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Performance of Two Fruit Fly (Diptera: Tephritidae) Pupal Parasitoids (Coptera Haywardi [Hymenoptera: Diapriidae] and Pachycrepo

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Performance of Two Fruit Fly (Diptera: Tephritidae) Pupal Parasitoids (Coptera Haywardi [Hymenoptera: Diapriidae] and Pachycrepo Biological Control 23, 219–227 (2002) doi:10.1006/bcon.2001.1011, available online at http://www.idealibrary.com on Performance of Two Fruit Fly (Diptera: Tephritidae) Pupal Parasitoids (Coptera haywardi [Hymenoptera: Diapriidae] and Pachycrepoideus vindemiae [Hymenoptera: Pteromalidae]) under Different Environmental Soil Conditions Larissa Guille´n,* Martı´n Aluja,*,1 Miguel Equihua,* and John Sivinski† *Instituto de Ecologı´a, A.C., Apartado Postal 63, CP 91000 Xalapa, Veracruz, Mexico; and †Center for Medical, Agricultural, and Veterinary Entomology, USDA-ARS, 1600/1700 SW 23rd Drive, Gainesville, Florida 32608 Received October 12, 2000; accepted October 28, 2001 with larval–pupal parasitoids (Wharton, 1989; Sivin- We evaluated the performance of Coptera haywardi ski, 1996). Parasitoid species such as Diachasmimor- (Ogloblin) (Diapriidae) and Pachycrepoideus vin- pha tryoni (Cameron) and D. longicaudata (Ashmead) demiae (Rondani) (Pteromalidae), both hymenopteran (Hymenoptera: Braconidae) have been mass-released pupal parasitoids of Anastrepha spp. (Diptera: Te- to suppress populations of Mediterranean fruit flies phritidae). Performance was studied by manipulating (Wong et al., 1991, 1992) and Caribbean fruit flies the following environmental conditions in the labora- (Sivinski et al., 1996), respectively. Currently, alterna- tory: (1) soil type, (2) soil moisture content, (3) soil compaction, and (4) depth at which pupae were buried tive parasitoid species are being considered as addi- in the soil. There were two experiments: in the first, tions to the typical mass-releases of larval–pupal bra- exposure time of pupae was held constant and in the conids for the control of the Mediterranean fruit fly second, it varied. In the first experiment, C. haywardi (Medfly), Ceratitis capitata (Wiedemann), in Mexico was significantly more effective than P. vindemiae in and Central America. If combined mass-releases of egg parasitizing fly pupae. With exposure time held con- (e.g., Fopius arisanus (Sonan) (Hymenoptera: Bra- stant (36 h), only soil type and pupal burial depth were conidae), larval–pupal, and particularly pupal parasi- significantly related to parasitism rates. While P. vin- toids were attempted, it is possible that flies escaping demiae only parasitized pupae located on the soil sur- one form of natural enemy may sucumb to the other face, C. haywardi attacked pupae that were buried up (Sivinski, 1996). to 5 cm deep, performing better in clayey than in Many hymenopterous parasitoids of fruit fly pupae, loamy soil. In the second experiment, exposure time despite being described early in the 20th century (Sil- (24, 36, 48, and 72 h) had no significant effect on para- vestri, 1914), have received little subsequent attention. sitism rates, but soil type did. P. vindemiae again only For example, Dirhinus giffardii Silvestri (Chalcididae), attacked pupae on the soil surface while C. haywardi Coptera silvestri (Kieffer) (Diapriidae), Muscidifurax was also able to parasitize pupae that were buried up vorax Girault (Pteromalidae), and Pachycrepoideus to 5 cm deep. We conclude that C. haywardi represents vindemiae (Rondani) (Pteromalidae) were introduced a viable candidate to replace the environmentally un- from Africa and India to the Hawaiian Islands friendly P. vindemiae in augmentative biological con- (Clausen, 1978), but their effect on fruit fly populations trol programs against fruit flies. © 2002 Elsevier Science (USA) Key Words: Coptera haywardi; Pachycrepoideus vin- has never been seriously evaluated. demiae; pupal burial depth; Tephritidae; parasitoids; Based on the paucity of information on the role of biological control; soil type. pupal parasitoids in fruit fly ecology and control, our aim in this study was to compare parasitism rates in a native (Coptera haywardi (Ogloblin), Hymenoptera: INTRODUCTION Diapriidae) and an exotic (P. vindemiae, Hymenoptera: Pteromalidae) parasitoid species known to attack fly Augmentative biological control of fruit flies pupae. In an attempt to render the comparison as (Diptera: Tephritidae) has generally been attempted robust and meaningful as possible from an applied and biological point of view, we evaluated the following 1 To whom correspondence should be addressed. Fax: ϩ 52-228- factors under controlled experimental conditions: (1) 121897. E-mail: [email protected]. environmental soil conditions (soil type, soil moisture 219 1049-9644/02 $35.00 © 2002 Elsevier Science (USA) All rights reserved. 220 GUILLE´ NETAL. content, and soil compaction), (2) burial depths in the that included sources of water and honey. Tempera- soil where fly pupae were encountered, and (3) expo- ture, relative humidity (R.H.), and light regimes in the sure time of parasitoids to pupae. laboratory were 27 Ϯ 1°C, 60%, and 12:12 (L:D) h, C. haywardi, an endoparasitoid apparently found respectively. throughout Latin America (Ovruski et al., 2000), is a specialist species restricted to tephritid pupae such as Soil Characteristics Tested Anastrepha striata (Schiner), A. fraterculus (Wiede- Sandy, clayey, and loamy soils collected (respec- mann), and A. ludens (Loew) (Sivinski et al., 1998; tively) in Jalcomulco, Tejer´ıa, and Xalapa, Veracruz Lo´pez et al., 1999). Recently, Baeza-Larios et al. (2002) were tested. Each soil sample was classified by texture, also documented successful parasitization of the noto- according to the methods of Bouyoucos (1962), and rious pest C. capitata under seminatural conditions. In then sifted and autoclaved before being used. Soil pH contrast, P. vindemiae is a generalist ectoparasitoid values were 6.1, 5.6, and 5.6 for Jalcomulco, Tejer´ıa, attacking many species of cycloraphous flies across and Xalapa (sand, clay, and loam), respectively. Each numerous families and subfamilies, such as Phormia soil type was tested at four moisture levels and under regina (Meigen) (Calliphoridae: Chrysomyinae), Calli- two compaction states. Moisture levels corresponded to phora sp. (Calliphoridae: Calliphorinae), Piophila casei 30, 50, 70, and 90% saturation and soil compaction (L.) (Piophilidae), Musca domestica (L.) (Muscidae: 3 states were either 1 or 0 g/cm (i.e., uncompacted). To Muscinae), Stomoxys calcitrans (L.), Haematobia irri- obtain the required moisture levels, first we placed a tans (both Muscidae: Stomoxynae), Fannia canicularis 900-cc soil sample, previously maintained at 30% rel- (L.), F. scalaris (Fabricius) (Muscidae: Fanniinae), and ative humidity, in a 1-L plastic container and then Drosophila melanogaster Meigen (Drosophilidae: Dros- added water until the desired humidity level was ophilinae) (Crandell, 1939; Nostvik, 1954; Rueda and achieved. Moisture content was measured with a po- Axtell, 1985a,b,c). It has also been reported parasitiz- tentiometer (Kelway Soil Tester, Type-36). ing the following fruit fly species (Tephritidae): C. capi- tata, Rhagoletis indifferens Curran, R. fausta (Osten Experimental Protocol Sacken), A. ludens, and A. suspensa (Loew) (Jime´nez- Jime´nez, 1967; Clausen, 1978; Rueda and Axtell, We performed two sets of experiments. In the first, 1985a; Burditt and White, 1987). P. vindemiae was we determined how parasitism rates by C. haywardi originally introduced to the American continent from and P. vindemiae were affected by soil type, soil mois- Hawaii in 1955 (Clausen, 1978; Ovruski et al., 2000) ture content, degree of soil compaction, and depth in and into Mexico from Costa Rica in 1967 (Jime´nez- the soil at which fly pupae were encountered (i.e., Jime´nez, 1967). In Costa Rica it was recently mass- burial depth). In the second, we assessed how soil type, released as a control measure against the Medfly (Ca- depth of pupa in the soil, and length of pupal exposure macho, 1992, 1998), raising concerns about the nega- to female parasitoids affected parasitism rates (per- tive impact that thousands of generalist parasitoids centage of pupae parasitized) in both species. could have on the local dipterous entomofauna. Experiment 1. The design of the first experiment was a 2 ϫ 3 ϫ 4 ϫ 2 ϫ 6 factorial arrangement of treatments as follows: two parasitoid species (C. hay- MATERIALS AND METHODS wardi and P. vindemiae), three soil types (clay, sand, and loam), four soil moisture contents (30, 50, 70, and Study Site 90%), two soil compaction states (compacted and un- Studies were carried out at the Instituto de Ecolog´ıa, compacted), and six burial depths of pupae within the A.C. in Xalapa, Veracruz, Mexico (19°31Ј N. latitude soil (0, 1, 2, 3, 5, and 7 cm). This means that there were and 96°54Ј W. longitude; 1440 m above sea level). 288 combinations of treatments. Given that there was Mean annual temperature and rainfall at this site are a set of 10 pupae for each combination (see below), a 19.9°C and 1515 mm, respectively. total of 2880 pupae were used. For this experiment we used 288 (144 per parasitoid species) 1-L plastic containers (11.4 cm upper diame- Study Insects ter; 9.35 cm lower diameter; 13 cm height) filled with Individuals of both C. haywardi and P. vindemiae moistened soil to a height of 3, 5, 7, 8, or 10 cm. used in this study were reared from a laboratory stock Subsequently, 10 A. ludens pupae (3 days old) were of A. ludens pupae. On the same day that adult para- placed in each container and immediately covered with sitoids emerged, both males and females were trans- soil to a constant level in all containers (10 cm). This ferred to 30 ϫ 30 ϫ 30-cm Plexiglas cages and fed on an meant, for example, that in the case of burial depth 7 ad libitum diet of water and honey. Twenty-four hours cm, pupae were placed at 3 cm from the bottom and before the experiment began, groups of five females (4 then covered with soil until reaching the 10-cm mark to 6 days old) were placed in 250-ml plastic containers in the container. In all cases, there were 3 cm of free PERFORMANCE OF C. haywardi AND P. vindemiae IN SOIL 221 space between the soil surface and the lid covering the fitted using the program Genstat 5 (Genstat Commit- container. Following this, soil was compacted in half of tee, 1995).
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