從生活史不同階段初探虎灰蝶與樹棲舉尾蟻的共生關係

Abstract

本研究以虎灰蝶（Spindasis lohita formosana Moore, 1877，灰蝶科Lycaenidae虎灰蝶屬Spindasis）為題材，建立幼生期形態及生態資料，並從生活史不同階段探索虎灰蝶與懸巢舉尾蟻（Crematogaster rogenhoferi Mayr, 1879）之間的共生關係。 虎灰蝶幼蟲齡期數變異大而且不固定，最少者為六齡，最多者為九齡，以六齡佔最多數。幼蟲共具有四種類型的喜蟻器官，包括圓頂腺（PCOs）、蜜腺（DNO）、觸手器（TOs）及碟狀腺（SGs）。PCOs出現於一齡蟲第七腹節及氣孔前方，之後並出現於幼蟲DNO與SGs附近和蛹的氣孔周邊；TOs自一齡蟲第八腹節背面兩側有構造物出現，至三齡始有功能；DNO出現自二齡蟲腹部第七腹節後端；SGs最早出現於二齡蟲第七腹節背面中央，四齡蟲第二腹節背面中央出現另一碟狀腺，五齡蟲於第二至第四腹節背面中央有二至三個不等的碟狀腺，五齡蟲之後碟狀腺大小、數目有個體變異，終齡幼蟲腹部第一到第五腹節的碟狀腺已發育完成，共具有六個碟狀腺。根據不同齡期幼蟲喜蟻器官發育，配合幼蟲與螞蟻互動試驗顯示，隨著喜蟻器官的發育，幼蟲吸引螞蟻的能力會顯著增加。 雌蝶產卵偏好試驗中發現，螞蟻的存在是雌蝶產卵的關鍵因子。卵為聚產，其表面不具有吸引螞蟻的物質，卵粒產下後無法吸引螞蟻。蛹與螞蟻互動試驗則發現活蛹具有吸引螞蟻聚集的現象。野外觀察亦發現幼蟲皆伴隨有樹棲性舉尾蟻，齡期較大的幼蟲會和螞蟻合建如遮蔽所的蟲巢。實驗室內証實在天敵存在下，有螞蟻伴隨的幼蟲死亡率較低，且螞蟻會驅趕天敵；在野外存活率試驗中，沒有螞蟻伴隨的幼蟲死亡率高達100%，無法完成其生活史，顯見其為絕對性共生之喜蟻性灰蝶。 本研究認為虎灰蝶與懸巢舉尾蟻之互動存在有取捨（trade-off）現象。在花費（cost）方面，幼蟲分泌蜜露和螞蟻互動為耗能行為，結果造成成蝶體型顯著較小，從行為觀察與飼養試驗推論幼蟲可藉由群聚行為或額外補充糖類進行能量消耗之補償作用，而飼養狀況下幼蟲有被螞蟻咬死及感染疾病的紀錄，且有螞蟻照顧的幼蟲死亡率亦較高。在利益（benefit）方面，可得到螞蟻的保護，以降低被天敵捕食。In this study, immature morphology of Spindasis lohita formosana Moore, 1877 (Lepedoptera: Lycaenidae) and the symbiotic relationships with its attendant ants Crematogaster rogenhoferi Mayr, 1879 in different life stages were investigated. In this study, four types of myrmecophilous organs were recorded in the immature stages of S. lohita formosana, including pore cupolas (PCOs), dorsal nectar organ (DNO), tentacle organs (TOs) and Saucer-like glands (SGs). PCOs which surrounded DNO, SGs and spiracles were presented on the larva of all instars, and were also formed in the front of the spiracles of the pupae. DNO located at dorsal-posterior end of the seventh-abdominal segment (A7) in all stages except the first instar. TOs were located on the A8 of the first instar. This organ had no function until the third instar. It was presented from the second instar on and it was located on the central dorsum of the A7. Another SG appeared on A2 from the fourth instar on. The numbers of SGs varied with different individuals. Fiveth instar larvae bore two to three SGs on A2 to A4. Late instar larvae (mainly sixth instar, sometimes seventh or eighth instar, rarely ninth instar) possess the well-developed SGs located on A1 to A5 and A7. The ability to attract the ants significantly increased with the development of myrmecophilous organs. The oviposition experiments showed that the appearance of the attendant ants was the key factor for oviposition behavior of S. lohita formosana. The eggs were laid in clutch and without attractants to attract the ants. However, the ants were always found aggregated on the pupae in laboratory experiments or at field observations. These results suggest that the pupae can attract the ants. The larvae of S. lohita formosana were always attended by Crematogaster ants on the field, and the elder larvae made nests with the ants cooperatively. Predation experiments showed that the larvae attended by ants had lower mortality and the attendant ants would expel the predators. None of the larvae survived without attendant ants, which indicates that S. lohita formosana is an obligatory myrmecophilous butterfly. Trade-off phenomenon existed in the symbiotic relationships between S. lohita formosana and its attendant ants C. rogenhoferi. On the one hand, energy-consumed behaviors of the larvae, such as honeydew secretion by DNO to attract the ants, result in the smaller body size of adult butterflies (“cost”). Energy compensation hypotheses such as larval aggregation and searching extra-floral nectars were proposed. On the other hand, the attendant ants offer protection and enhance the survival opportunity of the larvae (“benefit”).