Spatial and temporal dynamics in the development of invading cynipid communities in Britain Tracey Begg Thesis submitted for the degree of Doctor of Philosophy The University of Edinburgh 2007 ii Declaration This thesis has been composed by me and is the result of my own work. It contains no work done in collaboration except where stated otherwise. The text does not exceed 100,000 words. No part of this thesis has been submitted to any other University in application for a higher degree. Tracey Begg – November 2007 iii Abstract The British Isles have been invaded by 12 alien cynipid gallwasps over the past 150 years. The first 4 of these species have been studied in depth and represent a model system in phytophagous insect community structure. In this thesis, I extend this research programme to incorporate 8 further invaders. I examine recent changes in the distribution of invading oak gallwasps in Britain and spatial patterns in the composition of the associated communities of phytophagous cynipid inquilines and parasitoids. I use fully quantitative webs to assess the diversity and strength of trophic interactions between native and invading species and assess the potential for apparent competition between gallwasps mediated by shared natural enemies. Of the first 4 invaders to be studied, 3 have expanded their range since 1991/2. Three of these 4 species are now well established in Scotland, while Andricus corruptrix remains confined to England. Four new invaders (A. aries, A. lucidus, A. grossulariae, Aphelonyx cerricola) are established in southern England and are spreading. Rates of range expansion vary across species (between means of 3.3 and 24.4 km per year), and may be correlated with variation in lifecycles and abundance. The four newest invaders (Neuroterus saliens, Plagiotrochus australis, P. coriaceus, P. quercusilicis) are currently restricted to their sites of first record. Previous studies on one of the early invaders, Andricus quercuscalicis, identified south to north and east to west declines in community species richness and in the abundance of specific parasitoid species. I find that: 1) Parasitoid associations with the asexual galls of A. quercuscalicis track inquiline recruitment to this host. 2) The longitudinal and latitudinal gradients in parasitoid species richness demonstrated in previous work are no longer apparent, suggesting that younger northern communities may be converging on their older southern counterparts. 3) Inquilines show increasing survivorship with distance from the original centre of their distribution in south east England, suggesting at iv least temporary exploitation of enemy-free space. 4) The recently invading Andricus and Aphelonyx species have all rapidly recruited parasitoids and inquilines. Fully quantitative webs were constructed for 4 sites in England and Scotland incorporating both native and invading cynipids. I tested the hypothesis that newly arriving gallwasp generations would fall within food web compartments based on their host oaks and location on the tree as demonstrated in previous work. Counter to this hypothesis, parasitoids attacking one of the newest invaders (A. grossulariae) break down host tree-associated compartmentalisation. Where A. grossulariae has yet to become established, host-based compartmentalisation remains pronounced. Despite extensive sharing of parasitoid species, I found only one strong indirect interaction between species (both aliens) and no evidence for widespread apparent competition. Spatial density dependent predation on an appropriate scale can stabilise population dynamics. I quantified predation by blue tits (Parus caeruleus) of spring generation bud galls on Turkey oak (Q. cerris) at three spatial scales (shoots within branches, branches within trees, trees within sites). I found significant levels of bird predation, with most variation occurring between trees rather than between shoots within branches. Spatial density dependence was detected at sites in southern England, primarily at the level of trees within a site. Relationships at finer spatial scales were far more variable in magnitude and sign. My results suggest that blue tits forage primarily at the level of trees. This thesis presents comprehensive new data on the establishment and spread of 12 invading cynipid species and on their interactions with native communities. The results further understanding of both spatial and temporal aspects of natural enemy recruitment to invading species. In particular, it is clear that individual invading species can significantly modify trophic linkage between established food web compartments. Finally, my data emphasise the significant (but often unstudied) contribution of highly mobile vertebrate predators to otherwise closed ecological microcosms. v Acknowledgements I would like to thank both of my supervisors, Karsten Schönrogge and Graham Stone, firstly for their huge enthusiasm for the world of galls, enthusiasm I found inspiring and infectious and which will remain with me long after the intensity of effort a PhD brings has passed. Secondly, I am grateful for their good advice, imparted knowledge and reassurance which always gave me confidence that I could achieve my goals. Particular thanks go to Karsten for his unwavering support, generosity and patience throughout. As well as Karsten, I want to extend thanks to Chris Schönrogge for making me most welcome during time spent at CEH Dorset. I would like to thank the small army of people who gave me valuable assistance at various stages throughout my PhD: Dr George Melika, Dr Dick Askew, Dr Gyorgy Csóka, Rae Bishop, Sonja Preuss, Zoe Randle, Simon Hately, Will Goodall-Copestake, Kevin Conway, Chloe Bellamy and Chantelle Martin. I would also like to thank all the staff at Ashworth who helped smooth progress through my PhD with their assistance including Carol in the Post-graduate office, Jayne and David in accounts, all the staff in stores and the lab technicians for supplying me with equipment when I most needed it. Special thanks go to various family and friends for support, accommodation during field trips and pet-sitting while I was away from home. In particular, thanks to Eric, for the best support and assistance I could have had, wherever and whenever I needed it and to whom I dedicate this thesis. I also dedicate this thesis to the memory of Rae Bishop whose kindness and warmth will be missed but never forgotten by all her family and friends. Finally, I would like to thank the Natural Environmental Research Council and the CEH CASE studenship which funded my PhD. Contents Declaration ...................................................................................................................... ii Abstract ........................................................................................................................... iii Acknowledgements ....................................................................................................... v Contents .......................................................................................................................... vi Chapter 1. General Introduction ........................................................................... 1 1.1 Introduction ............................................................................................................... 1 1.2 Cynipid biology ........................................................................................................ 3 1.3 Natural enemies of cynipid gallwasps ...................................................................... 4 1.4 Ecological theory and the role of cynipids as model systems .................................. 8 1.5 Invading cynipid communities in Britain ............................................................... 16 1.6 Contents of this thesis ............................................................................................. 25 1.7 Contributors to the contents of this thesis ............................................................... 28 ........................................................................................................................................... Chapter 2. The current distribution of invading cynipids in Britain and the status of their associated communities ....................................................... 29 2.1 Introduction ............................................................................................................. 29 2.2 Methods .................................................................................................................. 33 2.2.1. Collection, rearing and identification of invading galls in Britain .................. 33 2.3 Results ..................................................................................................................... 34 2.3.1. Invading cynipid distributions in Britain ......................................................... 34 2.3.2. Rates of spread of invading cynipids in Britain .............................................. 35 2.3.3. The communities associated with invading cynipids in Britain ...................... 39 2.4 Discussion ............................................................................................................... 43 2.4.1. Distribution and rates of range expansion. ...................................................... 43 2.4.2. Parasitoid and inquiline communities ............................................................. 47 Chapter 3. Spatial and temporal