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1- by ARISTOBULO LOPEZ AVILA Mo. a Thesis Submitted for the Degree -1- A COMPARATIVE STUDY OF FOUR SPECIES OF Encarsia (HYMENOPTERA: APHELINIDAE) AS POTENTIAL CONTROL AGENTS FOR Bemisia tabaci (GENNADIUS) (HOMOPTERA: ALEYRODIDAE) By ARISTOBULO LOPEZ AVILA Mo. A thesis submitted for the degree of Doctor of Philosophy of the University of London and for the Diploma of Imperial College of Science and Technology Dept. of Pure and Applied Biology Imperial College Field Station Silwood Park Ascot, Berkshire May 1988 -2- ABSTRACT Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) is a serious pest of some important crops in tropical and subtropical regions of the world. The aim of this work was to study some fundamental components of the host-parasitoid interrelationship between it and four species of parasitoids of the genus Encarsia (Hymenoptera: Aphelinidae) in order to estimate their potential for the control of the pest. The study was conducted in the laboratory under enviromentally controlled conditions and quarantine regulations. Some aspects of the biology and morphology of the whitefly and the effect of different host plants on its development were explored in the first phase of the study. The life cycle and survival of the immature stages of B. tabaci were influenced by the host plant on which it developed. A comparative study of aspects of biology, morphology and ecology of the four parasitoid species was conducted. Important differences were found between species in life cycle duration, adult longevity, fecundity, sex ratio, and rates of growth of the population. The four species of Encarsia exhibited a Holling type II functional response. The rate of attack of the parasitoids varied with the host stage exposed, increasing from the earlier to the intermediate instars and then decreasing in the pupal stage. The time spent handling the different host stages showed little variation between the four nymphal instars, but was significantly different in the pupal stage, within parasitoid species. The calculated value of handling time in the four species was far higher than the actual observed time spent parasitizing a host. -3- Differences in number of hosts parasitized between stages within parasitoid species were interpreted as an expression of host preference for the stages more efficiently parasitized. The second, third and fourth nymphal instars were the most efficiently parasitized. The four species of Encarsia exhibited a predatory behaviour characterized by the host-feeding and host-mutilation habits of the females. Results suggested a particular strategy of the these parasitoids when they allocate their feeding and oviposition bouts, using more intensively the youngest and oldest host stages for feeding and the intermediate ones for oviposition. Results also suggested that the predatory behaviour is a significant contributor to the total host mortality and therefore has an important effect in the depression of the host population. Finally, the host plant of the whitefly was shown to have a significant effect on levels of parasitism by two of the parasitoid species. The species Encarsia cibeensis Lopez-Avila and E. adrianae Lopez-Avila were described in the course of this investigation. -4- ACKNOWLEDGEMENTS I am deeply indebted to many people for their help in the course of this work. Foremost among these are my supervisor Dr. J. K. Waage and my advisor Dr. D. J. Greathead for their guidance and encouragement throughout the duration of this study. Sincere thanks are also due to Professor M. P. Hassell, and Drs. T. Ludlow, M. J. Crawley, H. C. J. Godfray, M. J. W. Cock for their advice in different topics of this work. I wish to express my deep gratitude to Mrs. A. H. Greathead for her inexhaustible patience reading and correcting the typescript. I am very grateful for the friendship and occasional helping hand given to me by menbers of CIBC at Silwood Park especially Dr. D. J. O'Donnell, Mr. C. Speed, Mr. T. Cross and members of the Munro Lab. and Insect Ecology group at Silwood Park, Sivasubramaniam Raveendranath (Ravi), Carlos Garcia, and Mike Hochberg deserve special mention. I would also like to thank to Dr. I. A. Mohyuddin at CIBC Pakistan and Professor D. Gerling at Tel Aviv University who forwarded field material to establish the cultures at Silwood Park, Mr. D. J. Girling for finding literature through the computer data bank at CIE. I wish to acknowledge the helping hand given to me by members of the Imperial College staff especially Mr. R. Webb and Mr. C. Merryman in the Glasshouses. My sincere thanks to Dr. D. J. Greathead for the use of the CIBC facilities at Silwood Park. For the finacial assistance I am indebted to the Instituto Colombiano Agropecuario and the Colombian people. Finally, I wish to thank all my friends and the Silwood Park community for making my stay in England a rewarding and unforgettable experience. -5- TABLE OF CONTENTS Page ABSTRACT 2 ACKNOWLEDGEMENTS 4 TABLE OF CONTENTS 5 LIST OF FIGURES 9 LIST OF TABLES 11 CHAPTER 1 INTRODUCTION 14 1.1 Bemisia tabaci as a pest 14 1.2 Biological control 16 1.3 Parasitoids as biological control agents 19 1.4 Characteristics of an effective natural enemy 23 1.5 Aims of this study 24 CHAPTER 2 LIFE HISTORY AND MORPHOLOGY OF THE HOST Bemisia tabaci 26 2.1 Review o f literature 26 2. 1. 1 Taxonomy 26 2. 1. 2 Biology 29 2. 1. 3 Distribution and host plants 30 2. 1. 4 Economic importance 30 2. 1. 5 Natural enemies 38 2. 1. 5. 1 The recorded species 38 2. 1. 5. 2 Encarsia lutea 42 2. 1. 5. 3 Eretmocerus mundus 44 2.2 Biology and morphology of Bemisia tabaci 45 2. 2. 1 Materials and methods 45 2. 2. 2 Results and discussion 50 2. 2. 2. 1 Life cycle and morphology 50 2. 2. 2. 2 Fecundity and preoviposition period 65 -6- Page 2.2.2.3 Parthenogenesis and sex ratio 66 2.3 Life cycle on five host plant species 67 2.3.1 Matarials and methods 67 2.3.2 Results and discussion 68 CHAPTER 3 COMPARATIVE BIOLOGY, MORPHOLOGY AND ECOLOGY OF THE PARASITOID SPECIES 72 3. 1 Review of literature 72 3.1.1 Encarsia formosa 72 3.1.2 Encarsia deserti 78 3.1.3 Encarsia cibeensis and Encarsia adrianae 79 3. 2 Life history and morphology 79 3.2.1 Materials and methods 80 3.2.2 Results and discussion 84 3. 3 Effect of the host stage on parasitism and development of the parasitoid species 105 3.3.1 Materials and methods 107 3.3.2 Results and discussion 108 3. 4 Adult longevity 118 3.4.1 Materials and methods 120 3.4.2 Results and discussion 121 3. 5 Oviposition, mating and feeding behaviour 122 3.5.1 Materials and methods 126 3.5.2 Results and discussion 128 3. 6 Fecundity 140 3.6.1 Materials and methods 141 3.6.2 Results and discussion 143 3. 7 Sex ratio 152 3.7.1 Materials and methods 155 -7- Page 3.7.2 Results and discussion 157 3.8 Rate of growth of the populations of the parasitoids 161 3.8.1 Introduction 161 3.8.2 Results and discussion 163 CHAPTER 4 EFFECT OF THE HOST DENSITY ON LEVELS OF PARASITISM AND OTHER FACTORS AFFECTING EFFICIENCY 166 4.1 Comparative functional responses 166 4.1.1 Review of literature 166 4.1.1.1 Type I Functional Response 167 4.1.1.2 Type II Functional Response 170 4.1.1.3 Type III Functional Response 172 4.1.1.4. The domed type of functional response curve 175 4.1.1.5 Estimating parameter values 176 4.1.2 Materials and methods 179 4.1.3 Results and discussion 181 4.2 Overall host mortality 219 4.2.1 Introduction 219 4.2.2 Materials and methods 222 4.2.3 Results and discussion 222 4.3 Survival of the parasitoid progeny 227 4.3.1 Introduction 227 4.3.2 Materials and methods 228 4.3.3 Results and discussion 228 CHAPTER 5 EFFECT OF THE HOST PLANT ON LEVELS OF PARASITISM 231 5.1 Introduction 231 5.2 Materials and methods 233 5.3 Results and discussion 234 -8- Page CHAPTER 6 GENERAL DISCUSSION AND CONCLUSIONS 237 APPENDIX 1 Two new species of Encarsia Foerster (Hymenoptera: Aphelinidae from Pakistan, associated with the cotton whitefly, Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) 249 APPENDIX 2 Experimental results of effect of host density on levels of parasitism 255 APPENDIX 3 Mean number of hosts parasitized by four species of Encarsia on five stages and six densities of Bemisia tabaci 268 APPENDIX 4 Life and fertility tables and rate of growth of the populations of four species of Encarsia 270 APPENDIX 5 Partial derivatives of the functions with respect to the parameters a' and Th 274 BIBLIOGRAPHY 275 -9- LIST OF FIGURES Figure Page 1. The presently recorded distribution of Bemisia tabaci. 31 2. Rearing cage. 48 3. Cylindrical cage. 48 4. Bemisia tabaci egg. 62 5. Bemisia tabaci first nymphal instar. 62 6. Bemisia tabaci pupal stage. 62 7. Bemisia tabaci vasiform orifice. 62 8. Survival curves of immature stages of Bemisia tabaci. 71 9. Leaf cage and its position on a plant. 81 10. Encarsia adrianae egg. 86 11. Encarsia adrianae third larval instar. 90 12. Pupal cases. 94 13. Developmental duration of four species of Encarsia. 102 14. Relationship between parasitism and the stage of host exposed to parasitoid. 110 15. Effect of the host stage on the developmental duration of the parasitoids. 116 16. Survival curves for Encarsia formosa, E. deserti E. cibcensis and E. adrianae. 124 17. Encarsia adrianae female in oviposition posture.
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