臺灣博碩士論文加值系統

養菌白蟻 (fungus-growing termite) 包含蜚蠊目 (Blattodea) 白蟻科 (Termitidae) 大白蟻亞科 (Macrotermitinae) 下所有的物種，具有建造菌圃 (fungus garden)、培養Termitomyces spp.真菌為食的行為，養菌白蟻廣布於古北區、衣索比亞區及東洋區，為熱帶及亞熱帶森林中主要的分解者，同時也是重要的農業害蟲。我的論文是以台灣的一種養菌白蟻，台灣土白蟻 (Odontotermes formosanus (Shiraki)) 為材料，研究養菌白蟻的族群建立機制 (第一章) 、覓食物候 (第二章) 及營養生態學 (第三章)。論文的最後 (第四章)，我統整目前養菌白蟻餌劑防治所遭遇的困難、並以我的研究結果推測其原因、作為總結。

養菌白蟻的族群建立機制
養菌白蟻在群體建立 (colony establishment) 的階段，必須搜尋築巢位置、挖掘土壤以建造蟻巢、且在建造菌圃前無法獲得營養，因此在群體建立的階段有較高死亡率。野外的養菌白蟻常以多雌性 (pleometrosis) 之方式建立群體，較多的繁殖型個體可能增加其適存度，但未被驗證。為了驗證較多的繁殖型個體是否在族群建立階段具有優勢，本研究將台灣土白蟻的雌雄繁殖型配對，以1-4對不同的配對數建立初始群體，一共建立了647個群體，並量化其搜尋築巢位置及挖掘蟻巢的效率、群體存活率及蟻巢內每個個體的存活率、以及量化每個群體的繁殖力。研究結果顯示，台灣土白蟻的繁殖型會在搜尋築巢位置時，加入正在挖掘蟻巢的群體，降低其搜尋築巢地點的時間。當群體的繁殖型數量增加時，挖掘的蟻巢深度及空間亦增加，但每個繁殖型個體所獲得的空間會減少。分析繁殖型數量對生存率及族群成長的影響，發現1對的群體較易因損失單一的個體而死亡、而個體死亡率在群體具有3對繁殖型時顯著增加，繁殖力隨繁殖型數量增加。檢視屍體上觸角及足損失的頻率，發現其與繁殖型數量呈正相關，推測過多的繁殖型增加個體間的攻擊性。研究結果支持2對繁殖型的新群體在生存率及族群成長上較有優勢。

養菌白蟻的營養生態學
養菌白蟻的覓食行為被認為具季節性，且可能與氣候因子及天敵的發生頻率有關。為了驗證這些假說，我自2013年開始，每月監測484根木樁上台灣土白蟻的發生率、取食量、及覓食群體大小，並以路徑分析 (path analysis) 檢測氣候因子、螞蟻的發生頻率及兩者的交互作用對台灣土白蟻覓食活動之影響 (第二章)。結果顯示，溫度及雨量為影響台灣土白蟻覓食季節性的主要因子。台灣土白蟻在較濕熱的季節會佔據較少的木樁，該季節的螞蟻的發生頻率亦較高，但路徑分析顯示白蟻與螞蟻的發生頻率並無直接關聯，而是各自反應氣候因子。由於台灣土白蟻每個月捨棄大部分佔據的木樁、並尋找新的木樁，推測其具有”吃即跑” (eat-and-run) 之覓食策略。
養菌白蟻透過建造菌圃培養真菌的過程，將採集到的植物組織轉換為真菌孢子球 (fungal nodule) 與成熟菌圃 (aged fungus garden) 兩種食物，藉此獲得營養。為了瞭解真菌轉換是否增加食物對白蟻的營養價值，本研究分析了三個地點台灣土白蟻體內、孢子球、及其菌圃在發酵前與發酵後的α-氨基酸及脂肪酸之組成。研究結果顯示，各地的新鮮菌圃營養組成均不相同、而成熟菌圃及孢子球營養組成相似，菌圃發酵會將營養的比例均質化、轉換為與白蟻體內營養相似的比例，推測白蟻藉由菌圃發酵生產均質且均衡的營養，有助於適應其多樣的食物組成。另外，比較孢子球與菌圃上的胺基酸組成，發現菌圃中無法偵測到色胺酸、其出現於孢子球中。由於色胺酸為必需胺基酸，推測真菌可能透過減少菌圃內的色胺酸濃度、或增加孢子球內的色胺酸濃度，促進白蟻傳遞其孢子。

養菌白蟻餌劑防治困難之文獻回顧及論文總結
目前的白蟻餌劑是針對取食木建構物及樹木的地下白蟻 (Rhinotermitidae) 所設計。白蟻餌劑通常以幾丁質合成抑制劑為有效成分、並以纖維素材料作為介質。餌劑的施作方式是在白蟻覓食的地點設置監測餌站，餌站內包含木料及餌劑供白蟻取食。在熱帶及亞熱帶地區使用白蟻餌劑時，除了地下白蟻外、養菌白蟻也會取食餌劑，目前白蟻餌劑被認為無法有效地防治養菌白蟻，且其原因不明。本研究統整過去的文獻，發現幾丁質合成抑制劑能在養菌白蟻的不同階級之間傳播、會使幼蟲死亡率增加、且對群體大小有負面影響，推測幾丁質合成抑制劑並非防治無效之原因。養菌白蟻會分別搜尋纖維素介質及蛋白質介質的材料，而目前的白蟻餌劑皆是以纖維素為介質，應難以符合養菌白蟻的營養需求。此外，由於養菌白蟻具有 ”吃即跑” 的覓食策略、每個月捨棄70-90% 其佔據的食物資源，監測站亦難以持續誘捕白蟻取食。根據以上結果，推測白蟻餌劑在營養上的不平衡及現今的餌站監測方式為防治無效之原因，若能以監測區域內白蟻活動力的方式評估餌劑效力、並增加餌劑中蛋白質的比例，可能改進白蟻餌劑對養菌白蟻的防治效果。

Fungus-growing termites represent all species under the Order Blattodea, Family Termitidae, and subfamily Macrotermitinae, which construct fungus gardens, and cultivate the symbiont fungus Termitomyces spp. as food. Fungus-growing termite widely distributed in Palearctic region, Ethiopian region, and Oriental region, is a major decomposer in tropical and subtropical forests, and also an agriculture pest. In this thesis, I majorly studied the colony establishment mechanisms (Chapter 1), foraging phenology (Chapter 2), and nutritional ecology (Chapter 3) of a single species of fungus-growing termites, Odontotermes formosanus (Shiraki). In the overall conclusion (Chapter 4), I summarized the current challenges on baiting of fungus-growing termites, and proposed solutions, based on my own researches.

Colony establishment of fungus-growing termites
Fungus-growing termites encounter multiple stresses in colony-founding stage, such as the searching of nesting site, excavation of nest, no supply of nutrition before establishment of fungus gardens. Only few of the incipient colonies survived in colony-founding stage. In field, fungus-growing termites were commonly observed founding a colony by pleometrosis, which is hypothesized to increase the fitness. To test the impact of pleometrosis on colony-founding success, I established a total of 647 colony-founding groups with 1-4 pairs of termite alates of O. formosanus in laboratory, and observed their excavation behavior, recorded the survival rates and counted number of each caste. I found that alates of O. formosanus decreased the time of searching nesting site and increased the depth and space of nest by joining the groups that have started excavation. By analyzing the impact of pair number on survival rate and colony growth, I found that pair number and colony growth rate were positively correlated, one-pair groups are more likely to fail with the mortality of one single individual, and the individual mortality significantly increased in three-pair groups. I examined the corpses of alates, and found that the occurrence of broken body parts was correlated with pair number, supported aggression increased with pair number. Overall, two-pair groups are advantageous on colony survival and growth.

Nutritional ecology of fungus-growing termites
Foraging behavior of fungus-growing termites was hypothesized to be seasonal, and correlated with climatic factors and occurrence of natural enemy. To test these hypotheses, I started to monitor the monthly occurrence, consumption, foraging population size of O. formosanus on 484 wood stakes, since 2013 (Chapter 2). By using path analysis, I found that temperature and rainfall were the major factors affected foraging activity of O. formosanus. O. formosanus occupied less number of wood stakes in hot-wet seasons, which were generally high in ant occurrence. The result of path analysis also showed that termite activity and ant occurrence contrast responded to climatic factors. We suggest O. formosanus performed eat-and-run foraging strategy, since they leaved most of the wood stakes occupied and forage new wood stakes monthly.
Fungus-growing termite transform plant nutrition into two fungal products as food, namely fungal nodule and aged fungus garden. To understand the nutritive values of fungal nodule and aged fungus garden to termites, I analyzed the compositions of α-amino acids and fatty acids in termite tissue, fungal nodule, and fresh and aged fungus gardens in three localities. The results showed nutritional composition in fresh fungus garden was different among localities, and that of aged fungus garden or fungal nodules were similar among localities. Fungal transformation homogenized and transformed the nutritional composition, and the nutritional composition was similar to that of termites, which may benefit termites on adapting the variation of diet nutrition. In addition, an essential amino acid, tryptophan was present only in fungal spores. I hypothesized that the symbiont fungus forced termites to transfer fungal spores by decreasing the concentration of tryptophan in fungus garden or increasing the concentration of tryptophan in fungal nodules.

Overall conclusion with special reference to challenges on baiting of fungus-growing termites in the light of their biology
Termite bait is designed to control the subterranean termites (Rhinotermitidae) which attack wood structures and trees. Modern termite baits majorly constitute chitin synthesis inhibitor (CSI) as active ingredient and a cellulose-based matrix. Application of termite bait requires to install monitoring stations at the foraging sites of termites, which contains pieces of wood to recruit termites or the CSI baits to control termites. In tropical and subtropical areas, termite baits were consumed by not only subterranean termites, but also by fungus-growing termites (Termitidae: Macrotermitinae). Termite baits were reported being inefficient to suppress the colony of fungus-growing termites, and the cause is unknown. Previous studies confirmed that CSIs were transferred between castes, lethal to larvae, and significantly reduced colony size of fungus-growing termites. I suggest CSI is not the cause of bait inefficacy. Different to subterranean termites, fungus-growing termites forage for both cellulose-based and protein-based diets. Modern termite baits are all cellulose-based, not likely to satisfy the nutritional requirement of fungus-growing termites. Fungus-growing termites performed an eat-and-run foraging strategy by leaving 70–90% of the pieces of wood they occupied per month, in consequence, monitoring stations are not likely to recruit the termites continuously. I suggest the imbalanced bait matrix and the termite monitoring method are the causes of bait inefficacy.

TABLE OF CONTENTS

Chapter 1 Colony-founding success of pleometrosis in a fungus-growing termite Odontotermes formosanus………1


1.1. Introduction………2
1.1.1. Colony foundation through pleometrosis………2
1.1.2. Polygamy and pleometrosis in termites………2
1.1.3. Costs and benefits of pleometrosis for termites………3
1.1.4. Purpose of this study………4

1.2. Material and Methods………5
1.2.1. Alate sampling………5
1.2.2. Nest excavation bioassay………5
1.2.3. Colony-survival bioassay………6
1.2.4. Field observation………7
1.2.5. Statistical analysis………8

1.3. Results………15
1.3.1. Nest excavation………15
1.3.2. Mortality and mutilation………15
1.3.3. Colony growth………17
1.3.4. Survival of pleometrotic groups in the field………17

1.4. Discussion………21
1.4.1. Benefits of pleometrosis………21
1.4.2. Adverse effects of pleometrosis………22
1.4.3. Pleometrosis in subfamily Macrotermitinae………24
 

Chapter 2 Foraging phenology of the fungus-growing termite Odontotermes formosanus (Blattodea: Termitidae)………25


2.1. Introduction………26
2.1.1. Fungus-growing termites as forest decomposer and agriculture pest………26
2.1.2. Foraging behavior of fungus-growing termites………26
2.1.3. Impact of climatic factors and natural enemy………27
2.1.4. Purpose of this study………28

2.2. Material and Methods………29
2.2.1. Experimental plot………29
2.2.2. Climatic factors and ant presence………30
2.2.3. Statistical analysis………31

2.3. Results………39
2.3.1. Seasonality of the foraging activity of O. formosanus………39
2.3.2. Direct and indirect effects of climatic factors………39

2.4. Discussion………44
2.4.1. Major climatic factors: temperature and rainfall………44
2.4.2. Climatic factors have various effects on foraging behaviors………45
2.4.3. Eat-and-run foraging strategy………45
 

Chapter 3 Nutritional allocation enhanced the mutualism between fungus-growing termites and their symbiont fungi………47


3.1. Introduction………48
3.1.1. Insect agriculture system………48
3.1.2. Agriculture system of Odontotermes formosanus………48
3.1.3. Functions of α-amino acids and fatty acids………49
3.1.4. Fungi as regulator of α-amino acids and fatty acids………50
3.1.5. Purpose of this study………51

3.2. Material and Methods………53
3.2.1. Sampling of fungus garden and termites………53
3.2.2. Estimating the amounts of fungal nodules harvested………54
3.2.3. Analysis of nutrition………56
3.2.4. Statistical analysis………57

3.3. Results………60
3.3.1. Production of fungal nodules………60
3.3.2. Nutrition of fungal nodules and fungus gardens………60
3.3.3. Nutrition of termites………61

3.4. Discussion………66
3.4.1. The nutritional function of nodules and aged fungus garden………66
3.4.2. Nitrogen source of fungus-growing termites………68
 

Chapter 4 Overall conclusion with special reference to challenges on baiting of fungus-growing termites in the light of their biology………72


4.1. Introduction………73
4.1.1. Baiting of fungus-growing termites………73
4.1.2. Fungus-growing termites as pest………74
4.1.3. Chemical control of fungus-growing termites………75

4.2. Chitin synthesis inhibitor as active ingredient………77
4.2.1. Effects of chitin synthesis inhibitor………77
4.2.2. The transfer of chitin synthesis inhibitor………77

4.3. Bait matrix composition………80

4.4. Monitoring and baiting of termite colony………82

4.5. Conclusion………83


List of reference………84

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