Fruit flies (Diptera, Tephritidae) and their parasitoids on cultivated and wild hosts in the Cerrado-Pantanal ecotone in Mato Grosso do Sul, Brazil

BIOLOGY, ECOLOGY AND DIVERSITY

Fruit flies (Diptera, Tephritidae) and their parasitoids on cultivated and wild hosts in the Cerrado-Pantanal ecotone in Mato Grosso do Sul, Brazil

Tiago Ledesma Taira^I; Alfredo Raúl Abot^I; José Nicácio^II; Manoel Araécio Uchôa^II; Sérgio Roberto Rodrigues^I; Jorge Anderson Guimarães^III

^IUniversidade Estadual de Mato Grosso do Sul, Rodovia Aquidauana-CERA, km 12, 79200000 Aquidauana-MS, Brasil. [e-mail]

^IIUniversidade Federal da Grande Dourados, Av. Guaicurus km 12, 79804970 Dourados-MS, Brasil

^IIIEmbrapa Hortaliças, Rodovia Brasília/Anápolis BR 060, Km 09, 70359970 Gama-DF, Brasil

ABSTRACT

Fruit flies (Diptera, Tephritidae) and their parasitoids on cultivated and wild hosts in the Cerrado-Pantanal ecotone in Mato Grosso do Sul, Brazil. Information on frugivorous flies in cultivated or wild host plants and their parasitoids in the Cerrado-Pantanal ecotone in Aquidauana, Mato Grosso do Sul is presented and discussed. Fruit fly samples were collected weekly in specific fruit trees, and McPhail^® traps were installed in the same trees for a period of two years. The fruit flies infested ripe and unripe fruits of Averrhoa carambola L., Schoepfia sp., Psidium guajava L. and Pouteria torta (Mart.) Radlk and mature fruits of Anacardium occidentale L. and Inga laurina (Sw.) Willd. Nineteen fruit fly species were obtained with the combination of sampling methods (collecting fruits and trapping), nine of them obtained with both methods, five found only in fruits and five only in traps. This is the first record of Anastrepha striata Schiner in a species of Sapotaceae, as well as for A. castanea Norrbom and A. daciformes Bezzi in Schoepfia sp. (Olacaceae), and for A. distincta Greene in fruits of P. guajava in the state of Mato Grosso do Sul. Fruit collections simultaneously associated with capture of fruit flies by McPhail traps in the same host plants are essential to understand the diversity of fruit flies and their relationship with hosts and parasitoids. Species of Braconidae and Pteromalidae were recovered, where Doryctobracon areolatus (Szépligeti) was the most abundant parasitoid in larvae of tephritids infesting both cultivated and wild host fruits.

KEYWORDS: Insecta; Mediterranean fruit fly; quarantine pests; Tephritoidea.

Tropical fruits are important for developing regions due to their economic and nutritional characteristics. About 90% of these fruits produced worldwide are consumed in the countries where they are produced, and the rest is exported in natura or processed. The value of tropical fruit production was estimated at 43.7 billion dollars in 2008 (FAO 2009). Brazil is the third largest producer of fruits after China and India, with annual production of about 43 million tons (INCT 2009).

Frugivorous fruit flies, especially species of Tephritidae, which in the larval stage consume fruit pulp from different botanical families (Zucchi 2000a; Gonçalves et al. 2006; Garcia & Norrbom 2011; Ronchi-Teles et al. 2011), have been a major problem for world fruit production. Although known as fruit flies, some species of larval Tephritoidea can feed on flower buds, flowers, buds, leaves, seeds and roots (Evstigneev 2011; Khaghaninia et al. 2011; Sabedot-Bordin et al. 2011; Uchôa 2012).

The genera of greatest importance to Brazil are Anastrepha Schiner, 1868, Ceratitis Macleay, 1829, Bactrocera Macquart, 1835 and Rhagoletis Loew, 1862, with an emphasis on the first two due to the large number of hosts which they utilize (Zucchi 2000b, 2007). In Mato Grosso do Sul, the occurrence of Ceratitis capitata (Wiedemann, 1824) has been reported along with nearly 30 species of Anastrepha (Uchôa-Fernandes et al. 2002, 2003a; Rodrigues et al. 2006; Canesin & Uchôa-Fernandes et al. 2007; Uchôa & Nicácio 2010).

Losses to Brazilian fruticulture related to these pests vary between 120 and 200 million dollars annually, due to high cost of control (Felix et al. 2009) and phytosanitary barriers of importing countries (Paranhos et al. 2007). Knowledge of the relationship between frugivorous tephritids and their hosts is critical for the control of pest species (Nicácio & Uchôa 2011). However, it is important to know the phenology of these fruit trees, mainly native and/or non-cultivated species, since tephritid pests may use them to maintain their populations during the offseason of planted fruit crops.

Several studies have been conducted with Tephritidae using traps, especially those of the model McPhail^®, used worldwide for monitoring and/or control of these insects (Rousse et al. 2005; Canesin & Uchôa-Fernandes et al. 2007; Jemâa et al. 2010). However, when seeking to understand the diversity of economically important fruit flies it is necessary to conduct intensive analyses in the fruits themselves (Zucchi 2000b), since not only is the association between the fly species with the host plant verified, but there is also identification of its parasitoids.

The objective of this study was to understand the interaction between fruit flies (Tephritidae) and their parasitoids in cultivated and wild hosts, based on survey of plant reproductive structures and use of McPhail^® traps, in an area of the Cerrado-Pantanal ecotone of Mato Grosso do Sul, Brazil.

MATERIAL AND METHODS

The study was conducted on the campus of the State University of Mato Grosso do Sul (UEMS) in Aquidauana and in an adjacent area during two years, from June 27, 2009 to June 26, 2011. The climate, according to the Köppen classification, is type Aw (Tropical warm wet) with rainy summer and dry winter, with annual precipitation of 1,250 to 1,500 mm and an average temperature of 26°C. The region is comprised of native vegetation, large areas of pasture (cultivated grasses), small domestic orchards and an experimental area of fruit and annual crops of the UEMS, where guava, mango, banana and coconut are grown along with various plant species.

McPhail^® traps, baited with 300 ml of 5% hydrolzed corn protein (Uchôa-Fernandes et al. 2003b), were used in association with collecting of plant reproductive structures from wild and cultivated fruit species (Table I). The bait was renewed weekly when the captured flies were also collected, which were placed in labeled vials containing 80% ethanol. Each fruit species was represented by one plant and in each plant one trap was installed at 1.7 m above the ground. The reproductive structures were collected concurrently with the collection of material from the traps. Phenological phases were classified as bud, flower, unripe fruit and ripe fruit. The quantity of reproductive structures was dependent on the availability in the field (Table II). Ripe fruits were randomly collected from the plant in which the trap was installed, and in previous stages fruits were also collected from plants of the same species surrounding the plant in which the trap was installed.

The reproductive structures were placed on wooden pallets with a sombrite screen, with 1 cm² openings. The pallets were placed inside black plastic containers measuring 57x37x12 cm, containing water at a depth of 2 cm to retain third instar larvae in the case they abandoned the fruits (Uchôa-Fernandes & Zucchi 1999).

The recipients were monitored daily between 7h00 and 17h00 to avoid death of the larvae by drowning. Larvae were transferred to transparent plastic vials (200 mL), one used as a base and the other as a lid, secured with adhesive tape. A 4 cm layer of sterilized sand moistened with distilled water was placed on the base. The recovered adults and their parasitoids were sacrificed 24 hours after emergence and were stored in 80% ethanol for later identification. The Tephritidae specimens were identified by Prof. Dr. Manoel A. Uchôa (Federal University of Grande Dorados (UFGD), Dourados, Mato Grosso do Sul, Brazil) and the parasitoids by Dr. Jorge Anderson Guimarães (Embrapa Hortaliças, Brasília, Distrito Federal, Brazil). Some Tephritidae specimens are deposited in the entomology collection of the UEMS and at the Museum of Biodiversity, School of Biological and Environmental Sciences of the UFGD; the parasitoid specimens are stored at Embrapa Hortaliças.

The absolute and relative abundances of Tephritidae species were expressed in relation to total females recovered, while the absolute abundance of parasitoids was in relation to the total number of individuals. For analysis of the population fluctuation of frugivorous fly species and the quantity (weight) of fruit, the data obtained per week was used, i.e., the means from 4-5 repetitions per month. The parasitism percentage was calculated according to the equation: [number of parasitoids recovered*100/Number of larvae (3^rd instar) of Tephritidae].

RESULTS

Of the reproductive structures from the fruit plants assessed, only the fruits themselves were infested by tephritids. Of these, 6,746 larvae were obtained in fruits of Anacardium occidentale L., Averrhoa carambola L., Inga laurina (Sw.) Willd., Pouteria torta (Mart.) Radlk, Psidium guajava L. and Shoepfia sp., which resulted in 4,424 adults (67.74% viability), with a sex ratio of 1:1. The sum of larvae in fruits of A. carambola (2,372), P. guajava (2,711) and P. torta (1,635) accounted for 99.58% of the total (Table III).

Larvae were recovered in unripe and ripe fruits of A. carambola, P. torta, P. guajava and Shoepfia sp. and ripe fruits of A. occidentale and de I. laurina. Of the total number of larvae in A. carambola fruits, 98.61% were obtained from ripe fruit and they presented viability of 71.13%, where in unripe fruits larval viability was 62.50%. Among larvae collected from P. guajava fruits, 86.28% were obtained from ripe fruits with viability of 60.00%, while those from unripe fruit presented viability of 76.00%. In fruits of P. torta, 91.38% of larvae were obtained from ripe fruits with viability of 73.57%, lower than the viability of larvae obtained from unripe fruits (Table III).

Fruits of P. guajava, A. carambola and P. torta presented the highest rates of infestation with 20.48, 56.24 and 97.27 larvae kg^-1, respectively. Contrarily, the fruits of A. occidentale, I. laurina and Shoepfia sp. which had the lowest number of larvae showed infestations of 0.16, 2.11 and 4.68 larvae kg^-1, respectively.

In all the traps associated with fruit trees at least one frugivorous tephritid specimen was captured (Table III). Of the 378 flies captured with this method, 113 were females and 265 males, resulting in a 1:2 sex ratio (F:M). Of the total number of flies captured, 0.79% were acquired from traps installed in A. occidentale; 5.82% from Annona muricata L.; 14.81% from A. carambola; 2.65% from Buchenavia tomentosa Eichler; 0.26% from Citrus sinensis (L.) Osbeck; 3.97% from Dipterix alata Vogel; 2.38% from I. laurina; 9.26% from P. torta; 58.73% from P. guajava and 1.32% from Shoepfia sp. (Table III).

Nineteen fruit fly species were obtained with the combination of sampling methods (collecting fruits and trapping), nine of them obtained with both methods, five found only in fruits and five only in traps (Table IV). In relation to the fruit samples, A. carambola presented the greatest number of positive samples (818), followed by P. guajava (767) and P. torta (599). These same fruits showed a larger number of associated fly species, where eight species were found in P. guajava, five in P. torta and four in A. carambola (Table IV).

The increased number and diversity of fruit fly species in the collecting method using traps were confirmed in those installed in P. guajava (45.13% of the species; 6 species), followed by those installed in A. carambola (22.12% of the species; 4 species) and P. torta (12.39% of the species; 5 species) (Table IV).

Of the 14 species associated with fruits, five infested both unripe and ripe fruits, seven occurred only in ripe fruits and two were found only in unripe fruits (Table V). More than 90% of fruit flies from fruits of A. carambola, I. laurina, P. torta and P. guajava were acquired from larvae infesting ripe fruits. In Shoepfia sp., 75% of the flies were also associated with this maturation phase (Table V).

Anastrepha obliqua occurred in July and August of 2009, during seven months of 2010 and six months of 2011 in A. carambola, presenting three population peaks (Fig. 1). This species also occurred in P. guajava from November 2009 to February 2010 and in April 2010. Ceratitis capitata infested A. carambola fruits during six months of 2010 and five of 2011, with the highest average number of larvae in July 2010 and February 2011 (Fig. 1). In P. guajava this species was obtained from December 2010 to February 2011.

Larvae of A. striata obtained from fruits of P. guajava were recovered from August to December 2009, with a population peak in November, occurring during eight months of 2010 and five in 2011 (Fig. 2). These larvae were also obtained in November and December of 2010 infesting P. torta fruits and in March, April and June of 2011 in A. carambola. Anastrepha sororcula obtained from larvae infesting fruits of P. guajava presented a population peek in January 2010 (Fig. 2) and occurred in March, April and June of 2011 in A. carambola fruits.

A total of 215 parasitoids were recovered from the families Braconidae (96.74%) and Pteromalidae (3.26%). Braconidae were represented by Doryctobracon areolatus (Szépligeti, 1911), Utetes anastrephae Viereck, 1913 and Opius bellus Gahan, 1930, while Pteromalidae was represented by an unidentified species (Table VI).

Parasitism of larvae in A. carambola fruit was 5.88% in 2009, 5.61% in 2010 and 2.07% in 2011. In P. guajava it was 3.73% in 2009, 0.71% in 2010 and 4.42% in 2011. In P. torta, parasitism of 1.48% was observed in 2010 (Table VI). Most parasitoids were acquired from larvae infesting mature fruits, except one specimen of D. areolatus that parasitized larvae infesting unripe fruit of A. carambola.

Doryctobraconareolatus was the most abundant (82.79%) and generalist among the parasitoids obtained, parasitizing larvae acquired from A. carambola, P. guajava and P. torta. The parasitism percentage per insect in larvae obtained from A. carambola was 2.99%, 3.14% in P. guajava and 1.35% in P. torta. This parasitoid was recovered in November and December of 2009, from March to August and October to December of 2010 and from January to May of 2011, most expressively in March 2010 when the parasitism percentage of larvae obtained from A. carambola was 19.44% (Table VI).

Utetes anastrephae was the second most abundant species parasitizing larvae from P. guajava and A. carambola, while Opius bellus and Pteromalidae sp.1 were associated only with tephritid larvae in A. carambola (Table VI).

DISCUSSION

The higher number of tephritids obtained from fruits compared to that from traps was probably due to the greater attractiveness of the fruit, since the fruit flies utilized them to reproduce, whereas the bait used in the traps is only a food source for the adults. Another factor that may imply an increased abundance in fruits may be related to the features of each sampling method, since in the fruits one or more females may oviposit at each visit, and a female has the ability to oviposit over 200 eggs during her life in different periods and fruits, in the trap, when captured, each fly is sampled once. The attraction of females to the fruit is enhanced by color and by the release of volatiles, as highlighted by Malo et al. (2005) and Zarbin et al. (2009).

Montes et al. (2011) obtained a 1:2 sex ratio (F:M) in areas with cucurbits, as in this study, however it appears that there is no common standard with regards to the sex ratio of tephritids captured in traps baited with proteins, as verified by various authors who obtained a higher number of females (Montes & Raga 2006; Dutra et al. 2009; Trindade & Uchôa 2011; Santos et al. 2011). The variation of the number of males and females in the traps may likely be related to the number of samples of each sex in the field or that females are feeding and copulating in areas near the trap and then moving towards the oviposition sites.

The fact that frugivorous fruit flies developing in unripe fruits of P. torta, P. guajava and Shoepfia sp. had greater viability than in mature fruits can be explained by the lower number of larvae obtained from unripe fruits. However, this demonstrates that although unripe fruits were not preferred for oviposition, they allowed for successful reproduction of the species.

Pereira-Rêgo et al. (2011) obtained larvae of A. fraterculus from unripe, semiripe and ripe fruits of Psidium cattleyanum var. lucidum (Mart. ex O. Berg) Kiaersk. (araçá-amarelo), P. cattleyanum (Mart. ex O. Berg) Kiaersk. (araçá-vermelho) and P. guajava. These larvae transformed into adults similar in relation to pupal weight and wing area within each botanical species, independent of the stage of ripeness. Carvalho et al. (1998), in studies of the biology of Anastrepha obliqua (Macquart, 1835), confirmed that peak oviposition is attained during the reproduction period. In the present study, the infestation of unripe fruit may also be due to concurrence with the peak of oviposition of this species during this maturation state. The ability to infest unripe fruits by some fruit fly species is a fact that may contribute to their predominance in some hosts. Moura & Moura (2006) confirmed that C. capitata was the only dominant and constant species in guava fruits and reported that this association may be due to the fact that it is the only species that fully infested the fruits.

The high tephritid infestation confirmed in the present study in fruits of P. guajava and A. carambola, was different than that observed by Sá et al. (2008) in the fruit production center in Anagé, Bahia, Brazil, where fruits of A. carambola were not attacked and infestation in P. guajava was reduced, which reinforces the need for regional studies.

Anastrepha alveatoides Blanchard, 1961 occurred only in the trap installed in D. alata, indicating that a specimen of sea lemon (Ximenia americana L.), its only reported host in Pantanal, Brazil (Uchôa & Nicácio 2010), is likely near the plant of D. alata. The infestation of Shoepfia sp. fruits by Anastrepha castanea Norrbom, 1998 and A. daciformes Bezzi, 1909 constitutes the first record for this host. However, these fly species are not the only ones who use it for oviposition, since Uchôa and Nicácio (2010) reported infestations by A. macrura, A. sororcula and A. zernyi in fruits of this species in the same region.

The presence of Anastrepha distincta Greene, 1934 in the study area, captured in the trap installed in P. torta and in ripe fruits of I. laurina and P. guajava was also observed by Uchôa and Nicácio (2010) in association with fruits of I. laurina in the same region. The association of this fly with fruits of P. guajava in the state of Mato Grosso do Sul, however, has not been reported before.

Although Anastrepha fraterculus (Wiedemann, 1830) was obtained in traps installed in P. torta and P. guajava, this species infest only fruits of Myrtaceae. In the state of São Paulo, Raga et al. (2005) found that this species is dominant in fruits of P. guajava.

Anastrepha hamata (Loew, 1873) was obtained in traps installed in P. torta and Shoepfia sp., not occurring in any fruit of the surveyed plants. According to Zucchi (2000a), the host of this tephritid species is unknown. The association of Anastrepha leptozona Hendel, 1914 with fruits of P. torta was also verified by Uchôa and Nicácio (2010) who conducted studies in the Pantanal region of Mato Grosso do Sul.

The capture of Anastrepha montei Lima, 1934 in the trap installed in A. carambola may be due to the abundant regional production of Manihot esculenta Crantz, which according to Zucchi et al. (2000a) is a host of this fly species.

Predominance of Anastrepha obliqua in A. carambola fruits was also observed by Souza-Filho et al. (2000) and Uramoto et al. (2004) in the state of São Paulo. Occurrence of Anastrepha serpentina (Wiedemann, 1830) in fruits of P. torta seems common in the region, since it was also verified by Uchôa and Nicácio (2010).

The presence of Anastrepha sororcula Zucchi, 1979 in more than one-half of the installed traps was due to the fact that P. guajava is common in the region and also resultant of the existence of an orchard of this fruit plant in the experimental unit of the UEMS Fruticulture. This tephritid is the main species infesting guava fruits in Mato Grosso do Sul (Uchôa & Nicácio 2010).

Anastrepha striata Schiner, 1868 infesting P. torta is the first report of the association between this fly species with fruits of Sapotaceae. Anastrepha turpiniae Stone, 1942 was obtained in the trap installed in I. laurina and also recovered from ripe fruits of P. guajava. Also verified was the presence of Anastrepha zenildae Zucchi, 1979 associated with ripe fruit of this Myrtaceae.

Anastrepha zernyi Lima, 1934 and Anastrepha sp.1 were sampled in unripe fruits of P. torta, however they were not captured in the trap installed in this fruit plant. Anastrepha sp.2 was obtained in the traps installed in I. laurina and P. torta, but was not associated with any fruit plant studied.

Ceratitis capitata (Wiedemann, 1824) was associated with the traps installed in A. muricata, A. carambola and P. guajava, however it was obtained only from fruit of the last two plants. The Mediterranean fruit fly was recovered from unripe and ripe fruits of A. carambola, but in P. guajava it occurred only in ripe fruits.

The absence of tephritid attack in A. muricata, C. sinensis and D. alata, and the low infestation in A. occidentale may possibly be explained by the fact that these flies are not adapted to colonize some fruits, as noted by Branco et al. (2000). Similar results were obtained by Souza et al. (2008) who found no infestations in fruits of A. muricata, C. sinensis and A. occidentale, and by Alvarenga et al. (2009), Pereira et al. (2010) and Silva et al. (2011) who also did not find any fruit fly specimens in fruits of A. muricata.

The temporal overlap of fruit production by different plant species may permit the maintenance of pest species populations (Ronchi-Teles & Silva 2005). However, the presence of native fruit species may be an alternative for the natural control of tephritids, since larvae of the fruit fly species that infest their fruits are reservoirs of Anastrepha parasitoids (López et al. 1999; Carvalho et al. 2010).

Fruit flies emerging from fruits infested with larvae occurred during the majority of the experimental period, possibly due to alternating hosts and the overlapping phenology of the fruit plant species sampled. Anastrepha obliqua, A. sororcula, A. striata and C. capitata were common throughout the study period while the other species occurred during isolated months. The population peaks of these four fly species were directly associated with the period of highest fruit production (Figs. 1 and 2). According to Ronchi-Teles & Silva (2005) the availability of the host is important for population fluctuation and abiotic factors only have little influence on these flies.

Parasitism of larvae of Tephritidae by Braconidae observed in this study was found in the same region by Nicácio et al. (2011) and is common in Brazil (Silva et al. 2007a; Souza-Filho et al. 2007; Leal et al. 2009; Ronchi-Teles et al. 2011). Doryctobracon areolatus is considered an important native species, mainly parasitizing species of Anastrepha in neotropical countries (Uchôa-Fernandes et al. 2003a; Uchôa 2012). Due to the frequency, abundance and capacity to parasitize fruit fly larvae in native and exotic fruits, this parasitoid species shows promise for integration in biological control programs of fruit flies in agroecosystems (Nunes et al 2011; Uchôa 2012). The low abundance of U. anastrephae and Opius bellus is common in other studies conducted in Brazil (Uchôa-Fernandes et al. 2003a; Lima Junior et al. 2007; Costa et al. 2009).

The dominance of D. areolatus is possibly related to the length of the ovipositor which permits reaching larvae in various hosts. Parasitoids with long ovipositors parasitize larvae in large and small fruit, but those with short ovipositor are limited to parasitism of larvae in small fruits (López et al. 1999; Sivinski et al. 1997, 2001; Ovruski et al. 2008). The higher parasitism incidence of fly larvae in ripe fruit implies possible susceptibility of these larvae during this period, since in this stage the fruits probably release a larger amount of volatiles and their pulp is softer, facilitating parasitism (Guimarães & Zucchi 2004; Silva et al. 2007b).

ACKNOWLEDGEMENTS

To the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for providing the scholarship to the first author, to Jorge Adriano de Deus Ricardo (UEMS) for his assistance in the execution of this work and MSc. Anderson Puker (Federal University of Viçosa) for his suggestions.

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Received 11 April 2013;

accepted 15 July 2013

Associate Editor: Rodrigo F. Krüger

Publication Dates

• Publication in this collection
  18 Nov 2013
• Date of issue
  Sept 2013

History

• Received
  11 Apr 2013
• Accepted
  15 July 2013