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Chapter 6. Bumblebee Activity and Forage Use in Upland Hay Meadows

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Chapter 6. Bumblebee Activity and Forage Use in Upland Hay Meadows The effects of invertebrates on the plant communities in upland hay meadows Sarah Elizabeth Barlow Doctor of Philosophy School of Biology Newcastle University December 2012 Abstract Species rich upland hay meadows are of high biodiversity importance and are internationally rare. There is increasing interest in restoring botanically diverse meadows in the uplands but little is known about the role of invertebrates. The purpose of the project was to investigate the role of (i) slugs as seedling herbivores and (ii) pollinators in affecting the plant communities. Research has revealed important interactions between invertebrates and plant life history traits with implications for grassland restoration. Slugs are known to affect plant communities by the selective seedling removal of more acceptable species, although few studies have considered their impact at restoration sites. A glasshouse feeding trial showed the acceptability of seedlings of different meadow plants to slugs is influenced by plant defensive properties. Field investigations of slug population densities identified a negative correlation with increasing levels of agricultural improvement. This relationship was partly driven by the increase in grass abundance cover in agriculturally improved meadows and may be influenced by the anti-feedant properties of silica-rich grass leaves. A 3-year mesocosm study found evidence that slugs are an important selective force affecting seedling recruitment and community composition. The selective seedling removal of the hemi-parasite and keystone species Rhinanthus minor was a key finding of this study. Use of Scanning Electron Microscopy showed the leaf surface of R. minor to be characterised by a diverse assemblage of trichomes which may play an important role in anti-herbivore defence. Parallel declines in pollinator and insect-pollinated plant populations have raised concerns that smaller populations of important pollinator groups such as bumblebees may be reducing seed set by plants. Survey work showed upland hay meadows to be an important forage resource for common and rare/scarce bumblebees. Bumblebees visited a small number of forage plants, most notably R. minor, Trifolium species and Geranium sylvaticum. Pollen supplementation tests did not find significant evidence that reproductive output of R. minor and G. sylvaticum (a gynodioecious species) was limited by pollination services. Testing of a new system to record pollinator visitors to flowers proved highly effective and i offers the potential to significantly reduce time and labour input into the study of plant-invertebrate interactions. The project has shown that invertebrates are an important functional group affecting the success of plant species in hay meadows. The findings provide new and important information to the industry in developing management prescriptions for restoring upland hay meadows and other botanically rich plant communities. ii Acknowledgements It is with much appreciation and gratitude that I thank the Perry Foundation for providing funding for this project. I thank and acknowledge Dr. Andrew Close (School of Biology, Newcastle University) for his advice and work in analysing much of the data generated by studies within this thesis, namely: i) in Chapter 2, the analysis of data using CAP, PERMANOVA and PERMDISP performed in PRIMER-E ; ii) in Chapter 3, the analysis of data using GAMM performed in R and writing of the statistical method; iii) in Chapter 4, the analysis of data using db- RDA, db-linear model, PERMANOVA and PERMDISP performed in PRIMER-E and assistance with writing the statistical method; and iv) in Chapter 6, the analysis of data using CAP and PCA performed in PRIMER-E and suggestions for future analyses. I am grateful to the technical staff at Close House Biology Field Station, Alan Craig and Robert Hodgson, for their continued support and advice, and help with setting-up and maintaining experiments. I thank Malcolm Barlow and Alan Craig for assistance in conducting field work in the Yorkshire Dales and landowners for granting access to study sites. For work detailed in Chapter 5, I thank Tracey Davey (Electron Microscopy Research Services, Newcastle University) and Pauline Carrick (Advanced Chemical and Materials Analysis, Newcastle University) for SEM and EDX spectroscopy expertise, respectively. I am grateful to Shaun Hackett (Ranger, Northumberland National Park) for his training in bumblebee identification and assistance with field work conducted at Barrowburn (Chapter 6). For work detailed in Chapter 8, the development of Rana was solely the work of Dr. Mark O’Neill. I also thank Daniel Reed for his assistance with experimental work involved in this Chapter. I thank Dr. Roger Smith (Newcastle University) for first introducing me to upland hay meadows and his help as second supervisor during the early stages of the project. I am also grateful to him for allowing data collected as part of the DIGFOR project (BD1451) to be used within the study detailed in Chapter 2. Finally, I thank my Supervisor Dr. Gordon Port for his much valued support and guidance throughout this project. iii Table of Contents Table of Contents Page Chapter 1. General Introduction 1 1.1 General Introduction 1 Chapter 2. Effects of agricultural intensification and 6 environmental factors on slug densities in upland hay meadows 2.1 Abstract 6 2.2 Introduction 7 2.3 Method 11 2.3.1 Statistical analysis 14 2.4 Results 16 2.4.1 Slug densities 16 2.4.2 Influence of management and environmental factors on 19 slug densities 2.5 Discussion 29 Chapter 3. The acceptability of meadow plants to the slug 39 Deroceras reticulatum and implications for grassland restoration 3.1 Abstract 39 3.2 Introduction 40 3.3 Method 43 3.3.1 Deroceras reticulatum 43 3.3.2 Collection and maintenance of slugs 43 3.3.3 Plant material and relative acceptability 44 3.3.4 Statistical analysis 45 3.4 Results 46 3.4.1 Cyanogenesis testing of Fabaceae seedlings 46 3.4.2 Relative acceptability 47 3.4.3 Plant traits 55 3.5 Discussion 55 iv Table of Contents Page Chapter 4. Effects of slug herbivory on meadow plant 62 communities and implications for grassland restoration 4.1 Abstract 62 4.2 Introduction 63 4.3 Method 66 4.3.1 Experimental design 66 4.3.2 Data collection 70 4.3.3 Statistical analysis 70 4.4 Results 74 4.4.1 Species richness and abundance cover of functional 75 groups 4.4.2 Species diversity 84 4.4.3 Treatment effects on community assemblages 84 4.4.4 Rhinanthus minor seedling recruitment in the unimproved 106 community 4.4.5 Hay biomass 107 4.4.6 Slug activity 108 4.5 Discussion 111 Chapter 5. Foliar trichomes of Rhinanthus minor: an adaptation 125 for herbivore defence? 5.1 Abstract 125 5.2 Introduction 126 5.3 Method 132 5.3.1 Plant material 132 5.3.2 Scanning Electron Microscopy (SEM) and Energy- 133 Dispersive X-ray (EDX) Spectroscopy 5.4 Results 134 5.4.1 Mature leaves 134 5.4.2 Seedling leaves 136 5.5 Discussion 148 v Table of Contents Page Chapter 6. Bumblebee activity and forage use in upland hay 155 meadows 6.1 Abstract 155 6.2 Introduction 156 6.3 Method 159 6.3.1 Statistical analysis 162 6.4 Results 163 6.4.1 Bumblebee activity 164 6.4.2 Forage use 170 6.5 Discussion 174 6.5.1 Study limitations and future recommendations 178 Chapter 7. Is plant reproductive output limited by pollinator 180 services in a species-rich upland hay meadow? A case study of Rhinanthus minor and Geranium sylvaticum 7.1 Abstract 180 7.2 Introduction 180 7.2.1 Study species 184 7.3 Method 188 7.3.1 Study site 188 7.3.2 Experimental design 188 7.3.3 Statistical analysis 190 7.4 Results 190 7.4.1 Rhinanthus minor 190 7.4.2 Geranium sylvaticum 192 7.5 Discussion 195 7.5.1 Conclusions and suggestions for future research 199 7.6 Glossary 200 vi Table of Contents Page Chapter 8. Recording pollinator visitation to flowers using an 202 automated motion detection system (Rana) 8.1 Abstract 202 8.2 Introduction 202 8.3 Materials & Method 204 8.3.1 Monitoring set-up 204 8.3.2 Recording pollinator visitors to Rhinanthus minor and 205 Centaurea nigra 8.4 Results & Discussion 206 8.4.1 Rhinanthus minor 206 8.4.2 Centaurea nigra 208 8.4.3 Conclusions 211 Chapter 9. General Discussion 212 9.1 General Discussion 212 9.1.1 Conclusions 218 APPENDIX – Supplemental Information 220 1. Supplementary information to Chapter 2: Effects of agricultural 220 intensification and environmental factors on slug densities in upland hay meadows 2. Supplementary information to Chapter 3: The acceptability of 221 meadow plants to the slug Deroceras reticulatum and implications for meadow restoration. 3. Supplemental information to Chapter 4: Effects of slug herbivory on 227 meadow plant communities and implications for grassland restoration References 230 vii List of Tables List of Tables Page Chapter 2. Effects of agricultural intensification and 6 environmental factors on slug densities in upland hay meadows Table 2.1. National Grid References of soil samples taken from 13 meadows in the Yorkshire Dales, UK. Table 2.2. Mean (±SEM) population densities of slug species 18 extracted from soil samples (0.09 m2) in meadows of different agricultural improvement categories (unimproved, semi-improved, improved) at five locations in the Yorkshire Dales. Table 2.3. Canonical Analysis of principal coordinates (CAP) for slug 23 densities within upland hay meadows, incorporating a cross validation test using Leave-one-out Allocation of Observations to Groups (for the choice of m: 3). Groups are agricultural improvement categories (I= improved; SI = semi-improved; UI = unimproved) representing a gradient of increasing management intensity. Table 2.4. Partial correlations between canonical axes and slug 27 species generated by a Canonical analysis of principal coordinates (CAP) for slug assemblages in meadows classified according to management type and constrained by environmental factors.
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