Nancy S. Carrejo and Ranulfo González O.

Universidad del Valle
Dpto. de Biología, Sección de Entomología
A. A. 25360. Cali, Colombia

Abstract

Parasitoids associated with 8 species of Anastrepha were recovered from host fruits that belonged to 9 species of plants in the Cauca Valley, Colombia. These parasitoids were identified and quantified. The most common parasitoid was Doryctobracon zeteki, which was associated with the species A. leptozona, A. serpentina, A. nunezae and A. striata recovered from Pouteria caimito, Chrysophyllum cainito and Campomanesia lineatifolia host fruits.

Key Words: Anastrepha, Doryctobracon, parasitoids, Valle del Cauca, Colombia

Resumen

Se identificaron y cuantificaron las especies de parasitoides asociadas a 8 especies de Anastrepha obtenidas de frutos pertenecientes a 9 especies de plantas del Valle del Cauca, Colombia. Doryctobracon zeteki fue la especie de parasitoide más frecuente y estuvo asociada a las especies A. leptozona, A. serpentina, A. nunezae y A. striata obtenidas de los frutos de Pouteria caimito, Chrysophyllum cainito y Campomanesia lineatifolia.

Knowledge of fruit fly natural enemies is of vital importance for biological control programs. Some programs have failed because of the absence of basic information in taxonomic, morphologic and biologic aspects of the parasitoids (Wharton 1989 in Canal-Daza et al. 1994).

Studies have been done in many countries of the New World on whether to make inventories of native parasitoids or to evaluate only the introduced ones. In Mexico Aluja et al. (1990) recorded fruits parasitized by fruit flies, especially by A. ludens (Loew), A. obliqua (Macquart), A. striata Shiner and A. serpentina (Weidemann). In these cases the most common parasitoid was Diachasmimorpha longicaudata (Ashmead). Jirón & Mexzon (1989) recognized 8 species of parasitoids from the 11% of fruits that were infested with 5 species of Anastrepha in 135 locations in Costa Rica. In Brazil, Canal-Daza et al. (1994) obtained 3 families of parasitoids (Braconidae, Eucoilidae and Pteromalidae) from samples of 11 species of fruit trees where Anastrepha species were developed; 93% of them belonged to Braconidae.

Some contributions have been made in Colombia. Olarte (1980) reported Psidium guajava L. attacked by A. striata, which was attacked by Utetes (Bracanastrepha) anastrephae (Viereck). Portilla et al. (1993) identified 3 species of parasitoids; Doryctobracon. crawfordi (Viereck), O. anastrephae, and Microscapis sp.; apparently associated with Ceratitis capitata (Wiedemann) and A. fraterculus in Coffea arabica L. in the Department of Nariño (Colombia). The inventory of parasitoids of fruit flies used in biological control includes 82 species, of which the majority were braconids (Wharton 1989).

It has been possible to colonize and mass-rear some parasitoid species; this has permitted introduction and release in other countries to reduce Anastrepha populations. Species like Diachasmimorpha longicaudata, Doryctobracon crawfordi, Ganaspis pelleranoi (Brethes), Biosteres giffardi (Silvestri), B. vandenboschi (Fullaway) and Aceratoneuromyia indica (Silvestri) have been imported and released in the U.S.A., Mexico, Costa Rica, Brazil, Peru and Argentina to control Anastrepha suspensa (Loew), A. ludens and A. fraterculus. Of these, D. longicaudata and D. crawfordi have established in many countries of America (Aluja 1994).

In Florida (U.S.A.), 15 parasitoid species (representing 4 families) have been imported to control the Caribbean fruit fly (A. suspensa). These parasitoids coexist with generalist native species that also attack this fly. In this case, Diachasmimorpha longicaudata released, most frequently especially during the periods when A. suspensa populations decreased because of host absence (Baranowski et al. 1993).

During a project directed to determine the diversity of species of Anastrepha in some localities of the Department of Valle del Cauca, 26 species of Anastrepha were recovered from different host plants and also caught in McPhail traps. Also, in this manuscript the results about the Anastrepha parasitoids found in fruits are presented.

Materials and Methods

Study Area

Many fruits were collected from about 13 municipalities of the Department of Valle del Cauca, but only the samples obtained from the municipalities of Buenaventura, Jamundí, La Cumbre and Yumbo were considered in this study, in which at least one parasitoid was recovered besides the Anastrepha fruit fly.

Collection of Parasitoids

Fruit were collected in plastic, 15 × 12 cm containers that held a mixture of humid sawdust and sieved river sand that had been sterilized. Each container was covered with white muslin and held at a temperature of + 24°C and 70% R. H. The pupae that were formed were removed and transferred to emergence containers that had the same mixture. When the imagos of Anastrepha and parasitoids were obtained the mixture in the container was sieved to quantify the number of larvase the number of pupae viable, that formed parasitoids. The parasitization calculation was based on the number of adult flies produced and not on the number of larvae, due to high mortality different from parasitism.

All emerged flies and parasitoids were maintained in vials filled with 70% alcohol until identified. The Anastrepha species were identified with the authors’ knowledge and the literature available. Some determinations of parasitoids were made by P.M. Marsh and A.S. Menke (Systematic Entomology Laboratory of USDA). Phaenocarpa sp. (Braconidae) was identified by Dr. R. A. Wharton (Dept. of Entomology, Texas A & M. University, College Station). Percent of parasitism was calculated following the formula of Baranowski et al. (1993), number of parasitoids emerged/number of parasitoids + number of flies × 100. When more than one parasitoid specimen/pupae was obtained, only one was considered because the formula implies that when parasitism occurs, each parasitoid will replace a pupa; this is not valid for all species that parasitize Anastrepha fruit flies.

The specimens were deposited in the Museum of Entomology at the Universidad del Valle (Department of Biology, Cali-Colombia).

Results and Discussion

From 447 different fruits we obtained 1759 Anastrepha flies and 204 parasitic larvae (Table 1). Anastrepha was not recovered from 10 of the plant species. From Garcinia madruno (Kunth) Hammel, Inga spp., Spondias purpurea L., Averrhoa carambola L., Coffea arabica and Sysigium malaccense (L) flies were produced but no parasitoids.

No correlation was observed between number of flies per fruit host and percent of parasitism (r = 0.26; p = 0.51) (Table 2). Apparently parasitism is mainly influenced by fruit characteristics, the available alternate hosts and the environment. In Quararibea cordata Vischer fruits, a high number of A. nunenzae Steyskal per fruit (18.8) was observed, but only 3.5% parasitism. In other samples of this fruit that were colonized in the same way with flies at different locations, no parasitoids were observed; this may be because the husk thickness does not permit a high rate of parasitism. The low frequency of parasitoids in Anastrepha species that attack P. guajava (2.7%), is strange. Our observations in the Valle del Cauca are similar to those of Olarte (1980) in Santander (Colombia).

Table 1. Larval / pupal Parasitoids In Species Of Anastrepha And Fruits That They Attack, Present At Four Municipalities Of The Department Of Valle Del Cauca, Colombia.[1-4 = buenaventura: 1, Sombrerillo; 2, Cisneros; 3, Sacarias; 4, Anchicayá; 5 = la Cumbre (Pavas); 6 = jamundí (Chagres); 7 = yumbo (Mulalî)]

Parasitoids
Species of Anastrepha
Fruit host
Braconidae (Opinae)
serpentina
Chrysophyllum cainito and
Doryctobracon zeteki
Pouteria caimito (1)
striata
Campomanesia lineatifolia Ruiz et. Pav. (1)
leptozona
P. caimito (3,4
nunezae
Quararibea cordata (6)
striata
C. lineatifolia (1), Psidium guajava (2)
D. areolatus
leptozona
P. caimito (4,1)
coronilli
Bellucia pentamera (3)
pickeli
Manihot esculenta (6)
obliqua
Mangifera indica (7)
Opius sp.
leptozona
P. caimito (1)
Phaenocarpa sp.
distincta
Inga edulis (3)
Eucoilidae
Aganaspis sp.
leptozona
P. caimito (1)
Proctotrupoidea
sp. indeterminate
obliqua
M. indica (7)
Hymenoptera
sp. indeterminate
striata
Psidium guajava (5,2)

Table 2. Percent Of Parasitism Seen In Fruits Of Nine Species Of Plants Affected With Anastrepha Sp. At Four Municipalities Of The Department Of Valle Del Cauca (Colombia).

Speciesof fruit
Number
Fruit
Number
Flies / Fruit
Number
Parasitoid/Fruit
%
Parasitism
Q. cordata
19
18.80
0.68
3.5
C. caimito
49
4.73
0.78
14.1
B. pentamera
41
1.20
0.15
10.9
P. guajava
72
6.01
0.17
2.7
Inga edulis
1
6.00
10.0
62.5
M. esculenta
32
0.09
0.03
25.0
M. indica
17
3.12
0.41
11.7
C. lineatifolia
64
0.73
0.47
39.0
P. caimito
152
3.80
0.56
12.8
Total
447
3.93
0.46
10.4

According to this author, considering the scarcity of U. anastrephae and D. crawfordi in this plant species, they have an insignificant effect on A. striata populations. In this study, specimens of D. areolatus (Szepligeti) associated with A. striata were observed in this crop, which also coincide with species observed by Canal-Daza et al. (1994) in the state of Amazonas (Brazil).

For Mangifera indica L. it is necessary to process a larger number of samples from different areas. The parasites observed came from fruits strongly attacked by A. obliqua (3.2 / fruit). When flies were not abundant parasitoids did not occur. The parasites were represented by 7 species classified in 3 families: Braconidae (4 species), Eucoilidae (1 species), Proctotrupoidea, (1 species) and one species that has not been identified to date.

At locations that had Anastrepha infested fruits and parasitoids, parasitism varied from 2.7% in P. guajava to 62.5% in Inga edulis Mart., but this last value is not reliable because of the size of the sample (Table 2).

Although the number of fruits sampled must be considered, it is evident that the Buenaventura locations had the largest frequency and diversity of parasitoids observed (Table 1). However, this was influenced by the Pouteria caimito Radlk. samples; 5 species of parasitoids were observed in this fruit. The most common species was Doryctobracon zeteki (Muesebeck) (69%). This species, besides being a parasitoid of A. leptozona, was also associated with A. serpentina, A. striata and A. nunenzae. In other fruits, D. aereolatus, Aganaspis sp. and Opius sp. were present at 15%, 13% and 3%, respectively. In other municipalities like Dagua, La Cumbre and Jamundi, which are located in an area with less precipitation, samples of the same species did not yield any parasitoids, even though there was abundant A. leptozona and A. serpentina emergence.

The second species in importance was D. areolatus; besides being a parasite of A. leptozona Hendel in P. caimito, it was also found in association with other species of Anastrepha such as A. pickeli Lima, A. striata, A. obliqua and A. coronilli Carrejo y G. This species is considered the most abundant parasitoid and also the one with the widest distribution in Costa Rica, where it is a parasitoid of A. obliqua, A. striata, A. distincta Greene and Anastrepha species that attack Chrysophyllum cainito L. fruits (Jirón & Mexzon 1989).

In Florida (U.S.A.), after this species was introduced, it was recovered from A. suspensa pupae (Baranowski et al. 1993). According to Canal-Daza et al. (1994), this species is distributed in Mexico, Costa Rica, Panamá, Trinidad, Colombia, Venezuela, Brasil and Argentina, having these hosts: A. bahiensis Lima, A. benjamini Kima, A. bistrigata Bezzi, A. consobrina (Loew), A. fraterculus, A. leptozona, A. ludens, A. montei Lima, A. obliqua, A. pickeli, A. pseudoparallela (Loew), A. serpentina, A. striata, A. sororcula Zucchi, A. suspensa, C. capitata and Rhagoletotrypeta sp.

Aganaspis was represented by 13 parasitoids that colonized A. leptozona (in P. caimito) in the municipality of Buenaventura. Phaenocarpa sp. was recovered only from A. distincta obtained from I. edulis at the same municipality. Apparently it caused a high percent of parasitism in this area but this should be confirmed with a larger number of fruits. According to R. Wharton (Dept. of Entomology, Texas A & M University College Station, personal communication) it was not possible to determine to which of the two neotropical species of this genera it belongs because it is poorly described. Canal-Daza et al. (1994) reported P. anastrephae attacking A. obliqua in Brasil.

There are many parasitoid species of Tephritidae in the genus Opius. Opius sp. was not very frequent during this study; the few specimens that were recovered were associated with A. leptozona in P. caimito in Buenaventura, and it represented only 2.8% of the parasitoids.

According to Canal-Daza et al. (1994) the species Opius bellus Gahan has been reported for Costa Rica, Belize, Panamá, Trinidad, Venezuela, Brasil and Argentina, associated with some Anastrepha species and other Tephritidae. This distribution suggests that it is also in Colombia.

The species of Proctotrupoidea has not yet been identified; it was found only in one of the processed mangos, and although it was abundant, it seems not to be important because of its small size and the frequency with which it appeared in the fruit. It is a group for which no specialist is known.

Acknowledgments

Special thanks to the Colombian Institute of Investigation and Special Projects "Francisco José de Caldas" (COLCIENCIAS) and to the Universidad del Valle for its financial support, to Philip Silverstone-Sopkin and Jorge Ramos of the Botanical Section, Dept. of Biology, Universidad del Valle, for their important help with identification of the host plants, to P. M. Marsh and A. S. Menke (Systematic Entomology Laboratory of USDA), to Dr. R. Warton (Dept. of Entomology, Texas A & M University College Station), and to Orlando Grijalva for his help with recovering the parasitoids at the laboratory.

References Cited

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Aluja, M., J. Gillen, P. Cabrera, E. Rios, G. De La Rosa, H. Celedon, and D. Mota. 1990. Fruit infesting tephritids (Dip.: Tephritidae) and associated parasitoids in Chiapas, Mexico. Entomophaga 35(1): 39-48.

Baranowski, R., H. Glenn, and J. Sivinski. 1993. Biological control of the Caribbean fruit fly (Diptera: Tephritidae). Florida Entomologist 76(2): 245-251.

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Portilla M., G. González, and L. Nuñez. 1993. Infestación, reconocimiento, identificación de moscas de las frutas y de sus controladores benéficos en el cultivo del café (Coffea arabica). XX Congreso de la Sociedad Colombiana de Entomología (Socolen). Resúmenes. p. 88.

Wharton, R. 1989. Classical biological control of fruit infesting Tephritidae, Pp. 303-313. In: A. S. Robinson and G. Hooper (eds.). Fruit flies: Their biology, natural enemies, and control. Elsevier, Amsterdam.