Pollination Ecology and the Functional Significance of Unusual Floral Traits in Two South African Stapeliads
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Pollination ecology and the functional significance of unusual floral traits in two South African stapeliads Marc du Plessis Submitted in fulfilment of the academic requirements for the degree of Master of Science in the Discipline of Ecological Sciences School of Life Sciences College of Agriculture, Engineering and Science University of KwaZulu-Natal Pietermaritzburg Supervisor: Dr Adam Shuttleworth [email protected] Co-supervisor: Prof. Steve Johnson [email protected] Co-supervisor: Prof. Sue Nicolson [email protected] ABSTRACT Carrion and dung mimicking plants often exhibit unusual floral traits which are believed to attract necro- and coprophagous insects as pollinators. Our understanding of these unusual traits and their functions is very limited. Stapeliads (Apocynaceae: Asclepiadoideae: Stapeliinae) are a monophyletic group of some 400 species of stem-succulent plants, many of which emit foul odours and exhibit unusual morphological traits that have anecdotally been assumed to represent adaptations to enhance the flowers’ resemblance to carrion or dung. This study looked at the pollination biology of two stapeliads, Orbea variegata and Stapelia hirsuta var. hirsuta, and explored the functional significance of some of the floral traits commonly associated with carrion or dung mimicking flowers. Further, odours emitted by both species were compared to the odours of putative models to explore the chemical basis for the assumed mimicry. Orbea variegata attracted flies from the families Muscidae, Calliphoridae and Sarcophagidae (at sites near Scarborough and Clifton, Western Cape) and individuals from each of these families were found carrying pollinia. The scent of O. variegata flowers was found to be dominated by dimethyl disulphide, dimethyl trisulphide as well as phenol. The presence of both these compounds suggests mimicry of both carrion and dung, although an ANOSIM analysis indicated that the odour of O. variegata shared more similarities with dung. This suggests that O. variegata is fairly generalist and explains the attraction of various flies that are associated with carrion or faeces by the flowers of this species. In experiments testing the importance of black versus yellow colouring and the importance of patterning, flies were found to prefer black coloured models in the presence of O. variegata odour, whereas the presence and size of blotching on the corolla lobes had no significant effect on fly visits. The colours of the black blotching and yellow of the corolla lobes showed minimal chromatic contrast when interpreted using the Troje (1993) fly vision model, although background rocks showed chromatic contrast, suggesting flies can distinguish between the flowers and the background. In an experiment testing the importance of odour for attracting flies, significantly fewer flies were able to locate concealed flowers compared to visible flowers, suggesting an important role for visual cues for flies to locate the odour source. Stapelia hirsuta var. hirsuta was found to exhibit two floral colour morphs at Swellendam (Western Cape). The yellow morph was rarer than the maroon morph. These flowers attracted flies belonging to the Muscidae, Calliphoridae and Sarcophagidae families, although only Calliphoridae and Sarcophagidae were found to carry pollinia. The odour composition of these two morphs differed i slightly, where the odour of the maroon morph was dominated by dimethyl disulphide, dimethyl trisulphide and p-cresol and the yellow morph was dominated by dimethyl disulphide, dimethyl trisulphide and limonene. The ANOSIM analysis of odours emitted by S. hirsuta var. hirsuta in relation to that of various fly oviposition substrates suggested that these flowers are dung mimics rather than carrion mimics, although the presence of sulphides suggests possible mimicry of both. The yellow morph had higher fly visitation rates than the maroon morph. In experiments testing the role of floral trichomes, the removal of floral trichomes significantly decreased the visitation rates to the flowers, as well as the amount of time visitors spend on the flowers. Again, visual cues were shown to be of importance, as visible flowers received more visits than concealed flowers. Analysis of colours of different floral morphs, using the Troje (1993) fly vision model, suggests that flies cannot perceive chromatic colour differences between morphs. In these studies, I have shown that O. variegata and S. hirsuta var. hirsuta are visited and pollinated by carrion associated flies, and the flowers emit odours associated with both carrion and dung. This work sheds light on some of the floral features that are often associated with carrion and dung mimicry by flowers and the roles they play in the attraction of flies. ii PREFACE The research described in this thesis was carried out at the School of Life Sciences, University of KwaZulu-Natal (Pietermaritzburg), from March 2015 to March 2017, under the supervision of Dr Adam Shuttleworth and the co-supervision of Prof. Steven Johnson (University of KwaZulu-Natal) and Prof. Sue Nicolson (University of Pretoria). The work presented in this thesis represents the original work of the author and has not been otherwise submitted in any other form for any degree or diploma to any other University. Where use has been made of the work of others, this has been duly acknowledged in the text. Signed: _________________________ Marc du Plessis (Candidate) _________________________ Dr Adam Shuttleworth (Supervisor) ________________________ Prof. Steven Johnson (Co-supervisor) ________________________ Prof. Sue Nicolson (Co-supervisor) iii COLLEGE OF SCIENCE AND AGRICULTURE DECLARATION 1 – PLAGIARISM I, Marc du Plessis, declare that 1. The research reported in this thesis, except where otherwise indicated, is my original research. 2. This thesis has not been submitted for any degree or examination at any other university. 3. This thesis does not contain other persons’ data, pictures, graphs or other information, unless specifically acknowledged as being sourced from other persons. 4. This thesis does not contain other persons' writing, unless specifically acknowledged as being sourced from other researchers. Where other written sources have been quoted, then: a. Their words have been re-written but the general information attributed to them has been referenced b. Where their exact words have been used, then their writing has been placed in italics and inside quotation marks, and referenced. 5. This thesis does not contain text, graphics or tables copied and pasted from the Internet, unless specifically acknowledged, and the source being detailed in the thesis and in the References sections _________________________ Marc du Plessis March 2017 iv ACKNOWLEDGEMENTS • I am grateful to the National Research Foundation as well as the Botanical Society of South Africa for the funding they have provided in order for me to complete this study. • I would like to thank my supervisor Dr Adam Shuttleworth especially for his guidance and assistance with this project. His knowledge on the topic as well as the literature is extensive, and he was always willing to help. I would also like to express my gratitude to my two co- supervisors, Prof. Steven Johnson and Prof. Sue Nicolson, for their support and guidance. • I would also like to thank Dr Sandy-Lynn Steenhuisen (University of Cape Town) for going out of her way to assist me when I needed assistance, as well as Prof. Peter Bruyns who was a great source of knowledge in terms of stapeliads and where they occur. • Lastly, thanks to my family who always offered emotional support especially through the difficult times. v TABLE OF CONTENTS ABSTRACT..........................................................................................................................................i PREFACE...........................................................................................................................................iii DECLARATION OF PLAGIARISM.................................................................................................iv ACKNOWLEDGEMENTS.................................................................................................................v CHAPTER 1: Introduction..................................................................................................................1 CHAPTER 2: Connecting the dots and sniffing out functions: The importance of visual versus olfactory signals for the attraction of fly pollinators by Orbea variegata............................................19 CHAPTER 3: Hairy and smelly: Functional significance of unusual floral traits in the attraction of flies by Stapelia hirsuta var. hirsuta....................................................................................................58 CHAPTER 4: General discussion and conclusion.............................................................................93 vi CHAPTER 1 Introduction THE IMPORTANCE OF POLLINATORS IN SHAPING FLORAL TRAITS The role of pollinators in shaping floral forms was first suggested by Darwin in the late 1800s (Darwin 1862; Darwin 1877) and this idea now forms the broad paradigm for much of the contemporary research on floral diversification. In other words, floral traits may often be interpreted as adaptations to the morphology and behaviour of pollinators that exist within the same area or habitat (Fenster et al. 2004). This micro-evolutionary concept of pollinator mediated evolution was later