(農業試驗所特刊第215號)2018 強化作物關鍵有害生物整合管理之前瞻技術國際研討會專刊 (電子書)

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(1)農試所特刊第 215 號 Special Publication of TARI No. 215. 2018 強化作物關鍵有害生物整合管理之前瞻技術國際研討會專刊 Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops 主編石憲宗張宗仁 Edited by Hsien-Tzung Shih and Chung-Jan Chang 行政院農業委員會 Council of Agriculture, Executive Yuan 行政院農業委員會農業試驗所 Taiwan Agricultural Research Institute, COA, Executive Yuan 台灣昆蟲學會 Taiwan Entomological Society 中華民國植物保護學會 The Plant Protection Society of Republic of China 中華民國 107 年 12 月 December, 2018 .

(2) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. Contents. Preface ------------------------------------------------------------------------------------- i Introduction to the 2018 international symposium on proactive technologies for enhancement of integrated pest management of key crops ----------------------------------------------------------------------------------------------- Hsien-Tzung Shih 1 Identification of the egg parasitoids of Auchenorrhyncha (Hemiptera) of economic importance in Taiwan: collaborative research between Taiwan Agricultural Research Institute and University of California at Riverside scientists ------------------------------------------------------ Serguei V. Triapitsyn 4 Insights into the biology, diversity, and origins of weedy red rice and the use of phylogeographical structures to control its seed-mediated contamination in Taiwan ------------------------------------------------------------- Dong-Hong Wu 17 The eradication projects and the preventative control for quarantine pests in Okinawa, Japan --------------------------------------------------- Tsuyoshi Ohishi 31 Development of vibrational control methods for grapevine pests in California ----------------------------------------------------------------------- Rodrigo Krugner 49 Identify key virulence gene as a control target to mitigate Pierce’s disease of grape ----------------------------------------------------------------------- Hong Lin 57 Utilization of electric pulse power for agricultural products cultivation: forest environment control ---------------------------------------------------- Shoji Ohga 69 Exploitation of new attractants for fruit fly pests of economic importance ------------------------------------------------------------------------------- Ritsuo Nishida 70 Recent progress in optical control of insect pests with light and color --------------------------------------------------------------------------------- Masami Shimoda 87 Migration analyses and predictions for migratory insect pests toward Japan ------------------------------------------------------------------------------ Akira Otuka 103 Recent regulations on safe plant protection materials in Taiwan ----------------------------------------------------------------------------------------- Ming-Hsun Ho 120.

(3) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. Potential application of immunoassay for the detection of pesticide ---------------------------------------------------------------------------------- Shu-Chen Chang 122 Development and utilization of plant vaccines in Japan ---------------------------------------------------------------------------------------------- Yasuhiro Tomitaka 134 Application of control-release formulation of biochemical reagent in the integrated pest control ------------------------------------------ Wei-Jyun Chien 145 Insecticide horizontal transfer from Tephritid male lures containing reduced risk pesticides ---------------------------------------------------------- Ming-Yi Chou 147 Control strategy for rice stripe virus transmitted by small brown plant hopper (Laodelphax striatellus) ----------------------------------------- Mitsuru Okuda 153 Winter climate and cultivar effects on severity of Pierce’s disease in table grapes ----------------------------------------------------------------- Lindsey P. Burbank 159 Occurrence and management of basal stalk rot of water bamboo in Taiwan ------------------------------------------------------------------------- Jin-Hsing Huang 167 Application of a bio-control agent for controlling strawberry anthracnose in Taiwan ----------------------------------------------------------- Tsung-Chun Lin 180 An hierarchical method for identifying current and emerging pest threats under climate change uncertainty ------------------------------------- Darren Kriticos 195 Integrated management strategy of pests in response to climate change - A case study of oriental fruit fly ---------------------------------------- Yu-Bing Huang 197 Pest distribution model comparisons in integrated management of key crop pests: empirical studies of Taiwan and Southeastern Asia ------------------------------------------------------------------------------------------------------------ Li-Hsin Wu 213 Introduction of a model simulation program and its application in a demonstrative expert system to predict optimal spraying time for pest: PopModel 1.5 and Pest Forecast System ------------------------------------------------ Kyung San Choi 227.

(4) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. Preface In order to respond to the impacts of climate change that has been intensifying the extreme climate, as well as serious ongoing pest and disease problems on agricultural production system, the Taiwan Agricultural Research Institute has been working with domestic and foreign agricultural research institutions on different themes over the years to reduce the impacts of such problems on the agricultural economies. In 2012, to tackle the research bottlenecks, investigated all of the programs on the management of crop pests at that time and self-assessment were launched by the Bureau of Animal and Plant Health Inspection and Quarantine (BAPHIQ) and research institutions, respectively, and new programs included those that need to introduce domestic and foreign experts or new technologies to shorten their research schedules have been followed.. In the. meantime, TARI also organized “The 2013 International Symposium on Insect Vectors and Insect-Borne Diseases” in 2013, and invited a total of 18 domestic and foreign experts from USA, Japanese, Australian and Taiwan; the lecture topics were divided into taxonomy, biology, ecology and integrated pest management. Through the scientific exchanges, introduce new technologies, mutual visits, etc., researchers in Taiwan have broadened their view and bilateral collaboration on many research items have also been initiated. This year (2018), a total of 23 domestic and foreign experts to serve as speakers, including 10 Taiwan experts, 7 Japanese experts, 4 US experts, 1 Australian expert and 1 Korean expert have participated in this symposium. The lecture topics of the 2018 International are divided into (A) "Binational collaborative achievements on agricultural pest management between Taiwan and USA" and (B) "Improving the effectiveness on the integrated pest management", which includes (1) the proactive technologies for enhancement of integrated pest management, (2) regulation and application of pesticides, (3) management strategies for important plant diseases, and (4) integrated pest management strategy with regards to climate change. We look forward to this international symposium, which like the one held in 2013, will become a discussion platform for cooperation between Taiwan and foreign scholars. We sincerely hope that all speakers and other participants can fully engage in the discussion of the specific targeted issues in these three days. Future potential cooperation issues will effectively solve the common research bottlenecks, and look forward to joining the international agricultural science and technology research projects to enhance the vision of Taiwan's i.

(5) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. agricultural science and technology research. Finally, I would like to give thanks to the Council of Agriculture for supporting this symposium. My sincere thanks also extended to the staff members of TARI for their endeavor and assistance in planning and preparing the event. I have the confidence that the outcomes of this symposium will certainly be fruitful and successful. Once again, to all the distinguished speakers and participants, welcome to Taiwan and the campus of TARI.. To every one of you, thank you for your support and for coming to this. very meaningful occasion.. Junne-Jih Chen, Ph.D. Director General Taiwan Agricultural Research Institute Council of Agriculture, Taiwan ROC September, 2018. ii.

(6) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. 序為因應全球區域經濟整合的趨勢、氣候暖化與極端氣候及關鍵病蟲害對農業的影響日益加劇，農業試驗所歷年來一直與國內外農業研究機關，就不同主題共同合作，期能降低病蟲害問題對農業生產所造成的影響。 2012 年起農委會動植物防疫檢疫局及所轄試驗研究單位，透過盤點農業有害生物研究計畫項目及研究瓶頸，啟動新的國際合作的中程議題，期望可強化台灣農業有害生物的研究基礎。為此，農業試驗所舉辦「2013 年媒介昆蟲與蟲媒病害國際研討會」，共計邀請 18 位國內外專家擔任演講者，包括澳洲專家 1 位、日本專家 1 位、美國專家 9 位與台灣專家 7 位。演講主題則可歸類為分類學、生物學、生態學與整合管理。透過這樣的互動，及後續雙方的交流互訪，大幅擴展國內研究人員的視野，也啟動與各國在各個議題的多面向的合作。今年(2018 年) 的研討會共計邀請 23 位國內外專家擔任演講者，包括台灣專家 10 位、日本專家 7 位、美國專家 4 位、澳洲專家 1 位與韓國專家 1 位參與。所有演講內容可歸類為「分享國際合作重要研究成果」和「可提升有害生物整合管理效能」兩大主軸，其中後者又包括前瞻防治技術、因應氣候變遷的蟲害整合管理策略、重要病害管理與農藥管理等四個課題。我們期待本次國際研討會，可如 2013 年的國際研討會一樣，成為台灣與國外學者合作研究的討論平台，衷心盼望所有講者與聽眾，可在這三天針對特定的目標議題，充分討論未來的潛在合作議題，有效解決彼此的研究瓶頸，並期待藉此加入國際農業科技的跨國研究項目，提升台灣農業科技研究的視野。最後，感謝農業委員會支持本次研討會，也感謝農業試驗所工作人員為規劃和籌備活動所做的努力和協助。相信本次研討會的成果肯定會取得豐碩成果。也再次向所有演講者和來賓，表達歡迎來到台灣和農業試驗所，感謝您們對此重要會議的支持。行政院農業委員會農業試驗所所長. 中華民國 108 年 9 月. iii.

(7) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. SYMPOSIUM AGENDA. Date: September 4-6, 2018 Venue: International Conference Hall, Taiwan Agricultural Research Institute (TARI), Taichung, Taiwan, ROC Sponsor: TARI, Council of Agriculture (COA), Taiwan, ROC Co-organizers: COA, Executive Yuan, Taiwan, ROC; Taiwan Entomological Society; The Plant Protection Society of Republic of China Schedule Program/ schedule Speaker (Institution) Moderator (Institution) th September 4 (Tues.) 08:30-09:20 Registration 09:20-09:50 Opening Session: Opening Remarks: Welcome Address (Dr. Junne-Jih Chen, Director-General, TARI, COA) 09:50-10:10 Tea Break and Group Photo Session 1: Binational collaborative achievements on agricultural pest management between Taiwan and USA 台美農業有害生物國際合作成果 10:10-10:30 Introduction to the 2018 Dr. Hsien-Tzung Shih Ms. Ching-Hua Kao, international (Applied Zoology Director symposium on Division, TARI, COA, (Applied Zoology proactive technologies Taiwan, ROC) Division, TARI, COA, for enhancement of Taiwan, ROC) integrated pest management on key crops 10:30-11:20 Identification of the egg Dr. Serguei V. Triapitsyn parasitoids of (Department of Auchenorrhyncha Entomology, (Hemiptera) of UC Riverside, CA, USA) economic importance in Taiwan: collaborative research between Taiwan Agricultural Research Institute and University of California at Riverside scientists 11:20-12:00 Insights into the Dr. Dong-Hong Wu biology, diversity, and (Crop Science Division, origins of weedy red TARI, COA, rice and the use of Taiwan, ROC) phylogeographical structures to control its seed-mediated contamination in Taiwan 12:00-13:10 Lunch Break iv.

(8) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. Session 2: Important, proactive and potential technologies for the enhancement of integrated pest management 提升有害生物整合管理之重要、前瞻與具應用潛力之技術 13:10-13:50 The eradication projects Dr. Tsuyoshi Ohishi Dr. Chien-Chung Chen and the preventative (Okinawa Prefectural Plant (Applied Zoology control for quarantine Protection Center, Naha, Division, TARI, COA, pests in Okinawa, Japan Okinawa, Japan) Taiwan, ROC) 13:50-14:30 Development of Dr. Rodrigo Krugner vibrational control (Crop Diseases, Pests and methods for grapevine Genetics Research Unit, pests in California San Joaquin Valley Agricultural Sciences Center, USDA-ARS, Parlier, CA, USA) 14:30-15:10 Identify key virulence Dr. Hong Lin gene as a control target (Crop Diseases, Pests and to mitigate Pierce’s Genetics Research Unit, disease of grape San Joaquin Valley Agricultural Sciences Center, USDA-ARS, Parlier, CA, USA) 15:10-15:30 Tea Break 15:30-16:10 Utilization of electric Dr. Shoji Ohga Dr. Chien-Chung Chen pulse power for (Department of Agro(Applied Zoology agricultural products environmental Sciences, Division, TARI, COA, cultivation: forest Faculty of Agriculture, Taiwan, ROC) environment control Kyushu University, Japan) 16:10-16:50 Exploitation of new Dr. Ritsuo Nishida attractants for fruit fly (Department of Applied pests of economic Life Sciences, Kyoto importance University, Japan) 16:50-17:30 Panel Discussion 1 Moderators: Dr. Chung-Jan Chang; Ms. Ching-Hua Kao, Director; Dr. Chien-Chung Chen th September 5 (Wed.) 08:30-09:00 Registration 09:00-09:40 Recent progress in Dr. Masami Shimoda Dr. Chien-Chung Chen optical control of insect (Institute of (Applied Zoology pests with light and Agrobiological Division, TARI, COA, color Sciences, NARO, Japan) Taiwan, ROC) 09:40-10:20 Migration analyses and Dr. Akira Otuka predictions for (Institute of Agricultural migratory insect pests Machinery, NARO, Japan) toward Japan 10:20-10:30 Tea Break Session 3: Regulation and application of pesticides 農藥管理與應用. v.

(9) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. 10:30-11:20. Recent regulations on safe plant protection materials in Taiwan. 11:20-12:00. Potential application of immunoassay for the detection of pesticide residues in agriculture. Dr. Ming-Hsun Ho. (Taiwan Agricultural Chemicals and Toxic Substances Research Institute, COA, Taiwan, ROC). Ms. Ching-Hua Kao, Director (Applied Zoology Division, TARI, COA, Taiwan, ROC). Ms. Shu-Chen Chang (Applied Zoology Division, TARI, COA, Taiwan, ROC) 12:00-13:10 Lunch Break 13:10-13:50 Development and Dr. Yasuhiro Tomitaka Ms. Ching-Hua Kao, utilization of plant (Kyushu Okinawa Director vaccines in Japan Agriculture Research (Applied Zoology Center, NARO, Japan) Division, TARI, COA, Taiwan, ROC) 13:50-14:30 Application of controlDr. Wei-Jyun Chien release formulation of (Pheromone Center; biochemical reagent in Department of Applied the integrated pest Chemistry, Chaoyang control University of Technology, Taiwan, ROC) 14:30-15:10 Insecticide horizontal Dr. Ming-Yi Chou transfer from Tephritid (Agricultural Extension male lures containing Center, National Chungreduced risk pesticides Hsing University) 15:10-15:20 Tea Break Session 4: Management strategies for important plant pests 重要病蟲害管理策略 15:20-16:00 Control strategy for rice Dr. Mitsuru Okuda Dr. Ruey-Jang Chang, stripe virus transmitted (Central Region Director by small brown plant Agricultural Research (Plant Pathology hopper (Laodelphax Center, NARO, Japan) Division, TARI) striatellus) 16:00-16:40 Winter climate and Dr. Lindsey P. Burbank cultivar effects on (Crop Diseases, Pests and severity of Pierce’s Genetics Research Unit, disease in table grapes San Joaquin Valley Agricultural Sciences Center, USDA-ARS, Parlier, CA, USA) 16:40-17:20 Panel Discussion 2 Moderators: Dr. Chung-Jan Chang; Ms. Ching-Hua Kao, Director; Dr. Chien-Chung Chen; Dr. Ruey-Jang Chang, Director September 6th (Thurs.) 08:30-09:00 Registration 09:00-09:40 Occurrence and Dr. Jin-Hsing Huang Dr. Ruey-Jang Chang, management of basal (Plant Pathology Division, Director TARI, COA, Taiwan, (Plant Pathology vi.

(10) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. 09:40-10:20. stalk rot of water bamboo in Taiwan Application of a biocontrol agent for controlling strawberry anthracnose in Taiwan. ROC). Division, TARI). Dr. Tsung-Chun Lin (Plant Pathology Division, TARI, COA, Taiwan, ROC) 10:20-10:30 Tea Break Session 5: Integrated pest management strategy with regards to climate change 因應氣候變遷之蟲害整合管理策略 10:30-11:20 An hierarchical method Dr. Darren Kriticos Dr. Chung-Jan Chang for identifying current (Commonwealth Scientific (University of and emerging pest and Industrial Research Georgia, USA) threats under climate Organisation (CSIRO); change uncertainty University of Queensland, Australia) 11:20-12:00 Integrated management Dr. Yu-Bing Huang strategy of pests in (Applied Zoology response to climate Division, TARI, COA, change - A case study Taiwan, ROC) of oriental fruit fly 12:00-13:10 Lunch Break 13:10-13:50 Pest distribution model Dr. Li-Hsin Wu Dr. Chung-Jan Chang comparisons in (National Pingtung (University of integrated management University of Science and Georgia, USA) of key crop pests: Technology, Taiwan, empirical studies of ROC) Taiwan and Southeastern Asia 13:50-14:30 Introduction of a model Dr. Kyung San Choi simulation program and (Rural Development its application in a Administration, National demonstrative expert Institute of Horticultural system to predict and Herbal Sciences, optimal spraying time Research Institute of for pest: PopModel1.5 Climate Change and and Pest Forecast Agriculture, South Korea) System 14:30-15:00 Panel Discussion 3 Moderators: Dr. Chung-Jan Chang; Ms. Ching-Hua Kao, Director; Dr. Chien-Chung Chen; Dr. Ruey-Jang Chang, Director 15:00-15:20 Tea Break 15:20-16:30 Discussion on the international research collaboration among Taiwan, USA, Japan, South Korea and Australia Moderators: Dr. Chung-Jan Chang; Ms. Ching-Hua Kao, Director; Dr. Chien-Chung Chen; Dr. Ruey-Jang Chang, Director. vii.

(11) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. Introduction to the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops Hsien-Tzung Shih 1, 2, Yu-Bing Huang 1, Ming-Yaw Chiang 1, and Ching-Hua Kao 1 1. Applied Zoology Division, Taiwan Agricultural Research Institute, Council of Agriculture, Executive Yuan, Taichung, Taiwan, ROC. 2. Corresponding author, e-mail: [email protected]. ABSTRACT The 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management on Key Crops, including "Binational collaborative achievements on agricultural pest management between Taiwan and USA" and "Improving the effectiveness on the integrated pest management", which includes the proactive technologies for enhancement of integrated pest management, regulation and application of pesticides, management strategies for important plant diseases, and integrated pest management strategy with regards to climate change. We invited 22 experts from Taiwan, Australia, the United States, Japan and South Korea to be our symposium speakers. The sponsors sincerely hope that the symposium will not only provide proactive technologies or innovative pest management strategies for Republic of China, but also serve as a platform for future cooperation between domestic and foreign scholars, which can make a significant contribution to the advancement of Taiwan and global agriculture. Keywords: agriculture, international cooperation, integrated pest management, proactive technology Taiwan is located in eastern Asia and is one of the many islands in the East and Southeast Asia island arcs. It covers an area of 36,000 square kilometers and is the 38th largest island in the world. Nearly 70% of the area is mountainous and hilly. The topography and altitude on the western coast vary greatly. Due to the fact that the Tropic of Cancer runs through the middle of Taiwan, the climate of Taiwan covers the tropical and subtropical zones. The north of the Tropic of Cancer is the subtropical monsoon climate and the south is the tropical monsoon. 1.

(12) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. climate. The population of Taiwan has exceeded 23.57 million in May 2018. Based on the gross domestic product (GDP) report released by the International Monetary Fund (IMF) in 2013, Taiwan was the 27th largest in the global economy. Taiwan’s economic structure has been shifted to high-tech industries, which replaced labor-intensive industries e.g., plastic products manufacturing, textile, and garment industry, etc., while the proportion of agriculture in GDP fell from 35% in 1952 to 2%. Although the proportion of agriculture industry has decreased, the deep foundation in science education in the past has enabled Taiwan's agriculture to quickly integrate crossdomain technology when faced with man-made and natural disadvantages. That surely provides a great opportunity to promote and make agriculture an important industry again to Taiwan. In order to respond to the impacts on the global and regional economic integration due to climate change and the intensification of extreme climate, and the aging of rural employment in Taiwan, the Taiwan Agricultural Research Institute (TARI) has been working with domestic and foreign agricultural research institutions on different themes over the years to reduce the impacts of such problems on the agricultural economies. Using the various themes of this 2018 international symposium as an example, it can be traced back to 2012 when Mr. Bao-Liang Chen, the then chief executive of the Animal and Plant Health Inspection and Quarantine Promotion Group in the International Collaboration Field in the Council of Agriculture, Executive Yuan of ROC, entrusted the Taiwan Agricultural Experimental Institute to consult with different agricultural institutes of COA to tackle the research bottlenecks with selfassessment after he has investigated all of the programs on the mnagement of crop pests. The proposed programs included those that need to introduce domestic and foreign experts or new technologies to shorten their research schedules. It is clearly illustrated in the themes of this symposium that fits the purpose of proposed program introducing foreign experts and technologies, which can be used as the basis for handling international cooperation plans. Therefore, in 2012, we have prioritized five issues as a medium-term plan for international cooperation, including "Insect vectors and insect-borne diseases", "Integrated pest management strategy with regards to climate change", "Proactive technologies for enhancement of integrated pest management", "Regulation and application of pesticides" and "Establish an information platform for transnational and inter-disciplinary pest management and natural enemy applications". Based on the above-metioned five issues, we expect to strengthen the research base of agricultural pests in Taiwan. Afterward, through the program. 2.

(13) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. review, researchers from the different institutes of COA would be sent to the United States, Australia, Japan and other countries for short-term studies ranging from 2 weeks to 2 months, with that we traced the cooperation effects between Taiwan researchers and foreign experts. Besides, we will establish a list of foreign experts as potential international partners in the research of integrated pest management in Taiwan based on the recommendations from the above researchers or other domestic experts. Some experts will be invited to serve as lecturers for specific technologies, and some of them conduct cooperative research through bilateral scientific and technological exchange programs signed by Taiwan and foreign countries, and in the meantime we also organized “The 2013 International Symposium on Insect Vectors and Insect-Borne Diseases” and “2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management on Key Crops” in 2013 and 2018, respectively, by inviting specific domestic and foreign experts. In the 2013 symposium, we invited a total of 18 domestic and foreign experts to serve as speakers, including 7 Taiwan experts, 11 US experts and 1 Australian expert. This year (2018), a total of 23 domestic and foreign experts to serve as speakers, including 10 Taiwan experts, 7 Japanese experts, 4 US experts, 1 Australian expert and 1 Korean expert. We look forward to this international symposium, which like the one held in 2013, will become a discussion platform for cooperation between Taiwan and foreign scholars. We sincerely hope that all speakers and other participants can fully engage in the discussion of the specific targeted issues in these three days. Future potential cooperation issues will effectively solve the common research bottlenecks, and look forward to joining the international agricultural science and technology research projects to enhance the vision of Taiwan's agricultural science and technology research.. 3.

(14) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. Identification of the Egg Parasitoids of Auchenorrhyncha (Hemiptera) of Economic Importance in Taiwan: Collaborative Research between Taiwan Agricultural Research Institute and University of California at Riverside Scientists Serguei Vladimirovich Triapitsyn 1, 4, Hsien-Tzung Shih 2, 5, and Shou-Horng Huang 3 1. Entomology Research Museum, Department of Entomology, University of California, Riverside, CA, 92521, USA. 2. Applied Zoology Division, Taiwan Agricultural Research Institute, Council of Agriculture, Executive Yuan, 189 Chung-Cheng Road, Wufeng, Taichung, 41362, Taiwan, ROC. 3. Department of Plant Protection, Chiayi Agricultural Experiment Station, Taiwan Agricultural Research Institute, 2 Minquan Road, Chiayi, 60044, Taiwan, ROC. 4, 5. Corresponding authors, e-mail: [email protected] ; [email protected]. ABSTRACT An overview of the three collaborative projects between Taiwan Agricultural Research Institute (TARI), Taiwan, ROC, and University of California at Riverside, USA, scientists is given, as follows: 1) collecting (H.-T. Shih), rearing (S.-H. Huang), and identification (S. V. Triapitsyn) of the egg parasitoids (Hymenoptera: Mymaridae and Trichogrammatidae) of rice leafhoppers and planthoppers (Hemiptera: Cicadellidae and Delphacidae) of economic importance in west central Taiwan; 2) rearing (H.-T. Shih) and identification (S. V. Triapitsyn) of the egg parasitoids (Mymaridae and Trichogrammatidae) of the leafhopper Kolla paulula (Walker) (Cicadellidae), vector of the phytopathogenic bacterium Xylella fastidiosa; and 3) a preliminary study of the biodiversity and taxonomy of Mymaridae in Taiwan (S. V. Triapitsyn) based largely on the specimens in the insect collection of TARI. Keywords: rice pests, Cicadellidae, Delphacidae, Kolla paulula, vector, Mymaridae, Trichogrammatidae, egg parasitoid, biological control, biodiversity, taxonomy, Taiwan INTRODUCTION Since 2013, scientists from the Taiwan Agricultural Research Institute (TARI), Wufeng, Taichung, Taiwan, ROC (H.-T. Shih) and the Entomology Research Museum, University of. 4.

(15) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. California, Riverside, California, USA (S. V. Triapitsyn) have collaborated on the three research projects which are important for applied entomology in Taiwan, particularly for biological control of some key agricultural pests belonging to Auchenorrhyncha (Hemiptera). Several years later, S.-H. Huang (Chiayi Agricultural Experiment Station, TARI) joined the effort on one of these projects, rearing egg parasitoids of rice leafhoppers and planthoppers in Chiayi and Yunlin counties of Taiwan. As outlined by Triapitsyn. (15). , the most common egg parasitoids of Auchenorrhyncha. belong to two families of Hymenoptera, Mymaridae and Trichogrammatidae of the superfamily Chalcidoidea. Worldwide, they are largely responsible for the natural control of leafhopper (Cicadellidae), planthopper (Delphacidae), and treehopper (Membracidae) species, including some economically important pests. Therefore, knowledge of their taxonomy (for correct identification) and biology is very important for biological control, ecological, and biodiversity studies. Triapitsyn. (15). also provided an overview of the history and current status of the. taxonomy and biology of these two groups of egg parasitoids in Taiwan. COLLABORATIVE PROJECTS 1. Collecting, rearing, and identification of egg parasitoids of rice leafhoppers and planthoppers of economic importance in west central Taiwan Project rationale. Recently, Triapitsyn (20) gave a critical analysis of the history of prior identifications of the egg parasitoids (Mymaridae only) of rice leafhoppers and planthoppers in Taiwan. Chu and Hirashima. (3). summarized the earlier Taiwanese literature on the natural. enemies of rice leafhoppers and planthoppers, while Hirashima (5) provided information on their survey in Taiwan. Lin (6) and Chen (1) also reported on the egg parasitoids of rice leafhoppers and planthoppers in Taiwan, while Chen and Yu (2) studied Anagrus Haliday egg parasitoids of brown rice planthopper, Nilaparvata lugens (Stål) (Delphacidae). Unfortunately, almost no voucher specimens from these earlier studies in Taiwan could be found in the museum collections either there (including that of TARI) or in Japan very few exceptions. (20). , so it was impossible, with a. (20). , to verify their identity with confidence; it seems likely that most of. them were misidentified at species level (20). Therefore, we decided to conduct a new survey of egg parasitoids of rice leafhoppers and planthoppers in west central Taiwan (Taichung as well as Chiayi and Yunlin counties) with the aim of identifying them properly. The latter, however, has proven to be not a small task by itself as a lot of confusion exists in Asia (in the Oriental. 5.

(16) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. region and southern part of the eastern Palaearctic region) in regard of their identification. For instance, without providing much of critical analysis, Gurr et al. (4) summarized many published records of parasitoids of Asian planthopper pests of rice; among the mymarid egg parasitoids they included both valid species and, separately, their several current synonyms, as well as some obvious misidentifications, species of unknown identity such as Gonatocerus longicrus (Kieffer), and a genus which is not known to have species that parasitize eggs of either leafhoppers or planthoppers (Anaphes spp.). Specimen collection and preparation. During 2015 and 2016, egg parasitoids of selected species of rice pests belonging to the Auchenorrhyncha were reared in Chiayi and Yunlin counties by S.-H. Huang by exposing their sentinel eggs in rice plants in pesticide-free rice fields. For obtaining sentinel eggs, 30-day-old rice plants were used; each pot contained 3 to 5 tillers. Five gravid female adults each of the green rice leafhopper Nephotettix cincticeps (Uhler) (Cicadellidae) or the planthoppers (Delphacidae) Laodelphax striatella (Fallén) (small brown planthopper), Nilaparvata lugens (Stål) (brown planthopper), and Sogatella furcifera (Horváth) (whitebacked planthopper) were released into caged pots with rice plants for oviposition. The host leafhoppers or planthoppers were removed from the cages after 24 hours, and the pots with their sentinel eggs were taken to the rice fields and exposed there for parasitization for 48 hours. Then the rice plants with both unparasitized (Fig. 1) and parasitized (Fig. 2) eggs were taken back to the laboratory. The tillers with host eggs were transferred to vials lined with a moistened filter paper to avoid desiccation. The parasitized host eggs turned reddish (Fig. 2). The emerging parasitoids were collected daily, labeled, and placed in 95% ethanol for storage at -20°C until shipped to H.-T. Shih and/or S. V. Triapitsyn for identification and record keeping. In Taichung, egg parasitoids of rice leafhoppers and planthoppers were collected using a Malaise trap (Fig. 11) and yellow pan traps in an experimental organic rice field at TARI, Wufeng, during S. V. Triapitsyn’s visit in October 2016. Thereafter several Malaise traps were installed in rice fields in Taichung by H.-T. Shih and M.-R. Tzeng, who collected and processed the samples. The obtained data will be used for both parasitoid identification and for obtaining information on their species composition, abundance, and population dynamics. These will be reported elsewhere in a forthcoming joint publication to be submitted to the Journal of Taiwan Agricultural Research.. 6.

(17) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. Most of the collected or reared specimens were identified directly in ethanol. Selected specimens were dried from ethanol using a critical point drier, point-mounted, and labeled; these were then sorted to morphospecies, and some of the specimens were slide-mounted by Vladimir V. Berezovskiy. Both ethanol-preserved, pointed- and slide-mounted voucher specimens were deposited in the insect collection of TARI and the Entomology Research Museum, University of California, Riverside, California, USA. Specimen identification. The most common and abundant parasitoid reared from sentinel eggs of all four aforementioned host species (one leafhopper and three planthoppers) was Anagrus nilaparvatae Pang and Wang (Mymaridae) (Figs 3, 4), both in Chiayi and Yunlin counties of Taiwan. Anagrus nilaparvatae was originally described from Wushan (Fuoshan), Guangdong, China, as an egg parasitoid of brown planthopper Nilaparvata lugens then it was reported, in numerous publications partially summarized by Gurr et al.. (7). . Since. (4). , from. many countries in the Oriental and eastern Palaearctic regions as the main egg parasitoid of several economically important leafhoppers and planthoppers in rice field agroecosystems. As noted by Triapitsyn and Berezovskiy (22) and Triapitsyn (15), A. nilaparvatae is morphologically practically indistinguishable from the common, widespread, polyphagous Palaearctic species A. incarnatosimilis Soyka (as A. incarnatus Haliday). Its proper taxonomic identity was recently figured out as part of this project. (23). using both morphometric analysis and genetic. studies. The second most common egg parasitoid of rice leafhoppers in Chiayi and Yunlin counties of Taiwan was Mymar taprobanicum Ward (Mymaridae), a rather common and almost cosmopolitan species. Illustrated here is a female of M. taprobanicum (Fig. 5) reared from eggs of green rice leafhopper Nephotettix cincticeps. Also reared in west central Taiwan were a few specimens of Gonatocerus aegyptiacus Soyka (Mymaridae) (Fig. 6) from eggs of Nephotettix cincticeps and Oligosita sp. (Trichogrammatidae) (Fig. 7) from eggs of small brown planthopper Laodelphax striatella. In the Malaise trap installed in the rice field at TARI, also collected were the rice green leafhopper Nephotettix nigropictus (Stål) and the zig-zag leafhopper Maiestas dorsalis (Motschulsky) (Cicadellidae) (identifications by S. V. Triapitsyn). The known egg parasitoid Pseudoligosita nephotetticum (Mani) (Trichogrammatidae) (Fig. 8) was collected there in yellow pan traps but not in the Malaise trap standing next to them, whereas Anagrus nilaparvatae was collected in the same location in both types of traps.. 7.

(18) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. 2. Rearing and identification of egg parasitoids of the leafhopper Kolla paulula (Walker), vector of Xylella fastidiosa In Taiwan, the cicadelline (Cicadellidae: Cicadellinae: Cicadellini) leafhopper Kolla paulula (Walker) is a known vector of the phytopathogenic bacterium Xylella fastidiosa (8), the causative agent of Pierce's disease of grapes and similar diseases of other affected plants, and thus of particular economic importance. Two species of parasitoids were reared by W.-F. Hung and H.-T. Shih from its eggs in plant tissue of spreading dayflower, Commelina diffusa (Commelinaceae), and then identified by S. V. Triapitsyn as Pseudoligosita nephotetticum (Mani) (Trichogrammatidae) (Fig. 9) and one male of Cosmocomoidea sp. (Mymaridae) (Fig. 10) [as Gonatocerus (Cosmocomoidea) sp.] (24). Pseudoligosita nephotetticum was redescribed and illustrated; also provided was a summary of the known records of egg parasitoids (Mymaridae and Trichogrammatidae) of other leafhoppers from the tribe Cicadellini in the entire world (24). 3. A preliminary study of the diversity and taxonomy of Mymaridae in Taiwan General information. Biogeographically, the fairyfly (Mymaridae) fauna of Taiwan is primarily Oriental, although at high altitudes it fits more that of the Palaearctic ecozone. While generic identifications of most Mymaridae in the region are generally relatively easily available, species identifications are still a major problem. Expensive and time-consuming special preservation and mounting techniques, such as critical point drying from ethanol and making microscopic slides in Canada balsam, are usually required to be able to identify most mymarids to species based on morphology. Overall, prior to this study, taxonomic reports on the diversity of Mymaridae in Taiwan were scarce and either included some random identifications of the Taiwanese specimens as parts of broader generic revisions or those of specimens of interest to biological control projects, mainly of egg parasitoids of rice pests. Keys and taxonomic revisions of importance. Keys and taxonomic revisions that include Taiwanese specimens of certain fairyfly genera are unfortunately few, but some can be helpful to recognize some species: Taguchi. (9, 10, 11, 12, 13). for a number of genera, Triapitsyn. (16). for. Nepolynema Triapitsyn, Triapitsyn (17) for Himopolynema Taguchi (a revision of the Taiwanese species with descriptions of several new taxa), Triapitsyn. 8. (18). for Arescon Walker, Triapitsyn.

(19) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. (19). for Alaptus Westwood, Triapitsyn et al. (21) for Zeyanus Huber, Triapitsyn and Berezovskiy. (22). for Anagrus Haliday, etc. Recent achievements. Triapitsyn (20) just published an annotated checklist of Mymaridae. of Taiwan, which includes records of 28 genera and 60 named species. Of these, 13 genera and 33 species were newly recorded from Taiwan, including 5 new species described. Information on their distribution and available host records was also provided, along with illustrations of some species and keys to several genera. In addition, a number of the undescribed species were identified in the course of this study; these await thorough taxonomic revisions of the genera to which they belong. The previous published records of mymarid egg parasitoids of rice leafhoppers and planthoppers in Taiwan were critically analyzed. This checklist was based largely on the collection of Mymaridae in TARI, almost all mounted on individual microscopic slides, captured mostly by sweeping during the 1950s1970s by Kwei-Shui Lin (1921-2002), a taxonomist and prolific collector of parasitic Hymenoptera, who worked at TARI in Taipei City before moving to Taichung. He collected almost 3,000 specimens of fairyflies throughout Taiwan (the bulk from Taipei City and its environs). These were examined and identified by S. V. Triapitsyn mostly during visits to TARI in August 2013 and October 2016. Tian et al.. (14). reported a surprisingly low generic diversity index for the Mymaridae of. Taiwan which they suggested, along with Tibet’s, to be significantly lower than that for Fujian, China. However, Triapitsyn. (20). demonstrated that to be a misleading conclusion because the. mymarid fauna of Taiwan was at that time too poorly known. One would expect, due to the large size of the island, diversity of its habitats, and relative proximity to Fujian, a greater fairyfly diversity than reported, along with some possible endemism (particularly in the mountains). Thus, the mymarid fauna of Taiwan could likely be almost as diverse as that of Fujian. Looking ahead. Clearly, what is now known about biodiversity and taxonomy of Mymaridae in Taiwan, as summarized recently by Triapitsyn. (20). , is not enough, primarily. because of the lack of systematic collecting efforts of micro-Hymenoptera throughout Taiwan Island and in the surrounding smaller islands using both various modern trapping methods and rearings from known hosts. Likewise, there hasn’t been any significant effort to sort, dry, mount, label, and identify any fairyflies from the numerous existing bulk alcohol samples, primarily those from Malaise traps, in any major Taiwanese collections of insects. Thus, more. 9.

(20) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. species are expected to be discovered there once such efforts take place sometimes in the future, provided interest, taxonomic expertise, and appropriate funding become available. As noted by Triapitsyn. (20). , at least 5 more genera of Mymaridae are likely to occur in. Taiwan, besides those included in that checklist. Indeed, after it was accepted for publication and it was too late to add any taxa to it, one more genus, Dorya Noyes and Valentine, was found in Taiwan (John T. Huber, personal communication, material in the Canadian National Collection of Insects, Arachnids and Nematodes, Ottawa, Ontario, Canada). Thus, once all or almost all the genera are found and properly recorded from there, the next step would be to compile a key to both sexes of the genera occurring in Taiwan and to identify (and describe, if necessary) species in each genus. The latter, however, may require revising at least the Oriental species of some genera. ACKNOWLEDGMENTS We thank Mr. Vladimir V. Berezovskiy (UCRC) for mounting specimens, Ms. Mei-Rong Tzeng (TARI) for processing Malaise trap samples, Dr. John T. Huber (Canadian National Collection of Insects, Arachnids and Nematodes, Ottawa, Ontario, Canada) for sharing valuable information, and Dr. Chi-Feng Lee for access to the mymarid collection of TARI. LITERATURE CITED 1. Chen, B. H. 1994(1993). Occurrence and preference of Anagrus incarnatus Haliday (Hymenoptera: Mymaridae) on eggs of two rice planthoppers in Taiwan. Plant Prot. Bull. 35:267-275. 2. Chen, B.-h., and Yu, J.-z. 1989. Anagrus incarnatus Haliday, a new record from eggs of brown planthopper in Taiwan. J. Agric. Res. China 38:458-462. 3. Chu, Y.I., and Hirashima, Y. 1981. Survey of Taiwanese literature on the natural enemies of rice leafhoppers and planthoppers. Esakia 16:33-37. 4. Gurr, G. M., Liu, J., Read, D. M. Y., Catindig, J. L. A., Cheng, J. A., Lan, L. P., and Heong, K. L. 2011. Parasitoids of Asian rice planthopper (Hemiptera: Delphacidae) pests and prospects for enhancing biological control by ecological engineering. Ann. Appl. Biol. 158:149-176.. 10.

(21) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. 5. Hirashima, Y. 1981. Field studies on the biological control of leafhoppers and planthoppers (Hemiptera: Homoptera) injurious to rice plants in South-East Asia. An account for the year 1979. Esakia 16:1-4. 6. Lin, K. S. 1974. Notes on some natural enemies of Nephotettix cincticeps (Uhler) and Nilaparvata lugens (Stal) in Taiwan. J. Taiwan Agric. Res. 23:91-115. (In Chinese with English summary) 7. Pang, X., and Wang, Y. 1985. New species of Anagrus from south China (Hymenoptera : Mymaridae). Entomotaxonomia 7:175-184. 8. Su, C. C., Shih, H. T., Lin, Y. S., Su, W. Y., and Kao, C. W. 2011. Current status of Pierce's disease of grape and its vector in Taiwan. Pages 25-50 in: Proceedings of the Symposium on Integrated Management Technology of Insect Vectors and Insect- borne Diseases. Special Publication of TARI No. 152. Taiwan Agricultural Research Institute, Bureau of Animal and Plant Health Inspection and Quarantine, H. T. Shih, and C. J. Chang eds. (In Chinese with English abstract) 9. Taguchi, H. 1974. Records of two Mymar species from Japan and Taiwan (Hymenoptera: Mymaridae). Trans. Shikoku Entomol. Soc. 12:22. 10. Taguchi, H. 1975. Two new Chaetomymar species from Japan and Taiwan (Hymenoptera: Mymaridae). Trans. Shikoku Entomol. Soc. 12:111-114. 11. Taguchi, H. 1977a. A new genus belonging to the tribe Mymarini from Japan, Taiwan and Malaysia (Hymenoptera: Mymaridae). Trans. Shikoku Entomol. Soc. 13:137-142. 12. Taguchi, H. 1977b. Two new species of the genus Camptoptera from Taiwan (Hymenoptera: Mymaridae). Trans. Shikoku Entomol. Soc. 13:143-146. 13. Taguchi, H. 1978. A new species of the genus Stephanodes from Japan and Taiwan (Hymenoptera: Mymaridae). Trans. Shikoku Entomol. Soc. 14:73-76. 14. Tian, H.-x., Lin, N.-q., and Lin, J. 2006. Preliminary analysis of generic diversity of Trichogrammatidae and Mymaridae from 10 provinces of China. J. Fujian Agric. For. Univ. (Nat. Sci. Ed.) 35:480-485. 15. Triapitsyn, S. V. 2013. Taxonomy and biology of egg parasitoids of Auchenorrhyncha of economic importance in Taiwan and adjacent countries, and of proconiine sharpshooters in. 11.

(22) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. the New World. p. 123-144. In: C.-J. Chang, C.-Y. Lee, and H.-T. Shih [eds], Proceedings of the 2013 International Symposium on Insect Vectors and Insect-Borne Diseases, Taichung, Taiwan, 6-8 August 2013 Special Publication of TARI No. 173, Council of Agiculture, Executive Yuan, Taiwan Agricultural Research Institute, Bureau of Animal and Plant Health Inspection and Quarantine. 16. Triapitsyn, S. V. 2014. Nepolynema, a new genus of Mymaridae (Hymenoptera: Chalcidoidea), and its two new species from Costa Rica and Papua New Guinea. Proc. Russian Entomol. Soc. 85:170-182. 17. Triapitsyn, S. V. 2015. The genus Himopolynema (Hymenoptera: Mymaridae) in Taiwan and taxonomic comments on some extralimital species. Formosan Entomol. 35:79-116. 18. Triapitsyn, S. V. 2016. Review of the Oriental species of the genus Arescon Walker, 1846 (Hymenoptera: Mymaridae). Euroasian Entomol. J. 15:137-151. 19. Triapitsyn, S. V. 2017. Revision of Alaptus (Hymenoptera: Mymaridae) in the Holarctic region, with taxonomic notes on some extralimital species. Zootaxa 4279:1-92. 20. Triapitsyn, S. V. 2018. An annotated checklist of Mymaridae (Hymenoptera: Chalcidoidea) in Taiwan, with descriptions of five new species. J. Taiwan Agr. Res. 67:113165. 21. Triapitsyn, S. V., Aishan, Z., and Hu, H.-y. 2017. Descriptions of two new species of Zeyanus Huber (Hymenoptera: Mymaridae), with notes on some other congeneric taxa from the Oriental part of China. Oriental Insects 51:145-159. 22. Triapitsyn, S. V., and Berezovskiy, V. V. 2004. Review of the genus Anagrus Haliday, 1833 (Hymenoptera: Mymaridae) in Russia, with notes on some extralimital species. Far East. Entomol. 139:1-36. 23. Triapitsyn, S. V., Rugman-Jones, P. F., Tretiakov, P. S., Shih, H.-T., and Huang, S.-H. Untangling the Anagrus incarnatus Haliday species complex (Hymenoptera: Mymaridae): genetic data corroborate conspecificity of several morphologically similar nominal species from the Holarctic region and a common egg parasitoid of the economically important leafhopper and planthopper (Hemiptera: Cicadellidae and Delphacidae) pests of rice in Asia. J. Nat. Hist., in review.. 12.

(23) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. 24. Triapitsyn, S. V., and Shih, H.-T. 2014. Egg parasitoids (Hymenoptera: Mymaridae and Trichogrammatidae) of Kolla paulula (Walker) (Hemiptera: Cicadellidae) in Taiwan. J. Asia-Pacific Entomol. 17:673-678.. 13.

(24) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. Fig. 1. Unparasitized eggs of brown Fig. 2. Eggs of brown planthopper, planthopper Nilaparvata lugens (Taiwan). Nilaparvata lugens, parasitized by Anagrus nilaparvatae (Taiwan).. Fig. 3. Female of Anagrus nilaparvatae,. Fig. 4. Male of Anagrus nilaparvatae,. egg parasitoid of brown planthopper. egg parasitoid of brown planthopper. Nilaparvata lugens (Lucao, Taiwan).. Nilaparvata lugens (Lucao, Taiwan).. Fig. 5. Female of Mymar taprobanicum,. Fig. 6. Female of Gonatocerus. egg parasitoid of green rice leafhopper. aegyptiacus, egg parasitoid of green rice. Nephotettix cincticeps (Gukeng, Taiwan). leafhopper Nephotettix cincticeps (Gukeng, Taiwan).. 14.

(25) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. Fig. 7. Male of Oligosita sp., egg. Fig. 8. Female of Pseudoligosita. parasitoid of small brown planthopper. nephotetticum (rice field, TARI, Wufeng,. Laodelphax striatella (Gukeng,. Taichung, Taiwan).. Taiwan).. Fig. 9. Female of Pseudoligosita. Fig. 10. Male of Cosmocomoidea sp., egg. nephotetticum, egg parasitoid of Kolla. parasitoid of Kolla paulula (Wufeng,. paulula (Wufeng, Taichung, Taiwan).. Taichung, Taiwan).. 15.

(26) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. Fig. 11. A Malaise trap in the experimental organic rice field (TARI, Wufeng, Taichung, Taiwan).. 16.

(27) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. Insights into the Biology, Diversity, and Origins of Weedy Red Rice and the Use of Phylogeographical Structures to Control its Seed-mediated Contamination in Taiwan Dong-Hong Wu 1, 4, David Gealy 2, Yi-Chien Wu 3, Melissa Jia 2, Jeremy D. Edwards 2, Ming-Hsin Lai 1, and Anna McClung 2 1. Crop Science Division, Taiwan Agricultural Research Institute, Council of Agriculture (COA), Taiwan, ROC. 2. Dale Bumpers National Rice Research Center, US Department of Agriculture - Agricultural Research Service, Stuttgart, Arkansas, USA. 3. Taichung District Agricultural Research and Extension Station, COA, Taiwan, ROC. 4. Corresponding author, e-mail: [email protected]. ABSTRACT Weedy red rice (WRR) possesses traits, including seed dormancy and shattering, that facilitate its infestation in rice paddies from one crop season to the next. These plants are not only the potential source of pollen-mediated gene flow and hosts for diseases or other pests, but also are competitors for fertilizer due to their vigorous growth. In addition to increased production costs to control this weed, the red pericarp and undesirable eating qualities of WRR lead to reduced product value, consequently putting production constraints on the global rice industry. In rice cultivation regions world-wide, the rice industry is in search of effective ways to control WRR. The rice production system in Taiwan relies on transplanting which is recommended for effective control of weeds in rice fields during the seedling stage. However, the infestation of WRR in rice paddies has become increasingly severe in the past few years in Taiwan. Although WRR occurs at a rate of only 0.5 to 1% in contaminated paddies, it can be spread easily through use of shared field equipment among rice fields. Ratoon cropping or tillage immediately after harvest increases the population densities of WRR, resulting in future yield losses. Effective control strategies for WRR should meet the balance between economic benefit, efficiency, and feasibility. The recommended WRR control measures under a transplanting system begin with irrigating the paddy field after harvest to induce the sprouting of shattered seed, followed by plowing the WRR seedlings into the land. Herbicide is then. 17.

(28) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. applied three times in succession every seven days to kill emerging WRR and to field infestations. The final step is the manual removal of the remaining off-type plants of WRR. Keywords: weedy red rice, seed shattering, seed dormancy, transplanting system, control strategy INTRODUCTION Weeds, soil fertility, availability of fertilizers, and variable climates are the major factors that limit rice growth. Weedy red rice (WRR) and cultivated rice are classified under the same genus and species (Oryza sativa L.) and have similar appearance and features; moreover, WRR plants in Taiwan are typically short, making them difficult to distinguish from crop rice, and exhibit rapid growth and high levels of seed shattering and dormancy, all of which are traits that make them invasive weeds. Consequently, once WRR forms a stable population in cultivated fields, controlling it and tracking its distribution patterns become difficult. (29). . The. hazards that WRR causes are detailed as follows: (1) Because of high levels of seed shattering and dormancy, seeds become established readily in the soil seed bank, resulting in plants that become a medium for gene flow as well as pest and disease transmission; (2) The biomass growth advantage of WRR from seedling to maturity leads to nutrient competition; (3) WRR exhibits negative qualities such as a red pericarp and undesirable cooked texture. All of these hazards lead to a sharp rise in rice production costs and decline in the commercial value of cultivated rice, hindering the development of the global rice industry. Hence, governments worldwide have actively searched for solutions to the hazards of WRR (4). In addition, WRR has been an obstacle in the development of rice industries worldwide (3, 16, 29). . The invasion of WRR has been particularly problematic in Brazil, South Korea, and the. United States of America (USA), where various WRR biotypes are present and rice planting is generally mechanized. (9, 15, 25). . WRR has reduced rice production in some countries by 10%–. 50% and prevented subsequent rice planting in some cultivated fields; a density of 35–40 WRR plants per m2 hampers the production of tall varieties of rice by 60% and that of dwarf varieties by as much as 90% (22). In Japan, where a transplant system is implemented, a WRR density of 5 WRR plants per m2 reduces rice production by 10% (20). Furthermore, reduced rice production caused by 1–3 WWR plants is equivalent to that of 5–10 plants of barnyardgrass (Echinochloa crus-galli). WRR outweighs barnyardgrass in its damage to rice production and is difficult to contain because its appearance is so similar to that of cultivated rice (21).. 18.

(29) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. To effectively prevent the invasion, latency, and spread of WRR as well as reinforce the knowledge of rice farmers regarding its detriment to rice industries, this study described the morphological diversity and phylogeographical structures of WRR, and generated control strategies for farmers to reference. High Morphological Diversity and Adaptability of WRR WRR is notorious for its high morphological diversity and environmental adaptability. In the Japonica rice production zones in Italy, WRR is divided into three variants, namely the long-awned, short-awned, and awnless strains. Long-awned WRR has the longest flag leaves and grains of the three variants; short-awned WRR produces small seeds and exhibits low germination rates; and awnless WRR has wide grains and high germination rates after 30 days of maturity. In particular, long-awned WRR displays the highest morphological diversity and environmental adaptability of all three variants. (8). . The WRR in the southern USA has two. major variants, namely the strawhull awnless and blackhull awned strains. Strawhull awnless WRR features earlier heading dates than those of cultivated rice, whereas blackhull awnless WRR exhibits later heading dates than those of cultivated rice; both strains have a greater plant height than cultivated rice. In addition to hull color and awn length diversity, the characteristics of the WRR plants vary between strains. The WRR plants having a dense plant architecture and long awns have been noted for their high germination rates and seed vitality, whereas those with a loose plant architecture and no awns were noted for high tolerance to salt (23). In the Indica rice production zones in Thailand, the early generations of WRR were categorized as a mixture between the cultivated crop and weedy biotypes according to the WRR morphology inspection in multiple regions in 2005–2009 (27). This may have been caused by crossbreeding between the two biotypes. (17, 18). ; following the accumulation of invading generations, WRR. gradually became identical to cultivated Indica rice in appearance. Nevertheless, regardless of its generations and regions, WRR exhibits high adaptability to various cultivation methods employed in rice fields because of its early maturity, high levels of seed shattering, and robust productivity (27). In 2016 Cheng et al. (4) compared the morphological diversity of 521 locally collected WRR strains with that of Indica and Japonica rice and previously obtained red rice germplasm collections. The results indicated that all 521 WRR plants exhibited earlier maturity, greater seed shattering, more tillers, and shorter plant heights than cultivated rice plants; furthermore, pericarps were consistently red (Fig. 1). In a follow-up principal component analysis, the WRR populations exhibited similar degrees of dispersion with those of the. 19.

(30) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. cultivated rice; their geographic distributions were similar, but the grains of the WRR populations were identical in appearance to the wide and short grains of the early Indica crop rice varieties, and profoundly different from the slender grains of recent Indica varieties and the short and round grains of Japonica varieties. It is speculated that the grain traits of off-type plants were not influenced by human selection when these plants were eradicated intensively from rice nurseries. This indicated that the WRR collections are closely associated with the early rice strains. Divided Arguments Worldwide on the Origins and Evolution Mechanisms of WRR The genetic backgrounds of WRR vary considerably between countries, and arguments regarding its origins remain divided among scientific disciplines; however, the various hypotheses pertaining to the evolutionary methods of WRR have been supported by different studies. (7). . According to De-Wet and Harlan (6), WRR originated from the adaptation of wild. rice to agricultural habitats. In environments where no native wild rice biotypes are present, these can be introduced as a result of seed movement through trade and other means. For example, the WRR in Brazil is hypothesized to originate from Africa during the colonial era (2). . WRR is often closely associated with the genetic background of the rice varieties commonly. produced in the areas to which it has been introduced. In Thailand and Malaysia, where rice can be planted every season and the growth areas and heading dates of cultivated rice overlap with those of its wild relatives, the weedy traits of wild rice have been introduced as a result of outcrossing with cultivars (5, 26); subsequently these descendants evolved into WRR. Moreover, gene flow between wild and cultivated rice has also been identified in the USA. (13). . In areas. without wild rice, cultivated rice evolves into WRR after the adaptive mutation and dedomestication of the cultivated species and the accumulation of multiple effective mutations (10, 12, 14, 19). . In Brazil, China, South Korea, and the southern USA, WRR apparently originated. from a background of closely related Indica rice. (12, 15, 19, 25). , whereas in Italy and California,. WRR is speculated to have originated from crossbreeding among the Japonica species (8, 29). According to the whole genome sequencing and domestication-related gene analyses employed by Li et al.. (12). , the WRR in the USA was produced from the de-domestication of. cultivated rice and that weedy traits are sustained through selection in a few areas of the genome of the species. Qiu et al. (19) compared the de-domesticated genome sections of WRR with the domesticated genome sections of cultivated rice, revealing that the de-domestication of WRR. 20.

(31) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. did not involve changing the genotypes of the cultivated species back into wild genotypes, but it did involve adopting new genetic variations and molecular mechanisms to adapt to changing environments. On the basis of allele frequency distribution, a significant difference was identified among Indica and Japonica WRR groups in their standing variations and new mutations. Genetic diversity of WRR has been augmented through balancing selections to adapt to complicated survival environments, which is the opposite of the forward selections of cultivated rice. These results enhance existing knowledge of the genetic domestication and dedomestication mechanisms of cultivated crops, enabling an understanding of the environmental adaptation mechanisms of WRR and an exploration of strategies to prevent and eliminate it. However, the origins of WRR vary with its background cultivation ecology. In Taiwan, WRR has become adapted to the transplantation system, which has exacerbated its threat to the rice industry of Taiwan. Historical Significance, Immediate Causes, and Ultimate Causes of the WRR in Taiwan In Taiwan’s pre-twentieth century agricultural era, cultivated rice primarily consisted of environmentally competitive tall Indica cultivars owing to insufficient technology, facilities, and resources. At that time, contamination of cultivated rice with red, black, and glutinous rice landraces, as well as with barnyardgrass, was severe and undermined the quality and appearance of rice products. During 1906–1921, systematic WRR control strategies were conducted to effectively contain the contamination. In 1953, a general survey of the Indica rice cultivation area revealed dwarf blackhull long-grain rice as the leading local Indica landrace. However, Indica red rice, which is drought- and salt-tolerant, was also cultivated by farmers after the primary crop had been harvested in the same year or on arid land; a total of 10 local land races of Indica red rice suitable for upland cultivation were recorded to have been planted. In 1959, the local red rice land races became extinct when the highly productive semidwarf “Taichung Native 1” Indica variety entered mass production and irrigation infrastructure was improved. Thus, more than 50 years of red rice cultivation was recorded in the rice cultivation history of Taiwan (11). According to a 2005 analysis of rice seed nurseries, most off-type plants in Taiwan were tall, had early maturity, and slender, long grains. (28). . Further examination revealed that these. off-type plants originated from natural crossbreeding, contamination, or unsatisfactory uniformity among the contemporary varieties. Particularly, the samples displayed insufficient. 21.

(32) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. genetic similarities with their neighboring cultivated plants; these samples exhibited large numbers of tillers (36.4), average dwarf height of 73.2 cm, early maturity, and intermediate size grains. Their genetic backgrounds were highly homozygous and were similar to the Indica background, rendering the sample plants identical to the recent biotypes of WRR that predominate (4). The rice production and sales policy has recently changed from recommended fallowing (1997) to a system where farmers are subsidized for cultivating leased fallowed lands (2012). Starting from 2003, the Environmental Protection Agency in Taiwan prohibited burning straw to reduce the detrimental effects of high temperature on soil surfaces. However, low-cost production methods such as ratoon stubble and volunteer rice have been applied in some regions during the second cultivation period. After 2012, severe red rice contamination was identified during the second cultivation period even though high-quality rice seed was planted during the previous cultivation period, leading to a drop in the government procurement price for paddy rice. In 2014, rice seed nurseries were invaded by WRR; 5% of registered seed fields (six fields) and 24% of certified seed fields (137 fields) were contaminated with red rice at an average rate of 0.47 ± 0.55%. In 2015, red rice contamination was detected in approximately 43% of the 187 townships in Western Taiwan where paddy rice was harvested for public stocks (data not published). Starting from the second cultivation period in 2014, Taiwan authorities discontinued the procurement of rice produced through perennial roots or seed shattering; however, these low-cost rice production approaches have continued and are a persistent source for the spread of WRR. Phylogeographical Structures of Weedy Rice Weedy rice can produce a large number of seeds at maturity and these can be accidentally mixed with cultivated rice seeds during harvest, which may promote the long-distance dispersal of weedy rice seeds due to shipment of seedlings between regions. In Taiwan, farmers grow rice based on a transplanting system, and generally use agricultural machinery during soil preparation, transplanting, fertilizer application and harvesting. The transplanting model is helpful in the control of weeds, and the purchase of seedlings from specialized commercial nurseries should reduce the occurrence of volunteer seedlings. In the field survey of 2015, we collected rice samples from seven counties and found that the contamination of weedy red rice was serious in 83 townships (Fig. 2). The contamination rate of each township is the average. 22.

(33) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. of all paddy fields in the same area. Of the four townships in Taoyuan City, Daxi District had the highest contamination rate of 0.73%, and neighboring Pingzhen, Longtan, and Myrica rubra District possessed red rice contamination rates of 0.17-0.41%. Among the five townships in Miaoli County, contamination rates were highest in Houlong Town, up to 0.51%, and decreased sequentially in the neighboring towns of West Lake, Tofen, Tongxiao, and Yuanli Town, ranging from 0.15 to 0.40%. Similar cases have occurred in Taichung, Changhua, Yunlin, Chiayi and Tainan counties. The contamination rate exceeded 0.6% in Daxi District of Taoyuan City (0.73%), Huatan Township of Changhua County (0.69%), Nantou City of Nantou County (0.74%) and Dongpotential Town of Yunlin County (0.85%). It is worth mentioning that more than half of the eight townships had a contamination rate of 0.20-0.40%, indicating that the invasion of weed type red rice is widespread and serious. In order to establish an effective control strategy for weedy red rice, the first priority was to identify the degree to which the invasion in Taiwan occurred through seed-mediated contamination or pollen-mediated contamination, and if the transport distances in these two possibilities were significantly different from each other. In Sri Lanka for example, the abundant within-population genetic diversity coupled with limited population genetic structure and differentiation was likely caused by considerable seed-mediated gene flow of weedy rice along with long-distance exchange of farmer-saved rice seeds between weedy-rice contaminated regions. (10). . Knowledge of genetic diversity and spatial structure of weedy rice. populations will facilitate the design of effective methods to control this weed by tracing its origins and dispersal patterns in a given region. In our study, we used information on genetic diversity and geographical location to understand the transmission patterns of Taiwan's weedy red rice. First, we used molecular markers to determine the genetic clusters of weedy rice populations and then measured the level of genetic diversity among different sub-populations. Second, we plotted the genetic cluster information of weedy rice on a map to reveal the geographical distribution of each group. WRR Control Strategies Adopted in Japan The WRR control strategies adopted by Japan, which uses a transplantation system similar to Taiwan, can be applied to treat WRR in Taiwan. These strategies have reduced the WRR contamination rate in fields with a WRR density of 100 plants/ 0.1 ha from 2.3% to 0.1%, fulfilling the safe production standard. (20). . These cultural practices include submerging fields. 23.

(34) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. with shallow water and plowing before planting, applying a three-phase herbicide treatment, or removing off-type plants manually, which are used on 78%, 20%, and 2%, respectively, of the areas treated for WRR.. (20). . Although various strategies are applied to eradicate WRR, a. minimum rate of 99.6% depletion is required for lowering the contamination rate annually; a 95% depletion rate causes the contamination rate to rise from 5% to 15% in three years (24). The focal points of WRR control during each cultivation period as used in Japan are listed as follows (20): 1. Rice variety purity control and management: Only rice varieties qualified through examination are permitted for use; using self-reserved seed or seedlings of questionable purity raises the risks of contamination. 2. Cultivated seed and rice nursery management: When broken grains and by-products of rice milling are used in the tray medium for growing seedlings, they must decay prior to use. Alternatively, rice mills should enforce the elimination of any residual germs within the pericarps. Use of any seed from contaminated fields is forbidden. 3. Pre-cultivation plow management: A.. Plowing residual rice plants is avoided. The germination periods of WRR are closely related to its dormancy, maturity, and buried depths. WRR plants that are buried at a depth of 1 cm germinate at day 10 and reach a germination rate of 80% at day 14. Those that are buried at a depth of 3 cm germinate at day 14 and reach a germination rate of 70% at day 40. Those buried at 5 cm display no signs of germination even at day 35. These reports explain the factors leading to the emergence of volunteer plants in cultivated fields. Accordingly, plowing should be avoided before any control strategies are applied to prevent seeds from entering the deep layers of soil.. B.. When crop rotation is applied, gramineous selective herbicides should be used alternatively. The dormancy of residual seeds in the deep layers of soil are disrupted and any residual plants are eliminated when plowing. Seed at the soil surface or during fallowing periods may be consumed by birds, lowering germination rates.. C.. A long-period of flooding should be applied before preparing the soil. The finely prepared soil is covered with a shallow flood for a minimum of 30 days before plowing or from the previous cultivation period to reduce the WRR survival rate to. 24.

(35) Proceedings of the 2018 International Symposium on Proactive Technologies for Enhancement of Integrated Pest Management of Key Crops. 50%. D.. The soil should be managed after each rice harvest. Furthermore, the flooding treatment should be applied before preliminary plowing. One week after the germination begins during the treatment, at which point the sheath has grown to 20 mm, plowing is performed once to lower the germ survival rate by 10%. Nonselective herbicides are the most effective when used before plowing, raising the WRR elimination rate in a field with a contamination density of 12.7 plants per m2 to as high as 78% when the soil is plowed after germination.. E.. The soil should be cleaned thoroughly using high-temperature steam when environmentally friendly cultivation approaches are applied. A self-propelled hightemperature fumigation machine should be used to clean the cultivated fields, thereby eliminating seed in the shallow soil layers and killing the volunteers.. 4. Field management after transplantation: A three-phase herbicide treatment is implemented. Pre-germination and post-germination herbicides are applied to the WRR seeds at various depths of soil, once during transplantation, followed by additional applications at seven and 14 days after transplantation. The herbicides butachlor and pretilachlor can be applied three times to effectively eliminate volunteer plants and improve the WRR elimination rate in a field with a contamination density of 12.7 plants per m2 by 20%. Attention must be paid to the quality of herbicides, time points of their implementation, and maintenance of flooded fields, all of which affect the effectiveness of the herbicide. Moreover, the growth status of WRR must be considered. Selective herbicides are only effective against volunteer plants before or immediately after their germination, but not against seedlings having one or two leaves emerged. 5. Field management after heading: A.. Off-type plants must be thoroughly uprooted and removed from cultivated fields.. B.. WRR typically exhibits earlier heading dates and higher morphological variation than cultivated rice does. Therefore, the plants that display inconsistent heading dates and plant traits compared with surrounding plants must be removed.. C.. Off-type plants must be uprooted within 14 days after the heading date. The maturity rate of shattered seeds increases from 10% at 14 days after heading to 50%–70% at 21 days after heading.. 6. Sequence of harvest: Harvesters must be thoroughly cleaned after use; moreover,. 25.