Fruit flies (Diptera: Tephritidae) are well-known phytophagous insect species that have been extensively studied in tropical regions because of the damage they cause to several economically important fruits (Aluja 1994; Araujo et al. 2018). Their larvae develop by feeding on the fruit pulp of various species, making the fruits unsuitable for sale, fresh consumption, and industrialization (Paranhos et al. 2004; Aluja & Mangan 2008). Furthermore, some flies may violate the phytosanitary barriers imposed by fresh fruit-importing countries that necessitate the absence of pests, thereby causing indirect damage and impacting fruit export (Malavasi 2000; Paranhos et al. 2004). Oliveira et al. (2013) revealed that the annual economic losses in agriculture caused by insects are estimated to be approximately US$12 billion, including US$1.14 billion associated with fruit production and $1.6 billion associated with the introduction of exotic species. Production losses, control costs, and marketing analyses estimate that fruit flies cause annual losses of approximately US$36 million (R$180 million) in Brazil (MAPA 2015; Nava et al. 2019).

In Brazil, Anastrepha is the most diverse fruit fly genus, with 128 recorded species (Zucchi & Moraes 2023) distributed across all Brazilian states, harming different host families (Malavasi et al. 2000). Seventy-eight species have been reported in the Brazilian Amazon, with the Amazonas and Amapá states having the highest numbers of species, 41 and 37, respectively (Adaime et al. 2023). In addition to Anastrepha species, 2 exotic species, Bactrocera carambolae Drew & Hancock, the carambola fruit fly, and Ceratitis capitata (Wiedemann), the Mediterranean fruit fly occur in the region (Costa et al. 2022).

Bactrocera carambolae is native to Southeast Asia and was first recorded in the municipality of Oiapoque (Amapá, Brazil) in 1996. It occurs in specific areas of Amapá, Pará, and Roraima states (MAPA 2018). It is a polyphagous species, with 26 host plant species registered in Brazil, affecting fruits of high economic relevance, such as citrus and mangoes (Adaime et al. 2016a; Belo et al. 2020). This pest is considered as the main phytosanitary barrier to the export of fruits produced in Brazil (Silva et al. 2004; Ferreira & Rangel 2015; Miranda & Adami 2015). Ceratitis capitata, is native to the African continent (White & Elson-Harris 1992) but currently is observed in various tropical, subtropical, and warm temperate areas around the world, causing significant damage to host plants (Silva et al. 1998; Malacrida et al. 2007; Malavasi 2009).

Recently, fruit fly studies have gained attention in the Brazilian Amazon, especially those scientists focusing on the diversity, geographic distribution, and identification of host plants (Deus et al. 2013; Almeida et al. 2016; Adaime et al. 2017). Moreover, the risk of multiplication and proliferation of these flies is high due to their ability to use different host fruit species. Therefore, it is crucial to identify and investigate the host plants of these insects and assess their infestations from fruit sampling (Almeida 2016). Frequent reports of B. carambolae hosts in Brazil reinforces the need to intensify field sampling to confirm new host species of economic interest as well as those widely reported in other countries. Additionally, it is crucial to carry out studies based on fruit sampling, to obtain information about the parasitoid species (Hymenoptera) that act in the natural biological control of fruit flies (Silva et al. 2011a).

Although various studies have investigated frugivorous flies in the Brazilian Amazon, some areas, such as the extreme north of the state of Amapá (Brazil) that includes the municipality of Oiapoque at the border with French Guiana, have not yet been studied (Adaime et al. 2017). It is necessary to investigate the fruit flies in Brazil as the transport of infested fruits is the main method of fruit fly dispersion in this region (Duarte & Malavasi 2000), with the Brazilian Amazon acting as the gateway for several agricultural and forestry pests, some of which are quarantined (Morais et al. 2016). Transportation through the Oiapoque River basin consists of formal land traffic and informal river traffic, and the goods are carried in small boats to the riverbank communities (Silva et al. 2019).

Adaime et al. (2017, 2018a) reported the significant risk of introducing Anastrepha suspensa (Loew), which has quarantine potential, in Brazil via the state of Amapá, especially due to the vehicle traffic over the bridge connecting the French and Brazilian territories. Insect dispersion can occur via the transport of fruits containing live larvae in international trade or passenger traffic. Natural movement is also an important means of dispersal for some Anastrepha species that can fly up to 135 km (Fletcher 1989).

Oiapoque is the original entry point for B. carambolae in Brazil (Silva et al. 1997; Silva et al. 2004; Godoy et al. 2011; Malavasi 2015), which supports the risk of introducing A. suspensa. As it is a border region, a more intensive fruit sampling effort is necessary to understand the dynamics among B. carambolae, other fruit fly species, and their associated parasitoids in Oiapoque. Therefore, in this study, we aimed to identify the fruit fly species, their host plants, and associated parasitoids in the municipality of Oiapoque in the extreme north of the state of Amapá, Brazil.

Materials and Methods

OBTAINING PUPAE AND ADULT INSECTS

We analyzed the fruits as described by Silva et al. (2011a). Fruits were counted, weighed, and arranged on plastic trays (30.3 × 22.1 × 7.5 cm) on a 2 cm layer of moistened vermiculite. Trays were covered with organza, which was secured using an elastic band.

Fruits were examined every 5 d, for 20 to 30 d for the presence of fruit fly pupae. After this period, the fruits (in general already almost completely consumed by fruit fly larvae) were placed in an oven at a temperature of 120 °C, to eliminate any immature forms, as recommended by Silva et al. (2011a) prior to disposal. The pupae obtained from the fruits of each sample were removed and transferred to transparent plastic bottles (8 cm in diameter) containing a thin layer of moistened vermiculite. Flasks were covered with organza and a vented lid before being placed in a room under controlled temperature (26 ± 0.5 °C), relative humidity (70 ± 10%), and photophase (12 h). Humidity in the trays and flasks was maintained by replacing the water with a pipette.

Flasks containing pupae were inspected daily for 30 d, a period sufficient for the emergence of all viable insects (Silva et al. 2011a). Fruit flies and emerging parasitoids were stored in glass vials containing 70% ethanol until taxonomic identification.

Fig. 1.

Location of fruit sample collection points in the municipality of Oiapoque, state of Amapá, Brazil.

Results

In this study, we collected 240 samples (11,126 fruits; 288.8 kg) from 33 plant species (16 native and 17 introduced species) belonging to 19 families (Table 1). Fruit fly infestations were observed in 136 samples (56.7%) of 18 plant species among 12 families (Table 1). Of the total 12,196 puparia, we observed the emergence of 1,678 females and 1,824 males of 8 Anastrepha species, 2,257 females and 2,282 males of B. carambolae, and 5 species of parasitoids (3 Braconidae and 2 Figitidae species).

We reared 8 Anastrepha species from larvae to adults from several host plant species. Anastrepha antunesi Lima (11 females) was reared from Spondias mombin L. (Anacardiaceae); A. coronilli Carrejo and González (17 females) was reared from Bellucia grossularioides (L.) Triana (Melastomataceae); A. distincta Greene (80 females) was reared from Inga edulis Mart. (Fabaceae), Inga laurina (Sw.) Willd (Fabaceae), and Psidium guajava L. (Myrtaceae); A. fraterculus (Wiedemann) complex (68 females) was reared from S. mombin, Spondias purpurea L. (Anacardiaceae), and P. guajava; A. obliqua (Macquart) (257 females) was reared from Averrhoa carambola L. (Oxalidaceae), S. purpurea, S. mombin, and P. guajava; A. turpiniae Stone (1 female) was reared from P. guajava; A. striata Schiner (1,241 females and 1,386 males) was reared from P. guajava and Psidium guineense Sw. (Myrtaceae); and A. sororcula Zucchi (3 females) was reared from S. mombin.

Bactrocera carambolae was obtained from the fruits of 13 plant species: Annona mucosa Jacq. (Annonaceae), Artocarpus heterophyllus Lam. (Moraceae), Averrhoa bilimbi L. (Oxalidaceae), A. carambola, Citrus x aurantium L. (Rutaceae), Citrus reticulata Blanco (Rutaceae), Malpighia emarginata DC. (Malpighiaceae), Passiflora quadrangularis L. (Passifloraceae), Pouteria caimito Radlk. (Sapotaceae), P. guajava, S. mombin, Syzygium malaccense (L.) Merr. & L. M. Perry (Myrtaceae), and Z. mauritiana (Table 1).

We also obtained 3 species of Braconidae parasitoids: Doryctobracon areolatus (Szepligeti); 7 females and 3 males, Opius bellus Gahan; 14 females and 5 males, and Utetes anastrephae (Viereck); 8 females and 3 males and 2 species of Figitidae: Aganaspis pelleranoi (Brèthes); 13 females and 27 males and Aganaspis nordlanderi Wharton; 1 female and 1 male (Table 1). Specimens of the parasitoid D. areolatus were obtained from the tephritid-infested fruits of B. grossularioides and P. guajava. Opius bellus was obtained from S. mombin, and U. anastrephae was obtained from both I. edulis and S. mombin. The highest percentage of parasitism was observed in B. grossularioides (11.6%) (Table 1).

Discussion

This study is the most comprehensive survey conducted in the extreme north region of Brazil. Previously, there were only spot collections, except for the work carried out by Adaime et al. (2017), who collected 126 samples from 29 plant species of 18 families.

Bactrocera carambolae accounted for the majority (56.4%; 4,539) of all collected tephritids, followed by Anastrepha spp. (43.6%; 3,502). Highest abundance of tephritids was observed in P. guajava, with A. striata (1,236 females and 1,369 males) being the predominant species, followed by B. carambolae (416 females and 456 males). In contrast to the report of Adaime et al. (2017), B. carambolae was predominant over Anastrepha spp. in this study, possibly due to the collection of various fruits with high pest infestation, such as P. guajava (52.28 kg), M. emarginata (19.43 kg), A. carambola (21.71 kg), and S. malaccense (9.85 kg).

Notably, B. carambolae was obtained from 13 host plant species. We observed that the larvae were feeding exclusively on the fruit pulp. The species had never been obtained from so many host plants in surveys in Amapá. Prior to this work, B. carambolae had the following hosts in Oiapoque: A. carambola, C. aurantium, M. emarginata, P. guajava and S. malaccense (Creão 2003; Adaime et al. 2016a; Deus et al. 2016a; Adaime et al. 2017; Sousa et al. 2019). Bactrocera carambolae also infests Anacardium occidentale L. (Anacardiaceae), A. bilimbi, Byrsonima crassifolia (L.) Kunth (Malpighiaceae), Calycolpus goetheanus (Mart. Ex DC.) (Myrtaceae), Capsicum chinense Jacq. (Solonaceae), C. reticulata, Chrysobalanus icaco L. (Chrysobalanaceae), Eugenia stipitata McVaugh (Myrtaceae), Eugenia uniflora L. (Myrtaceae), Licania sp. (Chrysobalanaceae), Mangifera indica L. (Anacardiaceae), Manilkara zapota (L.) P. Royen (Sapotaceae), P. caimito, Pouteria macrophylla (Lam.) Eyma (Sapotaceae), P. guineense, S. mombin, S. purpurea, Syzygium cumini (L.) Skeels (Myrtaceae), Syzygium jambos (L.) Alston (Myrtaceae), and Syzygium samarangense (Blume) Merr. & L.M. Perry (Myrtaceae) in other municipalities of Amapá (Adaime et al. 2016a; Belo et al. 2020).

To the best of our knowledge, our study adds 3 new records to the list of host plants for B. carambolae in Brazil (A. heterophyllus, P. quadrangularis and Z. mauritiana), 2 of them (A. heterophyllus and P. quadrangularis) new records for South America (Fig. 2). Also, the occurrence of B. carambolae in P. quadrangularis is probably the first record worldwide.

The sample of A. heterophyllus infested by B. carambolae was collected in the backyard of a residence in an urban area of Vila Vitória, close to the border with French Guiana. Less than 100 m from this plant, there were fruits of A. carambola and P. guajava infested by the pest. Artocarpus heterophyllus, known as jackfruit in Brazil, belongs to the Moraceae family and is native to Southeast Asia (Prakash et al. 2009). In Brazil, A. heterophyllus is an invasive species with a high density of individuals, high regeneration efficiency, and allelopathy (Boni et al. 2009; Abreu & Rodrigues 2010). It is economically important, and its fruits, wood, leaves, and latex are used for various purposes (Corrêa 1984). In Northeast Brazil, jackfruit is popular for its sweet taste and widely used in sweets, jellies, juices, and compotes (Jagtap et al. 2010). Artocarpus heterophyllus is also a host of B. carambolae at the center of origin (Southeast Asia) of the pest (Allwood et al. 1999; Chinajariyawong et al. 2000). In South America, specifically in Suriname (van Sauers-Muller 2005) and French Guiana (Vayssières et al. 2013), no fruit infestation by B. carambolae has been reported in this species. In Brazil, only A. striata infestations have been reported in fruits of A. heterophyllus (Silva et al. 2009).

Fruits of infested P. quadrangularis were obtained in the urban area of the municipality, in the backyard of a residence. Less than 50 m away there were fruits of P. guajava infested by the pest. Passiflora quadrangularis, native to the Neotropics, is known as passion fruit melon or giant passion fruit in Brazil because of its size and shape. It is widely distributed in the tropical regions of the world and produced on a small scale, as it is usually cultivated close to its place of consumption due to the challenges of post-harvest conservation. It is cultivated throughout tropical America; however, some authors consider it to be native to the Amazon region and South America (Montero et al. 2013). In Southeast Asia, there is only 1 report of the infestation of P. quadrangularis by Bactrocera papayae Drew & Hancock (Allwood et al. 1999). In South America, no infestation of P. quadrangularis by B. carambolae has been reported in French Guiana nor Suriname (van Sauers-Muller 1991, 2005; Vayssières et al. 2013).

Table 1.

Infestation by fruit flies in different plant species in the municipality of Oiapoque, Amapá, Brazil (Mar to Sep 2022).

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Fig. 2.

New hosts of Bactrocera carambolae: A) Artocarpus heterophyllus (Moraceae); B) Passiflora quadrangularis (Passifloraceae); C) Ziziphus mauritiana (Rhamnaceae). Photos: José Victor T. A. Costa.

In the case of Z. mauritiana, fruits were collected in the urban area of the municipality, in the locality called Patauá, in a backyard of a residence. Nearby, there were plants of P. guajava, but the fruits were not infested by the pest. Ziziphus mauritiana is native to the tropical and subtropical areas of India and Southeast Asia (Lorenzi et al. 2015). In Brazil, it is known as “dão” and used for urban afforestation in gardens in the state of Roraima (Ronchi-Teles et al. 2008). Moreover, its fruits, when light green, yellow, or red, are widely consumed in Brazil (Lorenzi et al. 2015). Until this study, the only species of fruit fly obtained from Z. mauritiana in Brazil was Anastrepha zenildae Zucchi, in Boa Vista, Roraima (Ronchi-Teles et al. 2008; Marsaro Júnior et al. 2011; Dutra et al. 2013).

Among the species of Anastrepha¸ A. striata was the predominant species in Oiapoque because of its association with P. guajava, the most abundantly sampled plant species in this study (Table 1). A strong association between A. striata and P. guajava is commonly reported in the Brazilian Amazon (Adaime et al. 2023).

Highest infestation by fruit flies were observed in S. mombin (98.3 puparia/kg), A. carambola (97.1 puparia/kg), P. guajava (95.4 puparia/kg), and M. emarginata (90.8 puparia/kg). Anastrepha obliqua was the main species found in S. mombin, consistent with the findings of Deus et al. (2016b). In P. guajava, the highest infestation was of A. striata, followed by B. carambolae, similar to the results of Sousa et al. (2019). Bactrocera carambolae infests common guava fruits as do Anastrepha species; however, its presence does not affect the autochthonous populations. Deus et al. (2016a) reported that the spatial distribution of A. striata and B. carambolae may enable their co-occurrence in fruits and that the high degree of aggregation of these species in the fruits indicates the coexistence potential of these tephritids in guava in northern Brazil.

Coexistence of B. carambolae with other species of the genus Anastrepha was less evident in A. carambola and M. emarginata, which were predominantly infested by B. carambolae. A high infestation was observed in A. carambola as the fruit is the preferred host of the pests, having co-evolved in the native habitat of the pest. Psidium guajava and A. carambola are the primary hosts of B. carambolae in Southeast Asia and Suriname (Allwood et al. 1999; van Sauers-Muller 2005). Although M. emarginata is originally from tropical America, B. carambolae has adapted well to infest this plant. Van Sauers-Muller (2005) reported M. emarginata as an important host plant in Suriname. In French Guiana, Vayssières et al. (2013) reported greater infestation in M. emarginata than in P. guajava and demonstrated A. carambola and M. emarginata as the species widely infested by the carambola fruit fly.

In the state of Amapá, Lemos et al. (2014) reported high infestation in M. emarginata, reaching 620.7 puparia/kg. We suspect that M. emarginata has a significant impact on the persistence of B. carambolae in the municipality of Oiapoque as we could observe females laying eggs on green fruits even during the fruit collection process in this study (personal observation).

Vayssières et al. (2013) reported that B. carambolae became dominant over time on 4 hosts (A. carambola, M. emarginata, Spondias dulcis G. Forst. (Anacardiaceae), and S. samarangense) that were previously predominantly infested by species of the genus Anastrepha in French Guiana, which may be related to competitive shifts in species. Between 1994 and 2003, no native fruit trees were reported to be infested with the carambola fruit fly in French Guiana (Vayssières et al. 2003). However, since 2005, some specimens of B. carambolae have been obtained from the native fruit plants of this region (Vayssières et al. 2013).

Despite the existence of an official control program in Brazil, B. carambolae has been dominant in Oiapoque since 1996, possibly due to the adaptation of the species to new hosts. All studies on host plants of this pest were carried out in the state of Amapá, where B. carambolae has several host plant species, including P. guajava, A. carambola, S. malaccense, and M. emarginata, which are the most frequently infested species, unlike 2 decades ago, when this pest almost exclusively infested A. carambola (R. Adaime, personal communication). Bactrocera carambolae is capable of infesting fruits of plant species native to the Amazon region, such as E. stipitata and P. macrophylla, using them as alternative hosts. However, so far this has only been recorded in areas already altered by human activity (Lemos et al. 2014). Belo et al. (2020) reported the species C. goetheanus as a host plant for B. carambolae, native to the Neotropical region and naturally occurring in peri-urban forests, revealing the adaptive capacity of this species. Iwahashi (1999, 2000) observed that B. carambolae evolved an aculeus-length adaptation capable of ovipositing on host plants native to Asian tropical forests. Therefore, complementary studies on the length of the aculeus must be conducted to confirm whether this adaptation also is observed in B. carambolae in the tropical forests of the Amazon region and in urban and peri-urban areas.

Considering the results obtained in this work and others already carried out, it is known that in addition to B. carambolae, 23 species of Anastrepha were reported in Oiapoque, and the host plants are unknown for 13 of them because they were captured in McPhail-type traps (Ronchi-Teles 2000; Carvalho 2003; Norrbom & Uchôa 2011; Trindade & Uchôa 2011). In this study, there were no new records of species of the genus Anastrepha in this municipality. However, we identified 8 new associations between species of Anastrepha and host plants. Additionally, 8 new associations of B. carambolae with host species were identified (Table 2).

Braconidae species identified in this study had previously been reported in the Brazilian Amazon (Sousa et al. 2021, 2023). Between the 2 species of Figitidae identified in this study, A. pelleranoi, which has previously been reported in the Brazilian Amazon (states of Amapá, Amazonas, Pará and Roraima) and other Brazilian states (Sousa et al. 2021; Zucchi & Moraes 2023), was the most abundant. The other Figitidae species, A. nordlanderi, previously was reported only in the states of Amazonas and Santa Catarina in Brazil (Zucchi & Moraes 2023). However, our study presents the first record of A. nordlanderi in the state of Amapá. Considering all the studies carried out in Oiapoque, 7 species of parasitoids are currently reported (Table 3).

Notably, except A. turpiniae, all Tephritidae species identified in this study have previously been reported in French Guiana border via the municipality of Oiapoque (Brazil) (Vayssières et al. 2013). Interestingly, we did not detect the quarantine pest, A. suspensa, in the study area. Adaime et al. (2018a) reported a significant risk of introducing this species in Brazil. Therefore, it is important to conduct further studies, focusing on fruit sampling, in this region to validate these findings.

Due to the great socioeconomic importance of B. carambolae for national fruit growing (Silva et al. 2004; Godoy et al. 2011; Lemos et al. 2014; Ferreira and Rangel 2015; Miranda and Adami 2015), it is imperative that studies be carried out to identify new host plants. This knowledge then can be used in official pest control programs, with the adoption of more targeted and effective control measures. Moreover, future studies should focus on plant species native to South America to verify the possible adaptation of pests to fruits in this region.

Table 2.

List of fruit flies (Tephritidae) and their host plants in the municipality of Oiapoque, Amapá, Brazil.

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Table 3.

List of parasitoids and their hosts in the municipality of Oiapoque, Amapá, Brazil.