigration occurred in 2012, and there were 76 peaks and 391,363 light-trap catches in total. In each year, the largest number of peaks was in May, and very few peaks occurred in March. Fig. 2. View largeDownload slide The cumulative light-trap catches of S. furcifera from March to May of each site in southern China during 2011–2016. Fig. 2. View largeDownload slide The cumulative light-trap catches of S. furcifera from March to May of each site in southern China during 2011–2016. Table 1. Cumulative light-trap catches of S. furcifera and numbers of peaks in southern China from 2011 to 2016 Year  Cumulative light-trap catchesa  Numbers of peaksb      March  April  May  2011  4,491  0  0  0  2012  391,363  0  17  59  2013  53,015  0  3  11  2014  160,798  0  0  19  2015  242,918  0  5  39  2016  77,103  1  10  21  Year  Cumulative light-trap catchesa  Numbers of peaksb      March  April  May  2011  4,491  0  0  0  2012  391,363  0  17  59  2013  53,015  0  3  11  2014  160,798  0  0  19  2015  242,918  0  5  39  2016  77,103  1  10  21  aCumulative light-trap catches from March to May for 20 sites in southern China of each listed year. The 20 light-trap sites in southern China are denoted by the red circles in Fig. 1. bThe number of catches peaks for 20 sites in Southern China. View Large Early Immigration of S. furcifera in 2012 The first appearance of S. furcifera in southern China in 2012 occurred in the middle of April (Fig. 3). In southern China in 2012, the immigration peaks started from late April to late May, and the main period of numbers of immigration events was in early May (April 30–May 9). The number of immigrants in many stations would suddenly increase at the same time, even at sites be far from each other. The peaks of light-trap catch in Nam Dan and Thang Binh in northern Vietnam occurred from mid-April to early May. Fig. 3. View largeDownload slide Daily light-trap catches of S. furcifera from March to May of each site in southern China and Vietnam in 2012. HH-Hai hao, ND-Nam Dan, TB-Thang Binh. The arrangement of 23 sites from bottom to top is according to their latitudes from south to north. Fig. 3. View largeDownload slide Daily light-trap catches of S. furcifera from March to May of each site in southern China and Vietnam in 2012. HH-Hai hao, ND-Nam Dan, TB-Thang Binh. The arrangement of 23 sites from bottom to top is according to their latitudes from south to north. Source Areas of S. furcifera in Southern China in the Early Season The total number of immigration peaks of S. furcifera in March from 2011 to 2016 was only one (Table 1), so the immigration events in April and May in southern China were given further attention. To explore the distribution of S. furcifera sources in different periods, the 61 days from April to May was divided into three periods, April 1–20, April 21–May 10, and May 11–31. In the aggregate, 5,520 backward trajectories were calculated on 184 peak days in 2011–2016 for 20 destination sites in southern China. The 20 destination sites in southern China were divided into three areas (Fig. 1). Area II included the southern parts of Guangdong and Guangxi provinces; there were five light-trap sites. S. furcifera in this area might came from Hainan province; a few were from central Vietnam and central Laos during April 1–20 (Fig. 4A). During April 21 to May 10, backward trajectories arrived in Hainan, north-central Vietnam, Laos, and northeastern Thailand (Fig. 4B). During May 11–31, endpoints mostly distributed in Hainan, northern Vietnam, Laos, and a few in northeastern Thailand (Fig. 4C). Eight light-trap sites distributed in Area IV included north-central Guangxi and southern Hunan; the backward trajectories from the eight sites arrived in northern Vietnam, northern Laos, and southern Guangxi in the early period (Fig. 4D), and in the middle period mainly in Guangxi and partly in north-central Vietnam, Laos, and southern Yunnan (Fig. 4E). In the last period, the endpoints were widely distributed in southern China and north-central Vietnam, Laos, and some in northeastern Thailand (Fig. 4F). Area V had seven sites in northern Guangdong, southern Jiangxi, and southern Hunan. Backward trajectories suggested that S. furcifera in Area V mostly migrated from Hainan, Guangdong, and east Guangxi in China, and a few came from northern and central parts of Vietnam and Laos in the early immigration season (Fig. 4G–I). In conclusion, the source areas from abroad of S. furcifera in southern China were mainly in north-central Vietnam, Laos, and a few in northeastern Thailand. Fig. 4. View largeDownload slide Density distributions of endpoints of backward trajectories from experimental sites in Areas II, IV, and V in southern China during April–May in 2011–2016. Red circles represent start locations of the backward trajectories. Fig. 4. View largeDownload slide Density distributions of endpoints of backward trajectories from experimental sites in Areas II, IV, and V in southern China during April–May in 2011–2016. Red circles represent start locations of the backward trajectories. On the 2012 case, the endpoints of back trajectories mostly distributed around the starting sites and partly in Hainan, north-central Vietnam, and Laos (Fig. 5). The size of source area in 2012 was smaller than in the total 6 yr, but the locations abroad were almost the same. Fig. 5. View largeDownload slide Density distributions of endpoints of backward trajectories from experimental sites in Areas II, IV, and V in southern China during April–May 2012. Red circles represent start locations of the backward trajectories. Fig. 5. View largeDownload slide Density distributions of endpoints of backward trajectories from experimental sites in Areas II, IV, and V in southern China during April–May 2012. Red circles represent start locations of the backward trajectories. Causes of the Huge Immigration of S. furcifera in the Early Season of 2012 Autumn Return Migration of S. furcifera in 2011 Regarding October and November of 2011–2016 in southern China, the light-trap catches of S. furcifera in 2011 were more than in other years (Fig. 6). S. furcifera badly damaged the late rice crop in southern China in 2011. Meanwhile, during October and November 2011, the monthly average northeast wind was stronger than the 6-yr average (2011–2016) in Guangdong, Guangxi, Beibu Gulf, and north-central Vietnam (Fig. 7). Strong northeast winds dominated this area in this period of 2011, which served as a driving force and carried S. furcifera populations southward back to the northern part of the Indo-China Peninsula. Forward trajectories from southern China in October and November of 2011 suggested that many migrants returned to central and northern parts of Vietnam, and some arrived in Laos and eastern Thailand (Fig. 8). In a word, S. furcifera had a serious outbreak in southern China in the autumn of 2011, and the migrants returned to overwintering areas in the Indo-China Peninsula. Fig. 6. View largeDownload slide Annual cumulative light-trap catches of S. furcifera during October and November in 20 sites in southern China in 2011–2016. Fig. 6. View largeDownload slide Annual cumulative light-trap catches of S. furcifera during October and November in 20 sites in southern China in 2011–2016. Fig. 7. View largeDownload slide Wind field anomaly at 925 hPa in October 2011 (A), and in November 2011 (B) in southern China and Vietnam. The climatic mean was between 2011 and 2016. Fig. 7. View largeDownload slide Wind field anomaly at 925 hPa in October 2011 (A), and in November 2011 (B) in southern China and Vietnam. The climatic mean was between 2011 and 2016. Fig. 8. View largeDownload slide Density distributions of autumn-returned S. furcifera populations from southern China during October and November in 2011. Red circles represent start locations of the forward trajectories. Fig. 8. View largeDownload slide Density distributions of autumn-returned S. furcifera populations from southern China during October and November in 2011. Red circles represent start locations of the forward trajectories. Overwintering Temperature in Initial Source Areas in 2012 The temperature in winter is one of the important factors to S. furcifera population development. In January 2012, the surface temperature was 0.5°C higher than the 30-yr average in southern Vietnam, western Laos, and Thailand (Fig. 9A). Similarly, in February 2012, the temperature was approximately 0.5–1°C higher in most parts of the Indo-China Peninsula (Fig. 9B). However, the surface temperature in northern Vietnam was about 1.5°C lower in January and February, 2012 (Fig. 9). Fig. 9. View largeDownload slide Surface temperature anomaly in southern China and the Indo-China Peninsula in January 2012 (A), and in February 2012 (B). The climatic mean was the average value between 1987 and 2016. Fig. 9. View largeDownload slide Surface temperature anomaly in southern China and the Indo-China Peninsula in January 2012 (A), and in February 2012 (B). The climatic mean was the average value between 1987 and 2016. The development of S. furcifera populations in the spring of 2012 Early immigration of S. furcifera in southern China came from north-central parts of Vietnam and Laos, especially from the northern part (Fig. 4). The number of cumulative light-trap catches in the spring of 2012 in Hai Hau was the seasonal maximum from 2011 to 2016, as was the case in Nam Dan. The number of 2012 from Thang Binh was not the maximum, as this site was in central Vietnam and was not the main source area of S. furcifera in southern China (Fig. 10). Hai Hau and Nam Dan were in northern Vietnam, indicating that the population of S. furcifera in the source area was large, which caused the huge immigration in southern China in the spring of 2012. Fig. 10. View largeDownload slide Annual cumulative light-trap catches of S. furcifera from March to May at Hai Hau, Nam Dan, and Thang Binh in Vietnam during 2011 to 2016. Fig. 10. View largeDownload slide Annual cumulative light-trap catches of S. furcifera from March to May at Hai Hau, Nam Dan, and Thang Binh in Vietnam during 2011 to 2016. The major immigration into southern China in 2012 was from April 30 to May 9 (Fig. 3). Thousands of S. furcifera were recorded during these 10 days at most observation sites in southern China and at the two sites in northern Vietnam. The average wind field of 850 hPa for these 10 days showed prevailing southwest winds in the northern part of the Indo-China Peninsula, Beibu Gulf, and southern China (Fig. 11). The southwest low-level jet stream in this period was very helpful for the long-distance northward migration of S. furcifera into southern China. Fig. 11. View largeDownload slide Total light-trap catches of S. furcifera during April 30 to May 9 in 2012 at each station in Vietnam and southern China and wind field at 850 hPa during the same period. Fig. 11. View largeDownload slide Total light-trap catches of S. furcifera during April 30 to May 9 in 2012 at each station in Vietnam and southern China and wind field at 850 hPa during the same period. Discussion The outbreaks of migratory insects result from many factors. The outbreak of S. furcifera was influenced by rice varieties, cropping systems, and weather conditions. Huge immigration in the early season is always an important cause of population eruption in China. In the 21st century, the occurrence of S. furcifera was a serious matter in East and Southeast Asia, and infestations of SRBSDV transmitted by S. furcifera were widespread in southern China and Vietnam. Researchers have made great progress in the development of rice insect-resistant cultivars and against pesticide resistance, but the population dynamics of early immigration into southern China remains unclear. It is important to analyze the early immigration events of S. furcifera in southern China in recent years (2011–2016) and to focus on the great immigration that occurred in 2012. To explore the causes of the early population eruption in southern China, the distribution of source areas, the dynamics of the returned population in autumn, the dynamics of the overwintering population and weather conditions were all considered. Source Areas of Early S. furcifera Immigration Into Southern China Were in North-Central Vietnam and Laos in 2012 The previous studies noted that the direct source area was the Red River delta in northern Vietnam, but the initial S. furcifera immigrants came from the Mekong Delta in southern Vietnam (Wu et al. 1997). Our trajectory analyses suggested that central Vietnam and Laos may be the main source areas besides the Red River delta in 2012 (Fig. 5). The expansion of the source area definitely increased early immigration cardinal numbers. Indeed, in the past decade the government of Laos strongly encouraged rice cultivation and developed irrigation projects, and winter-spring rice acreage was several times larger than in the late 1990s (Li et al. 2010). The rice growth stage in Laos and central Vietnam was a month earlier than in the Red River delta in northern Vietnam, and winter-spring rice in this area had been harvested by late May. In April, the rice was at the late growth stage; meanwhile, large numbers of local S. furcifera emigrated away. This meant that this population could migrate to southern China a month earlier if the wind field was appropriate, and one more generation could be added to the progeny of migrants from the Red River delta. Thus, the expansion of the source area may have been a precondition for the great immigration of S. furcifera to southern China in 2012. The Initial Population of S. furcifera Was Increased by the Large Size of the Returned Population and Warm Temperature of Overwintering Areas in Winter S. furcifera undertake long-distance round-trip migrations every year to maintain their populations in the long run, causing heavy rice losses along the journey. The periodical migrations and eruptions across Asia make the outbreaks of S. furcifera hard to control and prevent (Riley et al. 1994, 2003; Hu et al. 2013; Zhang et al. 2016). There was little concern about return migration of S. furcifera compared to northward migration. There were two reasons: first, in autumn rice is approaching the ripening stage in the mainland of China; S. furcifera would not inflict much damage on rice at this late growth stage. Second, large-scale population return to the Indo-China Peninsula is rare. However, many peak light-trap catches appeared in the autumn of 2011 in southern China, and the total light-trap catches during October and November of 2011 were the highest from 2011 to 2016 (Fig. 6). During the periods of peak return migration, a sustained northeast wind was essential for migrants to fly back to the Indo-China Peninsula successfully. In October and November 2011, continuous northeast winds prevailed over southern China and the Indo-China Peninsula at 925 hPa (Fig. 7). Forward analysis of the returned population in this period showed that endpoints could land in the Indo-China Peninsula (Fig. 8). The successful return migration would increase the cardinal number of the overwintering population, and establish the foundation for the eruption of the S. furcifera population in the spring of 2012. In winter, the rice plant is fallow in southern China. S. furcifera populations begin their northward migration into southern China in late March every year (the National Coordinated Research Group for White Back Planthoppers 1981, Wu et al. 2017a). However, rice can grow all year round in Southern Central Vietnam, which is a permanent breeding area of S. furcifera (Hu et al. 2017). Development of overwintering populations there could indirectly affect the quantity of initial immigration into China, and temperature is a key factor (Syobu et al. 2012, Hu et al. 2010). The suitable temperature range for S. furcifera is 20–30°C, and temperatures over 35°C or under 20°C are unfavorable for development and reproduction. When in the suitable temperature range, a higher temperature is more conducive to population growth (Feng et al. 1985, Ye et al. 1994). Laos and north-central Vietnam were as the direct source areas and the southern Vietnam as the initial source area (Zhai et al. 2011).The temperatures in January and February of 2012 were 0.5–1°C higher than the average temperature during 1987 to 2016 in southern Vietnam and Laos (Fig. 9). The higher temperature in winter would have increased the effective accumulated temperature, causing a shortened developmental duration of S. furcifera leading to earlier emergence and additional generations. Meanwhile, northern Vietnam experienced lower temperatures in January and February, which might decrease the local population. However, the increasing progeny of WBPH in southern Vietnam might migrate to northern Vietnam in spring and indirectly affect the immigration into southern China. During the Major Immigration Period, Sustained Strong Southwest Winds Were Conducive to the Northward Migration of the Population For a mass immigration to occur in the early season, two conditions must be satisfied. On the one hand, there must be plentiful migrants in the source area. On the other hand, there must be suitable air flow that can transport migrants a long distance. The above analysis has shown there were abundant S. furcifera in the source area in the spring of 2012 (Fig. 9). In addition, a prevailing southwest wind at 850 hPa was dominant over the Indo-China Peninsula and southern China (Fig. 10), which would have facilitated the long migration of S. furcifera populations from the Indo-China Peninsula to southern China. In summary, the size of the early immigration of S. furcifera was co-determined by each part of the whole process of round-trip migration. The number of returning migrants in the autumn has an impact on the cardinal number of the overwintering population, and the development and reproduction of S. furcifera in winter will decide the size of the early immigration in the next spring. Meanwhile, each part is closely related to meteorological factors. The surface temperature is an important factor in the development of population, and the direction and speed of the wind determine the direction and distance of population migration. The huge immigration of S. furcifera that occurred in the spring of 2012 resulted from the combined effects of all the above factors. The number of overwintering S. furcifera could only be predicted by trajectory simulation and meteorological analysis due to a lack of insect data from the Indo-China Peninsula in our study. Further work should be done to strengthen international cooperation on diseases and pests and sharing information between Eastern Asian countries. Finally, we have clarified the connections between the early immigration size and each link in the whole migration process from the macroscopic point of view. Acknowledgments This study was sponsored by the National Natural Science Foundation of China (41075086; 30671340), Science Research Program of Universities and Colleges in Jiangsu Province (14KJA170003), Priority Academic Program Development of Jiangsu Higher Education Institutions (IRT1147), and Youth Science and Technology Talent Growth Project of Guizhou Provincial Education Department (KY[2017]246). We thank the National Agricultural Techniques Extension and Service Center for providing insect data in China. We also thank the Plant Protection Bureau of the Ministry of Agriculture and Rural Development for sharing insect data from Vietnam. References Cited Bao, Y.X., Xu X. Y., Wang J. Q., Wang C. H., Miao Q. L., and Zhai B. P.. 2007. 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Analysis of the Huge Immigration of Sogatella furcifera (Hemiptera: Delphacidae) to Southern China in the Spring of 2012

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Abstract

Abstract Sogatella furcifera (Horváth) is a migratory rice pest that periodically erupts across Asia, and early immigration is an important cause of its outbreak. The early immigration of S. furcifera into southern China shows evident annual fluctuations. In the spring of 2012, the huge size of the immigrant population and the large number of immigration peaks were at levels rarely seen prior to that year. However, little research has been done on the entire process of round-trip migration to clarify the development of the population, the long-distance migration and the final eruption. In this study, the light-trap data for S. furcifera in southern China and Vietnam in 2011–2016 were collected, and the trajectory modeling showed that the early immigrants to southern China came from the northern and central Vietnam, Laos, and northeastern Thailand. Analysis of the development of the population, the migration process and meteorological factors revealed the reasons for the huge size of the early immigration: 1) the expansion of the source area could be seen as a precondition; 2) the large size of the returned population in the last autumn and the warm temperature of southern Vietnam and Laos in the last winter increased the initial populations; 3) the sustained strong southwest winds were conducive to the northward migration of the population during the major immigration period in early May. Therefore, the large-scale immigration of S. furcifera to southern China in the spring of 2012 resulted from the combined effects of several factors involved in the process of round-trip migration. Introduction Many insects in nature have migratory characteristics (Holland et al. 2006). Migratory insects undertake regular long-distance movements in groups from one habitat to another during certain periods of their lives (Hugh and Drake 2007, Chapman et al. 2010). Examples include the monarch butterfly (Danaus plexippus), desert locusts (Schistocerca gregaria), and the armyworm (Mythimna separate (Walker)) (Bartel et al. 2011, Homberg 2015). At present, many major agricultural pests have been identified as migratory insects. For example, the rice planthoppers of whitebacked planthoppers (WBPH, Sogatella furcifera (Horváth)) and brown planthoppers (Nilaparvata lugens (Stål)) are migratory. Rice, as the staple food eaten by more than half of the global population, suffers heavy losses from the insects. The periodic eruption of rice planthoppers in Asia can result in heavy losses of rice production, and the insects are hard to control. Before the 1960s, S. furcifera and N. lugens were secondary pests of rice; they occasionally occurred in China and Southeast Asian countries, and the affected areas were not very large (Cheng et al. 1979, the National Cooperated Research Group of Brown Planthoppers 1980, Deng 1981). In the 1970s and 1980s, Southeast Asian countries promoted high-yield rice varieties, adopted dense-planting cultivation measures and abused wide-spectrum insecticides. The living environment of rice planthoppers was greatly improved, and populations erupted to make the insects the number-one pest for rice in Asia (the National Cooperated Research Group of Brown Planthoppers 1980, 1981). In the 1990s, N. lugens’ population was effectively controlled by promoting large-scale high-yield indica hybrid rice that is resistant to planthoppers. S. furcifera became the dominant species in many areas (Pender 1994; Riley et al. 1994; Crummay and Atkinson 1997; Zhai 2011). In 2012, the early immigration population of S. furcifera was at an unprecedented level in southern China; outbreaks occurred in many rice fields. Therefore, the resource areas, migratory patterns and huge immigration of S. furcifera have been hot topics in research and challenges under the background of the current cropping systems and climate. Chinese researchers ascertained the basic migratory pattern and biological and ecological characteristics of WBPH by national coordinated research in the late 1970s and early 1980s. S. furcifera cannot overwinter in most rice fields in China; only a few overwintering sites are distributed in ratooning rice, original seedlings and rice stubble in Hainan and the southern parts of Guangdong, Guangxi, and Yunnan. The main overwintering source areas are in the warm Indo-China Peninsula (Luo et al. 2013). A northward migration of S. furcifera from the Indo-China Peninsula to southern China occurs by southwest windborne airflow every spring and summer, and progeny of the migrant populations in southern China expand the distribution northward to the middle and lower Yangtze Valley Plain. In autumn, the populations return to overwintering areas in the South (the National Coordinated Research Group for White Back Planthoppers 1981). Outbreaks of S. furcifera populations are often associated with rice varieties, cultivation systems, meteorological conditions, early immigration, resistance to pesticides and others. Rice varieties, cultivation systems, and resistance to pesticides change relatively slowly among these factors. However, meteorological factors are more changeable and difficult to control (Furuno et al. 2005, Bao et al. 2007, Wu et al. 2015). The occurrence of S. furcifera depends largely on the size of the early migrant population, which is affected not only by the population cardinal number but also by weather conditions (Syobu et al. 2012). The year 2012 was the most serious year of S. furcifera occurrence area and degree in China. Large-scale immigration occurred in various rice regions at the same time in early May in southern China. During this period, peaks of light-trap catches were observed at many monitoring sites in southern China, and the number of light-trap catches was more than 10,000 in a single day at Zhaoping, Yongfu, and Wan’an site. The large size of the immigrant population and the many immigration peaks were rarely seen before this year. Therefore, an exploration of S. furcifera immigration dynamics in the spring of 2012 would help us to clarify the pattern of migration, and study of the meteorological background during the large immigration period would help reveal the mechanism of outbreak development. Although some studies have been done on the occurrence of S. furcifera in 2012, most of these have focused on the local situation or one factor in immigration (Chen et al. 2012, Ma et al. 2013, Wang et al. 2017). The causes of the great S. furcifera immigration are still not explained at the macroscale, and thus this study was conducted to investigate the entire immigration process of 2012 from the aspects of the source area, the migration process, and the weather background. The study seeks to answer the following three questions: 1) Where were the source areas of S. furcifera in the early season in southern China in recent years? 2) How did the meteorological factors affect the outbreak of the early immigrant population? 3) How did the returned populations of the last autumn and the overwintering populations affect the scale of immigration in the next spring? Materials and Methods Meteorological Data Data on meteorological factors were provided by the European Center for Medium-Range Weather Forecasts (ECMWF) (http://www.ecmwf.int). Wind data in 2012 were recorded daily at 00:00, 06:00, 12:00, and 18:00 (UTC) with a spatial horizontal resolution of 0.75°. Climate data including wind and surface temperature were monthly means of daily means from 1987 to 2016, and the spatial resolution was 0.75°. The climatic mean could represent longer-lasting mean states calculated over a 30-yr period (from 1987 to 2016). Light-Trapped S. furcifera in Southern China and Vietnam Daily light-trap data from 2011 to 2016 from 20 sites in Southern China were collected by the National Agriculture Technology Extension and Service Center in China. The 20 monitoring sites were distributed in four provinces, eight in Guangxi Province (Longzhou, Bobai, Xingbin, Yizhou, Zhaoping, Babuqu, Yongfu, and Quanzhou), seven in Guangdong Province (Gaozhou, Yangchun, Kaiping, Zijin, Wengyuan, Meixian, and Qujiang), three in the southern part of Hunan Province (Hongjiang, Shaodong, and Youxian), and two in southern Jiangxi Province (Dayu and Wan’an). The daily data of S. furcifera in Vietnam were provided by the Plant Protection Bureau of Ministry of Agriculture and Rural Development. Light-trap monitors were placed at three sites in northern and central Vietnam (Hai Hau, Nam Dan, and Thang Binh). At each experimental site in China, a 20 W black light lamp (Jiaduo Brand, Industry and Trade Co. Ltd, Henan Province) was placed in a major rice field. In China, these lamps were turned on from 19:00 h to 07:00 h (Beijing Time) the next morning every day. In Vietnam, black light traps were turned on from 18:00 h to 06:00 h (Ho Chi Minh Time) daily. The number of light-trap catches of S. furcifera was recorded daily. In this study, early immigration of S. furcifera was the focus of our research. In southern China, the initial immigrants often appear in March, and the immigrant population increases in April and May. Thus, only the daily light-trap data of S. furcifera in spring (March–May) were considered, including southern China and Vietnam. In addition, an abrupt increase in the daily count data was defined as the beginning of a peak period, and an abrupt decrease defined as the end. The date of the peak value in the period was regarded as the peak day. The number of light-trap catches exceeding 50 in March, exceeding 100 in April, or exceeding 500 in May were the peak values, the dates of which were identified as peak days. Trajectory Analysis Probable source and landing areas of migratory S. furcifera were defined by constructing backward and forward trajectories using the HYSPLIT model, which was developed by the National Oceanic and Atmospheric Administration (NOAA) in the United States and Australian Bureau of Meteorology (Lu et al. 2013). The trajectory simulations used the following assumptions: 1) S. furcifera mostly take-off at dusk and partly at dawn (Cheng et al. 1979, Riley et al. 1991, Hu et al. 2014). 2) S. furcifera flies downwind (Ohkubo and Kisimoto 1971, Riley et al. 1991, Chapman et al. 2010, Hu et al. 2017). 3) The low-temperature threshold is 16.5°C for S. furcifera flight (Riley et al. 1991, 1994; Otuka et al. 2005). 4) Migrant flights are concentrated at a height of 800–1,500 m in spring and autumn (Deng 1981, Riley et al. 1991, Furuno et al. 2005). 5) The maximum flight time of S. furcifera is 36 h. (Zhang et al. 1992, Wang and Zhai 2004). 6) S. furcifera landed in the period that the light-trapped lamps were on. Moreover, all these endpoints of backward/forward trajectories should satisfy the following two requirements: 1) The source or landing areas were located in rice planting areas (Diao et al. 2012). 2) The source areas must have sufficient long-winged adults that can fly away. During the peak days of light-trap catches in spring in Southern China, backward trajectories from light-trap locations were set every 1 h during peak periods (from 19:00 to 05:00 (UTC + 8 h) of the next day) and terminated at the take-off time of S. furcifera (about 18:00) at 3 initial heights above mean sea level: 1,000, 1,200, and 1,500 m (Hu et al. 2014, Zhang et al. 2016, Wu et al. 2017b). Dawn take-off was not considered as its number is much lower than that at dusk (Riley et al. 1991, Hu et al. 2017). A total of 30 trajectories (10 h × 3 heights) were calculated for each location on a peak day, and the total run time (flight duration) of each trajectory was 36 h. The backward endpoints were considered likely source areas. The forward trajectories analysis of autumn returning across southern China set heights at 800, 1,000, and 1,200 m, and started every 24 h with a starting time of 19:00 (UTC + 8 h). The flight duration was also 36 h. The endpoints of forward trajectories were viewed as possible landing areas. Date Processing According to the rice cultivation system and occurrence of S. furcifera in the early season (the National Coordinated Research Group for White Back Planthoppers in China 1981), the distribution area of S. furcifera in southern China and Vietnam was divided into six areas (Fig. 1). Area I was located south of 23°N and west of 106.5°E, Area II was located south of 23°N and east of 106.5°E, Area III was located between 23°N–27.5°N and west of 108°E, Area IV was located between 23°N–27.5°N and 108°E–113°E, Area V was located between 23°N–27.5°N and 113°E–117°E, and Area VI was located between 23°N–27.5°N and east of 117°E. The probability of a source area was calculated from the number of endpoints in each area using Visual FoxPro and ArcGIS. The darker regions indicated denser endpoints, meaning that the probability that migrants land there is larger. Fig. 1. View largeDownload slide Location of light-trap sites of S. furcifera in Southern China and Vietnam. Red circles represent light-trap sites in southern China, and blue triangles represent light-trap sites in Vietnam. HJ-Hongjiang, SD-Shaodong, YX-Youxian, WA-Wan’an, QZ-Quanzhou, DY-Dayu, YF-Yongfu, QJ-Qujiang, YZ-Yizhou, WY-Wengyuan, BBQ-Babuqu, MX-Meixian, ZP-Zhaoping, XB-Xingbin, ZJ-Zijin, LZ-Longzhou, KP-Kaiping, YC-Yangchun, BB-Bobai, GZ-Gaozhou. Fig. 1. View largeDownload slide Location of light-trap sites of S. furcifera in Southern China and Vietnam. Red circles represent light-trap sites in southern China, and blue triangles represent light-trap sites in Vietnam. HJ-Hongjiang, SD-Shaodong, YX-Youxian, WA-Wan’an, QZ-Quanzhou, DY-Dayu, YF-Yongfu, QJ-Qujiang, YZ-Yizhou, WY-Wengyuan, BBQ-Babuqu, MX-Meixian, ZP-Zhaoping, XB-Xingbin, ZJ-Zijin, LZ-Longzhou, KP-Kaiping, YC-Yangchun, BB-Bobai, GZ-Gaozhou. Results Early Immigration of S. furcifera Into Southern China in 2011–2016 The accumulative light-trap catches of S. furcifera from March to May at each of 20 sites in southern China during 2011–2016 showed that the early immigration in 2012 was huge, greater than in other years (Fig. 2). The immigrating catches at most observation sites in 2012 were over 5,000. Numbers of immigration peaks of S. furcifera were recorded in each month from March to May in 2011–2016 at the 20 sites in southern China (Table 1), and the annual fluctuations vary greatly among these years. The greatest immigration occurred in 2012, and there were 76 peaks and 391,363 light-trap catches in total. In each year, the largest number of peaks was in May, and very few peaks occurred in March. Fig. 2. View largeDownload slide The cumulative light-trap catches of S. furcifera from March to May of each site in southern China during 2011–2016. Fig. 2. View largeDownload slide The cumulative light-trap catches of S. furcifera from March to May of each site in southern China during 2011–2016. Table 1. Cumulative light-trap catches of S. furcifera and numbers of peaks in southern China from 2011 to 2016 Year  Cumulative light-trap catchesa  Numbers of peaksb      March  April  May  2011  4,491  0  0  0  2012  391,363  0  17  59  2013  53,015  0  3  11  2014  160,798  0  0  19  2015  242,918  0  5  39  2016  77,103  1  10  21  Year  Cumulative light-trap catchesa  Numbers of peaksb      March  April  May  2011  4,491  0  0  0  2012  391,363  0  17  59  2013  53,015  0  3  11  2014  160,798  0  0  19  2015  242,918  0  5  39  2016  77,103  1  10  21  aCumulative light-trap catches from March to May for 20 sites in southern China of each listed year. The 20 light-trap sites in southern China are denoted by the red circles in Fig. 1. bThe number of catches peaks for 20 sites in Southern China. View Large Early Immigration of S. furcifera in 2012 The first appearance of S. furcifera in southern China in 2012 occurred in the middle of April (Fig. 3). In southern China in 2012, the immigration peaks started from late April to late May, and the main period of numbers of immigration events was in early May (April 30–May 9). The number of immigrants in many stations would suddenly increase at the same time, even at sites be far from each other. The peaks of light-trap catch in Nam Dan and Thang Binh in northern Vietnam occurred from mid-April to early May. Fig. 3. View largeDownload slide Daily light-trap catches of S. furcifera from March to May of each site in southern China and Vietnam in 2012. HH-Hai hao, ND-Nam Dan, TB-Thang Binh. The arrangement of 23 sites from bottom to top is according to their latitudes from south to north. Fig. 3. View largeDownload slide Daily light-trap catches of S. furcifera from March to May of each site in southern China and Vietnam in 2012. HH-Hai hao, ND-Nam Dan, TB-Thang Binh. The arrangement of 23 sites from bottom to top is according to their latitudes from south to north. Source Areas of S. furcifera in Southern China in the Early Season The total number of immigration peaks of S. furcifera in March from 2011 to 2016 was only one (Table 1), so the immigration events in April and May in southern China were given further attention. To explore the distribution of S. furcifera sources in different periods, the 61 days from April to May was divided into three periods, April 1–20, April 21–May 10, and May 11–31. In the aggregate, 5,520 backward trajectories were calculated on 184 peak days in 2011–2016 for 20 destination sites in southern China. The 20 destination sites in southern China were divided into three areas (Fig. 1). Area II included the southern parts of Guangdong and Guangxi provinces; there were five light-trap sites. S. furcifera in this area might came from Hainan province; a few were from central Vietnam and central Laos during April 1–20 (Fig. 4A). During April 21 to May 10, backward trajectories arrived in Hainan, north-central Vietnam, Laos, and northeastern Thailand (Fig. 4B). During May 11–31, endpoints mostly distributed in Hainan, northern Vietnam, Laos, and a few in northeastern Thailand (Fig. 4C). Eight light-trap sites distributed in Area IV included north-central Guangxi and southern Hunan; the backward trajectories from the eight sites arrived in northern Vietnam, northern Laos, and southern Guangxi in the early period (Fig. 4D), and in the middle period mainly in Guangxi and partly in north-central Vietnam, Laos, and southern Yunnan (Fig. 4E). In the last period, the endpoints were widely distributed in southern China and north-central Vietnam, Laos, and some in northeastern Thailand (Fig. 4F). Area V had seven sites in northern Guangdong, southern Jiangxi, and southern Hunan. Backward trajectories suggested that S. furcifera in Area V mostly migrated from Hainan, Guangdong, and east Guangxi in China, and a few came from northern and central parts of Vietnam and Laos in the early immigration season (Fig. 4G–I). In conclusion, the source areas from abroad of S. furcifera in southern China were mainly in north-central Vietnam, Laos, and a few in northeastern Thailand. Fig. 4. View largeDownload slide Density distributions of endpoints of backward trajectories from experimental sites in Areas II, IV, and V in southern China during April–May in 2011–2016. Red circles represent start locations of the backward trajectories. Fig. 4. View largeDownload slide Density distributions of endpoints of backward trajectories from experimental sites in Areas II, IV, and V in southern China during April–May in 2011–2016. Red circles represent start locations of the backward trajectories. On the 2012 case, the endpoints of back trajectories mostly distributed around the starting sites and partly in Hainan, north-central Vietnam, and Laos (Fig. 5). The size of source area in 2012 was smaller than in the total 6 yr, but the locations abroad were almost the same. Fig. 5. View largeDownload slide Density distributions of endpoints of backward trajectories from experimental sites in Areas II, IV, and V in southern China during April–May 2012. Red circles represent start locations of the backward trajectories. Fig. 5. View largeDownload slide Density distributions of endpoints of backward trajectories from experimental sites in Areas II, IV, and V in southern China during April–May 2012. Red circles represent start locations of the backward trajectories. Causes of the Huge Immigration of S. furcifera in the Early Season of 2012 Autumn Return Migration of S. furcifera in 2011 Regarding October and November of 2011–2016 in southern China, the light-trap catches of S. furcifera in 2011 were more than in other years (Fig. 6). S. furcifera badly damaged the late rice crop in southern China in 2011. Meanwhile, during October and November 2011, the monthly average northeast wind was stronger than the 6-yr average (2011–2016) in Guangdong, Guangxi, Beibu Gulf, and north-central Vietnam (Fig. 7). Strong northeast winds dominated this area in this period of 2011, which served as a driving force and carried S. furcifera populations southward back to the northern part of the Indo-China Peninsula. Forward trajectories from southern China in October and November of 2011 suggested that many migrants returned to central and northern parts of Vietnam, and some arrived in Laos and eastern Thailand (Fig. 8). In a word, S. furcifera had a serious outbreak in southern China in the autumn of 2011, and the migrants returned to overwintering areas in the Indo-China Peninsula. Fig. 6. View largeDownload slide Annual cumulative light-trap catches of S. furcifera during October and November in 20 sites in southern China in 2011–2016. Fig. 6. View largeDownload slide Annual cumulative light-trap catches of S. furcifera during October and November in 20 sites in southern China in 2011–2016. Fig. 7. View largeDownload slide Wind field anomaly at 925 hPa in October 2011 (A), and in November 2011 (B) in southern China and Vietnam. The climatic mean was between 2011 and 2016. Fig. 7. View largeDownload slide Wind field anomaly at 925 hPa in October 2011 (A), and in November 2011 (B) in southern China and Vietnam. The climatic mean was between 2011 and 2016. Fig. 8. View largeDownload slide Density distributions of autumn-returned S. furcifera populations from southern China during October and November in 2011. Red circles represent start locations of the forward trajectories. Fig. 8. View largeDownload slide Density distributions of autumn-returned S. furcifera populations from southern China during October and November in 2011. Red circles represent start locations of the forward trajectories. Overwintering Temperature in Initial Source Areas in 2012 The temperature in winter is one of the important factors to S. furcifera population development. In January 2012, the surface temperature was 0.5°C higher than the 30-yr average in southern Vietnam, western Laos, and Thailand (Fig. 9A). Similarly, in February 2012, the temperature was approximately 0.5–1°C higher in most parts of the Indo-China Peninsula (Fig. 9B). However, the surface temperature in northern Vietnam was about 1.5°C lower in January and February, 2012 (Fig. 9). Fig. 9. View largeDownload slide Surface temperature anomaly in southern China and the Indo-China Peninsula in January 2012 (A), and in February 2012 (B). The climatic mean was the average value between 1987 and 2016. Fig. 9. View largeDownload slide Surface temperature anomaly in southern China and the Indo-China Peninsula in January 2012 (A), and in February 2012 (B). The climatic mean was the average value between 1987 and 2016. The development of S. furcifera populations in the spring of 2012 Early immigration of S. furcifera in southern China came from north-central parts of Vietnam and Laos, especially from the northern part (Fig. 4). The number of cumulative light-trap catches in the spring of 2012 in Hai Hau was the seasonal maximum from 2011 to 2016, as was the case in Nam Dan. The number of 2012 from Thang Binh was not the maximum, as this site was in central Vietnam and was not the main source area of S. furcifera in southern China (Fig. 10). Hai Hau and Nam Dan were in northern Vietnam, indicating that the population of S. furcifera in the source area was large, which caused the huge immigration in southern China in the spring of 2012. Fig. 10. View largeDownload slide Annual cumulative light-trap catches of S. furcifera from March to May at Hai Hau, Nam Dan, and Thang Binh in Vietnam during 2011 to 2016. Fig. 10. View largeDownload slide Annual cumulative light-trap catches of S. furcifera from March to May at Hai Hau, Nam Dan, and Thang Binh in Vietnam during 2011 to 2016. The major immigration into southern China in 2012 was from April 30 to May 9 (Fig. 3). Thousands of S. furcifera were recorded during these 10 days at most observation sites in southern China and at the two sites in northern Vietnam. The average wind field of 850 hPa for these 10 days showed prevailing southwest winds in the northern part of the Indo-China Peninsula, Beibu Gulf, and southern China (Fig. 11). The southwest low-level jet stream in this period was very helpful for the long-distance northward migration of S. furcifera into southern China. Fig. 11. View largeDownload slide Total light-trap catches of S. furcifera during April 30 to May 9 in 2012 at each station in Vietnam and southern China and wind field at 850 hPa during the same period. Fig. 11. View largeDownload slide Total light-trap catches of S. furcifera during April 30 to May 9 in 2012 at each station in Vietnam and southern China and wind field at 850 hPa during the same period. Discussion The outbreaks of migratory insects result from many factors. The outbreak of S. furcifera was influenced by rice varieties, cropping systems, and weather conditions. Huge immigration in the early season is always an important cause of population eruption in China. In the 21st century, the occurrence of S. furcifera was a serious matter in East and Southeast Asia, and infestations of SRBSDV transmitted by S. furcifera were widespread in southern China and Vietnam. Researchers have made great progress in the development of rice insect-resistant cultivars and against pesticide resistance, but the population dynamics of early immigration into southern China remains unclear. It is important to analyze the early immigration events of S. furcifera in southern China in recent years (2011–2016) and to focus on the great immigration that occurred in 2012. To explore the causes of the early population eruption in southern China, the distribution of source areas, the dynamics of the returned population in autumn, the dynamics of the overwintering population and weather conditions were all considered. Source Areas of Early S. furcifera Immigration Into Southern China Were in North-Central Vietnam and Laos in 2012 The previous studies noted that the direct source area was the Red River delta in northern Vietnam, but the initial S. furcifera immigrants came from the Mekong Delta in southern Vietnam (Wu et al. 1997). Our trajectory analyses suggested that central Vietnam and Laos may be the main source areas besides the Red River delta in 2012 (Fig. 5). The expansion of the source area definitely increased early immigration cardinal numbers. Indeed, in the past decade the government of Laos strongly encouraged rice cultivation and developed irrigation projects, and winter-spring rice acreage was several times larger than in the late 1990s (Li et al. 2010). The rice growth stage in Laos and central Vietnam was a month earlier than in the Red River delta in northern Vietnam, and winter-spring rice in this area had been harvested by late May. In April, the rice was at the late growth stage; meanwhile, large numbers of local S. furcifera emigrated away. This meant that this population could migrate to southern China a month earlier if the wind field was appropriate, and one more generation could be added to the progeny of migrants from the Red River delta. Thus, the expansion of the source area may have been a precondition for the great immigration of S. furcifera to southern China in 2012. The Initial Population of S. furcifera Was Increased by the Large Size of the Returned Population and Warm Temperature of Overwintering Areas in Winter S. furcifera undertake long-distance round-trip migrations every year to maintain their populations in the long run, causing heavy rice losses along the journey. The periodical migrations and eruptions across Asia make the outbreaks of S. furcifera hard to control and prevent (Riley et al. 1994, 2003; Hu et al. 2013; Zhang et al. 2016). There was little concern about return migration of S. furcifera compared to northward migration. There were two reasons: first, in autumn rice is approaching the ripening stage in the mainland of China; S. furcifera would not inflict much damage on rice at this late growth stage. Second, large-scale population return to the Indo-China Peninsula is rare. However, many peak light-trap catches appeared in the autumn of 2011 in southern China, and the total light-trap catches during October and November of 2011 were the highest from 2011 to 2016 (Fig. 6). During the periods of peak return migration, a sustained northeast wind was essential for migrants to fly back to the Indo-China Peninsula successfully. In October and November 2011, continuous northeast winds prevailed over southern China and the Indo-China Peninsula at 925 hPa (Fig. 7). Forward analysis of the returned population in this period showed that endpoints could land in the Indo-China Peninsula (Fig. 8). The successful return migration would increase the cardinal number of the overwintering population, and establish the foundation for the eruption of the S. furcifera population in the spring of 2012. In winter, the rice plant is fallow in southern China. S. furcifera populations begin their northward migration into southern China in late March every year (the National Coordinated Research Group for White Back Planthoppers 1981, Wu et al. 2017a). However, rice can grow all year round in Southern Central Vietnam, which is a permanent breeding area of S. furcifera (Hu et al. 2017). Development of overwintering populations there could indirectly affect the quantity of initial immigration into China, and temperature is a key factor (Syobu et al. 2012, Hu et al. 2010). The suitable temperature range for S. furcifera is 20–30°C, and temperatures over 35°C or under 20°C are unfavorable for development and reproduction. When in the suitable temperature range, a higher temperature is more conducive to population growth (Feng et al. 1985, Ye et al. 1994). Laos and north-central Vietnam were as the direct source areas and the southern Vietnam as the initial source area (Zhai et al. 2011).The temperatures in January and February of 2012 were 0.5–1°C higher than the average temperature during 1987 to 2016 in southern Vietnam and Laos (Fig. 9). The higher temperature in winter would have increased the effective accumulated temperature, causing a shortened developmental duration of S. furcifera leading to earlier emergence and additional generations. Meanwhile, northern Vietnam experienced lower temperatures in January and February, which might decrease the local population. However, the increasing progeny of WBPH in southern Vietnam might migrate to northern Vietnam in spring and indirectly affect the immigration into southern China. During the Major Immigration Period, Sustained Strong Southwest Winds Were Conducive to the Northward Migration of the Population For a mass immigration to occur in the early season, two conditions must be satisfied. On the one hand, there must be plentiful migrants in the source area. On the other hand, there must be suitable air flow that can transport migrants a long distance. The above analysis has shown there were abundant S. furcifera in the source area in the spring of 2012 (Fig. 9). In addition, a prevailing southwest wind at 850 hPa was dominant over the Indo-China Peninsula and southern China (Fig. 10), which would have facilitated the long migration of S. furcifera populations from the Indo-China Peninsula to southern China. In summary, the size of the early immigration of S. furcifera was co-determined by each part of the whole process of round-trip migration. The number of returning migrants in the autumn has an impact on the cardinal number of the overwintering population, and the development and reproduction of S. furcifera in winter will decide the size of the early immigration in the next spring. Meanwhile, each part is closely related to meteorological factors. The surface temperature is an important factor in the development of population, and the direction and speed of the wind determine the direction and distance of population migration. The huge immigration of S. furcifera that occurred in the spring of 2012 resulted from the combined effects of all the above factors. The number of overwintering S. furcifera could only be predicted by trajectory simulation and meteorological analysis due to a lack of insect data from the Indo-China Peninsula in our study. Further work should be done to strengthen international cooperation on diseases and pests and sharing information between Eastern Asian countries. Finally, we have clarified the connections between the early immigration size and each link in the whole migration process from the macroscopic point of view. Acknowledgments This study was sponsored by the National Natural Science Foundation of China (41075086; 30671340), Science Research Program of Universities and Colleges in Jiangsu Province (14KJA170003), Priority Academic Program Development of Jiangsu Higher Education Institutions (IRT1147), and Youth Science and Technology Talent Growth Project of Guizhou Provincial Education Department (KY[2017]246). We thank the National Agricultural Techniques Extension and Service Center for providing insect data in China. We also thank the Plant Protection Bureau of the Ministry of Agriculture and Rural Development for sharing insect data from Vietnam. References Cited Bao, Y.X., Xu X. Y., Wang J. Q., Wang C. H., Miao Q. L., and Zhai B. P.. 2007. 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Environmental EntomologyOxford University Press

Published: Feb 1, 2018

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