MIAMI UNIVERSITY The Graduate School Certificate for Approving the Dissertation We hereby approve the Dissertation of David Jon Stasek Candidate for the Degree: Doctor of Philosophy ____________________________________________ Director Thomas O. Crist ____________________________________________ Reader Ann L. Rypstra ____________________________________________ Reader Bruce A. Steinly ____________________________________________ Michael J. Vanni ____________________________________________ Graduate School Representative Martin Henry H. Stevens ABSTRACT POPULATION RESPONSES OF A GENERALIST INSECT PREDATOR AND ITS PREY TO PATCH CHARACTERISTICS IN FORAGE CROPS by David Jon Stasek There is a large body of literature documenting the effect of habitat features on populations of single species, but there are fewer studies documenting the effects of patch characteristics on community and ecosystem processes. Specifically, there are few studies that document the effect of dispersal among habitat patches on species interactions. Using an experimental field of forage crops, I assessed the population response of a generalist predatory insect, the damsel bug ( Nabis spp.), to prey density and the patch characteristics of size, matrix type, and habitat fragmentation. I then determined the functional response and preference of the damsel bug to two common leafhopper species in the forage-crop system: the constricted leafhopper ( Agallia constricta ) and the clover leafhopper ( Ceratagallia agricola ). Finally, I studied how dispersal among habitat patches and leafhopper and damsel bug density affected the survival of A. constricta using connected experimental mesocosms. In the experimental field, damsel bugs had higher abundances in large patches and patches surrounded by an orchard-grass matrix. Both damsel bug nymphs and adults aggregated in patches with high densities of constricted leafhoppers and aphids. There was no effect of habitat fragmentation. In functional response experiments, the damsel bug displayed a Type I functional response to both species of leafhoppers and showed a preference for A. constricta . In experimental mesocosms, there was no difference in the survival probabilities of leafhoppers in any treatment when isolation and conspecific density were varied. Damsel bug density and dispersal did affect the survival probability of leafhoppers with leafhoppers having lower survival rates in patches that were not isolated from one another. This study is one of the first experimental tests of varying dispersal to assess the survival probability of species within a metacommunity, as well as assessing the effects of patch characteristics on interspecific interactions. Results from this research also indicate that the damsel bug may be a candidate to help control A. constricta in agroecosystems. POPULATION RESPONSES OF A GENERALIST INSECT PREDATOR AND ITS PREY TO PATCH CHARACTERISTICS IN FORAGE CROPS A DISSERTATION Submitted to the Faculty of Miami University in partial fulfillment of the requirements for the degree of Doctor of Philosophy Department of Zoology by David Jon Stasek Miami University Oxford, OH 2009 Dissertation Advisor: Thomas O. Crist TABLE OF CONTENTS List of Tables iii List of Figures iv Acknowledgements vi 1 Literature Review 1 2 The effects of landscape features and prey density 14 and composition on a generalist insect predator in red clover and grass forage crops 3 The predation rate and functional response of a 37 generalist insect predator to leafhopper prey: the roles of prey preference and habitat complexity 4 The effects of dispersal and predator density on 55 survival time of insects in an insect-red clover metacommunity 5 Synthesis 75 ii LIST OF TABLES Chapter 2 Table 1. Results of generalized linear models for treatment 29 effects on damsel bug nymphs Table 2. Herbivore covariates of best-fitting treatment models 30 for damsel bug nymphs. Table 3. Results of generalized linear models for 31 treatment effects on damsel bug adults. Table 4. Herbivore covariates of best-fitting treatment 32 models for damsel bug adults. Chapter 4 Table 1. Survival probabilities (±SE) and mean (±SD) 70 A. constricta surviving per day in response to varied isolation and leafhopper density. “Isolation” is the percentage of time per week that connecting tubes were open to movement. “Density” is the density of leafhoppers per mesocosm. “Time” is the hours since the experiment commenced. Table 2. Survival probabilities (±SE) and mean (±SD) 71 A. constricta surviving per day in response to varied isolation and damsel bug density. “Isolation” is the percentage of time per week that connecting tubes were open to movement. “Density” is the density of damsel bugs per mesocosm. “Time” is the hours since the experiment commenced. Different letters after isolations indicate a significant difference in survival probability (P<0.05). Chapter 5 Table 1. Summary of damsel bug responses towards 85 A. constricta and C. agricola . Results come from both field and mesocosm experiments. “Adult aggregation” refers to when prey species were added as covariates into generalized linear models to determine which prey species damsel bug adults aggregated. iii LIST OF FIGURES Chapter 2 Figure 1. Design of the experimental red clover field. 33 Dark, speckled areas represent red clover patches, light grey areas represent orchard grass, and white areas represent bare ground. Figure 2. Damsel bug density in July for A) nymphs 34 and adults (B and C) plotted against prey density. The pea aphid was the best-fitting model with prey in July for nymphs, while a model with both the pea aphid and the constricted leafhopper was the best-fitting model in July for adults. Both damsel bug and prey densities were ln-transformed. Figure 3. Damsel bug nymph density plotted against prey 35 density in September. The best-fitting model contained the main effects of size and matrix type and the constricted leafhopper (A and B) and the spotted alfalfa aphid (C and D). Both damsel bug and prey densities were ln-transformed. Figure 4. Damsel bug adult density in September. Matrix 36 type was the best model to explain damsel bug adult abundance. A model with both A) the spotted alfalfa aphid and B) the constricted leafhopper was the best-fitting model with prey added. Both damsel bug and prey densities were ln-transformed. Chapter 3 Figure 1. The proportion of prey eaten plotted against prey 51 density for A) Agallia constricta and B) Ceratagallia agricola . The damsel bug displayed a Type I functional response to both species with a near- constant proportion of prey eaten at each density. Figure 2. Calculated preference of the damsel bug to 52 A) A. constricta and B) C. agricola at five densities (n=5). Whiskers represent 25 th and 75 th percentiles, the dark line indicates the median, and the edges of the boxes represent the 10 th and 90 th deciles. iv Figure 3. Survival probability of A. constricta at five 53 densities with one damsel bug present over the course of 5 d. Treatments with a different letter are significantly different from each other (P= 0.05). Figure 4. The effect of habitat complexity and damsel bug 54 density on the predation rate of C. agricola . More leafhoppers were consumed in the single damsel bug, bare ground treatment than in the single damsel bug, clover treatment. Error bars are ±1 SD. Chapter 4 Figure 1. Diagram of experimental unit from two views 72 A) Above and B) Ground level. Each circle or cylinder represents a community connected by tubing to allow dispersal of insects among communities. A pot of red clover was placed in each cylinder. Figure 2. Survival probability of A. constricta in the 73 absence of predation at densities of A) 25 leafhoppers per mesocosm and B) 50 leafhoppers per mesocosm. Figure 3. Survival probability of A. constricta with 74 A) 1 damsel bug per mesocosm and B) 2 damsel bugs per mesocosm. Chapter 5 Figure 1. Arthropod food web in experimental 86 forage-crop ecosystems. Interaction strengths are indicated by the thickness of connecting lines. Box line thickness indicates the importance of the organism in the food web. v ACKNOWLEDGEMENTS I want to thank my advisor Tom Crist for all of his support and guidance over the past six years. I also wish to thank my committee members Ann Rypstra, Bruce Steinly, Hank Stevens, and Mike Vanni for all of their insightful suggestions and support over the course of my dissertation and master’s research. Many thanks go to Ashley Boerger, Stephanie Nguyen, and James Radl for all of their help in the field and laboratory. Thank you to Drs. John Miller and Michael Melampy for all of their inspiration and advice. Finally, a big thanks to my parents, Dennis and Nancy, and to all of my relatives and friends for all of their love and support. I could not have done it without you. vi Chapter 1 Literature Review As natural habitats are altered by human activities, it is increasingly important to determine the impact of these alterations on population, community, and ecosystem processes. As a result of habitat loss, animals must often move among local habitat patches to find food resources (Hanski et al. 1994, Kuussaari et al. 1996), mating opportunities (Kuussaari et al. 1996, Šálek and Marhoul 2008), or over-wintering sites (Thies and Tscharntke 1999, Tscharntke et al. 2002), thus linking population dynamics among patches. There is now a large body of literature documenting how the alteration of patch characteristics affects population dynamics and species abundance. Characteristics such as habitat patch size (Gustafson and Gardner 1996, Moilanen and Hanski 1998), isolation (Moilanen and Hanski 1998), shape (Diamond 1975, Stamps et al. 1987), arrangement (Holyoak 2000), and quality (Kuussaari et al. 1996, Thomas et al. 2001) all affect population dynamics of species in local habitat patches in fragmented landscapes. In addition to patch characteristics, the type of edge habitat surrounding a patch (Stamps et al. 1987, Schtickzelle and Baguette 2003), as well as the intervening matrix habitat (Ricketts 2001, Stasek et al. 2008), influence dispersal rates among suitable habitat patches.