Available online at www.sciencedirect.com Biological Control 44 (2008) 79–89 www.elsevier.com/locate/ybcon Psyttalia lounsburyi (Hymenoptera: Braconidae), potential biological control agent for the olive fruit fly in California Kent M. Daane a,*, Karen R. Sime a, Xin-geng Wang b, Hannah Nadel a,b, Marshall W. Johnson b, Vaughn M. Walton a,1, Alan Kirk c, Charles H. Pickett d a Department of Environmental Science, Policy, and Management, University of California, Berkeley, CA 94720-3114, USA b Department of Entomology, University of California, Riverside, CA 92521, USA c USDA – Agriculture Research Service, European Biological Control Laboratory, Montferrier sur Lez, 34988 St. Ge´ly Cedex, France d Biological Control Program, California Department of Food and Agriculture, 3288 Meadowview Road, Sacramento, CA 95832, USA Received 3 May 2007; accepted 30 August 2007 Available online 8 September 2007 Abstract The African parasitoid Psyttalia lounsburyi (Silvestri) was evaluated as part of a classical biological control program directed at the olive fruit fly, Bactrocera oleae (Rossi), in California, USA. Experimental assessment using three non-target species provided some evi- dence that P. lounsburyi restricts its host use to B. oleae. Female P. lounsburyi preferentially searched olives infested with mature third- instar B. oleae, over other non-target plants, but most offspring were reared from olives containing younger (second through young third instar) B. oleae larvae. Developmental time (egg to adult) and adult longevity were significantly affected by temperature and sex, with males tending to develop faster and females living longer, especially in the lower ranges of temperatures tested. The mean longevity of adult female P. lounsburyi was greatest when honey was available and lowest when they were provided water alone or nothing. The presence of hosts significantly decreased longevity. Females produced an average of 10.2 ± 2.6 progeny during their lifetimes, which was lower than expected for a parasitoid adapted to B. oleae and may be a consequence of increased fruit size—the result of cultivation and selection—reducing parasitoid effectiveness on cultivated vs. wild fruit, as well as constraints on oviposition behavior imposed by experimental design. The results are discussed with respect to the use of P. lounsburyi as a biological control agent for olive fruit fly in California. Published by Elsevier Inc. Keywords: Bactrocera oleae; Olea; Psyttalia lounsburyi; Biological control; Non-target assessment; Parasitoid biology 1. Introduction most commonly reared parasitoid of B. oleae in wild olives (Copeland et al., 2004). In South Africa, the minor impact The African parasitoid Psyttalia lounsburyi (Silvestri) of B. oleae in wild olives is largely attributed to the action (Hymenoptera: Braconidae) was imported to California of the resident natural enemy fauna (Hancock, 1989), of as part of a biological control program directed at the olive which Utetes africanus (Sze´pligeti) is the dominant parasit- fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), a oid and P. lounsburyi is a significant component (Walton, recent arrival in the state (Collier and van Steenwyk, 2003; 2005). Despite its promise, little is known of the biology Rice et al., 2003). The literature suggests that P. lounsburyi of P. lounsburyi. It was identified nearly 100 years ago (Sil- may be an effective B. oleae parasitoid. In Kenya, it is the vestri, 1914), but little effort has been made to use it in the longstanding biological control programs for B. oleae in Europe (Greathead, 1976). These programs have focused * Corresponding author. Fax: +1 559 646 6593. almost exclusively on Psyttalia concolor (Sze´pligeti) since E-mail address: [email protected] (K.M. Daane). 1 Present address: Department of Horticulture, Oregon State University, the 1950s, when an efficient mass-rearing technique for this Corvallis, OR 97331-7304, USA. parasitoid was developed that uses the Mediterranean fruit 1049-9644/$ - see front matter Published by Elsevier Inc. doi:10.1016/j.biocontrol.2007.08.010 80 K.M. Daane et al. / Biological Control 44 (2008) 79–89 fly, Ceratitis capitata (Wiedemann) (Tephritidae), in artifi- tephritid biological control agents, and a native species, cial diet (Clausen, 1978; Greathead, 1976). Rhagoletis fausta (Osten Sacken), which feeds on wild bit- Among the various parasitoids considered for B. oleae ter cherry fruit (Rosaceae). These non-target species repre- biological control in California (Sime et al., 2006a,b,c), sent the three major feeding niches of native California P. lounsburyi is especially attractive because there is tephritid larvae (flower heads of Asteraceae, galls, and evidence, again from the literature, that it is more of a fruits) (Foote et al., 1993). Given the challenges posed by specialist on B. oleae than other parasitoid species reared the large number of tephritid species in California, our from B. oleae. Its known geographic range—collections approach to assess the potential non-target host range of have been made from Kenya and South Africa—is entirely candidate parasitoids was to test a small number of tephri- contained within that of B. oleae (Nardi et al., 2005; Whar- tid species selected to span a broad range of phylogenetic ton and Gilstrap, 1983). Unlike other common braconid diversity and larval habitats, and to compare parasitoid parasitoids of B. oleae, such as P. concolor and Bracon celer behavioral responses and reproductive success relative to Sze´pligeti, which are often collected from Ceratitis species, the target species and its habitat. Second, we determined in field collections P. lounsburyi has been reared only from basic biological parameters of P. lounsburyi, including B. oleae (Narayanan and Chawla, 1962; Neuenschwander, adult longevity and fecundity, in order to compare its 1982; Wharton and Gilstrap, 1983; Wharton et al., 2000). potential with other braconids imported and evaluated The absence of other host records is not for lack of inves- for B. oleae biological control. The accumulated experience tigative effort. Likely alternative hosts have been reared gained during these studies will be helpful in developing throughout Africa during decades of foreign exploration field-release protocols and techniques for rearing P. louns- for natural enemies of various tephritid pests (Clausen, buryi on B. oleae. 1978; Clausen et al., 1965; Wharton, 1989; Copeland et al., 2004). That P. lounsburyi has not been reared from 2. Materials and methods C. capitata despite intensive efforts to find natural enemies of this pest (Wharton et al., 2000) and despite the fact that 2.1. Sources of insects and plants, and colony maintenance it can be cultured on C. capitata in the laboratory (Billah et al., 2005) suggests that other tephritid species are accept- Separate colonies of B. oleae and P. lounsburyi were able but not attacked. Many tephritid parasitoids use cues established at two University of California facilities, the from host plants to help locate their insect hosts (Messing College of Natural Resource’s Quarantine in Berkeley and Jang, 1992; Godfray, 1994). Therefore, the apparent and the Kearney Agricultural Center’s Insectary in Parlier, field specialization of P. lounsburyi on B. oleae might also California. Bactrocera oleae were reared on olive fruit include cues from the olive tree or fruit. using methods described by Sime et al. (2006b). In brief, Field evidence of specialization and efficacy alone is not adult flies were held in ventilated cages (50 cm3) that were considered sufficient for obtaining permission to release provisioned ad libitum with water and a 2:1 mixture of parasitoids exotic to the USA and often additional experi- honey and dry yeast extract (Fisher Biotech, Fairlawn, mental evidence of host specificity is also required (Hoel- NJ). Susceptible olives were exposed to the fly colony until mer and Kirk, 2005; van Driesche and Reardon, 2004). each fruit had 3–5 oviposition marks, typically <1 day, and Over 140 native tephritids inhabit California, including then removed to a separate rearing cage. The inoculated some endemic species (Foote et al. 1993). In California olives were held until the mature fly larvae exited the fruit there is also concern that introduced parasitoids of tephri- to pupate, upon which the puparia were collected and tid pests might attack beneficial tephritids used or consid- transferred to Petri dishes. The olives were collected from ered for biological control of weeds. Direct testing of orchards in Fresno County. Small to medium-size olives imported parasitoids’ responses to those tephritids is neces- (‘Mission’ or ‘Manzanillo’ cv.) were used for all experi- sary. Currently these include Chaetorellia succinea (Costa), ments, while olives of various cultivars, including ‘Ascolano’ which feeds in the flower heads of yellow starthistle, Cen- and ‘Sevillano,’ were also used for maintenance of the fly taurea soltitialis L. (Asteraceae) (Balciunas and Villegas, and parasitoid colonies. 2001), and Parafreutreta regalis (Munro), which forms The P. lounsburyi colony used in the Berkeley Quaran- stem galls in Cape ivy, Delairea odorata Lemaire (Astera- tine originated from adults that had emerged from B. oleae ceae) (Balciunas and Smith, 2006). These weeds can occur collected in wild (Olea europaea L. subsp. cuspidata (Wall. near olive trees, and this may promote encounters with par- ex G. Don)) and cultivated (ornamental) olives near Stel- asitoids of B. oleae. Yellow starthistle grows in low-eleva- lenbosch, South Africa, and were sent as puparia to the tion disturbed areas, and Cape ivy is widespread in Berkeley Quarantine in June 2004 and August 2005. After coastal habitats of California. a USDA-APHIS permit was granted to move P. lounsburyi We conducted a series of experiments to determine the out of Quarantine, experiments were conducted at the potential of P. lounsburyi as a biological control agent Kearney Agricultural Center using a P. lounsburyi colony for B. oleae in California and to proceed, if warranted, with established from 400 parasitoids shipped from the its field release. First, we evaluated the non-target impact USDA-ARS European Biological Control Laboratory in of P.