PUTTING POLLINATION QUALITY INTO ANALYSES OF FLORAL ECOLOGY: TESTING SYNDROMES THROUGH POLLINATOR PERFORMANCE Caroline King A Thesis Submitted for the Degree of PhD at the University of St. Andrews 2012 Full metadata for this item is available in Research@StAndrews:FullText at: http://research-repository.st-andrews.ac.uk/ Please use this identifier to cite or link to this item: http://hdl.handle.net/10023/3219 This item is protected by original copyright Putting Pollination Quality into Analyses of Floral Ecology: Testing Syndromes through Pollinator Performance Caroline King This thesis is submitted in partial fulfilment for the degree of PhD at the University of St Andrews Date of Submission: 05/09/2011 This thesis is dedicated to my parents, Kevin and Fiona King, who have put up with a lot over the years, but never stopped supporting me and pretending to understand what I was studying. I wouldn’t have got this far without them. “In the long history of humankind (and animal kind, too) those who learned to collaborate and improvise most effectively have prevailed.” Charles Darwin “No power in the ‘verse can stop me.” River Tam, Firefly “Live now; make now always the most precious time. Now will never come again" Jean-Luc Picard, Star Trek Next Generation 1. Candidate’s declarations: I, Caroline King hereby certify that this thesis, which is approximately 85,000 words in length, has been written by me, that it is the record of work carried out by me and that it has not been submitted in any previous application for a higher degree. I was admitted as a research student in June, 2007 and as a candidate for the degree of PhD in September 2011; the higher study for which this is a record was carried out in the University of St Andrews between 2007 and 2011. Date: signature of candidate: 2. Supervisor’s declaration: I hereby certify that the candidate has fulfilled the conditions of the Resolution and Regulations appropriate for the degree of PhD in the University of St Andrews and that the candidate is qualified to submit this thesis in application for that degree. Date: signature of supervisor: 3. Permission for electronic publication: In submitting this thesis to the University of St Andrews I understand that I am giving permission for it to be made available for use in accordance with the regulations of the University Library for the time being in force, subject to any copyright vested in the work not being affected thereby. I also understand that the title and the abstract will be published, and that a copy of the work may be made and supplied to any bona fide library or research worker, that my thesis will be electronically accessible for personal or research use unless exempt by award of an embargo as requested below, and that the library has the right to migrate my thesis into new electronic forms as required to ensure continued access to the thesis. I have obtained any third-party copyright permissions that may be required in order to allow such access and migration, or have requested the appropriate embargo below. The following is an agreed request by candidate and supervisor regarding the electronic publication of this thesis: (i) Access to printed copy and electronic publication of thesis through the University of St Andrews. Date: signature of candidate: signature of supervisor: Contents Acknowledgements pg. 1 Abstract pg. 2 Chapter 1: Introduction pg. 3 Chapter 2: Assessing Single Visit Pollen Deposition pg. 64 Chapter 3: Testing Pollination Syndromes: The Hummingbird Pollination Syndrome pg. 68 Chapter 4: Testing Pollination Syndromes: The General Hoverfly-Pollination Syndrome pg. 116 Chapter 5: Testing Pollination Syndromes: The Bee- Pollination Syndrome pg. 140 Chapter 6: Testing Pollination Syndromes: The Oil-Flower Pollination Syndrome pg. 167 Chapter 7: Testing Pollination Syndromes: The Long-Tongued Insect-Pollination Syndrome pg. 187 Chapter 8: Testing Pollination Syndromes: The Generalist Pollination Syndrome pg. 242 Chapter 9: Scaling up Single Visit Pollen Deposition pg. 300 Chapter 10: Testing Proxies for Pollinator Effectiveness pg. 318 Chapter 11: Conclusions and Future Directions pg. 337 References pg. 349 Acknowledgements Firstly, and most importantly, I would like to thank my supervisor Pat Willmer for her never-ending support, encouragement and patience (a great deal of which was required given my atrocious writing skills). I would also like to thank her for giving me the opportunity to study with her in the first place. I have learned a great deal over the past four years, and I promise I will never again use the passive voice. I would like to thank my labmates Gavin Ballantyne and Jonathan Pattrick, for support, encouragement, fieldwork assistance, proof-reading and of course chat, silly you tube videos and other such stress relief. The completion of this thesis would have been a much more taxing process without them. I would also like to extend my gratitude to Will Cresswell for statistical advice, and Jane Wishart and Steve Hubbard for help and advice on almost everything. I’d like to thank Jim Cobb for his assistance at West Quarry Braes, and all the staff and residents of Parque Nacionale Santa Rosa for assistance with fieldwork. I must of course thank my friends and family for their support. While my parents may still have little understanding other than that I study “something to do with bees”, they have always been incredibly supportive of my studies. In particular I want to thank my “wife”, Dawn Toshack, for not only tolerating and alleviating my stressed out moods over the years, but also for her assistance in illustrating several images for this thesis. Without her dragging me out to watch horror movies and socialise I would probably have snapped a long time ago. I also owe a huge debt to the Dundee Roller Girls Roller Derby team, for offering me a great source of stress relief and exercise, as well as endless amounts of fun (and bruises). To my partner, Stu Turner, I extend my gratitude for not only putting up with an almost non-existent and grouchy girlfriend, but also helping me with proof-reading and formatting and making sure I remember to sleep and eat every now and then. You have the patience of a saint. This thesis would not have been completed without the assistance of coffee, chocolate and (the occasional) Jack Daniels. It would probably have been completed sooner without the “assistance” of my cats Grissom and Horatio. I would like to clarify that any further typos or spelling mistakes are likely the result of them sprawling across the laptop whenever the opportunity arose. Thank you to everyone who helped me, supported me and put up with me. It’s finally over. Acknowledgements 1 Abstract Over recent years, the extent of specialised and generalised plant-pollinator relationships, and the predictive powers of floral traits (often grouped into “pollination syndromes”) as indicators of the most effective pollinators of plant species, have been questioned. Such studies, however, have used proxies such as visitation frequency rather than direct measurements of pollinator effectiveness (PE). The main objective of this thesis was to test the predictive powers of various pollination syndromes using a specific measure of PE: single-visit stigmatic pollen deposition (SVSPD). Six different classical pollination syndromes were tested, using 13 different plant species from tropical and temperate habitats, and in the case of flowers typical of the hummingbird, hoverfly, bee, oil flower and long-tongued insect syndromes, the expected pollinators were the most effective at a single-visit scale. For generalist pollination syndrome flowers, not all observed visitors were significant pollinators, and the species studied were not as broadly generalised as their visitor assemblages would suggest. In all 13 plant species, pollinator performance could appear consistent within functional visitor groups but was variable between visitor species, and in almost all cases not all of the observed visitors were effective pollinators. The pollinator performance proxies of visit duration and feeding behaviour were neither significantly, nor consistently, related to PE. Visit duration was not an accurate indicator of pollinator performance on its own, though it was useful when combined with SVSPD to define pollinator performance at a given time scale, for example per hour, per day or per season. My findings suggest that the results of recent “pollination” networks and webs, based on visitors but not necessarily pollinators, should be treated with caution. SVSPD therefore proved to be an effective and relatively simple direct measure of PE, confirming the predictive powers of pollination syndromes, and giving further insight into the extent of specialisation and generalisation. 2 Abstract Chapter 1: Introduction “Among plants, the nuptials cannot be celebrated without the intervention of a third party to act as a marriage priest” (Rothrock, 1867) The Importance of Animal Pollination Pollination by Animals Pollination represents a key animal-plant relationship vital to both wild flower communities (Ashman et al., 2004; Aguiler et al., 2006) and agricultural productivity (Klein et al ., 2007; Ricketts et al ., 2008), playing an important functional role in most terrestrial ecosystems. Angiosperms, or flowering plants, account for approximately one sixth of all the described species on earth (Willmer, 2011) and it is estimated that 90% or more of angiosperm species benefit from animal pollination (Linder, 1998; Renner, 1998). Flowers are usually hermaphroditic, with both male and female parts. For effective fertilisation, the male gametophyte (pollen) produced from the male structure of the flower (the anther) must come into contact with the female structure (the stigma) and the genetic material must then be transported to the female gametophyte (the ovule). While this process can be effected by abiotic pollination methods such as wind or water, biotic pollination, or animal pollination, is a much more common strategy (Linder, 1998; Renner, 1998; Willmer, 2011).