The Ability of Coptera Haywardi
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Biological Control 23, 213–218 (2002) doi:10.1006/bcon.2001.1010, available online at http://www.idealibrary.com on The Ability of Coptera haywardi (Ogloblin) (Hymenoptera: Diapriidae) to Locate and Attack the Pupae of the Mediterranean Fruit Fly, Ceratitis capitata (Wiedemann) (Diptera: Tephritidae), under Seminatural Conditions Gustavo Baeza-Larios,* John Sivinski,† Tim Holler,‡ and Martı´n Aluja§ *Programa Moscamed, Laboratorio La Aurora, Avenida Hincapie´ y 18 Calle Zona 13, Ciudad de Guatemala 01013, Guatemala; †USDA-ARS, Center for Medical, Agricultural, and Veterinary Entomology, P. O. Box 14565, Gainesville, Florida 32604; ‡USDA-APHIS, PPQ-PPPC, GaPPL, 1913 SW 34th St., Gainesville, Florida 32602; and §Instituto de Ecologia, A.C., Apartado Postal 63, Xalapa, Veracruz, Mexico Received October 12, 2000; accepted October 28, 2001 et al., 1996; Montoya et al., 2000). A pupal parasitoid In Latin America, the diapriid Coptera haywardi may be a useful addition to such releases, because (Ogloblin) attacks the pupae of tephritid fruit flies. insects that escape one form of natural enemy might be Anastrepha spp. are among its natural hosts, but in the vulnerable to another (Sivinski, 1996). Mixed mass- laboratory it also develops in the exotic Mediterra- releases of sterile male Mediterranean fruit flies, Cer- nean fruit fly, Ceratitis capitata (Wiedemann). Field atitis capitata (Wiedemann), braconid larval parasi- cage tests demonstrated that C. haywardi could locate toids, and the pteromalid pupal parasitoid Pachycrep- and parasitize Mediterranean fruit fly pupae under seminatural conditions as found in a Guatemalan cof- oideus vindemiae (Rondani) have been popular with fee plantation. A mean of 18.3% of the pupae buried Costa Rican agriculturalists (Camacho, 1992, 1998). artificially at depths of ϳ5 mm were parasitized by C. The role that the exotic P. vindemiae plays in control haywardi, while those buried at 15 mm suffered 3.2% remains to be demonstrated (see Guillen et al., 2001), parasitism. In a laboratory experiment, larvae that and it is possible that such a generalist species with an buried themselves to pupate were not significantly extremely broad host range may negatively impact more likely to be parasitized than artificially buried nontarget flies such as tachinid parasitoids and polli- pupae, although they may have left a physical or nators. chemical trail that betrayed their presence. Thus, the Coptera haywardi (Ogloblin) is a diapriid pupal artificial burial of pupae is unlikely to grossly under- parasitoid and one that has attractive qualities as a estimate C. haywardi efficacy in the field. Another biological control agent in augmentative release pro- field cage test found that mortality levels due to un- grams (Sivinski et al., 1998). First among these at- successful parasitoid attacks were similar to those re- tributes is its relative specificity. While most pupal sulting from successful parasitism. Thus, the actual parasitoids of Diptera are ectoparasitic generalists effect of a mass-release might be considerably greater (e.g., P. vindemiae), the endoparasitic C. haywardi de- than that suggested from parasitism data alone. The results are considered sufficiently positive to encour- velops only in Tephritidae (Sivinski et al., 1998). To age further testing of C. haywardi as a biological con- date, the outstanding difficulty facing its use in aug- mentation programs is its inability to develop in irra- trol agent of the Mediterranean fruit fly. © 2002 Elsevier Science (USA) diated hosts (Menezes et al., 1998). Host irradiation is Key Words: medfly; biological control; augmentative a means of eliminating unparasitized flies in many, release; pupal parasitoid; integrated pest manage- although not all, fruit fly parasitoid mass-rearing sys- ment. tems (e.g., Sivinski et al., 1996). C. haywardi has been collected from southern Mex- ico through much of South America (Ovruski et al., INTRODUCTION 2000). Across its range, it attacks the pupae of native Anastrepha spp. resulting from the larvae that develop Augmentative releases of braconid larval–pupal in a number of native and introduced fruits (e.g., Lopez parasitoids have suppressed populations of various te- et al., 1999). In the laboratory it develops in the Med- phritid fruit fly pests (e.g., Wong et al., 1991; Sivinski iterranean fruit fly (Sivinski et al., 1998), a species 213 1049-9644/02 $35.00 © 2002 Elsevier Science (USA) All rights reserved. 214 BAEZA-LARIOS ET AL. introduced into the New World during historical times Laboratory Comparison of Parasitism in Artificially (e.g., Gilstrap and Hart, 1987 and citations). To pursue Buried and Self-Buried Pupae the possibility of augmentative releases of C. haywardi to suppress Mediterranean fruit fly populations in Cen- To determine whether burrowing larvae leave phys- tral America and elsewhere, it is first necessary to ical or chemical trails that might be exploited by for- demonstrate its capacity to locate and parasitize host aging C. haywardi, moistened soil was placed in 400-ml plastic cups to a depth of 10 mm. In 10 such pupae under natural conditions, particularly under the Ͼ conditions prevailing in coffee plantations, the prin- cups, 25 2-day-old Mediterranean fruit fly pupae cipal source of Mediterranean fruit flies in Latin were placed at the 5 mm level and then buried under 5 America. mm of soil. On the previous day, in a second set of 10 Here we report on a test of the capacity of field-caged cups, 25 late instar larvae were placed on the surface of C. haywardi to attack Mediterranean fruit fly pupae the soil and allowed to bury themselves and pupate. artificially buried at two different depths. The field This schedule ensured that the artificially buried and cages were located in a coffee plantation in the volcanic self-buried pupae were of the same age. On the follow- highlands of Guatemala, a region where augmentative ing day, 10 female C. haywardi adults were placed in braconid parasitoid releases have been employed in the the cups. Females were 5–10 days of age, had been recent past to suppress Mediterranean fruit fly popu- caged with males, and had been previously given ac- lations (e.g., Sivinski et al., 2000a), and where future cess to Mediterranean fruit fly pupae. Cups and insects were kept at ambient temperature (ϳ25°C) and rela- releases of C. haywardi might be reasonably contem- ϳ plated. Because Mediterranean fruit fly pupae in the tive humidity ( 65%). After 5 days, female parasitoids field cage were to be buried by hand, and because it is were removed, and the pupae from the top 5 mm of soil possible that larvae burrowing into the soil to pupate in the self-burial cups were separated from those occu- may leave a chemical or physical trail exploited by pying the bottom 5 mm. This insured that parasitism of foraging parasitoids, an experiment was performed in the artificially buried pupae could be compared to that the laboratory (MOSCAMED Laboratorio La Aurora, of self-buried pupae that had dwelt at least as deeply in Ciudad de Guatemala) to determine whether parasit- the soil and were similarly vulnerable to burrowing C. ism by C. haywardi of artificially buried pupae was haywardi. similar to that inflicted on self-buried pupae. Emergence of adult insects from the various cohorts (artificially buried at 5 mm, self-buried at Ͻ5 mm, and self-buried at Ͼ5 mm) was monitored for an additional MATERIALS AND METHODS 30 days. Adult insects were counted, and the mean ϩ Study Site percentage parasitism (adult parasitoids/[adult flies adult parasitoids]), mean Mediterranean fruit fly sur- Field cage tests on the ability of C. haywardi to vival (adult flies/total pupae, both surviving and non- parasitize Mediterranean fruit fly under seminatural surviving), and percentage parasitoid production conditions were carried out in Finca El Capetillo, ϳ12 (adult parasitoids/total pupae, both surviving and non- km SW of Antigua, Departamento Sacatepe´quez, Gua- surviving) of the artificially buried and the Ͼ5mm temala, at an altitude of 1388 m. C. haywardi is most self-buried cohorts were compared by Student t tests abundant at relatively high altitudes in nature, and following arcsine transformation of the square roots of along one altitudinal transect in Mexico it was found at the data (SAS Institute, 1988). The values for percent- 600–1000 m (Sivinski et al., 2000b). A hygrothermo- age parasitism and percentage parasitoid production graph, placed near the experimental site for the dura- differ because substantial numbers of puparia failed to tion of the tests, recorded temperatures ranging from 9 produce an adult insect of either species. Because this to 26°C and relative humidities from 38 to 98%. The mortality might have been due in part to unsuccessful vegetation in the vicinity consists for the most part of parasitoid attacks (examinations of puparia known to coffee bushes grown under various species of shade have been stung did not reveal recognizable oviposition trees. scars, so attacked but unparasitized pupae were diffi- cult to identify), means of both percentage parasitism Study Insects and percentage parasitoid production were analyzed. C. haywardi were from a colony initiated with indi- Field Cage Comparison of Parasitism of Pupae viduals collected in the vicinity of Xalapa, Veracruz, Buried at Different Depths Mexico and maintained for ϳ2 years (ϳ20 generations) at the MOSCAMED Aurora facility in Guatemala City. The comparison of parasitism of pupae buried at Mediterranean fruit flies were obtained at the different depths