In Northeast China

ACTA ECOLOGICA SINICA Volume 28, Issue 4, April 2008 Online English edition of the Chinese language journal

Cite this article as: Acta Ecologica Sinica, 2008, 28(4), 1521í1535. RESEARCH PAPER

Source area of spring population of meadow moth, Loxostege sticticalis L. (Lepidoptera: Pyralidae), in Northeast China

Chen Xiao1, Zhai Baoping1,*, Gong Ruijie2, Yin Minghao3, Zhang You4, Zhao Kuijun5

1 Key Laboratory of Monitoring and Management of Plant Diseases and Insects, Ministry of Agriculture, Nanjing Agricultural University, Nanjing 210095, China 2 Plant Protection Station of Chifeng, Chifeng 024001, China 3 Plant Protection Station of Xinganmeng, Wulanhaote 137400, China 4 Plant Protection Station of Hulunbeier, Hailaer 021000, China 5 College of Agriculture, Northeast Agricultural University, Harbin 150030, China

Abstract: The meadow moth, Loxostege sticticalis L., is an important outbreak pest in Northeast China. The spring population in Northeast China was considered as immigrants from North China; however, the population dynamics during 1996–2007 was not consistent with this traditional theory. In this study, the source area of the spring population of the meadow moth in Northeast China was identified by trajectory analysis using the wind field simulated by mesoscale numerical forecast model MM5. The results indicated that the population of the meadow moth in North China was able to migrate into Northeast China, but had not made a crucial contribution to the outbreaks there since the weather systems were generally adverse for such a long range migration in most of the years. On the other hand, high density cocoons of L. sticticalis have frequently been found in autumn in Northeast China since 1996. The trajectory analyses indicated that most of L. sticticalis in Northeast China in spring emerged from the cocoons that had overwintered either locally or in neighboring countries, i.e. Mongolia and Russia. The development of overwintering areas at higher lati- tudes coincides with the increased frequency of second-generation larvae; both phenomena might be attributed to the regional climate change associated with global warming.

Key Words: Loxostege sticticalis; migration; outbreak population; trajectory analysis

The meadow moth, Loxostege sticticalis L. (Lepidoptera: (Mongolia), into Northeast China. However, the population Pyralidae), is an important outbreak pest in Northern China, dynamics in the recent outbreak periods (since 1995) present causing serious damage to the crops and forage such as soy- abnormal features. For example, in some years, the peaks of bean, sugar beet, alfalfa and sunflower, and leading to severe the spring population in Northeast China occurred 10 days losses. Northeast China is the outbreak area of L. sticticalis, earlier than those in North China, or most of the females in the and Songnen Plain is the most serious agricultural region in- peaks were still in the 1st grade (immature stage). It is obvious fested by L. sticticalis. that the immigrants were not from the “permanent breeding According to the studies in 1980s, the meadow moth sel- area”. The source of the meadow moth is unclear. On the other dom overwintered in Northeast China, and most of them ap- hand, the overwintering areas of L. sticticalis frequently peared in spring were from other areas[1–3]. There is a “perma- emerged in Northeast China in recent years, which is contra- nent breeding area” in North China, covering Wulanchabu of dictory to the traditional theory[5–8]. Inner Mongolia, the northern area of Shanxi and Zhangjiakou Therefore, it is necessary to further study where the spring of Hebei[4]. The adults from this area make a long-range mi- population of L. sticticalis in Northeast China came from and gration by two ways, within the border of China or outside how the local overwintering cocoons influenced the emer-

Received date: January 23, 2007; Accepted date: December 12, 2007 *Corresponding author. E-mail: [email protected] Copyright © 2008, Ecological Society of China. Published by Elsevier BV. All rights reserved. CHEN Xiao et al. / Acta Ecologica Sinica, 2008, 28(4):1521–1535 gence of L. sticticalis in the next spring. Confirming the point every 20 min, saved the point coordinate in text format, source of L. sticticalis in Northeast China is not only basic to and displayed the results on the platform of the geographical explore the occurrence regularity, but also meaningful to im- information system (ArcGIS). prove the long-term forecast ability and secure the agricultural The cases of emigration and immigration were analyzed production. The objective of this study is to investigate the forward and backward, respectively, to study the relationship main source area of the spring population of the meadow moth of population in different areas and track back to the source in Northeast China during the 3rd outbreak period since 1949. area. The following are the main parameters: Flying height. Radar observations of L. sticticalis by the 1 Materials and methods Institute of Plant Protection, Jilin Academy of Agricultural Sciences showed that the adults migrated at an altitude below 1.1 Data source 400 m above the emerging area where the elevation was around Insect data. Insect monitoring data, including the number 1670 m. The airborne adults of L. sticticalis were mainly con- of light trap catches and the number of moths in 100 steps in centrated at the altitude of 200–650 m above the ground when the field, were collected from Plant Protection Stations in they migrated into the plain areas of lower elevation to de- North China. scend in Northeast China[10]. In the model under study, the Meteorological data. The data used in the model included V NNRP reanalysis data (horizontal resolution 2.5º×2.5º, col- coordinate system with value 0.945 (sig945) was used, which lected every 6 h) from the National Center for Environmental was about 400 m above the ground, corresponding to the fly- Prediction/the National Center for Atmospheric Research ing height of L. sticticalis. Thus, the wind field on the level (NCEP/NCAR) and Global Final (FNL) analysis data (hori- sig945 was used for trajectory analysis. zontal resolution 1.0º×1.0º, collected every 6 h) from NCEP. Orientation and flying speed. Radar observations in The observation data were regular sounding data collected Yingxian of Shanxi Province by the Institute of Plant Protec- every 12 h and surface observation data sent out by the Na- tion, Jilin Academy of Agricultural Sciences showed that the tional Meteorological Bureau of China (received by the Satel- flying direction of L. sticticalis was almost consistent with the [11] lite Data Receiver and the Analysis System PCVSATTM in our wind direction . Radar observations in Langfang of Hebei lab) every 3 h. The sounding data at Zhangjiakou Station and Province by the Institute of Plant Protection, Chinese Acad- the surface temperature data every 10 d at Hailaer Station emy of Agricultural Sciences showed that L. sticticalis had [12] were obtained from the National Meteorological Information migration preference toward the northeast in spring . Con- Centre of China. sidering the weak flying ability of L. sticticalis, the action of Map. The China map with administrative division at prov- orientation had faint effects on the displacement when the ince level (1:4000000) was downloaded from the National wind was strong, and the strong wind was necessary for a long Fundamental Geographic Information System of China (http:// range of migration. Therefore, the orientation of L. sticticalis nfgis.nsdi.gov.cn). was ignored in the program, and the sum of wind speed and 1.2 Trajectory analysis and key parameters air speed was used as the real speed. Based on the test of the The mesoscale non-hydrostatic meteorological numerical flying ability, the average flying speed of L. sticticalis within [13] model (MM5, non-hydrostatic version 3.7) developed by 12 h is 2.5–4.6 km/h . The middle value 1.0 m/s was used in Pennsylvania State University and NCAR was employed in this study. the present study to simulate the atmospheric dynamic field Time parameters for taking off and landing. L. sticticalis during the migration of L. sticticalis. The FNL (or NNRP) migrates at night, and the time points for taking-off and land- [11,12] data as the background incorporated with the regular sounding ing are around the sunset and sunrise, respectively . In the data and the surface observation data for re-analysis, and program, the trajectory was calculated based on the dynamic formed the initial field and lateral boundary conditions of the treatment of the time points for taking-off and landing, which coarse mesh. The start point was 20:00 every day, the forecast were determined by the definite time of the sunset and sunrise length was 24 h and the time-step for the fine mesh was 180 s. of the place where the trace point was located. The time points Four-dimensional data assimilation (FDDA) was performed to of the sunset and sunrise were calculated following the [14] the coarse mesh during the whole simulation process for ac- method of Zhai et al . curacy. The result was output every 1 h. After the model was Length of trajectory analysis. The length of trajectory run, the horizontal wind field was extracted to calculate the analysis was 3 nights except for extra explanation. If the tra- trajectory. jectory passed an outbreak area of L. sticticalis adults, then According to the flying parameters of L. sticticalis, the tra- another trajectory analysis was made according to the popula- jectory analysis program was compiled with the method ap- tion dynamics at the same location. plied in the numerical weather broadcast by calculating the 1.3 Definition and division of migration peaks trajectory of particles in the air[9]. The procedure exported one Because L. sticticalis has ability to re-migrate, in order to CHEN Xiao et al. / Acta Ecologica Sinica, 2008, 28(4):1521–1535 avoid the repeated counting, we define the migration peak east China a concentrated overwintering area of 6.7u103 hm2 following the standards: (1) the number of moths in the field appeared in Tuquan of Xinganmeng, where the amount of must exceed 1000 per 100 steps; (2) the coherent migratory cocoons in average was 95.9 cocoon/m2[6]. Severe outbreaks process of one swarm of moths within several consecutive occurred in Bashang of Hebei Province and Wulanchabu of days was defined as one peak; (3) the first peak caused by one Inner Mongolia in 1997. However, the outbreak time in all swarm of moths was defined as immigration peak (including areas was commonly later than that in the normal years, and immigration population and local population). After staying at the peak did not emerge until June 18–19. Before these dates, one place for several days, the peak caused by the re-migra- the meadow moths were scarce[15]. For example, the number tion was totally defined as a remigration peak. of moths in the field was 0–10 per 100 steps in Wulanchabu of 1.4 Stages of ovarian development Inner Mongolia before June 18, 3–50 in Kangbao of Hebei According to “Technical Standards of Prediction and Fore- Province before June 17, and only sporadic moths were caught casting of the Meadow Moth in Farming Area”, the stages of by the light trap before June 23 in Yingxian of Shanxi Prov- ovarian development were defined as follows: (1) Transparent ince. stage: there is no oocyte in the ovary; (2) Vitellogenesis stage: In Northeast China, severe outbreaks of the meadow moth there is oocyte in the ovary and some distinct eggs can be seen; occurred in Xinganmeng of Inner Mongolia, and moderate (3) Ovipositing stage: mature eggs are tightly packed laterally, outbreaks occurred in Baicheng of Jilin Province. The emer- and common oviducts and part of the eggs have been laid; (4) gence of outbreaks concentrated on the early half of June (Ta- Late egg-laying stage, oviducts are atrophic and only a little ble 1). Analysis of the migration process showed that the eggs are left. overwintering generation of adults first emerged massively in Xinganmeng in June 5, lasted to June 8, dispersed towards 2 Results Baicheng of Jilin Province along with the strong northwest 2.1 Analysis of the immigration peaks in Northeast China airflow during the nights of June 8–10, and then migrated into during 1997–2007 Qiqihaer of Heilongjiang Province with the southwest airflow Since 1997, L. sticticalis had occurred frequently in North- during the night of June 13. east China. During the 11 years from 1997 to 2007, except for The adults of L. sticticalis emerged in Xinganmeng of slight occurrence in 2000 and 2006 and moderate to slight in Northeast China 10 d earlier than those in Hebei Province. 2005, L. sticticali had caused serious damages in different According to the occurrence time, the source area would not areas, especially in 2004. The following is the analysis of the be the “permanent breeding area” in North China. When the immigration peaks of moths during outbreaks. peak of L. sticticalis emerged, the ovarian development of 2.1.1 Case study of 1997 many females was in the 1st grade, suggesting that they were In the autumn of 1996, the amount of L. sticticalis cocoons just eclosed. By consulting the historical synoptic chart and in the “permanent breeding area” in North China was very low, simulating the wind field, the areas around Xinganmeng, i.e., 1.7–3.1 cocoon/m2 at Xinghe of Inner Mongolia and 0.05 Qiqihaer and so on were under a weak high pressure in June moth/m2 at Kangbao of Hebei Province. However, in North- 4–5, and the wind was so weak for the swarm of L. sticticalis

Table 1 Migration peaks of the meadow moth in northern China in 1997

Moth of peak day Ovarian Longitude Latitude Peak stage First peak day Location Light trap Moth/100 steps in development (ºE) (ºN) (month.day) (month.day) catches the field grades Siziwangqi, Wulanchabu 111.68 41.37 6.18–6.26 6.24 322 500 Ċ–ċ Chayouqianqi, Wulanchabu 113.18 40.78 6.18–6.30 6.22 107 5000 ċ–Č Jining, Wulanchabu 113.08 41.03 6.23–7.20 7.10 4958 3000 – Kangbao, Zhangjiakou 114.60 41.87 6.19–6.25 6.21 201748 – – Yingxian, Shuozhou 113.18 39.58 6.24–7.11 7.80 658 – ċ–Č Yanggao, Datong 113.72 40.38 6.21–7.11 6.28 1812 – Keyouqianqi, Xinganmeng 122.03 46.12 6.50–6.80 6.60 639 1000 ĉ–Ċ Zhalaiteqi, Xinganmeng 122.90 46.72 6.50–6.80 6.60 – 2500 ĉ–Ċ Zhenlai, Baicheng 123.17 45.85 6.90–6.17 6.11 – 5000 – Balinyouqi, Chifeng 118.65 43.52 6.13–6.23 6.13 – 608 ĉ–ċ Tailai, Qiqihaer 123.45 46.40 6.10–6.17 6.14 – 2000 – CHEN Xiao et al. / Acta Ecologica Sinica, 2008, 28(4):1521–1535 to immigrate. On the other hand, high-density cocoons from 3000 per 100 steps in the field. Since there were few overwin- the last autumn were reserved at the local site, thus providing tering cocoons from the year before (1.03/m2 in pasture and adequate moths for the local occurrence. Therefore, L. sticti- 0.8/m2 in agriculture area) and the ovarian development of calis in Northeast China in 1997 came from the overwintering some females during the peak was in the 2nd grade, the popu- areas of Xinganmeng and its surroundings. lation was defined as the immigration swarm. During May 2.1.2 Case study of 1998 23–30, a north wind prevailed from Siberia to North China, The amount of L. sticticalis cocoons was very low domes- and therefore the population was considered to come from the tically in the autumn of 1997. In the spring of 1998, the peak areas out of China (Fig.1). The swarm of moths settled in of moths emerged in most areas in North China since June 10, Siziwangqi temporarily and emigrated with the strong south- except in Siziwangqi of Wulanchabu. For example, in most west wind during the night of May 30–31. Since the southwest counties of Wulanchabu, the outbreaks of L. sticticalis ap- wind only extended to 45ºN, the swarm of moths could only peared in the middle of June; in Kangbao of Zhangjiakou, a migrate into the north of Cilinguolemeng on June 2, and failed peak was monitored with light trap catches on May 31, but the to fly towards northeast further. Meanwhile, in Kangbao of moths in the field were scarce before June 11; in Wanquan of Zhangjiakou, the moths in the field were few, so the peak of Zhangjiakou, the peak emerged on June 15; in Shanxi Prov- light trap catches on May 31 was caused by the passing-by ince, the peak appeared during June 15–28, but the moths in moths (Fig. 2). the field was sporadic, only 10–20 per 100 steps in Yingxian. The outbreak of the meadow moth emerged in the early In Siziwangqi, the amount of moths rose since May 19 and June in Northeast China (Table 2). On the west side of Daxin- burst into a peak in May 29 when the amount of moths reached ganling Mountain, plenty of adults, 2400 per 100 steps in the

Table 2 Migration peaks of the meadow moth in northern China in 1998

Fig. 1 Wind field on the sig945 level at 22:00, May 28, 1998 and the Fig. 2 Forward trajectory of the meadow moth emigrating from 2nd backward trajectory of the meadow moth immigrating in Sizi- Siziwangqi on May 30, 1998 (A) and backward trajectory of the wangqi on May 29, 1998 meadow moth immigrating in Keyouqianqi on June 6, 1998 (B); Kangbao (C) CHEN Xiao et al. / Acta Ecologica Sinica, 2008, 28(4):1521–1535 field, were found on June 2 in Yakeshi. On the east side, the west of Hulunbeier, Chifeng, Tongliao, Inner Mongolia, the peak of moths emerged in June 6–8 in Keyouqianqi of Xin- center of Heilongjiang Province and Baicheng of Jilin Prov- ganmeng, and then dispersed northwards with the southwest ince. The peaks emerged in June 1–10. In the end of May and airflow before a cold cyclone. The immigration peaks emerged the beginning of June, peaks emerged in Keshenketeng of from south to north in Tailai, Dumeng, Yian, Fuyu and so on Chifeng and Yakeshi of Hulunbeier. The amount of moths in in June 7–11. the field was 3000–4000 and 1500–2000, respectively, and the The ovarian development of females during the peak in ovarian development of females was in the 1st or 2nd grade. Yakeshi was in the 1st grade, indicating that the eclosion site There was a cyclone passing by in the night of June 4. The was nearby. Considering the wind direction, most areas of population of L. sticticalis in the north of Chifeng massively Northeast China were controlled by northwest airflow behind migrated into the center of Heilongjiang Province with the the cyclone in May 28–31. Since June 1, the far east area of strong southwest wind in front of the cyclone. The main land- Russia was controlled by high pressure, the center of a low ing sites were Qinggang, Lanxi, Wangkui and so on. The last- pressure moved from Mongolia to Xilinhaote, and the wind ing northwest wind behind the cyclone made the swarm in the direction in the north of Northeast China shifted to east and west of Hulunbeier migrate into Balinyouqi of Linxi in the lasted for 2 days. Since June 4, most areas were controlled by north of Chifeng, leading to another peak (Fig. 3). a weak high pressure, leading to slight wind. Since there was The emergence time of L. sticticalis in Northeast China was no south wind during this period, the outbreak in Yakeshi in 15 d earlier than that in North China, so the swarm was im- the early June was not from North China. The source should possible from the “permanent breeding area” in North China. be local or in the area out of China. From May 29 to June 1, the south area of Mongolia and the The ovarian development of females in the outbreak of drainage area of Yellow River were under a high pressure, and Keyouqianqi on June 6 was in the 3rd or 4th grade, suggesting the lasting northwest wind prevailed in the north of North that the population was from other places. Backward trajec- China and Chifeng. Backward trajectory from Keshenketengqi tory could be traced back to the north of Cilinguolemeng, and led to northwest (Fig. 4), indicating that the source area was then turned northeastwards. It showed that the population the east of Mongolia. On the other hand, Plant Protection Sta- came from the north area of Cilinguolemeng and linked up tion of Xinganmeng observed high density moths on June 13 with the emigrating population from Siziwangqi (Fig. 2). Thus, in Yierxie of Aershan, a place located near the border of China the population of L. sticticalis in the east side of Daxinganling and Mongolia. The amount of moths in the pasture was Mountain was from Siziwangqi and could be traced back fur- 3000–5000 per 100 steps and the ovarian development of 90% ther to the area out of China. females was in the 1st or 2nd grade[17]. It was confirmed that 2.1.3 Case study of 1999 there were plenty of moths eclosing near the border in the The outbreak of L. sticticalis occurred in China in 1999. spring of 2001. The occurring areas of the first generation of larvae were 2.1.5 Case study of 2002–2004 only next to those of the most severe outbreak in 2004. There Because the larva of the 2nd or 3rd generation of L. sticti- were several immigration peaks with large amounts, and the calis occurred seriously during 2001–2003, large amounts of source out of China played an important role on the outbreak. cocoons were found in each autumn and formed 2 separate Three out of the four main immigration peaks originated from overwintering areas. outside China or the bordering areas between China and In the spring of 2002, the overwintering area in Hulunbeier Mongolia, only one from Siziwangqi, Wulanchabu[16]. was 6.7×104 hm2 with a maximal density of 620 cocoon/m2. In 2.1.4 Case study of 2001 the spring of 2003, the scale of overwintering area in the west L. sticticalis cocoons were scarce in the autumn of 2000. In of Hulunbeier was 1.2×106 hm2 with a maximal density of 100 North China, L. sticticalis occurred moderately in 2001. The cocoon/m2, and the survival percentage over winter was peaks emerged mainly around June 20 in North China, later 50%[7]. In the middle of September 2003, larva of the 3rd gen- than the normal years (Table 3). The peak in Siziwangqi of eration occurred in Fuyu and Nehe of Qiqihaer. The total Wulanchabu emerged on June 17. Before June 17, the number overwintering area was 7.1×104 hm2. The average density was of moths was less than 10 with light trap catches and 2–4 per 64.5 cocoon/m2 [8] and the survival percentage over winter was 100 steps in the field. The amount of moths in Kangbao of 85%. It was very unusual that the massive overwintering areas Zhangjiakou started rising on June 5, but the first peak didn’t emerged in Northeast China consecutively. emerge until the night of June 22. Before June 23, the number In 2002, the peak emerged firstly in the east of Hulunbeier of moths per 100 steps in the field was 9–43 in general and and the north of Xinganmeng in May 26–28 with the maximal 100 at most; the peak emerged in the north of Shanxi during amount of moths of 5000–6000 per 100 steps in the field. The June 25–July 2. ovarian development of most females was in the 1st grade, In Northeast China, a series of outbreaks occurred in the indicating that the population was from the local area. With a CHEN Xiao et al. / Acta Ecologica Sinica, 2008, 28(4):1521–1535

Table 3 Migration peaks of the meadow moth in northern China in 2001

Moth of peak day Longitude Latitude Peak stage First peak day Ovarian devel- Location Light trap Moth/100 steps in (ºE) (ºN) (month.day) (month.day) opment grade catches the field Siziwangqi, Wulanchabu 111.68 41.37 6.17–6.26 6.17 402 700 Ċ–ċ Kangbao, Zhangjiakou 114.60 41.87 6.50–7.10 6.24 – 3000 Ċ–Č Yingxian, Shuozhou 113.18 39.58 7.10–7.30 7.10 402 – ĉ–Ċ Yanggao, Datong 113.72 40.38 6.25–6.30 6.26 736 – ĉ–Č Wuzhai, Xinzhou 111.82 38.93 6.28–6.20 6.30 7820 50000 – Late May to Keshenketengqi, Chifeng 117.48 43.28 – – 3000 ĉ mid-June Balinyouqi, Chifeng 118.65 43.52 6.20–6.14 6.60 386 – ĉ–ċ Yakeshi, Hulunbeier 120.73 49.30 5.29–6.25 6.70 – 10000 ĉ–Ċ Keyouzhongqi, Xinganmeng 121.47 45.05 – 6.11 – 10000 Ċ–ċ Aershan, Xinganmeng 119.95 47.17 – 6.13 – 5000 ĉ–Ċ Lanxi, Suihua 126.30 46.28 6.50–6.10 6.50 – 3000 – Qinggang, Suihua 126.13 46.68 6.50–6.10 6.50 – 1500 – Suiling, Suihua 127.12 47.22 6.50–6.12 6.50 15000 5000 –

Fig. 3 Wind field on the sig 945 level at 20:00, June 5, 2001 and the Fig. 4 Wind field on the sig 945 level at 20:00, May 31, 2001 and backward trajectory of the meadow moth immigrating in Balinyouqi the 2nd backward trajectory of the meadow moth immigrating in on June 6, 2001 Keshenketengqi on May 31, 2001 cyclone passing by, the peak emerged in counties in the west ward trajectory analysis indicated that the population in of Heilongjiang Province in succession. Trajectory analysis Heilongjiang Province was from the outbreak area in the west indicated that the main immigration peak came from Hulun- of Hulunbeier (Fig. 5). In the spring of 2003, the temperature beier, the north of Xinganmeng and the border between Mon- in the “permanent breeding area” in North China was con- golia and China. In June 3–4, another peak emerged in the tinuously lower than that in the normal years, so the eclosion north of Chifeng, and the swarm was from Heibei Province. progress of L. sticticalis was inhibited. With the high tem- In 2003, L. sticticalis outbreaks occurred in the west of Hu- perature emerging temporarily in the end of May, part of co- lunberer, the center of Heilongjiang Province and the north of coons eclosed and formed the peak from the end of May to the Chifeng. The overwintering cocoons in the west of Hulunbeier early June. Most of the moths emigrated out of China. Since eclosed massively in the early June. Peak emerged in June 5–6 June 16, temperature began to rise significantly; the second in Baiquan, Hailun and Suiling of Heilongjiang Province with peak emerged in Wulanchabu and Zhangjiakou on June 18. a maximal amount of 10000 per 100 steps in the field. Back- Part of the adults migrated northward and formed the peak in CHEN Xiao et al. / Acta Ecologica Sinica, 2008, 28(4):1521–1535 the north of Chifeng in June 19–25. ince, including Fuyu, Lindian, Dumeng, Nehe, Yian, Baiquan In 2004, L. sticticalis outbreak reached a summit in the 3rd and Keshan, in May 30–June 1, with 4000–10000 moths per outbreak period since 1949, leading to extremely serious 100 steps. The ovarian development of most females was in damage in Heilongjiang Province. The first immigrating peak the 1st grade, indicating that the peak coincided with the eclo- in Northeast China emerged on May 25. A peak was moni- sion peak. The wind during this period was very weak, and the tored with light trap catches in the morning of May 25 (3652 condition was not suitable for immigration. Thus it was con- moths were caught with ovarian development of females in cluded that the population was from the local area. On June 2, the 1st or 2nd grade); meanwhile, the adults in the field were a massive peak emerged in the west of Heilongjiang Province. scarce (only 3–5 per 100 steps), indicating that a swarm mi- The amount of moths in the field was 10000–20000 in Yian, grated by in the night of May 24. The peak emerged in Taonan Keshan and Baiquan, and 40000 at most. Backward trajectory of Jilin Province on May 25 with over 10000 moths per 100 traced back to Jinlin Province, and then returned, indicating steps in the field. Backward trajectory indicated that the im- that the population was still from the local area (Fig. 6–8). The migrants were from the border area adjacent to Russia or population of L. sticticalis in North China migrated into Mongolia, corresponding to the investigations in Russia in the Northeast China for several times. For example, an immigra- spring of 2004. tion emerged in Kangbao in the end of May with 10000– Peak emerged in the center and west of Heilongjiang Prov- 20000 moths per 100 steps in the field. The moth swarm emi-

Fig. 5 Backward trajectories of the meadow moth immigrating in Fig. 6 Backward trajectory of the meadow moth immigrating in Longjiang (A) and Tailai (B) on May 28, 2002 Baiquan on June 5, 2003

Fig. 7 Five day backward trajectory of the meadow moth Fig. 8 Backward trajectories of the meadow moth immigrating in immigrating in Taonan, China (A), Halahei of Keyouqianqi, Heilongjiang Province on June 2, 2004 China (B) and Chita, Russia (C) on May 25, 2004 CHEN Xiao et al. / Acta Ecologica Sinica, 2008, 28(4):1521–1535 grated northeastwards and formed immigration peaks in the The amount of moths reduced day by day from May 29 to north of Xinganmeng, Baicheng on June 3 and in the south of June 3. The adults emigrated into the area out of China and Heilongjiang Province on June 4 (Fig. 9). near the borders. The local eclosion peak appeared in June 2.1.6 Case study of 2007 1–10 with 5000 moths per 100 steps in the field of Siziwang. In the autumn of 2006, L. sticticalis cocoons were mainly In the night of June 9, the moth swarm in Siziwangqi and located in the north of Yinshan Mountain. The massive over- Kangbao emigrated northeastwards massively (Fig. 10). wintering area was Siziwangqi of Wulanchabu. In May 25–26, In 2007, L. sticticalis outbreaks occurred seriously in immigration peak emerged in Kangbao of Zhangjiakou with Northeast China. A peak was monitored firstly in Tongliao on 4000–5000 moths per 100 steps in the field, and ovarian de- June 6, which was from the area out of China (Fig. 11). With a velopment of part of the females was in the 2nd grade. Mean- cyclone passing by in June 10–12, the massive adults of L. while, cocoons in China had not eclosed massively. On the sticticalis immigrated consecutively. On June 10, immigration other hand, center of a cyclone was located in the east of Bai- peaks emerged in Xinganmeng and the southwest of Qiqihaer. kal in May 23–25, the northwest airflow behind the cyclone Backward trajectory traced back to Tongliao and Chifeng, prevailed from the center of Mongolia to North China, and indicating that the peaks were formed by the remigration of thus the immigration peak on May 25 was from the area out of swarms from the area out of China (Fig. 12). On June 11, the China. Due to the abnormal drought, the peak lasted shortly. main immigration peak emerged in Xinganmeng, Qiqihaer

Fig. 9 Two day forward trajectory of the meadow moth emigrating Fig. 10 Two day forward trajectory of the meadow moth from Kangbao (A) and Zhenlai (B) on June 1, 2004 emigrating from Kangbao on June 9, 2007

Fig. 11 Four day backward trajectories of the meadow moth Fig. 12 Backward trajectory of the meadow moth immigrating in immigrating in Naimanqi (A) and Kezuohouqi (B) on June 6, 2007 Tailai on June 10, 2007 CHEN Xiao et al. / Acta Ecologica Sinica, 2008, 28(4):1521–1535 and Hulunbeier, which was linked up to the emigrating popu- The moths came from the local area (e.g. in 1997) or the areas lation perfectly on a spatio-temporal scale. On June 12, with a near the borders and out of China (e.g. in 2001 and 2005). In cyclone moving out of China, the immigrating population 1998, the peak emerged since the middle of June in North dispersed further with the northwest airflow after the cyclone. China except Siziwangqi. The population out of China immi- 2.1.7 Statistics on the source area of the spring grated into Siziwangqi at the end of May and migrated again population of L. sticticalis in Northeast China into Northeast China in the early June. There were a total of 46 peaks during 1997–2007, including (2) In the last autumn, there were some overwintering co- 26 immigration peaks and 20 remigration peaks. The source coons in the “permanent breeding area”, but the density was areas were divided into 4 sections (Fig. 13) and the immigra- low. In 1999, the peak emerged almost at the same time as in tion peaks were summarized by groups (Table 4). Northeast and North China. Most of the population in North- Eight peaks could be traced back to the “permanent breed- east China was from the area out of China or near the borders. ing area” in North China, including two from Wulanchabu and (3) In the last autumn, there were concentrated overwintering six from the northwest of Hebei Province or the south of Xil- Table 4 Statistics on peaks of the meadow moth in Northeast inguolemeng. The characteristics of these peaks were that the China (1997–2007) amount was large and the females were mature. But the num- Number of immigration peaks Number of ber of peaks was less than one third of the total number of Year A B1 B2 C remigration peaks peaks. Only the immigrants in 2007 formed the main peak. 1997 1 2 Eight peaks could be traced back to the east of Inner Mongolia 1998 1 1 and Songnen Plain. Ten peaks could be traced back to the area out of China including the east of Mongolia and Siberia of 1999 1 3 2 Russia. 2000 – – – – – 2.2 Effects of overwintering amount of L. sticticalis in the 2001 1 2 3 “permanent breeding area” on the outbreak in Northeast 2002 1 1 4 China 2003 2 1 1 1 4 The concentrated overwintering areas of L. sticticalis in 2004 2 3 1 2 China were summarized (Table 5). The years during the 3rd 2005 1 1 outbreak of L. sticticalis in China were divided into 4 types by 2007 1 1 2 the difference of overwintering amount: Total 8 4 4 10 20 (1) In the last autumn, there were no or scarce overwinter- Note: A, B1, B2 and C represent the same areas in Fig. 11 ing cocoons in the “permanent breeding area”. In the years 1997, 2001 and 2005, the peaks in North China emerged on Table 5 Distributions of concentrated overwintering areas of June 20, but peaks in Northeast China emerged in the early the meadow moth in China since 1996 half of June, over 10 days earlier than those in North China. Proportion Density Year Location (hm2) (/m2) 1996 Xinganmeng 6.7×103 95.90 1999 Datong 1.1×104 20.00–30.00 2001 Hulunbeier 6.7×104 3.00–5.00 Datong, Shuozhou 5.3×104 10.00 Kangbao 1.9×104 16.20 Erdos – 19.20 Wulanchabu 6.7×105 18.50 2002 Hulunbeier(2) 1.2×106 3.00–5.00 Datong 4.5×104 23.00 Zhangjiakou and Chengde 15.7×104 8.90 Erdos 6.7×104 4.50 2003 Qiqihaer 7.1×104 64.40 Hulunbeier 2.0×104 0.50 Datong 1.7×105 51.20 Shuozhou 8.0×104 40.00 Fig. 13 Partition of the source area of the meadow moth 2006 Siziwangqi, Wulanchabu 1.0×105 9.13 (A) Permanent breeding area in North China; (B1) east of Inner Mongo- (1) Investigation was conducted in the autumn or the next spring. lia; (B2) Songnen Plain; (C) overwintering areas in Mongolia (2) Most of the cocoons were located in the west of Daxinganling and Russia Mountain in 2002. CHEN Xiao et al. / Acta Ecologica Sinica, 2008, 28(4):1521–1535 areas in the “permanent breeding area”, but none in Northeast emigrating moths could not keep a persistent direction, the China. In the autumn of 1999, the concentrated overwinter ovarian development of the females became mature, and then areas were located in Datong of Shanxi Province. In the spring the chance to immigrate into Northeast China would reduce of 2000, a large number of spring adults emerged consecu- gradually. tively in Datong of Shanxi Province, Zhangjiakou of Hebei In spring, the low pressure was formed in the downstream Province and Wulanchabu of Inner Mongolia. In Northeast of Heilongjiang River due to the rising temperature of the China, only the north of Chifeng was influenced by the little ground, while the high pressure was located over Japan Sea immigrants. L. sticticalis occurred a little in most of the areas. and Yellow Sea[18]. This situation led to prevalence of the In the autumn of 2006, the concentrated overwintering areas south wind in Northeast China in spring, especially when a were located in Siziwang of Wulanchabu. The spring popula- cyclone passed by or was generated in Northeast China. In tion in 2007 migrated into the east of Inner Mongolia and the North China, May and June are the time for the exchange of west of Heilongjiang Province. winter wind and summer wind. In most of the areas, the south (4) In the last autumn, there were concentrated overwinter- wind began to prevail, but the northwest wind still frequently ing areas both in the “permanent breeding area” and in North- appeared in the “permanent breeding area” in the north of east China. In the spring of 2002–2004, overwintering areas North China, and the southwest wind was not predominant appeared in North China and Northeast China, respectively. In (Fig. 14). each of these years, there were one or two immigration peaks The frequency of strong southwest wind at altitude of 600 from the “permanent breeding area”, but all the outbreak m (speed > 8 m/s) was calculated based on the sounding data population in the main peak was from the local areas. in June of 1997–2003. The result showed that the strong The analysis showed that the outbreak of L. sticticalis in southwest wind concentrated in the plain area of Northeast Northeast China was influenced weakly by the overwintering China and was scarce in the “permanent breeding area” (Fig. amount in the “permanent breeding area” (including the areas 15). Thus, there was no suitable wind for the meadow moth to around) in North China, but related strongly to the local area take a long-range migration towards Northeast China. and the areas out of China at the same latitude. 2.4 Reasons of overwintering area emerging in Northeast 2.3 Restraint factors of long-range migration into Northeast China China for adults in the “permanent breeding area” In Hulunberer, the larva of the 2nd generation could dia- Since the flying ability is weak, L. sticticalis must take ad- pause and overwinter. As the 2nd generation occurred rarely vantage of strong wind to finish a long-range migration. Thus, before 1990s, the overwintering moths were scarcely found in the key factor for L. sticticalis in North China to migrate into any year[1]. Studies of Luo et al. showed that the effective Northeast China is whether southwest strong wind exists on a accumulated temperature for the whole generation of L. stic- large scale or not when the females are in the immature stages. ticalis was 531.2qC/day[13]. By analyzing the surface mete- If the wind was weak or the direction changed frequently, the orological data in 1951–1983, the effective accumulated tem-

Fig. 14 Statistics of wind directions at 850 hPa at Zhangjiakou Plant Fig. 15 Occurrences of strong southwest wind at an altitude of Protection Station from May 11 to June 20 (1997–2007) 600 m in June, 1997–2003 (wind speed > 8m/s, and the wind direction was between 180° and 270°) CHEN Xiao et al. / Acta Ecologica Sinica, 2008, 28(4):1521–1535 perature in Hailaer was enough for L. sticticalis to develop 1.4 In the area of Zhangjiakou of Hebei Province, Datong of generations, suggesting that one generation could occur in Shanxi Province and Wulanchabu of Inner Mongolia, the ter- Hailaer. This result corresponded to the practical phenomena rain and climate are very complex, the larva of the last genera- at that time[19]. tion could find suitable place to overwinter every year, and With the global warming since 1990s, the surface tempera- hence this area became the “permanent breeding area” in ture in North China had increased notably, e.g., the annual China. But the analysis on the population dynamics of L. stic- average temperature of Hailaer in 1991–1999 was 2qC higher ticalis during the 3rd outbreak period since 1949 showed that than that in 1951–1980. The field investigation showed that most of the spring populations of L. sticticalis in Northeast the frequency of the 2nd generation in the east of Inner Mon- China were not from the “permanent breeding area” in North golia increased notably and left behind a large number of China. The followings are the main reasons: overwintering cocoons since 1996. In order to understand the (1) In some years (i.e. 1997, 2001 and 2005), the peaks of L. effects of temperature change on the number of generations, sticticalis in Northeast China were 10 days earlier than those the effective accumulated temperature and the variation in the in North China. There was no relationship between the two number of generations were calculated with the average sur- areas during these years. face temperature in Hailaer in 1951–2006 (Fig. 16). (2) Since 1996, concentrated overwintering areas had been Figure16 showed that number of the calculated generation found in the east of Inner Mongolia and Heilongjiang Prov- was less than 1.5 in most of the years before 1990s. But since ince for several times. The investigation on survival percent- 1990s, the effective accumulated temperature increased nota- age after overwintering indicated that most of the larva over- bly, and thus number of the calculated generation was about 2 wintered successfully and provided abundant local source for in 2000–2002. In 2001–2002, the serious outbreak of the 2nd the outbreak for the next year. generation larva in Hulunbeier was just under such a climate (3) When the moth swarm from the “permanent breeding warming condition. Though no 2nd generation was monitored area” arrived in the plain in Northeast China after flying for in Hulunbeier in 2000 (because the adults of the overwintering consecutive days, the ovarian development of most females generation and larva of the 1st generation occurred a little). should be in the 2nd or 3rd grade. But the first peak in North- However, based on the analysis before, it was concluded that east China often emerged with many females in the 1st grade, in the autumn of 2000, the overwintering amount out of China which is a typical characteristic of local population. was high and the concentrated overwintering area would be in (4) The analysis of the migration process in each year the east of Mongolia, just close to the borders. It could be showed that the immigration peaks from North China only presumed that the 2nd generation of L. sticticalis occurred accounted for one third of the total peaks in Northeast China seriously there. These analyses showed that climate warming and only the immigrants in 2007 formed the main source. On is the main reason for the increasing frequency of the 2nd the other hand, the moths from North China were not always generation of L. sticticalis in Hulunbeier. The physical condi- the local population. Considerable population was from the tion in the east of Mongolia was similar to that in Hulunbeier, overwintering area out of China. and thus the overwintering L. sticticalis would emerge in the ex- (5) Whether the cocoons of L. sticticalis could overwinter pansive grassland in the years when the 2nd generation occurred. in one place or not depends on the local occurrence of larva of 3 Discussion and conclusions the 2nd and 3rd generation, whose occurrence degree is influenced by the climate remarkably and the varied outbreak areas 3.1 “Permanent breeding area” of China is not the source between years. Thus, even in the “permanent breeding area”, area of L. sticticalis in Northeast China the concentrated overwinter area didn’t emerge every autumn. The summary of the overwintering areas in China since 1996 showed that the overwintering amount in the “permanent breeding area” (including the areas around) had little effect on the outbreak in Northeast China. Therefore, the spring populations of L. sticticalis in North- east China and North China were relatively independent; the moth swarm in North China could migrate into Northeast China and act as one of the sources, in particular the main source during the outbreak period. The frequency of southwest Fig. 16 Variation in the number of generations of the meadow wind in the “permanent breeding area” each June is low, which moth calculated with the effective accumulated temperature in might be one important reason to restrain the local population Hailaer during 1951–2006; the effective accumulated tempera- to take long-range migration northeastwards. ture of the whole generation is 531.2qC/day CHEN Xiao et al. / Acta Ecologica Sinica, 2008, 28(4):1521–1535

3.2 Moth swarms in the south area of Yinshan Mountain from the areas out of China. Thus, the overwintering area out with little probability to migrate into Northeast China of China influences the outbreak of L. sticticalis in Northeast By analyzing the migration processes, the immigrants from China strongly. North China could be traced back to Zhangjiakou of Heibei Is there one or several “permanent breeding areas” out of Province and the north of Wulanchabu, Inner Mongolia (at the China? Where are they distributed and how do they form? north side of Yinshan Mountain), and linked with the emigra- Whether the abnormal fluctuation of the population of L. stic- tion peak locally. Only a few swarms among them can be ticalis in China among years and generations, and the phe- traced back further to Datong and Xinzhou of Shanxi Province nomena of periodic outbreak are their behavior of migrations and Erdos of Inner Mongolia. More information could be col- on large spatio-temporal scales or not? These problems need lected when the distributions of overwintering areas were con- to be studied further in the future. sidered. In the autumn of 1999, concentrated overwintering areas were located in the south of Yinshan Mountain and the Acknowledgements outbreak range in the next year could only be expanded to the This work was supported by the National Basic Research north of Heibei. In the autumn of 2006, concentrated over- Program of China (No. 2006CB102007) and the National Key wintering areas were located in the north of Yinshan Mountain Technology R&D Program of China (No. 2006BAD08A01). and the spring adults in the next year could migrate into Northeast China massively. 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