Assessing Natural Incidence of Resident Pupal Parasitoids on the Drosophila suzukii (Diptera: Drosophilidae) Population in Non-crop Fruits.

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), world-renowned as spotted-wing drosophila, is an invasive pest mainly affecting healthy, soft and stone fruit crops throughout Argentinian fruit-growing regions. Natural environments overgrown by exotic feral host plants apparently favour D. suzukii proliferation. This is common in the subtropical northwestern Argentina's berry-producing region. An assemblage of resident parasitoid species has been associated with D. suzukii in crop and non-crop areas of Tucumán, the Argentina's leading berries producer and exporter. Consequently, the hypothesis that the combined action of two pupal parasitoid species, Pachycrepoideus vindemiae Rondani (Hymenoptera: Pteromalidae) and Trichopria anastrephae Lima (Hymenoptera: Diapriidae), occurring in non-crop fruit areas, has a significant impact on D. suzukii natural regulation in such invaded habitats was tested. A survey of D. suzukii puparia from both feral peach [Prunus persica (L.) Batsch] (Rosaceae) and guava (Psydium guajava L.) (Myrtaceae) fallen fruits and soil surrounding them was performed in a wilderness area of Tucumán. Abundance of D. suzukii and associated parasitoids, and parasitism levels were assessed. Whole of 3437 D. suzukii puparia were recovered; 78% and 22% were surveyed from fruits and soil underneath the fruit, respectively. Tested fruits are important D. suzukii multiplying hosts. Both P. vindemiae and T. anastrephae accounted for 99.8% of total parasitoid individuals. Pupal parasitoids contribute to the D. suzukii natural mortality, as they killed a quarter of all puparia. Mostly T. anastrephae foraged on host puparia located in the fruit and P. vindemiae in both microhabitats. This information supports an augmentative biological control strategy in non-crop areas.

Survey on Drosophila suzukii and Ceratitis capitata (Diptera: Drosophilidae, Tephritidae) and Associated Eucoilinae Species (Hymenoptera: Figitidae) in Northwestern Argentina. First Record of Dicerataspis grenadensis and Leptopilina boulardi as Parasitoids of D. suzukii.

The Southeast Asian-native Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), also known as "spotted-wing Drosophila," is one of the most globally invasive agricultural species. Although D. suzukii is a pest spread throughout all the Argentinian fruit-growing regions, few information has been published on its impact on local fruit production. Parasitoid species associated with D. suzukii in Argentina belong to Pteromalidae (Chalcidoidea), Diapriidae (Diaprioidea), both attacking host pupae, and Figitidae (Cynipoidea), which attack host larvae. Nine Eucoilinae (Figitidae) species, belonging to Dicerataspis, Dieucoila, Euxestophaga, Ganaspis, Hexacola, and Leptopilina genera, have been associated with D. suzukii in Argentina. Ceratitis capitata (Wiedemann), commonly known as "medfly," is native to Africa and has a worldwide distribution, covering many tropical, subtropical, and temperate regions. In Argentina, C. capitata has been associated with several native hymenopterous parasitoids belonging to Braconidae (Ichneumonioidea), Eulophidae (Chalcidoidea), Pteromalidae, Diapriidae, and Figitidae families. Only two eucoline species, Ganaspis pelleranoi (Brèthes) and Leptopilina haywardi (Blanchard) have been related to medfly in Argentina. We report new trophic associations between the parasitoids Dicerataspis grenadensis Ashmead and Leptopilina boulardi (Barbotin, Carton and Kelner-Pillault) and D. suzukii, and between the parasitoid Odontosema albinerve Kieffer and C. capitata, after surveys conducted in Tucumán, northwestern Argentina. An annotated checklist and a taxonomic key of Eucoilinae associated with both invasive pests, in Argentina, are also provided.

The Population Dynamics and Parasitism Rates of Ceratitis capitata, Anastrepha fraterculus, and Drosophila suzukii in Non-Crop Hosts: Implications for the Management of Pest Fruit Flies.

Understanding the seasonal dynamics inherent to non-crop host-fruit fly-parasitoid interactions is vitally important for implementing eco-friendly pest control strategies. This study assessed the abundance and seasonal infestation levels of three pest fly species, Ceratitis capitata (Wiedemann), Anastrepha fraterculus (Wiedemann), Drosophila suzukii (Matsumura), as well as the related saprophytic drosophilids, and their natural parasitism in a disturbed wild habitat characterized by non-crop hosts in northwestern Argentina over 40 months. Juglans australis Griseb (walnut), Citrus aurantium L. (sour orange), Eriobotrya japonica (Thunb.) Lindley (loquat), Prunus persica (L.) Batsch (peach), and Psydium guajava L. (guava) were sampled throughout their fruiting seasons. Fruits were collected from both the tree canopies and the ground. The most abundant puparia was A. fraterculus, followed by C. capitata and D. suzukii. Drosophila species from the D. melanogaster group were highly abundant only in fallen fruits. Spatiotemporal overlaps of different host fruit availability provided suitable sources for pest proliferation throughout the year. The populations of both invasive pests peaked from December to January, and were related to the highest ripe peach availability, whereas the A. fraterculus population peaked from February to April, overlapping with the guava fruiting period. The three pest fly species were parasitized mainly by three generalist resident parasitoids, which are potential biocontrol agents to use within an integrated pest management approach.

Drosophila suzukii in Argentina: State of the Art and Further Perspectives.

Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), commonly known as spotted-wing drosophila or SWD, is an invasive, severe, and damaging pest, which is able to inflict huge economic losses on soft thin-skinned fruits worldwide. Argentina was not excluded from the rapid invasion of this new and aggressive pest. Berries and cherries are among the most economically important fruits, showing an increasing demand from both domestic and export markets, which make necessary the application of effective and early protection measures. Although SWD is currently established almost everywhere in Argentina, the scarcity of research on and rapid regulatory actions against this pest have probably contributed to its fast spread throughout the country. In view of that, the article reviews first the current threat status of SWD in Argentina, provides summarized information on crop and non-crop host fruits, seasonal variation and population dynamics, resident natural enemy assemblages, and describes control actions implemented to date. Finally, the need to focus local control actions within an integrated national SWD management program is emphasized. The development and application of complementary eco-friendly strategies, such as Sterile Insect Technique, biological control, mass trapping, and the use of innovative lactone-derived synthetic insecticides with extremely low toxicity for SWD parasitoids, in environmentally distinguishable Argentinian regions is also highlighted.

Implications of the Niche Partitioning and Coexistence of Two Resident Parasitoids for Drosophila suzukii Management in Non-Crop Areas.

Understanding the mechanisms associated with the coexistence of competing parasitoid species is critical in approaching any biological control strategy against the globally invasive pest spotted-wing drosophila (=SWD), Drosophila suzukii (Matsumura). This study assessed the coexistence of two resident pupal parasitoids, Trichopria anastrephae Lima and Pachycrepoideus vindemiae Rondani, in SWD-infested fruit, in disturbed wild vegetation areas of Tucumán, northwestern Argentina, based on niche segregation. Drosophilid puparia were collected between December/2016 and April/2017 from three different pupation microhabitats in fallen feral peach and guava. These microhabitats were "inside flesh (mesocarp)", "outside flesh", but associated with the fruit, and "soil", i.e., puparia buried close to fruit. Saprophytic drosophilid puparia (=SD) belonging to the Drosophila melanogaster group and SWD were found in all tested microhabitats. SD predominated in both inside and outside flesh, whereas SWD in soil. Both parasitoids attacked SWD puparia. However, T. anastrephae emerged mainly from SD puparia primarily in the inside flesh, whereas P. vindemiae mostly foraged SWD puparia in less competitive microhabitats, such as in the soil or outside the flesh. Divergence in host choice and spatial patterns of same-resource preferences between both parasitoids may mediate their coexistence in non-crop environments. Given this scenario, both parasitoids have potential as SWD biocontrol agents.

Augmentative Releases of Two Diachasmimorpha longicaudata (Hymenoptera: Braconidae) Population Lines Under Field-Cage Conditions to Control Ceratitis capitata (Diptera: Tephritidae).

Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), known as Medfly, is a severe agricultural invasive pest in Argentinian fruit-producing regions. The native habitat disturbance and introduction and spread of exotic host plants strongly favored Medfly proliferation. This scenario is common throughout the northern subtropical citrus-growing region. Environmentally friendly strategies to suppress Medfly populations by the National Fruit Fly Control and Eradication Program have currently been taken. One of these actions involves augmentative biological control through releases of the exotic parasitoid Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae). Consequently, the hypothesis that the effectiveness of D. longicaudata females, from two different population lines, in controlling Medfly larvae progressively increases as the density of released females increases was tested. One parasitoid line derives from larvae of a biparental Medfly strain. The other hails from irradiated larvae of the genetic sexing Temperature Sensitive Lethal Vienna-8 medfly strain reared at the "BioPlanta San Juan" biofactory. Parasitoids foraged for 24 h on peaches artificially inoculated with naked lab-reared biparental Medfly larvae. Peaches were placed near the roof or on the ground in field cages. Five treatments (20, 40, 80, 160, and 320 females released) and a control (no parasitoids) for each population line were carried out throughout summer and autumn 2016. Host density (200 larvae) remained constant. At 320 released parasitoid females, both D. longicaudata population lines highly increased the Medfly mortality in both testing seasons, and foraged skillfully on peaches at both fruit height levels. These data encourage the application of augmentative biological control against Medfly.

Host Suitability and Fitness-Related Parameters in Coptera haywardi (Hymenoptera: Diapriidae) Reared on Irradiated Ceratitis capitata (Diptera: Tephritidae) Pupae Stemming From the tsl Vienna-8 Genetic Sexing Strain.

Coptera haywardi (Ogloblin) is a pupal endoparasitoid of tephritid flies with great potential as a biological control agent worldwide as it does not attack other Diptera. To reach its full potential, its mass rearing needs to be enhanced lowering costs. Here, we focused on the use of irradiated pupae of Ceratitis capitata (Wiedemann) stemming from the temperature-sensitive lethal (tsl) Vienna-8 genetic sexing strain (= CcVienna-8), which is mass-produced in the San Juan Medfly and Parasitoid Mass Rearing Facility in Argentina. Exposure of 1- to 2-d-old CcVienna-8 pupae irradiated at 90 Gy to 6- to 8-d-old C. haywardi females at a 10:1 host/parasitoid ratio for 24 h turned out to be highly successful for the rearing of this parasitoid. High radiation doses (90-100 Gy) did not adversely influence fitness parameters of C. haywardi offspring F1, namely lifetime reproductive rates, adult life expectancy, and survival time. Demographic parameters in C. haywardi F1 from irradiated CcVienna-8 young pupae were improved compared to those values recorded from parasitoid originated from nonirradiated CcVienna-8 pupae. These findings will help to enhance parasitoid mass rearing for augmentative releases against medfly in Argentinean fruit-producing regions.

Radiation on Medfly Larvae of tsl Vienna-8 Genetic Sexing Strain Displays Reduced Parasitoid Encapsulation in Mass-Reared Diachasmimorpha longicaudata (Hymenoptera: Braconidae).

Improvements in the mass rearing of Diachasmimorpha longicaudata (Ashmead) on larvae of the Vienna-8 temperature-sensitive lethal genetic sexing strain of Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) (= GSS Vienna-8) at the San Juan biofactory, Argentina, are currently under way. Lowering cost production is a key factor regarding parasitoid rearing. Thus, the variation in mass-reared parasitoid encapsulation levels and the incidence of superparasitism were determined; also, the gamma radiation dose-effect relation on host larvae and the influence of Mediterranean fruit fly strain were considered. Naked Mediterranean fruit fly larvae of both GSS Vienna-8 and a wild bisexual strain (= WBS) aged 6-d-old were irradiated at 0, 20, 40, 60, 80, 100, and 120 Gy, and exposed to parasitoid females. Melanization level was tested for encapsulated parasitoid larval first-instars (= L1). Non-irradiated and irradiated WBS larvae at 20-40 Gy displayed a significantly higher incidence of encapsulation when compared with GSS Vienna-8 larvae. The low melanized level in encapsulated parasitoid L1 was the most common melanization process at 72 h puparium dissection. A high melanized level was only found in non-irradiated WBS larvae. Irradiated GSS Vienna-8 larvae can neutralize the host immunological reactions over irradiated WBS larvae much more quickly. Superparasitism intensity in both Mediterranean fruit fly strains was not affected by radiation doses. High levels of superparasitism seemingly helped to overcome the host's immune reaction by the surviving parasitoid larva. Parasitoid emergence increased from 60 Gy onwards in both Mediterranean fruit fly strains. Radiation in GSS Vienna-8 larvae may favor host's antagonistic reactions decrease in relation with D. longicaudata development.