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A Thesis Entitled Influence of Soil-Quality on Coffee-Plant Quality A Thesis entitled Influence of Soil-Quality on Coffee-Plant Quality and a Complex Tropical Insect Food Web by David J. Gonthier Submitted to the Graduate Faculty as partial fulfillment of the requirements for the Master of Science in Biology (Ecology track) Dr. Stacy Philpott, Committee Chair Dr. Scott Heckathorn, Committee Member Dr. Ivette Perfecto, Committee Member Dr. Patricia Komuniecki, Dean College of Graduate Studies The University of Toledo May 2010 Copyright 2010, David J. Gonthier This document is copyrighted material. Under copyright law, no parts of this document may be reproduced without the expressed permission of the author. An Abstract of Influence of Soil-Quality on Coffee-Plant Quality and a Complex Tropical Insect Food Web by David J. Gonthier Submitted to the Graduate Faculty as partial fulfillment of the requirements for the Master of Science in Biology (Ecology track) The University of Toledo May 2010 Tropical systems are complex, species diverse, and are often regulated by top-down forces (higher trophic levels control lower trophic levels). In many ecosystems insects, especially herbivores and their mutualists, may be strongly affected by plant quality and other bottom-up controls (nutrient availability, plant genetic variation, ect.). Yet few have asked how plant quality (nutritional and defensive plant traits) can contribute to the population regulation and the complexity of these systems. In this thesis, I investigate the importance of soil-quality to both the elemental and secondary metabolite content in coffee and ask how changes to plant quality can influence hemipteran herbivores, their ant-mutualists, predators, and insect communities in a tropical coffee agroecosystem. First, I investigated the relationship between nitrogen fertilization and coffee growth, carbon and nitrogen balance, and the production of caffeine, one of coffee’s most abundant secondary metabolites. Second, I determined how elemental nutrients and caffeine content correlated with the distribution of the phloem-feeding herbivore, Coccus viridis, in the proximity of Azteca instabilis ant nests, a keystone mutualist with C. iii viridis. Third, I examined whether changes in soil-quality alter coffee-plant quality (N and caffeine), and how soil-quality and the presence of ant-mutualists regulate population size of C. viridis, the abundance of ant partners, the abundance of natural enemies, and the insect community as a whole. The laboratory experiment suggested N fertilization resulted in greater leaf N and phloem caffeine exudation. However, root, stem, leaf, and total caffeine did not differ with fertilization treatment. In the field, I found a positive association between leaf N and the density of C. viridis. Stepwise multiple regression revealed that A. instabilis ant activity and leaf N explained 45 % in the variation in C. viridis abundance. Caffeine concentration in coffee leaves and phloem exudates had no relationship with C. viridis density. Finally, in the field experiment, high-soil-quality resulted in higher plant growth rate, greater leaf N, and greater phloem caffeine. High- soil-quality plants had 45% greater C. viridis population sizes than plants in the low- quality treatment. Additionally ant-exclusion also increased scale population size by 34% relative to control plants. However, greater C. viridis density did not result in greater recruitment of A. instabilis. Overall, there were 40% more arthropods on high-soil-quality treatment plants relative to low and 20% more arthropods on ant-excluded plants than control. However, this result was driven by changes in the abundance of ants and hemipterans. Additional experimentation revealed Pheidole sp. ants increased recruitment by more than three times to C. viridis on high-soil-quality plants relative to low. Thus, soil-quality, plant growth rate, and percent N appear to be important in the distribution and population size of C. viridis and for recruitment of Pheidole ant-mutualists. However, other factors likely more strongly affect A. instabilis tending of C. viridis. Further, caffeine may not be an important regulator of C. viridis in field settings. Overall, iv soil-quality had important impacts at the community level through changes in abundance of the dominant arthropod group (ant-hemipteran mutualism) on coffee seedlings. This study contributes to the under-represented literature describing the effects of bottom-up forces in tropical systems by 1) showing how host-plant quality can affect the density and growth of a herbivore in coffee agroecosystems and 2) comparing the indirect effect of soil-quality on the recruitment of multiple ant species to hemipteran mutualists. v Acknowledgments Many people played important roles in the production of this thesis. S. Philpott, contributed to all aspects of research. G. Dominguez helped with the majority of field work. J. Witter & A. Spongberg provided equipment and laboratory work for analysis of caffeine. J. Frantz and the USDA provided elemental analysis. C. Murnen, L. Moorhead, G. Pardee, R. Friedrich helped in lab and field work. S. Heckathorn and I. Perfecto contributed greatly to the preparation of this thesis. J. Vandermeer and K. Ennis aided in field work and project design. The Colegio de la Frontera Sur was gracious in allowing the use of their laboratories and A. De la Mora, E. Ruiz Suarez, R. Bello, G. M. Gonzalez, M. Sokolov, and Ibarra‐Núñez aided in logistics, equipment, and storing of samples. The Peter’s family allowed work on their coffee plantation. This research was supported by University of Toledo Travel Grant, Grant in aid of Research- Sigma xi, Grant in aid of research- Society of Integrated and Comparative biology, start up funds to Stacy Philpott, and NSF # DEB-0349388 to I. Perfecto and J. Vandermeer. vi Table of Contents Abstract...............................................................................................................................iii Acknowledgments................................................................................................................v Table of Contents............................................................................................................Vvii List of Tables.......................................................................................................................x List of Figures....................................................................................................................xii 1 Chapter 1: Introduction and background...........................................................1 1.1 Introduction..................................................................................................1 1.2 Study System...............................................................................................5 1.3 Research Objectives.....................................................................................7 2 Chapter 2: Effect of nitrogen availability on plant growth, leaf nutrient concentrations, and the production of caffeine in coffee ...................................9 2.1 Materials & Methods...................................................................................9 2.1.1 Experimental Setup.............................................................................9 2.1.2 Plant Growth Measurements & Water Status...................................10 2.1.3 Plant Caffeine Concentration & Content..........................................11 vii 2.1.4 Plant Nitrogen & Carbon..................................................................12 2.1.5 Statistical Analysis ................…………………...............................13 2.2 Results............................………………………………………................13 2.2.1 Plant growth and water status…………………………………...…13 2.2.2 Leaf carbon & nitrogen balance………………………………...….14 2.2.3 Effect of Nitrogen availability on caffeine production……….……15 2.3 Discussion……………………………………………………….…..…...16 3 Chapter 3: Influence of plant quality on the distribution of a keystone ant- hemipteran mutualism in a coffee agroecosystem……………...….…………25 3.1 Materials & Methods……………………………………..……….……..25 3.2 Results…………..........…………………………………………………..28 3.3 Discussion…………………..……………………………………………29 4 Chapter 4: Impact of soil-quality on plant quality and a coffee insect community….………………………………………………………………...…34 4.1 Material & Methods…………..………………………………………….34 4.1.1 Field methods………………………………………..……………..34 4.1.2 Data Analysis……………………………………………..………..38 4.1.3 Pheidole sp. recruitment to scale insects ………………………….40 4.1.4 Effect of ant-exclusion on Azya orbigera larval foraging...……...…………..…………………………………….....41 4.2 Results……………………………..……………………………………..40 viii 4.2.1 Effect of soil-quality treatment on scales, aphids, and ant- mutualist……………………………...…………………………..40 4.2.2 Effect of soil and ant treatments on C. viridis predators, parasitoids, and pathogens.…….…………………………………….....……..41 4.2.3 Insect community……………….…………………………...……..42 4.2.4 Plant growth and quality……………………..…………………….42 4.2.5 Plant and food web variables correlated with green scales….……..43 4.2.6 Effect of soil-quality on Pheidole sp. recruitment to C. viridis……44 4.2.7 Effect of ant-exclusion on Azya orbigera larval foraging……...….44 4.3 Discussion..….………………………………….………………………..45 4.3.1 Effect of treatments on green scale growth………………………..45 4.3.2 Effect of treatments on ant attendance of green scales…………….47 4.3.3 Effect of treatments on predators, parasitoids, and pathogens……..48 4.3.4 Community level effects of treatments……………………...……..49
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