Seasonal Patterns of Protoschinia scutosa (Lepidoptera: Noctuidae) Migration Across China’s Bohai Strait

Seasonal Patterns of Protoschinia scutosa (Lepidoptera: Noctuidae) Migration Across China’s... Abstract The spotted clover moth, Protoschinia scutosa (Denis & Schiffermüller) (Lepidoptera: Noctuidae), is an important polyphagous pest that is widely distributed in the world. P. scutosa overwinters as pupae in agricultural soils in Northern China. Yet, it is unclear whether P. scutosa also engages in seasonal migration over mid- to long-range distances. In this study, we employ light trapping, field surveys, and ovarian dissection of captured adults over a 2003–2015 time period to assess P. scutosa migration in Northern China. Our work shows that P. scutosa migrates across the Bohai Strait seasonally; the mean duration of its windborne migration period was 121.6 d, and the mean trapping number was 1053.6 moths. Nightly catches of P. scutosa were significantly different between months, but the differences between years were not significant. During 2009–2011 and 2013, the monthly proportion of migrating females (65.5%) was significantly higher than that of males and showed no difference between months. In May to June, the majority of females (May: 63.0%; June: 61.1%) were mated individuals with relatively high level of ovarian development; however, in August and September, most females were unmated. The mean proportion of mated females was significantly different across months but did not differ between years. The results of long-term searchlight trapping and ovarian dissection indicate that P. scutosa exhibits a seasonal characteristic of typical population dynamics and reproductive development of migratory insects. Our work sheds light upon key facets of P. scutosa ecology and facilitates the future development of pest forecasting systems and pest management schemes. spotted clover moth, aerobiology, light trapping, ovarian dissection, trans-regional migration Migration, an important part of many insects’ life history, can facilitate the rapid exploitation of alternative habitat in response to seasonal environmental changes (Dingle 1972, Holland et al. 2006, Chapman et al. 2015). Large biomass of insects migrates within and between continents seasonally, which usually accounts for sudden outbreaks of crop pests and insect-vectored plant diseases (Chapman et al., 2015). A better understanding of the migratory behavior of agricultural pests in particular can constitute the basis for further development of forecasting and early-warning systems or for the deployment of integrated pest management (IPM) strategies (Dingle 1985, Rankin and Burchsted 1992, Irwin 1999, Wu and Guo 2005, Nathan et al. 2008, Dingle 2014). Many insect species were reported as migrants; however, the general pattern of how these species undertake long-distance seasonal migration across different locations or regions is unknown in most cases. And also, the phenomenon that sexually immature individuals were the initiator of emigration contributed to the proposal of “oogenesis-flight syndrome” (Johnson 1969), in which reproductive development and migratory behavior were regarded as two incompatible physiological states. But, the intrinsic relationship between reproduction and migration is not simply an antagonistic relationship in many insect species. The spotted clover moth (SCM), Protoschinia scutosa (Denis & Schiffermüller) (Lepidoptera: Noctuidae), is an occasional pest in agricultural and forage-production systems of Northern China. As a polyphagous herbivore, SCM has been recorded from more than 20 different host plants, including agricultural or fodder crops such as soybean (Glycine max Merrill [Fabales: Leguminosae]) (He 1997), alfalfa (Medicago sativa L. [Fabales: Leguminosae]) (Wang et al. 2011, Zhang et al. 2016), quinoa (Chenopodium quinoa Willd [Caryophyllales: Chenopodiaceae]) (Li et al. 2017), sunflower (Helianthus annuus L. [Asterales: Asteraceae]) (Dekhtiarev 1928), wild wormwood (Artemisia argyi H. Lév. & Vaniot [Asterales: Asteraceae]), and pigweed (Chenopodium serotinum L. [Caryophyllales: Chenopodiaceae]) (Abdurakhmanov et al. 2013). On these plants, P. scutosa larvae feed on seedlings, tender leaves, and stems (He 1997, Skinner 1998, Bradley 2000). The species is widely distributed across the globe and has been reported from Europe, North America, Asia, and North Africa (He 1997, Chen 1999, Bradley 2000, Sokolova 2002, Matov et al. 2008). In China, P. scutosa occurs nationwide and completes 3–6 generations per year depending upon local climatic conditions. In certain areas, SCM overwinters as pupae in soil, while the species sustains continuous populations in southernmost parts of the country (Liu and Zhang 1989, Fan 1990, Xu and Yang 2007). In recent years, the range of occurrence of SCM has expanded and increasing crop damage on several crops in Northern China, such as soybean (He 1997), quinoa (Li et al. 2017), and alfalfa (Zhang et al. 2016). P. scutosa and the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), possess similar morphology, life history, dietary host range, and geographical distribution (Wang 1981). For H. armigera, its wide distribution and pest status in several crops are mainly due to its omnivorous feeding and behavior strategies, facultative diapauses, and seasonal migration (Fitt 1989, Feng et al. 2005, Feng et al. 2009). More specifically, H. armigera overwintering generations migrate in early spring from the Yellow River Valley into northeastern China, where they feed on spring maize and soybeans (Feng et al. 2009). In autumn, large numbers of H. armigera then migrate back from northeastern China (Feng et al. 2005). Diapause and migration are two different strategies to adapt to environmental changes (Dingle 2014). Previous research suggests SCM might be a migratory species (Oku 1978); however, the seasonal patterns of migrant species exhibits in Northern China remain unclear. Considering the climate-induced poleward expansion of many insect species (Robertson 2009, Pateman et al. 2012) and the increasing pest status of P. scutosa in Northern China, it is critical to gain further insights into migration patterns of this species. In this study, we rely upon light trapping and ovarian dissection of field-caught individuals to assess P. scutosa migration over 13 consecutive years on Beihuang Island (BH), at the center of the Bohai Strait in Northern China. This work not only provides critical insights into P. scutosa life history and ecology but also is important for the further development of pest forecasting systems and pest management strategies. Materials and Methods Study Site All research was conducted at the field experimental station of the Chinese Academy of Agricultural Sciences (CAAS) on BH (38º24′ N; 120º55′ E), Shandong province, China. BH has a land area of 2.5 km2 and located in the center of the Bohai Strait, approximately 40 km from Liaodong Peninsula and 60 km from Jiaodong Peninsula (Zhao et al. 2016). Light Trapping and Field Observation Light trapping was conducted from April to October during 2003–2015 on BH. The trapping device was adapted to sample insects flying at high altitude and was equipped with a 1,000 W metal halide lamp (model JLZ1000BT; Shanghai Yaming Lighting Co. Ltd., Shanghai, China), mounted on a platform approximately 8 m above sea level (asl). The device emitted a beam of light with a 105,000 lm, a color temperature of 4,000 K, and a color rendering index of 65 to attract moths migrating overhead at altitudes up to 500 m above the ground level (Feng et al. 2009; Fu et al. 2014a, b). To collect insects, a nylon net bag (60 mesh) was placed beneath the trap and changed every 2 h throughout the night. The lamp was turned on at sunset and solely operated at night and was used on a daily basis from April to October 2003–2015. Incomplete data sets caused by extreme weather conditions (e.g., heavy rains, typhoon, thunderstorm) or long-term power outages were excluded from the analysis. For nights during which trapping proceeded normally, but no P. scutosa was caught, a “zero” was entered in the dataset. Trapped insects were stored at −20°C for at least 4 h prior to laboratory processing and ovarian dissection. The island has no farmland, and none of the main host plant of P. scutosa is present, but potential host plants, such as graminaceous weeds, mulberry (Morus alba L.), and some pine trees, still exist. To ascertain whether there is a local population of P. scutosa on these plants, field investigations for larvae and pupae were conducted from April to October in 2003–2015. Ovarian Dissection To test the hypothesis of “oogenesis-flight syndrome” for P. scutosa migratory population, we select a subsample of maximum 20 females randomly during each night in 2009–2011 and 2013. Under a stereomicroscope (model JNOEC-Jsz4; Motic China Group Co. Ltd., Xiamen, China), we dissected the subsample and estimated the level of ovarian development (from 1 to 5) using criteria of H. armigera (Zhang and Mou 1994). These data were used to generate an average monthly level of ovarian development (i.e., the sum of individual levels of ovarian development divided by the number of females dissected in a month. Females with ovarian development levels 1–2 were regarded as “sexually immature” individuals, while those with levels 3–5 were regarded as “sexually mature” individuals (Zhang et al. 1979, Shi 1984, Li et al. 1987). Moreover, mating occurrence and frequency of P. scutosa were determined by assessing the presence and number of spermatophores in female’s spermatheca (Zhang et al. 1979). We calculated the proportion of mated females monthly and regarded the average of daily reproductive in that month as a monthly value. Data Analysis Differences in the daily P. scutosa captures and monthly records of sex ratio, sexually mature female proportion, and mated ratio were analyzed using generalized linear mixed models (GLMM), in which the month was a fixed effect and the year was a random effect. Monthly sex ratios (female: male) were compared using a chi-square test (PROC FREQ). Differences in the mean proportions of mated females and between sexually mature and immature females in each month were assessed with t-tests (PROC TTEST, the proportion data were arcsine square root transformed). Total annual catches of P. scutosa were analyzed by hierarchical cluster analysis, using the “Nearest-neighbor method” based on Euclidean distances (Zhang et al. 2015). The generalized linear mixed-effect regressions and hierarchical cluster analysis were statistically processed using SPSS version 20 (IBM Corp, New York, NY, 2011) and Data Processing System (DPS) version 9.5 (Tang 2013), respectively. Other statistical analyses were performed by SAS version 9.2 (SAS Institute, Cary, NC, 2001). Results Temporal Migration Pattern During field surveys on BH Island, no P. scutosa larvae were found. However, SCM was regularly captured in the halid lamp (Table 1, Fig. 1), with daily number of catches significantly different between months (F6, 2051 = 17951.1, P < 0.001) and with a significant month × year interaction (P < 0.001) (Table 2). However, the variation between years (P = 0.181) was not significant (Table 2). Table 1. Overall introduction of Protoschinia scutosa moths caught in the light trapping on BH during 2003–2015 Year Date of first capture (n)* Date of final capture (n)* Duration (d) Date of peak catches (n)* Total catches 2003 19 July (5) 27 Aug. (6) 40 25 Aug. (1224) 1,291 2004 15 May (1) 13 Sept. (2) 122 25 Aug. (29) 1,27 2005 20 May (1) 14 Sept. (6) 118 29 July (229) 1,146 2006 17 May (2) 29 Sept. (1) 136 1 Aug. (165) 1,195 2007 19 May (3) 13 Sept. (2) 135 31 May (40) 677 2008 15 May (1) 28 Sept. (1) 142 14 Aug. (200) 1,501 2009 13 May (1) 17 Sept. (1) 139 26 May (196) 1,767 2010 5 June (1) 13 Sept. (1) 101 9 Aug. (213) 1,194 2011 23 May (3) 9 Sept. (1) 110 2 Sept. (52) 603 2012 6 May (1) 13 Sept. (1) 131 20 Aug. (297) 1,208 2013 7 May (1) 14 Sept. (25) 131 6 Aug. (48) 875 2014 2 May (1) 20 Sept. (1) 153 9 Aug. (72) 1,074 2015 9 May (1) 8 Sept. (2) 123 14 July (88) 1,039 Mean – – 121.6 – 1053.6 SE – – 7.8 – 115.3 Year Date of first capture (n)* Date of final capture (n)* Duration (d) Date of peak catches (n)* Total catches 2003 19 July (5) 27 Aug. (6) 40 25 Aug. (1224) 1,291 2004 15 May (1) 13 Sept. (2) 122 25 Aug. (29) 1,27 2005 20 May (1) 14 Sept. (6) 118 29 July (229) 1,146 2006 17 May (2) 29 Sept. (1) 136 1 Aug. (165) 1,195 2007 19 May (3) 13 Sept. (2) 135 31 May (40) 677 2008 15 May (1) 28 Sept. (1) 142 14 Aug. (200) 1,501 2009 13 May (1) 17 Sept. (1) 139 26 May (196) 1,767 2010 5 June (1) 13 Sept. (1) 101 9 Aug. (213) 1,194 2011 23 May (3) 9 Sept. (1) 110 2 Sept. (52) 603 2012 6 May (1) 13 Sept. (1) 131 20 Aug. (297) 1,208 2013 7 May (1) 14 Sept. (25) 131 6 Aug. (48) 875 2014 2 May (1) 20 Sept. (1) 153 9 Aug. (72) 1,074 2015 9 May (1) 8 Sept. (2) 123 14 July (88) 1,039 Mean – – 121.6 – 1053.6 SE – – 7.8 – 115.3 *The numbers of P. scutosa moths captured on the indicated dates are provided in parentheses. View Large Table 1. Overall introduction of Protoschinia scutosa moths caught in the light trapping on BH during 2003–2015 Year Date of first capture (n)* Date of final capture (n)* Duration (d) Date of peak catches (n)* Total catches 2003 19 July (5) 27 Aug. (6) 40 25 Aug. (1224) 1,291 2004 15 May (1) 13 Sept. (2) 122 25 Aug. (29) 1,27 2005 20 May (1) 14 Sept. (6) 118 29 July (229) 1,146 2006 17 May (2) 29 Sept. (1) 136 1 Aug. (165) 1,195 2007 19 May (3) 13 Sept. (2) 135 31 May (40) 677 2008 15 May (1) 28 Sept. (1) 142 14 Aug. (200) 1,501 2009 13 May (1) 17 Sept. (1) 139 26 May (196) 1,767 2010 5 June (1) 13 Sept. (1) 101 9 Aug. (213) 1,194 2011 23 May (3) 9 Sept. (1) 110 2 Sept. (52) 603 2012 6 May (1) 13 Sept. (1) 131 20 Aug. (297) 1,208 2013 7 May (1) 14 Sept. (25) 131 6 Aug. (48) 875 2014 2 May (1) 20 Sept. (1) 153 9 Aug. (72) 1,074 2015 9 May (1) 8 Sept. (2) 123 14 July (88) 1,039 Mean – – 121.6 – 1053.6 SE – – 7.8 – 115.3 Year Date of first capture (n)* Date of final capture (n)* Duration (d) Date of peak catches (n)* Total catches 2003 19 July (5) 27 Aug. (6) 40 25 Aug. (1224) 1,291 2004 15 May (1) 13 Sept. (2) 122 25 Aug. (29) 1,27 2005 20 May (1) 14 Sept. (6) 118 29 July (229) 1,146 2006 17 May (2) 29 Sept. (1) 136 1 Aug. (165) 1,195 2007 19 May (3) 13 Sept. (2) 135 31 May (40) 677 2008 15 May (1) 28 Sept. (1) 142 14 Aug. (200) 1,501 2009 13 May (1) 17 Sept. (1) 139 26 May (196) 1,767 2010 5 June (1) 13 Sept. (1) 101 9 Aug. (213) 1,194 2011 23 May (3) 9 Sept. (1) 110 2 Sept. (52) 603 2012 6 May (1) 13 Sept. (1) 131 20 Aug. (297) 1,208 2013 7 May (1) 14 Sept. (25) 131 6 Aug. (48) 875 2014 2 May (1) 20 Sept. (1) 153 9 Aug. (72) 1,074 2015 9 May (1) 8 Sept. (2) 123 14 July (88) 1,039 Mean – – 121.6 – 1053.6 SE – – 7.8 – 115.3 *The numbers of P. scutosa moths captured on the indicated dates are provided in parentheses. View Large Table 2. Summary of analysis of GLMM on catches, female captures, mated female catches, and mature female catches of Protoschinia scutosa moths on BH Island from April to October during 2003–2015 Target variable Main results of GLMM analysis Moth catches Fixed effect Factor F df1 df2 P value Month 17951.1 6 2051 <0.001 Random effect Factor Variance SE Z P value Year 0.2 0.2 1.3 0.181 Month×Year 0.8 0.2 4.2 <0.001 Female catches Fixed effect Factor F df1 df2 P value Month 1.3 4 4434 0.146 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.9 0.346 Month×Year 0a Mated female catches Fixed effect Factor F df1 df2 P value Month 46.8 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.6 0.579 Month×Year 0.1 0.1 1.1 0.283 Mature female catches Fixed effect Factor F df1 df2 P value Month 34.2 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0a Month×Year 0.1 0.1 1.4 0.165 Target variable Main results of GLMM analysis Moth catches Fixed effect Factor F df1 df2 P value Month 17951.1 6 2051 <0.001 Random effect Factor Variance SE Z P value Year 0.2 0.2 1.3 0.181 Month×Year 0.8 0.2 4.2 <0.001 Female catches Fixed effect Factor F df1 df2 P value Month 1.3 4 4434 0.146 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.9 0.346 Month×Year 0a Mated female catches Fixed effect Factor F df1 df2 P value Month 46.8 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.6 0.579 Month×Year 0.1 0.1 1.1 0.283 Mature female catches Fixed effect Factor F df1 df2 P value Month 34.2 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0a Month×Year 0.1 0.1 1.4 0.165 Moth catches of P. scutosa was subject to a Poisson distribution with Poisson regression as link function, and other target variables were subject to a binomial distribution with logistic regression as link function in the analysis of GLMM. LB and UB: lower and upper bound of the 95% CI. a: Redundant parameter. View Large Table 2. Summary of analysis of GLMM on catches, female captures, mated female catches, and mature female catches of Protoschinia scutosa moths on BH Island from April to October during 2003–2015 Target variable Main results of GLMM analysis Moth catches Fixed effect Factor F df1 df2 P value Month 17951.1 6 2051 <0.001 Random effect Factor Variance SE Z P value Year 0.2 0.2 1.3 0.181 Month×Year 0.8 0.2 4.2 <0.001 Female catches Fixed effect Factor F df1 df2 P value Month 1.3 4 4434 0.146 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.9 0.346 Month×Year 0a Mated female catches Fixed effect Factor F df1 df2 P value Month 46.8 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.6 0.579 Month×Year 0.1 0.1 1.1 0.283 Mature female catches Fixed effect Factor F df1 df2 P value Month 34.2 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0a Month×Year 0.1 0.1 1.4 0.165 Target variable Main results of GLMM analysis Moth catches Fixed effect Factor F df1 df2 P value Month 17951.1 6 2051 <0.001 Random effect Factor Variance SE Z P value Year 0.2 0.2 1.3 0.181 Month×Year 0.8 0.2 4.2 <0.001 Female catches Fixed effect Factor F df1 df2 P value Month 1.3 4 4434 0.146 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.9 0.346 Month×Year 0a Mated female catches Fixed effect Factor F df1 df2 P value Month 46.8 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.6 0.579 Month×Year 0.1 0.1 1.1 0.283 Mature female catches Fixed effect Factor F df1 df2 P value Month 34.2 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0a Month×Year 0.1 0.1 1.4 0.165 Moth catches of P. scutosa was subject to a Poisson distribution with Poisson regression as link function, and other target variables were subject to a binomial distribution with logistic regression as link function in the analysis of GLMM. LB and UB: lower and upper bound of the 95% CI. a: Redundant parameter. View Large Fig. 1. View largeDownload slide Nightly catches of each year (A) and annual mean logarithm of nightly catches (B) of Protoschinia scutosa moths in the light trap on BH Island from April to September during 2003–2015. Fig. 1. View largeDownload slide Nightly catches of each year (A) and annual mean logarithm of nightly catches (B) of Protoschinia scutosa moths in the light trap on BH Island from April to September during 2003–2015. The average number of moths captured annually in the halid lamp was 1053.6 ± 115.3 during 2003–2015. The cluster analysis indicated that total annual SCM captures could broadly be divided into five groups (Table 3). The largest migration occurred in 2009 with 1767 catches; the mass migration appeared in 2008; the normal migration appeared in 2003, 2005, 2006, 2010, and 2012–2015; the weak migration occurred in 2007 and 2011; the rare migration occurred in 2004 with a total catches of 127 individuals. Table 3. Hierarchical clustering analysis of group on the annual number of Protoschinia scutosa captured in a light trap on BH Island during 2003–2015 Group Year Observed value (total capture per year) Distance to the center Group mean Root mean square deviation First group 2004 127 0.0 127 – Second group 2003 1,291 163.3 1127.8 57.8 2005 1,146 18.3 2006 1,195 67.3 2010 1,194 66.3 2012 1,208 80.3 2013 875 252.8 2014 1,074 53.8 2015 1,039 88.8 Third group 2007 677 37.0 640 23.4 2011 603 37.0 Fourth group 2008 1,501 0.0 1,501 – Fifth group 2009 1,767 0.0 1,767 – R2 0.9 Pseudo F 32.6 P <0.001 Group Year Observed value (total capture per year) Distance to the center Group mean Root mean square deviation First group 2004 127 0.0 127 – Second group 2003 1,291 163.3 1127.8 57.8 2005 1,146 18.3 2006 1,195 67.3 2010 1,194 66.3 2012 1,208 80.3 2013 875 252.8 2014 1,074 53.8 2015 1,039 88.8 Third group 2007 677 37.0 640 23.4 2011 603 37.0 Fourth group 2008 1,501 0.0 1,501 – Fifth group 2009 1,767 0.0 1,767 – R2 0.9 Pseudo F 32.6 P <0.001 View Large Table 3. Hierarchical clustering analysis of group on the annual number of Protoschinia scutosa captured in a light trap on BH Island during 2003–2015 Group Year Observed value (total capture per year) Distance to the center Group mean Root mean square deviation First group 2004 127 0.0 127 – Second group 2003 1,291 163.3 1127.8 57.8 2005 1,146 18.3 2006 1,195 67.3 2010 1,194 66.3 2012 1,208 80.3 2013 875 252.8 2014 1,074 53.8 2015 1,039 88.8 Third group 2007 677 37.0 640 23.4 2011 603 37.0 Fourth group 2008 1,501 0.0 1,501 – Fifth group 2009 1,767 0.0 1,767 – R2 0.9 Pseudo F 32.6 P <0.001 Group Year Observed value (total capture per year) Distance to the center Group mean Root mean square deviation First group 2004 127 0.0 127 – Second group 2003 1,291 163.3 1127.8 57.8 2005 1,146 18.3 2006 1,195 67.3 2010 1,194 66.3 2012 1,208 80.3 2013 875 252.8 2014 1,074 53.8 2015 1,039 88.8 Third group 2007 677 37.0 640 23.4 2011 603 37.0 Fourth group 2008 1,501 0.0 1,501 – Fifth group 2009 1,767 0.0 1,767 – R2 0.9 Pseudo F 32.6 P <0.001 View Large A pronounced seasonal pattern was evident in SCM captures, with the mean migration period being 121.6 ± 7.8 d (ranging from 40 to 153 d,). The first capture of SCM in a year generally occurred in mid-May. Subsequently, SCM was trapped intermittently with mean captures 95.9 ± 22.9 individuals from May to June. Trap catches increased in mid-July and continued through mid-August to then gradually decrease to zero by mid-September (Fig. 1, Table 1). Seasonal Sex Ratio and Mating Patterns During 2009–2011 and 2013, the proportion of females in total trap captures was significantly greater than that of males (Table 4; Fig. 2a and b). The monthly proportion of migrating females (65.5 ± 2.5%) was significantly higher than that of males (Table 4), and average monthly trapping amount of females did not differ between months (F4, 4434 = 1.3, P = 0.146) and years (P = 0.346) (Table 2.). Table 4. Results of chi-square tests on the sex ratio of monthly Protoschinia scutosa catches on BH during 2009–2011 and 2013 Month Female Male df Chi-square (χ2) P value Mean (%) SE (%) Mean (%) SE (%) May 67 3.6 33 3.6 1 6.3 0.012 June 64.9 1.3 35.1 1.3 1 45.5 <0.001 July 63.8 0.8 36.2 0.8 1 75.3 <0.001 Aug. 61.5 0.7 38.5 0.7 1 89 <0.001 Sept. 61.3 2.5 38.7 2.5 1 12.1 <0.001 Month Female Male df Chi-square (χ2) P value Mean (%) SE (%) Mean (%) SE (%) May 67 3.6 33 3.6 1 6.3 0.012 June 64.9 1.3 35.1 1.3 1 45.5 <0.001 July 63.8 0.8 36.2 0.8 1 75.3 <0.001 Aug. 61.5 0.7 38.5 0.7 1 89 <0.001 Sept. 61.3 2.5 38.7 2.5 1 12.1 <0.001 View Large Table 4. Results of chi-square tests on the sex ratio of monthly Protoschinia scutosa catches on BH during 2009–2011 and 2013 Month Female Male df Chi-square (χ2) P value Mean (%) SE (%) Mean (%) SE (%) May 67 3.6 33 3.6 1 6.3 0.012 June 64.9 1.3 35.1 1.3 1 45.5 <0.001 July 63.8 0.8 36.2 0.8 1 75.3 <0.001 Aug. 61.5 0.7 38.5 0.7 1 89 <0.001 Sept. 61.3 2.5 38.7 2.5 1 12.1 <0.001 Month Female Male df Chi-square (χ2) P value Mean (%) SE (%) Mean (%) SE (%) May 67 3.6 33 3.6 1 6.3 0.012 June 64.9 1.3 35.1 1.3 1 45.5 <0.001 July 63.8 0.8 36.2 0.8 1 75.3 <0.001 Aug. 61.5 0.7 38.5 0.7 1 89 <0.001 Sept. 61.3 2.5 38.7 2.5 1 12.1 <0.001 View Large Fig. 2. View largeDownload slide Proportions of females (a, b), mated females (c, d), and sexually mature females (e, f) of Protoschinia scutosa captured from May to September during 2009–2011 and 2013. The histograms in (a) and (c) indicate the mean proportion in each month. The histograms in (e) indicate the mean ovarian development level in each month. Vertical bars in (a), (c), and (e), represent the standard errors between years in that month. Open circles in (b), (d), and (f) indicate the center, while the error bars correspond to the upper and lower limits of the 95% CI in the GLMM analysis. Different uppercase letters above each error bar show a significant difference intermonth (P < 0.01) in Fig. 2 (b, d, and f). The estimation was based on a generalized linear mixed-effect Poisson regression (b) and logistic regression (d, f) using raw data of individual moths during 2009–2011 and 2013. Fig. 2. View largeDownload slide Proportions of females (a, b), mated females (c, d), and sexually mature females (e, f) of Protoschinia scutosa captured from May to September during 2009–2011 and 2013. The histograms in (a) and (c) indicate the mean proportion in each month. The histograms in (e) indicate the mean ovarian development level in each month. Vertical bars in (a), (c), and (e), represent the standard errors between years in that month. Open circles in (b), (d), and (f) indicate the center, while the error bars correspond to the upper and lower limits of the 95% CI in the GLMM analysis. Different uppercase letters above each error bar show a significant difference intermonth (P < 0.01) in Fig. 2 (b, d, and f). The estimation was based on a generalized linear mixed-effect Poisson regression (b) and logistic regression (d, f) using raw data of individual moths during 2009–2011 and 2013. In June, most P. scutosa females were mated (Table 5). There was no difference between the proportion of mated versus unmated females in May and July (Table 5). However, in August and September, the vast majority of females were unmated (Table 5). The mean proportion of mated females was significantly different across months (F4, 2198 = 46.8, P < 0.001) but did not differ between years (P = 0.579) and for a month × year interaction (P = 0.283) (Table 2). Overall, the monthly proportion of mated females decreased from May to September (Fig. 2d), and the majority (72.8 ± 4.6%) of mated females had mated once, while 25.3 ± 4.3% of individuals had mated twice (Fig. 3). Table 5. Results of t-tests on the mated ratio of monthly Protoschinia scutosa female catches on BH during 2009–2011 and 2013 Month Mated female Unmated female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 63 19.3 37 19.3 2 0.7 0.555 June 61.1 2.6 38.9 2.6 3 4.2 0.025 July 43.2 4.4 56.8 4.4 3 1.5 0.221 Aug. 9.55 1.5 90.45 1.5 3 17.9 <0.001 Sept. 8.5 3.9 91.5 3.9 3 5.6 0.011 Month Mated female Unmated female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 63 19.3 37 19.3 2 0.7 0.555 June 61.1 2.6 38.9 2.6 3 4.2 0.025 July 43.2 4.4 56.8 4.4 3 1.5 0.221 Aug. 9.55 1.5 90.45 1.5 3 17.9 <0.001 Sept. 8.5 3.9 91.5 3.9 3 5.6 0.011 View Large Table 5. Results of t-tests on the mated ratio of monthly Protoschinia scutosa female catches on BH during 2009–2011 and 2013 Month Mated female Unmated female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 63 19.3 37 19.3 2 0.7 0.555 June 61.1 2.6 38.9 2.6 3 4.2 0.025 July 43.2 4.4 56.8 4.4 3 1.5 0.221 Aug. 9.55 1.5 90.45 1.5 3 17.9 <0.001 Sept. 8.5 3.9 91.5 3.9 3 5.6 0.011 Month Mated female Unmated female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 63 19.3 37 19.3 2 0.7 0.555 June 61.1 2.6 38.9 2.6 3 4.2 0.025 July 43.2 4.4 56.8 4.4 3 1.5 0.221 Aug. 9.55 1.5 90.45 1.5 3 17.9 <0.001 Sept. 8.5 3.9 91.5 3.9 3 5.6 0.011 View Large Fig. 3. View largeDownload slide Proportions of mating occurrences of Protoschinia scutosa females trapped in the halid lamp on BH Island from May to September during 2009–2011 and 2013. Fig. 3. View largeDownload slide Proportions of mating occurrences of Protoschinia scutosa females trapped in the halid lamp on BH Island from May to September during 2009–2011 and 2013. In June, most P. scutosa females were sexually mature individuals (Table 6). In May and July, the proportion of sexually mature and immature individuals did not differ (Table 6). In August and September, the vast majority of females were sexually immature (Table 6). The monthly mean proportion of sexually mature females was significantly different between months (F4, 2198 = 34.2, P < 0.001) but did not differ across years or for a month × year interaction (P = 0.165) (Table 2). Overall, the mean proportion of sexually mature females in trap captures significantly declined from May to September (Fig. 2f). Table 6. Results of t-tests on the mature ratio of monthly Protoschinia scutosa female catches on BH during 2009–2011 and 2013 Month Mature female Immature female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 70.7 12.1 29.3 12.1 2 0.7 0.336 June 69.9 1.5 30.1 1.5 3 4.2 0.003 July 52.6 4.2 47.4 4.2 3 1.5 0.668 Aug. 19.7 1.2 80.3 1.2 3 17.9 0.002 Sept. 9.1 3.4 90.9 3.4 3 5.3 0.013 Month Mature female Immature female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 70.7 12.1 29.3 12.1 2 0.7 0.336 June 69.9 1.5 30.1 1.5 3 4.2 0.003 July 52.6 4.2 47.4 4.2 3 1.5 0.668 Aug. 19.7 1.2 80.3 1.2 3 17.9 0.002 Sept. 9.1 3.4 90.9 3.4 3 5.3 0.013 View Large Table 6. Results of t-tests on the mature ratio of monthly Protoschinia scutosa female catches on BH during 2009–2011 and 2013 Month Mature female Immature female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 70.7 12.1 29.3 12.1 2 0.7 0.336 June 69.9 1.5 30.1 1.5 3 4.2 0.003 July 52.6 4.2 47.4 4.2 3 1.5 0.668 Aug. 19.7 1.2 80.3 1.2 3 17.9 0.002 Sept. 9.1 3.4 90.9 3.4 3 5.3 0.013 Month Mature female Immature female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 70.7 12.1 29.3 12.1 2 0.7 0.336 June 69.9 1.5 30.1 1.5 3 4.2 0.003 July 52.6 4.2 47.4 4.2 3 1.5 0.668 Aug. 19.7 1.2 80.3 1.2 3 17.9 0.002 Sept. 9.1 3.4 90.9 3.4 3 5.3 0.013 View Large Discussion Our work shows how light trapping, field surveys, and ovarian dissection of field-caught individuals provide unambiguous evidence that P. scutosa engages in long-distance migration, in a similar way as other species of Lepidoptera, Odonata, and Coleoptera (Wu et al. 1998, Feng et al. 2003, Feng et al. 2004, Feng et al. 2005, Feng et al. 2006, Wu 2006, Feng et al. 2008, Feng et al. 2009). Migration was likely initiated during times of seasonally favorable, night-time high-altitude tailwinds (Johnson 1969, Dingle 1985). More specifically, East Asian monsoon airflow could be an advantageous carrier for long-distance migration of several insect species including P. scutosa (Drake and Farrow 1988). From May to July, south winds (ESE to WSW) are the prevailing airflow over the Bohai Strait (Zhao et al. 2016), and P. scutosa moths in Hebei or Shandong likely immigrate for new suitable habitats in northeastern China with this prevailing airflow. In late summer and autumn (August–October), northerly winds (WNW to ENE) then become the prevailing airflow (Zhao et al. 2016), permitting offspring of summer populations of P. scutosa to emigrate to the south. Similar migration patterns have been recorded for some noctuids: H. armigera, Heliothis viriplaca (Hufnagel) (Lepidoptera: Noctuidae), Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae), Mythimna separata (Walker) (Lepidoptera: Noctuidae), and Agrotis segetum L. (Lepidoptera: Noctuidae) at the same station.(Feng et al. 2004, Feng et al. 2005, Feng et al. 2008, Feng et al. 2009, Guo et al. 2015, Zhao et al. 2016). The observed seasonal pattern of P. scutosa migration across the Bohai Strait is largely similar to that of windborne migration by potato leafhopper, Empoasca fabae (Harris) (Hemiptera: Cicadellidae), in Central Pennsylvania (Taylor and Reling 1986) and many butterflies and moths of Lepidoptera, such as the Red admiral Vanessa atalanta (L.) (Lepidoptera: Nymphalidae), in Helsinki (Mikkola 2003), Cnaphalocrocis medinalis Guenée (Lepidoptera: Crambidae) in eastern China (Riley et al. 1995), Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae) in China and North America. (Showers 1997), M. separata in Northern China (Feng et al. 2008), H. armigera in Northern China (Feng et al. 2009), and Autographa gamma (L.) (Lepidoptera: Noctuidae) in the United Kingdom (Chapman et al. 2012). These patterns of seasonal migration were all driven by the prevailing airflow between the high and low latitude year round. More specifically, these areas where the insect migration occurred had a relatively steady north–south seasonal air current or monsoon, and the spring migrant populations utilized the southern warm air currents and immigrated to the north for breeding; on the contrary, the autumn offspring populations were relocated to the south for overwintering with the northern air flow. Across sampling events and years, the ratio of females was significantly higher than that of males. This potentially can be ascribed to the superior migratory ability of female moths compared with male individuals (Dingle and Drake 2007) or sex-related differences in phototactic behavior or visual perception ability (Meyer 1978, Dingle and Drake 2007). This pronounced female bias of P. scutosa migratory populations may benefit subsequent colonization ability, particularly when encountering adverse conditions in the novel environment. Hence, further research is warranted into the eventual sex-related differences in flight performance, phototactic behavior, and associated colonization success in P. scutosa. From June to September, the proportion of mated and sexually mature females gradually declined. In the experiment of ovarian dissection, there were only 11 female individuals trapped in the searchlight in May 2013, and due to fewer samples, a larger sampling error was generated. That may explain why the proportion of mated and sexually mature female SCMs showed no difference from the mated and the sexually mature in May. The high rate of mating and ovarian development in summer reveals how P. scutosa migratory behavior is not inhibited by ovarian development, and this species does not exhibit an “oogenesis-flight syndrome” (Johnson 1969, Rankin et al. 1986). Similar patterns were observed in A. segetum (Guo et al. 2015) and H. viriplaca (Zhao et al. 2016). On the contrary, P. scutosa migrants in August and September have a substantially lower mating rate or lower level of ovarian development. Traditional migratory theory considers migratory behavior to be antagonistic to ovarian development, i.e., migratory behavior mostly occurs in younger moths, which consume large amounts of energy for mating and ovarian development (Kennedy 1961, Kisimoto 1976, Riley et al. 1995). The majority of trapped P. scutosa were virgin females with little or no ovarian development from August to September, supporting the idea of the above theory. However, this phenomenon may also be due to the distance between the insect source and the monitoring site is relatively close (about 40–60 km), migratory moth not yet completed development. Some studies have shown that different host plants have a significant effect on reproduction and flight ability on rice leaf roller C. medinalis (Gueneé) (Huang 2014). In spring and early summer, P. scutosa larvae mainly feed on lamb’s quarters, Chenopodium album L. (Caryophyllales: Chenopodiaceae), in the Huang-Huai-Hai Region and then move to soybean in summer and autumn in the Northeast China Region. This shift in food plants may also explain the difference in sexual maturation and mating behavior between P. scutosa spring and summer migrant populations. In addition, environmental cues, such as photoperiod, regulate the interaction between migration and sexual maturation (Chapman et al. 2015). Previous studies have shown that photoperiod has a significant impact on reproduction and flight in M. separata (Walker) (Cao 1997), which can provide another perspective to explain this phenomenon in our study. Therefore, the potential impacts of host diet and photoperiod on flight performance or sexual maturation could be a worthwhile topic of follow-up research. Our work shows a pronounced variability in P. scutosa migration patterns across seasons. Previous research showed that climate change readily affects H. armigera migration in the East Asia monsoon region (Feng et al. 2005) and could equally influence movement patterns of P. scutosa. Furthermore, differing summer and autumn temperatures influence ovarian development, and development rates can be significantly lower in fall than spring seasons (Showers 1997). We believe that comprehensive factors, including environmental cues such as host plant, photoperiod, temperatures, and monsoon in different seasons, collaboratively effect the seasonal migrant pattern of P. scutosa, which will be our next work. In conclusion, our work sheds light upon long-distance migration processes by P. scutosa in Northern China and reveals how this species readily employs the prevailing southerly winds during late spring and early summer to colonize new regions and return south using northerly winds during early autumn. This study constitutes a solid basis for further elucidation of seasonal migration pathways, flight parameters during migration and trajectory analysis. Such work could improve existing P. scutosa monitoring and forecasting systems and help devise IPM strategies for key agricultural crops such as soybean, alfalfa, and sunflower. Acknowledgments We thank Chao Li, Xiaoyang Zhao, Zhenlong Xing, Bingtang Xie, Xiao Wu (Institute of Plant Protection, Chinese Academy of Agricultural Sciences), Kai Xiong, Yu Cui, Congzheng Yuan (the College of Agronomy and Plant Protection, Qingdao Agricultural University), Ning Liu, and Haohao Li (the College of Plant Protection, Henan Agricultural University) for their contributions in field investigations and ovarian dissection. This research was supported by the National Natural Sciences Foundation of China (31727901 and 31621064) and China Agriculture Research System (CARS-15–19). References Cited Abdurakhmanov , G. M. , A. A. Teimurov , A. G. Abdurakhmanov , N. S. Kurbanova , and N. M. Melikova . 2013 . Ecological faunistic and zoogeo-graphical analysis of the fauna of Noctuidae (Lepidoptera, Noctuidae) of the island Nordoviy of the North-Western Caspian Sea . Izv. Samar. Naucn. Centra. Ross. Akad. Nauk . 15 : 435 – 442 . (in Russian) Bradley , J. D . 2000 . 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Seasonal Patterns of Protoschinia scutosa (Lepidoptera: Noctuidae) Migration Across China’s Bohai Strait

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Abstract

Abstract The spotted clover moth, Protoschinia scutosa (Denis & Schiffermüller) (Lepidoptera: Noctuidae), is an important polyphagous pest that is widely distributed in the world. P. scutosa overwinters as pupae in agricultural soils in Northern China. Yet, it is unclear whether P. scutosa also engages in seasonal migration over mid- to long-range distances. In this study, we employ light trapping, field surveys, and ovarian dissection of captured adults over a 2003–2015 time period to assess P. scutosa migration in Northern China. Our work shows that P. scutosa migrates across the Bohai Strait seasonally; the mean duration of its windborne migration period was 121.6 d, and the mean trapping number was 1053.6 moths. Nightly catches of P. scutosa were significantly different between months, but the differences between years were not significant. During 2009–2011 and 2013, the monthly proportion of migrating females (65.5%) was significantly higher than that of males and showed no difference between months. In May to June, the majority of females (May: 63.0%; June: 61.1%) were mated individuals with relatively high level of ovarian development; however, in August and September, most females were unmated. The mean proportion of mated females was significantly different across months but did not differ between years. The results of long-term searchlight trapping and ovarian dissection indicate that P. scutosa exhibits a seasonal characteristic of typical population dynamics and reproductive development of migratory insects. Our work sheds light upon key facets of P. scutosa ecology and facilitates the future development of pest forecasting systems and pest management schemes. spotted clover moth, aerobiology, light trapping, ovarian dissection, trans-regional migration Migration, an important part of many insects’ life history, can facilitate the rapid exploitation of alternative habitat in response to seasonal environmental changes (Dingle 1972, Holland et al. 2006, Chapman et al. 2015). Large biomass of insects migrates within and between continents seasonally, which usually accounts for sudden outbreaks of crop pests and insect-vectored plant diseases (Chapman et al., 2015). A better understanding of the migratory behavior of agricultural pests in particular can constitute the basis for further development of forecasting and early-warning systems or for the deployment of integrated pest management (IPM) strategies (Dingle 1985, Rankin and Burchsted 1992, Irwin 1999, Wu and Guo 2005, Nathan et al. 2008, Dingle 2014). Many insect species were reported as migrants; however, the general pattern of how these species undertake long-distance seasonal migration across different locations or regions is unknown in most cases. And also, the phenomenon that sexually immature individuals were the initiator of emigration contributed to the proposal of “oogenesis-flight syndrome” (Johnson 1969), in which reproductive development and migratory behavior were regarded as two incompatible physiological states. But, the intrinsic relationship between reproduction and migration is not simply an antagonistic relationship in many insect species. The spotted clover moth (SCM), Protoschinia scutosa (Denis & Schiffermüller) (Lepidoptera: Noctuidae), is an occasional pest in agricultural and forage-production systems of Northern China. As a polyphagous herbivore, SCM has been recorded from more than 20 different host plants, including agricultural or fodder crops such as soybean (Glycine max Merrill [Fabales: Leguminosae]) (He 1997), alfalfa (Medicago sativa L. [Fabales: Leguminosae]) (Wang et al. 2011, Zhang et al. 2016), quinoa (Chenopodium quinoa Willd [Caryophyllales: Chenopodiaceae]) (Li et al. 2017), sunflower (Helianthus annuus L. [Asterales: Asteraceae]) (Dekhtiarev 1928), wild wormwood (Artemisia argyi H. Lév. & Vaniot [Asterales: Asteraceae]), and pigweed (Chenopodium serotinum L. [Caryophyllales: Chenopodiaceae]) (Abdurakhmanov et al. 2013). On these plants, P. scutosa larvae feed on seedlings, tender leaves, and stems (He 1997, Skinner 1998, Bradley 2000). The species is widely distributed across the globe and has been reported from Europe, North America, Asia, and North Africa (He 1997, Chen 1999, Bradley 2000, Sokolova 2002, Matov et al. 2008). In China, P. scutosa occurs nationwide and completes 3–6 generations per year depending upon local climatic conditions. In certain areas, SCM overwinters as pupae in soil, while the species sustains continuous populations in southernmost parts of the country (Liu and Zhang 1989, Fan 1990, Xu and Yang 2007). In recent years, the range of occurrence of SCM has expanded and increasing crop damage on several crops in Northern China, such as soybean (He 1997), quinoa (Li et al. 2017), and alfalfa (Zhang et al. 2016). P. scutosa and the cotton bollworm, Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae), possess similar morphology, life history, dietary host range, and geographical distribution (Wang 1981). For H. armigera, its wide distribution and pest status in several crops are mainly due to its omnivorous feeding and behavior strategies, facultative diapauses, and seasonal migration (Fitt 1989, Feng et al. 2005, Feng et al. 2009). More specifically, H. armigera overwintering generations migrate in early spring from the Yellow River Valley into northeastern China, where they feed on spring maize and soybeans (Feng et al. 2009). In autumn, large numbers of H. armigera then migrate back from northeastern China (Feng et al. 2005). Diapause and migration are two different strategies to adapt to environmental changes (Dingle 2014). Previous research suggests SCM might be a migratory species (Oku 1978); however, the seasonal patterns of migrant species exhibits in Northern China remain unclear. Considering the climate-induced poleward expansion of many insect species (Robertson 2009, Pateman et al. 2012) and the increasing pest status of P. scutosa in Northern China, it is critical to gain further insights into migration patterns of this species. In this study, we rely upon light trapping and ovarian dissection of field-caught individuals to assess P. scutosa migration over 13 consecutive years on Beihuang Island (BH), at the center of the Bohai Strait in Northern China. This work not only provides critical insights into P. scutosa life history and ecology but also is important for the further development of pest forecasting systems and pest management strategies. Materials and Methods Study Site All research was conducted at the field experimental station of the Chinese Academy of Agricultural Sciences (CAAS) on BH (38º24′ N; 120º55′ E), Shandong province, China. BH has a land area of 2.5 km2 and located in the center of the Bohai Strait, approximately 40 km from Liaodong Peninsula and 60 km from Jiaodong Peninsula (Zhao et al. 2016). Light Trapping and Field Observation Light trapping was conducted from April to October during 2003–2015 on BH. The trapping device was adapted to sample insects flying at high altitude and was equipped with a 1,000 W metal halide lamp (model JLZ1000BT; Shanghai Yaming Lighting Co. Ltd., Shanghai, China), mounted on a platform approximately 8 m above sea level (asl). The device emitted a beam of light with a 105,000 lm, a color temperature of 4,000 K, and a color rendering index of 65 to attract moths migrating overhead at altitudes up to 500 m above the ground level (Feng et al. 2009; Fu et al. 2014a, b). To collect insects, a nylon net bag (60 mesh) was placed beneath the trap and changed every 2 h throughout the night. The lamp was turned on at sunset and solely operated at night and was used on a daily basis from April to October 2003–2015. Incomplete data sets caused by extreme weather conditions (e.g., heavy rains, typhoon, thunderstorm) or long-term power outages were excluded from the analysis. For nights during which trapping proceeded normally, but no P. scutosa was caught, a “zero” was entered in the dataset. Trapped insects were stored at −20°C for at least 4 h prior to laboratory processing and ovarian dissection. The island has no farmland, and none of the main host plant of P. scutosa is present, but potential host plants, such as graminaceous weeds, mulberry (Morus alba L.), and some pine trees, still exist. To ascertain whether there is a local population of P. scutosa on these plants, field investigations for larvae and pupae were conducted from April to October in 2003–2015. Ovarian Dissection To test the hypothesis of “oogenesis-flight syndrome” for P. scutosa migratory population, we select a subsample of maximum 20 females randomly during each night in 2009–2011 and 2013. Under a stereomicroscope (model JNOEC-Jsz4; Motic China Group Co. Ltd., Xiamen, China), we dissected the subsample and estimated the level of ovarian development (from 1 to 5) using criteria of H. armigera (Zhang and Mou 1994). These data were used to generate an average monthly level of ovarian development (i.e., the sum of individual levels of ovarian development divided by the number of females dissected in a month. Females with ovarian development levels 1–2 were regarded as “sexually immature” individuals, while those with levels 3–5 were regarded as “sexually mature” individuals (Zhang et al. 1979, Shi 1984, Li et al. 1987). Moreover, mating occurrence and frequency of P. scutosa were determined by assessing the presence and number of spermatophores in female’s spermatheca (Zhang et al. 1979). We calculated the proportion of mated females monthly and regarded the average of daily reproductive in that month as a monthly value. Data Analysis Differences in the daily P. scutosa captures and monthly records of sex ratio, sexually mature female proportion, and mated ratio were analyzed using generalized linear mixed models (GLMM), in which the month was a fixed effect and the year was a random effect. Monthly sex ratios (female: male) were compared using a chi-square test (PROC FREQ). Differences in the mean proportions of mated females and between sexually mature and immature females in each month were assessed with t-tests (PROC TTEST, the proportion data were arcsine square root transformed). Total annual catches of P. scutosa were analyzed by hierarchical cluster analysis, using the “Nearest-neighbor method” based on Euclidean distances (Zhang et al. 2015). The generalized linear mixed-effect regressions and hierarchical cluster analysis were statistically processed using SPSS version 20 (IBM Corp, New York, NY, 2011) and Data Processing System (DPS) version 9.5 (Tang 2013), respectively. Other statistical analyses were performed by SAS version 9.2 (SAS Institute, Cary, NC, 2001). Results Temporal Migration Pattern During field surveys on BH Island, no P. scutosa larvae were found. However, SCM was regularly captured in the halid lamp (Table 1, Fig. 1), with daily number of catches significantly different between months (F6, 2051 = 17951.1, P < 0.001) and with a significant month × year interaction (P < 0.001) (Table 2). However, the variation between years (P = 0.181) was not significant (Table 2). Table 1. Overall introduction of Protoschinia scutosa moths caught in the light trapping on BH during 2003–2015 Year Date of first capture (n)* Date of final capture (n)* Duration (d) Date of peak catches (n)* Total catches 2003 19 July (5) 27 Aug. (6) 40 25 Aug. (1224) 1,291 2004 15 May (1) 13 Sept. (2) 122 25 Aug. (29) 1,27 2005 20 May (1) 14 Sept. (6) 118 29 July (229) 1,146 2006 17 May (2) 29 Sept. (1) 136 1 Aug. (165) 1,195 2007 19 May (3) 13 Sept. (2) 135 31 May (40) 677 2008 15 May (1) 28 Sept. (1) 142 14 Aug. (200) 1,501 2009 13 May (1) 17 Sept. (1) 139 26 May (196) 1,767 2010 5 June (1) 13 Sept. (1) 101 9 Aug. (213) 1,194 2011 23 May (3) 9 Sept. (1) 110 2 Sept. (52) 603 2012 6 May (1) 13 Sept. (1) 131 20 Aug. (297) 1,208 2013 7 May (1) 14 Sept. (25) 131 6 Aug. (48) 875 2014 2 May (1) 20 Sept. (1) 153 9 Aug. (72) 1,074 2015 9 May (1) 8 Sept. (2) 123 14 July (88) 1,039 Mean – – 121.6 – 1053.6 SE – – 7.8 – 115.3 Year Date of first capture (n)* Date of final capture (n)* Duration (d) Date of peak catches (n)* Total catches 2003 19 July (5) 27 Aug. (6) 40 25 Aug. (1224) 1,291 2004 15 May (1) 13 Sept. (2) 122 25 Aug. (29) 1,27 2005 20 May (1) 14 Sept. (6) 118 29 July (229) 1,146 2006 17 May (2) 29 Sept. (1) 136 1 Aug. (165) 1,195 2007 19 May (3) 13 Sept. (2) 135 31 May (40) 677 2008 15 May (1) 28 Sept. (1) 142 14 Aug. (200) 1,501 2009 13 May (1) 17 Sept. (1) 139 26 May (196) 1,767 2010 5 June (1) 13 Sept. (1) 101 9 Aug. (213) 1,194 2011 23 May (3) 9 Sept. (1) 110 2 Sept. (52) 603 2012 6 May (1) 13 Sept. (1) 131 20 Aug. (297) 1,208 2013 7 May (1) 14 Sept. (25) 131 6 Aug. (48) 875 2014 2 May (1) 20 Sept. (1) 153 9 Aug. (72) 1,074 2015 9 May (1) 8 Sept. (2) 123 14 July (88) 1,039 Mean – – 121.6 – 1053.6 SE – – 7.8 – 115.3 *The numbers of P. scutosa moths captured on the indicated dates are provided in parentheses. View Large Table 1. Overall introduction of Protoschinia scutosa moths caught in the light trapping on BH during 2003–2015 Year Date of first capture (n)* Date of final capture (n)* Duration (d) Date of peak catches (n)* Total catches 2003 19 July (5) 27 Aug. (6) 40 25 Aug. (1224) 1,291 2004 15 May (1) 13 Sept. (2) 122 25 Aug. (29) 1,27 2005 20 May (1) 14 Sept. (6) 118 29 July (229) 1,146 2006 17 May (2) 29 Sept. (1) 136 1 Aug. (165) 1,195 2007 19 May (3) 13 Sept. (2) 135 31 May (40) 677 2008 15 May (1) 28 Sept. (1) 142 14 Aug. (200) 1,501 2009 13 May (1) 17 Sept. (1) 139 26 May (196) 1,767 2010 5 June (1) 13 Sept. (1) 101 9 Aug. (213) 1,194 2011 23 May (3) 9 Sept. (1) 110 2 Sept. (52) 603 2012 6 May (1) 13 Sept. (1) 131 20 Aug. (297) 1,208 2013 7 May (1) 14 Sept. (25) 131 6 Aug. (48) 875 2014 2 May (1) 20 Sept. (1) 153 9 Aug. (72) 1,074 2015 9 May (1) 8 Sept. (2) 123 14 July (88) 1,039 Mean – – 121.6 – 1053.6 SE – – 7.8 – 115.3 Year Date of first capture (n)* Date of final capture (n)* Duration (d) Date of peak catches (n)* Total catches 2003 19 July (5) 27 Aug. (6) 40 25 Aug. (1224) 1,291 2004 15 May (1) 13 Sept. (2) 122 25 Aug. (29) 1,27 2005 20 May (1) 14 Sept. (6) 118 29 July (229) 1,146 2006 17 May (2) 29 Sept. (1) 136 1 Aug. (165) 1,195 2007 19 May (3) 13 Sept. (2) 135 31 May (40) 677 2008 15 May (1) 28 Sept. (1) 142 14 Aug. (200) 1,501 2009 13 May (1) 17 Sept. (1) 139 26 May (196) 1,767 2010 5 June (1) 13 Sept. (1) 101 9 Aug. (213) 1,194 2011 23 May (3) 9 Sept. (1) 110 2 Sept. (52) 603 2012 6 May (1) 13 Sept. (1) 131 20 Aug. (297) 1,208 2013 7 May (1) 14 Sept. (25) 131 6 Aug. (48) 875 2014 2 May (1) 20 Sept. (1) 153 9 Aug. (72) 1,074 2015 9 May (1) 8 Sept. (2) 123 14 July (88) 1,039 Mean – – 121.6 – 1053.6 SE – – 7.8 – 115.3 *The numbers of P. scutosa moths captured on the indicated dates are provided in parentheses. View Large Table 2. Summary of analysis of GLMM on catches, female captures, mated female catches, and mature female catches of Protoschinia scutosa moths on BH Island from April to October during 2003–2015 Target variable Main results of GLMM analysis Moth catches Fixed effect Factor F df1 df2 P value Month 17951.1 6 2051 <0.001 Random effect Factor Variance SE Z P value Year 0.2 0.2 1.3 0.181 Month×Year 0.8 0.2 4.2 <0.001 Female catches Fixed effect Factor F df1 df2 P value Month 1.3 4 4434 0.146 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.9 0.346 Month×Year 0a Mated female catches Fixed effect Factor F df1 df2 P value Month 46.8 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.6 0.579 Month×Year 0.1 0.1 1.1 0.283 Mature female catches Fixed effect Factor F df1 df2 P value Month 34.2 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0a Month×Year 0.1 0.1 1.4 0.165 Target variable Main results of GLMM analysis Moth catches Fixed effect Factor F df1 df2 P value Month 17951.1 6 2051 <0.001 Random effect Factor Variance SE Z P value Year 0.2 0.2 1.3 0.181 Month×Year 0.8 0.2 4.2 <0.001 Female catches Fixed effect Factor F df1 df2 P value Month 1.3 4 4434 0.146 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.9 0.346 Month×Year 0a Mated female catches Fixed effect Factor F df1 df2 P value Month 46.8 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.6 0.579 Month×Year 0.1 0.1 1.1 0.283 Mature female catches Fixed effect Factor F df1 df2 P value Month 34.2 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0a Month×Year 0.1 0.1 1.4 0.165 Moth catches of P. scutosa was subject to a Poisson distribution with Poisson regression as link function, and other target variables were subject to a binomial distribution with logistic regression as link function in the analysis of GLMM. LB and UB: lower and upper bound of the 95% CI. a: Redundant parameter. View Large Table 2. Summary of analysis of GLMM on catches, female captures, mated female catches, and mature female catches of Protoschinia scutosa moths on BH Island from April to October during 2003–2015 Target variable Main results of GLMM analysis Moth catches Fixed effect Factor F df1 df2 P value Month 17951.1 6 2051 <0.001 Random effect Factor Variance SE Z P value Year 0.2 0.2 1.3 0.181 Month×Year 0.8 0.2 4.2 <0.001 Female catches Fixed effect Factor F df1 df2 P value Month 1.3 4 4434 0.146 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.9 0.346 Month×Year 0a Mated female catches Fixed effect Factor F df1 df2 P value Month 46.8 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.6 0.579 Month×Year 0.1 0.1 1.1 0.283 Mature female catches Fixed effect Factor F df1 df2 P value Month 34.2 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0a Month×Year 0.1 0.1 1.4 0.165 Target variable Main results of GLMM analysis Moth catches Fixed effect Factor F df1 df2 P value Month 17951.1 6 2051 <0.001 Random effect Factor Variance SE Z P value Year 0.2 0.2 1.3 0.181 Month×Year 0.8 0.2 4.2 <0.001 Female catches Fixed effect Factor F df1 df2 P value Month 1.3 4 4434 0.146 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.9 0.346 Month×Year 0a Mated female catches Fixed effect Factor F df1 df2 P value Month 46.8 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0.0 0.0 0.6 0.579 Month×Year 0.1 0.1 1.1 0.283 Mature female catches Fixed effect Factor F df1 df2 P value Month 34.2 4 2198 <0.001 Random effect Factor Variance SE Z P value Year 0a Month×Year 0.1 0.1 1.4 0.165 Moth catches of P. scutosa was subject to a Poisson distribution with Poisson regression as link function, and other target variables were subject to a binomial distribution with logistic regression as link function in the analysis of GLMM. LB and UB: lower and upper bound of the 95% CI. a: Redundant parameter. View Large Fig. 1. View largeDownload slide Nightly catches of each year (A) and annual mean logarithm of nightly catches (B) of Protoschinia scutosa moths in the light trap on BH Island from April to September during 2003–2015. Fig. 1. View largeDownload slide Nightly catches of each year (A) and annual mean logarithm of nightly catches (B) of Protoschinia scutosa moths in the light trap on BH Island from April to September during 2003–2015. The average number of moths captured annually in the halid lamp was 1053.6 ± 115.3 during 2003–2015. The cluster analysis indicated that total annual SCM captures could broadly be divided into five groups (Table 3). The largest migration occurred in 2009 with 1767 catches; the mass migration appeared in 2008; the normal migration appeared in 2003, 2005, 2006, 2010, and 2012–2015; the weak migration occurred in 2007 and 2011; the rare migration occurred in 2004 with a total catches of 127 individuals. Table 3. Hierarchical clustering analysis of group on the annual number of Protoschinia scutosa captured in a light trap on BH Island during 2003–2015 Group Year Observed value (total capture per year) Distance to the center Group mean Root mean square deviation First group 2004 127 0.0 127 – Second group 2003 1,291 163.3 1127.8 57.8 2005 1,146 18.3 2006 1,195 67.3 2010 1,194 66.3 2012 1,208 80.3 2013 875 252.8 2014 1,074 53.8 2015 1,039 88.8 Third group 2007 677 37.0 640 23.4 2011 603 37.0 Fourth group 2008 1,501 0.0 1,501 – Fifth group 2009 1,767 0.0 1,767 – R2 0.9 Pseudo F 32.6 P <0.001 Group Year Observed value (total capture per year) Distance to the center Group mean Root mean square deviation First group 2004 127 0.0 127 – Second group 2003 1,291 163.3 1127.8 57.8 2005 1,146 18.3 2006 1,195 67.3 2010 1,194 66.3 2012 1,208 80.3 2013 875 252.8 2014 1,074 53.8 2015 1,039 88.8 Third group 2007 677 37.0 640 23.4 2011 603 37.0 Fourth group 2008 1,501 0.0 1,501 – Fifth group 2009 1,767 0.0 1,767 – R2 0.9 Pseudo F 32.6 P <0.001 View Large Table 3. Hierarchical clustering analysis of group on the annual number of Protoschinia scutosa captured in a light trap on BH Island during 2003–2015 Group Year Observed value (total capture per year) Distance to the center Group mean Root mean square deviation First group 2004 127 0.0 127 – Second group 2003 1,291 163.3 1127.8 57.8 2005 1,146 18.3 2006 1,195 67.3 2010 1,194 66.3 2012 1,208 80.3 2013 875 252.8 2014 1,074 53.8 2015 1,039 88.8 Third group 2007 677 37.0 640 23.4 2011 603 37.0 Fourth group 2008 1,501 0.0 1,501 – Fifth group 2009 1,767 0.0 1,767 – R2 0.9 Pseudo F 32.6 P <0.001 Group Year Observed value (total capture per year) Distance to the center Group mean Root mean square deviation First group 2004 127 0.0 127 – Second group 2003 1,291 163.3 1127.8 57.8 2005 1,146 18.3 2006 1,195 67.3 2010 1,194 66.3 2012 1,208 80.3 2013 875 252.8 2014 1,074 53.8 2015 1,039 88.8 Third group 2007 677 37.0 640 23.4 2011 603 37.0 Fourth group 2008 1,501 0.0 1,501 – Fifth group 2009 1,767 0.0 1,767 – R2 0.9 Pseudo F 32.6 P <0.001 View Large A pronounced seasonal pattern was evident in SCM captures, with the mean migration period being 121.6 ± 7.8 d (ranging from 40 to 153 d,). The first capture of SCM in a year generally occurred in mid-May. Subsequently, SCM was trapped intermittently with mean captures 95.9 ± 22.9 individuals from May to June. Trap catches increased in mid-July and continued through mid-August to then gradually decrease to zero by mid-September (Fig. 1, Table 1). Seasonal Sex Ratio and Mating Patterns During 2009–2011 and 2013, the proportion of females in total trap captures was significantly greater than that of males (Table 4; Fig. 2a and b). The monthly proportion of migrating females (65.5 ± 2.5%) was significantly higher than that of males (Table 4), and average monthly trapping amount of females did not differ between months (F4, 4434 = 1.3, P = 0.146) and years (P = 0.346) (Table 2.). Table 4. Results of chi-square tests on the sex ratio of monthly Protoschinia scutosa catches on BH during 2009–2011 and 2013 Month Female Male df Chi-square (χ2) P value Mean (%) SE (%) Mean (%) SE (%) May 67 3.6 33 3.6 1 6.3 0.012 June 64.9 1.3 35.1 1.3 1 45.5 <0.001 July 63.8 0.8 36.2 0.8 1 75.3 <0.001 Aug. 61.5 0.7 38.5 0.7 1 89 <0.001 Sept. 61.3 2.5 38.7 2.5 1 12.1 <0.001 Month Female Male df Chi-square (χ2) P value Mean (%) SE (%) Mean (%) SE (%) May 67 3.6 33 3.6 1 6.3 0.012 June 64.9 1.3 35.1 1.3 1 45.5 <0.001 July 63.8 0.8 36.2 0.8 1 75.3 <0.001 Aug. 61.5 0.7 38.5 0.7 1 89 <0.001 Sept. 61.3 2.5 38.7 2.5 1 12.1 <0.001 View Large Table 4. Results of chi-square tests on the sex ratio of monthly Protoschinia scutosa catches on BH during 2009–2011 and 2013 Month Female Male df Chi-square (χ2) P value Mean (%) SE (%) Mean (%) SE (%) May 67 3.6 33 3.6 1 6.3 0.012 June 64.9 1.3 35.1 1.3 1 45.5 <0.001 July 63.8 0.8 36.2 0.8 1 75.3 <0.001 Aug. 61.5 0.7 38.5 0.7 1 89 <0.001 Sept. 61.3 2.5 38.7 2.5 1 12.1 <0.001 Month Female Male df Chi-square (χ2) P value Mean (%) SE (%) Mean (%) SE (%) May 67 3.6 33 3.6 1 6.3 0.012 June 64.9 1.3 35.1 1.3 1 45.5 <0.001 July 63.8 0.8 36.2 0.8 1 75.3 <0.001 Aug. 61.5 0.7 38.5 0.7 1 89 <0.001 Sept. 61.3 2.5 38.7 2.5 1 12.1 <0.001 View Large Fig. 2. View largeDownload slide Proportions of females (a, b), mated females (c, d), and sexually mature females (e, f) of Protoschinia scutosa captured from May to September during 2009–2011 and 2013. The histograms in (a) and (c) indicate the mean proportion in each month. The histograms in (e) indicate the mean ovarian development level in each month. Vertical bars in (a), (c), and (e), represent the standard errors between years in that month. Open circles in (b), (d), and (f) indicate the center, while the error bars correspond to the upper and lower limits of the 95% CI in the GLMM analysis. Different uppercase letters above each error bar show a significant difference intermonth (P < 0.01) in Fig. 2 (b, d, and f). The estimation was based on a generalized linear mixed-effect Poisson regression (b) and logistic regression (d, f) using raw data of individual moths during 2009–2011 and 2013. Fig. 2. View largeDownload slide Proportions of females (a, b), mated females (c, d), and sexually mature females (e, f) of Protoschinia scutosa captured from May to September during 2009–2011 and 2013. The histograms in (a) and (c) indicate the mean proportion in each month. The histograms in (e) indicate the mean ovarian development level in each month. Vertical bars in (a), (c), and (e), represent the standard errors between years in that month. Open circles in (b), (d), and (f) indicate the center, while the error bars correspond to the upper and lower limits of the 95% CI in the GLMM analysis. Different uppercase letters above each error bar show a significant difference intermonth (P < 0.01) in Fig. 2 (b, d, and f). The estimation was based on a generalized linear mixed-effect Poisson regression (b) and logistic regression (d, f) using raw data of individual moths during 2009–2011 and 2013. In June, most P. scutosa females were mated (Table 5). There was no difference between the proportion of mated versus unmated females in May and July (Table 5). However, in August and September, the vast majority of females were unmated (Table 5). The mean proportion of mated females was significantly different across months (F4, 2198 = 46.8, P < 0.001) but did not differ between years (P = 0.579) and for a month × year interaction (P = 0.283) (Table 2). Overall, the monthly proportion of mated females decreased from May to September (Fig. 2d), and the majority (72.8 ± 4.6%) of mated females had mated once, while 25.3 ± 4.3% of individuals had mated twice (Fig. 3). Table 5. Results of t-tests on the mated ratio of monthly Protoschinia scutosa female catches on BH during 2009–2011 and 2013 Month Mated female Unmated female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 63 19.3 37 19.3 2 0.7 0.555 June 61.1 2.6 38.9 2.6 3 4.2 0.025 July 43.2 4.4 56.8 4.4 3 1.5 0.221 Aug. 9.55 1.5 90.45 1.5 3 17.9 <0.001 Sept. 8.5 3.9 91.5 3.9 3 5.6 0.011 Month Mated female Unmated female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 63 19.3 37 19.3 2 0.7 0.555 June 61.1 2.6 38.9 2.6 3 4.2 0.025 July 43.2 4.4 56.8 4.4 3 1.5 0.221 Aug. 9.55 1.5 90.45 1.5 3 17.9 <0.001 Sept. 8.5 3.9 91.5 3.9 3 5.6 0.011 View Large Table 5. Results of t-tests on the mated ratio of monthly Protoschinia scutosa female catches on BH during 2009–2011 and 2013 Month Mated female Unmated female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 63 19.3 37 19.3 2 0.7 0.555 June 61.1 2.6 38.9 2.6 3 4.2 0.025 July 43.2 4.4 56.8 4.4 3 1.5 0.221 Aug. 9.55 1.5 90.45 1.5 3 17.9 <0.001 Sept. 8.5 3.9 91.5 3.9 3 5.6 0.011 Month Mated female Unmated female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 63 19.3 37 19.3 2 0.7 0.555 June 61.1 2.6 38.9 2.6 3 4.2 0.025 July 43.2 4.4 56.8 4.4 3 1.5 0.221 Aug. 9.55 1.5 90.45 1.5 3 17.9 <0.001 Sept. 8.5 3.9 91.5 3.9 3 5.6 0.011 View Large Fig. 3. View largeDownload slide Proportions of mating occurrences of Protoschinia scutosa females trapped in the halid lamp on BH Island from May to September during 2009–2011 and 2013. Fig. 3. View largeDownload slide Proportions of mating occurrences of Protoschinia scutosa females trapped in the halid lamp on BH Island from May to September during 2009–2011 and 2013. In June, most P. scutosa females were sexually mature individuals (Table 6). In May and July, the proportion of sexually mature and immature individuals did not differ (Table 6). In August and September, the vast majority of females were sexually immature (Table 6). The monthly mean proportion of sexually mature females was significantly different between months (F4, 2198 = 34.2, P < 0.001) but did not differ across years or for a month × year interaction (P = 0.165) (Table 2). Overall, the mean proportion of sexually mature females in trap captures significantly declined from May to September (Fig. 2f). Table 6. Results of t-tests on the mature ratio of monthly Protoschinia scutosa female catches on BH during 2009–2011 and 2013 Month Mature female Immature female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 70.7 12.1 29.3 12.1 2 0.7 0.336 June 69.9 1.5 30.1 1.5 3 4.2 0.003 July 52.6 4.2 47.4 4.2 3 1.5 0.668 Aug. 19.7 1.2 80.3 1.2 3 17.9 0.002 Sept. 9.1 3.4 90.9 3.4 3 5.3 0.013 Month Mature female Immature female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 70.7 12.1 29.3 12.1 2 0.7 0.336 June 69.9 1.5 30.1 1.5 3 4.2 0.003 July 52.6 4.2 47.4 4.2 3 1.5 0.668 Aug. 19.7 1.2 80.3 1.2 3 17.9 0.002 Sept. 9.1 3.4 90.9 3.4 3 5.3 0.013 View Large Table 6. Results of t-tests on the mature ratio of monthly Protoschinia scutosa female catches on BH during 2009–2011 and 2013 Month Mature female Immature female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 70.7 12.1 29.3 12.1 2 0.7 0.336 June 69.9 1.5 30.1 1.5 3 4.2 0.003 July 52.6 4.2 47.4 4.2 3 1.5 0.668 Aug. 19.7 1.2 80.3 1.2 3 17.9 0.002 Sept. 9.1 3.4 90.9 3.4 3 5.3 0.013 Month Mature female Immature female df t-value P value Mean (%) SE (%) Mean (%) SE (%) May 70.7 12.1 29.3 12.1 2 0.7 0.336 June 69.9 1.5 30.1 1.5 3 4.2 0.003 July 52.6 4.2 47.4 4.2 3 1.5 0.668 Aug. 19.7 1.2 80.3 1.2 3 17.9 0.002 Sept. 9.1 3.4 90.9 3.4 3 5.3 0.013 View Large Discussion Our work shows how light trapping, field surveys, and ovarian dissection of field-caught individuals provide unambiguous evidence that P. scutosa engages in long-distance migration, in a similar way as other species of Lepidoptera, Odonata, and Coleoptera (Wu et al. 1998, Feng et al. 2003, Feng et al. 2004, Feng et al. 2005, Feng et al. 2006, Wu 2006, Feng et al. 2008, Feng et al. 2009). Migration was likely initiated during times of seasonally favorable, night-time high-altitude tailwinds (Johnson 1969, Dingle 1985). More specifically, East Asian monsoon airflow could be an advantageous carrier for long-distance migration of several insect species including P. scutosa (Drake and Farrow 1988). From May to July, south winds (ESE to WSW) are the prevailing airflow over the Bohai Strait (Zhao et al. 2016), and P. scutosa moths in Hebei or Shandong likely immigrate for new suitable habitats in northeastern China with this prevailing airflow. In late summer and autumn (August–October), northerly winds (WNW to ENE) then become the prevailing airflow (Zhao et al. 2016), permitting offspring of summer populations of P. scutosa to emigrate to the south. Similar migration patterns have been recorded for some noctuids: H. armigera, Heliothis viriplaca (Hufnagel) (Lepidoptera: Noctuidae), Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae), Mythimna separata (Walker) (Lepidoptera: Noctuidae), and Agrotis segetum L. (Lepidoptera: Noctuidae) at the same station.(Feng et al. 2004, Feng et al. 2005, Feng et al. 2008, Feng et al. 2009, Guo et al. 2015, Zhao et al. 2016). The observed seasonal pattern of P. scutosa migration across the Bohai Strait is largely similar to that of windborne migration by potato leafhopper, Empoasca fabae (Harris) (Hemiptera: Cicadellidae), in Central Pennsylvania (Taylor and Reling 1986) and many butterflies and moths of Lepidoptera, such as the Red admiral Vanessa atalanta (L.) (Lepidoptera: Nymphalidae), in Helsinki (Mikkola 2003), Cnaphalocrocis medinalis Guenée (Lepidoptera: Crambidae) in eastern China (Riley et al. 1995), Agrotis ipsilon (Hufnagel) (Lepidoptera: Noctuidae) in China and North America. (Showers 1997), M. separata in Northern China (Feng et al. 2008), H. armigera in Northern China (Feng et al. 2009), and Autographa gamma (L.) (Lepidoptera: Noctuidae) in the United Kingdom (Chapman et al. 2012). These patterns of seasonal migration were all driven by the prevailing airflow between the high and low latitude year round. More specifically, these areas where the insect migration occurred had a relatively steady north–south seasonal air current or monsoon, and the spring migrant populations utilized the southern warm air currents and immigrated to the north for breeding; on the contrary, the autumn offspring populations were relocated to the south for overwintering with the northern air flow. Across sampling events and years, the ratio of females was significantly higher than that of males. This potentially can be ascribed to the superior migratory ability of female moths compared with male individuals (Dingle and Drake 2007) or sex-related differences in phototactic behavior or visual perception ability (Meyer 1978, Dingle and Drake 2007). This pronounced female bias of P. scutosa migratory populations may benefit subsequent colonization ability, particularly when encountering adverse conditions in the novel environment. Hence, further research is warranted into the eventual sex-related differences in flight performance, phototactic behavior, and associated colonization success in P. scutosa. From June to September, the proportion of mated and sexually mature females gradually declined. In the experiment of ovarian dissection, there were only 11 female individuals trapped in the searchlight in May 2013, and due to fewer samples, a larger sampling error was generated. That may explain why the proportion of mated and sexually mature female SCMs showed no difference from the mated and the sexually mature in May. The high rate of mating and ovarian development in summer reveals how P. scutosa migratory behavior is not inhibited by ovarian development, and this species does not exhibit an “oogenesis-flight syndrome” (Johnson 1969, Rankin et al. 1986). Similar patterns were observed in A. segetum (Guo et al. 2015) and H. viriplaca (Zhao et al. 2016). On the contrary, P. scutosa migrants in August and September have a substantially lower mating rate or lower level of ovarian development. Traditional migratory theory considers migratory behavior to be antagonistic to ovarian development, i.e., migratory behavior mostly occurs in younger moths, which consume large amounts of energy for mating and ovarian development (Kennedy 1961, Kisimoto 1976, Riley et al. 1995). The majority of trapped P. scutosa were virgin females with little or no ovarian development from August to September, supporting the idea of the above theory. However, this phenomenon may also be due to the distance between the insect source and the monitoring site is relatively close (about 40–60 km), migratory moth not yet completed development. Some studies have shown that different host plants have a significant effect on reproduction and flight ability on rice leaf roller C. medinalis (Gueneé) (Huang 2014). In spring and early summer, P. scutosa larvae mainly feed on lamb’s quarters, Chenopodium album L. (Caryophyllales: Chenopodiaceae), in the Huang-Huai-Hai Region and then move to soybean in summer and autumn in the Northeast China Region. This shift in food plants may also explain the difference in sexual maturation and mating behavior between P. scutosa spring and summer migrant populations. In addition, environmental cues, such as photoperiod, regulate the interaction between migration and sexual maturation (Chapman et al. 2015). Previous studies have shown that photoperiod has a significant impact on reproduction and flight in M. separata (Walker) (Cao 1997), which can provide another perspective to explain this phenomenon in our study. Therefore, the potential impacts of host diet and photoperiod on flight performance or sexual maturation could be a worthwhile topic of follow-up research. Our work shows a pronounced variability in P. scutosa migration patterns across seasons. Previous research showed that climate change readily affects H. armigera migration in the East Asia monsoon region (Feng et al. 2005) and could equally influence movement patterns of P. scutosa. Furthermore, differing summer and autumn temperatures influence ovarian development, and development rates can be significantly lower in fall than spring seasons (Showers 1997). We believe that comprehensive factors, including environmental cues such as host plant, photoperiod, temperatures, and monsoon in different seasons, collaboratively effect the seasonal migrant pattern of P. scutosa, which will be our next work. In conclusion, our work sheds light upon long-distance migration processes by P. scutosa in Northern China and reveals how this species readily employs the prevailing southerly winds during late spring and early summer to colonize new regions and return south using northerly winds during early autumn. This study constitutes a solid basis for further elucidation of seasonal migration pathways, flight parameters during migration and trajectory analysis. Such work could improve existing P. scutosa monitoring and forecasting systems and help devise IPM strategies for key agricultural crops such as soybean, alfalfa, and sunflower. 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Google Scholar CrossRef Search ADS PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)

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