The Ecology and Evolution of Ant- Aphid Interactions
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The Ecology and Evolution of Ant- Aphid Interactions THOMAS HENRY OLIVER Division of Biology, Silwood Park campus, Ascot, Berkshire, SL5 7PY, U.K. A thesis submitted for the degree of Doctor of Philosophy of Imperial College London March 2008 Supervisors: Dr James Cook Dr Simon Leather 1 Lasius niger ants tending aphids on ornamental daisies. Photo taken by the author at Wye College, Kent, UK, June 2006. 2 Abstract The evolution of species interactions is a fascinating subject, and one of vital importance if we are to understand how biological communities change over time. This thesis considers the interaction between aphids (Homoptera) and ants (Formicidae). Ants tend aphids for sugary honeydew and in return provide a variety of protective services. A literature review in Chapter 1 introduces the subject and provides background information. Chapter 2 considers ant- aphid interactions in a community setting. Specifically, I consider the fitness effects of the ant- aphid interaction on host plants. Net benefits or costs to plants depend on the densities of ants and aphids; these densities may themselves change depending on context dependent factors. Chapters 3 and 4 consider how semiochemicals can allow species to respectively maintain or avoid synchrony in space and time with mutualists or antagonists. Chapter 3 shows ladybirds avoid prey patches guarded by ants by reducing oviposition in response to ant semiochemicals. Chapter 4 shows that aphid walking dispersal can be limited by ant semiochemicals. This may be adaptive for aphids to remain in areas of enemy- free space. Alternatively, if levels of kin competition are high limited dispersal could be costly to aphids. In Chapter 5 I consider interactions between invasive and native ants. Ecological dominance in ants may be mediated by the ability to monopolise honeydew- producing resources. Chapter 6 explores ants’ decisions whether to tend or prey upon aphids. Predation of aphids depends on colony demand (e.g. through cues from the presence of larvae) as well as the quality or quantity of supply (e.g. increased predation of unproductive aphids). Finally, Chapter 7 deals with macroevolutionary patterns in the interaction between ants and aphids. Specifically, I identify ecological traits that characterise aphid- tending ants. A final discussion chapter summarises how ant-aphid interactions fit into existing mutualism theory. 3 Declaration I hereby confirm that all the work within this thesis is my own, with the exception of a small number of replicates of the experiment in Chapter 3, which were conducted by a student, Ian Jones, under my supervision and also collaborative work with Ms. Alla Mashanova in Chapter 4. Dr. Tim Pettitt aided the research published in Chaper 7 by providing ant cultures from the Eden Project, Bodelva, Cornwall, UK. In addition, my supervisors James Cook and Simon Leather helped by reading draft copies of published manuscripts mentioned herein. Signed: T H OLIVER Date: 20/03/2008 4 Table of Contents Page Abstract .........................................................................................................................3 Declaration ....................................................................................................................4 Chapter 1 ..........................................................................................................................8 Literature Review ........................................................................................................9 Aphids .......................................................................................................................9 Ants ..........................................................................................................................10 Evolutionary Interactions .....................................................................................10 Costs and benefits ..................................................................................................12 Aphids .................................................................................................................12 Costs .................................................................................................................12 Benefits ............................................................................................................15 Ants ......................................................................................................................18 Costs .................................................................................................................18 Benefits ............................................................................................................19 Context dependence and ecological dynamics .....................................................20 Adaptations for mutualism ...................................................................................20 Aphid adaptations ..............................................................................................21 Ant adaptations ..................................................................................................22 Pre-adaptation ....................................................................................................23 Phenotypic plasticity ..............................................................................................24 Summary .................................................................................................................25 Chapter 2 ........................................................................................................................26 When are ant-attractant devices a worthwhile investment? Vicia faba extrafloral nectaries and Lasius niger ants .................................................................................27 Summary .................................................................................................................27 Introduction ............................................................................................................28 The model ...........................................................................................................29 The Experiment ..................................................................................................33 Study system ....................................................................................................33 Materials and Methods ..........................................................................................34 STATISTICAL ANALYSIS .............................................................................35 Results .....................................................................................................................35 Ant counts ...........................................................................................................35 Herbivore damage ..............................................................................................36 Plant fitness .........................................................................................................38 Discussion ................................................................................................................40 Chapter 3 ........................................................................................................................44 Avoidance responses of an aphidophagous ladybird, Adalia bipunctata , to aphid- tending ants .................................................................................................................45 Summary .................................................................................................................45 Introduction ............................................................................................................46 Materials and Methods ..........................................................................................47 Insect culture ......................................................................................................47 5 Expt. 1: Efficiency of aphid-defence by Lasius niger ants .............................48 Expt. 2: Oviposition response to ant semiochemicals .....................................48 Expt. 3: Avoidance and oviposition response to ant presence .......................49 Expt. 4: Fitness effects of ants on coccinellid eggs ..........................................49 STATISTICAL ANALYSIS .............................................................................50 Results .....................................................................................................................50 Expt. 1: Efficiency of aphid-defence by Lasius niger ants .............................50 Expt. 2: Oviposition response to ant semiochemicals .....................................51 Expt. 3: Avoidance and oviposition response to ant presence .......................51 Expt. 4: Fitness effects of ants on coccinellid eggs ..........................................52 Discussion ................................................................................................................53 Chapter 4 ........................................................................................................................55 Ant semiochemicals limit apterous aphid dispersal ................................................56 Summary .................................................................................................................56