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Pollination Ecology and Evolution of Epacrids

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Pollination Ecology and Evolution of Epacrids Pollination Ecology and Evolution of Epacrids by Karen A. Johnson BSc (Hons) Submitted in fulfilment of the requirements for the Degree of Doctor of Philosophy University of Tasmania February 2012 ii Declaration of originality This thesis contains no material which has been accepted for the award of any other degree or diploma by the University or any other institution, except by way of background information and duly acknowledged in the thesis, and to the best of my knowledge and belief no material previously published or written by another person except where due acknowledgement is made in the text of the thesis, nor does the thesis contain any material that infringes copyright. Karen A. Johnson Statement of authority of access This thesis may be made available for copying. Copying of any part of this thesis is prohibited for two years from the date this statement was signed; after that time limited copying is permitted in accordance with the Copyright Act 1968. Karen A. Johnson iii iv Abstract Relationships between plants and their pollinators are thought to have played a major role in the morphological diversification of angiosperms. The epacrids (subfamily Styphelioideae) comprise more than 550 species of woody plants ranging from small prostrate shrubs to temperate rainforest emergents. Their range extends from SE Asia through Oceania to Tierra del Fuego with their highest diversity in Australia. The overall aim of the thesis is to determine the relationships between epacrid floral features and potential pollinators, and assess the evolutionary status of any pollination syndromes. The main hypotheses were that flower characteristics relate to pollinators in predictable ways; and that there is convergent evolution in the development of pollination syndromes. Four case-studies obtained information on specific epacrid-pollinator relationships using a combination of field observation, breeding systems experiments, and comparative phylogenetics. A further study develops a molecular phylogeny for the 38 recognised genera of the epacrids, and the final study places the ecological pollination research into this evolutionary context. Epacrid floral traits were related to bird, bee, and fly pollination systems. Bird pollination occurs in the most basal tribe, but insect pollination is also predicted for this tribe. Fly and bee pollination are widely supported by epacrid flowers, while red flowers and long floral tubes are the most important predictors for those visited by birds. Insect pollination is widespread across the evolutionary tree, but bird pollination coincides largely with the convergent evolution of red flowers. Purple, green, yellow, and nectarless flowers are distributed across the tree, also consistent with a hypothesis of convergent evolution. Nectarless flowers tend to be associated with wind or buzz pollination. Nocturnal mammals and lizards forage on epacrids but their role in pollination remains uncertain. Overall, the data suggest that pollinators have played a major role in the morphological diversification of the epacrids. v Acknowledgments Thanks to my supervisors Peter McQuillan and Jamie Kirkpatrick. Thanks Pete for help in conceptualising the project, for numerous discussions, and for sharing your vast knowledge of invertebrates. Thanks Jamie for your constant support and enthusiasm, availability for discussion, and awesome feedback. I am grateful to Dave, Annette, Trish, Tracey, Paulene and Kate for morning tea chats and the supportive environment they created. Surviving the whole process would have been much less entertaining without the other students and HRAs that filled the postgrad offices and that were easily swayed towards cups of tea and chats: Jon, Cynthia, Pip, Jane, Bec, Grant, Gloria, Steve, Jen, Jade, Mel, Sarah, Millie, Anna, Catherine, Jayne, Kate, Madiha, Bob, Mahni, Vishnu and everyone – Thanks! I am indebted to the reviewers of the three published papers that are chapters 2, 3 and 4 of the thesis. Their critical feedback on my work resulted in a higher standard of research and writing in each of these and the 3 subsequent papers. Thanks to my friends and family who provided encouragement and very, very welcome distractions. Finally, to Barbs who supported me in every aspect of my studies and the rest of life; and Percy who always kept me company. Percy consults the Flora of Tasmania vi Contents Declaration of originality and statement of access ..................................................................iii Abstract ...............................................................................................................................v Acknowledgments ....................................................................................................................vi List of Figures.........................................................................................................................viii List of Tables.............................................................................................................................x List of Appendices....................................................................................................................xi List of Supplementary Material................................................................................................xi Chapter 1 Introduction and aim..............................................................................................1 Chapter 2 Bird Pollination of the climbing heath Prionotes cerinthoides ...........................15 Chapter 3 Nocturnal mammals, diurnal lizards and the pollination ecology of the cryptic flowering Acrotriche serrulata............................................................................41 Chapter 4 Comparative floral presentation and bee-pollination of two Sprengelia spp. .....69 Chapter 5 Evolution of floral diversity relates to pollinator profiles but not taxonomic divisions in Richea ..............................................................................................85 Chapter 6 Supermatrices, supertrees and the scaffold of serendipity: Inferring a well- resolved phylogeny for the Styphelioideae despite missing data......................111 Chapter 7 Revealing the evolution of epacrid pollination systems: Inferring syndromes from a known subset of pollinators ...................................................................147 Chapter 8 Conclusion and future directions.......................................................................215 vii List of Figures Figure 2-1 Capsule mass by breeding system treatments for Prionotes.................................. 25 Figure 2-2 Flowering and fruiting phenology in Prionotes cerinthoides ................................ 26 Figure 2-3 Prionotes cerinthoides showing position of anthers and style............................... 27 Figure 2-4 Damage to corollas of Prionotes cerinthoides over the flowering period ............. 28 Figure 2-5 Profile of bruise damage in Prionotes cerinthoides flowers.................................. 28 Figure 2-6 Profile of hole damage in Prionotes cerinthoides flowers..................................... 29 Figure 3-1 Male-phase Acrotriche serrulata flowers with secondary pollen presented; female-phase A. serrulata flowers ................................................................................... 43 Figure 3-2 Fruit set for breeding system treatments and open controls for Acrotriche........... 53 Figure 3-3 Phenology of Acrotriche ........................................................................................ 54 Figure 3-4 A-B. N. ocellatus forages on A. serrulata during feeding observations; C. E. whitii forages on presented A. serrulata; D. E. whitii with secondary pollen presenters contacting face during feeding observations.................................................................... 58 Figure 3-5 Percentage of interest of skinks in presented flowers and meat............................. 58 Figure 4-1 Sprengelia incarnata pollen grain; S. propinqua pollen grain............................... 76 Figure 4-2 Lasioglossum bees on Sprengelia incarnata showing: A. folded wing position; B. hunched position during sonication; C. pollen accumulation; and D. anther position in S. propinqua................................................................................................................. 77 Figure 5-1 A. Yellow throated honeyeater (Phylidonyris pyrrhoptera) visiting Richea pandanifolia; B. Corolla abscission in R. acerosa; C. Tachinid fly visiting R. scoparia; D. Native bee (Exoneura sp.) scraping pollen from R. procera; E. Exoneura sp. collecting pollen from R. milliganii; F. Snow skink (Niveoscincus sp.) with operculum it has removed from R. scoparia...................................................................................... 96 viii Figure 5-2 Ordination of all Richea according to floral trait and flowering time profiles.......98 Figure 5-3 Ordination of all Richea according to their potential pollinator profiles................99 Figure 5-4 Evolutionary mapping of floral traits and pollinators of Richea species..............101 Figure 6-1 RAxML tree..........................................................................................................123 Figure 6-2 MrBayes majority rule tree...................................................................................124 Figure 6-3 Consensus network displaying conflict within the Styphelieae ...........................125 Figure 6-4 MRP supertree
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