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Interrelationships Between Diglyphus Isaea, Phaedrotoma Scabriventris and Endophytic Fungi in the Control of Liriomyza Leafminers

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Interrelationships Between Diglyphus Isaea, Phaedrotoma Scabriventris and Endophytic Fungi in the Control of Liriomyza Leafminers Interrelationships between Diglyphus isaea, Phaedrotoma scabriventris and endophytic fungi in the control of Liriomyza leafminers KS Akutse 23389796 Thesis submitted for the degree Doctor of Philosophy in Environmental Sciences at the Potchefstroom Campus of the North-West University Promoter: Prof J van den Berg Co-Promoter: Dr JNK Maniania Assistant-Promoters: Dr S Ekesi Dr KKM Fiaboe September 2013 Interrelationships between Diglyphus isaea, Phaedrotoma scarbiventris and endophytic fungi in the control of Liriomyza leafminers KOMIVI SENYO AKUTSE Thesis submitted in fulfilment of the requirements for the award of the degree Doctor of Environmental Sciences at the North-West University (Potchefstroom Campus) Supervisor: Prof. J. Van den Berg Co-supervisors: Dr. N. K. Maniania Dr. S. Ekesi Dr. K. K. M. Fiaboe April 2013 NORTH-WEST UNIVERSITY, SOUTH AFRICA DEDICATION To my beloved parents Komi Venyo Akutse and Aku Agnes Agbeke-Akutse for their constant sacrifices and supports To my beloved wife Ama E. Genevieve Amenya-Akutse and our dear daughter Esther Sitsofe A. Akutse for their encouragements and love To the Late Dr. A. Chabi-Olaye for conceptualizing this research topic and for his various advice, assistance and supports. This is a fruit of your dreams on this project of tackling Liriomyza leafminers i ii ACKNOWLEDGEMENTS My special thanks to Prof. Johnnie van den Berg my supervisor for his keen interest in both my academic and professional welfare. You built up a special relationship of friendship and professionalism that strengthened me from the beginning to the end of the present study. I sincerely appreciate the nice combination of celebrity, simplicity and humility I discovered during this time I interacted with you. I am deeply indebted to you for your diligent guidance, corrections, motivations and supports in diverse ways for the accomplishment of this research. I also wish to express special thanks to Dr. Nguya Kalemba Maniania for all his scientific endeaviour he built in me. I am very gratefull for all his supports and his simplicity and humility combine with all his celebrity. Although you were busy for the first time of my arrival at icipe and I was dopting to have you as supervisor, you gave me more assurance and strength to work hard and fullfil my objective. You have never stopped to assist me and accepted to supervise me at all cost. I am very grateful. My special thanks to Dr. Komi Kouma Mokpokpo, who came at last to fill the gap Dr. Chabi-Olaye left behind. I really appreciate the fastest way you catch everything up with me at all levels. I am very grateful for all your assistance and your keen interest in both my academic and extra-academic welfare. You built up a special relationship of friendship and professionalism that strengthened me from the beginning to the end of the present study. My sincere appreciation and thanks also go to Dr. Sunday Ekesi for his quick reaction to lift my spirits at the critical moment when we lost the Late Dr. Chabi-Olaye. Your intervention had given me a lot of confidence and strength to work hard and accomplish the dream of Dr. Chabi-Olaye on this scientific work. I am very gratefull also that you have accepted to be my supervisor and assist me to achieve this degree despite your busy schedule. My special thanks to Dr. Daisy Salifu and Mr. Benedict Orindi for all your advice and guidance on statistical data analysis, for which I am grateful. Further gratitude goes to Dr. Sevgan Subramanian for his advice during the preparation of this research proposal. iii I am very gratefull to Ms. Ouna Elizabeth, Mr. Wafula SosPeter, Mr. Shem Odianka, Mrs Faith Nyamu and all the rest of technicians at the Leafminer Project and Arthropod Pathology Unit for all their assistance, collaboration, support and advice. I also wish to thank Capacity Bulding, especially Mrs. Lillian Igweta for all her various assistance and supports. I am very grateful. I am very grateful to International Centre of Insect Physiology and Ecology (icipe) who gave me this doctoral study opportunity on behalf of the African Regional Postgraduate Programme in Insect Science (ARPPIS) network partners, funded by the German Academic Exchange / Deutcher Akademischer Austausch Dienst (DAAD) in Germany. I thank all my colleagues who in divert ways encouraged me during this study, especially Caroline Foba Ngichop, Venansio Tumuhaise, Dr. Lorna Migiro, Ayuka Fabon, David Pumo, Siti Bendera, Dr. Paulin, and Olivia Lwande. My special thanks to Dr. Max Badziklou, Mr. Komi Melesusu, Mr. Kokou Melesusu and Dr. Anani Bruce for their various assistances and supports. My profound gratitude goes to my sister, brother and parents back home. I remain eternally grateful to the Lord God Almighty for the gift of life, and the privilege to attain this level of academic achievement. iv ABSTRACT Horticulture is a major foreign exchange earner in Kenya and provides employment to approximately 75% of the population. However, the growth of the horticultural industry is constrained by pests such as the leafminer flies, Liriomyza sativae, L. trifolii and L. huidobrensis (Diptera: Agromyzidae). These pests do not only cause damage to crops, but are also tagged as quarantine pests, resulting in export rejections, loss of export markets and consequently loss of revenue to smallholders. The management of leafminers worldwide has commonly relied on the use of chemical insecticides, but due to associated negative effects thereof, biological control using parasitoids and entomopathogenic fungi has been proposed as major components of integrated pest management (IPM) strategies. The indigenous ectoparasitoid Diglyphus isaea and exotic endoparasitoid Phaedrotoma scabriventris are the two key natural enemies being considered. A number of endophytic fungal isolates have been identified with potential for use as biological control agents of pests. Although there have been previous reports on toxicity of fungal endophytes to leafminers, no attempts have been made to exploit them for control of Liriomyza leafminers. The objectives of this study were to investigate the mechanisms by which fungal endophytes control Liriomyza spp., as well as the interactions between these endophytic fungi and the L. huidobrensis, endoparasitoid Phaedrotoma scabriventris and ectoparasitoid Diglyphus isaea. This study showed that under laboratory conditions, while used separately, parasitism rates of L. huidobrensis by D. isaea and P. scabriventris were 63.6 ± 7.7% and 30.4 ± 10.9% respectively and increased to 77.0 ± 5.3% when used simultaneously. In addition, both parasitoids induced leafminer mortality through larval-feeding and stinging. In order to identify and characterize endophytic fungi that could possibly be used for control of these pests, fungi were isolated from the aboveground parts of maize, sorghum, Napier grass, Coleopteran larvae and Busseola fusca pupae. Identified fungi were evaluated endophytically in two host plants species (Phaseolus vulgaris and Vicia faba) through seed inoculation. The fungal isolates that succeeded in colonizing the host plants were all pathogenic to L. huidobrensis, causing 100% mortality within 13.2 ± 0.7-15.0 ± 0.6 days. They were also able to reduce the longevity of the progeny, the number of pupae and adult emergence and survival. In addition, results also showed that endophytically- v inoculated and L. huidobrensis-infested V. faba plants had no adverse effects on parasitism rates and life history parameters of P. scabriventris and D. isaea. Bio- prospecting for fungal endophytes in P. vulgaris and V. faba seeds, followed by morphological and molecular identification revealed the presence of various species of fungal entomopathogens, including Beauveria bassiana, Epacris microphylla, Phanerochaete chrysosporium and Metarhizium anisopliae. Key words: Biological control, entomopathogens, endophytes, horticulture, leafminers, Liriomyza sp., parasitoids, Phaedrotoma scabriventris, Diglyphus isaea vi UITTREKSEL Tuinbou is „n belangrike verdiener van buitelandse valuta in Kenia en verskaf werk aan ongeveer 75% van die bevolking. Ontwikkeling van die tuinbou-industrie word egter beperk deur insekplae soos die bladmynervlieë Liriomyza sativae, L. trifolii en L. huidobrensis (Diptera: Agromyzidae). Hierdie plae beskadig nie alleen gewasse nie maar is ook geïdentifiseer as kwarantynplae, wat gevolglik lei tot afkeur van uitvoerprodukte, verlies aan uitvoermarkte en gevolglike verlies aan inkomste vir kleinboere. Die bestuur van bladmyners wêreldwyd het grootliks berus op die gebruik van chemiese insekdoders maar as gevolg van die geassosieerde negatiewe effekte daarvan word biologiese beheer deur die gebruik van parasitoïede en entomopatogeniese fungi voorgestel as belangrike komponente van geïntegreerde plaagbestuursprogramme. Die inheemse ektoparasiet, Diglyphus isaea en uitheemse endoparasiet, Phaedrotoma scabriventris is die twee natuurlike vyandspesies wat hiervoor oorweeg word. „n Aantal endofitiese fungi-isolate met potensiaal vir gebruik as biologiese beheeragente is geïdentifiseer. Alhoewel daar voorheen toksisiteit van fungus-endofiete op bladmyners waargeneem is, is nog geen pogings aangewend om hierdie organismes vir die beheer van Liriomyza-bladmyners aan te wend nie. Die doelstellings van hierdie studie was om ondersoek in te stel na die volgende: die meganismes waardeur fungus-endofiete Liriomyza spp. beheer, die interaksies tussen hierdie endofiete en L. huidobrensis, die endoparasitoïed Phaedrotoma scabriventris en
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