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The underestimated taxa: the role of non-bee pollinators in temperate vegetable crops, experimental research in strawberry (Fragaria spp.) crops by Ellen Richard A Thesis presented to The University of Guelph In partial fulfilment of requirements for the degree of Master of Science in School of Environmental Sciences Guelph, Ontario, Canada © Ellen Richard, September, 2019 ABSTRACT THE UNDERESTIMATED TAXA: THE ROLE OF NON-BEE POLLINATORS IN TEMPERATE VEGETABLE CROPS, EXPERIMENTAL RESEARCH IN STRAWBERRY (Fragaria spp.) CROPS Ellen Richard Advisor(s): University of Guelph, 2019 Dr. Nigel E. Raine Dr. Dirk Steinke Pollination services are critical to agricultural systems, providing a third of global food production. Non-bee pollinators have received little recognition with regards to their role in commercial agricultural pollination. Diverse pollinator communities often provide better pollination services, and non-bee pollinators represent 95% of this diversity. Additionally, research demonstrates that many non-bee pollinators are more resilient to land use intensification and climate change due to their nomadic life-history and tolerance to inclement weather. The aim of this thesis is two-fold. It demonstrates the diversity of non-bee insects that visit temperate vegetable crops in a comprehensive review. Secondly, it presents research on the non-bee floral visiting community of day- neutral strawberries in Southern-Ontario. Using barcoding methods as well as quantitative analysis it characterises flower visitor communities, their foraging preferences and levels of floral fidelity. Hoverflies were found to be important non-bee flower visitors, carrying comparable amounts of pollen to bees. ACKNOWLEDGEMENTS I would like to thank the members of the Raine lab that were present for the duration of my master’s degree, providing support and help when they could, in particular, Dr. Elizabeth Franklin, Leah Blechschmidt and Hayley Tompkins. Additional thank you to members of the Steinke lab for their training and patience, special thanks to Dr. Thomas Braukmann. Finally, thank you to Dr. Dirk Steinke for being available; for your help, support and guidance during the second half of my thesis and giving me the opportunity to attend the 8th iBOL conference in Norway. Thank you to the growers that allowed me access to their properties and allowed me to sample in their fields. I would also like thank the financial support I received to support my research. The Natural Sciences and Engineering Research Council (NSERC: Discovery grant 2015-06783 awarded to N.E.R.), the Food from Thought: Agricultural Systems for a Healthy Planet Initiative, by the Canada First Research Excellent Fund (grant 000054), and W.G. Matthewman Scholarship awarded to me in 2017. iii AUTHOR’S DECLARATION OF WORK COMPLETED I declare that all work presented in this thesis is my own, with the following exceptions: Dr. Thomas Braukmann assisted with development of protocol for pollen metabarcoding. iv TABLE OF CONTENTS Abstract ............................................................................................................................ii Acknowledgements ......................................................................................................... iii Author’s Declaration of Work Completed ........................................................................iv Table of Contents ............................................................................................................ v List of Tables .................................................................................................................. vii List of Figures ................................................................................................................ viii List of Appendices ...........................................................................................................ix 1 Chapter 1: General Introduction ............................................................................... 1 1.1 Importance of non-bee pollinators ...................................................................... 3 2 Chapter 2: The underestimated taxa: the role of non-bee pollinators in temperate crops ............................................................................................................................... 7 2.1 Introduction ........................................................................................................ 7 2.2 Methods ............................................................................................................. 9 2.3 Crop Assessments ........................................................................................... 12 2.3.1 Fruits.......................................................................................................... 12 2.3.2 Vegetables ................................................................................................. 24 2.3.3 Nuts ........................................................................................................... 42 2.4 Discussion ........................................................................................................ 46 3 Chapter 3: Assessing non-bee flower visiting community of strawberries .............. 48 3.1 Introduction ...................................................................................................... 48 3.2 Methods ........................................................................................................... 51 3.2.1 Experimental Fields ................................................................................... 51 v 3.2.2 Field Sampling ........................................................................................... 52 3.2.3 Pollen Removal and Quantification ............................................................ 53 3.2.4 Molecular Identification .............................................................................. 54 3.2.5 Data Analysis ............................................................................................. 58 3.3 Results ............................................................................................................. 60 3.3.1 Diversity and Pollen Loads ........................................................................ 60 3.3.2 Pollen Metabarcoding and Pollinator Networks ......................................... 72 3.3.3 Environmental Variance on Community Structure ..................................... 77 3.4 Discussion ........................................................................................................ 81 3.5 General Conclusions ........................................................................................ 85 References .................................................................................................................... 87 Appendices ................................................................................................................. 114 vi LIST OF TABLES Table 2.1: List of temperate crops assessed in this review, the degree of pollination dependence and assessment of whether non-bee pollination is likely, based on the literature reviewed. ........................................................................................................ 11 Table 3.1: Primers used for barcoding .......................................................................... 58 Table 3.2: Insect visitors collected from day-neutral strawberries ................................. 63 Table 3.3: Insect visitors observed on day-neutral strawberries .................................... 69 Table 3.4: A generalized linear model representing non-bee pollen count data at the genus level (n=53). ........................................................................................................ 71 vii LIST OF FIGURES Figure 2.1: Pollinator papers assessed during literature review of non-bee pollinators, presenting trends across the years 1930 to present........................................................ 9 Figure 3.1: Total pollen load on non-bee strawberry visitors ......................................... 66 Figure 3.2: Abundance of strawberry flower visiting species ......................................... 67 Figure 3.3: Average pollen carried by species visiting strawberry ................................. 68 Figure 3.4: Plant-flower visitor network at the family level ............................................. 75 Figure 3.5: Plant-syrphid network at the plant family level ............................................ 76 Figure 3.6: Triplot of redundancy analysis with species scaling .................................... 79 Figure 3.7: Boxplot representation of observed abundance .......................................... 80 viii LIST OF APPENDICES Appendix 1: List of species recorded visiting flowers of the focal crops assessed. ..... 114 Appendix 2: Species-level identification of specimens caught in strawberry fields, accompanied by the number of individuals caught and their average pollen load count. .................................................................................................................................... 154 Appendix 3: Plant genera and families of pollen found on insect visitors of strawberry crops ........................................................................................................................... 157 Appendix 4: Triplot of redundancy analysis coloured by site ....................................... 160