Introduction

Sugarcane thrips, Fulmekiola serrata (Kobus) (Thysanoptera: Terebrantia), is a common leaf pest on sugarcane1,2. F. serrata is native to eastern Asia and was first described in sugarcane in Java, and has spread to Africa, North America, and South America3,4. It occurs in Yunnan, Guangxi, Guangdong, Hainan, Fujian, Taiwan, Guizhou, Sichuan, Hunan, Jiangsu, Zhejiang, and other provinces and regions in China5. In recent years, the process of global economic integration has accelerated, the abnormal change of climate has intensified, the adjustment of the sugarcane industry has accelerated, the sugarcane production mode has changed, the adaptability and harmfulness of pests have increased, and F. serrata has risen from its previous status as a secondary pest to its current status as a major pest. Its area of occurrence is expanding, the frequency of damage is increasing, and the degree of disaster is aggravating, causing great losses to sugarcane production and seriously threatening the sustainable, stable, and healthy development of the sugarcane industry6. According to a previous survey, damage from F. serrata in South Africa could reduce sugarcane yields by a range of 18.0% to 26.8% and sucrose production by a range of 16.2% to 24.0%7. In Yunnan, the yield and sugar losses of more-resistant varieties range from 13.04% to 21.06% and 8.33% to 8.40%, respectively, whereas those of less-resistant varieties have reached 40.58% and 8.44%8.

Overwintering is an important biological habit of thrips. The overwintering generation of thrips plays an important role in thrips development, directly affecting the occurrence period and frequency and degree of damage the following year9. Some scholars have conducted extensive studies on the overwintering of many thrips species with different hosts in different regions. In New York, Thrips tabaci Lindeman adults overwinter in winter wheat, alfalfa, and weedy vegetation, overwintering females lay eggs in the spring, and winter wheat, oats, and alfalfa are the best oviposition and reproduction hosts10. They also overwinter in the soil within and near onion fields, and volunteer onions and weeds are the best hosts for onion thrips after onion harvesting11. On Jeju Island, Korea, Thrips palmi Karny overwinters as adults, with a sex ratio of at least 98.8% females, and Stellaria media ViII. and Artemisia princeps Pampan. are important overwintering hosts12. In central England, western flower thrips, Frankliniella occidentalis (Pergande), overwinters as females, breed on several crop weeds that often flower throughout the year, including common chickweed (Stellaria media (L.) Vill.), groundsel (Senecio vulgaris L.) and dandelion (Taraxacum officinale L.), and when overwintering, contribute to the accumulation of thrips the following season13. In China, six species of thrips are known to infest winter crops in Wenshan prefecture, Yunnan Province, namely Thrips flavus Schrank, Thrips flavidulus Bagnall, Thrips tabaci Lindeman, Frankliniella intonsa (Trybom), Thrips hawaiiensis (Morgan) and Aeolothrips fasciatus Linnaeus, with T. flavus being the dominant species causing significant damage, in contrast, the thrips that harms notoginseng is T. tabaci, which uses notoginseng, wheat, and rape as the main overwintering sites14. There are 11 species of thrips in the main citrus-producing areas of Jiangxi Province, among which the main species of thrips that damage young fruits and scar the surfaces of fruits is T. flavidulus, which overwinters in the soil and reaches peak numbers during the flowering and young fruiting stages of citrus15. There are also large differences in the overwintering developmental stage of Scirtothrips dorsalis Hood in different hosts in different regions, overwintering as adults in lychee and longan bark cracks and camellias in Sichuan Province, as 4-instar nymphs in Ginkgo biloba L. in Shandong Province, and as adults and a few nymphs in tea plantations of Jiangxi Province, but not overwintering in Guangdong Province16,17,18,19.

F. serrata mainly feeds on gramineous plants, occasionally appearing on tobacco, and is now found on Ficus trees and continues to expand its host plants20. To date, studies on F. serrata have focused mainly on biological characteristics, degree of damage, population dynamics, variety resistance, monitoring, and control21,22,23,24,25,26,27. In the 1990s, some scholars have reported that thrips overwintered in Sichuan Province as adults in the heart leaves of unharvested sugarcane used as seedlings in winter, sugarcane planted in autumn, and sugarcane shoots in autumn28,29. With changes to optimize sugarcane planting areas and improve and renew sugarcane varieties, sugarcane production has gradually been concentrated into three areas, namely, central southern Guangxi, southwestern Yunnan, and western Guangdong, China30. Sugarcane varieties have been updated from the fourth generation of sugarcane varieties such as ‘ROC 22’ and ‘ROC 20’ to the fifth generation of ‘Yunzhe 081,609’, ‘Guitang 42’, ‘Guiliu 05,136’, ‘Guitang 44’, ‘Yunzhe 0551’ and other new varieties with high sugar contents and high yields31. Since the sugarcane planting areas in Yunnan are mainly dry sloping lands, with the vigorous promotion of autumn-planted and winter-planted sugarcane, the overwintering situation of F. serrata and its influencing factors in the Yunnan sugarcane areas are still unclear. We investigated the relationship between the overwintering of F. serrata and its host sugarcane and the geographic environment to preliminarily analyze the ecological adaptive mechanism of thrips. Therefore, this study conducted a detailed survey on the morphology, sex (female and male), and location of overwintering thrips of different sugarcane varieties during different growth periods at three research bases of the Sugarcane Research Institute of Yunnan Academy of Agricultural Sciences from January to February 2023. The study also analyzed the factors influencing overwintering, aiming to reveal the occurrence and overwintering of thrips in Yunnan during winter, to clarify the main influencing factors, and to provide an important basis for monitoring and effective control of F. serrata.

Materials and methods

Time and place of investigation

A survey of the overwintering population of F. serrata was conducted from January 5 to February 6, 2023, at the research bases of the Sugarcane Research Institute of Yunnan Academy of Agricultural Sciences and the Lengshuigou in Lebaidao Street, Kaiyuan City, Yunnan Province, China, and the research base of Mabao, Pengpu Town, Mile City, Yunnan Province, China. The information of the three bases is shown in Table 1.

Table 1 Basic information of three bases.
Full size table

Survey of sugarcane varieties

Five sugarcane varieties were investigated: Yunzhe 081,609, Yunzhe 0551, Guiliu 05,136, ROC 22, and Yuetang 93,159. Based on the results of a previous study, the sugarcane varieties were divided into 4 resistance grades: the first grade was Guiliu 05,136, the second grade was ROC 22 and Yunzhe 0551, the third grade was Yuetang 93,159, and the fourth grade was Yunzhe 08160926.

Survey and acquisition methods

Three fields for each sugarcane variety at each trial site were used. A five-point sampling method was used, with 10 plants collected at each point, and the young leaves at the tip of the sugarcane were collected at the seedling and mature stages. The tops of the young leaves of sugarcane were cut off with scissors, put into sealing pockets, and brought back to the laboratory. The statistics of F. serrata were carried out under a stereoscopic microscope (Leica, EZ4W, Germany). Moreover, the time, location, sugarcane varieties, and growth period of the survey were recorded, and the number and morphology of overwintering thrips on the five sugarcane varieties during the two growth periods of the three research bases were statistically analyzed.

Statistical analysis

The average number of F. serrata in all samples of each treatment was counted, and box plots illustrating significant differences were generated using the R programming language. One-way analysis of variance and multi-factor analysis of variance were conducted using the SAS software package, version 9.4 (SAS Institute Inc., Cary, NC, USA) (https://www.sas.com/zh_cn/home.html) to assess the effects of four factors, namely, survey time, sugarcane variety, sugarcane growth period, and survey location, on the average number of adults in sugarcane. The contribution of each factor and its correlation with the average variance in the number of adults were analyzed and computed to derive an F-value and a P-value and to determine statistical significance based on the magnitude of the P-value.

Results

Analysis of the overwintering developmental stage of F. serrata

There were differences in the average numbers of adults and nymphs of F. serrata among the five varieties (Fig. 1). The average number of adults from five surveys in two sugarcane growth periods of five varieties at three bases was 2.86 individuals/plant, which was significantly greater than that of nymphs, at 0.07 individuals/plant (F(1,2498) = 1195.07, P < 0.001). Yunzhe 081,609 had the most adults and nymphs, at 4.61 individuals/plant and 0.21 individuals/plant, respectively, whereas Guiliu 05,136 had the fewest, at 1.24 individuals/plant and 0.02 individuals/plant, respectively.

Fig. 1
figure 1

The overwintering developmental stage of Fulmekiola serrata. Asterisks (****) represents the significance of the difference at P < 0.0001, the same below.

Full size image

Analysis of the average numbers of overwintering female and male adults of F. serrata

There were differences in the average numbers of females and males of F. serrata among the five varieties (Fig. 2). The average number of females of thrips from five surveys in two sugarcane growth periods of five varieties at three bases was 1.87 individuals/plant, which was significantly greater than that of males thrips, at 0.06 individuals/plant (F(1, 2498) = 241.01, P < 0.001). Yunzhe 081,609 had the most female thrips, at 3.18 individuals/plant, and Guiliu 05,136 had the fewest, at 0.02 individuals/plant.

Fig. 2
figure 2

The average numbers of overwintering females and males of Fulmekiola serrata.

Full size image

Analysis of the overwintering of F. serrata in different sugarcane varieties

The analysis of the overwintering situation of F. serrata in different sugarcane varieties showed that there were differences in the average numbers of adults in the five varieties in the five surveys (P < 0.05) (Table 2). In the first survey, the highest average number of adults was 3.72 individuals/plant on ROC 22, while the lowest average number of adults was 1.31 individuals/plant on Guiliu 05,136, which was significantly higher than that on the remaining four varieties. From the second survey to the fifth survey, the average numbers of adults of Yunzhe 081,608 were the highest with 4.57, 4.45, 2.09, and 2.52 individuals/plant, respectively, while the average numbers of adults on Guiliu 05,136 were the lowest with 1.34, 0.64, 0.46 and 0.50 individuals/plant, respectively.

Table 2 The overwintering of Fulmekiola serrata in different sugarcane varieties in the five surveys.
Full size table

Analysis of the overwintering of F. serrata during different sugarcane growth periods

According to the analysis of the overwintering of F. serrata during different sugarcane growth periods (Fig. 3), thrips infestation was found during both the seedling and mature stages in the five varieties, and the average number of thrips at the seedling stage (2.86 individuals/plant) was significantly greater than that at the mature stage (0.98 individuals/plant) (F(1,498) = 321.41, P < 0.001). The average number of adults at the seedling stage was the highest, at 4.56 individuals/plant in the second survey, and the average number of adults at the mature stage was the lowest, at 0.56 individuals/plant in the fourth survey, indicating F. serrata overwinters mainly at the seedling stage of sugarcane.

Fig. 3
figure 3

The overwintering of Fulmekiola serrata during different sugarcane growth periods.

Full size image

Analysis of the overwintering of F. serrata at different survey sites

According to the analysis of the overwintering of F. serrata at different survey sites, the average number of adults in sugarcane at the Mabao, Sugarcane Institute, and Lengshuigou bases greatly differed (Fig. 4). The average numbers of adults at the Mabao base and Sugarcane Institute base were 2.48 individuals/plant and 2.12 individuals/plant, respectively, which were significantly greater than that at the Lengshuigou base, at 1.16 individuals/plant (Sugarcane Institute base vs Lengshuigou base F(1, 498) = 78.56, P < 0.001; Mabao base vs Lengshuigou base F(1, 498) = 164.01, P < 0.001). The average number of adults in the second survey was the highest, at 3.96 individuals/plant at the Sugarcane Institute base, and the average number of adults in the fifth survey was the lowest, at 0.57 individuals/plant at the Lengshuigou base.

Fig. 4
figure 4

The overwintering of Fulmekiola serrata at different survey sites. The number of asterisks (*) indicates the significance levels: one asterisk (*) indicates P < 0.05, two asterisks (**) indicate P < 0.01, four asterisks (****) indicate P < 0.0001 and ns indicates non-significant differences. SI: Sugarcane Institute base, LS: Lengshuigou base, MB: Mabao base.

Full size image

Analysis of the main factors influencing the overwintering of F. serrata

Through analysis and evaluation of the effects of four factors, namely, survey time, sugarcane variety, sugarcane growth period, and survey location, on the average number of F. serrata adults (Table 3), the results revealed that the main effects of all factors were significant, indicating that each factor independently had a significant effect on the average number of adults in sugarcane. The sugarcane growth period had the most significant main effect, explaining 13.7% of the greater variance in the number of adults (η2 = 0.137). The results of the two-factor interaction analysis revealed that the interaction effect between survey time and sugarcane variety was significant, indicating that the effects of different survey times and different sugarcane varieties on the average number of adults varied. The interaction effect between survey time and sugarcane growth period was significant, indicating that the effects of different survey times and different growth periods on the average number of adults differed. The interaction effect between sugarcane variety and survey location was also significant, indicating that there were significant changes in the influence of different sugarcane varieties on the average number of adults at different survey locations. The interaction effect between sugarcane growth period and survey location was significant, indicating that different sugarcane growth periods at different survey locations had different effects on the average number of adults. The interaction results of the three factors of survey time, sugarcane variety, and sugarcane growth period were significant, indicating that the combination of survey time, sugarcane variety, and sugarcane growth period had a joint effect on the average number of adults. The interaction effect of the three factors of survey time, sugarcane variety, and survey location was significant, indicating that the combination of survey time, sugarcane variety, and survey location had a joint effect on the average number of adults. The results of the four-factor interaction analysis revealed that the four-factor interaction effect of survey time, sugarcane variety, sugarcane growth period, and survey location was also statistically significant. Although the variance explained by this interaction was small, it suggested that the combination of the four factors still had a complex influence on the average number of adults in sugarcane.

Table 3 Statistical analysis of the average number of adult Fulmekiola serrata by multivariate analysis of variance.
Full size table

Discussion

F. serrata overwintered mainly as adults in the sugarcane areas of Yunnan, which was consistent with the behavior of thrips in Sichuan28,29. This study on the overwintering of F. serrata found that mainly females overwintered, similar to T. palmi12 and possibly related to the parthenogenesis of F. serrata, with its parthenogenetic offspring after autumn being mostly female29. The overwintering site of thrips is in the heart leaves of sugarcane, which is consistent with its feeding characteristics28 and may be related to the tender habit of thrips29. The results of the overwintering of thrips at the three bases revealed that the average numbers of adults at the Mabao, Sugarcane Institute, and Lengshuigou bases were significantly different. The average numbers of adults at the Mabao and Sugarcane Institute bases were significantly greater than that at the Lengshuigou base, which may be related to the longer duration of sugarcane planting at the Mabao and Sugarcane Institute bases, as a previous study found that the average number of thrips on an established variety of rooted sugarcane was greater than that on newly planted sugarcane2. This result may also be related to the lack of timely irrigation due to drought and water shortages at the Mabao and Sugarcane Institute bases, resulting in the slowing of sugarcane growth and slowed development of heart leaves, which makes F. serrata more harmful29.

As a long-term pest common to sugarcane, F. serrata has an aggregated spatial distribution32, its occurrence is closely related to the host sugarcane as well as the geographic environment, and a relatively stable zonal composition has been formed during long-term phylogeny to adapt to different environments. Some studies in Cuba have reported that different planting times, ages, and varieties of sugarcane affect the occurrence time, population dynamics, and infestation level of F. serrata24. The present study also revealed that five sugarcane varieties, namely, ROC22, Yuetang 93,159, Yunzhe 0551, Yunzhe 081,609, and Guiliu 05,136, were affected by thrips at both the seedling and maturity stages, but the average number of F. serrata differed. The average number of thrips on Guiliu 05,136 was lower than that of the other four varieties, which is consistent with the results of long-term field observations26,33. Among the high-sugar and high-quality varieties with the same planting and management conditions in central Guangxi, Guiliu 05,136 suffered less damage from thrips due to its strong growth. This may also explain why the hemicellulose and lignin contents in the sugarcane leaves of Guiliu 05,136 were the lowest among the five varieties34. In the past three years, the damage to sugarcane caused by F. serrata has become increasingly serious, and the spread of thrips has accelerated. In particular, the leaf symptoms of the sugarcane variety Yuetang 93,159 after being damaged by thrips were extremely prominent. The leaf infestation index was significantly negatively correlated with only the activities of polyphenol oxidase and superoxide dismutase in sugarcane leaves and not with other physiological and biochemical indices35. Therefore, research on the mechanism of resistance to thrips in sugarcane can provide a theoretical basis for the breeding of thrips-resistant varieties of sugarcane and for the scientific control of F. serrata.

The complex geographical and climatic conditions in the sugarcane areas of Yunnan provide a diverse environment for the occurrence and spread of F. serrata. The sugarcane areas in Yunnan have complex topography, great differences in site conditions, and diverse climate types, which are mainly divided into subtropical humid, multiluminescent sugarcane areas dominated by western Yunnan and subtropical semihumid sugarcane areas dominated by southern Yunnan36. However, in the sugarcane areas of Wenshan and Guangnan in Yunnan, where there are large differences in altitude and occasional frosts occur in local high-elevation areas, it is not clear how cold resistance of F. serrata during overwintering, and whether its cold resistance affects the safe overwintering of thrips needs further research. At present, the areas of fall-planted sugarcane and winter-planted sugarcane in Yunnan are increasing annually, which provide sufficient food and convenient sites for F. serrata to overwinter, and the threat of thrips spreading in winter is also increasing; thus, research on the overwintering adaptability of thrips may facilitate the precise monitoring and effective control of F. serrata.

Conclusion

By studying the occurrence of damage and overwintering of F. serrata in five varieties during two sugarcane growth periods at three bases over five surveys, multivariate analysis of variance was used to evaluate the effects of four factors, namely, survey time, sugarcane variety, growth period and survey location, on the average number of overwintering adults. The results revealed that F. serrata overwintered mainly in the heart leaves of sugarcane at the seedling stage, with females being the most prevalent. The survey time, sugarcane variety, sugarcane growth period, and survey location all had different degrees of influence on the average number of thrips, among which the growth period of sugarcane had the greatest influence on the average number of thrips.