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Citrus Host Utilisation by the Queensland Fruit Fly, Bactrocera Tryoni (Frogatt) (Diptera: Tephritidae): from Individuals to Populations

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Citrus Host Utilisation by the Queensland Fruit Fly, Bactrocera Tryoni (Frogatt) (Diptera: Tephritidae): from Individuals to Populations Citrus host utilisation by the Queensland fruit fly, Bactrocera tryoni (Frogatt) (Diptera: Tephritidae): from individuals to populations W. Sakuntala Nayanatara Muthuthantri, B.Sc. (Agriculture), M.Phil. Submitted in fulfilment of the requirements for a Doctor of Philosophy School of Earth, Environmental and Biological Sciences Queensland University of Technology Brisbane, Australia 2013 Key words Citrus, oviposition preference, larval survival, citrus peel chemicals, citrus peel structure, host quality, DYMEX, population dynamics, Dacini i Abstract Queensland fruit fly, Bactrocera tryoni, is a multivoltine pest species that is distributed throughout large parts of eastern Australia. The adult female lays eggs into ripening fruits, where the emergent larvae feed before emerging to pupate in soil. Bactrocera tryoni is a polyphagous species and has been breed from 117 species of native and commercially produced fruits and fleshy vegetables. While temperature and rainfall are thought to regulate B. tryoni populations in temperate Australia, the presence of suitable larval hosts has been postulated as being a key population drivers in subtropical and tropical parts of its distribution. However, such assumptions have not been tested and the role of host quality on B. tryoni oviposition and larval survival, and the impact that has on the abundance and phenology of fly populations has not been well studied. This thesis examines the impact of B. tryoni host use at multiple scales from individuals through to populations. The work is done with a focus on commercial fruits of the genus Citrus and has applied implications for fruit fly area-wide management and resistance breeding. Bactrocera tryoni oviposition preference and offspring performance was investigated among five citrus types, Murcott mandarin, Navel orange, Eureka lemon, Valencia orange and yellow grapefruit, under laboratory choice and no-choice conditions. An oviposition preference hierarchy was exhibited by ovipositing females among the citrus types, with Murcott mandarin and grapefruit highly preferred. The overall rate of F1 adult production was poor among all citrus types with Murcott mandarin, at ~20% egg to adult survival, a substantially better host than the other four citrus types (0-6%). In contrast, egg to adult survival in non-citrus hosts such as nectarine, loquat and mulberry were around 60-80%. Further studies were performed to determine the mechanisms acting to limit survival to the adult stage in citrus varieties. Existing literature reporting the suitability of citrus as a host for other tephritid species suggest that, fruit peel properties play an important role in oviposition and survival of the immature life stages. Consequently, I focused on the role of citrus morphological and chemical properties on survival of B. tryoni to the adult stage. Using the same five citrus types as in the previous study, peel toughness, thickness (including the zest [flavedo] and pith [albedo] layers), oil gland size and density, and depth of oviposition were measured using stereo and ii light microscopy. With the exception of oil gland size, all morphological measurements, including oviposition depth, differed significantly among the five citrus types. The deepest oviposition depth, with eggs laid in the oil, less albedo layer were found in mandarin, while for the four citrus types oviposition depth was shallower and eggs were deposited into the oil rich flavedo layer. Of physical properties tested, peel toughness and oil gland density showed significant negative correlations with ovipositor depth. It has been demonstrated in other studies that different layers of the citrus peel have different chemical compositions. Having found that eggs laid by females in the flavedo, which is rich in oils and lipid-soluble volatile compounds, my next aim was to investigate the direct effects of a selections of these compounds on B. tryoni offspring survival. Peel essential oils were extracted from each of the five citrus types used in earlier experiments, and along with six individual essential oil components common across Citrus, dose-dependent larval feeding bioassay experiments were conducted. Navel orange, lemon and grapefruit essential oils had significant negative effect on B. tryoni egg/larval survival, while the oils of Murcott mandarin and Valencia orange did not significantly affect larvae. Of the six individual oil fractions tested, only D- limonene showed a significant negative effect on B. tryoni larvae – but this was very dramatic, with tiny concentrations of the chemical in diet causing 100% larval mortality. While B. tryoni citrus host use was examined under laboratory conditions, I also investigated host use behaviour under field conditions to ensure conclusions reached from laboratory data were transferable to the field. Using Ellendale mandarins, Valencia orange, Eureka lemon and nectarines, I assessed B. tryoni clutch size and offspring emergence from both bagged (after oviposition) and unbagged fruit. B. tryoni clutch size was significantly different among the fruit types, with lemon receiving the largest egg clutches. Fly emergence from the citrus was very low, at levels comparable to the laboratory studies, while fly production from nectarine was very high. Host effects on the population dynamics of B. tryoni were investigated by modifying an existing, mechanistic B. tryoni population model to allow the incorporation of host quality and abundance parameters. The sensitivity of the model to a host- iii related larval mortality parameter was tested and found to be significant. The dynamics of B. tryoni populations under different hypothetical arrangements of changing host abundance were then tested. In these scenarios, host quality was found to be a more important parameter than host abundance for population growth and survival. This study concludes that B. tryoni shows a preference hierarchy among citrus and that citrus fruits, in general, are poor hosts for B. tryoni. It further concludes that the quality of available hosts plays a major role on the dynamics of B. tryoni populations in subtropical and tropical systems. iv Table of Contents Keywords i Abstract ii Table of contents v List of figures xi List of tables xviii Declaration xx Acknowledgements xxi Chapter 1: General Introduction 1 1.1 Introduction 1 1.1.1 Phytophagous insect host use behaviour 2 1.2. Tephritid host acceptance 4 1.2.1 Exogenous factors influencing fruit fly host acceptance 5 1.2.1.1 Host physical properties 5 1.2.1.2 Fruit Odour 11 1.2.1.3 Non-volatile host chemicals 11 1.2.1.4 Influence of insect produced chemicals 12 1.2.2 Other exogenous factors influencing host acceptance by 13 fruit flies 1.2.2.1 Conspecific flies 13 1.2.2.2 Abiotic environmental factors 15 1.2.3 Endogenous factors influencing fruit fly host acceptance 15 1.2.3.1 Experience 15 1.2.3.2 Egg load 16 1.2.3.3 Insect nutritional status 17 1.3 Clutch size 17 1.3.1 Effect of host variables on Tephritid clutch size 18 v 1.3.1.1 Fruit availability 18 1.3.1.2. Fruit physical properties 18 1.4 Offspring performance 19 1.4.1 Fruit genotype 19 1.4.2 Fruit ripeness 20 1.4.3 Presence of non dietary (secondary) compounds in host 20 1.4.4 Presence of nutritional compounds in host 21 1.4.5 Fruit physical attributes 21 1.5 Host use and populations of tropical Tephritids 22 1.5.1 Fruit phenology 22 1.5.2 Local host plant composition 23 1.6 Scope and structure of thesis 23 Chapter 2 :Oviposition preference and offspring performance of 27 Bactrocera tryoni among citrus types 2.1 Introduction 28 2.2 Methods 30 2.2.1 Flies and fruit 30 2.2.2 Choice and no-choice oviposition tests 31 2.2.3 Clutch size evaluation 32 2.2.4 Immature performance of B. tryoni in citrus 33 2.2.5 Fecundity of B. tryoni reared from citrus 34 2.2.6 Assessment of fruit characteristics 34 2.3 Results 35 2.3.1 Oviposition choice tests 35 2.3.2 Oviposition no-choice tests 37 2.3.3 Fruit characteristics 40 2.3.4 Immature performance 40 2.3.5 Fecundity of B. tryoni reared from citrus 41 2.4 Discussion 43 Chapter 3: Effect of citrus peel physical properties on Bactrocera tryoni 47 oviposition behaviour vi 3.1 Introduction 48 3.2 Methods 51 3.2.1 Fruit material 51 3.2.2 Tissue preparation for digital stereo microscopy 52 3.2.3 Tissue preparation for light microscopy 55 3.2.4 Data from light microscopy 57 3.3 Results 58 3.3.1 Physical peel properties 58 3.3.2 Location of B. tryoni eggs in the citrus peel 64 3.4 Discussion 70 Chapter 4 :Effect of citrus peel volatiles on Bactrocera tryoni larval 73 survival 4.1 Introduction 74 4.2. Methods 77 4.2.1 Citrus essential oil extraction 77 4.2.1.1 Peel preparation 77 4.2.1.2 Oil extraction 77 4.2.1.3 Chromatographic analysis 78 4.2.2 Citrus oil feeding assay 79 4.2.2.1 Larval diet 79 4.2.2.2 Oil concentrations used in feeding bioassays 79 4.2.2.3 Insects 81 4.2.2.4 Preliminary experiments 82 4.2.2.5 Main feeding bioassays 82 4.2.3 Citrus oil fraction feeding assay 83 4.3 Results 85 4.3.1 Citrus essential oil yield and composition 85 4.3.2 Essential oil feeding assay 88 4.3.3. Citrus essential oil fraction feeding assay 90 4.4 Discussion 93 Chapter 5: Bactrocera tryoni oviposition and offspring performance in 97 vii field unpicked citrus fruits 5. 1 Introduction 98 5.2 Methods 99 5.2.1 Study Site 99 5.2.2 Flies 99 5.2.3 Fruit infestation by laboratory reared B. tryoni flies 100 5.2.4 Fruit infestation by wild B.
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