Biodiversity and Ecosystem Services: Pollination, Biological Control, and Nature Conservation in Agricultural Landscapes Gorm Shackelford Submitted in accordance with the requirements for the degree of Doctor of Philosophy The University of Leeds School of Biology September 2014 The candidate confirms that the work submitted is his own, except where work which has formed part of jointly-authored publications has been included. The contribution of the candidate and the other authors to this work has been explicitly indicated below. The candidate confirms that appropriate credit has been given within the thesis where reference has been made to the work of others. Chapter 2 is based on a jointly-authored publication [Shackelford G., Steward, P. R., Benton, T. G., Kunin, W. E., Potts, S. G., Biesmeijer, J. C., Sait, S. M. (2013). Comparison of pollinators and natural enemies: a meta-analysis of landscape and local effects on abundance and richness in crops. Biological Reviews 88(4):1002–1021]. The candidate designed the research, collected and analyzed the data, and wrote and revised the manuscript for this publication. Peter Steward contributed to data collection. The other authors supervised the research and gave feedback on the manuscript. A plural pronoun (“we”) is used in parts of this thesis, and this is not meant to suggest that the candidate (“I”) is not the author, but it is meant to acknowledge the feedback that others have given, or to prepare these parts of the thesis for jointly-authored submissions to scientific journals. All of Chapter 2 was written only by the candidate. Chapter 3 is based on a jointly-authored manuscript [Shackelford G. E., Steward, P. R., German, R. N., Sait, S. M., Benton, T. G. (in press). Conservation planning in agricultural landscapes: hotspots of conflict between agriculture and nature. Diversity and Distributions]. The candidate designed the research, collected and analyzed the data, and wrote and revised the manuscript. The other authors gave feedback on the manuscript. In particular, Tim Benton suggested that hotspots for agricultural intensification could also be identified, as a counterpoint to the hotspots of conservation conflict that the candidate had suggested. The candidate then redesigned the conceptual framework, reanalyzed the data, and completely rewrote the manuscript. Three anonymous peer reviewers gave feedback on the manuscript. In particular, one of them suggested that hotspots of agricultural intensification should not be identified, because it implied that agricultural intensification could not or should not be stopped or questioned. The candidate again redesigned the conceptual framework, replaced hotspots for agricultural intensification with coldspots of conservation conflict, reanalyzed the data, and completely rewrote the manuscript. All of Chapter 3 was written only by the candidate. This copy has been supplied on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgment. The right of Gorm Eirik Shackelford to be identified as Author of this work has been asserted by him in accordance with the Copyright, Designs and Patents Act 1988. Copyright © 2014 Gorm Eirik Shackelford and The University of Leeds — 2 — Acknowledgments Thanks to the Biotechnology and Biological Sciences Research Council (BBSRC) of the United Kingdom, Africa College of the University of Leeds, and Ecosystem Services for Poverty Alleviation (ESPA) for funding this research. Thanks to Francis Namisiko, my field assistant, for all his hard work, making and collecting so many trap nests, and riding so many kilometers by motorcycle on the rough and often muddy roads of the Taita Hills. Thanks also to my many supervisors in the UK and Kenya, especially Steve Sait, Mary Gikungu, and Tim Benton, who all gave me feedback and support whenever I asked, but also gave me the freedom to work unsupervised in Kenya, which was a very special time and place in my life, and for which I will always be thankful. Thanks also to Jacobus Biesmeijer, William Kunin, Simon Potts, and Richard German for feedback. Thanks to Peter Steward, my fellow PhD student, who also gave me feedback, and who, together with Radhika Timbadia, lived the hard, weird, and wonderful lifestyle of the Taita Hills with me. Thanks also to the MSc students who came to work with me in the Taita Hills, Justin Lampley, Joseph Makaure, Tomasz Przybylowicz, and Rebecca Newman. Thanks to James Carpenter and Josef Gusenleitner for identifying Rhynchium marginellum sabulosum, and thanks to the National Museums of Kenya, Jayne Macharia, Mary Gikungu, and Connal Eardley for giving me taxonomic support in Kenya and South Africa. Thanks to Lilian Igweta and ICIPE for providing permits and visas for Kenya. Thanks to A. S. Dippenaar-Schoeman for sending me a copy of her key to the genera of African spiders, which was used by one of the MSc students (Joseph Makaure). Thanks to the many suppliers of tools and materials that were used in this research, especially Milimani Hardware, Pamtech, and Nakumatt in Kenya, Home Chip in the UK, and Adorama and B&H Photo in the USA. Thanks to the staff of Java House and Artcaffé in Nairobi, which often functioned as my offices. Thanks to Katana, Gideon, and James, for driving me to the National Museums of Kenya or the airport on many days. Thanks to the free and open-source software community, especially those who have worked on LibreOffice, QGIS, R, Scribus, Zotero, and the fonts, Droid Sans, Droid Sans Mono, and Droid Serif. Thanks to my family, Frankie, Jole, and Leif Shackelford, for supporting me from the USA, whether I was in the UK, Kenya, or South Africa. Thanks to my cousin-in- law, Diane Skinner, for camaraderie, accommodation, and entertainment in Nairobi, and for making light of my many dark evenings of work on the meta-analysis (the “MA”), through which she suffered by proximity to me, and to which she often referred by a colorful acronym (the “MFMA”), which shall remain undefined. And, of course, many, many thanks to Sarah Norman, my partner in life, for always being there for me, and for being here, there, and everywhere with me. — 3 — Abstract Agriculture has done more damage to nature than any other human activity, and yet food production could need to be doubled by the middle of this century. As agricultural land is expanded and intensified, critical thresholds in the loss of natural habitats are crossed. This loss of non-crop habitats can have negative feedback on crop production, because it can cause a loss of “ecosystem services” that support and regulate crop production, such as the pollination of crops by bees and the biological control of crop pests by their natural enemies. Because of this connection between non-crop habitats and crop yields, there could be potential for habitat conservation to benefit both agriculture and nature. The research in this thesis focuses on pollinators and natural enemies, because these species constitute a vital connection between food production and biodiversity conservation. Could habitat management be used to conserve both pollinators and natural enemies in agricultural landscapes? Will the relationships between pollinators, natural enemies, and natural habitats change with climate change? Where should we prioritize the resolution of conflict between agriculture and nature, and how? This thesis addresses these questions through literature review and meta- analysis, geographic information systems (GIS) and hotspot analysis, field research on the distributions of trap-nesting bees and wasps on environmental gradients, and laboratory research on the development of bees and wasps at high temperatures. This thesis suggests that it might be possible to conserve communities of both pollinators and natural enemies, in general, by means of habitat management, but it might not be possible to conserve specific combinations of pollinators and natural enemies, which might have opposite responses to some forms of environmental change, such as global warming. This thesis also suggests that the resolution of conflict between agriculture and nature should be prioritized in sub-Saharan Africa, and it outlines a conceptual framework for systematic conservation planning in agricultural landscapes. — 4 — Table of contents Acknowledgments..................................................................................................................3 Abstract................................................................................................................................... 4 List of tables............................................................................................................................ 8 List of figures.......................................................................................................................... 9 Chapter 1: Biodiversity and ecosystem services: conservation of pollinators, natural enemies, and natural habitats in agricultural landscapes............................................11 Introduction to the thesis.........................................................................................11 The search for compromise between food production and other ecosystem services................................................................................13 The sustainable intensification of agriculture in sub-Saharan Africa.......15 Kenya and the Taita Hills............................................................................16 Crop