Thermal Performance of Two Indigenous Pupal Parasitoids Attacking the Invasive Drosophila suzukii (Diptera: Drosophilidae).

Pachycrepoideus vindemiae (Rondani) and Trichopria drosophilae (Perkins) are among a few indigenous parasitoids attacking the invasive Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in North America. Both parasitoid species occur in California, whereas only P. vindemiae has been reported from Oregon. We compared the thermal performance of the California populations of P. vindemiae and T. drosophilae, and the Oregon population of P. vindemiae at eight constant temperatures (12.6-32.8°C). Both P. vindemiae populations could develop at all tested temperatures. T. drosophilae failed to develop at or above 29.6°C. This species was, however, able to develop at a diurnal temperature regime of 15-32°C, and survival was higher in older developmental stages. T. drosophilae was less tolerant to both low and high temperatures than P. vindemiae, whereas the Oregon P. vindemiae population was more cold-tolerant but less heat-tolerant than the California population in terms of offspring survival, development, and reproduction. To develop storage strategies for mass-cultured parasitoids, we compared the cold tolerance of immature P. vindemiae and T. drosophilae of the California populations at 12°C for 1, 2, or 3 mo, followed by a 23°C holding period. Successful development to the adult stage decreased as cold storage duration increased. Successful development, however, increased when cold storage was initiated during the older developmental stages for 1-mo exposure for both parasitoid species. The results are discussed with regards to parasitoid thermal adaptation and the potential use of P. vindemiae and T. drosophilae for biological control of spotted-wing drosophila.

Linear functional response by two pupal Drosophila parasitoids foraging within single or multiple patch environments.

Functional response describes the number of prey or hosts attacked by a predator or parasitoid as a function of prey or host density. Using three different experimental designs, we found a linear functional response by two insect parasitoids (the pteromalid Pachycrepoideus vindemiae and the diapriid Trichopria drosophilae) to their hosts (the drosophilids Drosophila suzukii and D. melanogaster). A linear function response is considered unusual for insect parasitoids. The first design was a 'fixed time within patch experiment' where individual parasitoids were exposed to a range of host densities for 24 h; the second two designs were a 'variable time functional response' and a 'selective functional response' experiments where individual parasitoids were presented with a range of host patches and allowed to freely select and explore only one patch (variable time) or forage for 24 h (selective). In all experimental designs, the number of hosts parasitized increased linearly until reaching an upper limit. Under the laboratory conditions used, the functional response of P. vindemiae was limited by its egg supply and time (host handling time) whereas T. drosophilae was limited by time only. The linear functional response by both parasitoids likely resulted from a constant attack rate and an incremental foraging strategy where the parasitoids left a poor (low density) host patch or remained in a higher quality host patch when there was successful oviposition and adequate host density.

Overwintering Survival of Drosophila suzukii (Diptera: Drosophilidae) and the Effect of Food on Adult Survival in California's San Joaquin Valley.

The overwintering survival and development of Drosophila suzukii Matsumura were investigated in California's San Joaquin Valley. Drosophila suzukii were exposed to overwintering conditions in cages hung in a citrus orchard, and the pupae were buried in the soil. Eggs exposed from late November to January did not survive; a low percentage (<3%) of larvae and pupae developed into adults. Survival of pupae was significantly higher when buried in the soil than on the citrus tree. From late January to March, all life stages developed into adults and overwintered adult female D. suzukii produced eggs when provided with 10% honey-water and sliced oranges. Adult survival varied among fruit juice provision treatments and overwintering exposure periods, ranging from 3.4 ± 0.9 d (water) to 44.1 ± 3.0 d (10% honey-water). Fruit juices of apple, cherry, grape, orange, and pomegranate were tested as adult food sources; results showed that adult female and male D. suzukii lived only 2 d with water only, whereas adults survived from 14.2 to 34.8 d with fruit juice treatments and the 10% honey-water control. An unexpected event was the oviposition and immature development of D. suzukii with the fruit juice. In a follow-up laboratory trial, when 10% honey-water or orange juice were provided along with an artificial diet for oviposition and immature development, female D. suzukii survived for 21.6 ± 2.4 or 21.6 ± 1.5 d, and produced 106.8 ± 14.1 or 98.5 ± 13.1 offspring, respectively. We discuss factors potentially influencing overwintering survival of D. suzukii.

Tri-trophic movement of carotenoid pigments from host plant to the parasitoid of a caterpillar.

Insect parasitoids normally produce white colored eggs. Habrobracon gelechiae (Hymenoptera: Braconidae) is a gregarious ectoparasitoid of various caterpillars. We found that adult female H. gelechiae lays yellow colored eggs when its larvae developed from host larvae of Choristoneura rosaceana and Epiphyas postvittana (both Lepidoptera: Tortricidae) that were fed green plant leaves, but white colored eggs when these same host larvae species were fed non-plant diets. This study investigated the causes of egg color in H. gelechiae and the possible consequences in terms of parasitoid fitness resulting from differential egg color. Using high-performance liquid chromatography we demonstrated that the yellow coloration resulted from the uptake of carotenoid plant pigments (mainly lutein and ß-carotene) that were initially ingested by the caterpillar larvae from plant leaves, later absorbed by the parasitoid larvae (F0) feeding on the host and carried over to the adult parasitoids, and finally translocated to the eggs (F1) of the parasitoids. The amount of plant pigments consumed by the parasitoid larvae (F0) affected the intensity of the yellow color of the parasitoid's eggs (F1). Similarly, egg color was affected by the adult female parasitoids lifetime egg production and deposition rate. Further tests suggest that the observed differences in egg color did not have a genetic basis and did not affect egg viability or fitness. To our best knowledge, this is the first report of a tri-trophic and multi-stage translocation of carotenoid plant pigments in parasitoids. We discuss possible evolutionary significance and putative functions of the absorption of plant pigments by parasitoid species.

Factors Limiting Peach as a Potential Host for Drosophila suzukii (Diptera: Drosophilidae).

The spotted wing drosophila, Drosophila suzukii Matsumura, has widely established in North America and become an economic concern for a variety of fruit crops. To better understand fruit susceptibility, we evaluated peach surface characteristics on the pest's oviposition success. The number of D. suzukii eggs laid into the fruit flesh was tested on 1) peaches with or without indumenta (commonly referred to as peach fuzz), 2) peaches physically damaged by harvest operations, 3) peaches damaged by the peach twig borer Anarsia lineatella Zeller or the forktailed bush katydid, Scudderia furcata Brunner von Wattenwyl, and 4) peaches with punctures that simulated stink bug damage. Female D. suzukii did not lay eggs in intact fuzzy sections of the fruit or into small punctures (0.3 or 0.5 mm), but readily laid eggs in sections without fuzz, with insect damage, and with large punctures (1 mm). The number of eggs per treatment was positively related to the area of the damaged section; the overall fruit firmness and sugar content was not related to the number of eggs laid in treated or damaged spots. Direct observations of D. suzukii oviposition confirmed that peach fuzz appeared to be an obstacle for the fly's oviposition success, and female flies ceased ovipositional attempts on fuzzy peach sections after a short period of time. Successful oviposition times were associated with substrate firmness, with shorter oviposition time in damaged spots than in cherry fruit or shaved spots of the peach. The results indicate that intact, preharvest peach fruit are unlikely to be infested by the fly, but any surface damage could render the fruit susceptible to the fly.

Overwintering survival of olive fruit fly (Diptera: Tephritidae) and two introduced parasitoids in California.

The overwintering survival and development of olive fruit fly, Bactrocera oleae (Rossi), and the endoparasitoids, Psyttalia humilis Silvestri and P. lounsburyi (Silvestri), were investigated at sites in California's interior valley and coastal region. In the interior valley, adult flies survived up to 4-6 mo during the winter when food was provided. Adult female flies could oviposit in late fall and early winter on nonharvested fruit and, although egg survival was low (0.23-8.50%), a portion of the overwintered cohort developed into adults the following spring; percentage of survival was negatively correlated to daily minimum temperature. P. humilis and P. lounsburyi successfully oviposited into host larvae in late fall, and their progeny developed into adults the following spring, although with a low percentage (0-11.9%) survivorship. Overwintering survival of puparia of the olive fruit fly and immature larvae of P. humilis and P. lounsburyi (inside host puparia), buried in the soil, were tested at an interior valley and coastal site. Survival of olive fruit fly ranged from 0 to 60% and was affected by the trial date and soil moisture. Overwintering survival of both the fruit fly and tested parasitoids was lower at the colder interior valley than the coastal site; P. humilis immature stages had the highest mortality levels while B. oleae pupae had the lowest mortality levels. The spring emergence pattern of the tested insects was well predicted by a degree-day model. We discuss factors potentially impeding establishment of introduced olive fruit fly parasitoids in California and elsewhere.

Performance of Psyttalia humilis (Hymenoptera: Braconidae) reared from irradiated host on olive fruit fly (Diptera: Tephritidae) in California.

The parasitoid Psyttalia humilis (Silvestri) was reared on Mediterranean fruit fly, Ceratitis capitata (Wiedemann), third instars irradiated at 0-70 Gy at the USDA, APHIS, PPQ, Moscamed biological control laboratory in San Miguel Petapa, Guatemala, and shipped to the USDA, ARS, Parlier, CA. Irradiation dose did not affect the parasitoid's offspring sex ratio (53-62% females), percentage of unemerged adults (12-34%), number of progeny produced per female (1.4-1.8), and parasitism (19-24%). Host irradiation dose had no significant effect on the forewing length of female P. humilis and its parasitism on olive fruit fly, Bactrocera oleae (Rossi) and offspring sex ratio, but dissection of 1-wk-old female parasitoids reared from hosts irradiated with 70 Gy had a significantly lower number of mature eggs than females from nonirradiated hosts. Longevity of P. humilis adults decreased with increased temperature from 15 to 35°C, regardless of food provisions, gender, and host irradiation dose. Females survived 37-49 d at 15°C with water and food, and only 1-2 d at 35°C without food, whereas males lived shorter than females at all temperatures and food combinations tested. Adult P. humilis reared from fertile C. capitata and aspirated for dispensing in cups lived significantly longer after shipment than those specimens chilled and dispensed by weight. At 21 and 32°C, 50% of parasitoids departed release cages after 180 and 30 min, respectively, but none departed at 12°C. Thirteen shipments of P. humilis (2,980-21,922 parasitoids per shipment) were received between September and December 2009, and seven shipments (7,502-22,560 parasitoids per shipment) were received between October and December 2010 from San Miguel Petapa, Guatemala. Daily number of olive fruit fly adult and percentage female trap captures ranged <1-19 and 8-58% in 2009, and <1-11 and 0-42% in 2010, respectively. The number of parasitoids released ranged 848-12,257 in 2009 and 3,675-11,154 in 2010. Percentage parasitism of olive fruit fly third instars at all locations ranged 0-9% in 2009 and 0-36% in 2010.

Light brown apple moth in California: a diversity of host plants and indigenous parasitoids.

The light brown apple moth, Epiphyas postvittana (Walker), an Australia native tortricid, was found in California in 2006. A field survey of host plants used by E. postvittana was conducted in an urban region of the San Francisco Bay Area. An inspection of 152 plant species (66 families), within a 23-ha residential community, found E. postvittana on 75 species (36 families). Most (69 species) host plants were not Australian natives, but had a wide geographic origin; 34 species were new host records for E. postvittana. Heavily infested species were the ornamental shrubs Myrtus communis L., Pittosporum tobira (Thunb.) W.T. Aiton, Euonymus japonicus Thunb., and Sollya heterophylla Lindl. To survey for parasitoids, four urban locations were sampled, with E. postvittana collected from five commonly infested plants [M. communis, P. tobira, E. japonicus, Rosmarinus officinalis L., and Genista monspessulana (L.) L.A.S. Johnson]. Twelve primary parasitoid species and two hyperparasitoids were reared; the most common were the egg parasitoid Trichogramma fasciatum (Perkins), the larval parasitoids Meteorus ictericus Nees, and Enytus eureka (Ashmead), and the pupal parasitoid Pediobius ni Peck. Meteorus ictericus accounted for >80% of the larval parasitoids, and was recovered from larvae collected on 39 plant species. Across all samples, mean parasitism was 84.4% for eggs, 43.6% for larvae, and 57.5% for pupae. The results are discussed with respect to the potential for resident parasitoid species to suppress E. postvittana populations.

High summer temperatures affect the survival and reproduction of olive fruit fly (Diptera: Tephritidae).

The olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), is an invasive pest in California. Identifying environmental constraints that affect the geographic distribution and abundance of any invasive insect pest is fundamental to its effective management. California's Central Valley, where most commercial olives are grown, is extremely hot during the summer, with maximum daily temperatures consistently >35.0 degrees C. This study examined the effects of two diurnal temperature regimens (low 18.3 degrees C, high 35.0 or 37.8 degrees C) reflecting summer conditions in the valley, and one control temperature regimen (low 18.3 degrees C, high 23.9 degrees C) on the fly's survival and reproductive success in the laboratory. The temperature regimen of 18.3-35.0 degrees C resulted in delayed egg maturation and reduced production of mature eggs compared with the control temperature regimen. Egg maturation was possible at the higher temperature regimen when females were provided with water and food, and egg-laying occurred during the cold phase of the temperature cycle. Access to olive fruit and oviposition itself further promoted egg maturation. Under exposure to the 18.3-35.0 degrees C temperature regimen, approximately 50% of eggs died, and the remainder that hatched died as first instars. No egg hatch occurred at the temperature treatment of 18.3-37.8 degrees C. We confirmed these laboratory results through field cage studies with adult B. oleae, conducted in the summer of 2007 and 2008. Under ambient summer temperatures, adult B. oleae survived for 1-2 wk, and females readily laid eggs when provided water and food. No offspring developed in midsummer of 2007, and <2% of the offspring developed to adults in summer 2008 trials. These results suggest that high summer temperatures limit the fly's abundance in California's Central Valley.

Effects of Peganum harmala (Zygophyllaceae) seed extract on the olive fruit fly (Diptera: Tephritidae) and its larval parasitoid Psyttalia concolor (Hymenoptera: Braconidae).

Peganum harmala L. (Zygophyllaceae) is an herb native to arid and semiarid regions of Central Asian deserts. This study investigated the effects of ethanol extracts of P. harmala seeds on the olive fruit fly, Bactrocera oleae (Rossi) (Diptera: Tephritidae), i.e., adult repellency, reproductive activity, and larval growth, as well as parasitism levels by Psyttalia concolor (Szépligeti). Olive fruit treated with 2% extract reduced B. oleae oviposition. In choice tests, female B. oleae spent >99% of their time foraging on untreated fruit rather than P. harmala-treated fruit. These changes in ovipositional behavior resulted in a nearly 30-fold decrease in oviposition marks on treated fruit compared with untreated fruit during a 48 h exposure period. When female B. oleae were fed liquid diet containing 0.2% P. harmala extract, there was no effect on the number of ovipositional marks on exposed fruit, but up to 21.4% of the deposited eggs were deformed. SDS-polyacrylamide gel electrophoresis analyses of deformed eggs revealed that some protein bands were missing. Consequently, the number of offspring produced by treated females was lower than by untreated females. Neither the sex ratio nor body size of the fly's offspring were affected by adults fed diet containing 0.2% P. harmala extract. However, there was a slightly prolonged developmental time from egg to adult. Parasitism of larval B. oleae by P. concolor was not affected by infested fruit treatment with 2% P. harmala extract. P. harmala extracts as a potential control for insect pest species are discussed.

Feeding and attraction of non-target flies to spinosad-based fruit fly bait.

A spinosad-based fruit fly bait, GF-120, has recently become a primary tool for area-wide suppression or eradication of pest tephritid fruit flies. The present study assessed the attraction and feeding of five non-target fly species to GF-120 in Hawaii. These non-target flies include three beneficial tephritid species [Eutreta xanthochaeta (Aldrich), Tetreuaresta obscuriventris (Loew), Ensina sonchi (L.)] introduced for weed biological control, an endemic Hawaiian tephritid [Trupanea dubautiae (Bryan)] (all Diptera: Tephritidae) and the cosmopolitan Drosophila melanogaster Meigen (Diptera: Drosophilidae). All five non-target fly species were susceptible to GF-120, as was the target pest Mediterranean fruit fly Ceratitis capitata (Wiedemann). Feeding on, or even brief tasting of, GF-120 killed all fly species within 2 h. When individual flies were provided with a choice of GF-120 or honey solution, there was no difference in the frequency of first food encounter by E. xanthochaeta, D. melanogaster or C. capitata. The other three non-target species approached honey more often than GF-120 in their first food encounter. Feeding times on GF-120 and honey were not significantly different for D. melanogaster and C. capitata, while the other four non-target species fed longer on honey than on GF-120. There was no significant difference in feeding time on honey versus GF-120 between males and females of each species. These results suggest that area-wide treatment using GF-120 for the purpose of eradication of pest fruit flies has potential negative impacts on these and other non-target fly species in Hawaii.