Assembly and disassembly of bird pollination communities at the Cape of Africa by Sjirk Geerts Dissertation presented for the degree of Doctor of Philosophy at Stellenbosch University Department of Botany and Zoology Faculty of Natural Sciences Supervisor: Dr. A. Pauw March 2011 Declaration By submitting this thesis electronically, I declare that the entirety of the work contained therein is my own, original work, unless to the extent explicitly stated otherwise (Chapter 6 and 8), that I am the owner of the copyright thereof and that I have not previously in its entirety or in part submitted it for obtaining any qualification. November 2010 Copyright © 2010 University of Stellenbosch All rights reserved 1 Abstract With the current global decline in pollinators, and the concurrent decline in plant species, pollination research is becoming increasingly important. However, studies outside Europe and North-America and on groups other than insects are needed to make generalisations possible. In this thesis I study how pollination structures plant and bird communities in a biodiversity hotspot, the Cape Floristic Region of South Africa. I show that bird-plant pollination mutualisms are an important ecological factor structuring ornithophilous Proteaceae and nectar-feeding bird communities. This close association between plant and bird communities suggests an important role for community wide pollination mutualisms. How these mutualisms disassemble in reaction to a range of anthropogenic impacts is determined. Firstly, I use experimental manipulation of honeybee density to test whether honeybee farming affects nectar-feeding birds. Hive addition increased honeybee abundance far above natural levels but nectar-feeding bird pollinators were not consistently affected. Secondly, I document the impact of a two lane tar road on the bird pollination community. The two-fold decline found in pollination along roadsides, should have important implications for the way we view and manage road verges for ecological processes. Thirdly, I investigated how fragmentation affects bird-pollination communities by assessing an endangered, bird- pollinated plant, Brunsvigia litoralis. The only flower visitor at the urban sites, the shorter billed Greater Double-collared Sunbird is unable to access the nectar due to a long perianth tube. The longer billed Malachite Sunbird was the sole pollinator of B. litoralis at the rural site, significantly increased seed set. The lack of ecological analogs in these urban fragments might place pollinator specialist plants, such as B. litoralis, at risk. Fourthly, fire is a frequent disturbance in communities of bird-pollinated plants. In a before/after fire observation study and a burnt/unburnt transplant study, birds visited flowers in the “before fire” and “unburnt” areas only. The results are surprising given the large number of bird-pollinated plants flowering in the early post-fire vegetation. Lastly, I find that alien invasive plant species are incorporated into the native pollination community in a spectacular way; sunbirds adapt to a hummingbird-like, hovering lifestyle to obtain nectar. Alien invasive plants greatly increase nectar-feeding bird abundance; in turn, birds enhance seed set in these alien plants. I conclude by asking whether the disassembling of bird pollination communities really matters. To answer this question I report on a decade of demographic data on the geophytic bird-pollinated Brunsvigia orientalis. In the demographic analysis, the elasticity component 2 for reproduction was more important than expected for a long lived plant. Reduced population growth in the shade and a large investment in a winged inflorescence, suggest B. orientalis is a light demanding, well dispersed, gap colonising species. The link between pollination and seed has been made before, but I take this one step further and show that pollination intensity predicts population growth rate. By linking plant demography and pollination, I was able to predict the future of plant populations under variable pollination conditions. The disassembly of bird pollination communities only becomes important for population persistence once the mutualism has almost entirely broken down. 3 Abstrak Met die huidige globale afname in bestuiwers en die gelyktydige afname in plant spesies, word bestuiwing navorsing toenemend belangrik. Studies buite Europa en Noord-Amerika en op groepe anders dan insekte is nodig on veralgemenings moontlik te maak. In hierdie tesis bestudeer ek hoe bestuiwing struktuur gee and plant en voël gemeenskappe in 'n biodiversiteit hotspot, die Kaapse Floristiese Ryk van Suid-Afrika. Ek wys dat voël-plant bestuiwings mutualismes 'n belangrike ekologiese faktor is in die strukturering van voël bestuifde Proteaceae gemeenskappe en nektar-etende voël gemeenskappe. Hierdie noue assosiasie tussen plant en voël gemeenskappe impliseer 'n belangrike rol vir gemeenskapwye bestuiwings meganismes. Ek bepaal hoe hierdie mutualismes aftakel in reaksie op 'n verskeidenheid van antropogeniese impakte. Eerstens gebruik ek 'n eksperimentele manipulasie van heuningby getalle om te toets of bye boerdery nektar-etende voëls affekteer. Byekorf toevoeging het heuningby getalle laat toeneem tot ver bo natuurlike vlakke maar nektar-etende voël bestuiwers is nie konsekwent beïnvloed nie. Tweedens dokumenteer ek die impakte van 'n twee baan teerpad op die voël bestuiwings gemeenskap. Die twee-malige afname in bestuiwing langs paaie sal belangrike implikasies hê vir die manier hoe ons pad reserwes sien en bestuur met betrekking tot ekologiese prosesse. Derdens bestudeer ek hoe fragmentasie die voël-plant gemeenskappe affekteer deur die bedreigde voël-bestuifde Brunsvigia litoralis te assesseer. Die enigste besoeker in die meer stedelike area, die Groot-rooibandsuikerbekkie, wat 'n korter snawel het, is nie in staat om die nektar te bereik nie, weens 'n te lang blombuis. Die Jangroentjie suikerbekkie met sy langer snawel is die enigste bestuiwer van B. litoralis in die meer landelike area, met 'n betekenisvolle vermeerdering in saad vorming. Die gebrek aan ekologies analogiese spesies in die stedelike fragmente kan 'n risiko inhou vir bestuiwer gespesialiseerde plante soos B. litoralis. Vierdens, vuur is 'n gereelde versteuring van voël- plant gemeenskappe. In 'n voor/na vuur observasie studie en 'n brand/nie-brand verplasing studie, het voëls blomme net in die “voor brand” en “nie-brand” areas besoek. Hierdie resultate is verrassend siende die groot hoeveelheid voël-bestuifde plante wat blom direk na brande. Laastens het ek gevind dat uitheemse indringer plante geïnkorporeer word in die inheemse bestuiwers gemeenskappe op 'n skouspelagtige manier; suikerbekkies pas aan tot 'n kolibri-tipe, fladderende lewenswyse om nektar te bekom. Uitheemse indringer plante het nektar-etende voël hoeveelhede laat toeneem; in reaksie het voëls saad opbrengs vermeerder. 4 In konklusie vra ek of hierdie aftakeling van die voël bestuiwers gemeenskap belangrik is. Om hierdie vraag te antwoord assesseer ek 'n dekade van demografiese data van die geofietiese, voël-bestuifde plant, Brunsvigia orientalis. In die demografiese analises was die elastisiteit komponent van reproduksie belangriker as verwag vir 'n langlewende plant. Verminderde populasie groei in die skaduwee en 'n hoë investering in 'n gevlerkte bloeiwyse suggereer dat B. orientalis 'n lig afhanklike, goed verspreide, gaping koloniserende spesie is. Die skakel tussen bestuiwing en saadvorming is voorheen gemaak, maar ek neem dit een stap verder en wys dat bestuiwings intensiteit populasie groeikoers voorspel. Deur plant demografie en bestuiwing te koppel was ek in staat om die toekoms van populasies onder variërende bestuiwings kondisies te voorspel. Die aftakeling van voël bestuiwings gemeenskappe word slegs belangrik vir populasies se voortbestaan wanneer die mutualisme amper heeltemal verdwyn het. 5 Acknowledgements I would like to thank the following people and institutions for their support. My supervisor for his support and encouragement and his ability to motivate and convey his in depth knowledge and understanding of the natural world. A better supervisor would be hard to find. Several anonymous reviewers of published chapters, whose comments and critique improved the quality of this thesis. Prof. Daan Nel and Mnr. Justin Harvey from the Centre for Statistical Analysis for help with statistical analysis. The Harry Crossley fund, Van Ewijck fund, Ernst en Ethel Eriksen Trust, Stellenbosch University and the National Research Foundation (South Africa) for funding. The Department of Botany and Zoology for a pleasant and organised PhD experience. To my brother Jan for teaching me the basics of photography. To my parents for encouragement and interest in my research. Finally and most importantly, I want to thank my wife, Elisabeth, who enjoyed sharing my interest in nature with me. Thanks for keeping me company on field trips and spending many hours in the field doing “weird stuff” like counting leaves of plants. And of course then there is Lulu, the African Grey, who kept me company during the many lonely hours of writing. 6 TABLE OF CONTENTS Declaration......................................................................................................................... 1 Abstract .............................................................................................................................. 2 Abstrak .............................................................................................................................