Parasitoids as biological control agents of thrips pests

Keywords: Thysanoptera, Frankliniella occidentalis, Hymenoptera, Ceranisus menes, Ceranisus americensis, biological controlThe thesis presented here is the result of a joint European Research project "Biological Control of Thrips Pests". Specific aims of the project were to collect, evaluate, mass produce and commercially apply natural enemies of thrips species. To evaluate natural enemies we applied specified selection criteria, which had proven its value in previous pre-introduction selection of natural enemies of several other greenhouse pests. In my part of the evaluation programme, I studied what prospects hymenopterous parasitoids might have as biological control agents of thrips, in particular the western flower thrips, Frankliniella occidentalis (Pergande).First ( Chapter 1 ) I summarised available information on the thrips pests which currently play a key role in protected cultivation in Europe. In particular I looked into F. occidentalis, Thrips tabaci Lindeman and two other species that I studied: Frankliniella schultzei Trybom and Frankliniella intonsa (Trybom) and reviewed their geographical distribution, economic impact, followed by additional information on thrips biology, ecology and ways of control. Then the state of the art is discussed of the most important groups of natural enemies that are currently evaluated and/or applied as biological control agents: predatory mites, pirate bugs, entomopathogenic fungi and entomophilic nematodes. Specific emphasis is put on the current status of hymenopterous parasitoids attacking thrips, their biology, ecology and life-history and the prospects they might have for thrips control in European greenhouses. Finally, I present the aim of my research project and the outline of this thesis.When the research project started, no parasitoid of western flower thrips was known. In our search for parasitoid candidates, presented in Chapter 2 , a sampling programme was developed, surveying F. occidentalis populations in its original area of distribution (USA) and newly invaded areas (South of Europe). Parasitoids of closely related thrips species, distributed worldwide, preferably from areas with climatically conditions similar to northwest European glasshouses were collected as well . Based on the host and geographic distribution records in the literature, mainly species were collected within the genus Ceranisus (Walker), solitary larval endoparasitoids of thrips species closely related to F. occidentalis. Our collection efforts resulted in a number of parasitoid species and various geographical strains, the most important being Ceranisus menes (Walker) and Ceranisus americensis (Girault) (Hymenoptera: Eulophidae). Both are solitary koinobiont endoparasitoids of thrips larvae that reproduce asexually.A critical phase in any evaluation programme, is the development of an adequate and reliable rearing procedure, allowing a standardised supply of insects of a constant quality and large enough quantities. For laboratory bioassays on thrips and parasitoids, and eventually mass-production, it is essential that large cohorts of even aged groups of larvae are available. In Chapter 3 we describe and evaluate laboratory methods for rearing various species of thrips, such as Frankliniella occidentalis , F. intonsa, Thrips palmi (Karny) and Thrips tabaci Lind. (Thysanoptera: Thripidae) and their parasitoids. When using a method based on honey-solution and pine pollen, large numbers could be produced of high quality, with relatively little time investment. For rearing parasitoids the method proved adequate as well, but less efficient in yield and time.A number of basic evaluation criteria for pre-introduction selection of useful natural enemies, is based on the outcome of behavioural and developmental interactions with their target host in laboratory experiments. Specific aspects of the parasitoid's host selection process are evaluated in Chapter 4 (host age selection) and chapter 5 (host species selection). Results presented in Chapter 4 show that host acceptance by C. menes and C. americensis was negatively correlated with size, age and stage of the larval host. Observations on the parasitoid's behaviour showed that the extent to which a wasp could complete and attack and oviposit significantly decreased with increasing size (age) of host larvae. The apparent preference for small sizes of larvae is largely caused by defensive reactions (walking away, wagging the abdomen, anal exudate production) upon an encounter to vehement resistance (wriggling, dragging) of the larvae when attacked and stung. In larvae smaller or equal to her own size, a wasp could manage its victim, whereas larvae larger than herself managed to escape prior or during an attack. The apparent preference for small and young host larvae is valuable for developing a mass-production system for thrips parasitoids, for the timing of releases in the greenhouse and, because only a small part of the population is prone to attack, has consequences for the population dynamics of the host and the parasitoid.Although in a greenhouse grown crop F. occidentalis often is the major, but not the only thrips species around it is important to know the host preference of the parasitoids with respect to different species. No-choice tests, presented in Chapter 5 show that differences in the behaviour and biology of both the host and the parasitoid species strongly influenced their development and fitness. On the species level as well as on the population level parasitoids differed in host acceptance behaviour, parasitoid developmental time and size of their offspring. C. americensis preformed best on its original co-evolved host F. occidentalis . C. menes consists of a large complex of regional populations, that either reproduce sexually or asexually. They differ morphologically, geographically, behaviourally and physiologically in their response to different geographical populations of thrips species, each of them having its unique characteristics.Life-history studies performed on C. menes and C. americensis in the laboratory ( Chapter 6 ) shows that developmental and reproductive biology were significantly affected by temperature and characteristic for each species / strain. It was found that immature developmental time took much longer when temperature decreased, in particular for C. americensis . Pupal development times in C. menes varied greatly at both temperatures for certain types (yellow) but not for others (brown). Both species have different reproduction strategies: C. americensis has a higher daily reproduction, but a shorter reproduction period, compared to various strains of C. menes, that reproduce less during a longer period. The population growth rates differed per species / strain and temperature, but where in almost all cases lower than (literature) data of F. occidentalis .In Chapter 7 it is shown that short-range host location by C. menes and C. americensis is positively affected by visual and chemical stimuli. Both species are attracted to yellow colours and were arrested on sites were larvae had been feeding. Wasps did react to the presence or damage inflicted by feeding of non-hosts, but arrestment did not seem to be very host specific: within a parasitoid species no difference was found in reaction to feeding spots of one host species, Thrips tabaci or another F. occidentalis . Parasitoid females were not attracted to the synthetic compounds of the alarm pheromone (decylacetate plus dodecylacetate) of western flower thrips in short-range flight tests, indicating a non-volatile effect.In Chapter 8 evaluation studies were performed on a larger scale: experimental and commercial greenhouses. In spite of repeated introductions in infested crops, either vegetables like sweet pepper and cucumber, or ornamentals like rose and potted plants, very low levels of parasitism were found. Searching efficiency and dispersal ability in a greenhouse crop were very low and parasitoids performed poorly under (temperate) greenhouse conditions. Both parasitoid species could maintain themselves, dispersed and reproduced at Dutch glasshouse conditions, but they were unable to reduce thrips populations to sufficiently low levels.Finally, in Chapter 9, I summarise and discuss the main results of my research, placed in perspective of the pre-introduction criteria we used. It is concluded that, based on behavioural (host selection and searching efficiency), biological (climatic adaptation, development and reproduction capacity) and practical (mass-production) characteristics, thrips parasitoids have very limited prospects for greenhouse biological control for both seasonal inoculative and inundative release programmes in temperate and in Mediterranean greenhouses.