In many countries, tephritid species have caused tremendous losses in fruit production and imposed limits on the export market (Aluja & Mangan 2008). There are relatively few records of fruit flies on native plant species because the majority of publications report data from commercial orchards (Norrbom & Korytkowski 2009). However, current restrictions include fruit species for which there is scant information regarding fruit fly host status (Rengifo et al. 2011). In Brazil, the main fruit fly pests are native Anastrepha species and the exotic medfly, Ceratitis capitata (Wiedemann).

Anastrepha Schiner is the largest and most economically important genus of Tephritidae in the Americas (Norrbom et al. 2000). Of the 235 described species of Anastrepha, about 104 are reported in Brazil (Uchôa-Fernandes & Nicácio 2010), and the majority of these has unknown hosts. Anastrepha species in Brazil are associated with fruit bearing trees of 29 families. Of the 41 Anastrepha species associated with host plants, 37% feed on Myrtaceae and 24% on Sapotaceae (Zucchi 2000a).

The genus Ceratitis comprises approximately 65 species, found mostly in tropical Africa. Yet, one of its species, C. capitata (Mediterranean fruit fly) is dispersed throughout almost all tropical and temperate warm areas of the planet. It is considered the most cosmopolitan and harmful of all fruit flies, an invader which causes more dam- ages to crops than any other species (Garcia 2009). The host range of C. capitata includes more than 350 fruit and vegetables around the world, and this pest has shown a preference for ripe and succulent fruits (Liquido et al. 1991). Zucchi (2001) has listed 59 hosts for medfly in Brazil with a wide distribution around the country. Souza-Filho et al. (2000) reported medfly and 35 Anastrepha species in São Paulo State of which only 20 have known hosts.

In São Paulo State, there are 248,809 square kilometers planted with a high diversity of commercial crops, many of which are hosts of fruit flies (Tephritidae). Due to intensive urbanization in the State, the fruit fly distribution and infestation period have changed with implications for the ecology of fruit flies and the strategies of IPM Programmes.

Lonchaeidae species have also been commonly recovered from fruit samples or McPhail traps (Raga et al. 2005, 2006), but in some cases without association with previous tephritid infestation (Uchôa-Fernandes & Nicácio 2010).

The capacity of tephritids to infest so many distinct hosts under different ecosystems has important implications in ecology and pest management. Indeed there are requirements for information on spatial and temporal distribution (UchôaFernandes & Nicácio 2010) and competition among the fruit fly. Tephritid diversity is related to the host phenology in a complex manner, but knowledge thereof is crucial to understand the population dynamics of fruit flies (Souza-Filho et al. 2009), and for implementation of quarantine restrictions and management and control programs (McPheron 2000).

The present work reports the fruit fly and lance fly species (Tephritoidea) associated with fruits in natural conditions, collected from several localities in São Paulo State, Brazil.

MATERIALS AND METHODS

From Mar 1997 to Sep 2003, a total of 536 fruit samples of 63 species in 28 botanical families (Table 1) were collected from 67 municipalities of all regions of Sao Paulo State, Brazil. A total of 117,396 fruits (2,130.70 kg) were collected randomly from the canopies and from the ground beneath the trees (Table 1). Samples were obtained from unsprayed trees and brought to the Laboratory of Economic Entomology, Instituto Biológico, located in the municipality of Campinas, São Paulo State. The fruits were counted, weighed and placed in fruit-holding boxes containing sterilized sand at the bottom and a piece of cotton cloth at the top. About 15–20 d later, the sand in the boxes was sieved to remove Tephritoidea pupae, which were counted and transferred to a glass cage (6,000 cc) with a small amount of dry sand at the bottom and kept at 25 ± 2 °C and 70 ± 10% relative humidity for 25 d to allow adult emergence. Adults were fed with a mixture of sugar/yeast extract (3:1) and water. Adults were killed in a freezer and placed in labeled vials with 70% ethanol for identification. Tephritidae adults were separated by sexes and the Anastrepha females were identified based on Stone (1942), Steyskal (1977) and Zucchi (2000b). Specimens of Lonchaeidae were not identified below family level. Infestation indices of Tephritoidea from each fruit species were measured by pupae per fruit and pupae per kg of fruits.

RESULTS AND DISCUSSION

From overall infested collections the infestation average indices ranged from 0.01 to 22.98 pupae per fruit, obtained respectively from Manihot esculenta Crantz and Cucurbita moschata Duch. ex Poir. (Table 1). The maximum average infestations in samples were recovered from C. moschata (107.1 pupae), followed by Mangifera indica L. and sweet passion fruit, Passiflora alata Curtis, with 107.1, 59.0, and 38.5 pupae/fruit, respectively. In terms of pupae/kg of fruit, the average indices ranged from 0.01 (M. esculenta) to 277.9 (Citharexylum myrianthum Cham.). The maximum average infestations in samples were recovered from C. myrianthum (1,217.6), Schinus terebenthifolius Raddi (520.0), Eriobotrya japonica (Thunb.) Lindl. (430.6), P. alata (342.2), peach Prunus persica (L.) Batsch (418.2), passion fruit, Passiflora edulis Sims (287.5), and mango M. indica (283.3). According to Raga et al. (2004), some samples of ‘Kumquat’ and ‘Cravo’ mandarin collected in the state of São Paulo reached 64.0 and 37.9 pupae/kg of fruits, respectively. In the present work, only 17 plant species showed no fruit samples infested with fruit flies (Tephritoidea).

Considering all collections, we obtained 43,104 pupae and 26,368 adults of Tephritoidea (Table 2). The following frequencies of Tephritoidea adults were obtained during the experiment: 79.2% Tephritidae (63.5% Anastrepha spp. and 15.7% C. capitata) and 20.8% Lonchaeidae. No adult fly was obtained in 22 botanical species (Table 2) of which 6 had been reported to be hosts of Anastrepha spp. or C. capitata in the remaining Brazilian states (Zucchi 2001). Only C. capitata emerged from Annona muricata L. samples. The following hosts were only infested by Lonchaeidae: atemoya (A. squamosa L. × A. cherimola Mill.), Annona reticulata L., Capsicum sp., Carica papaya L., Gossypium hirsutum L., P. edulis, avocado (Persea americana Mill.), Rollinia mucosa (Jacq.) Baill., S. terebinthifolius and Swartzia langsdorfii Raddi. Only 5 hosts showed infestation by Anastrepha spp.: Cryptocarya aschersoniana Mez, Cucurbita maxima (Duchesne), Picramnia sp., Punica granatum Linnaeus, and Rubus ulmifolius Schott.

TABLE 1.

HOST PLANTS OF TEPHRITOIDEA AND RESPECTIVE INFESTATION INDICES FROM SAMPLES COLLECTED IN THE STATE OF SÃO PAULO, BRAZIL (MAR 1997 TO SEP 2003).

In all the hosts infested by C. capitata or Anastrepha spp. in the present work we also registered Lonchaeidae infestations (Table 2). Medfly and Lonchaeidae infestations were observed exclusively in Solanum gilo Radd. Eight plant species were considered hosts for both Anastrepha spp. and Lonchaeidae. Seventeen hosts showed infestation by C. capitata and Anastrepha species. Medfly and Lonchaeidae were recovered from 12 hosts while Anastrepha spp. and Lonchaeidae were recovered from 24 hosts.

We observed infestations by C. capitata, Anastrepha spp. and infestations by Lonchaeidae in the following 16 host plant species:Averrhoa carambola L., C. myrianthum, Dyospyros kaki L. f., E. japonica, Garcinia brasiliensis Mart., Inga spp., Malpighia emarginata Sessé & Moc ex DC, Malus domestica L., Manilkara zapota (Linnaeus) van Royen, P. alata Dryander, Pouteria caimito (Ruiz & Pav.) Radlk., Prunus munie Sieb. & Zucc, P. persica, Pyrus communis (Linnaeus) Batsch. Spondias purpurea L. and Terminalia catappa.

TABLE 2.

TEPHRITOIDEA ADULTS RECOVERED FROM SAMPLES COLLECTED IN THE STATE OF SAO PAULO, BRAZIL (MAR 1997 TO SEP 2003).

(CONTINUED)

TABLE 3.

ANASTREPHA FEMALE DIVERSITY OBTAINED FROM FRUIT SAMPLES COLLECTED IN THE STATE OF SÃO PAULO, BRAZIL (MAR 1997 TO SEP 2003).

Medfly has become established in most areas of the country (Zucchi 2001). In the present work we reported for the first time medfly infestations on C. myrianthum, P. mume, and S. gilo. Ceratitis capitata is dominant in urban areas of São Paulo State (Raga et al. 2004) and it has shown a preference for coffee (Raga et al. 2002) and peach (Souza-Filho et al. 2009), although it can also infest native hosts (Table 2).

Our data indicated that Lonchaeidae is not exclusively an opportunistic group, although in the majority of fruits infested by them, previous infestation by tephritids can make them more suit- able due to physical and chemical changes. Several Brazilian publications have shown an increasing number of reports of Lonchaeidae from fruit samples collected in different agro-ecosystems and biomes (Garcia & Corseuil 2004; Raga et al. 2004, 2005; Uchôa-Fernandes et al. 2002, 2003; Souza-Filho et al. 2009; Uchôa-Fernandes & Nicácio 2010). In the present work, lonchaeids were recovered from 23 introduced hosts (Table 2).

Ten Anastrepha species were recovered from the following fruit samples: A. amita Zucchi, A. bahiensis Lima, A. distincta Greene, A. fraterculus (Wiedemann), A. grandis (Macquart), A. leptozona Hendel, A. obliqua (Macquart), A. pseudoparallela (Loew), A. serpentina (Wiedemann) and A. sororcula Zucchi. These Anastrepha species are associated with 16 botanical families (Table 3). Six species belong to the fraterculus Group: A. amita, A. bahiensis, A. distincta, A. fraterculus, A. obliqua, and A. sororcula. Anastrepha pseudoparallela is thought to infest P. alata exclusively although only lonchaeids emerged from fruit samples from P. edulis.

Although Barbados cherry (M. emarginata) showed low infestations, their samples presented the highest diversity of tephritids: C. capitata, A. fraterculus, A. obliqua and A. sororcula. Anacardiaceae, Rosaceae and Sapotaceae were infested by 4 tephritid species each.

Among the fruit fly species recovered from the fruit samples, the South-American fruit fly, A. fraterculus, was the most polyphagous species, infesting 22 hosts from 13 botanical families. Anastrepha fraterculus is the most economically important fruit fly in São Paulo State, where it infests 33 hosts, including introduced ones (SouzaFilho et al. 2000). We report for the first time the infestation of A. fraterculus on C. aschersoniana (Lauraceae), Manilkara zapota (L.) P. Royen (Sapotaceae), and Picramnia sp. (Picramniaceae) in Brazil. We report A. fraterculus infesting organic strawberry for the first time in São Paulo State (Table 3) at high infestation rates (up to 91.8 pupae kg^-1).

Our study showed new fruit fly-host associations in São Paulo State, probably due to the adaptation evolution of stenophagous/polyphagous species in highly disturbed ecosystems. Further studies should improve the knowledge of ecological aspects of Tephritoidea complex in different edapho-climatic conditions of São Paulo.