Global change and predator–prey interactions on a woody perennial by William Thomas Hentley B.Sc. M.Sc. Cardiff University School of Biosciences Submitted for the degree of Doctor of Philosophy September 2014 Doctor of Philosophy – Cardiff University 2014 Contents Table of Figures ....................................................................................................... vi Table of Tables ...................................................................................................... viii Declaration ................................................................................................................ x Acknowledgements ................................................................................................. xi General introduction ................................................................................................ 1 1.1 Global change ................................................................................................ 1 1.2 Factors driving herbivore abundance ............................................................ 2 1.2.1 Bottom-up processes .............................................................................. 2 1.2.1.1 Host plant acceptance ...................................................................... 3 1.2.1.2 Digesting plant material .................................................................... 3 1.2.2 Top -down processes ............................................................................... 4 1.2.3 Synergy of bottom-up and top-down processes ...................................... 5 1.3 Impact of global climate change on herbivory ............................................... 5 1.3.1 Elevated atmospheric CO2 ...................................................................... 8 1.3.2 Altered precipitation ................................................................................ 9 1.3.3 Invasive species interactions .................................................................. 9 1.4 Aphid herbivory ............................................................................................ 12 1.5 Study system ............................................................................................... 13 1.5.1 Amphorophora idaei .............................................................................. 14 1.5.2 UK raspberry breeding – a brief history ................................................ 15 1.5.3 Impacts of global change on the study system ..................................... 16 1.5.4 Natural enemies .................................................................................... 17 1.6 Thesis rationale ........................................................................................... 17 1.7 Overall aim ................................................................................................... 18 1.8 Thesis scope and outline ............................................................................. 18 i Chapter 2: Population abundance and distribution of the large raspberry aphid (Amphorophora idaei) in relation to host plant resistance and growth ............ 20 2.1 Abstract ........................................................................................................ 20 2.2 Introduction .................................................................................................. 21 2.3 Materials and methods ................................................................................ 23 2.3.1 Introduction ........................................................................................... 23 2.3.2 Host plant .............................................................................................. 23 2.3.3 Aphids ................................................................................................... 24 2.3.4 Experimental design .............................................................................. 24 2.3.5 Statistical analysis ................................................................................. 25 2.4 Results ......................................................................................................... 27 2.5 Discussion ................................................................................................... 32 2.5.1 Individual and population performance ................................................. 32 2.5.2 Cultivars and feeding site ...................................................................... 33 2.5.3 Aphid impacts on plant growth .............................................................. 33 2.5.4 Conclusions ........................................................................................... 34 Chapter 3: Top-down control by Harmonia axyridis mitigates the impact of elevated atmospheric CO2 on a plant–aphid interaction .................................... 35 3.1 Abstract ........................................................................................................ 35 3.2 Introduction .................................................................................................. 36 3.3 Materials and methods ................................................................................ 38 3.3.1 Chambers .............................................................................................. 38 3.3.2 Host plant .............................................................................................. 38 3.3.3 Aphids ................................................................................................... 39 3.3.4 Coccinellids ........................................................................................... 39 3.3.5 Experiment 1: Trophic interactions ........................................................ 39 3.3.6 Experiment 2: Coccinellid development ................................................ 40 3.3.7 Statistical analysis ................................................................................. 41 ii 3.3.7.1 Experiment 1 .................................................................................. 41 3.3.7.2 Experiment 2 .................................................................................. 42 3.4 Results ......................................................................................................... 42 3.4.1 Experiment 1: Trophic interactions ........................................................ 42 3.4.1.1 Hypothesis 1 – Plant responses ..................................................... 42 3.4.1.2 Hypothesis 2 – Aphid responses .................................................... 44 3.4.2 Experiment 2: Coccinellid development ................................................ 47 3.5 Discussion ................................................................................................... 47 3.5.1 Conclusions ........................................................................................... 52 Chapter 4: Elevated atmospheric CO2 impairs aphid escape responses to predators and conspecific alarm signals ............................................................. 53 4.1 Abstract ........................................................................................................ 53 4.2 Introduction .................................................................................................. 54 4.3 Materials and Methods ................................................................................ 55 4.3.1 Insects, plants and environmental chamber conditions ........................ 55 4.3.2 Behavioural assays ............................................................................... 55 4.3.3 Statistical analysis ................................................................................. 56 4.4 Results ......................................................................................................... 58 4.5 Discussion ................................................................................................... 59 4.5.1 Conclusions ........................................................................................... 60 Chapter 5: Antagonistic interactions between an invasive and native coccinellid species may promote coexistence ................................................... 61 5.1 Abstract ........................................................................................................ 61 5.2 Introduction .................................................................................................. 62 5.3 Methods ....................................................................................................... 65 5.3.1 Aphid prey ............................................................................................. 65 5.3.2 Experiment 1: individual feeding preferences ....................................... 66 5.3.3 Experiment 2: interspecific coccinellid competition ............................... 66 iii 5.3.4 Statistical analysis ................................................................................. 66 5.4 Results ......................................................................................................... 67 5.4.1 Experiment 1: individual feeding preferences ....................................... 67 5.4.2 Experiment 2: interspecific coccinellid competition ............................... 68 5.5 Discussion ................................................................................................... 72 5.5.1 Interspecific aphid consumption rates ..................................................