Biological Responses and Control of California Red Scale Aonidiella Aurantii (Maskell) (Hemiptera: Diaspididae)

Biological responses and control of California red scale Aonidiella aurantii (Maskell) (Hemiptera: Diaspididae) by Khalid Omairy Mohammed Submitted to Murdoch University in fulfilment of the requirements for the degree of Doctor of Philosophy College of Science, Health, Engineering and Education Murdoch University Perth, Western Australia March 2020 Declaration The work described in this thesis was undertaken while I was an enrolled student for the degree of Doctor of Philosophy at Murdoch University, Western Australia. I declare that this thesis is my own account of my research and contains as its main content work which has not previously been submitted for a degree at any tertiary education institution. To the best of my knowledge, all work performed by others, published or unpublished, has been duly acknowledged. Khalid O. Mohammed Date: March 10, 2020 I Acknowledgements بِ ْس ِمِِاللَّ ِـه َِّالر ْح َم ٰـ ِن َِّالر ِح ِيمِ ُ َويَ ْسأَلُ َونَك َِع ِن ُِّالروحِِِۖقُ ِل ُِّالر ُوح ِِم ْنِأَ ْم ِر َِر ِب َيِو َماِأ ِوتيتُ ْم ِِم َن ِْال ِع ْل ِمِإِ ََّّل َِق ِل ايًلِ﴿٨٥﴾ The research for this thesis was undertaken in the School of Veterinary and Life Science, Murdoch University. I would like to express my heartfelt gratitude to my supervisors Professor Yonglin Ren and Dr Manjree Agarwal “Postharvest Biosecurity and Food Safety Laboratory Murdoch” for their support with enthusiasm, constructive editing, and patience throughout the years of this wonderful project. I deeply appreciate their encouragement, assistance and for being so willing to take me on as a student. I would like to express my sincere gratitude to all those who helped me in completing this thesis. I thank all the members of the Postharvest Biosecurity and Food Safety Laboratory staff members in the past and present especially Mr James Newman and Mr Xin Bob Du for their helpfulness and supporting use of the experimental equipment and facilities. My sincere gratitude also goes to Professor Giles Hardy and Professor Ismail Karaka. Their names were not officially listed in my supervisors, but indeed they are both playing an indispensable role in directing me to complete my thesis. They gave me great support and help in the statistical analysis of raw data, in conceiving questions addressed and setting assumptions in models, and in checking and revising papers. I thank the Manager of Murdoch University farm in Whitby, Western Australia Bob Fawcett for allowing us doing some experiments and collecting citrus fruit specimens for this study. I would like to thank my family; my wife Saba Al-qassab and my kids for their love, support and endurance. Special thanks to my mother, brothers and sisters who share happiness and good wishes. Thank you for trusting me! Thanks to all my friends, especially Brian Smith and Penny Kirkland-Smith, for encouragement and good wishes. I was nominated to study a PhD by Mosul University, and this PhD project was funded by Iraqi Ministry of High Education and Scientific Research. I am very grateful indeed for this support. II Abstract In many citrus areas around the world and within citrus-producing regions of Australia, the California red scale (CRS), Aonidiella aurantii (Maskell) (Hemiptera: Diaspididae), is considered the most important pests of citrus. The main biological control agents of Ao. aurantii in this zone are the parasitoid Aphytis melinus DeBach (Hymenoptera: Aphelinidae). In order to improve the biological control of Ao. aurantii several biotic and abiotic factors were studied, that may affect the efficiency of A. melinus in the laboratory and the field. More concretely, reproductive potential and age-specific fecundity schedules of Ao. aurantii were studied in the laboratory at constant temperatures (20, 23 and 27°C), while the biological parameters of its parasitoid A. melinus were conducted at 27°C. Results revealed that the net reproduction rate (Ro) was considerably higher for Ao. aurantii than A. melinus, which reached 28.14 at 27°C, indicating its high reproductive capacity. Moreover, the net reproduction rate obtained for A. melinus indicates a low substitution potential for each female having Ao. aurantii as a host under laboratory conditions. The intrinsic rate of increase (rm) of A. melinus (0.188 ♀/♀/day) was significantly greater than that of Ao. aurantii (0.080) at 27°C. Plants produce volatile organic compounds (VOCs) in response to herbivore attack, and these VOCs can be exploited by parasitoids of the herbivore as host location cues. The VOCs from non-infested and Ao. aurantii-infested citrus fruit were investigated using headspace solid- phase microextraction (HS-SPME) coupled with gas chromatography-mass spectrometry (GC- MS). The data showed that more than 52 different compounds were identified, and different emissions associated attributed to herbivore activity were found for all fruit species (lemon, orange, mandarin and Tahitian lime). However, a single compound was exclusively produced by infested lemon fruit, while two compounds were significantly increased, and two compounds were only present in non-infested lemon. Five compounds were significantly increased in infested mandarins. For orange, five compounds were increased, and five compounds were exclusively presented in infested fruit. For lime fruit, eighteen of these compounds were increased, one was decreased, whereas five compounds were produced exclusively from infested lime fruit. Two putative herbivores-induced plant volatiles, d- limonene and 훽-ocimene, were significantly increased by Ao. aurantii infestation in all infested fruit, regardless of the citrus species. Subsequently, the preferences of female parasitoid on infested or healthy fruit in olfactometer bioassays were evaluated. Then in order to understand the magnitude of volatile attractiveness, III the innate attractiveness of VOCs to A. melinus females in varying densities were tested in the laboratory. The results of the olfactometer assays that tested the behaviour of A. melinus to the different compounds emitted from infested and non-infested citrus fruit showed no such preference when compared between non-infested and infested oranges, mandarins and lime fruit; whilst, there were significant preferences for lemon fruit infested with Ao. aurantii over non-infested ones. For assessment, the attraction of synthetic Herbivore induced plant volatiles (HIPVs), four different concentrations (5,10, 15 and 20 μl/ml) of d-l-limonene and 훽-ocimene were investigated. However, mated A. melinus females preferred the reward-associated VOC more than hexane control in the case of d-limonene at the tested dosages of 15 and 20 μl/ml, 훽-ocimene at tested dosages of 10, 15 and 20 μl/ml. Finally, this study evaluated the dispersal ability of released A. melinus adults and their effect on the parasitism percentage, using d-limonene and 훽-ocimene with yellow sticky traps and scoring percentage parasitism on infested fruit. Under field conditions, the natural enemies’ effectiveness in controlling pests is largely correlated with their capability to spread towards infested crops. In this study, d-limonene and 훽-ocimene were examined for their attractiveness to California red scale parasitoid A. melinus in the field after augmentative releases. Field experiments demonstrated that lures baited with isolates of d-limonene and\or 훽-ocimene, which significantly attracted some species of natural enemies but had no significant impact on others. The number of A. melinus captured during the whole trial was greater in the traps treated with volatiles than the control. Finally, the overall parasitism rates were not increased by synthetic HIPV lures, but there was evidence that lures may increase parasitism of California red scale when there is a decrease in the amount of volatile organic compounds due to lack of healthy and infested fruit. In conclusion, HIPVs can potentially play important roles in attracting and exploiting natural enemies to reduce pest infestations. IV Table of Contents Declaration I Acknowledgements II Abstract III Table of contents V List of tables X List of figures XI Publications and presentations XIII Poster Presentations XIII List of abbreviations XV Chapter One 1 General introduction and literature review 1.1 General Introduction 2 1.2. Literature Review 5 1.2.1. Citrus 5 1.2.2. The California red scale, Aonidiella aurantii (Maskell) 6 1.2.2.1. Systematic classification of Aonidiella aurantii 7 1.2.2.2. Origin and distribution 8 1.2.2.3. Host plants 8 1.2.2.4. Injurious effects of Aonidiella aurantii 9 1.2.2.5. Life cycle stages of Aonidiella aurantii 10 1.2.2.5.1. Morphology and developmental stages of Aonidiella aurantii 10 1.2.2.5.2. Sex ratio 12 1.2.2.5.3. Ecology and life cycle of Aonidiella aurantii 12 1.2.2.5.3.1. Influence of abiotic factors 12 1.2.2.5.3.2. Influence of biotic factors 14 1.2.3. Biological control of Aonidiella aurantii 15 1.2.3.1. Classification of parasitoids 17 1.2.3.2. Ectoparasitoids of Ao. aurantii: Aphytis Howard 18 1.2.3.2.1. Life history and morphology of Aphytis 20 1.2.3.2.2. Biology and ecology of Aphytis 22 1.2.3.2.3. Factors affecting Aphytis efficiency 24 1.2.3.2.3.1. Abiotic factors 24 1.2.3.2.3.2. Biotic factors 25 1.2.3.2.4. Ahytis melinus DeBach 29 1.2.4. Age-specific fecundity tables 30 1.2.5. Volatile organic compounds 33 1.2.5.1. Volatile compounds released from the plants 34 1.2.5.2. Volatiles released by citrus fruit 35 V 1.2.5.3. Herbivore-Induced Plant volatiles 36 1.2.5.4. Synthetic herbivore-induced plant volatiles 37 1.2.5.4.1. D-limonene 38 1.2.5.4.2. 훽-ocimene 39 1.2.6. Host search in parasitoids 40 1.2.7. Insect olfaction and olfactory learning in parasitoids 42 1.2.8.

Load more