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INFOILVJ:Atlon to USERS a Note Will Indicate INFOILVJ:aTlON TO USERS This manuscriptPas been reproduced from the microfilm master. UMI films the text directly from the original or copy submitted Thus, some thesis and dissenation' copies are in typewriter face, while others may be from any type ofcomputer printer. The quality of this reproductioD is depeDdent DpOD the quality of the copy submitted. Broken or indistinct print, colored or poor quality illustrations and photographs, print bleedthrough, substandard margins, and improperalignment can adversely affect reproduction. In the unlikely. event that the author did not send UMI a complete mam1script and there are missing pages, these will be noted. Also, if unauthoriZed copyright material had to be removed, a note will indicate the deletion. Oversize materials (e.g., maps, drawings, charts) are reproduced by sectioning the original, beginning at the upper left-hand comer and continuing from left to right inequal sections with small overlaps. Each original is also photographed in one exposure and is included in reduced form at the back ofthe book. Photographs included in the origiDal mam1script have been reproduced xerographically in this copy. Higher quality 6" x 9" black and white photographic prints are available for any photographs or illustrations appearing in this copy for an additional charge. Contact UMI directly to order. UMI A Bell & Howell Information Company 300 North Zeeb Road. Ann Arbor. MI48106-1346 USA 3131761-4700 800:521-0600 THE STATUS OF THE BIOLOGICAL CONTROL OF PINEAPPLE MEALYBUGS IN HAWAD A DISSERTATION SUBMITTED TO THE GRADUATE DIVISION OF THE UNIVERSITY OF HAWAII IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY IN ENTOMOLOGY DECEMBER 1995 By Hector Gonzalez-Hernandez Dissertation Committee: Marshall W. Johnson, Chairperson Neil 1. Reimer Diane E. Ullman John W. Beardsley Kenneth G. Rohrbach OMI Number: 9615523 UMI Microform 9615523 Copyright 1996, by UMI Company. All rights reserved. This microform edition is protected against unauthorized copying under Title 17, United States Code. UMI 300 North Zeeb Road Ann Arbor, MI 48103 © Copyright 1995 by Hector Gonzalez-Hernandez III DEDICATION Dedicated to my wife Pili and my daughter Mariana whose love and dedication have enriched every day ofmy live. IV ACKNOWLEDGMENTS Special thanks to my major professor, Dr. Marshall W. Johnson, whose encouragement, teaching, valuable advisory work, and friendship made it possible to successfully finish this enterprise. Also to my advisor Dr. Neil 1. Reimer, for his effort, and time spent teaching me to work with ants, and for his friendship. I would like to thank my other committee members, Dr. John W. Beardsley, Dr. Diane E. Ullman, and Dr. Kenneth G. Rohrbach for all their suggestions and support to conduct this work. Thanks to Dr. Bruce E. Tabashnik for his suggestions through my experiments. I am pleased to thank the Consejo Nacional de Ciencia y Tecnologia (National Council ofScience and Technology) and Colegio de Postgraduados ofthe Mexican government; Hawaii Governor's Agricultural Coordinating Committee and the Hawaii Sugar Planters Association for providing financial support to conduct this Ph. D. program. Many thanks to Calvin H. Oda, Vaeleti Tyrell, and Francisco Bareng from Del Monte Fresh Produce (Hawaii) Inc., and Dr. Herbert Fleisch from the Maui Land and Pineapple Co., for providing pineapple fields and technical support for my field experiments. Thanks to Claide Ragasa and Pamela Fukada for their technical support. I am grateful to all the Faculty, Staffand graduate students ofthe Department ofEntomology for their valuable help during my program. Special thanks to Mildred E. Uegawachi, Lynn H. Hata and Jamie L Wong, secretaries ofthe Department of Entomology for their hard work that was an essential part ofmy project. My gratitude goes to my parents Vicente Gonzalez Vaquera and Antelia Hernandez de Gonzalez, and my brothers, especially Alejandro Gonzalez Hernandez who always encouraged me to continue working for a higher education. v ABSTRACT The pink pineapple mealybug, Dysmicoccus brevipes (Cockerell), and the gray pineapple mealybug, D. neobrevipes Beardsley, (Homoptera: Pseudococcidae) are associated with the disorder mealybug wilt ofpineapple (MWP). High mealybug densities promote the occurrence ofMWP, an important disease limiting pineapple production. In the absence ofants, such as the big-headed ant, Pheidole megacephala (Fabricius), mealybug densities are usually low. However, in the presence ofants, mealybug densities on pineapple may reach damaging levels, and ultimately result in the occurrence ofMWP. Several theories have been proposed to explain the relationships among the mealybugs and the ants. Studies were undertaken to better define the role ofestablished biological control agents in suppressing mealybug populations in Hawaii. In surveys in abandoned pineapple fields on the Hawaiian islands ofOahu and Maui from July 1992 to November 1993, mealybug densities ranged from a mean of22 to 157 mealybugs per plant. P. megacephala was the dominant ant species found. Five natural enemy species, previously introduced into Hawaii for mealybug control, were associated with D. brevipes and D. neobrevipes. Anagynls ananatis Gahan (Hymenoptera: Encyrtidae) was the most common parasitoid associated with D. brevipes. The only predators that appeared to have any potential were Nephus bilucernarius Mulsant (Coleoptera: Coccinellidae) and Lobodiplosispseudococci (Felt.) (Diptera: Cecidomyiidae). Field evaluation studies using the biological check method suggested that A. ananatis was predominantly responsible for the decline ofD. brevipes densities in the VI absence ofants. A study combining the biological check method and the paired-cage exclusion technique indicated that in the absence ofP. megacephala, D. brevipes densities were heavily impacted by natural enemies and probably the lack ofsanitation (e.g., honeydew removal). Laboratory studies indicated that P. megacephala significantly decreased mealybug parasitization and predation by adult A. ananatis and N. bilucernarius by 73 and 48 percent, respectively. Biological studies were conducted on A. ananatis and N. bilucemarius to define and quantify biological characteristics such as mealybug host and stage preference, developmental times, longevity and fecundity. Additionally, the functional response ofA. ananatis was determined when using D. brevipes as a host species. VII TABLE OF CONTENTS Page Acknowledgments v Abstract vi List ofTables xiii List ofFigures xv I. INTRODUCTION 1 II. LITERATURE REVIEW 3 Worldwide Pest Status ofMealybugs 3 Mealybugs Infesting Pineapples and Other Crops 4 Nature ofMealybug Damage to Pineapple 5 Direct Damage 5 Indirect Damage...................................................................... 6 Factors Impacting Mealybug Population Ecology 7 Host Plants in Hawaii 7 Honeydew Accumulation 8 Association with Various Ant Species 8 Role ofAnts in Survival ofPM 9 Natural Enemies 10 Current Understanding ofMealybug Wilt ofPineapple Disease 10 Causes ofMealybug Wilt ofPineapple 10 Distribution ofMealybug Wilt ofPineapple 10 VlIl Management ofDysmicoccils Species 14 Management Options and Constraints 15 Chemical Control 15 Physical and Cultural Control 16 Host Plant Resistance 17 Biological Control 17 Interactions ofAnts and Biological Control Agents 19 Control ofAnts to Conserve Natural Enemies 22 Conclusions and Recommendations 23 References Cited 25 III. SURVEY OF THE NATURAL ENEMIES OF THE PINEAPPLE l\1EALYBUGS 36 Introduction 36 Materials and Methods 37 Results 41 Parasitoids 41 Predators 45 Discussion 49 References Cited 53 IV. IMPACT OF PHEIDOLEMEGACEPHALA (F.) (HYMENOPTERA: FORMICIDAE) ON THE CONTROL OF DYSMICOCCUS BREVIPES (COCKERELL) (HOMOPTERA: PSEUDOCOCCIDAE) .. 58 ix Introduction 58 Materials and Methods 60 Biological Check Method 60 Combined Biological Check and Exclusion Method 62 Impact ofP. megacephala on Mealybug Natural Enemies 64 Nephus billicernarius 64 Anagynls ananatis 68 Results 68 Biological Check Method 68 Combined Biological Check and Exclusion Method 75 Impact ofP. megacephala on Mealybug Natural Enemies 79 Nephus billicernarius 79 Anagyrus ananatis 79 Discussion 80 References Cited 85 V. HOST PREFERENCE, REPRODUCTION, AND FUNCTIONAL RESPONSE OF ANANGYRUS ANANATIS GAHAN (HYMENOPTERA: ENCYRTIDAE), A PARASITOID OF DYSMICOCCUS BREVIPES (COCKERELL) (HOMOPTERA: PSEUDOCOCCIDAE) 89 Introduction 89 Materials and Methods 91 Host Species Preference 92 x Host Stage Preference 93 Reproduction, Longevity, and Sex Ratio 93 Functional Response ofAnagynls ananatis 94 Results 95 Host Species Preference 95 Host Stage Preference 95 Reproduction, Longevity, and Sex Ratio 98 Functional Response ofAnagynls anana/is . 98 Discussion 102 References Cited 106 VI. PREY PREFERENCE, AND FECUNDITY OF NEPHUS BILUCERNARIUS (COLEOPTERA: COCCINELLIDAE), A PREDATOR OF DYSMICOCCUS BREVIPES (COCKERELL) 110 Introduction 110 Materials and ~.1ethods III Prey Species Preference 112 Prey Stage Preference 112 Fecundity ofN. bilucemarius 113 Results 114 Prey Species Preference 114 Prey Stage Preference 114 Fecundity ofN. bilucemarius 114 Xl Discussion 116 References Cited 120 VII. CONCLUSIONS 123 Xli LIST OF TABLES Table Page 2.1. Predators introduced into Hawaii from 1894 to 1936 for controlling pineapple mealybugs 11 2.2. Parasitoids introduced into Hawaii from 1894 to 1936 for controlling pineapple mealybugs in the genus Dysmicoccus spp. 13 3. 1. Locations and dates (1992-1993) that Anagyros
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