The Role of Learning in the Ecology of Diachasmimorpha Kraussii (Fullaway) (Hymenoptera: Braconidae: Opiinae), and Implications for Tephritid Pest Management
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The role of learning in the ecology of Diachasmimorpha kraussii (Fullaway) (Hymenoptera: Braconidae: Opiinae), and implications for tephritid pest management Aead M Abdelnabi Muhmed Submitted in fulfilment of the requirements for the degree of Doctor of Philosophy 2018 School of Earth, Environmental and Biological Sciences Science and Engineering Faculty Queensland University of Technology Keywords Diachasmimorpha kraussii, parasitoid, fruit-mimicking bag, learning behaviour, Bactrocera tryoni, Tephritidae, wasp, odour, host, biological control, inundative release. i Abstract Many species of braconid wasp (Hymenoptera: Braconidae) are agriculturally important, having been successfully used in biological control. Members of the braconid subfamily Opiinae have particularly been used as agents against tephritid fruit fly pests (Diptera: Tephritidae). The braconid Diachasmimorpha kraussii (Fullaway) is a larval endoparasitoid of at least 18 fruit fly species. This wasp is native to Australia and Papua New Guinea, and has been introduced to many countries worldwide as a fruit fly biological control agent. The ability of adult female D. kraussii to find their host larvae is crucial to their survival and reproduction, and a better understanding of host finding behaviour in this species could improve the effectiveness of wasps released in the field by improved identification of hosts and odour recognition in complex environments. This PhD studies host finding in D. kraussii, with a specific focus on olfaction and the role of experience (= learning). The first research chapter develops rearing methods for the wasp, comparing a novel method designed by me that presents host larvae in hanging bags of artificial diet, with an existing method of presenting larvae and artificial diet in a petri dish, and with whole fruits (nectarines). Wild parasitoids showed poor parasitism rates when using the petri-dish method, and parasitism rates using the ‘bag’ method are equal to those in nectarines. Furthermore, because artificial diet rears more fly larvae per 100 fly eggs than nectarines, the bag method cultures significantly more wasps than whole fruits. This methodology therefore provides a new technique for mass culturing wasps and for carrying out behavioural tests in the laboratory and field. ii The aim of the second research chapter is to improve our understanding of how D. kraussii finds its main host, the Queensland fruit fly (Bactrocera tryoni (Froggatt)), and more explicitly how experience with host-derived olfactory cues may reinforce successful host finding. Y-tube olfactometer studies were used as a behavioural assay to investigate the influence of naïve and experienced female wasps’ orientation to odours of fruits infested with physiologically suitable larval hosts (B. tryoni) compared to fruits infested by non-host larvae (Drosophila melanogaster). The results showed that naïve wasps had significant attraction to odours of uninfested and B. tryoni infested nectarines, with the preference for odours of infested fruits significantly greatly than that for uninfested fruits.Naïve wasps also showed a clear preference toward fruit infested with B. tryoni versus fruit infested with D. melanogaster. There was no significant difference in choices between uninfested fruits and nectarines infested by D. melanogaster. Experience of wasps on B. tryoni infested fruits significantly increased wasp preference for odours of host infested fruits compared to naïve preferences. However, prior wasp experience on non-host (i.e. D. melanogaster) infested fruits did notsignificantly changepreferences for the odours of host and non-host infested fruits compared to naïve wasps. Experience of both host and non-host infested fruits significantly increasedwasppreference for odours of host infested fruits compared to naïve wasps, but no more so than experience on host infested fruits alone. As a continuation of investigating wasp learning, I examined operant learning. In operant learning, an individual learns to carry out a specific behaviour to increase the frequency of an outcome: in my experiments this outcome was the ability of a wasp to successfully locate larvae within a fruit. I trained wasps by iii exposing them to fruits where the position of larvae was always in a predictable location; either at the top or base of the fruit. The exploratory movement and probing rate of experienced wasps was then compared with naïve wasps. The results showed that wasps displayed operant learning to improve searching in order to better locate fly larvae. To my knowledge, this is one of the first times operant learning has been demonstrated in wasps. The final research chapter investigated how learning influences parasitoid behaviour at multiple spatial scales: in laboratory, semi-field and open field conditions. Based on this learning capacity, it has been suggested that providing pre- release training to parasitoids reared for inundative release may lead to a subsequent increase in their efficacy as biological control agents. Using the fruit fly parasitoid Diachasmimorpha kraussii we tested this hypothesis in a series of associative learning experiments which involved the parasitoid, two host fruits (tomatoes and nectarine), and one host fly (Bactrocera tryoni). In sequential Y-tube olfactometer studies, large field-cage studies, and then open field studies, naïve wasps showed a consistent preference for nectarines over tomatoes. In large field-cages, wasps with prior learning on tomato significantly increased orientation to tomato, in comparison to naïve wasps. Prior experience to nectarine did not, however, significantly increase orientation to this fruit in comparison to naïve wasps. In an open orchard, and using my fruit mimicking ‘bags’ modified to provide either nectarine or tomato odours but with the same visual cues, prior experience again significantly increased host location towards tomato, but not towards nectarine. Prior experience did not increase parasitism rates within located bags for either tomato or nectarines. These results demonstrate that learning results developed from laboratory bioassays can be up- iv scaled to the open field environment, something which is very rarely tested in parasitoid learning studies. Results are discussed in the context of the adaptive benefits of learning in the ecology of parasitoid wasps, and the implications of prior experience when releasing wasps as inundative biological control agents. v Table of Contents Keywords ...................................................................................................................... i Abstract ....................................................................................................................... ii Table of Contents ...................................................................................................... vi List of Tables ............................................................................................................... x List of Figures ............................................................................................................ xi Thesis by publication statement .............................................................................. xv List of supplementary material .............................................................................. xvi Statement of Original Authorship ........................................................................ xvii Acknowledgements ................................................................................................ xviii Chapter 1: General Introduction .............................................................................. 1 1.1 General Introduction…………………………………………………………2 1.2 Fruit flies and their biological control with Opiinae…………………….5 1.2.1 The Opiinae ............................................................................................ 6 1.2.2 Fruit fly biological control ........................................................................... 7 1.2.3 Culturing and Mass release of parasitoids for biological control ......... 10 1.3 Parasitoid host selection ............................................................................ 13 1.3.1 Olfaction ............................................................................................... 13 1.3.2 Visual cues ........................................................................................... 17 vi 1.3.3 Adult feeding sites................................................................................ 18 1.4 Learning Behaviour .................................................................................. 18 1.4.1 Associative learning (Classical conditioning) ...................................... 19 1.4.2 Operant learning ................................................................................... 20 1.4.3 Learning in parasitoids ......................................................................... 21 1.4.4 Olfactory learning in parasitoids and its adaptive significance ........... 23 1.4.5 Visual learning ..................................................................................... 26 1.4.6 Learning on multiple host cues and other factors ................................ 27 1.5 Thesis foci organisms: Diachasmimorpha kraussii and Bactrocera tryoni.. .................................................................................................................... 28 1.5.1 D. kraussii life cycle ...........................................................................