DISTRIBUTION AND FORAGING BY THE LEAF-CUTTING ANT, Atta cephalotes L., IN COFFEE PLANTATIONS WITH DIFFERENT TYPES OF MANAGEMENT AND LANDSCAPE CONTEXTS, AND ALTERNATIVES TO INSECTICIDES FOR ITS CONTROL A Dissertation Presented in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy with a Major in Entomology in the College of Graduate Studies University of Idaho and with an Emphasis in Tropical Agriculture In the Graduate School Centro Agronómico Tropical de Investigación y Enseñanza by Edgar Herney Varón Devia June 2006 Major Professor: Sanford D. Eigenbrode, Ph.D. iii ABSTRACT Atta cephalotes L., the predominant leaf-cutting ant species found in coffee farms in the Turrialba region of Costa Rica, is considered a pest of the crop because it removes coffee foliage. I applied agroecosystem and landscape level perspectives to study A. cephalotes foraging, colony distribution and dynamics in coffee agroecosystems in the Turrialba region. I also conducted field assays to assess effects of control methods on colonies of different sizes and to examine the efficacy of alternatives to insecticides. Colony density (number of colonies/ha) and foraging of A. cephalotes were studied in different coffee agroecosystems, ranging from monoculture to highly diversified systems, and with either conventional or organic inputs. A. cephalotes colony density was higher in monocultures compared to more diversified coffee systems. The percentage of shade within the farm was directly related to A. cephalotes colony density. The proportion of coffee plant tissue being collected by A. cephalotes was highest in monocultures and lowest in farms with complex shade (more than three shade tree species present). Number of colonies and total surface area of colonies were greater near the edges of coffee farms than closer to the interior (>30 m from edge). This effect was significantly stronger for edges adjacent to riparian forest strips than other edge types. There was only limited evidence of the influence of landscape features at greater distances from farms (up to 2000 m) on within-farm colony densities. Sulfluramid and sodium octoborate caused the greatest mortality among 9 treatments tested in bait formulations on A. cephalotes colony activity and mortality. One of the alternative baits tested (active ingredient, propagules of Paecilomyces sp. 0484) caused significant reduction in colony activity (worker movements into and out of nest openings), but failed to cause significant colony mortality. Effects of treatments on colony activity were stronger on large (>30 m2 of nest surface area) than on medium (1.1-30 m2) and small colonies 0.03-1 m2. Coffee farmers would benefit from reduced attack by A. cephalotes by increasing the amount of shade, planting shade species palatable to A. cephalotes but economically unimportant or capable of withstanding ant attacks. iv VITA Edgar Herney Varón Devia was born in Cajamarca (Colombia) in 1973. In 1990, he began studying Agronomy at the Universidad del Tolima in Ibagué (Colombia), receiving the Agronomist Engineer degree in 1995. In 1996, he worked developing research projects in the Amazonian region of Colombia within the Corporación Colombiana de Investigación Agropecuaria (CORPOICA) Regional 10, including agroforestry projects with small farmers that included the management of soil improving systems with legumes, planning and establishment of polycultures with fruit and wood trees, management and conservation of germplasm of promissory species, germplasm breeding of Amazonian fruit trees and the processing of products derived from Amazonian fruit-tree species. In 2001 he got involved in M.Sc. study at CATIE in Ecological Agriculture with an emphasis on Integrated Pest Management and a subspecialization in Tropical Agroforestry. His thesis dealed with the potential of ants as biological control agents of the coffee-berry borer and the mahogany shoot borer. In 2003, he started a Ph.D. study in Entomology within a Joint Program between the University of Idaho and CATIE. The current dissertation analyzed on-farm and landscape variables influencing harvest, distribution and density of Atta cephalotes, a polyphagous herbivore ant present in coffee plantations of Costa Rica, as a way to improve control strategies for this pest. v ACKNOWLEDGMENTS I want to acknowledge my advisor Sanford D. Eigenbrode, who always had faith in my abilities and dedication, even before I began my dissertation research. I am also grateful to Luko Hilje, my dear M.Sc. advisor, who was essential to making this dissertation research possible. I thank the rest of the members of my Graduate Committee (Nilsa Bosque-Pérez, Jeffrey Jones and Penny Morgan), who supported my proposal and gave me their support and advice when needed. Many persons in the CATIE staff helped me in at different stages of my dissertation. The members of the UI-NSF-IGERT Turrialba team gave me the chance to share and learn with them from this experience. I am grateful to all the people that made my life easier out of my country. I also thank the institutions that gave me financial support for this research: The Idaho Agricultural Experiment Station, the USDA (USDA / FAS / ICD / RSED Working Capital Fund at CATIE), and the NSF-IGERT Project at the University of Idaho. Finally, a special thanks to all the coffee farmers who allowed us to work on their farms, never expecting a reward, but hoping for a better future for their families. I hope that my work will help them in some way. vi DEDICATION To God, who gave me the wisdom of taking advantage of the unique opportunity of pursuing a Ph.D. To my eternal love, my wife, Amparo, who enjoyed and suffered with me through this academic process. To my daughter, Jessica, who has grown up in Costa Rica and will always remember and miss this beautiful country. To my parents, who have missed us for almost six years. To my brother and my sister, who always supported my decision to specialize professionally. To my friends, who made my life easier and shared the difficulties. vii TABLE OF CONTENTS Page TITLE PAGE…………………………………………………………………………….… i AUTHORIZATION TO SUMBIT DISSERTATION……..……………………….……... ii ABSTRACT………………………………………………………………………....….….. iii VITA………………………………………………………………………………….....….. iv ACKNOWLEDGMENTS…………………………………………………………….……. v DEDICATION………………………………………………………………………….…... vi TABLE OF CONTENTS…………………………………………………………….……. vii LIST OF TABLES……………………………………………………………………..…... x LIST OF FIGURES…………………………………………………………………….…. xiii CHAPTER 1: INTRODUCTORY CHAPTER ……………………………………….…. 1 Importance of coffee in Costa Rica……………………………………………….… 1 Structural types of coffee plantations…………………………………………….…. 1 Biology of leaf-cutting ants…………………………………………………………... 2 Leaf-cutting ants as agricultural pests…………………………………………….… 2 Biological control of leaf-cutting ants…………………………………………….….. 3 Action thresholds and improved methods for managing leaf-cutting ants…….… 4 A landscape perspective to deal with leaf-cutting ants………………………….… 5 Organic coffee production and leaf-cutting ants………………………………….... 6 Proposed work: improved methods for control of leaf-cutting ants in coffee…… 7 References…………………………………………………………………………….. 9 CHAPTER 2: Effect of farm diversity on harvesting of coffee by the leaf-cutting ant Atta cephalotes……………………………………………………………………………. 17 Abstract……………………………………………………………………………….... 17 Introduction………………………………………………………………………….…. 18 Methods………………………………………………………………………………... 19 Results……………………………………………………………………………..…… 22 Discussion………………………………………………………………………….….. 23 Acknowledgments…………………………………………………………………….. 27 References…………………………………………………………………………..… 28 viii Page CHAPTER 3: Effect of coffee farm diversity and landscape on density of colonies of the leaf-cutting ant Atta cephalotes……………………………………………...…... 44 Abstract……………………………………………………………………………….... 44 Introduction………………………………………………………………………….…. 45 Methods ……………………………………………………………………………….. 47 Results………………………………………………………………………………..… 49 Discussion……………………………………………..…………………………….… 50 Acknowledgments………………………………………………………………….…. 53 References…………………………………………………………………………….. 54 CHAPTER 4: Effect of riparian forest edges on the distribution, abundance and survival of Atta cephalotes colonies in coffee farms in the Turrialba region, Costa Rica…….................................................................................................................... 71 Abstract……………………………………………………………………………….... 71 Introduction………………………………………………………………………….…. 72 Materials and methods…………………………………………………………….…. 73 Results………………………………………………………………………………..… 75 Discussion……………………………………………………………………….…….. 76 Conclusions……………………………………………………………………….…… 77 Acknowledgments…………………………………………………………………….. 79 References…………………………………………………………………………….. 80 CHAPTER 5: Effect of baits based on fungal strains or botanical extracts on Atta cephalotes colonies…………………………………………………………………….… 91 Abstract……………………………………………………………………………….... 91 Introduction………………………………………………………………………….…. 91 Materials and Methods………………………………………………………….……. 93 Results……………………………………………………………………………….…. 97 Discussion…………………………………………………………………..…….…… 98 Acknowledgments………………………………………………………………….…. 101 References………………………………………………………………………….…. 102 CHAPTER 6: CONCLUDING CHAPTER…………………………………………….… 114 Introduction………………………………………………………………………….…. 114 ix Page Objectives and Principal Findings……………………………………..…….. 115 Recommendatios to farmers………………………………………………..……… 120 Indicated additional research to improve A. cephalotes management and understand its ecology in working landscapes................................................... 121 References………………………………………………………………………….... 122 APPENDICES 125 Appendix 1. Plant species harvested by A. cephalotes colonies in coffee farms in Turrialba region, Costa Rica. 2004………………………………………………….….. 126 Appendix 2. Distribution of research farms in the proposed biological corridor Turriallba-Jimenez. 2005……………………………………………………………….… 127 Appendix 3. A. cephalotes colony distribution at El Sauce coffee farm. Turrialba region, Costa Rica. 2003.…………………………………………………………….….. 128 Appendix 4. Plot arrangement at coffee farms riparian and non-riparian forest edges. 2004-2005………………………………………………………………………... 129 Appendix 5. Main results of surveys of coffee farmers about Atta cephalotes control in the Turrialba region during different stages of the research. 2004- 2005………………………………………………………………………………………… 130 x LIST OF TABLES Page Table 2.1. Characteristics of the coffee management types studied in the Turrialba region, Costa Rica, 2004……………………………………………….…….. 32 Table 2.2. ANOVA results for the effect of coffee management type on the rate of harvest (g/colony/h) of different classes of plant material by A. cephalotes, Turrialba region, Costa Rica, 2004………………………………………………….….. 33 Table 2.3. ANOVA results for the effect of coffee management type on the percentage of biomass harvested by A. cephalotes for different classes of plant material, Turrialba region, Costa Rica, 2004………………………………………...… 34 Table 2.4. Plant species harvested by A. cephalotes in different coffee management types. Turrialba region, Costa Rica, 2004……………………….…….. 35 Table 2.5. Jaccard similarity indices for plant species collected by A. cephalotes among coffee management types differing in diversity and management. Turrialba region, Costa Rica, 2004………………………………………………………….……... 36 Table 2.6. Jaccard similarity indices for plant species among coffee management types differing in diversity and management based on LAI measurements. Turrialba region, Costa Rica, 2004……………………………………………….…….. 37 Table 2.7. Availability vs. harvest values for the main plant species taken by A. cephalotes in the different coffee management types. Turrialba region, Costa Rica, 2004…………………………………………………………………………………. 38 Table 3.1. Characteristics of coffee management types compared for density of A. cephalotes colonies. Turrialba region, Costa Rica, 2005……………………..…….... 58