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Abstract This paper discussed and summarized the parasitic characters and the protection and utilization of 7 species of dominant natural enemies of sugarcane pests in Yunnan, China. Sugarcane pests are numerous and there are rich natural enemy resources in Yunnan sugarcane areas. There are more than 283 species of natural enemies against sugarcane pests in Yunnan, among which the dominant natural enemies with protection and utilization value and research significance include Trichogramma, Apanteles flavipes(Cameron) and Sturmiopsis inferens Townsend parasitic on sugarcane borers, Synonycha grandis (Thunberg), Lemnia biplagiata (Swartz), Chilomenes sexmaculata (Fabricius) and Thiallela sp catching and feeding on Ceratovacuna lanigera Zehntner, and Euborellia pallipes Shiraki preying on Saccharicocus sacchari (Cocherell), Dysmicoccus bohinsis Kuw, Trochorhopalus humeralis Chevrolat and Diocalandra sp. There is also one fungal parasite, namely Beauveria bassiana, which is widely distributed in nature, and can parasitize in a variety of sugarcane pests including sugarcane borers, Exolontha serrulata (Gyllenhal), Alissonotum impressicolle Arrow, T. humeralis and Otidognathus rubriceps Chevrola. It has a natural parasitism rate generally around 10% and certain natural inhibition effect on sugarcane pests. Reasonably protecting and utilizing natural enemies and giving full play to the natural regulation of natural enemies on pests are of great significance for protecting the ecological environment, maintaining the ecological balance of sugarcane fields, improving the comprehensive management level of pests, and promoting the sustainable development of sugar industry.
Key words Sugarcane; Pest; Dominant natural enemies; Protection and utilization
Received: April 22, 2019Accepted: July 12, 2019
Supported by Sugar Crop Research System (CARS170303); Training Project of Yunling Industry and Technology Leading Talents (2018LJRC56); Special Fund of Agricultural Industry Research System in Yunnan Province.
Jie LI (1989-), female, P. R. China, master, research assistant, devoted to research about sugarcane pest control.
*Corresponding author. Email: huangyk64@163.com.
The cane sugar industry is the main economic source for the economic development of Yunnan and the increase of farmers income in frontier minority areas. Yunnan is Chinas second largest sugarcane planting area, as well as the key development area for Chinas sugarcane production and the most potential development area. For many years, the sugarcane pests in Yunnan sugarcane areas are mainly controlled depending on chemical pesticides. Due to the longterm continuous use of highlytoxic and broadspectrum pesticides such as methamidophos, omethoate and terbufos, a large number of natural enemies of pests in nature have been killed. As a result, new changes have taken place in the dynamic relationship between pests and natural enemies, and the natural enemy populations have been continuously reduced, resulting in a reduction of the natural factors that restrain pests, which makes pest control work more passive. Moreover, the abuse of chemical pesticides is also prone to pesticide residues and environmental pollution. Therefore, the management of pests from a comprehensive and environmental perspective is a new task which plant protection workers face today. In China, in recent years, biological control has become one of the important measures to comprehensively control pests and diseases. Its social and ecological benefits have attracted more and more attention from the state and society. The sugarcane planting area in Yunnan Province is large and widely distributed. The climate and environment of the sugarcane area are complex and varied, and there are many kinds of pests. There are also rich natural enemy resources. According to the survey and statistics, 283 natural enemies of sugarcane pests were found in the province. Among the natural enemies found, the dominant species with protection and utilization value and research significance include Trichogramma, Apanteles flavipes(Cameron) and Sturmiopsis inferens Townsend parasitic on sugarcane borers, Synonycha grandis (Thunberg), Lemnia biplagiata (Swartz), Chilomenes sexmaculata (Fabricius) and Thiallela sp catching and feeding on Ceratovacuna lanigera Zehntner［1-2］, and Euborellia pallipes Shiraki catching and feeding on Saccharicocus sacchari (Cocherell), Dysmicoccus bohinsis Kuw, Trochorhopalus humeralis Chevrolat and Diocalandra sp. There is also one fungal parasite, namely Beauveria bassiana, which is widely distributed in nature, and can parasitize in a variety of sugarcane pests including sugarcane borers, Exolontha serrulata (Gyllenhal), Alissonotum impressicolle Arrow, T. humeralis and Otidognathus rubriceps Chevrola, and has a natural parasitism rate generally around 10% and certain natural inhibition effect on sugarcane pests［2-4］. In order to meet the requirements of scientific plant protection, further give full play to biological control in the comprehensive prevention and control of sugarcane pests, promote the development of biological control of sugarcane pests in China, and continuously improve the level of comprehensive control of sugarcane pests, the natural enemies of sugarcane pests in Yunnan sugarcane area in China and their protection and utilization were discussed below.
Trichogramma
Parasitic characteristic
Trichogramma Westwood is kind of egg parasitoid belonging to Trichogramma of Trichogrammatidae in Hymenoptera, as well as a multiselective important natural enemy of the egg stage. Its life history goes through four periods, and the process from egg to adult is spent in parasitized eggs. In the sugarcane field, it can parasitize in the eggs of lepidopteran pests including Sesamia inferens Walker, Chilo infuscatellus Snellen, Argyroploce schistaceana (Snellen), Proceras venosatum Walker, Tryporyza intacta Snellen, Taiwanese Chilo auricilia Dudgeon and Mythimna separata (Walker)［3-10］. From the parasitized eggs come out the Trichogramma adults, which then fly to find new eggs to parasitize in before long. Trichogramma mainly relies on the olfactory organs on the tentacle to find parasitic eggs. When the host is found, it can ovulate later. It most likes parasitizing fresh eggs that are laid by sugarcane borers, and does not like discolored eggs that have developed to a certain degree. Trichogramma is a kind of natural enemy with great value. There are more than 140 varieties of Trichogramma in the world, among which 26 varieties are found in China［11］. Trichogramma varieties, which can parasitize sugarcane borer eggs, include Trichogramma confusum Viggiani, Trichogramma chilonis, Trichogramma dendrolimi Matsumra, Trichogramma japonicum Ashmead, Trichogramma poliae Nagaraja, Trichogramma nana Zehnter, Trichogramma ostriniae Pang et Chen, Trichogramma evanescens, etc.［3-10］. However, it is most important to study the T. confusum.
China has a very successful example of using T. confusum to control sugarcane borers. In the 1960s, the largescale release of Trichogramma in Taiwan Province had a gratifying effect on the control of sugarcane borers. The parasitism rate of eggs was 73.0%-74.8% in the fields where Trichogramma was released, and that in the control field was 10.2%-29.2%. The dead heart rate caused by borer attack decreased by 44.4%-75.3%, and the rate of bored internodes decreased by 37.5%-65.4%.
In 1958, the Chinas first Trichogramma station was established in Shunde County, Guangdong Province. Subsequently, sugarcane fields such as Guangxi, Fujian, Yunnan, Hunan and Sichuan also used Trichogramma to control sugarcane borers in succession. From 1974 to 1975, the Sugarcane Research Institute of Yunnan Province carried out a comprehensive study on the control of A. schistaceana in the sugarcane areas of the southeastern Yunnan Province, and achieved the control effect over 80%, thereby effectively controlling the damage of A. schistaceana. From 1981 to 1985, in the 13 333 hm2 sugarcane field of Institute of Plant Protection, Guangdong Academy of Agricultural Sciences in the Pearl River Delta, based on agricultural control, scientific control was carried out mainly by releasing Trichogramma combined with comprehensive preventive health measures including scientific drug use and protecting natural enemies, and achieved the effects of controlling 80% of the dead heartdamaged plants, reducing the rate of bored internodes by 71% and the dieback rate by 58.1%, and reducing the yield by 17 177.5 kg/hm2. From 1983 to 1985, in the 1 133 hm2 sugarcane field of Sugarcane Research Institute in Guigang of Guangxi, comprehensive measures combining agricultural control (including the selection of varieties with strong compensatory power and promotion of soybean intercropping) and rational use of drugs were taken based on ecological viewpoints (mainly releasing Trichogramma), and obvious effects were observed in controlling dead heart caused by sugarcane borers and reducing rate of bored internodes. The parasitism rate of eggs was 53.8%-72.5% in the fields where Trichogramma was released, and that in the control field was 11.6%-15.9%. And the rate of bored plants and rate of bored internodes in the fields where Trichogramma was released were 9.75% and 0.83%, respectively, and those in the control field were 43.95%-56.64% and 9.75%, respectively. The Institute of Sugarcane Science of Hubei Dayuan Farm and the Institute of Biology of Jilin Agricultural University conducted a study on the comprehensive control of C. infuscatellus, which mainly relied on releasing Trichogramma for three consecutive years from 1996. The cumulative area was 16 667 hm2, and they effectively controlled C. infuscatellus and increased the production by about 7 500 kg/hm2, receiving good economic, social and ecological benefits［3-10］. In order to improve the yield and quality of sugarcane, Zhanjiang Nongken Fengshou Co., Ltd. carried out the biological control of sugarcane borers using Trichogramma in 6 667 hm2 of cane area in 2007, during which a total of 7 batches of Trichogramma and a total of 3.58 billionindividuals were released. The average rate of bored internodes in the more than 1 000 sugarcane samples was 23.0%, which was 16.7% lower than that of the same period of last year, and it was expected to produce 4 800 t of sugar more, which meant an increase in the output value by 16.8 million yuan. Relying on the national "948" industry major project, Fujian Agriculture and Forestry University introduced it from Taiwan, and established a complete set of technical procedures for the use of the eggs of the C. cephalocrocis to breed T. chilonis, including following technical links as C. cephalocrocis breeding, collection of adult moths to lay eggs, collection of C. cephalocrocis eggs and making egg cards, Trichogramma reproduction, constant temperature preservation and field release. In 2009, under the support of the National Sugarcane Industry Technology Research System, the post scientists Dr. Xu, Dr. Zhang and other team members produced about 150 000 Trichogramma cards, and used Trichogramma to control sugarcane borers in the Zhanjiang sugarcane area of Guangdong Province with a demonstration area of 667 hm2 or more. The survey showed that the parasitism rates of borer eggs in the Trichogrammareleasing areas with different releasing densities all reached 100%, and compared with the control area, the rates of bored plants and bored internodes were significantly reduced, resulting in the control effects of 45% and 41% respectively. In the Guangxi sugarcane areas, Dr. Huang carried out the technology demonstration of reproducing Trichogramma in castor silkworms to control sugarcane borers, with a cumulative application area of 5 333 hm2. The survey showed that compared with the control area, the parasitism rate of sugarcane borer eggs in the Trichogrammareleasing area increased by more than 30%, and the rate of bored internodes increased by more than 44%.
Protection and utilization ways
Advocating intercropping
Interplanting soybean, peanut, vegetables, green manure and other crops in the sugarcane field can change the microclimate in the field, which is conducive to the survival and reproduction of Trichogramma.
Rational drug use
From the early spring, no or less broadspectrum pesticides are applied in sugarcane field, and selective pesticides are applied instead. Moreover, rootzone soil application can be adopted, to protect small initial amount of Trichogramma in early period. Artificially rearing and releasing Trichogramma
Sugarcane borer is one of the main control object in the utilization of Trichogramma. The key techniques for releasing Trichogramma in sugarcane field is to allow emerged Trichogramma to meet sugarcane borer eggs to the utmost extent with suitable quantity at suitable time. Therefore, the erisilkworm eggs can be used for artificial rearing of Trichogramma. When sugarcane borers begin to lay eggs in the middle and late March, Trichogramma is released in the sugarcane field. It can be released once every 10-15 d, 5-7 times totally a year. In each hectare of field, 75-120 release points can be set, and about 150 000 individuals can be released per time. And according to the repeated Trichogrammareleasing method, three batches of Trichogramma host eggs of different eclosion dates are put into a release device at the same time, and the eclosion dates of various batches of Trichogramma differ by 3-6 d, so that there are Trichogramma in the field within 12-15 d, which can greatly improve the control effect. When you release Trichogramma, you should pay attention to the weather changes. This activity can be carried out on a sunny day at 8:00 to 9:00 after the dew is evaporated, or after 16:00 when the sunshine is not strong. In the event of a storm, it cannot be released. The egg mass can be placed in a Trichogrammakeeping box and sealed with honey water, and then released after the weather turns fine.
A. flavipes
Parasitic characteristics
A. flavipes belongs to Apanteles Forster in Braconidae of Hymenoptera. It is a dominant natural enemy of the parasitized S. inferens and C. infuscatellus, and plays an effective role in the control of borer pests. The distribution of A. flavipes in Yunnan is quite common, and it has been discovered in the sugarcane areas in Qiaojia and Yongshan of northeastern Yunnan, Kaiyuan, Maitreya, Wenshan and Jinping of southern Yunnan and Binchuan and Huaning in central Yunnan in succession. A. flavipes is parasitic by larva in the larvae of S. inferens and C. infuscatellus. In the survey of Kaiyuan, it parasitized in the pests from the first generation to the fifth generation of the host, and coincided with the larvae of various generations of sugarcane borer larvae, and the natural parasitism rate was as high as 25%-40%, and was the highest from May to June; the multiplication rate was higher in that one sugarcane borer larva can produce more than 80-100 A. flavipes individuals in the body; and the parasitized sugarcane borer larvae were slowmovingand took greatly reduced and ultimately no food, which reduced the damage to sugarcane［1-3,6,10, 12］. Protection and utilization ways
Vigorously promoting intercropping
Interplanting maize, soybean, peanut, vegetables, green manure and other crops in the sugarcane field can change the microclimate in the field, which is conducive to the survival and reproduction of A. flavipes.
Rational drug use
From the early spring, no or less broadspectrum pesticides are applied in sugarcane field, and selective pesticides are applied instead. Moreover, rootzone soil application can be adopted, to protect small initial amount of A. flavipes in early period.
Artificially rearing and releasing A. flavipes
A. flavipes can be reproduced in the transtic host oriental armyworms. During the peak period of the first and second generations of sugarcane borer larvae from March to June, A. flavipes can be released to the sugarcane field in batches to increase the population of A. flavipes in sugarcane field and increase the parasitism rate.
Agricultural Biotechnology2019
S. grandi
Predation characteristics
S. grandi belongs to Coccinellidae in Coleoptera. It is a dominant predator of C. lanigera. It is widely distributed in the sugarcane areas in Yunnan, China and has a large population. One S. grandi can prey on 32 000 sugarcane C. lanigera, so it has obvious inhibitory effect on sugarcane C. lanigera. According to field investigations, adults and larvae of S. grandi both like preying on C. lanigera, and the food intake of the adults is larger than larvae. In winter and spring, when sugarcane C. lanigera is lacking, S. grandi can also prey on aphids of bamboo shoots, maize, citrus, beans and vegetables［1-8,10,13,16］.
Among the natural enemies of C. lanigera, S. grandi is used as a means for controlling C. lanigera the earliest. In Taiwan Province, as early as the late 1930s, S. grandi was raised indoors (the feed was sugarcane C. lanigera collected from the field) and then released to sugarcane field. From 1951 to 1954, it was recorded that 23 582 S. grandi were released to 60 hm2 of sugarcane field that was seriously damaged by sugarcane C. lanigera. In most cases, almost all the sugarcane C. lanigera was extinguished after the release of S. grandi was lasted for one month. From 1980 to 1981, Guangxi Academy of Agricultural Sciences and Guangxi Agricultural College collaborated on a comprehensive prevention and control experiment based on the biological control of releasing S. grandi to control sugarcane C. lanigera. Their experience is that in spring (March), S. grandi is released to autumn planting land to suppress the pest source; and in summer (May-June), 3-4 batches of S. grandi are released to the ratoon or spring planting sugarcane fields (the standard is the rate of C. lanigeradamaged plants at 5% and a pest index of about 0.006), which can effectively control the occurrence of sugarcane C. lanigera［1-8,10,13,16］. Protection and utilization ways
Artificial preservation and propagation
In December, before the sugarcane harvest, overwintering S. grandi can be collected into rooms in a timely manner, placed in glass jars, and artificially fed 5%-10% sugar water and C. lanigera preserved at 3-4 ℃, which can significantly improve the winter survival rate of S. grandi［14］. Combined with transplantation and artificial reproduction, in the beginning of June, when the sugarcane C. lanigera occurs in a spotted manner, S. grandi is released into the sugarcane field to allow proliferation, so as to effectively control the sugarcane C. lanigera. The released insects should be adults and older larvae. Meanwhile, sunny and warm weather should be selected for releasing. Generally, 750-1 500 heads of S. grandi adults or 37 500 heads of larvae are released per hectare onto sugarcane plants with a high C. lanigera population density.
Advocating intercropping
Maize, soybean, peanut, vegetables, green manure and other crops are intercropped in sugarcane fields as far as possible, which can change the microclimate environment of sugarcane fields and facilitate the habitat and growth of S. grandi. On the other hand, aphids occur early and in large quantities on the intercropping crops, which can significantly increase the number of S. grandi.
Rational drug use
S. grandi adults and larvae are very sensitive to pesticides. Therefore, chemical control must use selective pesticides, and the application times, application methods and application time should be controlled according to the situation of pests, so that the initial number of S. grandi, which are relatively less, can be protected and utilized.
Advocating returning sugarcane leaves into field
It is important to promote the return of sugarcane leaves to field to minimize the possibility of killing S. grandi, and to give full play to the natural control effect of S. grandi on sugarcane C. lanigera.
L. biplagiata
Predation characteristics
L. biplagiata belongs Coccinellidae in Coleoptera. It is another main natural predator of C. lanigera. Its food intake is only second to S. grandi. S. grandi adults and larvae both could prey on C. lanigera. It is distributed in Yunnan sugarcane areas in China and has a wide range of activities. It is often found in sugarcane and bamboo, maize, vegetables, fruit trees and other agricultural crops, and it is used to prey on aphids, woodlice, leafhoppers and planthoppers. L. biplagiata has a large body with high predation efficiency. According to the feeding observation, each L. biplagiata larva can prey on 580 heads of sugarcane C. lanigera during the whole larval stage, and can prey on 738 heads at most. The predation number is the largest at the 3 to 4 instar, accounting for 84.14% of the total food intake at the whole larval stage. At the adult stage, an average of 126 C. lanigera, 253 heads at most, can be eaten every day. L. biplagiata changes its predation objects in the field with the seasonal growth and decline of the prey in the field, and its population grows fast. The population density of pests is large in the spring field, while L. biplagiata has a greater inhibitory effect on the growth of sugarcane C. lanigera population in the early stage of occurrence［1-3,6-8,10,16］. Protection and utilization ways
Field investigations show that in the early stage of sugarcane C. lanigera, when sugarcane C. lanigera sporadically occurs, if the sugarcane field has a certain number of L. biplagiata, it can play a significant role in inhibiting the development of the sugarcane C. lanigera population, making it difficult for the C. lanigera population to form a peak. On the other hand, L. biplagiata can also be used in conjunction with S. grandi, another important natural enemy of C. lanigera, to play a greater role. Because the suitable temperature range for L. biplagiata is wider than that for S. grandi, plus its shorter life cycle, more generations and more prey, L. biplagiata often feeds and breeds in the field before S. grandi and also appears in the cane field before S. grandi. Because of its relatively smaller food intake than S. grandi, it is easy to form a community when C. lanigera sporadically occurs in sugarcane field. Consequently, C. lanigera in sugarcane field is controlled by L. biplagiata when the population is small, and after the population of C. lanigera is large, the two species of ladybugs can be used simultaneously, to achieve a more obvious effect. The protection and utilization measures of L. biplagiata are the same as S. grandi.
Thiallela sp.
Predation characteristics
Thiallela sp. belongs to Pyralidae in Lepidoptera. It is an another important natural enemy of C. lanigera. Thiallela sp. is distributed in the Philippines, Java, and the sugarcane areas in China such as Guangdong, Guangxi, Taiwan, Fujian, and Yunnan. It is widely distributed in Yunnans sugarcane areas. It preys on sugarcane C. lanigera in larvae. The larvae at the 1st instar mainly feed on the secretion of C. lanigera, and occasionally bite the tentacles and feet of sugarcane C. lanigera. The larvae at the 2nd instar can directly bite the abdomen of C. lanigera and absorb its body fluid. At the 3rd and 4th instars, the larvae have the food intake greatly increased, and can eat up C. lanigera only leaving the remains such as the tergum and head capsule. One larva can prey on 133 heads of C. lanigera, 152 heads at most during the whole lifetime. Therefore, Thiallela sp. has a significant inhibitory effect on the growth of C. lanigera population［2-3,6-8,10,15-16］.
Protection and utilization ways
Advocating intercropping
Interplanting soybean, peanut, vegetables, green manure and other crops in sugarcane field can change the microclimate in the field and create the diversity of farmland ecosystems, which is conducive to the preservation and reproduction of Thiallela sp. in early spring. Rational drug use
The broadspectrum chemical pesticides have obvious killing effects on the adults and larvae of Thiallela sp., especially the highlytoxic agents such as methamidophos, omethoate and terbufos. Therefore, starting from the early spring sugarcane field, no or less broadspectrum pesticides are applied in sugarcane field, and selective pesticides can be selected. Moreover, rootzone soil application can be adopted, to avoid the killing effect on the natural enemies such as Thiallela sp.
Advocating returning sugarcane leaves into field
Burning sugarcane leaves leads to the death of a large number of wintering Thiallela sp., while returning sugarcane leaves into field provides a good wintering place for Thiallela sp. and improves winter survival rate.
E. pallipe
Predation characteristics
E. pallipe belongs to Psalididae in Dermaptera. It is distributed in sugarcane provinces such as Guangdong, Guangxi, Taiwan, Fujian and Yunnan. It is widely distributed in Yunnan sugarcane area, and widely found in sugarcane fields. E. pallipe is an important natural enemy of various pests such as sugarcane Elaeidobius kamerunicus, borer, S. sacchari and F. serrata. E. pallipe adults and nymphs prey on sugarcane borer larvae, S. sacchari adults and nymphs, E. kamerunicus larvae and eggs, F. serrata adults and nymphs and blackcutworm. E. pallipe has a wide distribution, a large number, a wide predation range and a large food intake, and thus has obvious inhibitory effects on various important sugarcane pests［2-3］.
Protection and utilization ways
Advocating intercropping
Interplanting soybean, peanut, vegetables, green manure and other crops in sugarcane field can change the microclimate in the field and create the diversity of farmland ecosystems, which is conducive to the preservation and reproduction of E. pallipe in early spring.
Rational drug use
No or less broadspectrum pesticides are applied in sugarcane field, and selective pesticides can be selected. Moreover, rootzone soil application can be adopted, to avoid the killing effect on the natural enemies such as E. pallipe and control pests using natural populations.
Advocating returning sugarcane leaves into field
Burning sugarcane leaves leads to the death of a large number of wintering E. pallipe, while returning sugarcane leaves into field provides a good wintering place for Thiallela sp. and improves winter survival rate. Artificially rearing and breeding and releasing to sugarcane field
The indoor feeding method of E. pallipe is simple and easy to operate. Before entering the winter, in the place where E. pallipe inhabits, the adults are caught into a canned bottle containing fine sand and 3-4 dry leaf sheaths according to about 10 heads per bottle; the sugarcane S. sacchari is supplied as a food, and attention is paid to soil moisture (about 15%); after the adults lay eggs and the nymphs are hatched, some individuals should be moved to another bottle in time; and the fine sand used is changed according to the pollution situation once per 10-20 d.
Parasitic fungus: B. bassiana
In the muscardine disease of insects, the most common cause is B. bassiana, accounting for 21% of all insect fungal diseases. The pathogen belongs Beauveria in Moniliaceae of Moniliales. From south to north in China, B. bassiana can parasitize over 200 insects and mites. B. bassiana is also the most widely distributed in Yunnan sugarcane areas. Field investigations show that B. bassiana can infect larvae of E. serrulata and A. impressicolle larvae, and larvae, pupae and adults of T. humeralis and O. rubriceps, and its natural incidence is generally 8%-15%, so it has control these pests to a certain extent［3-4］.
B. bassiana is an entomopathogenic fungus that is widely used in China to control pests in the field. According to incomplete statistics in 1992, the application of B. bassiana to control more than 40 kinds of pests has been successful. Only in 10 provinces (regions) in southern China, there are 64 B. bassiana plants with an annual production capacity of more than 2 100 t, which has an annual control area over 503 000 hm2, playing a huge role in controlling the occurrence of pests and reducing environmental pollution［3-4］.
Foreign countries such as Australia, France and other sugarcane countries have long adhered to the use of B. bassiana to control underground pests such as sugarcane chafers, and have achieved obvious control effects and good environmental and ecological benefits［3-4］.
In controlling sugarcane pests with a B. bassiana preparation, it can be sprayed at a concentration of 100 million spores per ml when sugarcane borers begin to lay eggs in middle and late March. Or in April-May which is the peak period for E. serrulata, A. impressicolle T. humeralis and longicorn beetles, combined with lessening and ridging, 45-60 kg of 2% B. bassiana dust granules is applied per hectare by mixing with 600 kg of dry fine soil or chemical fertilizer and evenly applying to the base of sugarcane plants. The control effect is remarkable, and the effective period can be maintained for a long time. References
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Key words Sugarcane; Pest; Dominant natural enemies; Protection and utilization
Received: April 22, 2019Accepted: July 12, 2019
Supported by Sugar Crop Research System (CARS170303); Training Project of Yunling Industry and Technology Leading Talents (2018LJRC56); Special Fund of Agricultural Industry Research System in Yunnan Province.
Jie LI (1989-), female, P. R. China, master, research assistant, devoted to research about sugarcane pest control.
*Corresponding author. Email: huangyk64@163.com.
The cane sugar industry is the main economic source for the economic development of Yunnan and the increase of farmers income in frontier minority areas. Yunnan is Chinas second largest sugarcane planting area, as well as the key development area for Chinas sugarcane production and the most potential development area. For many years, the sugarcane pests in Yunnan sugarcane areas are mainly controlled depending on chemical pesticides. Due to the longterm continuous use of highlytoxic and broadspectrum pesticides such as methamidophos, omethoate and terbufos, a large number of natural enemies of pests in nature have been killed. As a result, new changes have taken place in the dynamic relationship between pests and natural enemies, and the natural enemy populations have been continuously reduced, resulting in a reduction of the natural factors that restrain pests, which makes pest control work more passive. Moreover, the abuse of chemical pesticides is also prone to pesticide residues and environmental pollution. Therefore, the management of pests from a comprehensive and environmental perspective is a new task which plant protection workers face today. In China, in recent years, biological control has become one of the important measures to comprehensively control pests and diseases. Its social and ecological benefits have attracted more and more attention from the state and society. The sugarcane planting area in Yunnan Province is large and widely distributed. The climate and environment of the sugarcane area are complex and varied, and there are many kinds of pests. There are also rich natural enemy resources. According to the survey and statistics, 283 natural enemies of sugarcane pests were found in the province. Among the natural enemies found, the dominant species with protection and utilization value and research significance include Trichogramma, Apanteles flavipes(Cameron) and Sturmiopsis inferens Townsend parasitic on sugarcane borers, Synonycha grandis (Thunberg), Lemnia biplagiata (Swartz), Chilomenes sexmaculata (Fabricius) and Thiallela sp catching and feeding on Ceratovacuna lanigera Zehntner［1-2］, and Euborellia pallipes Shiraki catching and feeding on Saccharicocus sacchari (Cocherell), Dysmicoccus bohinsis Kuw, Trochorhopalus humeralis Chevrolat and Diocalandra sp. There is also one fungal parasite, namely Beauveria bassiana, which is widely distributed in nature, and can parasitize in a variety of sugarcane pests including sugarcane borers, Exolontha serrulata (Gyllenhal), Alissonotum impressicolle Arrow, T. humeralis and Otidognathus rubriceps Chevrola, and has a natural parasitism rate generally around 10% and certain natural inhibition effect on sugarcane pests［2-4］. In order to meet the requirements of scientific plant protection, further give full play to biological control in the comprehensive prevention and control of sugarcane pests, promote the development of biological control of sugarcane pests in China, and continuously improve the level of comprehensive control of sugarcane pests, the natural enemies of sugarcane pests in Yunnan sugarcane area in China and their protection and utilization were discussed below.
Trichogramma
Parasitic characteristic
Trichogramma Westwood is kind of egg parasitoid belonging to Trichogramma of Trichogrammatidae in Hymenoptera, as well as a multiselective important natural enemy of the egg stage. Its life history goes through four periods, and the process from egg to adult is spent in parasitized eggs. In the sugarcane field, it can parasitize in the eggs of lepidopteran pests including Sesamia inferens Walker, Chilo infuscatellus Snellen, Argyroploce schistaceana (Snellen), Proceras venosatum Walker, Tryporyza intacta Snellen, Taiwanese Chilo auricilia Dudgeon and Mythimna separata (Walker)［3-10］. From the parasitized eggs come out the Trichogramma adults, which then fly to find new eggs to parasitize in before long. Trichogramma mainly relies on the olfactory organs on the tentacle to find parasitic eggs. When the host is found, it can ovulate later. It most likes parasitizing fresh eggs that are laid by sugarcane borers, and does not like discolored eggs that have developed to a certain degree. Trichogramma is a kind of natural enemy with great value. There are more than 140 varieties of Trichogramma in the world, among which 26 varieties are found in China［11］. Trichogramma varieties, which can parasitize sugarcane borer eggs, include Trichogramma confusum Viggiani, Trichogramma chilonis, Trichogramma dendrolimi Matsumra, Trichogramma japonicum Ashmead, Trichogramma poliae Nagaraja, Trichogramma nana Zehnter, Trichogramma ostriniae Pang et Chen, Trichogramma evanescens, etc.［3-10］. However, it is most important to study the T. confusum.
China has a very successful example of using T. confusum to control sugarcane borers. In the 1960s, the largescale release of Trichogramma in Taiwan Province had a gratifying effect on the control of sugarcane borers. The parasitism rate of eggs was 73.0%-74.8% in the fields where Trichogramma was released, and that in the control field was 10.2%-29.2%. The dead heart rate caused by borer attack decreased by 44.4%-75.3%, and the rate of bored internodes decreased by 37.5%-65.4%.
In 1958, the Chinas first Trichogramma station was established in Shunde County, Guangdong Province. Subsequently, sugarcane fields such as Guangxi, Fujian, Yunnan, Hunan and Sichuan also used Trichogramma to control sugarcane borers in succession. From 1974 to 1975, the Sugarcane Research Institute of Yunnan Province carried out a comprehensive study on the control of A. schistaceana in the sugarcane areas of the southeastern Yunnan Province, and achieved the control effect over 80%, thereby effectively controlling the damage of A. schistaceana. From 1981 to 1985, in the 13 333 hm2 sugarcane field of Institute of Plant Protection, Guangdong Academy of Agricultural Sciences in the Pearl River Delta, based on agricultural control, scientific control was carried out mainly by releasing Trichogramma combined with comprehensive preventive health measures including scientific drug use and protecting natural enemies, and achieved the effects of controlling 80% of the dead heartdamaged plants, reducing the rate of bored internodes by 71% and the dieback rate by 58.1%, and reducing the yield by 17 177.5 kg/hm2. From 1983 to 1985, in the 1 133 hm2 sugarcane field of Sugarcane Research Institute in Guigang of Guangxi, comprehensive measures combining agricultural control (including the selection of varieties with strong compensatory power and promotion of soybean intercropping) and rational use of drugs were taken based on ecological viewpoints (mainly releasing Trichogramma), and obvious effects were observed in controlling dead heart caused by sugarcane borers and reducing rate of bored internodes. The parasitism rate of eggs was 53.8%-72.5% in the fields where Trichogramma was released, and that in the control field was 11.6%-15.9%. And the rate of bored plants and rate of bored internodes in the fields where Trichogramma was released were 9.75% and 0.83%, respectively, and those in the control field were 43.95%-56.64% and 9.75%, respectively. The Institute of Sugarcane Science of Hubei Dayuan Farm and the Institute of Biology of Jilin Agricultural University conducted a study on the comprehensive control of C. infuscatellus, which mainly relied on releasing Trichogramma for three consecutive years from 1996. The cumulative area was 16 667 hm2, and they effectively controlled C. infuscatellus and increased the production by about 7 500 kg/hm2, receiving good economic, social and ecological benefits［3-10］. In order to improve the yield and quality of sugarcane, Zhanjiang Nongken Fengshou Co., Ltd. carried out the biological control of sugarcane borers using Trichogramma in 6 667 hm2 of cane area in 2007, during which a total of 7 batches of Trichogramma and a total of 3.58 billionindividuals were released. The average rate of bored internodes in the more than 1 000 sugarcane samples was 23.0%, which was 16.7% lower than that of the same period of last year, and it was expected to produce 4 800 t of sugar more, which meant an increase in the output value by 16.8 million yuan. Relying on the national "948" industry major project, Fujian Agriculture and Forestry University introduced it from Taiwan, and established a complete set of technical procedures for the use of the eggs of the C. cephalocrocis to breed T. chilonis, including following technical links as C. cephalocrocis breeding, collection of adult moths to lay eggs, collection of C. cephalocrocis eggs and making egg cards, Trichogramma reproduction, constant temperature preservation and field release. In 2009, under the support of the National Sugarcane Industry Technology Research System, the post scientists Dr. Xu, Dr. Zhang and other team members produced about 150 000 Trichogramma cards, and used Trichogramma to control sugarcane borers in the Zhanjiang sugarcane area of Guangdong Province with a demonstration area of 667 hm2 or more. The survey showed that the parasitism rates of borer eggs in the Trichogrammareleasing areas with different releasing densities all reached 100%, and compared with the control area, the rates of bored plants and bored internodes were significantly reduced, resulting in the control effects of 45% and 41% respectively. In the Guangxi sugarcane areas, Dr. Huang carried out the technology demonstration of reproducing Trichogramma in castor silkworms to control sugarcane borers, with a cumulative application area of 5 333 hm2. The survey showed that compared with the control area, the parasitism rate of sugarcane borer eggs in the Trichogrammareleasing area increased by more than 30%, and the rate of bored internodes increased by more than 44%.
Protection and utilization ways
Advocating intercropping
Interplanting soybean, peanut, vegetables, green manure and other crops in the sugarcane field can change the microclimate in the field, which is conducive to the survival and reproduction of Trichogramma.
Rational drug use
From the early spring, no or less broadspectrum pesticides are applied in sugarcane field, and selective pesticides are applied instead. Moreover, rootzone soil application can be adopted, to protect small initial amount of Trichogramma in early period. Artificially rearing and releasing Trichogramma
Sugarcane borer is one of the main control object in the utilization of Trichogramma. The key techniques for releasing Trichogramma in sugarcane field is to allow emerged Trichogramma to meet sugarcane borer eggs to the utmost extent with suitable quantity at suitable time. Therefore, the erisilkworm eggs can be used for artificial rearing of Trichogramma. When sugarcane borers begin to lay eggs in the middle and late March, Trichogramma is released in the sugarcane field. It can be released once every 10-15 d, 5-7 times totally a year. In each hectare of field, 75-120 release points can be set, and about 150 000 individuals can be released per time. And according to the repeated Trichogrammareleasing method, three batches of Trichogramma host eggs of different eclosion dates are put into a release device at the same time, and the eclosion dates of various batches of Trichogramma differ by 3-6 d, so that there are Trichogramma in the field within 12-15 d, which can greatly improve the control effect. When you release Trichogramma, you should pay attention to the weather changes. This activity can be carried out on a sunny day at 8:00 to 9:00 after the dew is evaporated, or after 16:00 when the sunshine is not strong. In the event of a storm, it cannot be released. The egg mass can be placed in a Trichogrammakeeping box and sealed with honey water, and then released after the weather turns fine.
A. flavipes
Parasitic characteristics
A. flavipes belongs to Apanteles Forster in Braconidae of Hymenoptera. It is a dominant natural enemy of the parasitized S. inferens and C. infuscatellus, and plays an effective role in the control of borer pests. The distribution of A. flavipes in Yunnan is quite common, and it has been discovered in the sugarcane areas in Qiaojia and Yongshan of northeastern Yunnan, Kaiyuan, Maitreya, Wenshan and Jinping of southern Yunnan and Binchuan and Huaning in central Yunnan in succession. A. flavipes is parasitic by larva in the larvae of S. inferens and C. infuscatellus. In the survey of Kaiyuan, it parasitized in the pests from the first generation to the fifth generation of the host, and coincided with the larvae of various generations of sugarcane borer larvae, and the natural parasitism rate was as high as 25%-40%, and was the highest from May to June; the multiplication rate was higher in that one sugarcane borer larva can produce more than 80-100 A. flavipes individuals in the body; and the parasitized sugarcane borer larvae were slowmovingand took greatly reduced and ultimately no food, which reduced the damage to sugarcane［1-3,6,10, 12］. Protection and utilization ways
Vigorously promoting intercropping
Interplanting maize, soybean, peanut, vegetables, green manure and other crops in the sugarcane field can change the microclimate in the field, which is conducive to the survival and reproduction of A. flavipes.
Rational drug use
From the early spring, no or less broadspectrum pesticides are applied in sugarcane field, and selective pesticides are applied instead. Moreover, rootzone soil application can be adopted, to protect small initial amount of A. flavipes in early period.
Artificially rearing and releasing A. flavipes
A. flavipes can be reproduced in the transtic host oriental armyworms. During the peak period of the first and second generations of sugarcane borer larvae from March to June, A. flavipes can be released to the sugarcane field in batches to increase the population of A. flavipes in sugarcane field and increase the parasitism rate.
Agricultural Biotechnology2019
S. grandi
Predation characteristics
S. grandi belongs to Coccinellidae in Coleoptera. It is a dominant predator of C. lanigera. It is widely distributed in the sugarcane areas in Yunnan, China and has a large population. One S. grandi can prey on 32 000 sugarcane C. lanigera, so it has obvious inhibitory effect on sugarcane C. lanigera. According to field investigations, adults and larvae of S. grandi both like preying on C. lanigera, and the food intake of the adults is larger than larvae. In winter and spring, when sugarcane C. lanigera is lacking, S. grandi can also prey on aphids of bamboo shoots, maize, citrus, beans and vegetables［1-8,10,13,16］.
Among the natural enemies of C. lanigera, S. grandi is used as a means for controlling C. lanigera the earliest. In Taiwan Province, as early as the late 1930s, S. grandi was raised indoors (the feed was sugarcane C. lanigera collected from the field) and then released to sugarcane field. From 1951 to 1954, it was recorded that 23 582 S. grandi were released to 60 hm2 of sugarcane field that was seriously damaged by sugarcane C. lanigera. In most cases, almost all the sugarcane C. lanigera was extinguished after the release of S. grandi was lasted for one month. From 1980 to 1981, Guangxi Academy of Agricultural Sciences and Guangxi Agricultural College collaborated on a comprehensive prevention and control experiment based on the biological control of releasing S. grandi to control sugarcane C. lanigera. Their experience is that in spring (March), S. grandi is released to autumn planting land to suppress the pest source; and in summer (May-June), 3-4 batches of S. grandi are released to the ratoon or spring planting sugarcane fields (the standard is the rate of C. lanigeradamaged plants at 5% and a pest index of about 0.006), which can effectively control the occurrence of sugarcane C. lanigera［1-8,10,13,16］. Protection and utilization ways
Artificial preservation and propagation
In December, before the sugarcane harvest, overwintering S. grandi can be collected into rooms in a timely manner, placed in glass jars, and artificially fed 5%-10% sugar water and C. lanigera preserved at 3-4 ℃, which can significantly improve the winter survival rate of S. grandi［14］. Combined with transplantation and artificial reproduction, in the beginning of June, when the sugarcane C. lanigera occurs in a spotted manner, S. grandi is released into the sugarcane field to allow proliferation, so as to effectively control the sugarcane C. lanigera. The released insects should be adults and older larvae. Meanwhile, sunny and warm weather should be selected for releasing. Generally, 750-1 500 heads of S. grandi adults or 37 500 heads of larvae are released per hectare onto sugarcane plants with a high C. lanigera population density.
Advocating intercropping
Maize, soybean, peanut, vegetables, green manure and other crops are intercropped in sugarcane fields as far as possible, which can change the microclimate environment of sugarcane fields and facilitate the habitat and growth of S. grandi. On the other hand, aphids occur early and in large quantities on the intercropping crops, which can significantly increase the number of S. grandi.
Rational drug use
S. grandi adults and larvae are very sensitive to pesticides. Therefore, chemical control must use selective pesticides, and the application times, application methods and application time should be controlled according to the situation of pests, so that the initial number of S. grandi, which are relatively less, can be protected and utilized.
Advocating returning sugarcane leaves into field
It is important to promote the return of sugarcane leaves to field to minimize the possibility of killing S. grandi, and to give full play to the natural control effect of S. grandi on sugarcane C. lanigera.
L. biplagiata
Predation characteristics
L. biplagiata belongs Coccinellidae in Coleoptera. It is another main natural predator of C. lanigera. Its food intake is only second to S. grandi. S. grandi adults and larvae both could prey on C. lanigera. It is distributed in Yunnan sugarcane areas in China and has a wide range of activities. It is often found in sugarcane and bamboo, maize, vegetables, fruit trees and other agricultural crops, and it is used to prey on aphids, woodlice, leafhoppers and planthoppers. L. biplagiata has a large body with high predation efficiency. According to the feeding observation, each L. biplagiata larva can prey on 580 heads of sugarcane C. lanigera during the whole larval stage, and can prey on 738 heads at most. The predation number is the largest at the 3 to 4 instar, accounting for 84.14% of the total food intake at the whole larval stage. At the adult stage, an average of 126 C. lanigera, 253 heads at most, can be eaten every day. L. biplagiata changes its predation objects in the field with the seasonal growth and decline of the prey in the field, and its population grows fast. The population density of pests is large in the spring field, while L. biplagiata has a greater inhibitory effect on the growth of sugarcane C. lanigera population in the early stage of occurrence［1-3,6-8,10,16］. Protection and utilization ways
Field investigations show that in the early stage of sugarcane C. lanigera, when sugarcane C. lanigera sporadically occurs, if the sugarcane field has a certain number of L. biplagiata, it can play a significant role in inhibiting the development of the sugarcane C. lanigera population, making it difficult for the C. lanigera population to form a peak. On the other hand, L. biplagiata can also be used in conjunction with S. grandi, another important natural enemy of C. lanigera, to play a greater role. Because the suitable temperature range for L. biplagiata is wider than that for S. grandi, plus its shorter life cycle, more generations and more prey, L. biplagiata often feeds and breeds in the field before S. grandi and also appears in the cane field before S. grandi. Because of its relatively smaller food intake than S. grandi, it is easy to form a community when C. lanigera sporadically occurs in sugarcane field. Consequently, C. lanigera in sugarcane field is controlled by L. biplagiata when the population is small, and after the population of C. lanigera is large, the two species of ladybugs can be used simultaneously, to achieve a more obvious effect. The protection and utilization measures of L. biplagiata are the same as S. grandi.
Thiallela sp.
Predation characteristics
Thiallela sp. belongs to Pyralidae in Lepidoptera. It is an another important natural enemy of C. lanigera. Thiallela sp. is distributed in the Philippines, Java, and the sugarcane areas in China such as Guangdong, Guangxi, Taiwan, Fujian, and Yunnan. It is widely distributed in Yunnans sugarcane areas. It preys on sugarcane C. lanigera in larvae. The larvae at the 1st instar mainly feed on the secretion of C. lanigera, and occasionally bite the tentacles and feet of sugarcane C. lanigera. The larvae at the 2nd instar can directly bite the abdomen of C. lanigera and absorb its body fluid. At the 3rd and 4th instars, the larvae have the food intake greatly increased, and can eat up C. lanigera only leaving the remains such as the tergum and head capsule. One larva can prey on 133 heads of C. lanigera, 152 heads at most during the whole lifetime. Therefore, Thiallela sp. has a significant inhibitory effect on the growth of C. lanigera population［2-3,6-8,10,15-16］.
Protection and utilization ways
Advocating intercropping
Interplanting soybean, peanut, vegetables, green manure and other crops in sugarcane field can change the microclimate in the field and create the diversity of farmland ecosystems, which is conducive to the preservation and reproduction of Thiallela sp. in early spring. Rational drug use
The broadspectrum chemical pesticides have obvious killing effects on the adults and larvae of Thiallela sp., especially the highlytoxic agents such as methamidophos, omethoate and terbufos. Therefore, starting from the early spring sugarcane field, no or less broadspectrum pesticides are applied in sugarcane field, and selective pesticides can be selected. Moreover, rootzone soil application can be adopted, to avoid the killing effect on the natural enemies such as Thiallela sp.
Advocating returning sugarcane leaves into field
Burning sugarcane leaves leads to the death of a large number of wintering Thiallela sp., while returning sugarcane leaves into field provides a good wintering place for Thiallela sp. and improves winter survival rate.
E. pallipe
Predation characteristics
E. pallipe belongs to Psalididae in Dermaptera. It is distributed in sugarcane provinces such as Guangdong, Guangxi, Taiwan, Fujian and Yunnan. It is widely distributed in Yunnan sugarcane area, and widely found in sugarcane fields. E. pallipe is an important natural enemy of various pests such as sugarcane Elaeidobius kamerunicus, borer, S. sacchari and F. serrata. E. pallipe adults and nymphs prey on sugarcane borer larvae, S. sacchari adults and nymphs, E. kamerunicus larvae and eggs, F. serrata adults and nymphs and blackcutworm. E. pallipe has a wide distribution, a large number, a wide predation range and a large food intake, and thus has obvious inhibitory effects on various important sugarcane pests［2-3］.
Protection and utilization ways
Advocating intercropping
Interplanting soybean, peanut, vegetables, green manure and other crops in sugarcane field can change the microclimate in the field and create the diversity of farmland ecosystems, which is conducive to the preservation and reproduction of E. pallipe in early spring.
Rational drug use
No or less broadspectrum pesticides are applied in sugarcane field, and selective pesticides can be selected. Moreover, rootzone soil application can be adopted, to avoid the killing effect on the natural enemies such as E. pallipe and control pests using natural populations.
Advocating returning sugarcane leaves into field
Burning sugarcane leaves leads to the death of a large number of wintering E. pallipe, while returning sugarcane leaves into field provides a good wintering place for Thiallela sp. and improves winter survival rate. Artificially rearing and breeding and releasing to sugarcane field
The indoor feeding method of E. pallipe is simple and easy to operate. Before entering the winter, in the place where E. pallipe inhabits, the adults are caught into a canned bottle containing fine sand and 3-4 dry leaf sheaths according to about 10 heads per bottle; the sugarcane S. sacchari is supplied as a food, and attention is paid to soil moisture (about 15%); after the adults lay eggs and the nymphs are hatched, some individuals should be moved to another bottle in time; and the fine sand used is changed according to the pollution situation once per 10-20 d.
Parasitic fungus: B. bassiana
In the muscardine disease of insects, the most common cause is B. bassiana, accounting for 21% of all insect fungal diseases. The pathogen belongs Beauveria in Moniliaceae of Moniliales. From south to north in China, B. bassiana can parasitize over 200 insects and mites. B. bassiana is also the most widely distributed in Yunnan sugarcane areas. Field investigations show that B. bassiana can infect larvae of E. serrulata and A. impressicolle larvae, and larvae, pupae and adults of T. humeralis and O. rubriceps, and its natural incidence is generally 8%-15%, so it has control these pests to a certain extent［3-4］.
B. bassiana is an entomopathogenic fungus that is widely used in China to control pests in the field. According to incomplete statistics in 1992, the application of B. bassiana to control more than 40 kinds of pests has been successful. Only in 10 provinces (regions) in southern China, there are 64 B. bassiana plants with an annual production capacity of more than 2 100 t, which has an annual control area over 503 000 hm2, playing a huge role in controlling the occurrence of pests and reducing environmental pollution［3-4］.
Foreign countries such as Australia, France and other sugarcane countries have long adhered to the use of B. bassiana to control underground pests such as sugarcane chafers, and have achieved obvious control effects and good environmental and ecological benefits［3-4］.
In controlling sugarcane pests with a B. bassiana preparation, it can be sprayed at a concentration of 100 million spores per ml when sugarcane borers begin to lay eggs in middle and late March. Or in April-May which is the peak period for E. serrulata, A. impressicolle T. humeralis and longicorn beetles, combined with lessening and ridging, 45-60 kg of 2% B. bassiana dust granules is applied per hectare by mixing with 600 kg of dry fine soil or chemical fertilizer and evenly applying to the base of sugarcane plants. The control effect is remarkable, and the effective period can be maintained for a long time. References
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