Deciphering Multitrophic Interactions for Aphid Control on Okra in Cameroon Akanksha Singh
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WISSENSCHAFTZENTRUM WEIHENSTEPHAN FÜR ERNÄHRUNG, LANDNUTZUNG UND UMWELT LEHRSTUHL FÜR TERRESTRISCHE ÖKOLOGIE Deciphering multitrophic interactions for aphid control on okra in Cameroon Akanksha Singh Vollständiger Abdruck der von der Fakultät Wissenschaftzentrum Weihenstephan für Ernährung, Landnutzung und Umwelt Der Technischen Universität München zur Erlangung des akademischen Grades eines Doktors der Naturwissenschaften genehmigten Dissertation. Vorsitzender: Univ.- Prof. Dr. J. Kollmann Prüfer der Dissertation: 1. Univ.-Prof. Dr. W. W. Weisser 2. Univ.-Prof. Dr. H. Schäfer Die Dissertation wurde am 04.07.2016 bei der Technischen Universität München eingereicht und durch die Fakultät für Wissenschaftzentrum Weihenstephan für Ernährung, Landnutzung und Umwelt am 14.09.2016 angenommen. To my parents Table of Contents Summary .................................................................................................................................... 1 Zusammenfassung...................................................................................................................... 4 Chapter 1: General Introduction ................................................................................................ 7 1.1 Biological control ......................................................................................................... 8 1.2 Integrated pest management (IPM) ............................................................................ 11 1.3 Potential multitrophic interactions in agroecosystems ............................................... 12 1.4 Research objective ...................................................................................................... 21 Chapter 2: Methods .................................................................................................................. 23 2.1 The study system and study species ........................................................................... 23 2.2 Method summary ........................................................................................................ 25 Chapter 3: Manuscript Overview and Author Contribution .................................................... 35 3.1 Manuscript I ................................................................................................................ 36 3.2 Manuscript II .............................................................................................................. 38 3.3 Manuscript III ............................................................................................................. 40 3.4 Manuscript IV ............................................................................................................. 42 Chapter 4: General Discussion................................................................................................. 44 4.1 Enhance natural predators .......................................................................................... 44 4.2 Utilize different plant traits ......................................................................................... 45 4.3 Manipulate plant density ............................................................................................ 46 4.4 Enhance ant abundance .............................................................................................. 47 4.5 Utilize plant defense traits and their variation across varieties .................................. 48 4.6 Higher emphasis on leaf beetle than aphid reduction ................................................. 49 4.7 Future research ........................................................................................................... 50 4.8 Conclusion .................................................................................................................. 51 Acknowledgements .................................................................................................................. 53 References ................................................................................................................................ 55 Appendix A: Manuscripts Included in the Thesis.................................................................... 71 Summary It is well established that intensive agricultural measures such as pesticide application reduce environmental quality and are therefore not sustainable. With crop pests being one of the dominant causes of crop productivity loss, it is crucial to develop environment friendly pest control measures. Numerous interspecific interactions occur in agroecosystems, which in turn can significantly affect pest abundances and plant yield. Understanding multitrophic interactions in agroecosystems may help in development of more resilient pest control measures. Okra is an economically important vegetable in Cameroon, often grown by small- scale farmers in intercropped fields. Many different okra plant varieties are grown in Cameroon. The main pest species of okra include aphids, leaf beetles and whiteflies. Natural predators such as spiders and syrphids larvae are also observed okra. In addition, ants are commonly found attending the cotton aphid on okra for their honeydew and are also observed carrying okra produced pearl bodies back to their nests. Multiple interspecific interactions can occur in such diverse okra-associated invertebrate community. My thesis aims to understand these interactions and their effect on okra yield. During my thesis field and controlled experiments were conducted in Germany and in Cameroon. The first chapter examined the role of additional crops on the okra-associated multitrophic interactions by intercropping okra with bean and maize at different plant densities (high and low). Crop identity and plant density were found to significantly affect okra pests, their predators and okra yield. Leaf beetles were the only pests that affected okra yield and their abundance reduced at high plant density. Overall, okra grown with bean at high plant density was found to be the most productive and profitable combination. Additional crop species did affect the okra-associated invertebrates therefore, to decipher the 1 okra-specific interactions; I focused only on the monocultures of okra in the second chapter. The field experiment showed that ants did not protect aphids in the field and syrphid larvae predators significantly reduced aphid numbers. Moreover, aphids were not found to reduce okra yield. Instead, ant attraction by aphids was beneficial for okra plants as ants reduced chewing herbivore damage. In the controlled experiment Pheidole ants even reduced aphids, but their reduction of aphids varied across different okra varieties; this was potentially mediated by okra pearl bodies. Therefore, these ant-aphid-plant interactions were further explored in the third chapter where I used 4-5 okra varieties and tested: (a) ant preference of okra pearl bodies over aphid honeydew, (b) effect of aphid presence on pearl body production and, (c) effect of pearl body removal on pearl body production. Only ants of genus Pheidole were found to favour okra pearl bodies over aphid honeydew. Additionally, pearl body production was higher, and was not affected by aphids when these were artificially removed. Interestingly, aphids were found to increase plant growth. Further, pearl body production and presence of Pheidole ants also varied across okra varieties. Thus, plant variety did mediate the ant-aphid interactions on okra. Belowground biota may also affect these interactions. To test the effect of plant genetic variation on the aboveground-belowground interactions, a controlled experiment using an earthworm-plant-aphid system was conducted. Effect of belowground earthworms on aboveground black bean aphid was mediated by plant genetic variation. Overall, my thesis provides evidence that species interactions vary with several factors such as plant variety, crop identity, plant density, presence of other species such as ants and belowground organisms. I suggest that farmers practicing intercropping can grow okra-bean at high densities to derive high yield and low pest numbers. Farmers growing okra in monocultures can enhance syrphid larvae abundance. Further, ant presence in okra fields should be enhanced, e.g. by growing varieties with pearl bodies favourable to ants. Finally, 2 more studies are needed to link aboveground-belowground interactions in agriculture as belowground biota can strongly affect plant yield. Understanding multitrophic interactions can help to suggest various pest control measures to farmers and provide vast opportunities to develop more resilient agroecosystems. 3 Zusammenfassung Es ist allgemein bekannt, dass die derzeitigen intensiven landwirtschaftlichen Maßnahmen, wie die Anwendung von Pestiziden, die Umwelt schädigen und somit nicht nachhaltig sind. Da Pflanzenschädlinge eine der Hauptursachen für Einbußen beim Ernteertrags von Nutzpflanzen sind, ist es wichtig, umveltverträgliche Maßnahmen zur Schädlingsbekämpfung zu entwickeln. In Agrarökosystemen existieren zahlreiche interspezifische Interaktionen, die das Vorkommen von Schädlingen und den Pflanzenertrag signifikant beeinflussen können. Ein besseres Verständnis der multitrophischen Interaktionen in agrarökologischen Systemen kann dabei helfen, belastbarere Schädlingsbekämpfungsmaßnahmen zu entwickeln. Okra ist ein wirtschaftlich bedeutendes Gemüse in Kamerun, das oft in Mischkultur von Kleinbauern angebaut wird. In Kamerun gibt es verschiedene Okra-Sorten, welche von