Dynamics of the guild structure in the parasitoids and inquilines of an alien gall wasp, Andricus quercuscalicis Burgsdorf by Karsten Schonrogge Thesis submitted for the Doctor of Philosophy of the University of London and for the Diploma of the Imperial College Department of Biology March 1994 Imperial College at Silwood Park Ascot/Berkshire Dynamics of the guild structure in parasitoids and inquilines of an alien gall wasp Abstract Rapid and substantial changes have occurred in the parasitoid and inquiline community associated with the agamic galls of Andricus quercuscalicis in Britain since the insect arrived in southern England. Over the last 5 years the species composition converged to that recorded from galls from the native range. High rates of attack by inquilines, virtually absent in previous surveys, were recorded in south-east England, but not at the edge of the invaded range. Inquiline abundance was positively correlated with parasitoid species richness, because most parasitoid species concentrated their attack on inquilines. An examination of the guild structure sampled in different parts of the native and invaded range revealed continuous trends away from the native range in a number of community and food-web parameters. The abundance patterns of 4 parasitoid species attacking the gall-maker, and 2 parasitoid species attacking inquiline larvae, were related to: 1) gall morphology; 2) the geographical location of the sample sites; and 3) the abundance of other members of the guild. While parasitism of the agamic galls was low (<5% in Britain, <15 % in the native range), ten parasitoid species caused local mortalities up to 80% in the sexual galls of A. quercuscalicis collected in the native range. An analysis for spatial variation in density dependent abundance patterns showed both positive and negative density dependence as well as density independent relationships between parasitism and host density at all spatial scales and for all parasitoid species. A comparison between the distributions of A. quercuscalicis and two other invading gall wasps, Andricus kollari and A. lignicola, showed that A. quercuscalicis was the only species positively associated with the presence of Turkey oak (an obligate host tree) and suggests that A. quercuscalicis exhibits the lowest rate of spread. 2 Dynamics of the guild structure in parasitoids and inquilines of an alien gall wasp Table of contents Abstract 2 Table of contents 3 List of Figures 7 List of Tables 8 1. Introduction 10 1.1. Life-cycle of Andricus quercuscalicis 11 1.2. Recruitment of native natural enemies by an invader 11 1.3. The process of recruitment and the role of pre-adaptation 11 1.4. Previous work on the communities of the galls of A. quercuscalicis 12 1.5. History of the invasion 13 1.6. Contents of this thesis 14 1.7. General statement to the production of this thesis 15 2. Alien herbivores and native parasitoids: rapid development of guild structure in an invading gall wasp, Andricus quercuscalicis (Hymenoptera: Cynipidae) 17 2.1. Introduction 17 2.1.1. Natural history of the invader 18 2.1.2. Earlier studies on the parasitoid and inquiline community 18 2.2. Methods 19 2.2.1. Sample sites 19 2.2.2. Rearings and dissections 19 2.2.3. Analysis of the geographical surveys 21 2.3. Results 23 2.3.1. Members of the community 23 2.3.2. Inquilines 24 2.3.2.1. Phenology of inquiline emergence 24 2.3.2.2. Geographical patterns of inquiline infestation in knopper galls 27 2.3.3. Parasitoids 29 2.3.3.1. Phenology of the parasitoid emergence 29 2.3.3.2. Parasitoid species richness 33 2.4. Discussion 33 2.4.1. The distribution of inquiline attack 34 2.4.2. Recruitment of parasitoids in the asexual galls of A. quercuscalicis over time 35 2.4.3. The communities of Andricus quercuscalicis in the future 36 2.4.4. Inquiline and parasitoid phenology 37 2.4.5. Coexistence with other cynipid galls 38 3 Dynamics of the guild structure in parasitoids and inquilines of an alien gall wasp 2.4.6. Conclusions 38 3. Spatial and temporal variation in guild structure: Parasitoids and inquilines of Andricus quercuscalicis Burgsd. (Hymenoptera: Cynipidae) in its native and alien ranges 39 3.1. Introduction 39 3.2. Methods 40 3.2.1. Sample sites 40 3.2.2. Rearings and Dissections 42 3.2.3. Community structure statistics 42 3.2.4. Food web properties 42 3.3. Results 43 3.3.1. Parasitoids and inquilines 43 3.3.1.1. Inquilines 44 3.3.1.2. Parasitoids 44 3.3.2. Distribution 44 3.3.3. Community structure 46 3.3.4. Food webs 48 3.4. Discussion 52 3.4.1. Food web properties 52 3.4.2. Associations between species and their distribution 53 3.4.3. Conclusion 54 4. The abundance and species richness of the parasitoid and inquilines of an invading gall wasp: Andricus quercuscalicis (Hymenoptera: Cynipidae) 56 4.1. Introduction 56 4.2. The guild of inhabitants associated with knopper galls 57 4.3. Methods 58 4.3.1. Sites 58 4.3.2. Rearing techniques 58 4.3.3. Local cynipid species richness 60 4.3.4. Modelling 60 4.4. Results 61 4.4.1. Geographic trends in the explanatory variables 61 4.4.2. Parasitoids 62 4.4.3. Parasitoids of the gall former 62 4.4.4. The inquilines 66 4.4.5. The common parasitoids of inquilines 67 4.4.6. Species richness of the A. quercuscalicis parasitoid guild 68 4.4.7. Species richness of the inquiline parasitoid guild 68 4.5. Discussion 70 4.5.1. Parasitoid and inquiline abundance and gall morphology 70 4.5.2. Parasitoid and inquiline abundance and geography 70 4.5.3. Patterns of parasitoid species richness 71 4 Dynamics of the guild structure in parasitoids and inquilines of an alien gall wasp 5. Patterns of mortality in galls of the sexual generation of the cynipid gall-wasp Andricus quercuscalicis (Hymenoptera; Cynipidae) 73 5.1. Introduction 73 5.1.1. Causes of mortality in the sexual generation of A. quercuscalicis. 73 5.1.2. Patterns of parasitoid-induced mortality in sexual galls 74 5.2. Methods 74 5.2.1. Sampling methods 74 5.2.2. Rearing methods 75 5.2.3. Detection of density dependence 76 5.3. Results 77 5.3.1. The parasitoid guild found in the sexual galls of A. quercuscalicis. 77 5.3.1.1. The 1000 catkin rearings. 77 5.3.1.2. Rearings from Tausendblum, Valdice and Zalaegerszeg. 78 5.3.1.3. Sex ratios of emerging parasitoids 81 5.3.2. Variation in mortality between trees within sites and between sites (Tausendblum, Valdice and Zalaegerszeg). 82 5.3.3. Analyses of density dependence within trees within sites 83 5.3.3.1. Mesopolobus fuscipes 83 5.3.3.2. Aulogymnus kelebiana 84 5.3.3.3. Mesopolobus xanthocerus 86 5.3.3.4. Total parasitoid-induced mortality 87 5.4. Discussion 87 5.4.1. Parasitoid sex-ratios 87 5.4.2. Mortality by parasitism in the sexual galls of A. quercuscalicis 88 5.4.3. Density dependent parasitoid attacks. 88 6. The distribution and abundance of alien, host-alternating Andricus spp. (Hymenoptera: Cynipidae) on oak in Ireland 91 6.1. Introduction 91 6.2. Methods 91 6.3. Results 93 6.3.1. Oaks 93 6.3.2. Cynipids 96 6.3.2.1. Distribution 96 6.3.2.1.1. Andricus kollari 99 6.3.2.1.2. Andricus lignicola 100 6.3.2.1.3. Andricus quercuscalicis 100 6.3.2.1.4. Andricus corruptrix 101 6.3.3. Cynipid species richness 101 6.4. Discussion 103 6.4.1. Dispersal 103 6.4.2. Intraspecific and interspecific competition 103 5 Dynamics of the guild structure in parasitoids and inquilines of an alien gall wasp 6.4.3. Cynipid species richness 104 7. Discussion 106 7.1. A community in development 106 7.2. The invasion of Andricus quercuscalicis and time as a determining factor for guild structure 107 7.2.1. The guild in knopper galls from Britain 107 7.2.2. The guild in knopper galls in continental Europe 108 7.3. Parasitism in the sexual generation of A. quercuscalicis 110 7.4. Further questions and future research 111 7.4.1. The future of the invasion 111 7.4.2. Interactions with native cynipid species in Britain 112 8. Bibliography 114 9. Acknowledgements 126 6 Dynamics of the guild structure in parasitoids and inquilines of an alien gall wasp List of Figures Figure 2.1 : The distribution of Andricus quercuscalicis and of the sample sites (aggregated in 10km squares) 20 Figure 2.2 : Collection scheme to establish dispersal from a point source 22 Figure 2.4 : Inquiline attack in knopper galls collected in Silwood Park from July to September 1992 26 Figure 2.5 : Distribution of inquiline attack rates (aggregated in 10km squares) 28 Figure 2.6 : Emergence periods for Andricus quercuscalicis and its coinhabiting inquilines and parasitoids in 1992 31 Figure 2.7 : Distribution of a) Sycophila biguttata and b) Mesopolobus jucundus in Knopper galls (aggregated in 10km squares) 32 Figure 3.1 : Geographical location of the collection sites in Europe 41 Figure 3.2a-g : Trophic relationships in the knopper gall guild from 7 areas within the collected range 49 Figure 4.1: Sites in Europe from which knopper galls were dissected 59 Figure 4.2 a-b: Average gall width and gall height according to the content to gall wasps larval chamber 63 Figure 4.3: The proportion Synergus gallaepomiformis of the number of inquilines emerged from samples collected across Europe 66 Figure 4.4: Positive density dependence of Cecidostiba adana on its inquiline hosts 67 Figure 4.5: Predicted number of inquiline parasitoid species according to the geographical location and the available number of hosts 69 Figure 6.1: Distribution of the host tree species, a) Quercus robur, b) Q.