Parasitoids as Biological Control Agents of Thrips Pests Promotor: Prof. dr. J.C. van Lenteren Hoogleraar in de Entomologie, Wageningen Universiteit Promotie Commissie: Prof. dr. L.E.M. Vet, Wageningen Universiteit, Wageningen Dr. B. Aukema, Plantenziektenkundige Dienst, Wageningen Dr. W.J. de Kogel, Plant Research International, Wageningen Prof. dr. H. Eijsackers, Vrije Universiteit, Amsterdam. Parasitoids as Biological Control Agents of Thrips Pests Antoon Loomans Proefschrift ter verkrijging van de graad van doctor op gezag van de rector magnificus van Wageningen Universiteit, Prof. Dr. Ir. L. Speelman, in het openbaar te verdedigen op maandag 8 september 2003 des namiddags te vier uur in de Aula Loomans, A.J.M. (2003) Parasitoids as Biological Control Agents of Thrips Pests Thesis Wageningen University – with references – with summaries in English, Dutch and Italian Subject headings / Thysanoptera / Frankliniella occidentalis / Hymenoptera / Ceranisus menes / Ceranisus americensis / biological control / ISBN : 90-5808-884-7 to Giorgio Nicoli aan Lois, Romi, Oskar, Viktor & Sofia Contents Chapter 1 Evaluation of hymenopterous parasitoids as biological control agents of 1 thrips pests in protected crops: introduction Chapter 2 Exploration for hymenopterous parasitoids of thrips 45 Chapter 3 Mass-rearing thrips and parasitoids 67 Chapter 4 Host selection by thrips parasitoids: effects of host age, host size and 79 period of exposure on behaviour and development Chapter 5 Host selection by Ceranisus menes and C. americensis: inter- and 103 intraspecific variation between populations of parasitoids and their thrips hosts Chapter 6 Life-history studies on larval parasitoids of western flower thrips 127 Chapter 7 Searching for hosts by Ceranisus menes (Walker) and Ceranisus 145 americensis (Girault), parasitoids of thrips: short-range host location Chapter 8 Releases of parasitoids (Ceranisus spp.) as biological control agents of 161 western flower thrips (Frankliniella occidentalis) in experimental greenhouses Chapter 9 Biological control of thrips pests: summarising discussion 179 Summary 189 Samenvatting 191 Riassunto 193 Nawoord 195 Curriculum vitae 197 List of publications 198 A.J.M. Loomans – Parasitoids as Biological Control Agents of Thrips Pests - 2003 1 Chapter 1 Evaluation of hymenopterous parasitoids as biological control agents of thrips pest in protected crops: introduction1 Antoon J.M. Loomans Laboratory of Entomology, Wageningen University, P.O. Box 8031, 6700 EH Wageningen, The Netherlands Abstract In this introduction a general overview of the current status is presented of hymenopterous parasitoids attacking thrips, their prospects as biological control agents. First, thrips pests which currently play a key role in protected cultivation (fruit vegetables and ornamentals) in Europe are discussed: Frankliniella occidentalis (Pergande) and Thrips tabaci Lindeman,. We also include data on two other thrips species which we used in our experiments, Frankliniella schultzei Trybom and Frankliniella intonsa (Trybom). Information is given on their distribution, biology, economical impact and ways for control. This is followed by a short description of the most important groups of natural enemies that are currently evaluated or applied as biological control agents of thrips (predatory mites, pirate bugs, entomopathogenic pathogens and entomophilic nematodes), their potentials and their flaws. This will be viewed upon as a state of the art at the onset of our project and the recent developments in retrospect. Finally, I present the aim of my research project and the outline of this thesis. INTRODUCTION Thrips pests in protected crops Of the more than 5600 recognised species of thrips (order Thysanoptera) a few hundred are recorded attacking cultivated plants. A number of species have become key pests in a wide range of agricultural and horticultural crops. During the past decades, the losses of agricultural and horticultural produce caused by thrips increased considerably, resulting in losses of millions of € (Lewis, 1997). Damage may be the result of direct feeding on leaves, flowers or fruits, transmission of viruses, as well as product contamination (Mound & Teulon, 1995). During the last decades thrips have become pests in many cultivated crops throughout Europe and elsewhere in the world (Lewis, 1973, 1997; Ananthakrishnan, 1984; Mound & Marullo, 1996; Lacasa & Lloréns, 1996, 1998). With a continuously expanding world trade in fresh horticultural produce, changes in production and marketing systems, thrips remain a constant threat to crop pest management systems. Despite post harvest and quarantine procedures, thrips species are spreading worldwide very quickly. They have become the number one key pests in many greenhouse and field crops, especially vegetables and ornamentals (Tommasini & Maini, 1995; Palmer, 1992; EPPO, 1988). Until the early 1980s, Thrips tabaci Lindeman was the most prevalent thrips pest in protected cultivation in Europe (Tommasini & Maini, 1995), but it caused problems only 1 Part of this chapter has been published in a different form in Lewis, T. (ed.), Thrips as Crop Pests, CAB International, Wallingford, UK, pp. 355-397. 2 Chapter 1 occasionally. Since its accidental introduction in 1983, the western flower thrips (Frankliniella occidentalis (Pergande)) has become the number one key pest in European greenhouses and, under Mediterranean conditions, also caused problems in field crops and orchards. Thrips palmi Karny started its expansion in about the same period in the Far East and the Pacific (Loomans & Vierbergen, 1997) and is currently an important pest throughout large parts of tropical and subtropical vegetable and flower producing areas. The continuous exchange of horticultural products all over the world makes this quarantine pest a serious threat to Europe as well. Interceptions from vegetables and cut flowers imported from the Caribbean, South America and Asia have increased in numbers over recent years. Apart from greenhouse crops in temperate areas, it is an important potential problem for the horticultural industry in the Mediterranean Region. While focussing on quarantine pests, another thrips species of nearctic origin managed to sneak in and establish itself on the European continent, Echinothrips americanus Morgan. It was introduced into Europe in 1993 and although known from a wide range of herbs and woody shrubs, it was at first exclusively found on bedding plants, in particular Araceae (e.g. Syngonium). Since 1995, however, several outbreaks occurred on sweet pepper (Capsicum annuum) in particular towards the end of the growing season and is now hampering IPM in this crop (Vierbergen, 1998). Various reviews on F. occidentalis have been published during the past years, once this pest entered a country (EPPO/OEPP, 1988; Brødsgaard, 1989; Del Bene & Gargani, 1989; Ebener et al., 1989; Mantel, 1989; Pèlikan, 1989 (for Europe), Waterhouse & Norris, 1989 (for the Pacific) and Monteiro et al., 1995 (for South America)), as a kind of pest alert paper’. More recently, updates have been published (F. occidentalis: CABI/EPPO1998; Hsu & Quarles, 1995; Cloyd et al., 1998; Van Driesche et al., 1998;T. tabaci: Suchalkin, 1983; both: Waterhouse & Norris, 1989; Tommasini & Maini, 1995) on the current state of knowledge on taxonomy, distribution, recognition, biology, plant virus vector capabilities, food plants, damage, economic importance and control of the thrips, Also through Internet one can consult various databases (Crop Protection Compendium, 2nd edition 2002), newsletters (e.g. WFT Newsletter: Miller & Moran, Australia; Sting: WPRS/IOBC, Europe; IOBC/NRS-Newsletter,Van Driesche, USA) and newsgroups (‘ThripsNet’) for news, developments, problems, discussion and research topics. In this chapter I summarise available information on the thrips pests which currently play a key role in protected cultivation in Europe, with particular emphasis on F. occidentalis and Thrips tabaci. I also include two other species that I studied: Frankliniella schultzei (Trybom) and Frankliniella intonsa (Trybom), 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, entomogenic pathogens and entomophilic nematodes. Specific emphasis is put on the current status of hymenopterous parasitoids attacking thrips, their prospects and the outline of my thesis work. It will be viewed as a state of the art at the onset of our project and, in retrospect, the most recent developments. Thrips Pests Species Frankliniella occidentalis (Pergande 1895) Frankliniella occidentalis (Pergande) or ‘Western Flower Thrips’ originates from the western part of the United States, west of the Rocky Mountains (Bryan & Smith, 1956), where it occurs from sea level to sub-alpine altitudes. It was recorded as a pest for the first time in 1881 in California on apricot and was subsequently described by Pergande in 1895. Later records originate from Canada (Alberta, British Columbia: Treherne, 1923), Oregon, Washington, Idaho, Montana, Wyoming, Colorado, Utah, Nevada, Arizona (Bailey, 1933), Iowa (Moulton & Andre, 1935), New Mexico (Eyer & Medler, 1941), Texas General Introduction Thrips and Parasitoids 3 Figure 1: Geographical distribution and spread of Frankliniella occidentalis (Pergande), = widespread, = present or