Sergio M. Ovruski

Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the southern United States: Diversity, distribution, taxonomic status and their use in fruit fly biological control

We first discuss the diversity of fruit fly (Diptera: Tephritidae) parasitoids (Hymenoptera) of the Neotropics. Even though the emphasis is on Anastrepha parasitoids, we also review all the information available on parasitoids attacking flies in the genera Ceratitis, Rhagoletis, Rhagoletotrypeta, Toxotrypana and Zonosemata. We center our analysis in parasitoid guilds, parasitoid assemblage size and fly host profiles. We also discuss distribution patterns and the taxonomic status of all known Anastrepha parasitoids. We follow by providing a historical overview of biological control of pestiferous tephritids in Latin American and Florida (U.S.A.) and by analyzing the success or failure of classical and augmentative biological control programs implemented to date in these regions. We also discuss the lack of success of introductions of exotic fruit fly parasitoids in various Latin American countries. We finish by discussing the most pressing needs related to fruit fly biological control (classical, augmentative, and conservation modalities) in areas of the Neotropics where fruit fly populations severely restrict the development of commercial fruit growing. We also address the need for much more intensive research on the bioecology of native fruit fly parasitoids.

Colonization and domestication of seven species of native New World hymenopterous larval-prepupal and pupal fruit fly (Diptera: Tephritidae) parasitoids

Abstract We describe the techniques used to colonize and domesticate seven native New World species of hymenopterous parasitoids that attack flies within the genus Anastrepha (Diptera: Tephritidae). All parasitoid species successfully developed on artificially reared Mexican fruit fly, Anastrepha ludens (Loew) larvae or pupae. The parasitoid species colonized were the following: Doryctobracon areolatus (Szépligeti), Doryctobracon crawfordi (Viereck), Opius hirtus (Fischer), Utetes anastrephae (Viereck) (all Braconidae, Opiinae), Aganaspis pelleranoi (Bréthes) and Odontosema anastrephae Borgmeier (both Figitidae, Eucoilinae) (all larval-pupal parasitoids), and the pupal parasitoid Coptera haywardi (Ogloblin) (Diapriidae, Diapriinae). We provide detailed descriptions of the different rearing techniques used throughout the domestication process to help researchers elsewhere to colonize local parasitoids. We also describe handling procedures such as number of hosts in parasitization units and compare optimal host and female age, differences in parasitism rate, developmental time, life expectancy and variation in sex ratios in each parasitoid species over various generations. In the case of D. crawfordi and C. haywardi we also provide partial information on mass-rearing techniques such as cage type, parasitization unit, larval irradiation dose and adult handling.

Relative abundance of Ceratitis capitata and Anastrepha fraterculus (Diptera: Tephritidae) in diverse host species and localities of Argentina.

Abstract Two fruit fly species (Diptera: Tephritidae) of economic importance occur in Argentina, the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), and Anastrepha fraterculus (Wiedemann). Here, we compared the relative abundance of these fruit pests in 26 fruit species sampled from 62 localities of Argentina in regions where C. capitata and A. fraterculus coexist. In general, C. capitata was predominant over A. fraterculus (97.46% of the emerged adults were C. capitata), but not always. Using the number of emerged adults of each species, we calculated a relative abundance index (RAI) for each host in each locality. RAI is the abundance of C. capitata relative to the combined abundance of A. fraterculus and C. capitata. Some families of fruit species were more prone to show high (Rutaceae and Rosaceae) or low (Myrtaceae) RAI values, and also native plants showed lower RAI values than introduced plants. RAI showed high variation among host species in different localities, suggesting a differential use of these hosts by the two flies. There were localities where A. fraterculus was not found in spite of suitable temperature and the presence of hosts. Most host species showed little variation in RAI among localities, usually favoring C. capitata, but peach, grapefruit, and guava showed high variation. This suggests that these fruit species are suitable for both fruit flies but more favorable to one or the other, depending on local environmental conditions (e.g., relative humidity and degree of disturbance) of each locality.

Abundance of Anastrepha fraterculus (Diptera: Tephritidae) and Its Associated Native Parasitoids (Hymenoptera) in “Feral” Guavas Growing in the Endangered Northernmost Yungas Forests of Argentina with an Update on the Taxonomic Status of Opiine Parasitoids Previously Reported in This Country

Abstract We report the results of a 2-yr survey aimed at determining the identity and abundance of native parasitoids of fruit infesting tephritids attacking Psidium guajava L. (common guava) in the endangered northernmost Yungas forests of Argentina, which are being encroached by commercial citrus groves. The 3,200 guavas collected during the peak of the short guava fruiting period (February and March), yielded 10,701 Anastrepha fraterculus (Wiedemann) and Ceratitis capitata (Wiedemann) adults (97.4 and 2.6%, respectively) and 712 native parasitoids. The parasitoid species and proportion in the total sample during the 2-yr study period were as follows: Doryctobracon areolatus (Szépligeti), 37.9%; Doryctobracon brasiliensis (Szépligeti), 17.7%; Utetes anastrephae (Viereck), 1.1%; Opius bellus (Gahan), 0.7%; (all Braconidae, Opiinae), and Aganaspis pelleranoi (Brèthes), 32.6% (Figitidae, Eucoilinae). All parasitoids emerged from A. fraterculus pupae (i.e., none from C. capitata). The discovery of D. crawfordi represents the first report for Argentina and the southernmost record for the species. We discuss the practical implications of the role of guava as a reservoir for A. fraterculus and the implications for the biological control of both fruit flies. We also update the taxonomic status of the opiine parasitoids of A. fraterculus in Argentina given that a number of species previously reported in the literature had never been formally described (i.e., represent nomina nuda) or had been misidentified.

Host Preference by Diachasmimorpha longicaudata (Hymneoptera: Braconidae) Reared on Larvae of Anastrepha fraterculus and Ceratitis capitata (Diptera: Tephritidae)

ABSTRACT The preferences of Diachasmimorpha longicaudata (Ashmead) for larvae of Anastrepha fraterculus (Wiedemann) and Ceratitis capitata (Wiedemann) were evaluated under laboratory conditions in no-choice and dual-choice tests, based on percent parasitism, proportion of emerged parasitoids, proportion of female offspring, and number of parasitoid female visits to and ovipositor probes on the artificial oviposition device as different measures of host preference. In no-choice tests D. longicaudata females did not demonstrate a significant preference between C. capitata and A. fraterculus larvae. Nevertheless, D. longicaudata females showed a strong preference for A. fraterculus larvae in dual-choice test. Although female biased parasitoid progeny resulted in all assays, significantly more D. longicaudata female offspring emerged from A. fraterculus pupae than from C. capitata pupae. Thus, this study confirmed that both C. capitata and A. fraterculus are appropriate host for rearing D. longicaudata, but also provided evidence that female parasitoid progeny yield can be substantially improved by using A. fraterculus larvae as the host instead of C. capitata larvae.

THE ESTABLISHMENT OF DIACHASMIMORPHA LONGICAUDATA (HYMENOPTERA: BRACONIDAE) IN MISIONES, NORTHEASTERN ARGENTINA

Diachasmimorpha longicaudata originated from the Indo-Pacific region, has been widely disseminated into America via Hawaii, and can be considered successfully established in most of the importing countries, such as Colombia, Costa Rica, Guatemala, El Salvador, Mexico, Nicaragua, Trinidad, United States of America (Florida), Venezuela (Ovruski et al. 2000), and Brazil (Carvalho & Nascimento 2002). This exotic parasitoid species is the most widely employed parasitoid now in use for augmentative biocontrol programs against fruit flies in Latin America and the southern United States, primarily because it is easily mass-rearing and it adapts readily to different fruit fly species of economic importance such as Anastrepha fraterculus , A. suspensa (Loew), A. ludens (Loew), A. obliqua (Macquart), A. striata Schiner, A. serpentina (Wiedemann) and Ceratitis capitata (Sivinski 1996), (Ovruski et al. 2000). Interestingly, D. longicaudata is a common parasitoid species of Anastrepha larvae particularly in exotic commercial fruit in the state of Veracruz, México (López et al. 1999), and it may enter a dry season diapause (Aluja et al. 1998). In 1961, Argentina’s Ministry of Agriculture and Cattle, together with the National Institute of Agricultural Technology (INTA), introduced the braconid parasitoid of fruit flies D. longicaudata to the country from Mexico. This biological control program was a direct response to the establishment of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann), in Argentina However, the effort also hoped to control A. fraterculus , The South American fruit fly, in several citrus-growing areas where both tephritid species coexisted in wild and commercial fruit. Diachasmimorpha longicaudata was released in 100,000 in the 1960s in the northeastern provinces of Misiones (Montecarlo county) and Entre Rios (Concordia county), in the northwestern provinces of Tucumán (San Miguel de Tucumán city) and Jujuy (Calilegua county) and the central province of Córdoba (Cruz del Eje and Yacanto counties) Turica (1968). New releases of D. longicaudata were made in citrus orchards in the Tucumán province in 1977 and 1986 (Ovruski & Fidalgo 1994). As noted by (Ovruski et al. 1999), D. longicaudata was recovered immediately following release in all sites. However, until now, there was no evidence of permanent establishment in any release site. Recent fruit fly parasitoid surveys made in Montecarlo county (Misiones province) included specimens of D. longicaudata . The first record of this species was in March 2000 attacking A. fraterculus larvae from Feijoa sellowiana L. (Myrtaceae), and it was subsequently found in February and March 2001 and April 2002 (all collection data are listed at the end of the paper), so that D. longicaudata was recovered approximately 40 years after its first release in Argentina. Thus this exotic parasitoid has become established in at least one province of Argentina, albeit in small numbers( ≈ 1% parasitism). Fruit flies and parasitoids were identified to species by the authors using Zucchi’s (2000) and Wharton and Gilstrap’s (1983) taxonomic keys, respectively. Voucher specimens were deposited in the Fundación Miguel Lillo (FML) entomological collection in San Miguel de Tucumán, Argentina.

Biological Control of Tephritid Fruit Flies in Argentina: Historical Review, Current Status, and Future Trends for Developing a Parasitoid Mass-Release Program

In Argentina there are two tephritid fruit fly species of major economic and quarantine importance: the exotic Ceratitis capitata that originated from Southeast Africa and the native Anastrepha fraterculus. In recent years, the use of fruit fly parasitoids as biocontrol agents has received renewed attention. This increasing interest has recently led to the establishment of a program for the mass rearing of five million Diachasmimorpha longicaudata parasitoids per week in the BioPlanta San Juan facility, San Juan, Argentina. The first augmentative releases of D. longicaudata in Argentina are currently occurring on commercial fig crops in rural areas of San Juan as part of an integrated fruit fly management program on an area-wide basis. In this context, research is ongoing to assess the suitability of indigenous parasitoid species for successful mass rearing on larvae of either C. capitata or A. fraterculus. The purpose of this article is to provide a historical overview of the biological control of the fruit fly in Argentina, report on the strategies currently used in Argentina, present information on native parasitoids as potential biocontrol agents, and discuss the establishment of a long-term fruit fly biological control program, including augmentative and conservation modalities, in Argentina’s various fruit growing regions.

Response of the fruit fly parasitoid Diachasmimorpha longicaudata to host and host-habitat volatile cues

Chemical information is crucial to insect parasitoids for successful host location. Here, we evaluated the innate response of Diachasmimorpha longicaudata (Ashmead) (Hymenoptera: Braconidae), a fruit fly larval parasitoid, to cues from host and host habitat (i.e., fruit infested with host larvae). We first assessed the preference of female parasitoids between oranges infested with Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) and non‐infested fruit. Females were highly attracted towards infested oranges on the basis of volatile chemical cues. After this initial experiment, we aimed at revealing the potential sources of volatile cues present in an infested fruit. To this end, we considered five potential sources: (1) punctured fruit; (2) fly feeding, frass, or host‐marking pheromone deposited on the orange surface; (3) larval activity inside the fruit; (4) the larvae themselves; and (5) fungi associated with infestation of oranges. Habitat cues associated with host activity and those produced by rotten oranges or oranges colonized by fungi were highly attractive for female wasps, whereas odours associated with the activity of the adults on the surface of the fruit, and those released by the fruit after being damaged (as happens during fruit fly egg‐laying) were not used as cues by female parasitoids. Once the female had landed on the fruit, direct cues associated with larval activity became important although some indirect signals (e.g., products derived from larval activity inside the fruit) also increased host searching activity. Our findings indicate that naïve D. longicaudata uses chemical cues during host habitat searching and that these cues are produced both by the habitat and by the host larvae.

PRESENCE OF DIACHASMIMORPHA LONGICAUDATA (HYMENOPTERA: BRACONIDAE) IN A GUILD OF PARASITOIDS ATTACKING ANASTREPHA FRATERCULUS (DIPTERA: TEPHRITIDAE) IN NORTHWESTERN ARGENTINA

Fil: Orono, Luis Eduardo. Consejo Nacional de Investigaciones Cientificas y Tecnicas. Centro Cientifico Tecnologico Conicet - Tucuman. Planta Piloto de Procesos Industriales Microbiologicos; Argentina

Aganaspis alujai (Hymenoptera: Figitidae: Eucoilinae), a New Species Attacking Rhagoletis (Diptera: Tephritidae) in the Neotropical Region

Abstract A new neotropical species of Aganaspis (Hymenoptera: Figitidae, Eucoilinae) is described and compared to other Aganaspis species occurring in the Neotropical Region. This thelytokous species was reared from pupae of 2 species of fruit flies in the genus Rhagoletis (Diptera: Tephritidae), both in the suavis species group, and collected from 2 species of native walnuts in Mexico. Evidence of host specialization through diapause timing and notes on basic biology are provided.