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Universita' Degli Studi Di Napoli “Federico UNIVERSITA’ DEGLI STUDI DI NAPOLI “FEDERICO II” Scuola Politecnica e delle Scienze di Base CURTIN UNIVERSITY School of Molecular and Life Sciences Joint thesis for Doctor of Philosophy XXX cycle Pollination Ecology and Pollination Evolutionary Processes with Relevance in Ecosystem Restoration – Pollination Biology of Diuris: Testing for Batesian Mimicry in Southwestern Australia PhD Candidate Daniela Scaccabarozzi Supervised by Professor Salvatore Cozzolino & Professor Kingsley Wayne Dixon May 2019 0 Declaration A dissertation submitted to the University of Naples Federico II for the degree of DOCTOR OF BIOLOGY presented by Daniela Scaccabarozzi Perth, 8th May 2019 PhD Candidate at University of Naples Federico II & Curtin University of Perth Born on July 19th, 1982 Citizen of Italy Revision has been submitted to the University of Naples Federico II on 11th June 2019 1 Table of Contents Table of Contents………………………………………………………………..2 Acknowledgements……………………………………………………………...3 Abstract……………………………………………………………………….…4 General Introduction…………………………………………………………...6 Chapter 1 Masquerading as pea plants: behavioural and morphological evidence for mimicry of multiple models in an Australian orchid…………………....21 Chapter 2 Pea plants in the southwestern Australia biodiversity hotspot: pronounced differences in potential pollinators between co-occurring species…......73 Chapter 3 A general pea flower image? Ecological factors affecting reproductive success in an orchid that exhibits imperfect floral mimicry……………..............121 Chapter 4 Rotating arrays of orchid flowers: a simple and effective effective methodology for studying pollination in deceptive plants..………………...................169 Conclusions …………………………………………………………………...179 Publication List ……………………………………………………………....181 2 Acknowledgements I would like to express my special appreciation and thanks to Professor Dr. Salvatore Cozzolino and Professor Dr. Kingsley Dixon for totally supporting and encouraging my research with enormous trust and passion. Your guidance on both research as well as on my professional pathway has been valuable. I am honoured to have shared this research with Dr. Lynne Milne, receiving from her a dedicated contribution. I deeply say thank you to Terry Houston, for the beautiful collaboration throughout the project and for his generosity in sharing his expertise. My appreciation extends to Dr. Ryan Phillips for providing excellent input to the chapters and the study design. I would also like to thank my committee members, Professor Katherine Trinajstic, Dr. Philip Bateman and Dr. Paul Nevill for serving as my committee members even at hardship due to my special case of Dual PhD. Always, I felt to be listened and stimulated from you. Thank you to all the bright co-authors who participated to the papers, especially Lorenzo Guzzetti, who contributed with immense tenacity, talent and professionality to two chapters. A special thanks to Dr. Andrea Galimberti, Professor Dr. Massimo Labra and Nicola Tommasi for their tremendous support and fruitful collaboration. My husband Andrea accompanied me throughout the project, helping me in keeping alive a beautiful vision. How grateful I am to be day by day with him, who was during the PhD a wonderful advisor and zealous assistant in the field. We both had the extraordinary possibility to share this journey together and I will be always grateful for that. Now is the time to remember my family. My words for you are full of gratitude, mum and dad, for all the immense support received, shortening the physical distance between you and me. You have not ever had any expectation on me and this was what brought me here. Thank you forever. I say thanks to Alexander Berlonghi, a dear friend who sent to me messages of support and strength during this challenging pathway. Thanks to our Planet Earth, for the gifts offered, foremost for the possibility to walk along its beauty and to share together this research journey. 3 Abstract Mimicry is based on the interaction between a mimic, a model and a receiver. While there is increasing recognition of Batesian floral mimicry in plants, there are few confirmed cases where mimicry involves more than one model species. The Australian orchid genus Diuris has been long hypothesised to engage in guild mimicry of a range of co-occurring pea plants (Faboideae). Some clades of Diuris are superficially similar in both colour and shape to those of a guild of yellow and brown pea plants (Faboideae). Here, we test for pollination via mimicry of pea plants in Diuris (Orchidaceae). Additionally, we test for further ecological interactions (non-model plants, pollination limitation, habitat size and plant frequency) in order to assess the reproductive success of the orchids. For addressing these hypothesis we select two study species, occurring in different habitat: Diuris brumalis (Jarrah forest) and Diuris magnifica (Banksia woodland), the latter occurring in fragmented habitat. We test for floral mimicry criteria in both of the species. In order to frame the pollination ecology of the putative model plants, we verify the type of pollinator interactions (generalised vs specialized) occurring in four communities of pea plants in the southwestern Australian Floristic Region (SWAFR). D. brumalis, D. magnifica and the pea plants showed strong flower similarity and were likely to be perceived as the same by pollinators, native bees (Trichocolletes; Colletidae). However, in D. brumalis the orchid reproductive success increased with the local abundance of the model species (Daviesia spp.), while in D. magnifica the reproductive success wasn’t in relation to the putative models. Alternatively, D. magnifica reproductive success was influenced by a non-model pea plant (Hardenbergia) which is locally abundant and widespread in all the study sites. Additionally, habitat size and orchid plant frequency influenced the orchid reproductive success. Pea plant species were visited by between one and four genera of native bees, indicating variation in levels of specialisation of the pollination systems of Faboideae. Several pea plant species showed specialised interactions with bee genera attracted. Unexpectedly, some pea plant species frequently attracted beetles that may play an important role in pollination. Evidence for mimicry of multiple models suggests that D. brumalis and D. magnifica may be engaged in guild mimicry system. Interestingly, D. brumalis and D. magnifica 4 belongs to a complex of species with similar floral traits, suggesting that this represents a useful system for investigating speciation in lineages that employ mimicry of food plants. Furthermore, the study on pollination of Faboideae species of SWAFR, offers a pivotal research for next investigations on pollinator webs and syndromes of Australian pea plants scarcely documented until now. 5 General introduction The present work aims to investigate a case of floral mimicry in South Western Australia where multiple ecological plant-pollinator interactions occur, including between co-occurring flowering plants. An understanding of floral mimicry, focused on orchids and legumes, is vital for unravelling pollination processes relevant to restoration ecology. A restored ecosystem must be supported by a solid network of pollinators in order to ensure plant reproductive continuity (Memmot et al., 2007; Klein et al., 2007). However, re-activation of pollination network within a restored ecosystem is a complex dynamic that needs to be framed by previous pollination studies (Furup et al., 2008). For example, in Australia the urban restoration programmes have neglected the inclusion of pollinator network due to the lack of knowledge of local pollination interactions (Dixon, 2009). To put this study of mimicry in Australian orchids of the genus Diuris (Orchidaceae) and co-occurring legumes in context, a general introduction to floral mimicry, pollination and diversity of the Australian pea plants is provided below. The study species / aims are presented, followed by the thesis outline. 1. Floral mimicry Mimicry was first recognised in animals by Henry Walter Bates in 1862, who discovered that palatable butterflies were imitating the wing pattern of unpalatable butterflies in order to avoid predation. However, the discovery of floral mimicry predated Bate’s work on butterfly mimicry. Sprengel in 1793, interpreted the carrion odour emanated by the succulent South African plant Stapelia hirsuta, as a deceit pollination system to attract flies. Vane-Wright (1980) defined mimicry as a phenomenon in which the mimic, the model and the operator interact with each other, causing a cognitive misclassification and behavioural response by the operator that leads to a fitness benefit for the mimic. The mimicry can be achieved through various signals, 6 including visual, acoustic, chemical, tactile and possibly electrical (Norman et al., 2001; de Jager and Peakall, 2016; Barbero et al., 2009; Schiestl and Johnson, 2013; Gaskett, 2011; Stoddard, 1999). Adaptive resemblance is a basal criterion occurring in all cases of mimicry (Johnson and Schiestl, 2016). While mimicry in animals has been well studied, in plants the phenomenon has rarely been reported and was largely controversial (Ruxton et al., 2004) for about 200 years. During the last three decades, there has been an increase in floral mimicry studies, suggesting that the phenomena may be widespread in some plant families (Johnson and Schiestl, 2016). The general criteria for floral mimicry (Roy and Widmer, 1999;
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