檬果壯鋏普癭蚋之潛在性天敵寄生蜂Aprostocetus sp. (膜翅目：釉小蜂科) 寄生行為

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(1)台灣農業研究 (J. Taiwan Agric. Res.) 68(3):246–253 (2019) DOI:10.6156/JTAR.201909_68(3).0006. 研究報告. 檬果壯鋏普癭蚋之潛在性天敵寄生蜂 Aprostocetus sp. (膜翅目：釉小蜂科) 寄生行為林聖豐 1 王釋玄 2 李昂勳 2 楊曼妙 3 郝秀花 4,* 摘要林聖豐、王釋玄、李昂勳、楊曼妙、郝秀花。2019。檬果壯鋏普癭蚋之潛在性天敵寄生蜂 Aprostocetus sp. (膜翅目：釉小蜂科) 寄生行為。台灣農業研究 68(3):246–253。本研究針對 Aprostocetus sp. 於檬果壯鋏普癭蚋的寄生率及寄生行為進行調查，分別在 2015 年 4 月及 10 月於高雄市兩樣區調查。結果顯示，其寄生率介於 11–19%。抽樣葉片的癭蚋蟲癭數量與被寄生數呈正相關 (r = 0.785, P < 0.001)，與寄生率之相關性低 (r = -0.291, P = 0.213)，顯示寄生蜂寄生率不隨癭蚋族群大小而增減。向光處蟲癭的被寄生率 (19.3% ± 3.2%, n = 9) 顯著高於背光處 (4.9% ± 2.6%, n = 9) (P < 0.050)，顯示寄生蜂寄生偏好會受環境因子影響。癭蚋被寄生之時期主要在蟲癭的成長分化期及定型成熟期。寄生蜂成蟲插入產卵管的寄生方位為蟲癭的底部 (葉背方向)，但其離癭位置則多與癭蚋相同，即由蟲癭的端部羽化孔 (葉面方向) 離癭，僅少數寄生蜂由葉背方向離癭。室內飼養寄生蜂成蟲存活天數比較結果顯示，對照無提供營養組 [4 d ± 1 d (n = 12)]，提供 20% 蜂蜜水組 [9 d ± 1 d (n = 12)] 之成蟲個體存活天數較長，推論於田間栽植蜜源植物可延長此蜂存活天數及提升其寄生效率。未來將進一步測試其 Aprostocetus sp. 成蟲日律活動及增放效果，以評估作為防治檬果壯鋏普癭蚋的天敵資材可行性。關鍵詞：檬果壯鋏普癭蚋、釉小蜂、寄生時期、產卵行為、防治策略。. 前言檬果壯鋏普癭蚋 (Procontarinia robusta Li, Bu & Zhang) 為雙翅目癭蚋科昆蟲，於檬果 (Mangifera indica L., Anacardiaceae) 葉片形成黑色小型蟲癭，可布滿葉面降低葉片光合作用，成蟲羽化離癭時會造成葉片傷口，引發病原菌感染影響植株生長，導致果實減產及影響產業經濟。近 20 年，該害蟲已發生於東非、中東及亞洲國家 (中國、東帝汶、印度、印尼及台灣等) (Li et al. 2003; Wang & Wang 2005; Zhao et al. 2005; Su et al. 2006; Cai et al. 2013; Shih et al. 2013; Zeng et al. 2014)。至今，台灣雖有檬果. * 1 2 3 4. 壯鋏普癭蚋相關的生物學研究，如 Hao & Shih (個人通訊) 指出其於台灣每年具 6–7 個世代，Lin et al. (2018) 記錄害蟲與蟲癭發育的對照時期、蟲癭的分布偏好及物理特性。然其防治策略除化學防治方式之外，其他防治策略資料仍缺乏。許多研究報告顯示，造癭癭蚋族群動態及其生態特性會受到寄生蜂影響 (Redfern & Cameron 1978; Sunose 1985; Yukawa & Rohfrisch 2005)。本研究針對檬果壯鋏普癭蚋的寄生蜂 Aprostocetus sp. (圖 1) 進行寄生率調查、寄生行為、成蟲室內條件飼養比較，以評估其作為天敵防治資材之可行性。. 投稿日期：2019 年 3 月 20 日；接受日期：2019 年 5 月 10 日。通訊作者：[email protected] 國立中興大學昆蟲學系博士生。台灣台中市。高雄市立明華國中學生。台灣高雄市。國立中興大學昆蟲學系教授。台灣台中市。農委會農業試驗所鳳山熱帶園藝試驗分所植物保護系助理研究員。台灣高雄市。.

(2) 247. 檬果壯鋏普癭蚋之寄生蜂寄生行為. (A). (B). (C). 0.5 mm. 0.5 mm. 圖 1. 檬果壯鋏普癭蚋蟲癭及其寄生蜂 (Aprostocetus sp.)。(A) 蟲癭、(B) 寄生蜂雌蟲及 (C) 寄生蜂雄蟲。 Fig. 1. Procontarinia robusta midge gall (A) and its parasitic Aprostocetus sp. female (B) and male (C).. 材料與方法調查地點、樣樹及蟲癭發生情形調查之檬果樣樹選自高雄市立明華國民中學校園 (N 22.661338, E 120.301073，以下稱為學校樣點) 4 株及行政院農委會農業試驗所鳳山熱帶園藝試驗分所 (N 22.642635, E 120.358871，以下稱為鳳試所樣點) 36 株檬果樹，樹高約為 1.5–3.0 m。試驗採樣的檬果葉片上的蟲癭密度，每葉平均超過 60 個蟲癭。. Aprostocetus sp. 寄生率本研究以寄生在檬果壯鋏普癭蚋之寄生蜂 Aprostocetus sp. 為調查對象，在上述兩樣區分別於 2015 年 4 月採樣 30 片著癭葉及 10 月採樣 12 片著癭葉，計算蟲癭數量及被寄生率。此外，於 2015 年 10 月在學校樣點隨機採集. 30 片著癭葉，進行解剖並計算被寄生率，探討寄生率與蟲癭數量之相關。. Aprostocetus sp. 寄生時期及行為依 Lalonde & Shorthouse (1984)、Rohfritsch (1992) 及 Yang (1999) 對於蟲癭發育時期的定義。選取檬果壯鋏普癭蚋蟲癭的初始形成期 (initiation stage)、成長分化期 (growth and differentiation stage) 及定型成熟期 (maturation stage) 進行寄生蜂寄生時期測試。於鳳試所樣點，選擇上述 3 時期的蟲癭葉片各 3 片，每片葉片包含超過 60 個蟲癭，分別以網袋包覆。待套網內葉片蟲癭發育為定型成熟期後 1 wk，將蟲癭解剖並記錄寄生率，進行 3 重覆。在鳳試所樣點採集向光及背光著癭葉各 9 片，記錄兩者葉片蟲癭數量及解剖，比較二者.

(3) 248. 台灣農業研究第 68 卷第 3 期. 寄生率之差異，並以 PAST 3.06 (Hammer et al. 2001) 進行 Kruskal-Wallist 測試比較。寄生蜂產卵位置：於兩樣區分別選擇具有初始形成期及成長分化期的蟲癭葉片 6 片，每片葉片包含超過 80 個蟲癭，分成葉背包覆組 (以網袋包覆葉背) 及葉面包覆組 (以網袋包覆其葉面) (圖 2)。每組各包含 3 片著癭葉，待蟲癭發育至定型成熟期後 1 wk，取回並解剖記錄，計算寄生率並比較兩組之差異。寄生蜂離癭位置：於鳳試所及學校樣點分別選擇定型成熟期著癭葉各 6 片，分成葉背包覆組 (以網袋包覆葉背) 及葉面包覆組 (以網袋包覆其葉面)，每組各包含 3 片著癭葉，記錄 2 組寄生蜂的羽化數量。. Aprostocetus sp. 成蟲室內條件飼養解剖檬果壯鋏普癭蚋蟲癭，將取得的寄生蜂幼蟲或蛹，置於舖有衛生紙的小容器中飼養。將取得之成蜂分為 2 組並於室溫 (25℃ ± 2℃) 進行飼養試驗，一組不提供食物及水，另. (A). 一組提供含有 20% 蜂蜜水之棉花球。記錄並比較兩組成蟲的存活日數。. 結果 Aprostocetus sp. 寄生率及其影響因子 Aprostocetus sp. 於學校樣點的寄生率為 17.26% (4 月) 及 18.56% (10 月)；於鳳試所樣點的寄生率為 14.47% (4 月) 及 11.76% (10 月) (表 1)。此外，每一葉片的蟲癭數量及寄生率相關性分析結果顯示，寄生蜂的寄生數量隨著蟲癭數量上升而增加，二者呈正相關 (r = 0.785，P < 0.001)，而寄生率卻隨著蟲癭數的增加而略顯下降，但兩者相關性低 (r = -0.291，P = 0.213) (圖 3)。. Aprostocetus sp. 寄生偏好及行為寄生蜂於蟲癭發育各時期套袋之寄生率，在初始形成期為 0% (n = 340)、於成長分化期為 11.7% (n = 316)、於定型成熟期為 21.0% (n. (B). 圖 2. Aprostocetus sp. 寄生偏好及其成蟲離癭試驗網袋包覆示意圖。(A) 葉背包覆組及 (B) 葉面包覆組。 Fig. 2. Experimental diagram of parasitize preference and adult emerge behavior of Aprostocetus sp. Meshed bag covers on (A) abaxial side and (B) adaxial side. Arrow indicates covered side. 表 1. Aprostocetus sp. 於檬果壯鋏普癭蚋之寄生率。 Table 1. Parasitism of Aprostocetus sp. on Procontarinia rubasta. April 2015 Sampling localityz. z. No. of gall. October 2015 Parasitism (%). No. of gall. Parasitism (%). MH. 2,335. 403 (17.26%). 1,907. 354 (18.56%). FS. 2,467. 357 (14.47%). 2,006. 236 (11.76%). MH: Minghua Junior High School; FS: Fengshan Tropical Horticultural Branch, Taiwan Agricultural Research Institute..

(4) 249. Parasitization (%) Number of Parasite (n). 檬果壯鋏普癭蚋之寄生蜂寄生行為. 60. Aprostocetus sp. 室內條件飼養. (A). 50. y = 0.1585x + 4.0035 R2 = 0.616 t = 5.3736, P < 0.001. 40 30. 剛羽化的成蜂於無食物供給狀態下可存活 4 d ± 1 d (n = 12)，另給予 20% 蜂蜜水的組別可存活 9 d ± 1 d (n = 12)，兩者呈顯著差異 (P < 0.05)。. 20 10 0 50%. (B). 40%. 討論. y = -0.0003x + 0.2449 R2 = 0.0845. Aprostocetus sp. 寄生率. t = -1.3287, P < 0.2. 30% 20% 10% 0%. 0. 50. 100. 150. 200. 250. 300. Number of gall (n) 圖 3. 檬果壯鋏普癭蚋蟲癭數量與 Aprostocetus sp. (A) 寄生數量及 (B) 寄生率之關聯。 Fig. 3. The correlation of gall number of Procontarinia robusta to (A) parasitized number (n) and (B) parasitization (%) of Aprostocetus sp.. = 276)；於向光面及背光面的寄生比率分別為 19.3% ± 3.2% (n = 9) 及 4.9% ± 2.6% (n = 9)，兩者具顯著差異 (表 2)。在寄生蜂產卵位置試驗，葉背 (葉面包覆組) 蟲癭的寄生率於鳳試所及學校分別為 12.5% 及 18.8%，葉面 (葉背包覆組) 的蟲癭寄生率於兩樣點均為 0 (表 3)。在寄生蜂離癭位置試驗，網袋包覆葉面組及網袋包覆葉背組均可蒐集到寄生蜂，前者組別於兩樣點之蒐集及寄生蜂數量分別為 9.0 ± 3.6 (n = 3，鳳試所樣點) 及 9.6 ± 2.1 (n = 3，學校樣點)；後者組別之寄生蜂數量分別為 5.3 ± 2.1 (n = 3，鳳試所. 天敵的寄生效力，對於害蟲族群的生物防治是不可或缺的資訊，選擇合適的天敵物種，方能提高防治效益及降低防治成本。例如為害板栗 (Castanea mollissima Blume) 作物的板栗癭蜂 (Dryocosmus kuriphilus Yasumatsu)，雖然於不同的國家發現數種天敵寄生蜂，但除了中華長尾小蜂 (Torymus sinensis Kamijo) 因具有高專一寄生性，被選為生物防治天敵之外，其他物種則因為寄生率均不超過 2% 而不受青睞 (Payne 1978; Murakami et al. 1980; Kamijo 1982; Murakami 1983; Huang et al. 1988; Aebi et al. 2006; Abe et al. 2007; Cooper & Rieske 2007; Quacchia et al. 2013a, 2013b)。以本研究而言，Aprostocetus sp. 於兩樣區的寄生率都在 10% 以上，最高甚至達到 18.56%。此外， Aprostocetus sp. 寄生數量隨著癭蚋蟲癭數量的增加而上升，即使寄生比率有略降，但統計結果指出蟲癭數量及被寄生率之相關性不顯著 (P = 0.213)。顯示天敵寄生率在癭蚋致死因子中占一定比例，對檬果壯鋏普癭蚋族群具有一定的抑制效果，具有發展為良好的生物防治天敵之潛力，亦可配合其他防治方法施行綜合防治。. Aprostocetus sp. 寄生偏好及行為. 樣點) 及 6.0 ± 2.0 (n = 3，學校樣點)。. Yukawa & Rohfrisch (2005) 將癭蚋的寄. 表 2. Aprostocetus sp. 於向光面及背光面蟲癭之寄生數量及寄生率。 Table 2. Parasitism of Aprostocetus sp. on apricus and downsun branch. Sampling branch Apricus branch (n = 9) Downsun branch (n = 9) z. No. of gall per leaf z. Parasitism (%). 181.0 ± 64.5 a. 35.3 ± 14.1 (19.3 ± 3.2%) a. 31.3 ± 9.2 b. 11.6 ± 1.10 (4.9 ± 2.6%) b. Means in the same column marked with the different letters are significantly different according to Kruskal-Wallist test (P < 0.050)..

(5) 250. 台灣農業研究第 68 卷第 3 期. 表 3. Aprostocetus sp. 於檬果壯鋏普癭蚋蟲癭於葉片之寄生偏好。 Table 3. Leaf side preference of parasitic preference of Aprostocetus sp. on Procontarinia robusta gall. Sampling localityz. z. Abaxial side (n = 3). Adaxial side (n = 3). MH. 20.3 ± 2.1 (18.8 ± 2.6%). 0 (0%). FS. 13.7 ± 2.1 (12.5 ± 3.1%). 0 (0%). MH: Minghua Junior High School; FS: Fengshan Tropical Horticultural Branch, Taiwan Agricultural Research Institute.. 生蜂分為兩類型，第一類是內寄生及單食性寄生蜂，主要寄生癭蚋的卵期及初齡幼蟲，如廣腹細蜂、旋小蜂及廣肩小蜂；另一類則為行外寄生及食性較廣的姬蜂及長尾小蜂物種，主要寄生較晚期或成熟的幼蟲齡期。Aprostocetus sp. 偏好寄生於成長分化期及定型成熟期蟲癭，顯示其應屬於寄生幼蟲後期齡期之類型。成長分化期的蟲癭寄生率偏低 (11.7%)，推論此時期僅有少部分的癭蚋已發育為體型較大的幼蟲，然而定型成熟期蟲癭的寄生率高 (21.0%)。顯示直至蟲癭發展後期，仍有寄生活動發生，其寄生的癭蚋齡期可能包含癭蚋 2 齡幼蟲期至蛹期階段。Chein & Ku (2001) 指出非洲菊斑潛蠅的 5 種寄生蜂 (4 種釉小蜂及 1 種繭蜂) 對其寄主幼蟲齡期具選擇性，主要寄生 3 齡幼蟲時期。此外，4 種釉小蜂的子代雌性比會受寄主齡期影響。未來可進一步測試 Aprostocetus sp. 的子代雌性比在寄生不同寄主齡期是否有差異，以降低偏雄現象 (雄蟲比例過高)，避免增加防治及飼養成本 (Chow & Heinz 2005)。寄生蜂搜尋行為乃其重要的存活能力之一，除了以視覺定位寄主之外，有時亦會利用寄主取食植物寄主所產生的揮發物質來進行定位 (Fellowes et al. 2005)。Wang & Yang (2008) 指出多數寄生蜂會以視覺或化學訊號來確認遠距離的寄主方位，再以聽覺、嗅覺確認寄主的確切位置。但寄生蜂的寄生行為有時於野外觀察不易，本研究藉由寄生偏好測試確認 Aprostocetus sp. 僅由蟲癭底部 (= 葉背) 進行寄生，但可由蟲癭底部 (= 葉背) 或端部 (= 葉面) 的位置離癭，且其於葉面/葉背的離癭的比例約為 1.5 倍，顯示寄生蜂的離癭位置較偏好於葉面離癭。目前，仍無法確認寄生蜂離癭行為的機制，但本研究結果顯示可藉由蟲癭的生態資. 訊提供寄生蜂寄生行為之判斷。 Lin et al. (2018) 證實檬果壯鋏普癭蚋於向光面的蟲癭數量較背光面高，本研究結果 Aprostocetus sp. 的寄生亦有類似的情形，顯示相同的環境中，其寄生偏好亦會受到不同微環境因子的影響。如向光或背光處的光照強度不同，未來可進一步確認光照因子或顏色對於寄生蜂誘引的程度，或可作為誘集寄生蜂或降低生物天敵干擾之資訊。. Aprostocetus sp. 成蟲室內飼養 Price (1974) 提出寄生蜂產卵及卵的形成主要分為兩種型式，原定式產卵 (proovigenic) 及應變式產卵 (synovigenic)。行前者型式之寄生蜂，雌蟲多為壽命及產卵期短、日產卵數變化大、無取食寄主食性、排卵自發性且於羽化時體內的卵皆已成熟；反之，行後者型式之寄生蜂，雌蟲壽命及產卵期較長、可藉由取食寄主獲得營養或提供卵之成熟及形成、其排卵受外界因子影響、其初羽化成蟲體內可能僅含少數成熟卵、可藉由卵吸收來調節產卵時機。如 Chien & Chang (2013) 顯示寄生斑潛蠅的 4 種釉小蜂 [異角釉小蜂 Hemiptarsenus varicornis (Girault)、華釉小蜂 Neochrysocharis formosa (Westwood)、底比斯釉小蜂 Chrysoncharis pentheus (Walker)、岡崎釉小蜂 Closterocerus okazakii (Kamijo)] 即是應變式產卵型式的寄生蜂物種，在無寄主可寄生時會藉由卵吸收的方式，保存生殖資源並調節產卵時機，但產卵調節的策略受成蟲的壽命影響。若能另提供蜜源植物，可延長 4 種釉小蜂的壽命，進而提升寄生蜂對斑潛蠅的抑制成效。本研究雖無法直接判定 Aprostocetus sp. 是屬於何種產卵型式的寄生蜂，但藉由取食蜂蜜可延長其存活天數之結果，或可推測其為應變式產卵型式之寄生蜂。.

(6) 檬果壯鋏普癭蚋之寄生蜂寄生行為. 未來可進行其卵量計算及相關測試，確立其產卵型式，以供生物防治發展作為參考。. 誌謝本研究以第二及第三作者於 2015 年與 2016 年參加國中科學展覽 (主題分別為「『癭』室了得，硬是了得！探討檬果壯鋏普癭蚋的生態及生物防治可行性」及「捕『蜂』捉『癭』 ─ 探討一種未知寄生蜂的生態及對檬果壯鋏普癭蚋寄生模式」) 之部分資料為基礎，由其他共同作者指導並進行彙整、分析、詮釋及轉寫。研究期間承高雄市立明華國民中學林品汝、倪羽薇、劉珈琳、李奕萱、蘇育弘、李冠徵協助調查採樣及整理數據。文成後，感謝中興大學邱俊禕先生於統計分析之協助、美國農業部 (United States Department of Agriculture) 唐昌廸博士及林業試驗所潘亮瑜博士提供文章修正建議及文稿斧正。. 引用文獻 Abe, Y., G. Melika, and G. N. Stone. 2007. The diversity and phylogeography of cynipid gallwasps (Hymenoptera: Cynipidae) of the oriental and eastern Palearctic regions, and their associated communities. Orient. Insects 41:169–212. Aebi, A., K. Schönrogge, G. Melika, A. Alma, G. Bosio, A. Quacchia, L. Picciau, Y. Abe, S. Moriya, K. Yara, and G. Seljak. 2006. Parasitoid recruitment to the globally invasive chestnut gall wasp Dryocosmus kuriphilus. p.103–121 in: Galling Arthropods and Their Associates: Ecology and Evolution. (Ozaki, K., J. Yukawa, T. Ohgushi, and P. W. Price, eds.) Springer Japan. Tokyo, Japan. 308 pp. Cai, H. J., P. Kolesik, H. Y. Wang, F. R. Liao, V. Quintao, F. M. Harris, and G. A. Bellis. 2013. Description of the immature stages and gall morphology, and molecular characterisation of Procontarinia robusta, a gall midge (Diptera: Cecidomyiidae) damaging leaves of mango Mangifera indica L. (Anarcadiaceae) in southern Asia. Aust. J. Entomol. 52:206–211.. 251. on leaf miners (Diptera: Agrimyzidae). J. Taiwan Agric. Res. 62:32–39. (in Chinese with English abstract) Chow, A. and K. M. Heinz. 2005. Manipulation of sex ratios in mass rearing of Diglyphus isaea (Walker), an ectoparasitoid of Agromyzid leafminers. IOBC WPRS Bull. 28:63–66. Cooper, W. R. and L. K. Rieske. 2007. Community associates of an exotic gallmaker, Dryocosmus kuriphilus (Hymenoptera: Cynipidae), in eastern North America. Ann. Entomol. Soc. Amer. 100:236–244. Fellowes, M. D. E., J. J. M. van Alphen, and M. A. Jervis. 2005. Foraging behaviour. p.1–17. in: Insects as Natural Enemies: A Practical Perspective. (Jervis, M. A., ed.) Springer. Dordrecht, the Netherlands. 748 pp. Hammer, Ø., D. A. T. Harper, and P. D. Ryan. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontol. Electron 4:1–9. Huang, J., Y. Luo, and D. Liao. 1988. Studies on the natural enemies of chestnut gall wasp in China. Scientia Silvae Sinicae 24:162–169. (in Chinese) Kamijo, K. 1982. Two new species of Torymus (Hymenoptera, Torymidae) reared from Dryocosmus kuriphilus (Hymenoptera, Cynipidae) in China and Korea. Kontyu 50:505–510. Lalonde, R. G. and J. D. Shorthouse. 1984. Developmental morphology of the gall of Urophora cardui (Diptera, Tephritidae) in the stems of Canada thistle (Cirsium arvense). Can. J. Bot. 62:1372–1384. Li, J., W. J. Bu, and Q. Y. Zhang. 2003. A new species of gall midge (Diptera: Cecidomyiidae) attacking mango leaves from China. Acta. Zootax. Sin. 28:148–151. Lin, S. F., P. R. Lin, Y. W. Ni, M. M. Yang, and H. H. Hao. 2018. Gall development, structure and preference position of the invasive cecidomyiid Procontarinia robusta Li, Bu & Zhang (Diptera: Cecidomyiidae). Formosan Entomol. 38:84–91. (in Chinsese) Murakami, Y., H. B. Ao, and C. H. Chang. 1980. Natural enemies of the chestnut gall wasp in Hopei Province, China: Hymenoptera: Chalcidoidea. Appl. Entomol. Zool. 15:184–186.. Chien, C. C. and S. C. Ku. 2001. Instar preference of five species of parasitoids of Liriomyza trifolii (Hymenoptera: Eulophidae, Braconidae). Formosan Entomol. 21:89–97. (in Chinese with English abstract). Murakami, Y. 1983. Comparison of the adult emergence periods between Torymus (Syntomaspis) beneficus, a native parasitoid of the chestnut gall wasp and a congeneric parasitoid imported from China (Hymenoptera: Torymidae). Proc. Assoc. Plant Prot. Kyushu 27:156–158. (in Japanese). Chien, C. C. and S. C. Chang. 2013. Oosorption in four eulophid wasps (Hymenoptera: Eulophidae) parasitic. Payne, J. A. 1978. Oriental chestnut gall wasp: New nut pest in North America. p.86–88. in: Proceedings of.

(7) 252. 台灣農業研究第 68 卷第 3 期. the American Chestnut Symposium. January 4–5, 1978. Morgantown, WV. West Virginia Univ. Press, Morgantown, WV. Price, P. W. 1974. Strategies for egg production. Evolution 28:76–84. Quacchia, A., S. Moriya, and G. Bosio. 2013a. Effectiveness of Torymus sinensis in the biological control of Dryocosmus kuriphilus in Italy. Acta. Hort. 1043:199–204. Quacchia, A., C. Ferracini, J. A. Nicholls, E. Piazza, M. A. Saladini, F. Tota, G. Melika, and A. Alma. 2013b. Chalcid parasitoid community associated with the invading pest Dryocosmus kuriphilus in north western Italy. Insect Conserv. Diver. 6:114–123. Redfern, M. and R. A. D. Cameron. 1978. Population dynamics of the yew gall midge Taxomyia taxi (Inchbald) (Diptera: Cecidomyiidae). Ecol. Entomol. 3:251–263. Rohfritsch, O. 1992. Patterns in gall development. p.60– 86. in: Biology of Insect-Induced Galls. (Shorthouse, J. D. and O. Rohfritsch, eds.) Oxford University Press. New York, NY. 285 pp. Shih, H. T., H. H. Hao, Y. C. Chiu, F. C. Lin, and M. M. Yang. 2013. A revised and annotated checklist of insects and mites of mangos from Taiwan. Formosan Entomol. 33:27–51. (in Chinese) Su, Y., W. Zhang, J. Wang, and H. Wang. 2006. Studies on the damage and the chemical control of Procontarinia robusta at Xiamen. Fujian Sci. Tech. Tropical Crop. 31(3):1–3. (in Chinese). Sunose, T. 1985. Population regulation of the euonymus gall midge Masakimyia pustulae Yukawa and Sunose (Diptera: Cecidomyiidae) by hymenopterous parasitoids. Res. Popul. Ecol. 27:287–300. Wang, W. X. and H. Y. Wang. 2005. A preliminary report on biological characters of Procontarinia robusta in mango. Fujian J. Agric. Sci. 20:74–76. (in Chinese) Wang, X. and Z. Yang. 2008. Behavioral mechanisms of parasitic wasps for searching concealed insect hosts. Acta. Ecol. Sin. 28:1257–1269. Yang, M. M. 1999. The Biology and evolution of gall-forming insects. p.113–126. in: Proceedings of the Symposium on Insect Systematic and Evolution. May 20–21, 1999. Taipei, Taiwan. National Taiwan University and National Museum of Natural Science, Taipei. (in Chinese with English abstract) Yukawa, J. and O. Rohfrisch. 2005. Biology and ecology of gall-inducing cecidomyiidae. p.274–304. in: Biology, Ecology, and Evolution of Gall-Inducing Arthropods. (Ramna, A., C. W. Schaefer, and T. M. Withers, eds.) Science Publishers. Enfield, NH. 817 pp. Zeng, C., Y. L. Li, R. R. Xiao, L. X. Huang, Y. D. Robleh, A. A. Bourhan, and Y. Peng. 2014. Preliminary study on Procontarinia robusta, one kind of pest of mango tree, in Djibouti. J. Hubei Univ. (Natural Science) 36:303–306. (in Chinese) Zhao, J. H., M. Xia, and Z. H. Zeng. 2005. Occurrence and control of Procontarinia mangicola (Shi). Sci. Tech. Sichuan Agric. 1:35. (in Chinese).

(8) 檬果壯鋏普癭蚋之寄生蜂寄生行為. 253. Parasitic Behavior of a Potentially Natural Enemy, Aprostocetus sp. (Hymenoptera: Eulophidae), on Mango Pest Cecidomyiid Procontarinia robusta (Diptera: Cecidomyiidae) Sheng-Feng Lin1, Shi-Shun Wang2, Ang-Shing Lee2, Man-Miao Yang3, and Hsiou-Hua Hao4,*. Abstract Lin, S. F., S. S. Wang, A. S. Lee, M. M. Yang, and H. H. Hao. 2019. Parasitic behavior of a potentially natural enemy, Aprostocetus sp. (Hymenoptera: Eulophidae), on mango pest cecidomyiid Procontarinia robusta (Diptera: Cecidomyiidae). J. Taiwan Agric. Res. 68(3):246–253.. The investigations on the parasitism and ovipositional behavior of Aprostocetus sp. were done on mango pest cecidomyiid, Procontarinia robusta, in providing fundamental information for developing biocontrol tactics. The parasitism was 11–19% at two sampling localities of Kaohsiung City in April and October 2015. Number of galls per leaf is positively correlated to the number of parasites per leaf (r = 0.785, P < 0.001) but insignificantly correlated to the percentage parasitization (r = -0.291, P = 0.213). It indicates that parasitism is not affected by population size of P. robusta. Besides, the parasitism of gall on apricus branch (19.3% ± 3.2%, n = 9) is significantly higher than that on downsun branch (4.9% ± 2.6%, n = 9), indicating the parasitism is influenced by environmental factor. The ovipositional phase of Aprostocetus sp. is associated with growth and differentiation stage and maturation stage of midge gall. The adult wasp lays the egg on abaxial side of leaf and most emergent adult leaves gall from adaxial side of leaf. The longevity of adult wasp treated with 20% honey water (9 d ± 1 d, n = 12) is higher than those in the treatment with no food (4 d ± 1 d, n = 12). The results showed that planting nectar plants could have positive biological control effect by prolonging the longevity of the Aprostocetus parasitoid. The biological rhythm and release test of Aprostocetus sp. is needed to evaluate biocontrol effectiveness of natural enemy on P. robusta in further studies. Key words: Procontarinia robusta, Aprostocetsu sp., Parasitic phase, Ovipositor behavior, Biological control.. Received: March 20, 2019; Accepted: May 10, 2019. * Corresponding author, e-mail: [email protected] 1 Ph.D. Student, Department of Entomology, National Chung Hsing University, Taichung, Taiwan, ROC. 2 Student, Kaohsiung Municipal Minghua Junior High School, Kaohsiung, Taiwan, ROC. 3 Professor, Department of Entomology, National Chung Hsing University, Taichung, Taiwan, ROC. 4 Assistant Research Fellow, Department of Plant Protection, Fengshan Tropical Horticultural Experimental Branch, Taiwan Agricultural Research Institute, Kaohsiung, Taiwan, ROC..

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