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Apis Mellifera) on the Pollination Ecology of Bird-And Insect-Adapted Australian Plants Thomas Martin Celebrezze University of Wollongong

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Apis Mellifera) on the Pollination Ecology of Bird-And Insect-Adapted Australian Plants Thomas Martin Celebrezze University of Wollongong University of Wollongong Research Online University of Wollongong Thesis Collection University of Wollongong Thesis Collections 2002 Effects of European honeybees (Apis mellifera) on the pollination ecology of bird-and insect-adapted Australian plants Thomas Martin Celebrezze University of Wollongong Recommended Citation Celebrezze, Thomas Martin, Effects of European honeybees (Apis mellifera) on the pollination ecology of bird-and insect-adapted Australian plants, Doctor of Philosophy thesis, Department of Biological Sciences, University of Wollongong, 2002. http://ro.uow.edu.au/theses/1046 Research Online is the open access institutional repository for the University of Wollongong. For further information contact the UOW Library: [email protected] Effects of European Honeybees (Apis mellifera) on the Pollination Ecology of Bird- and Insect-adapted Australian Plants *A thesis submitted in fulfilment of the requirements for the award of the degree DOCTOR OF PHILOSOPHY from UNIVERSITY OF WOLLONGONG by THOMAS MARTIN CELEBREZZE, BAS, MSc DEPARTMENT OF BIOLOGICAL SCIENCES 2002 CERTIFICATION I, Thomas M. Celebrezze, declare that this thesis, submitted in fulfilment of the requirements for the award of Doctor of Philosophy, in the Department of Biological Sciences, University of Wollongong, is wholly my own work unless otherwise referenced or acknowledged. The document has not been submitted for qualifications at any other academic institution. Thomas M. Celebrezze 18 October 2002 1 TABLE OF CONTENTS CHAPTER 1. GENERAL INTRODUCTION 1 1.1 GLOBAL TRENDS IN POLLINATION DISRUPTION 1 1.2 ENDEMIC AUSTRALIAN POLLINATION 3 1.3 THE POTENTIAL ROLE OF HONEYBEES IN AUSTRALIA 5 1.4 INTERACTIONS OF HONEYBEES AND HABITAT FRAGMENTATION 7 1.5 EVIDENCE FOR HONEYBEE EFFECTS IN AUSTRALIA 7 1.6 NEED FOR AN INTEGRATED, COMPARATIVE STUDY 8 1.7 STUDY DESIGN AND AIMS 10 CHAPTER 2. COMPARISON IN MYRTACEAE 14 2.1 INTRODUCTION 14 2.1.1 Myrtaceae pollination systems 14 2.1.2 Study aims and predicted results 15 2.1.3 Study species 16 2.1.4 Study sites 18 2.2 METHODS 21 2.2.1 Potential pollinator foraging frequency and behaviour 21 2.2.2 Selective pollinator exposure experiments 24 2.2.3 Germination experiments 25 2.3 RESULTS 26 2.3.1 Potential pollinators and their visitation frequency. 26 2.3.2 Honeybee behaviour 29 ii 2.3.3 Pollinator exposure experiments 30 2.3.4 Germination experiments 33 2.4 DISCUSSION 36 2.4.1 Predicted and observed outcomes 36 2.4.2 Pollination systems 37 2.4.3 Pollinator frequency and behaviour 39 2.4.4 Plant sexual systems 40 2.4.5 Potential inbreeding depression 41 2.4.6 Conservation significance and evolutionary implications 42 CHAPTER 3. COMPARISON IN EPACRIDACEAE 45 3.1 INTRODUCTION 45 3.1.1 Epacridaceae pollination systems 45 3.1.2 Study aims and predicted results 45 3.1.3 Study species. 48 3.1.4 Study sites 51 3.2 METHODS 52 3.2.1 Floral longevity 52 3.2.2 Potential pollinators 52 3.2.3 Insect floral visitors and visitation frequency 53 3.2.4 Honeybee and other insect foraging behaviour 54 3.2.5 Bird floral visitor frequency 55 3.2.6 Bird foraging behaviour 56 3.2.7 Other evidence of pollinator visits 56 3.2.8 Breeding systems 57 iii 3.2.9 Selective pollinator exposure experiments 58 3.2.10 Potential cage effects 60 3.3 RESULTS 61 3.3.1 Epacris microphylla 61 3.3.2 Styphelia tubiflora 72 3.4 DISCUSSION 81 3.4.1 Predicted and observed outcomes 81 3.4.2 Breeding systems 82 3.4.3 Foraging behaviour of birds and honeybees 82 3.4.4 Confounding effect of floral robbers 83 3.4.5 Bird visitation 84 3.4.6 Generalism in Epacris microphylla 85 3.4.7 Cage effect in Epacris microphylla populations 85 CHAPTER 4. COMPARISON IN PROTEACEAE 87 4.1 INTRODUCTION 87 4.1.1 Proteaceae pollination systems 87 4.1.2 Study aims and predicted results 88 4.2 METHODS 89 4.2.1 Study species 91 4.2.2 Study sites 95 4.2.3 Potential pollinator foraging frequency and behaviour 97 4.2.4 Breeding System 99 4.2.5 Selective pollinator exposure experiments 100 4.2.6 Genetic assessment 102 iv 4.3 RESULTS 107 4.3.1 Potential pollinators 107 4.3.2 Foraging behaviour of floral visitors 113 4.3.3 Breeding systems 116 4.3.4 Selective pollinator exposure experiments 122 4.3.5 Genetic assessment 125 4.4 DISCUSSION 134 4.4.1 Breeding and mating systems 134 4.4.2 Effect of honeybees on reproductive success 136 4.4.3 Potential pollinators and their apparent relative effectiveness 138 4.4.4 Evidence for honeybee-mediated geitonogamy in G. sphacelata 139 4.4.5 Conformity of genetic data with assumptions 142 4.4.6 Comparative effectiveness ofb ird and honeybee pollination 142 4.4.7 Genetic neighbourhood size 144 4.4.8 Evolutionary consequences and conservation implications 146 CHAPTER 5. GENERAL DISCUSSION 148 5.1 SUMMARY OF OUTCOMES 148 5.2 OVERVIEW OF RESULTS 149 5.3 THE STATUS OF KNOWLEDGE ON HONEYBEE EFFECTS IN AUSTRALIA 150 5.4 THE ROLE OF POLLINATION ADAPTATIONS 150 5.5 EVOLUTIONARY CONSEQUENCES AND CONSERVATION IMPLICATIONS 153 5.6 ASSESSMENT OF POLICY IMPLICATIONS 154 REFERENCES 156 v LIST OF TABLES Table 1.1 A comparison of the social pollinating insects by biogeographic region and a selection of examples of bird-pollination adaptations 2 Table 1.2 Comparative investigations undertaken in this study on the effects of honeybees (Apis mellifera) on the pollination ecology of bird-adapted versus insect-adapted Australian plants in three plant families 13 Table 2.1 Honeybee and bird foraging in populations of Callistemon citrinus, C. linearis andC. linearifolius 20 Table 2.2 Insect morphospecies observed visiting flowers of Baeckea imbricata and Callistemon citrinus 28 Table 2.3 Frequency of insects visits to Baeckea imbricata 29 Table 2.4 Honeybee foraging behaviour at flowers and plants oi Baeckea imbricata and Callistemon citrinus 30 Table 2.5 The effect of selective pollinator exposure on components of plant reproductive output in two populations of Callistemon citrinus near Sydney, Australia 32 Table 2.6 The proportion of capsules produced per flower by selective pollinator exclusion treatment in two populations of Baeckea imbricata 33 Table 3.1 The experimental power of selective pollinator exclusion experiments in Epacris microphylla and Styphelia tubiflora 60 Table 3.2 Insect morphospecies observed visiting flowers of Epacris microphylla in two populations in Royal National Park, Australia 62 Table 3.3 Pollinator behaviour while foraging among flowers and plants of two species of Epacridaceae 64 vi 3.4 Estimated average daily visits per flower and per plant by honeybees and native insects 67 Table 3.5 Results of selective pollinator exclusions and self- and cross-pollination experiments on reproduction of Epacris microphylla in two populations in two years 70 Table 3.6 Results of x tests of the presence of honeybees and native insects in caged inflorescences during hourly censuses 71 Table 3.7 Average number of among-plant movements per day by eastern spinebills on Styphelia tubiflora 75 Table 3.8 Percent of flowers which initiated fruitset and then aborted for open- pollinated, bird-excluded, bagging (autogamy), self-pollinated and cross- pollinated treatments for Styphelia tubiflora 81 Table 4.1 Investigations into potential effects of honeybees on the pollination systems of two species of Grevillea 90 Table 4.2 Insect morphospecies observed visiting Grevillea acanthifolia and G sphacelata flowers 108 Table 4.3 Floral visitor movement rates among inflorescences and plants in two Grevillea species 114 Table 4.4 Estimated daily visits per inflorescence and per plant 116 Table 4.5 The breeding systems of Grevillea acanthifolia and G. sphacelata from cross-and self-pollination experiments 117 Table 4.6 The proportion of fertile inflorescences and mean number of fruits per fertile inflorescences in Grevillea acanthifolia and G. sphacelata 124 Table 4.7 The allelic richness of all adults sampled and the total allelic richness of microsatellite loci in Grevillea acanthifolia in two populations 128 vii Table 4.8 Proportion of Grevillea acanthifolia seed that was detectably outcrossed and outcrossing rate estimates (t) for seed produced through open pollination and vertebrate exclusion in two populations 131 Table 4.9 Comparison of observed heterozygosity (H0) in adults in two Grevillea acanthifolia populations with expected values if populations are at Hardy-Weinberg equilibrium (HE) 133 viii LIST OF FIGURES Figure 2.1 Results of Callistemon citrinus germination experiments of seed produced selective pollinator exposures 35 Figure 3.1 The proportion of Epacris microphylla plants with visiting honeybees and native insects 65 Figure 3.2 The proportion of Styphelia tubiflora plants observed being visited by honeybees 74 Figure 3.3 The proportion of Styphelia tubiflora plants visited per hour by nectar- foraging eastern spinebills and/or New Holland honeyeaters during half- hour or one-hour observation periods 76 Figure 3.4 Proportion of flowers that produced fruit in two Styphelia tubiflora populations 79 Figure 4.1 Average proportion of Grevillea sphacelata plants observed being visited by honeybees and native insects 109 Figure 4.2 Average proportion of Grevillea acanthifolia plants observed being visited by honeybees 110 Figure 4.3 Proportion of Grevillea acanthifolia plants observed being visited by New Holland honeyeaters Ill Figure 4.4 Between plant movement distances of birds and honeybees foraging on Grevillea acanthifolia and honeybees foraging on G. sphacelata 115 Figure 4.5 The distribution of fruit set per inflorescence by experimental treatment in population
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