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Non-Target Host Acceptance and Parasitism by Trichogramma Brassicae Bezdenko (Hymenoptera: Trichogrammatidae) in the Laboratory

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Non-Target Host Acceptance and Parasitism by Trichogramma Brassicae Bezdenko (Hymenoptera: Trichogrammatidae) in the Laboratory Biological Control 26 (2003) 128–138 www.elsevier.com/locate/ybcon Non-target host acceptance and parasitism by Trichogramma brassicae Bezdenko (Hymenoptera: Trichogrammatidae) in the laboratory D. Babendreier,* S. Kuske, and F. Bigler Swiss Federal Research Station for Agroecology and Agriculture, Reckenholzstrasse 191, CH-8046 Zurich, Switzerland Received 7 December 2001; accepted 11 September 2002 Abstract As part of a risk assessment study, we exposed eggs of 23 non-target lepidopteran species including nine butterflies endangered in Switzerland to individual Trichogramma brassicae Bezdenko females under no-choice conditions in the laboratory. We could show that Papilio machaon L. (Papilionidae), Artogeia ( ¼ Pieris) napi L. (Pieridae), Argynnis adippe Denis & Schiffermuuller,€ Clossiana titania Esper, (Nymphalidae), Aphantopus hyperanthus L., Maniola jurtina L., Coenonympha pamphilus L., Melanargia galathea L., Erebia ligea L., Hipparchia alcyone Denis & Schiffermuuller€ (Satyridae), Polyommatus icarus Rottemburg and Plebejus idas L. (Lycaenidae) were well accepted and not parasitized significantly different (range 73–94%) than the target, Ostinia nubilalis Huubner€ (81%). Virtually all eggs of Vanessa atalanta L., Argynnis niobe L., Clossiana selene L. (Nymphalidae), and Cyaniris semiargus Rottemburg (Lycaenidae) were accepted for oviposition resulting in significantly higher parasitism rates of 94–97% compared with the target. Melitaea parthenoides Keferstein, M. diamina Lang, and nearly 50% of Mellicta athalia Rottemburg (Nymphalidae) eggs were rejected early in the host selection process. Ovipositional success on eggs of Zygaena filipendula L. (Zygaenidae), Hesperia comma L. (Hesperidae), Sphinx ligustri L., and Deilephila elpenor L. (Sphingidae) was less than 30%. The number of times a female left a host egg before acceptance as well as the time from first host egg contact to acceptance was not related to parasitism rate on the tested non-targets. Offspring emerging from non-target hosts was of similar or even larger size compared to offspring emerging from the target, and in all cases larger compared to individuals emerging from the factitious host, Ephestia kuehniella Zeller. We found that large T. brassicae individuals had significantly higher success in penetrating the chorion and parasitizing eggs of S. ligustri than smaller adults. The results show that T. brassicae parasitizes a number of non-target lepidopteran eggs belonging to different families. Host range and impact under field conditions have yet to be determined. Ó 2002 Elsevier Science (USA). All rights reserved. Keywords: Trichogramma brassicae; Biological control; Non-target effect; Risk assessment; Host specificity; Egg parasitoids; Endangered butterflies 1. Introduction biological control worldwide (Li, 1994; van Lenteren, 2000). While in some cases native species were mass Since the beginning of biological control, more than reared and released, in many cases the utilized Tricho- 5200 agent introductions against economically impor- gramma species were exotic. Trichogramma brassicae tant insect pests have been made (Greathead and Bezdenko was introduced 30 years ago from Moldavia Greathead, 1992, updated 2000; Waage, 1990). Egg (former Soviet Union) to control the European corn parasitoids of the genus Trichogramma have been used borer, Ostrinia nubilalis Huubner€ (Lepidoptera: Crambi- successfully as inundative biological control agents dae), in several parts of Western Europe. This was a against a range of agricultural pests, mainly lepidopt- complete success which markedly reduced the pesticide erans and are the most widely used natural enemies in levels applied in maize in those countries (Bigler, 1986; Hassan, 1988). In other parts of the world, the use of * Corresponding author. Fax: +41-1-377-72-01. Trichogramma spp. has also led to occasional specta- E-mail address: [email protected] (D. Babendreier). cular successes (Li, 1994; Smith, 1996). 1049-9644/02/$ - see front matter Ó 2002 Elsevier Science (USA). All rights reserved. PII: S1049-9644(02)00121-4 D. Babendreier et al. / Biological Control 26 (2003) 128–138 129 Biological control of insect pests has been viewed as US. However, very few butterflies and no rare species environmentally safe for much of its history. Over the were included in the analyses. last two decades, concerns about possible detrimental Virtually no information on parasitism by Tricho- effects for native fauna have been raised by ecologists gramma spp. of non-target butterflies, especially endan- (Howarth, 1983). Several papers have since reviewed the gered species, is available. Therefore, and because cases where non-target effects have been observed but, conservationists are much concerned about this group of more importantly, highlighted the fact that few studies non-target insects, we did not select host species from all on non-target effects were conducted and effects due to potential taxa but rather focused on butterflies. As a first exotic biological control agents may have been over- step of a general risk assessment procedure, we investi- looked (Howarth, 1991; Lynch et al., 2001; Simberloff gated whether eggs of potentially susceptible non-target and Stiling, 1996; Stiling and Simberloff, 2000). species were attacked by T. brassicae in the laboratory. One of the key parameters determining non-target We tested T. brassicae on butterfly species from all major effects is the range of species an agent is able to attack. It families occuring in Europe and included species re- is generally accepted that the release of agents with re- corded on the Swiss Red List of Endangered Species stricted host ranges should be favored in order to min- (Duelli, 1994). In addition, the performance of parasitoid imize potential non-target effects. Therefore, host offspring within non-target host eggs was investigated specificity testing has become a central issue in projects because this might have important implications for the on biological control of insect pests. However, methods risk of butterfly populations. This study should provide a to test the host specificity of biological control agents first indication as to which species of butterflies are po- have been refined significantly for weeds (McEvoy, tentially at risk and should also serve to identify species 1996) but not so for insects. There is an ongoing debate that have to be further evaluated under field conditions. on this issue with the aim to improve the predictability of non-target attack after introduction (Barratt et al., 1999; Kuhlmann et al., 2000). 2. Materials and methods The vast majority of Trichogramma species are known to be fairly polyphagous, attacking a wide range 2.1. Trichogramma brassicae strain of lepidopterans and even species of other insect orders (e.g., Clausen, 1940; Pinto and Stouthamer, 1994; Trichogramma brassicae used in this study originated Thomson and Stinner, 1989). Information on the host from a colony that was maintained at the Swiss Federal range of T. brassicae in general is scarce and virtually Research Station for Agroecology and Agriculture for absent regarding economically unimportant species. In about 60 generations on European corn borer eggs. Prior contrast with the current practice of biological control to experiments, parasitoids were reared for 4–5 genera- of insect pests, the host range of T. brassicae had not tions on the Mediterranean flour moth, Ephestia ku- been evaluated prior to introduction to Western Europe ehniella Zeller, at 16:8 (L:D) h, 25 °C, and 60–70% RH. because non-target effects were not considered an im- O. nubilalis egg masses laid on wax paper were obtained portant issue at that time. from the French Agricultural Research, Lambert (US), Because most Trichogramma are known to be highly every four weeks and then stored at 4 °C, 85% RH. E. polyphagous and are currently released annually on kuehniella eggs were provided by Biotop, Valbonne, several million ha worldwide, information on potential France, fortnightly and stored under the same condi- non-target effects due to Trichogramma is in demand. tions. In order to verify the identity of our T. brassicae Andow et al. (1995), using a theoretical approach rearing strain, material from our colony was sent to based partially on empirical data, could show that the Wageningen Agricultural University, NL, periodically Karner blue, an endangered butterfly in the USin- where it was identified by PCR. About 5000 parasitized habiting oak savanna, faces only a small risk due to eggs were put in a ventilated container of 1.3 L from mass releases of Trichogramma nubilale Ertle & Davis which T. brassicae adults could emerge. Adult parasi- in corn. Preliminary data provided by Suverkropp toids were stored at 25 Æ 0:5°C and 70 Æ 5% RH and (unpublished OECD report, 1997) showed that T. provided with small droplets of honey. One day-old brassicae parasitized some non-target host eggs (one mated females were used for the experiments. undetermined nymphalid and Pterostoma palpinum Clerck (Lepipoptera: Notodontidae)) in the vicinity of 2.2. Selection of butterfly species release fields in Switzerland, but the rate of parasitism was 4% or less. Only recently Orr et al. (2000) pub- Non-target host species selection was based mainly lished data on the potential host range of T. brassicae. on ecological criteria as well as on habitat and temporal In laboratory trials, these authors found that this overlap of hosts and inundatively released T. brassicae. parasitoid is able to attack several Lepidopterans
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