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Development, Swarming, Colony DEVELOPMENT, SWARMING, COLONY ORPHANING AND FLY PARASITISM IN SUBTERRANEAN TERMITES, Macrotermes gilvus (Hagen) AND Macrotermes carbonarius (Hagen) (BLATTODEA: TERMITIDAE) NEOH KOK BOON UNIVERSITI SAINS MALAYSIA 2010 DEVELOPMENT, SWARMING, COLONY ORPHANING AND FLY PARASITISM IN SUBTERRANEAN TERMITES, Macrotermes gilvus (Hagen) AND Macrotermes carbonarius (Hagen) (BLATTODEA: TERMITIDAE) by NEOH KOK BOON Thesis submitted in fulfillment of the requirements for the degree of Doctor of Philosophy April 2010 ACKNOWLEDGEMENT I would like to express my sincere appreciation to my supervisor, Professor Dr. Lee Chow Yang, for his endless guidance, assistance and advice throughout this research. I would like to thank my family especially my parents for their patience, understanding and support. Thanks to Lee Jin, who is always by my side and giving me endless support and assistance. Not forgetting all lab mates in the Urban Entomology Laboratory, Yee Fatt, Sam, Hui Siang, Evan, Tomoki, Rivo, Nellie, Ru Yuan, Beng Keok, Lay Tyng, Veera, Foong Kuan, Ching Cheng, Jia Wei, Ling Hui, Nadiah; former graduate students, Boon Hoi, Kim Fung, Jing Wen, not only for their help but also bringing the joyousness into my life. Gratitude is also directed to Associate Professor Dr. Zairi Jaal, the coordinator of Vector Control Research Unit, School of Biological Sciences, Universiti Sains Malaysia, who has given support and encouragements. I am also grateful to Dr. Michael Lenz (CSIRO, Australia) and Associate Professor Dr. Hu Xing Ping (Auburn University, US) for their guidance, assistance and advice. I would like to extend my appreciation to Mr. V. Somasundram, Puan Sabariah, Mr. Adrian from School of Biological Sciences and staffs of Vector Control Research Unit, especially Mr. Adanan, Mr. Nasir, Mr. Mahmud, Mr. Hamid, Mr. Rohaizat, Kak Siti, Kak Aishiah and Kak Ida for their technical assistance, equipment support and friendship. ii TABLE OF CONTENTS Page ACKNOWLEDGEMENTS ii TABLE OF CONTENTS iii LIST OF TABLES vii LIST OF FIGURES ix ABSTRAK xiii ABSTRACT xvi CHAPTER ONE: INTRODUCTION 1 CHAPTER TWO: LITERATURE REVIEW 2.1 Termites 3 2.2 Fungus-growing termites (subfamily Macrotermitinae) 4 2.2.1 Macrotermes gilvus 6 2.2.2 Macrotermes carbonarius 7 2.3 Economic importance of Macrotermitinae 9 2.4 Termites as beneficial insects 10 2.5 Castes of termites 11 2.5.1 Caste development pathways 13 2.6 Colony foundation and swarming 16 2.6.1 Abiotic factors 17 2.6.2 Biotic factors 18 2.6.3 Reproductive isolation 22 2.7 Secondary reproductives 23 2.7.1 Polygyny 24 2.7.2 Reproductive conflict 25 2.8 Parasitism 29 2.8.1 Family Calliphoridae 30 2.8.2 Family Phoridae 31 iii CHAPTER THREE: DEVELOPMENTAL STAGES AND CASTES OF TWO SYMPATRIC SUBTERRANEAN TERMITES Macrotermes gilvus (Hagen) AND Macrotermes carbonarius (Hagen) 3.1 Introduction 36 3.2 Materials and methods 3.2.1 Study site and specimen collection 37 3.2.2 Measurements of termite castes 37 3.2.3 Sex determination 39 3.3 Results 41 3.3.1 Larvae 41 3.3.2 Workers 41 3.3.3 Nymphs 46 3.3.4 Soldiers 46 3.3.5 Alates 49 3.4 Discussion 53 CHAPTER FOUR: FLIGHT ACTIVITY OF TWO SYMPATRIC TERMITE SPECIES, Macrotermes gilvus (Hagen) AND Macrotermes carbonarius (Hagen) 4.1 Introduction 57 4.2 Materials and methods 4.2.1 Study sites 58 4.2.2 Trapping of termite alates 58 4.2.3 Meteorological data 59 4.2.4 Data analysis 59 4.2.5 Field trip 62 4.2.6 Collection of sexual caste specimens 62 4.3 Results 4.3.1 Number of alates and period of flight 63 4.3.2 Seasonal production of sexual castes 65 iv 4.3.3 Relationship of flight activity to environmental variables 65 4.3.4 Relative frequency 73 4.5 Discussion 76 CHAPTER FIVE: IMPACT OF ORPHANING ON FIELD COLONIES OF Macrotermes gilvus (Hagen) AND M. carbonarius (Hagen) (Termitidae: Macrotermitinae) 5.1 Introduction 80 5.2 Materials and methods 81 5.3 Results 5.3.1 Colony orphaning after selected time intervals 83 5.3.2 Colony composition and the success rate of colony 89 re-establishment 5.3.3 Naturally orphaned field colonies 92 5.4 Discussion 96 CHAPTER SIX: MORPHOLOGICAL AND BEHAVIORAL CHANGES IN SOLDIERS OF Macrotermes gilvus (Hagen) (Termitidae: Macrotermitinae) PARASITIZED BY THE FLY Misotermes mindeni Disney & Neoh (Diptera: Phoridae) 6.1 Introduction 100 6.2 Materials and methods 6.2.1 Parasitism surveillance 101 6.2.2 Insect rearing 101 6.2.3 Pupation process of larval parasitoid from host (n=5) 102 6.2.4 Determination of parasitized host’s stages 102 6.2.5 Aggression behaviour 103 6.3 Results 6.3.1 Survey of dipteran parasitoid 103 6.3.2 The pupation process 104 v 6.3.3 Morphological changes 107 6.3.4 Behavioral changes 111 6.4 Discussion 114 CHAPTER SEVEN: PARASITOID-INDUCED MORPHOLOGICAL AND BEHAVIORAL CHANGES IN INFECTED SOLDIERS OF THE FUNGUS-GROWING TERMITE, Macrotermes carbonarius (Termitidae: Macrotermitinae) 7.1 Introduction 118 7.2 Materials and methods 7.2.1 Study sites 119 7.2.2 Pupation process of larval parasitoid 119 7.2.3 Morphometric analysis 119 7.2.4 Agonistic test 120 7.3 Results 7.3.1 Dipteran parasitoid infestation rates 120 7.3.2 Pupation of larval parasitoid from host 121 7.3.3 Morphological and behavioral alterations of host 123 7.3.4 Susceptibility of host caste to parasitization 125 7.4 Discussion 128 SUMMARY AND CONCLUSION 133 REFERENCES 139 LIST OF PUBLICATIONS & SEMINARS CURRICULUM VITAE vi LIST OF TABLES Page Table 2.1 Effects of environmental variables on termite flight activity 20 and flight patterns in different regions. Table 2.2 Selected species of subterranean termite with records of 26 secondary reproductives. A, adultoid; PI, pseudoimago; MI, microimago; Ny, nymphoid; E, ergatoid; N1–N5, nymphs of stages 2 through 5. Table 2.3 Records of the termite associated phorid flies and blow flies 33 (Diptera: Phoridae; Calliphoridae) in subfamily Macrotermitinae. Table 3.1 Range and mean (in parentheses) of measurements of larval 42 instars, workers, presoldiers, and nymphs from M. gilvus (in mm). Table 3.2 Range and mean (in parentheses) of measurements of larval 43 instars, workers, presoldiers, and nymphs from M. carbonarius (in mm). Table 3.3 Range and mean (in parentheses) of measurements of the 48 soldiers of M. gilvus and M. carbonarius (in mm). Table 3.4 Range and mean (in parentheses) of measurements of the 50 alates of M. gilvus and M. carbonarius (in mm), n = 10 (mixed sexes) for each species. Table 3.5 Range and mean (in parentheses) of measurements of the 51 mandibles of the alates from M. gilvus and M. carbonarius (in mm), n = 10 (mixed sexes) for each species. Table 4.1 Environmental conditions and flight time of M. 67 gilvus and M. carbonarius. Table 5.1 Number and fresh weight of reproductives before and 85 after orphaning in colonies of M. gilvus (in parentheses, mean and SD). Table 5.2 Number and fresh weight of reproductives before and after 90 orphaning in colonies of M.carbonarius . vii Table 6.1 Range and mean (in parentheses) of measurements of 109 individuals in the parasitized soldiers (n = 20) and healthy soldiers (major soldier, n = 10) of M. gilvus. Table 6.2 Aggression behaviours of parasitized soldiers and healthy 113 soldiers of M. gilvus (Mean ± SE, n = 7 for each combination). Table 7.1 Range and mean (in parentheses) of measurements in 124 individuals of the parasitized soldiers (major soldier, n = 10; minor soldier, n = 8) and healthy soldiers (major soldier, n = 24; minor soldier, n = 20) of M. carbonarius. Table 7.2 Aggression behaviour indices of parasitized soldiers and 126 healthy soldiers of M. carbonarius (mean ± SE, N a = 10 and Nb = 6). \ viii LIST OF FIGURES Page Figure 2.1 Major soldier. (A) M. gilvus ; (B) M. carbonarius 8 Figure 2.2 Central developmental pathway of Kalotermitidae (A) and 16 forked developmental pathway of Rhinotermitidae and Termitidae (B). E, egg; L1–L5, larval instars; N1–N2, nymphal instars; A, alates; PS, presoldier; PD, pseudergates; S, soldier. Modified from Roisin (2000) Figure 3.1 Diagram of measured parts of a termite. (a) WH = width of 38 head; WS = width of head to side base of mandibles; LS = length of head to side base of mandibles; LA = length of antenna. (b) WP = width of postmentum; LP = length of the postmentum. (c) WPr = width of pronotum; WMs = width of mesonotum; WMt = width of metanotum; LPr = length of pronotum. (d) LT = length of third hind tibia. (e) LH = length of head to tip of labrum; LE = long diameter of eye; SE = short diameter of eye; DO = distance between eye and ocellus. (f) D1 = distance between apical tooth and first marginal tooth; D2 = distance between first marginal tooth and second marginal tooth; D3 = distance between second marginal tooth and molar prominence; LM = length of molar plate; L1 = posterior cutting edge of apical tooth; L2 = anterior cutting edge of first marginal tooth; L3 = posterior cutting edge of first marginal tooth; L4 = anterior cutting edge of second marginal tooth Figure 3.2 Ventral abdomen of the larval instars after removal of fat 40 tissue, gut, and ventral cord and hematoxylin staining for sex determination: (A) female and (B) male. The rudiment of the spermatheca is only found in sternite 8 of the female. Scale bar = 0.5 mm. Figure 3.3 Canonical discriminant functions of the caste system in M. 44 carbonarius . L1 = first larval instar; FL2 – FL4 = female second to fourth larval instars; ML2 – ML3 = male second and third larval instars; N2(?) – N3(?) = predicted nymphal instars; W = major worker; PS = major presoldier; S = major soldier; w = minor worker; ps = minor presoldier; s = major soldier; A = alate.
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