Abundance of Anastrepha fraterculus (Diptera: Tephritidae) and Its

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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 SERGIO M. OVRUSKI,1, 2 ROBERT A. WHARTON,3 PABLO SCHLISERMAN,1 AND MARTI´N ALUJA4

Environ. Entomol. 34(4): 807Ð818 (2005)

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 (Sze´ pligeti), 37.9%; Doryctobracon brasiliensis (Sze´ pligeti), 17.7%; Utetes anastrephae (Viereck), 1.1%; Opius bellus (Gahan), 0.7%; (all Braconidae, Opiinae), and Aganaspis pelleranoi (Bre` thes), 32.6% (Figitidae, Eucoilinae). All parasitoids emerged from A. fraterculus pupae (i.e., none from C. capitata). The discovery of D. crawfordi represents the Þrst 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 ßies. 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 misidentiÞed. KEY WORDS Tephritidae, Braconidae, parasitoids, biological control, taxonomy

THE SOUTH AMERICAN FRUIT ßy, Anastrepha fraterculus (Wiedemann) (Diptera: Tephritidae), native of the neotropical region, is one of the most polyphagous and important pests of edible fruits in South America (Aluja 1994, Malavasi et al. 2000, Aluja et al. 2003a). This species is found in the warmest areas of the central and northern regions of Argentina, where it coexists with the exotic Mediterranean fruit ßy, Ceratitis capitata (Wiedemann) (Ovruski et al. 2003a). Other tephritid species of quarantine importance have not been reported in Argentina (Cosenzo 2003). ArgentinaÕs northwestern region (Provinces of Tucuma´n, Salta, Jujuy, and Catamarca; locally known as NOA) is characterized by a high diversity of native and exotic fruit ßy host plants growing adjacent to 1 PROIMI-Biotecnologõ´a, Divisio ´ n de Control Biolo´ gico de Plagas, T4001MVB San Miguel de Tucuma´n, Argentina. 2 Corresponding author: Salta 290, 4to. Piso, Depto,“G”, T4000EBG, San Miguel de Tucuma´n, Tucuma´n, Argentina (e-mail: [email protected] yahoo.com.ar). 3 Department of Entomology, Texas A&M University, College Station, TX 77843. 4 Instituto de Ecologia, A.C., Apartado Postal 63, 91000 Xalapa, Veracruz, Mexico. E-mail: [email protected]

commercial citrus orchards. Among the most common and widespread exotic fruit species in this region are Morus alba L. (white mulberry), M. nigra L. (black mulberry) (Moraceae), Ligustrum lucidum L. (Oleaceae), Citrus aurantium (sour orange) (Rutaceae), all originating from SE Asia, and Psidium guajava L. (common guava) (Myrtaceae), originating from tropical rainforests in Latin America but outside Argentina (Arago´ n 2000, Grau and Arago´ n 2000). P. guajava is a common A. fraterculus host fruit in northwestern Argentina (Nasca et al. 1981, Ovruski et al. 2003a) and throughout the distribution range of the A. fraterculus cryptic species group (Aluja et al. 2000a, 2003a; Norrbom 2004). Interest in an integrated approach to management of tephritid pests has resulted in numerous surveys of the natural enemy complex associated with A. fraterculus. At least 22 hymenopterous parasitoid species have been recorded from A. fraterculus in the neotropical region (Ovruski et al. 2000, 2004), and this represents the largest parasitoid assemblage known for any species of tephritid native to the neotropics. Surveys of the parasitoid species attacking the larvae of the various cryptic A. fraterculus species have been

0046-225X/05/0807Ð0818$04.00/0 䉷 2005 Entomological Society of America



published for Mexico (Lo´ pez et al. 1999, Sivinski et al. 2000, Aluja et al. 2003b), Colombia (Ye´ pes and Ve´ lez 1989, Carrejo and Gonza´lez 1999), Guatemala (EskaÞ 1990), Costa Rica (Wharton et al. 1981), Venezuela (Katiyar et al. 1995), Peru (Cruz 1995), and Brazil (Leonel et al. 1995, 1996, Salles 1996, Aguiar-Menezes and Menezes 1997, 2001, Canal and Zucchi 2000, Guimara˜es et al. 2000, Carvalho et al. 2000, AguiarMenezes et al. 2001). Eleven native fruit ßy parasitoid species have been recorded in Argentina (Ovruski et al. 2000), most of them associated only with A. fraterculus on native and exotic host fruit species in the Province of Tucuma´n (Ovruski and Fidalgo 1994, Wharton et al. 1998). Koinobiont, solitary larval-prepupal parasitoids belonging to the Braconidae (subfamily Opiinae) and Figitidae (subfamily Eucoilinae) are clearly the dominant parasitoids of A. fraterculus in Argentina, as recently conÞrmed by Ovruski and Schliserman (2003a) and Ovruski et al. (2004). The most commonly encountered of these species include the opines D. areolatus (Sze´ pligeti), Doryctobracon brasiliensis (Sze´ pligeti), Opius bellus Gahan, and Utetes anastrephae (Viereck) (Ogloblin 1937, Hayward 1940a, b, Nasca 1973, Ovruski 1995, Ovruski et al. 2004), and the eucoilines Aganaspis pelleranoi (Bre` thes), Lopheucoila anastrephae (Rohwer), and Dicerataspis grenadensis Ashmead (DeSantis 1965, Wharton et al. 1998). Only two idiobiont, solitary, pupal parasitoid species, Trichopria anastrephae Costa Lima (Nasca et al. 1980) and Coptera haywardi (Ogloblin) (Loia´cono 1981) (both Diapriidae), have been reared from Anastrepha in Argentina. Additional species thus far recorded, such as the braconid Opius trimaculatus Spinola and the eucoiline Rhoptromeris haywardi (Blanchard) (Lahille 1915, Blanchard 1947, DeSantis 1967, van Achterberg and Salvo 1997), need to be veriÞed as parasitoids of A. fraterculus because of possible misidentiÞcations of either the parasitoids or of the host (Turica and Mallo 1961, Ferna´ndez de Araoz and Nasca 1984, Wharton et al. 1998). Even though there are important citrusgrowing areas in the northwestern Provinces of Salta and Jujuy, only a limited amount of information on fruit ßy parasitoids has been published for these two provinces (Turica and Mallo 1961), with most of the published information thus far obtained from the province of Tucuma´n (Ovruski et al. 2004). During the early 1960s, Þve exotic parasitoid species [Fopius arisanus Sonan (reported as Opius oophilus Fullaway), Doryctobracon crawfordi (Viereck) (reported as Opius), Diachasmimorpha longicaudata (Ashmead) (reported as Opius longicaudatus) (all Braconidae), Aceratoneuromyia indica (Silvestri) (reported as Syntomosphyrum indicum) (Eulophidae), and Pachycrepoideus vindemiae (Rondani) (Pteromalidae)] were released in limited numbers in citrusgrowing areas of the northwestern Argentinean province of Jujuy. The last three parasitoid species were released in Tucuma´n for the biological control of A. fraterculus and C. capitata (Ovruski et al. 1999). Only A. indica and D. longicaudata, two exotic parasitoids widely employed in fruit ßy biological control

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programs (Purcell 1998), were recovered immediately after release in both provinces (Turica 1968). However, there is currently no evidence of permanent establishment of these parasitoid species in any northwestern release sites. Only in the case of D. longicaudata has permanent establishment on A. fraterculus been documented in the northeastern province of Misiones (Schliserman et al. 2003). To complete our picture on the distribution of native fruit ßy parasitoids in this country, particularly the highly endangered subtropical montane rainforest in northwest Argentina (locally known as Yungas forests) and to update the taxonomic status of fruit ßy parasitoids reported so far in Argentina, we report on a study with the following speciÞc aims: (1) determine whether the species composition of A. fraterculus parasitoids in wild guava habitats in the northernmost sector of the Yungas forest (Salta province) differs from that previously reported in the southernmost sector (Tucuma´n and Catamarca provinces) of this type of unique forest (Ovruski and Schliserman 2003b, Ovruski et al. 2004); (2) document natural distribution ranges of these parasitoid species along a latitudinal gradient; (3) identify candidate native parasitoid species for use in A. fraterculus biological control programs in South America (i.e., Argentina, Bolivia, Brazil, Uruguay, Paraguay); (4) determine variations in the level of fruit infestation by A. fraterculus and the abundance of its parasitoids during the relatively short wild guava fruiting season to be able to design biological control programs against this important pest; and (5) clarify the taxonomic status of several species of opiine parasitoids previously reported from or released against A. fraterculus in Argentina. There are few studies on the insects of the Yungas forest, but work on both plants and vertebrates (Brown et al. 2001) suggests that there are latitudinal differences in diversity with greater species richness and endemism in the north.

Materials and Methods Study Area. The collecting area was located between 22⬚45⬘ and 23⬚33⬘ S latitude and between 64⬚15⬘ and 64⬚ 25⬘ W longitude, with elevation ranging from 350 to 440 m, in Ora´n County, Province of Salta, northwest Argentina. The study area extended 90 km from the southern border with the Argentinean Province of Jujuy to the northern border with Bolivia. This area is located in the northernmost extension of the Argentinean subtropical montane rainforest (locally known as Yungas or selva tucumano-boliviana) (Cabrera 1976). Within this phytogeographical region, the study area is included in the environmental unit called Premontane forest (lowest sector of the Yungas), which has an altitudinal range of 300 Ð 600 m (Brown 1995). Climate is deÞned as humid warm-temperate with a summer rainy season (December through March) and winter dry season. Temperature of the warmest month is ⬎22⬚C, and mean annual temperature is 18⬚C (Anonymous 1992). In the study area

August 2005


(from Urundel to Aguas Blancas), annual rainfall varies from 259 to 1,947 mm (Bianchi and Yan˜ ez 1992). The native vegetation of this Premontane forest has been almost completely transformed into intensive agriculture. This has occurred through introduction of exotic plant species like citrus and sugarcane, replacement by antropic grassland for cattle raising (Brown 1995), or conversion to family orchards with high diversity of exotic fruits for personal consumption. Several of these agriculture Þelds have been abandoned and progressively revegetated, resulting in secondary forests with different structural and ßoristic characteristics (Grau et al. 1997). At present, old abandoned fruit orchards are sites with abundant exotic fruit plants, mostly animal-dispersed fruit species, such as Citrus aurantium, Morus spp., Ligustrum spp., and P. guajava (Grau and Arago´ n 2000). Fruit Sampling. The study area was divided into four sampling sites (Aguas Blancas, 22⬚45⬘ S, 64⬚22⬘ W, 405 m; San Ramo´ n de la Nueva Ora´n, 23⬚08⬘ S, 64⬚20⬘ W, 376 m; Tabacal, 23⬚17⬘ S, 64⬚15⬘ W, 435 m; and Urundel, 23⬚33⬘ S, 64⬚25⬘ W, 359 m). From 30 wild common guava trees of similar size (10.9 ⫾ 0.9 [SD] cm trunk diameter at breast height [dbh] measured 135 cm above ground level and 6.1 ⫾ 0.5 m in height) selected in each sampling site, 10 trees were chosen at random on each sample date. Trees were sampled every 2 wk during February and March in 1999 and 2000. Ten trees per site and four collecting sites resulted in 40 guava trees sampled during each sample date. Because abundance of opiine parasitoids is affected by the ripening of guava fruit (Purcell et al. 1994), only late-ripe fruit (guava uniformly yellow but with mottled brown spots and soft texture) were collected. Five fruits about to fall were harvested from each guava tree, and Þve fruits that had fallen from the tree canopy to the ground were also included in the sample. This protocol was followed because fallen host fruit samples provide a more accurate estimation of parasitization rates than tree-collected fruit samples alone (Wong and Ramadan 1987). Therefore, each sample consisted of 10 guavas per tree for a total of 100 fruit for each sampling site during each sample date. Each fruit sample was placed individually into a cloth bag and transported in a plastic crate to our laboratories at the CIRPON (Centro de Investigaciones para la Regulacio´ n de Poblaciones de Organismos Nocivos) in the city of San Miguel de Tucuma´n (26⬚50⬘ S, 65⬚13⬘ W, 426 m), Province of Tucuma´n, northwestern Argentina. All common guava trees sampled were located in small patches of disturbed secondary vegetation (exotic and native plant species combined) in areas surrounding commercial orchards, such as citrus and sugarcane. Guava is not a commercial fruit in this region of Argentina, and it is only cultivated in some family orchards for local consumption. Typically, the guava fruiting season in the study area is very short. Ripe fruit are most abundant (99%) during mid- and late summer (February and March, respectively) and least abundant (1%) during early summer (January).


For this reason, we only collected fruit during February and March. Fruit Processing. In the laboratory, all fruits in the sample were weighed and rinsed with a 20% solution of sodium benzoate and placed in closed styrofoam boxes (20 by 20 by 30 cm) with damp sand in the bottom as a pupation substrate for ßy larvae (fruits were placed on a metal screen [10-mm mesh] Þtted ⬇10 cm from the bottom). Mean individual fruit weight was 40.7 ⫾ 9.6 (SD) g (N ⫽ 3,200). Each styrofoam box contained one fruit sample (⫽10 guava fruit), and all samples of the same harvest date were grouped on shelves. During the Þrst 4 wk after they were collected, fruit samples were kept inside a room at 26 ⫾ 2⬚C, 65 ⫾ 10% RH, and a photoperiod of 14:10 (L:D) h, and the sand was sifted weekly to collect pupae. Afterward, fruit was dissected to determine the presence of larvae or pupae in the pulp. Live larvae were allowed to pupate and were added to the other pupae collected from the same sample. Pupae of C. capitata and Anastrepha Schiner were distinguished and separated using pupal characters (White and Elson-Harris 1992). All pupae were individually counted and placed in plastic cups Þlled with sterilized moist sand in the bottom and covered with an organdy lid. These cups were inspected daily for up to 3 mo, and any emerging adult ßy or parasitoid was removed and identiÞed. Because of Þnancial and space restrictions, we were not able to maintain unemerged pupae to ascertain if they contained diapausing parasitoids (according to Aluja et al. 1998, some native parasitoid species, such as the ones reported here, exhibit diapausing periods of up to 11 mo). Parasitoid and Fly Identification. Parasitoids were identiÞed by two of us (S.O. and R.W.). Nomenclature used for parasitoid species follows Wharton (1997). Fruit ßies were identiÞed by S.O. using the key provided by Zucchi (2000a). Voucher specimens were placed in the entomological collections of the Instituto Fundacio´ n Miguel Lillo (IFML; San Miguel de Tucuma´n, Argentina) and Texas A&M University. Environmental Conditions. Rainfall and maximum and minimum temperatures recorded between January and April 1999 and 2000 in the study area were provided by the local weather station in the Ora´n county administered by EVARSA (Evaluacio´ n de Recursos S.A.), Regional Noroeste, Delegacio´ n Ora´n, Province of Salta, and by the Subsecretarõ´a de Recursos Hõ´dricos de la Nacio´ n, Gobierno de la Repu´ blica Argentina. Maximum temperature was monitored at 1500 hours and minimum temperature at 0600 hours. Data Analysis. Fruit infestation values reported here are based on the number of Anastrepha or C. capitata puparia obtained per kilogram of guava fruit. The mean number of puparia per guava fruit was also calculated by dividing total number of puparia obtained from each subsample by 10 (the number of fruits in each subsample). Rates of parasitization were calculated on the basis of the total number of parasitoids recovered from the total number of puparia obtained from the fruit.



Fig. 1. Mean ⫾ SD daily precipitation and minimum and maximum temperatures in the study area during January (early summer), February (midsummer), March (late summer), and April (early fall) in 1999. Different letters indicate signiÞcant differences between means recorded during February and March (P ⫽ 0.05; t-test).

Where appropriate, means and SDs were calculated as summary statistics for the rates of parasitism, levels of infestation, and abundance of parasitoids and ßies. The numbers of parasitoids and ßies emerging from wild common guava, rates of parasitization, and infestation levels were compared by month in each year using a paired t-test. Data were pooled by month, independent of sampling site. For comparisons of emerged insect numbers and fruit infestation levels, data were previously transformed to ln(x ⫹ 1), whereas parasitism percentage data were subjected to an arcsine square-root transformation before analysis (Zolman 1993) (untransformed means are presented in the results). A simple regression analysis using a linear model to determine degree of association between larval infestation and parasitization rate was also performed. Finally, a StudentÕs t-test was used to compare mean daily rainfall and temperature records between sampling month using ln(x ⫹ 1)-transformed data. A signiÞcance level of 0.05 was used for all statistical tests. Results Environmental Conditions Prevalent During Sampling Dates. Figures 1 and 2 show mean daily rainfall and maximum and minimum temperatures for the 2 mo that encompassed this study (February [midsummer] and March [late summer]) and for 1 mo before (January [early summer]) and 1 mo after (April [early fall]). Mean daily precipitation in February was not signiÞcantly different from that in March during 1999 and 2000 (t ⫽ ⫺0.56, df ⫽ 27, P ⫽ 0.5767 and t ⫽ ⫺1.29, df ⫽ 28, P ⫽ 0.2046, respectively). Cumulative precipitation during February 1999 and March 1999 was 271.7 and 346.3 mm, respectively, and during February 2000 and March 2000 was 245.1 and 254.5 mm, respectively. Similarly, there were no statistically signiÞcant differences between daily mean minimum temperatures recorded in February relative to those in March during both sampling years (t ⫽ 0.32, df ⫽ 27, P ⫽ 0.7462 for 1999; t ⫽ 1.93, df ⫽ 28, P ⫽ 0.0640 for 2000). However, daily mean maximum temperatures recorded in February were signif-

Vol. 34, no. 4

Fig. 2. Mean ⫾ SD daily precipitation and minimum and maximum temperatures in the study area during January (early summer), February (midsummer), March (late summer), and April (early fall) in 2000. Different letters indicate signiÞcant differences between means recorded during February and March (P ⫽ 0.05; t-test).

icantly higher than those recorded in March (t ⫽ 3.72, df ⫽ 27, P ⬍ 0.0001 for 1999; t ⫽ 3.76, df ⫽ 28, P ⬍ 0.0001 for 2000). Fruit Fly Diversity and Abundance. Only two fruit ßy species, A. fraterculus and C. capitata, representing 97.4 and 2.6%, respectively, of the 10,701 adult ßies, were recovered from the 3,200 common guava fruits collected during 1999 and 2000 (Table 1). SigniÞcantly higher numbers of A. fraterculus adults per guava fruit were present in March 1999 and March 2000 (Table 2), reaching a maximum of 10.4 and 14.5 adults per fruit, respectively. Similarly, a signiÞcantly greater number of C. capitata were obtained in March 1999 and March 2000 (Table 2), reaching a maximum of 1.7 and 1.5 adults per fruit, respectively. The levels of infestation by A. fraterculus (ßies per kilogram of guava fruit) were 630, 21, 83, and 33 times higher than those by C. capitata during February 1999, March 1999, February 2000, and March 2000, respectively (Table 1). Parasitoid Diversity and Abundance. Six species of parasitoids, all native to the neotropical region, were recovered from A. fraterculus pupae obtained from common guava fruits during both 1999 and 2000. These were Doryctobracon areolatus, D. brasiliensis, D. crawfordi (Viereck), Opius bellus, Utetes anastrephae (all Braconidae, Opiinae), and Aganaspis pelleranoi (Figitidae, Eucoilinae). Notably, no parasitoids were recovered from C. capitata pupae. Of the 712 parasitoids recovered in the 2-yr study, braconid species represented ⬇67% of all emerged parasitoid adults. Relative abundance of each species by month and year is presented in Table 1. D. areolatus and A. pelleranoi accounted for 40.0 and 35.3% of the total number of parasitoids recovered at the study area in 1999 and 35.4 and 29.4% in 2000, respectively. The relative abundances of the other parasitoid species, for 1999 and 2000, were as follows: D. brasiliensis, 15.3 and 20.5%; U. anastrephae, 8.6 and 11.6%; D. crawfordi, 0.3 and 2.1%; and O. bellus, 0.5 and 0.9%. D. crawfordi and O. bellus were thus rarely collected (the former only in February and the latter only in March). As was the case with A. fraterculus, signiÞcantly greater numbers of parasitoids were obtained per

August 2005



Table 1. Total numbers of A. fraterculus and C. capitata pupae and adults and parasitoid species recovered from wild guava fruits collected in the Orán county, Salta province, northwestern Argentina (1999 and 2000) Total no. Sample date (mo and yr) Feb. 1999 Mar. 1999 Total 1999 Feb. 2000 Mar. 2000 Total 2000 Total

A. fraterculus parasitoid species


Weight (kg)

Cc (pupae)

Cc (adults)

Cc (inf.)

Af (pupae)

Af (adults)

Af (inf.)







All parasitoids

800 800 1,600 800 800 1,600 3,200

32.15 33.45 65.60 31.74 32.88 64.62 130.22

5 327 332 31 169 200 532

2 176 178 19 96 115 293

0.2 9.8 5.0 0.9 5.1 3.1 0.4

4,046 6,829 10,875 2,361 5,490 7,851 18,726

2,008 4,041 6,048 1,239 3,121 4,360 10,408

125.9 204.1 165.8 74.4 166.9 121.5 14.6

70 84 154 39 77 116 270

16 43 59 6 61 67 126

1 0 1 7 0 7 8

0 2 2 0 3 3 5

6 27 33 5 33 38 71

46 90 136 19 77 96 232

139 246 385 76 251 327 712

Cc, Ceratitis capitata; Cc inf., infestation level by C. capitata (pupae per kilogram of guava); Af, Anastrepha fraterculus; Af inf., infestation level by A. fraterculus (pupae per kilogram of guava); Da, Doryctobracon areolatus; Db, D. brasiliensis; Dc, D. crawfordi; Ob, Opius bellus; Ua, Utetes anastrephae; Ap, Aganaspis pelleranoi.

fruit in March 1999 and in March 2000 (Table 3). The four most commonly collected parasitoids, D. areolatus, D. brasiliensis, U. anastrephae, and A. pelleranoi, all increased in abundance from February to March in both 1999 and 2000 (Tables 1 and 3), with the most dramatic increases (3- and 10-fold, respectively) exhibited by the population of D. brasiliensis. Parasitization Rates in Wild Common Guavas. The parasitization rates on A. fraterculus varied over time. SigniÞcantly higher levels of parasitism on A. fraterculus per guava fruit were recorded in March during 1999 and 2000 (Table 2). A clear and statistically signiÞcant overall pattern in the relationship between parasitization rates and infestation levels was documented for both 1999 and 2000 by means of regression analyses [y ⫽ 1.08 ⫹ 0.75x, SE ⫽ 3.95, F(1,14) ⫽ 18.63, P ⬍ 0.007, R2 ⫽ 0.54 for 1999, and y ⫽ 1.76 ⫹ 0.71x, SE ⫽ 5.98, F(1,14) ⫽ 14.11, P ⬍ 0.002, R2 ⫽ 0.49 for 2000]. Taxonomic Status of A. fraterculus Neotropical Opiine Parasitoids in Argentina. A complete list of opiine species previously recorded as parasitoids of A. fraterculus in the Argentinean literature is presented in Table 4. Of the eight opiine names previously associated with A. fraterculus, three are invalid (the species were never described), one species is a misidentiÞcation, and the remaining four are valid species

(details in Table 4). The latter four species were recovered in this study. Discussion Fruit Fly Abundance and Fruit Infestation Levels. Anastrepha fraterculus was by far the dominant fruit ßy species in “feral” guava trees in the northern section of the Yungas forest. This Þnding is consistent with similar studies in the southern portion of Yungas, located in the Province of Tucuma´n (Ovruski et al. 2003a). For example, the number of A. fraterculus larvae infesting “feral” guavas in Tucuma´n was 2.5-fold higher than the number of C. capitata larvae (the only other tephritid of economic importance in the region; Ovruski et al. 2003a). Similarly, A. fraterculus was the most common fruit ßy species reared from P. guajava in the northeastern province of Misiones, Argentina (Ogloblin 1937), and in southern Brazil (Salles 1996, Zucchi 2000b). Although A. fraterculus has one of the broadest host plant ranges of all known Anastrepha species (Norrbom and Kim 1988, Norrbom 2004), fruits in the family Myrtaceae are among its favored hosts (Aluja et al. 2000a, b, 2003a), with P. guajava the most commonly recorded preferred host plant (Aluja 1999). Despite the fact that overall abundance patterns of A. fraterculus and C. capitata were similar in the

Table 2. Comparison of the mean ⴞ SD no. of A. fraterculus and C. capitata adults, infestation level, and A. fraterculus parasitization rate per wild common guava fruit between collecting date during 1999 and 2000 in Orán county, Salta province, northwestern Argentina Sample date (mo and yr)


A. fraterculus adults

Infestation level by A. fraterculus

A. fraterculus parasitization rate

C. capitata adults

Infestation level by C. capitata

Feb. 1999 Mar. 1999 Paired t-test df ⫽ 79.0 t value P value Feb. 2000 Mar. 2000 Paired t-test df ⫽ 79.0 t value P value

80 80

2.510 ⫾ 1.401a 5.049 ⫾ 2.203b

5.061 ⫾ 2.110a 8.541 ⫾ 3.081b

0.288 ⫾ 0.252a 0.369 ⫾ 0.237b

0.002 ⫾ 0.016a 0.238 ⫾ 0.387b

0.006 ⫾ 0.040a 0.415 ⫾ 0.672b

80 80

⫺10.70 ⬍0.0001 1.551 ⫾ 1.881a 3.902 ⫾ 3.304b

⫺10.50 ⬍0.0001 2.911 ⫾ 3.070a 6.669 ⫾ 5.090b

⫺2.09 0.0396 0.170 ⫾ 0.281a 0.369 ⫾ 0.388b

⫺5.52 0.0001 0.019 ⫾ 0.076a 0.120 ⫾ 0.274b

⫺5.40 0.0001 0.039 ⫾ 0.155a 0.211 ⫾ 0.447b

⫺7.04 ⬍0.0001

⫺7.35 ⬍0.0001

⫺4.31 ⬍0.0001

⫺3.09 0.0027

⫺3.18 0.0021

Within a column means followed by the same letter are not signiÞcantly different (P ⬎ 0.05; Paired t-test). a Number of samples. Each sample includes 10 guava fruits per tree.



Vol. 34, no. 4

Table 3. Comparison of the mean ⴞ SD no. of A. fraterculus parasitoid adults yielded per wild common guava fruit between collecting date during 1999 and 2000 in Orán county, Salta province, northwestern Argentina Sample date (mo and yr)


Feb. 1999 Mar. 1999 Paired t-test df ⫽ 79.0 t value P value Feb. 2000 Mar. 2000 Paired t-test df ⫽ 79.0 t value P value

Parasitoid species Ap






All parasitoids

80 80

0.057 ⫾ 0.074a 0.112 ⫾ 0.099b

0.084 ⫾ 0.085a 0.121 ⫾ 0.117b

0.020 ⫾ 0.043a 0.054 ⫾ 0.075b

0.001 ⫾ 0.011 0.0

0.0 0.004 ⫾ 0.019

0.006 ⫾ 0.024a 0.035 ⫾ 0.060b

0.174 ⫾ 0.161a 0.307 ⫾ 0.230b

80 80

⫺4.42 ⬍0.0001 0.024 ⫾ 0.048a 0.096 ⫾ 0.147b

⫺2.18 0.0304 0.049 ⫾ 0.104a 0.096 ⫾ 0.131b

⫺3.96 0.0002 0.007 ⫾ 0.026a 0.076 ⫾ 0.147b

0.0 0.009 ⫾ 0.032

⫺4.15 ⬍0.0001 0.007 ⫾ 0.025a 0.043 ⫾ 0.073b

⫺4.81 ⬍0.0001 0.095 ⫾ 0.158a 0.314 ⫾ 0.362b

⫺4.65 ⬍0.0001

⫺2.58 0.0117

⫺4.29 ⬍0.0001

⫺4.28 ⬍0.0001

⫺5.72 ⬍0.0001

0.004 ⫾ 0.019 0.0

Within a column means followed by the same letter are not signiÞcantly different (P ⬎ 0.05; Paired t-test). Number of samples. Each sample includes 10 guava fruits per tree. Da, Doryctobracon areolatus; Db, D. brasiliensis; Dc, D. crawfordi; Ob, Opius bellus; Ua, Utetes anastrephae; Ap, Aganaspis pelleranoi.


southern and northernmost Yungas forests of Argentina, we did Þnd a difference with respect to Anastrepha schultzi Blanchard. This relatively rare Anastrepha species has been reported principally infesting wild walnut (Juglans australis Grisebach) in the northwest province of Tucuma´n (Argentina) (Schliserman et al. 2004). The same authors also reported low levels of infestation of A. schultzi in P. guajava in the same study area. A similar pattern was reported by Ovruski et al. (2003a), who indicated that, of 13,803 P. guajava collected in 14 localities near Tucuma´n, only 33 (0.24%) were infested by Anastrepha sp. (later identiÞed as A. schultzi by Schliserman et al. 2004). Because the sampling effort by Ovruski et al. (2003a) was considerably larger than the one being reported here (13,800 versus 3,200 guavas, respectively), we cannot discard the possibility that A. schultzi also infests guavas in the southernmost Yungas forests of Argentina. More intensive sampling is therefore needed before more deÞnitive conclusions can be reached. Parasitoid Survey. The parasitoid survey revealed three new fruit ßy parasitoid species records for the Salta province (D. brasiliensis, U. anastrephae, and O. bellus) and the Þrst record of D. crawfordi for Argentina (representing the southernmost record for the species). Before this report, O. trimaculatus (Lahille 1915), D. areolatus (cited as Opius tucumanus), R. haywardi (Turica and Mallo 1961), and A. pelleranoi (DeSantis 1965) were the only parasitoids recorded from Anastrepha spp. in Salta. However, A. pelleranoi, D. areolatus, D. brasiliensis, O. bellus, and U. anastrephae have been previously recorded from A. fraterculus in the provinces of Misiones (northeast Argentina) (Ogloblin 1937, Turica and Mallo 1961), Tucuma´n (northwest Argentina) (Nasca 1973, Ferna´ndez de Araoz and Nasca 1984, Ovruski 1995, Ovruski et al. 2004), and Catamarca (northwest Argentina) (Ovruski and Schliserman 2003b). R. haywardi was not found during this study. However, as discussed by Wharton et al. (1998), published records for R. haywardi attacking tephritids (Blanchard 1947,

Turica and Mallo 1961, Nasca et al. 1980) are questionable and need veriÞcation. All records of this eucoiline species come from bulk samples of fruit, from which parasitoid species of both Drosophilidae and Tephritidae could emerge. Without isolation of tephritid puparia, correct host/parasitoid species associations cannot be made from bulk samples (Wharton et al. 1998). O. trimaculatus was only recorded from A. fraterculus in the Province of Salta by Lahille (1915), and then this parasitoid species appeared in catalogs of DeSantis (1941) and DeSantis and Esquivel (1966). According to Wharton and Gilstrap (1983), O. trimaculatus is a misidentiÞcation of anastrephae, bellus, or one of the species of Doryctobracon. Two interpretations are, in our opinion, equally plausible regarding the discovery of D. crawfordi in the Yungas forest of northwest Argentina. Since D. crawfordi was introduced to Argentina and released in the northwestern province of Jujuy ⬇42 yr ago (Ovruski and Fidalgo 1994), it is likely that this opiine species could have been successfully established on A. fraterculus in the release area (Calilegua [23⬚27⬘ S, 64⬚46⬘ W, 475 m], Ledesma County), and it could have spread to other neighboring Yungas areas of northwest Argentina, such as those in Ora´n County. Interestingly, the exotic opiine D. longicaudata was recently recovered in the northwestern province of Misiones (Montecarlo County) 40 yr after its Þrst release in that Argentinean province (Schliserman et al. 2003). Although D. crawfordi was not recovered after release in Calilegua during the 1960Õs (Ovruski et al. 1999), fruit ßy parasitoid surveys in the provinces of Jujuy and Salta have been largely neglected in the last 38 yr. Alternatively, and considering that D. crawfordi is a widespread neotropical opiine species (Ovruski et al. 2000) that was recovered in the Yungas forest of Santa Cruz Province in southern Bolivia (Escalante 1995), it is equally likely that the natural distribution range of this opiine species includes the northernmost portion of the Yungas forest of Argentina (i.e., the northern section of the Provinces of Salta and Jujuy). This Argentinean Yungas forest section continues

August 2005



Table 4. List of Opiinae neotropical species recorded as parasitoids of A. fraterculus in the Argentinean literature, status of names, and previously published names Opiinae species Doryctobracon areolatus (Sze´ pligeti, 1911) (valid name) Opius cereus Gahan, 1919 Diachasmoides tucumanus Blanchard, in litt. Diachasmoides tucumana Blanchard, in litt. Opius tucumanus Turica and Mallo, 1961 (nomen nudum) Opius tucumanus Blanchard, 1966 Doryctobracon tucumanus (Turica and Mallo) Doryctobracon brasiliensis (Sze´ pligeti, 1911) (valid name) Coeloides anastrephae Bre` thes, 1924 Opius anastrephae (Bre` thes) Diachasmoides anastrephae (Bre` thes) Opius brasiliensis (Sze´ pligeti) Opius brethesi Blanchard Opius (Diachasma) brasilianus Fischer, 1963 Doryctobracon flavofasciatus (Blanchard) (nomen nudum) Diachasmoides flavofasciatus Blanchard, in litt. (undescribed species) Opius bellus Gahan, 1930 (valid name) Opius turicai Blanchard, in litt. Opius turicai Blanchard, 1966 Doryctobracon turicai (Turica and Mallo, 1961) Bracanastrepha bella (Gahan, 1930) Opius trimaculatus Spinola, 1851 (valid name, most likely misidentiÞed) Opiellus trimaculatus Opius trimaculatus Spinola Bracanastrepha pseudobella Blanchard (nomen nudum) Opius pseudobellus Blanchard, in litt. (undescribed species) Bracanastrepha schultzi Blanchard (nomen nudum) Opius schultzi Blanchard, in litt. (undescribed species) Utetes anastrephae (Viereck, 1913) (valid name) Bracanastrepha argentina Bre` thes, 1924 Opius argentina (Bre` thes) Opius (Diachasma) argentinus (Bre` thes) Bracanastrepha anastrephae (Viereck, 1913)

References Ovruski and Wharton (1996) Ogloblin (1937), DeSantis (1941) Schultz (1938) Hayward (1944) Turica and Mallo (1961), Turica (1968) Blanchard (1966), Nasca (1973) Fernandez de Araoz and Nasca (1984), Van Achterberg and Salvo (1997) Fernandez de Araoz and Nasca (1984) Bre` thes (1924) Ogloblin (1937) Hayward (1944), Ratkovich (1950) Domato and Aramayo (1947) Nasca (1973) DeSantis (1967) van Achterberg and Salvo (1997) Hayward (1944); Ratkovich (1950); Turica and Mallo (1958); DeSantis (1967) Fernandez de Araoz and Nasca (1984) Turica and Mallo (1961), Turica (1968) Blanchard (1966); DeSantis (1967) van Achterberg and Salvo (1997) van Achterberg and Salvo (1997) DeSantis (1967) Lahille (1915) DeSantis (1941); DeSantis and Esquivel (1966) van Achterberg and Salvo (1997) Ratkovich (1950), Turica and Mallo (1958) van Achterberg and Salvo (1997) Ratkovich (1950); DeSantis (1967) Ovruski and Fidalgo (1994) Bre` thes (1924) Ogloblin (1937), DeSantis (1967) DeSantis (1941); Ratkovich (1950); Nasca (1973) van Achterberg and Salvo (1997)

throughout southern Bolivia (Brown et al. 2001), including the Bolivian provinces of Tarija, Sucre, and Santa Cruz (Kessler and Beck 2001). D. crawfordi has also been reported from Mexico (Lo´ pez et al. 1999, Sivinski et al. 2000), Guatemala (EskaÞ 1990), Colombia (Ye´ pes and Ve´ lez 1989), and Venezuela (Katiyar et al. 1995) as a parasitoid of A. fraterculus. Parasitoid Abundance and A. fraterculus Parasitization Rates. As previously reported by Vargas et al. (1993) studying the relationship between the abundance of Bactrocera dorsalis (Hendel) and their opiine parasitoids in wild (feral) and commercially grown guavas in Hawaii, our data here indicate that in the “feral” guavas of Salta, parasitoid abundance was closely tied to the abundance of their primary host (A. fraterculus). Among all A. fraterculus parasitoids recovered, D. areolatus and A. pelleranoi were the most abundant in wild guava habitats. This pattern of abundance was reported previously by Ovruski et al. (2004), collecting in the southernmost portion of the Yungas forest in Argentina. Thus, D. areolatus and A. pelleranoi are the two most abundant parasitoid species attacking A. fraterculus larvae in “feral” guavas in both the southern and northern portions of Yungas forest in northwest Argentina. Both D. areolatus and A. pelleranoi are widely distributed in the neotropical

region, attack a broad range of tephritid hosts, and have no apparent host plant preferences (Ovruski et al. 2000). In the case of the other larval opiine parasitoids found in our study (O. bellus and D. crawfordi), our information is still too scant to reach any deÞnitive conclusions on spatial and temporal abundance patterns. Aguiar-Menezes and Menezes (2001), working in neighboring Brazil, found substantial differences in the abundance of O. bellus stemming from the same fruit species over time. For example, these authors reported that O. bellus was not present in fruit samples collected during the cooler and drier months of the year, whereas D. areolatus was found throughout the year. Furthermore, Sivinski et al. (2000) working in tropical Veracruz, Mexico, found that D. crawfordi was more abundant at higher altitudes, that females would preferentially forage in moist, occasionally cool habitats, and that the host on which fruit ßy larvae developed had a signiÞcant effect on parasitism rates. Therefore, more intensive sampling, considering guava and other A. fraterculus hosts, is needed to determine if population size in the case of D. crawfordi and O. bellus is also inßuenced by environmental factors in our study region.



Applied Implications of Our Findings. We show that, in the province of Salta, A. fraterculus populations built up from midsummer (February) to late summer (March) in “feral” guavas located in areas near commercial citrus groves. A similar pattern has been reported in more southern localities of northwest Argentina (Ovruski et al. 2003a). A clear picture thus emerges, indicating that any effort to control A. fraterculus in commercial citrus groves will have to be intimately associated with actions aimed at lowering populations that build up in wild or “feral” hosts such as guavas and peaches. Such an approach was previously implemented in citrus growing areas of Florida to establish Caribbean fruit ßyÐfree zones (Sivinski et al. 1996, Burns et al. 2001). Our discovery here, coupled to the recent report by Ovruski et al. (2004), indicating that “feral” guavas also function as important reservoirs for native A. fraterculus parasitoids, opens up the possibility of delineating areawide management strategies such as the implementation of conservation biological control measures (Aluja 1996, 1999) or the use of inundative releases of native parasitoids during February and March in vegetation adjacent to commercial groves (approach described in Sivinski et al. 1996) followed by mass releases of sterile ßies (Allinghi et al. 2001) and the judicious application of new-generation bait sprays (Burns et al. 2001, Vargas et al. 2001). Such actions will greatly contribute to one of the objectives of the National Fruit Fly Control and Eradication Program in Argentina: establish low A. fraterculus prevalence areas in northern citrus-growing regions (Spinetta 2004). With respect to what species of native parasitoids should be selected for mass releases, decisions should be reached considering local conditions (e.g., native parasitoid guild (Sivinski et al. 1997), type of hosts attacked by ßies (Sivinski et al. 2001), the ability by parasitoid females to respond to varying densities of the host, and the feasibility of mass rearing. Based on our results here and Ovruski et al. (2000, 2004), D. areolatus, D. crawfordi, and A. pelleranoi (all larval-prepupal) and C. haywardi (pupal endoparasitoid) represent good candidates. Our results also conÞrm the ones by Ovruski et al. (2004) indicating that none of the native braconid parasitoids are able to parasitize the exotic C. capitata in Argentina. The latter implies that the only feasible approach to controlling this pestiferous fruit ßy species in Argentina by means of natural enemies will necessarily entail the use of exotic parasitoids (but see below). Candidate species and strategies are discussed by Purcell (1998), Wharton et al. (2000), Lo´ pez et al. (2003), and Ovruski et al. (2003b). Two egg-pupal parasitoids stand out: the recently colonized Afrotropical species Fopius ceratitivorus Wharton (Lo´ pez et al. 2003) and the Asian F. arisanus (Clausen et al. 1965, Wharton 1999). The task may be compounded by the fact that, in Argentina, C. capitata populations are not sustained in coffee as is the case in most of Latin America. As noted by Ovruski et al. (2003a, 2004), in the important citrus-growing areas of northwest Argentina, C. capitata is sustained in several

Vol. 34, no. 4

large exotic hosts that are known to hinder the activity of almost all parasitoid species. Therefore, control of C. capitata in large-scale citrus-growing areas in northwest Argentina by means of parasitoids may not be entirely feasible and should be pursued by other biorational methods such as the sterile insect technique in combination with new generation bait sprays (Burns et al. 2001, Vargas et al. 2001). Nevertheless, in areas where C. capitata populations build up in “feral” peaches and guavas, the situation would be different, because there, augmentative releases of, for example, the native A. pelleranoi or the exotic F. arisanus and F. ceratitivorus, may lower numbers to the point where the inßux of adults to commercial citrus orchards would become negligible and easily controlled by means of bait sprays or release of sterile ßies. Also, further research is needed on the possible use of native pupal parasitoids such as Coptera haywardi, which, based on the recent work by Baeza-Larios et al. (2002) and Guille´ n et al. (2002), show great promise as biological control agents against C. capitata and several pestiferous Anastrepha species. Egg and pupal parasitoids would hit the pest at a highly vulnerable stage and circumvent the problems confronted by larval parasitoids when trying to reach their host in large fruit. Finally, and importantly, what applies to northwest Argentina does not necessarily apply to other fruit-growing regions in the country such as the northeast or the series of irrigated fruit-producing valleys in desert areas of the central northwest provinces of La Rioja, San Juan, and Mendoza. Therefore, our recommendation is to design strategies that are tailored to local conditions. In some areas, biological control may become the backbone of area wide management approaches, whereas in others, its role may be negligible or still needs to be researched. Taxonomic Status of A. fraterculus Opiine Parasitoids in Argentina. The recent checklist of opiine species from Argentina published by van Achterberg and Salvo (1997) cited four species of Anastrepha parasitoids belonging to the genus Bracanastrepha and Þve species belonging to the genus Doryctobracon. Given that the latter checklist contains several inaccuracies that should not be multiplied through uninformed citation, we revised it (corrections and updates described in what follows are summarized in Table 4). The nomina nuda, Opius schultzi Blanchard in litt. and O. pseudobellus Blanchard in litt. were transferred to Bracanastrepha, and a third nomen nudum, Diachasmoides flavofasciatus Blanchard in litt., was transferred to Doryctobracon. These three names were cited only as Blanchard manuscript names in several nontaxonomic (Hayward 1944, Ratkovich 1950, Turica and Mallo 1958) and taxonomic (DeSantis 1967) articles and therefore should be treated as nomina nuda. A search by one of us (S.O.) for type material and other published “evidence” was unsuccessful, and thus no evidence was found to support the validity of these names. Van Achterberg and Salvo (1997) also listed Opius turicai Blanchard as a valid species and transferred it to Doryctobracon, overlooking the previous treatment of this species as a junior subjective

August 2005


synonym of Opius bellus (Wharton and Marsh 1978). Similarly, van Achterberg and Salvo (1997) listed Doryctobracon tucumanus (Turica and Mallo) as a valid name. However, because of the close timing of the two publications, these authors were no doubt unaware that Ovruski and Wharton (1996) had examined the type material and proposed D. tucumanus (with authorship correctly attributed to Blanchard rather than Turica and Mallo) as a junior subjective synonym of D. areolatus. Although van Achterberg and Salvo (1997) tranferred O. bellus to Bracanastrepha, O. bellus was retained in Opius s.l. by Wharton (1997), and a separate subgenus (Bellopius Wharton) was described for bellus and related species. Bracanastrepha shares the carinate hind tibia used by Wharton (1988) to characterize Utetes, and Bracanastrepha has thus been included in Utetes (Wharton 1988, 1997). In summary, the native Doryctobracon areolatus, D. brasiliensis, Utetes anastrephae, Opius bellus, Opius tafivallensis Fischer, and now D. crawfordi and the exotic Diachasmimorpha longicaudata are to date, the only valid species names of Opiinae parasitoids associated with fruit-infesting tephritid ßies in Argentina. All these species, with the exception of O. tafivallensis, have been associated with A. fraterculus and C. capitata (Wharton and Marsh 1978, van Achterberg and Salvo 1997, Ovruski et al. 2004). Acknowledgments We gratefully acknowledge the technical support of E. Frias, N. Ovruski, C. Colin (PROIMI-Biotecnologõ´a, Tucuma´n, Argentina), A. Soria, and L. Oron˜ o (Fundacio´ n Miguel Lillo-CIRPON, INSUE, Tucuma´n, Argentina). We also thank J. del Valle Mora (ECOSUR, Tapachula, Chiapas, Me´ xico) for providing valuable advice on statistical analysis. Financial support to S.O. was provided by the Consejo Nacional de Investigaciones Cientõ´Þcas y Te´ cnicas de la Repu´ blica Argentina (CONICET; grants PIP 0702/98 and PIP 02567/01), and by the Agencia Nacional de Promocio´ n Cientõ´Þca y Tecnolo´ gica de Argentina through the Fondo Nacional de Ciencia y Tecnologõ´a (grant FONCyT PICT/97 08 Ð 00000 Ð 01236). R.W. was supported in part by USDA/ CSREES/IFAFS grant 00 Ð52103Ð9651 and the Mexico-Texas A&M CONACYT program. Support to M.A. was provided by the Mexican Campan˜ a Nacional Contra Moscas de la Fruta (Secretarõ´a de Agricultura, Ganaderõ´a, Desarrollo Rural, Pesca y Alimentacio´ n-Instituto Interamericano de Cooperacio´ n para la Agricultura [SAGARPA-IICA]).

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