Biological Control 15, 119–129 (1999) Article ID bcon.1999.0711, available online at http://www.idealibrary.com on Hymenopterous Larval–Pupal and Pupal Parasitoids of Anastrepha Flies (Diptera: Tephritidae) in Mexico M. Lo´pez,* M. Aluja,*,1 and J. Sivinski† *Instituto de Ecologia, A.C., Apartado Postal 63, 91000 Xalapa, Veracruz, Mexico; and †Insect Attractants, Behavior and Basic Biology Research Laboratory, USDA–ARS, 1700 SW 23rd Drive, P.O. Box 14565, Gainesville, Florida 32604 Received February 20, 1998; accepted January 26, 1999 previous surveys carried out in Mexico and in Central We surveyed 15 wild and cultivated plant species in and South America. We also discuss the need to protect search of fruit fly (Diptera: Tephritidae) parasitoids native vegetation because of the important role such during 4 years (1993–1996) in the state of Veracruz, vegetation plays as reservoirs of fruit fly parasitoids. Mexico. The following species were infested by Anastre- ௠ 1999 Academic Press pha larvae: Spondias purpurea L., S. mombin L., Ta- Key Words: Anastrepha; Tephritidae; parasitoids; Do- pirira mexicana Marchand, Mangifera indica L. (all ryctobracon; Utetes; Opius; Aganaspis; Odontosema; Anacardiaceae), Ximenia americana L. (Olacaceae), Coptera; Diachasmimorpha; Aceratoneuromyia; Pachy- Citrus sinensis L. and Casimiroa edulis Llave & Lex. crepoideus. (Rutaceae), Psidium guajava L., P. sartorianum (Berg.), P. guineense Sw., Syzygium jambos L., Myrciaria flori- bunda (West) O. Berg. (all Myrtaceae), Chrysophyllum INTRODUCTION mexicanum (Brandegce) ex. Standley and Calocarpum mammosum L. (Sapotaceae), and Passiflora foetida L. Flies in the genus Anastrepha Schiner are found from (Passifloraceae). Of these, only C. mexicanum, C. edu- the southern United States to northern Argentina lis, and P. foetida did not harbor parasitoids. We identi- (Herna´ndez-Ortı´z and Aluja, 1993). Of the 187 reported fied 10 native and exotic larval–pupal parasitoid spe- species, 7 stand out because of their status as impor- cies (all Hymenoptera): Doryctobracon areolatus tant pests: Anastrepha fraterculus (Wiedemann), An- (Sze´pligeti), D. crawfordi (Viereck), Utetes (Bracan- astrepha grandis (Macquart), Anastrepha ludens astrepha) anastrephae (Viereck), and Opius hirtus (Fisher) (all Braconidae), Aganaspis pellenaroi (Loew), Anastrepha obliqua (Macquart), Anastrepha (Brethes) and Odontosema anastrephae Borgmeier (Eu- serpentina (Wiedemann), Anastrepha striata (Schiner), coilidae) (all native species), and Diachasmimorpha and Anastrepha suspensa (Loew) (Aluja, 1994). Histori- longicaudata (Ashmead) and Aceratoneuromyia in- cally, there has been heavy reliance on insecticidal bait dica (Silvestri) (Braconidae and Eulophidae, respec- sprays to control these flies (Aluja, 1993, 1996). Never- tively; both exotic species). We also identified two theless, some attempts to also apply classical or augmen- pupal parasitoids: Coptera haywardi (Ogloblin) (Diapri- tative biological control strategies have been made idae; native) and Pachycrepoideus vindemiae (Ron- (Wharton, 1989; Sivinski, 1996). The most common dani) (Pteromalidae; exotic). Parasitization levels approach has been to release exotic egg, larval–pupal, ranged between 0.4 and 83.8%. Native, wild plants or pupal parasitoids. For example, in Mexico Fopius harbored significantly more parasitoids per fruit than arisanus Sonan (reported as Opius oophilus Fullaway), cultivated ones. Interestingly, in P. guajava 2 fly spe- Opius novocaledonicus Fullaway, Opius formosanus cies and 5 parasitoid species were once identified in a Fullaway, Opius taiensis Fullaway, Opius vandenbos- single fruit. We found a negative correlation between chi Fullaway, Diachasmimorpha longicaudata (Ash- fruit size and number of parasitoids/fruit. We rank mead) (reported as Opius compensans Silvestri), Acera- parasitoids based on host breadth (fruit fly species toneuromyia indica (Silvestri) (Eulophidae) (reported attacked) and number of plant species visited. We as Syntomosphyrum), Dirhinus giffardi Silvestri, and discuss some general ecological and practical implica- Pachycrepoideus vindemiae (Rondani) (Pteromalidae) tions of our findings (e.g., effect of fruit size on parasit- were repeatedly released in the late 1950’s and early ism, mass-rearing, and augmentative releases of native 1960’s (Jime´nez-Jime´nez, 1956, 1958, 1967). Strikingly, vs exotic parasitoids) and compare our findings with in these classical biological control programs, little attention was paid to native parasitoids. More recently, 1 To whom correspondence should be addressed. exotic parasitoids were mass-released in an attempt to 119 1049-9644/99 $30.00 Copyright ௠ 1999 by Academic Press All rights of reproduction in any form reserved. 120 LO´ PEZ, ALUJA, AND SIVINSKI suppress Anastrepha populations on an area-wide ba- Climate is defined as Aw1(wЉ)(iЈ)g (intermediate warm- sis. This is illustrated by a recent study in Key Bis- subhumid) (Garcı´a, 1973), with a mean annual tempera- cayne and Clewiston, Florida, using the braconid larval– ture of 25°C and 1250 mm rainfall, mostly during the pupal parasitoid D. longicaudata (Sivinski et al., 1996). summer to early autumn rainy season. Occasional light The study of native Anastrepha parasitoids has a rains also fall during winter months. Llano Grande long history and began in Mexico. De la Barrera (cited (19°22Ј N, 96°53Ј W, elevation 950 m) has a climate by Herrera, 1905), McPhail and Bliss (1933), Darby and defined as (A)C(m)aig (semi-warm, humid) (Garcı´a, Knapp (1934), and Stone et al. (1965), collecting natu- 1973), with mean annual temperature of 25°C and 1250 ral enemies in various regions of Mexico, identified mm rainfall and with a summer rainy season. Tejerı´a Doryctobracon (ϭOpius) crawfordi (Viereck), Coptera (19°22Ј N, 96°56Ј W) is at an elevation of 1000 m. sp. (ϭGalesus sp.), Aganaspis sp. (ϭEucoila), and the Climate is defined as (A)C(fm)a (semi-warm, humid) bombylid fly Anthrax scylla Oster Sacken. Doryctobra- (Garcı´a, 1973), with a mean annual temperature of con crawfordi (reported as Diachasma crawfordi) was 21°C and 1600 mm rainfall. There is no distinct rainy also reported in Costa Rica by Picado (1920). More season. Monte Blanco (19°23Ј N, 96°56Ј W) is at an recently, systematic surveys on native Anastrepha para- elevation of 1050 m. Climate is defined as (A)C(m) sitoids were carried out in the United States (Florida) (wЉ)big (semi-warm, humid) (Garcı´a, 1973), with mean (Baranowski et al., 1993), Mexico (Nuevo Leo´n, Vera- annual temperature of 20°C and 1750 mm rainfall and cruz, Chiapas) (Gonza´lez-Herna´ndez and Tejada, 1979; with a summer rainy season. All material collected in Aluja et al., 1990; Piedra et al., 1993; Herna´ndez-Ortı´z the field was processed in Xalapa, Veracruz. Xalapa et al., 1994), Guatemala (Eskafi, 1990), Costa Rica (19°31Ј N, 96°54Ј W) is at an elevation of 1440 m. (Wharton et al., 1981; Jiro´n and Mexzon, 1989), Colom- Parasitoid collection and processing. We surveyed bia (Ye´pes and Ve´lez, 1989), Venezuela (Katiyar et al., parasitoids (1) in tree canopies and (2) at ground level. 1995), Brasil (Costa Lima, 1937; Nascimento et al., 1979; De Santis, 1980; Arrigoni, 1984; Aguiar et al., Survey of parasitoids in tree canopies. The fruit tree 1992; Canal et al., 1994, 1995; Leonel et al., 1995; species surveyed are summarized in Table 1. Only fruit Araujo et al., 1996), and Argentina (Turica and Mallo, that was about to fall from the tree was harvested. This 1961; Nasca, 1973; Ferna´ndez-de-Araoz and Nasca, allowed larvae to complete development and gave fruit 1984; Dı´az, 1986; Ovruski, 1995). Several points rel- fly parasitoids the opportunity to parasitize larvae evant to the work described here stand out from these throughout their development. To collect fruit, we used studies: (1) Doryctobracon areolatus (Sze´pligeti) is by a ladder or climbed the tree. A plastic basket attached far the most abundant and widespread native parasi- to a wooden pole (to reach all fruit) was placed beneath toid of Anastrepha (its range extends from central the fruit and the branch gently shaken. In this manner Florida to northern Argentina). (2) There is no report of only fruit that abscised naturally after the branch a native Anastrepha egg parasitoid. (3) Pupal parasi- shaking procedure were collected. With the exception of toids are poorly represented in samples probably be- Syzygium jambos L., Psidium guineense Sw., Myrciaria cause of the collection techniques used. (4) Most parasi- floribunda (West) O. Berg. (Myrtaceae), Calocarpum toid species are generalists (i.e., they attack many mammosum L., Chrysophyllum mexicanum (Brand- Anastrepha species). (5) Many native species are found egce) ex. Standley (Sapotaceae), Casimiroa edulis Llave preferentially parasitizing Anastrepha larvae in na- & Lex. (Rutaceae), and Passiflora foetida L. (Passiflora- tive, wild fruit species. ceae), which were in very short supply, all fruit were Our aim here was to systematically survey native placed individually in plastic containers into which and exotic plants in crop fields and large and small vermiculite or a mixture of sand and soil had been patches of native vegetation adjacent to crops and to previously added (pupation medium for larvae). A hole identify all larval–pupal and pupal fruit fly parasitoids was cut in the middle of the lid of each plastic container present in a region where fruit growing is an important and then covered with organdy for ventilation. If, agricultural activity. Detailed information