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Occurrence of fruit flies (Diptera: Tephritidae) in the municipality of Alvorada do Gurguéia in South Central Piauí, Brazil

ABSTRACT

The state of Piauí is in a Cerrado/Caatinga transition area, which is known the richness of its fauna and flora. Therefore, this work aims to know the diversity of fruit fly species in cashew orchards and native forest fragments in the south-central region of Piauí. Fruit flies were collected in McPhail traps and by sampling fruits. The material collected from the traps and the fruits in the two areas were taken to the Laboratory of Phytotechnics from Campus Prof. Cinobelina Elvas at the Universidade Federal do Piauí (UFPI/CPCE), municipality of Bom Jesus, Piauí, Brazil. In McPhail traps, six species of the genus Anastrepha: A. alveata, A. dissimilis, A. fraterculus, A. manihoti, A. obliqua, and A. zenildae were captured, of which A. fraterculus, A. obliqua, and A. zenildae were present in both areas. Anastrepha alveata, A. dissimilis and A. manihoti occurred only in the cashew orchard. In fruit sampling, A. fraterculus, A. obliqua, and A. zenildae infested wild-guava fruits, Myrcia tomentosa (Myrtaceae), in native forest. Anastrepha fraterculus, A. obliqua and A. zenildae were obtained directly from M. tomentosa fruits and from traps. The availability of host fruits is the factor that most influences the population fluctuation of fruit flies, mainly in the native forest area. Anastrepha manihoti is reported for the first time in the state of Piauí. This is the first record of A. fraterculus, A. obliqua and A. zenildae, infesting wild-guava fruits, M. tomentosa.

Keywords
Anastrepha ; host fruit; diversity; ecotone; McPhail traps

INTRODUCTION

Fruit flies (Diptera: Tephritidae) are among the main agricultural pests in the world and have an economic impact on the production and marketing of fruits and vegetables. Fruit flies are among the main reasons for concern in tropical developing countries, where fruit production is an important source of income. Fruits resulting from female oviposition and larvae feeding inside make them unfit for consumption (ALUJA; MANGAN, 2008ALUJA, M.; MANGAN, R.L. Fruit fly (Diptera: Tephritidae) host status determination: critical conceptual, methodological, and regulatory considerations. Annual Review of Entomology, Annapolis, v.53, n.1, p.473-502, 2008. https://doi.org/10.1146/annurev.ento.53.103106.093350
https://doi.org/10.1146/annurev.ento.53....
; BATISTA et al., 2019BATISTA, N.S.; SANTOS, J.M.; BROGLIO, S.M.F.; SANTOS, J.R.T. Moscas-frugívoras (Diptera: Tephritidae e Lonchaeidae) no Vale do Mundaú no estado de Alagoas. Revista Verde de Agroecologia e Desenvolvimento Sustentável, Pombal, v.14, n.4, p.512-517, 2019. https://doi.org/10.18378/rvads.v14i4.6243
https://doi.org/10.18378/rvads.v14i4.624...
).

Brazil has a great diversity of fruit plants and potential hosts for several species of fruit flies, mainly species of the genus Anastrepha Schiner, 1868, Bactrocera Macquart, 1835, and Ceratitis MacLeay, 1829 (Tephritidae). Bactrocera carambolae Drew & Hancock is a quarantine pest present in Brazil, being restricted to the states of Amapá, Pará and Roraima. From the genus Ceratitis, the only species introduced in Brazil is Ceratitis capitata (Wiedmann), which infests exotic and native fruits. Of the 128 species of Anastrepha that occur in Brazil, seven are particularly economically important (ZUCCHI, 2000ZUCCHI, R.A. Taxonomia. In: MALAVASI, A.; ZUCCHI, R.A. (Eds.). Moscas-das-frutas de Importância econômica no Brasil: conhecimento básico e aplicado. Ribeirão Preto: Holos, 2000. p. 13-24.; CASTILHO et al., 2019CASTILHO, A.P.; PASINATO, J.; SANTOS, J.E.V.D.; NAVA, D.E.; JESUS, C.R.; ADAIME, R. Biology of Bactrocera carambolae (Diptera: Tephritidae) on four hosts. Revista Brasileira de Entomologia, Curitiba, v.63, n.4, p.302-307, 2019. https://doi.org/10.1016/j.rbe.2019.09.002
https://doi.org/10.1016/j.rbe.2019.09.00...
; ZUCCHI; MORAES, 2022). Research on associations with host plants and their natural enemies in native forest areas is still incipient, this lack is greater in the phytophysiognomies of the Cerrado and Caatinga biomes in the Northeast region of Brazil.

The Northeast Brazilian provides a relatively rich flora that makes up different phytophysiognomies and biomes, with many fruit species that host fruit flies and that are also natural repositories of parasites of these tephritid species (ARAÚJO et al., 2014ARAÚJO, A.A.R.; SILVA, P.R.R.; QUERINO, R.B.; SOUSA, E.P.S.; SOARES, L.L. Moscas-das-frutas (Díptera: Tephritidae) associadas às frutíferas nativas de Spondias spp. (Anacardiaceae) e Ximenia americana L. (Olacaceae) e seus parasitoides no estado do Piauí, Brasil. Semina: Ciências Agrárias, Londrina, v.35, n.4, p.1739-1750, 2014. https://doi.org/10.5433/1679-0359.2014v35n4p1739
https://doi.org/10.5433/1679-0359.2014v3...
). Ecotone regions (or transition zones) have characteristics that are both unique and derived from adjacent domains, in which little is known about their flora and may have a high number of species in different types of habitats. Ecosystems in transition areas generally have a high diversity index, in which endemic species can occur due to the peculiar characteristics of the interface between confluent biomes (ALVES et al., 2013ALVES, A.R.; RIBEIRO, I.B.; SOUSA, J.R.L.; BARROS, S.S.; SOUSA, P.S. Análise da estrutura vegetacional em uma área de caatinga no município de Bom Jesus, Piauí. Revista Caatinga, Mossoró, v.26, n.4, p.99-106, 2013.; BOTREL et al., 2015BOTREL, R.T.; BRITO, D.R.S.; SOUSA, W.C.; SOUZA, A.M.; HOLANDA, A.C. Fenologia de uma espécie arbórea em ecótono Caatinga/Cerrado no sul do Piauí. Revista Verde de Agroecologia e Desenvolvimento Sustentável, Belém, v.10, n.3, p.7-12, 2015. https://doi.org/10.18378/rvads.v10i3.3587
https://doi.org/10.18378/rvads.v10i3.358...
). In Northeast Brazil, although these are semiarid regions, there are great variations in the physiognomies and diversity of flora (ALVES et al., 2013ALVES, A.R.; RIBEIRO, I.B.; SOUSA, J.R.L.; BARROS, S.S.; SOUSA, P.S. Análise da estrutura vegetacional em uma área de caatinga no município de Bom Jesus, Piauí. Revista Caatinga, Mossoró, v.26, n.4, p.99-106, 2013.).

The south central region of Piauí is in a Cerrado-Caatinga transition area. There are a lack of studies concerning fruit flies (Tephritidae) and their parasitoids, being 23 species of fruit flies having previously been reported in this state (ZUCCHI; MORAES, 2021ZUCCHI, R.A.; MORAES, R.C.B. Fruit flies in Brazil - Anastrepha species their host plants and parasitoids. 2021. Available from: http://www.lea.esalq.usp.br/anastrepha. Acessed on: 18 May 2021.
http://www.lea.esalq.usp.br/anastrepha...
). Fruit cropping in the state of Piauí has been strengthened as an economic activity with the implementation of irrigated fruit growing projects (e.g., Guadalupe Plateaus and the Tabuleiros Coastal Irrigation District of Piauí-DITALPI, and Gurguéia Valley), benefiting small farmers growing tropical fruits in the region (ARAÚJO et al., 2014ARAÚJO, A.A.R.; SILVA, P.R.R.; QUERINO, R.B.; SOUSA, E.P.S.; SOARES, L.L. Moscas-das-frutas (Díptera: Tephritidae) associadas às frutíferas nativas de Spondias spp. (Anacardiaceae) e Ximenia americana L. (Olacaceae) e seus parasitoides no estado do Piauí, Brasil. Semina: Ciências Agrárias, Londrina, v.35, n.4, p.1739-1750, 2014. https://doi.org/10.5433/1679-0359.2014v35n4p1739
https://doi.org/10.5433/1679-0359.2014v3...
, GOMES NETO et al., 2017GOMES NETO, A.V.; FRAZÃO, C.A.V.; SILVA, J.D.C.; FRANÇA, S.M.; RAMOS, J.E.R.; SILVA, P.R.R. Moscas-das-frutas e seus parasitoides em cajazeira no município de Teresina-PI. Revista de Ciências Agrárias: Amazonian Journal of Agricultural and Environmental, Belém, v.59, n.4, p.413-416, 2017. https://doi.org/10.4322/rca.2233
https://doi.org/10.4322/rca.2233...
). Despite the impetus of northeastern fruit cropping in Brazil, there are few publications on fruit flies from Piauí, especially regarding natural environments.

Population dynamics of fruit flies are subject to the influence of factors such as temperature, humidity, light, diversity and abundance of hosts (SANTOS et al., 2011SANTOS, M.S.; NAVACK, K.I.; ARAUJO, E.L.; SILVA, J.G. Análise faunística e flutuação populacional de moscas-das-frutas (Diptera: Tephritidae) em Belmonte, Bahia. Revista Caatinga, Mossoró, v.24, n.4, p.86-93, 2011. http://periodicos.ufersa.edu.br/index.php/sistema
http://periodicos.ufersa.edu.br/index.ph...
; ALUJA et al., 2012ALUJA, M.; ORDANO, M.; GUILLÉN, L.; RULL, J. Understanding long-term fruit fly (Diptera: Tephritidae) population dynamics: Implications for area wide management. Journal of Economic Entomology, Annapolis, v.105, n.3, p.823-836, 2012. https://doi.org/10.1603/EC11353
https://doi.org/10.1603/EC11353...
). Investigations on faunal patterns and the seasonality of the occurrence of fruit fly species are fundamental for decision-making and the establishment of integrated management strategies against pest species (SANTOS et al., 2011SANTOS, M.S.; NAVACK, K.I.; ARAUJO, E.L.; SILVA, J.G. Análise faunística e flutuação populacional de moscas-das-frutas (Diptera: Tephritidae) em Belmonte, Bahia. Revista Caatinga, Mossoró, v.24, n.4, p.86-93, 2011. http://periodicos.ufersa.edu.br/index.php/sistema
http://periodicos.ufersa.edu.br/index.ph...
).

It is known that fragmentation of forests leads to a great loss of biodiversity, affecting the discovery of useful information on the biology, ecology and evolution of species of fruit flies (QUERINO et al., 2014QUERINO, R.B.; MAIA, J.B.; LOPES, G.N.; ALVARENGA, C.D.; ZUCCHI, R.A. Fruit fly (Diptera: Tephritidae) community in guava orchards and adjacent fragments of native vegetation in Brazil. Florida Entomologist, Gainesville, v.97, n.2, p.778-786, 2014. https://doi.org/10.1653/024.097.0260
https://doi.org/10.1653/024.097.0260...
) and other phytophagous, decomposing, entomophagous insects. Thus, this paper aims to know the diversity of fruit fly species in cashew orchard and in a native forest fragment in the south central region of the state of Piauí, Brazil.

MATERIAL AND METHODS

Study area

The research was performed in two areas (native forest and cashew orchard) between February 2016 and April 2018. The native forest (approximately 30.3 ha) belongs to the University Experimental Farm (161.3 ha) from the Universidade Federal do Piauí (CPCE/UFPI) (8°22’08.90”S, 43°51’52.08”W, 224 m), which constitutes a legal reserve characterized by the presence of the Cerrado-Caatinga biomes.

The cashew production area (8.6 ha) is in Chácara Anda Sol (8°27’55.41”S, 43°53’46.22”W, 232 m), where the cashew species Anacardium occidentale L. ‘CP76’ of early ripening (April to October) is cultivated.

Both areas are in the municipality of Alvorada do Gurguéia, in the south central part of the state of Piauí, approximately 10 km from each other. The region is characterized by a hot and humid climate classified by Köppen as Awa (ALVARES, et al., 2013), with average rainfall between 900- and 1,200-mm year 1, distributed from December to April, with an average annual temperature of 26.6 °C.

Collections with McPhail traps and fruit sampling

To obtain fruit flies, two sampling methods were used: McPhail traps with food bait and fruit sampling, in the two study areas.

Five McPhail traps were installed in each location (total 10 traps) and baited with a 10% hydrolyzed corn protein solution (BioAnastrepha). These were attached to branches within the treetops approximately 1.5 m high from ground level. The attractant was replaced weekly, when the captured insects were also transferred to properly identified and preserved plastic bottles and preserved at 70% ethanol.

Fruits were collected weekly both from the ground and from the treetops, when possible, within a radius of 25 meters from the traps, was this distance established. The fruit flies from the traps and the native fruits collected weekly were transported to the Phytotechnics laboratory of Campus Prof. Cinobelina Elvas from the Universidade Federal do Piauí (UFPI/CPCE), municipality of Bom Jesus, Piauí. In the laboratory, the fruits were quantified, weighed individually, identified and placed in transparent plastic cups containing autoclaved sand and closed with voile tissue. The samples were kept under room conditions (26 ± 2 °C, 50 ± 10% RH). The sorting of fruits and sand was carried out for a period between 10 and 15 days after collection, and the pupae were transferred to other cups with autoclaved sand until the emergence of the adult fruit flies. Adults were quantified, properly labeled and kept in 70% ethanol for later identification.

The identification of fruit fly species was based on examining the genitalia of females of Anastrepha species, using taxonomic keys (STONE, 1942; ZUCCHI, 2000ZUCCHI, R.A. Taxonomia. In: MALAVASI, A.; ZUCCHI, R.A. (Eds.). Moscas-das-frutas de Importância econômica no Brasil: conhecimento básico e aplicado. Ribeirão Preto: Holos, 2000. p. 13-24.), and only the females were considered in the analyses.

Data analysis

For the analyses, were considered only the females of the species of Anastrepha. The faunistic analysis was based on the frequency, constancy, abundance and dominance indices, according to SILVEIRA-NETO et al. (1976)SILVEIRA-NETO, S.; NAKANO, O.; BARBIN, D.; NOVA, N.A.V. Manual de ecologia dos insetos. Agronômica Ceres. São Paulo, 1976., considering only the number of females for the species of Anastrepha. To better understand the discussion, the research was subdivided into two seasons: February 2016 to January 2017 (scarce rains) and February 2017 to April 2018 (rainiest period), according to the (ALVARES, et a., 2013).

RESULTS

McPhail trap collections

In the 10 traps a total of 954 individuals of different species of the genus Anastrepha were captured (386 females and 568 males). Of these total, 841 specimens (329 females and 512 males) were captured in the native forest area: Anastrepha zenildae (Zucchi, 1979), (n = 185), Anastrepha obliqua (Macquart, 1835), (n = 100) and Anastrepha fraterculus (Wiedemann, 1830), (n = 44) (Table 1). Only 113 specimens (57 females and 56 males) were captured in the cashew orchard, represented by Anastrepha alveata (Stone, 1942), (n = 16), A. zenildae (n = 14), Anastrepha dissimilis (Stone, 1942), (n = 10), A. fraterculus (n = 7), Anastrepha manihoti (Lima, 1934) (n = 6) and A. obliqua (n = 4) (Table 1).

Table 1
Analysis of fruit fly (Diptera: Tephritidae) fauna collected in a McPhail trap in an area of native forest and cashew orchard, Alvorada do Gurguéia, Piauí, Brazil (March 2016 to April 2018).

Population fluctuation

In the first period of the survey (February 2016 to March 2017, scarce rain), A. zenildae showed a population peak in March 2017 and another in May 2016 in the areas of native forest and cashew orchard, respectively (Fig 1a,c). Anastrepha alveata showed three population peaks (May 2016, October 2016 and February 2017) and occurred only in the cashew orchard (Fig. 1c). In the second survey period (February 2017 to April 2018, rainiest period), A. zenildae, A. fraterculus, and A. obliqua showed a population peak in January 2018 in the native forest area (Fig. 1b). In the cashew orchard, the six species showed peaks between May and July 2017. In addition, A. alveata showed two other population peaks in September and November 2017 (Fig. 1d).

Figure 1
Population fluctuation of fruit flies (Diptera: Tephritidae) captured in McPhail traps in the areas of native forest (a and c) and cashew orchard (b and d) in the municipality of Alvorada do Gurguéia, Piauí, Brazil (March 2017 to April 2018).

Faunistic analysis

Whiting the fruit flies, A. fraterculus had the highest frequency (0.118%), followed by A. zenildae (0.093%) and A. obliqua (0.059%) (Table 2). Six species of Anastrepha were captured in a McPhail trap during the sampling period (Table 1). No species was considered predominant, nor was it classified as superdominant, superabundant, superfrequent or superconstant in quantitative parameters (Table 3). Regarding the characteristics of the community, there was a significant difference in the diversity index (H) in the two years of study. The species richness index was higher in the area of cashews in both years of study. Due to the equitability index, the species distribution occurred more uniformly in the cashew orchard than in the native forest area (Table 3).

Table 2
Host of fruit flies (Diptera, Tephritidae) collected in an area of native forest and cashew orchard in the municipality of Alvorada do Gurguéia, Piauí, Brazil (February 2016 to April 2018).
Table 3
Faunistic indices of fruit flies (Diptera: Tephritidae) captured in McPhail traps in an area of native forest and in a cashew orchard, Alvorada do Gurguéia, Piauí, Brazil (March 2016 to April 2018).

Fruit sampling

A total of 276 fruits were sampled, within 25 m of the traps, which were collected according to their availability trees bearing fruit, being 160 of wild guava (Myrcia tomentosa Aubl. DC.) (3,368 g) in the native forest area and 116 fruits of A. occidentale L. ‘CP76’ (5,247 g) in the area of cashew orchard. The total mass of all fruits was 8,615 g. From the wild-guava fruits (native forest), 592 pupae were obtained from which 583 adults of fruit flies emerged (285 females and 239 males), being obtained the species: A. zenildae (160), A. fraterculus (79) and A. obliqua (46) (Table 2).

Climatic data

The temperature varied by only 11 °C during the research period, ranging from 28 to 39 °C, and rainfall was concentrated from October to March, with a maximum of 300 mm in March and a minimum of 7.8 mm in June and November 2016. The relative humidity of the air varied according to rain precipitation, with the highest rainfall observed during February and March (60%) and the lowest rainfall in August (approximately 29%) (Fig. 2).

Figure 2
Monthly averages of rainfall (mm), temperature (°C) and relative humidity (%) in native forest areas (A) and cashew orchards (B) during the collection of fruit fly species (Diptera, Tephritidae) in the municipality Alvorada do Gurguéia, Piauí, Brazil (February 2016 to April 2018).

DISCUSSION

Population fluctuation

Population fluctuation of fruit flies, both in the orchard and in the native forest fragment, showed the highest population peak during May 2016 (Fig. 1c), March, June and November 2017 (Fig. 1a,d), and January and March 2018 (Fig. 1b,d). These peaks coincide with the beginning of the rainy period and an increase in the relative humidity of the air in the evaluated region (Fig. 2). According to RONCHI-TELES; SILVA (2005)RONCHI-TELES, B.; SILVA, N.M. Flutuação populacional de espécies de Anastrepha Schiner (Diptera: Tephritidae) na região de Manaus, AM. Neotropical Entomology, Londrina, v.34, n.5, p.733-741, 2005. https://doi.org/10.1590/S1519-566X2005000500004
https://doi.org/10.1590/S1519-566X200500...
, climatic factors may indirectly affect the population fluctuation of fruit flies, as they may favor the ripening of the hosts in which their larvae grow.

Species richness varied between the two periods: February 2016 to January 2017 (scarce rains) and February 2017 to April 2018 (rainiest period) (Table 2). There was no use of biocides (insecticides, fungicides, herbicides) in the orchard, which minimized the mobility of fruit flies (ALUJA et al., 2012ALUJA, M.; ORDANO, M.; GUILLÉN, L.; RULL, J. Understanding long-term fruit fly (Diptera: Tephritidae) population dynamics: Implications for area wide management. Journal of Economic Entomology, Annapolis, v.105, n.3, p.823-836, 2012. https://doi.org/10.1603/EC11353
https://doi.org/10.1603/EC11353...
). The increase in rainfall in the second year (February 2017 to April 2018, Table 2) provided ripening conditions to the respective host plants and increased the abundance of fruit fly species.

Abiotic factors, such as rainfall, can strongly influence climatic components, such as temperature and relative humidity in the studied areas. In a study by MALAVASI et al. (2000)MALAVASI, A.; ZUCCHI, R.A.; SUGAYAMA, R.L. Biogeografia. In: MALAVASI, A.; ZUCCHI, R.A. (Eds.). Moscas-das-frutas de Importância econômica no Brasil: conhecimento básico e aplicado. Ribeirão Preto: Holos, 2000. p. 92-98. in the Northeast Region of Brazil, A. fraterculus predominated in the coastal region, which is more humid, and A. zenildae predominated in warmer areas, as in the case of the Cariri Cearense region. In the present work, these species were recorded in the south central Piauí in a Cerrado-Caatinga transition area with a hot and humid climate, which probably favored the high populations of these two species.

Faunistic analysis

Quantitative research on the species richness of fruit fly and their spatiotemporal variations in native forest areas is scarce in the neotropical region. The richness found in this study was small when compared to studies of fruit fly species in other tropical regions (ALUJA et al., 2003ALUJA, M.; RULL, J.; SIVINSKI, J.; NORRBOM, A.L.; WHARTON, R.A.; MACÍAS-ORDÓÑEZ, R.; DÍAZ-FLEISCHER, F.; LÓPEZ, M. Fruit flies of the genus Anastrepha (Diptera: Tephritidae) and associated native parasitoids (Hymenoptera) in the tropical rainforest biosphere reserve of Montes Azules. Environmental Entomology, Annapolis, v.32, n.6, p.1377-1385, 2003. https://doi.org/10.1603/0046-225X-32.6.1377
https://doi.org/10.1603/0046-225X-32.6.1...
; BOMFIM et al., 2007BOMFIM, D.A.; UCHOA, M.A.; BRAGANÇA, M.A.L. Biodiversidade de moscas-das-frutas (Diptera. Tephritoidea) em matas nativas e pomares domésticos de dois municípios do Estado do Tocantins, Brasil. Revista Brasileira de Entomologia, Curitiba, v.51, n.2, p.217-223, 2007. https://doi.org/10.1590/S0085-56262007000200012
https://doi.org/10.1590/S0085-5626200700...
; CANESIN, UCHOA, 2007CANESIN, A.; UCHOA, M.A. Análise faunística e flutuação populacional de moscas-das-frutas (Diptera. Tephritidae) em um fragmento de floresta semidecídua em Dourados, Mato Grosso do Sul, Brasil. Revista Brasileira de Zoologia, Curitiba, v.24, n.1, p.185-190, 2007. https://doi.org/10.1590/S0101-81752007000100023
https://doi.org/10.1590/S0101-8175200700...
; HERNÁNDEZ-ORTIZ; PÉREZ-ALONSO, 1993HERNÁNDEZ-ORTIZ, V.; PÉREZ-ALONSO, R. The natural host plants of Anastrepha (Diptera: Tephritidae) in a tropical rainforest of Mexico. Florida Entomologist, Gainesville, v.76, n.3, p.447-460, 1993. https://doi.org/10.2307/3495645
https://doi.org/10.2307/3495645...
; RONCHI-TELES; SILVA, 2005RONCHI-TELES, B.; SILVA, N.M. Flutuação populacional de espécies de Anastrepha Schiner (Diptera: Tephritidae) na região de Manaus, AM. Neotropical Entomology, Londrina, v.34, n.5, p.733-741, 2005. https://doi.org/10.1590/S1519-566X2005000500004
https://doi.org/10.1590/S1519-566X200500...
). Therefore, faunal studies using quantitative parameters (dominance, abundance, frequency and constancy) and species diversity indices help to understand the general patterns of biology, ecology and behavior of communities (URAMOTO et al., 2005URAMOTO, K.; WALDER, J.M.; ZUCCHI, R.A. Análise quantitativa e distribuição de populações de espécies de Anastrepha (Diptera: Tephritidae) no campus Luiz de Queiroz. Piracicaba, SP. Neotropical Entomology, Londrina, v.34, n.1, p.33-39, 2005. https://doi.org/10.1590/S1519-566X2005000100005
https://doi.org/10.1590/S1519-566X200500...
).

Among the species obtained in the present study, with fruit sampling and collections in McPhail traps, only A. zenildae, A. obliqua, and A. fraterculus have economic and quarantine importance (ZUCCHI, 2000ZUCCHI, R.A. Taxonomia. In: MALAVASI, A.; ZUCCHI, R.A. (Eds.). Moscas-das-frutas de Importância econômica no Brasil: conhecimento básico e aplicado. Ribeirão Preto: Holos, 2000. p. 13-24.). The greater dominance of species found in the second period (February 2017 to April 2018, rainiest period) can be explained by the presence of host plant species in the vicinity of the traps (Tables 2 and 3), where species of Anacardiaceae, Myrtaceae, Malpighiaceae and Rutaceae occur, constituting potential fruit hosts for fruit flies (ZUCCHI, 2000ZUCCHI, R.A. Taxonomia. In: MALAVASI, A.; ZUCCHI, R.A. (Eds.). Moscas-das-frutas de Importância econômica no Brasil: conhecimento básico e aplicado. Ribeirão Preto: Holos, 2000. p. 13-24.).

Inventories of fruit flies in the Neotropical Region employing both methods simultaneously are rare: traps and fruit sampling in undisturbed environments, although these locations are more suitable for studies of the population dynamics of fruit flies. However, fruit fly populations in commercial orchards and in unmanaged orchards also exhibit irregular fluctuations from year to year, which are dependent on regional climatic factors that influence host fruit availability (ALUJA, 1994ALUJA, M. Bionomics and management of Anastrepha. Annual Review of Entomology, Annapolis, v.39, n.1, p.155-178, 1994. https://doi.org/10.1146/annurev.en.39.010194.001103
https://doi.org/10.1146/annurev.en.39.01...
; ALUJA et al., 2012ALUJA, M.; ORDANO, M.; GUILLÉN, L.; RULL, J. Understanding long-term fruit fly (Diptera: Tephritidae) population dynamics: Implications for area wide management. Journal of Economic Entomology, Annapolis, v.105, n.3, p.823-836, 2012. https://doi.org/10.1603/EC11353
https://doi.org/10.1603/EC11353...
).

In McPhail traps, specimens of A. alveata in the cashew orchard occurred with high frequency (28.21%) (Table 1). To date, it is not known which fruit species is the host for A. alveata in the south central region of Piauí. This species was obtained from wild plum fruits in northern Piauí. However, wild plum Ximenia americana L. (Olacaceae), is a native species registered as the first host of A. alveata in Brazil (ARAÚJO et al., 2014ARAÚJO, A.A.R.; SILVA, P.R.R.; QUERINO, R.B.; SOUSA, E.P.S.; SOARES, L.L. Moscas-das-frutas (Díptera: Tephritidae) associadas às frutíferas nativas de Spondias spp. (Anacardiaceae) e Ximenia americana L. (Olacaceae) e seus parasitoides no estado do Piauí, Brasil. Semina: Ciências Agrárias, Londrina, v.35, n.4, p.1739-1750, 2014. https://doi.org/10.5433/1679-0359.2014v35n4p1739
https://doi.org/10.5433/1679-0359.2014v3...
). Its occurrence was also verified in other surveys with McPhail traps in semiarid and coastal regions from Rio Grande do Norte in the Caatinga area in northern Minas Gerais state in studies performed by ARAÚJO et al. (2000)ARAÚJO, A.A.R.; SILVA, P.R.R.; QUERINO, R.B.; SOUSA, E.P.S.; SOARES, L.L. Moscas-das-frutas (Díptera: Tephritidae) associadas às frutíferas nativas de Spondias spp. (Anacardiaceae) e Ximenia americana L. (Olacaceae) e seus parasitoides no estado do Piauí, Brasil. Semina: Ciências Agrárias, Londrina, v.35, n.4, p.1739-1750, 2014. https://doi.org/10.5433/1679-0359.2014v35n4p1739
https://doi.org/10.5433/1679-0359.2014v3...
and by ALVARENGA et al. (2000)ALVARENGA, C.D.; CANAL, N.A.; ZUCCHI, R.A. Minas Gerais. In: MALAVASI, A.; ZUCCHI, R.A. (Eds.). Moscas-das-frutas de Importância econômica no Brasil: conhecimento básico e aplicado. Ribeirão Preto: Holos, 2000. p. 265-270..

Anastrepha dissimilis was less abundant and was characterized as an accessory species. This species has already been recovered from three host fruit trees: Passiflora caerulea L., Passiflora elegans Mast. and Passiflora edulis Sims (Passifloraceae) in southern Brazil (GARCIA; NORRBOM, 2011GARCIA, F.R.M.; NORRBOM, A.L. Tephritoid flies (Diptera. Tephritoidea) and their plant hosts from the state of Santa Catarina in southern Brazil. Florida Entomologist, Gainesville, v.94, n.2, p.151-157, 2011. https://doi.org/10.1653/024.094.0205
https://doi.org/10.1653/024.094.0205...
; MARSARO JÚNIOR et al., 2014MARSARO JUNIOR, A.L. Novos registros de hospedeiros de moscas-das-frutas (Diptera: Tephritidae) para o Rio Grande do Sul. Revista de Agricultura, Piracicaba, v.89, n.1, p.65-71, 2014. https://doi.org/10.37856/bja.v89i1.116
https://doi.org/10.37856/bja.v89i1.116...
). The low level of abundance of A. dissimilis and A. manihoti in this study may be the result of the absence of their preferred hosts. Another possibility may be local competition for other species of Anastrepha or the presence of their natural enemies.

Several species of Anastrepha can be classified as specialists (monophages), colonizing a single fruitful host. For example, larvae of A. manihoti develop exclusively on fruits of Manihot esculenta Crantz (MARSARO JÚNIOR et al., 2017MARSARO JÚNIOR, A.L.; ADAIME, R.; TELES, B.R.; SOUZA FILHO, M.F.; SILVA PEREIRA, P.R.V.; MORAIS, E.G.F.; SILVA, E. Anastrepha species (Diptera: Tephritidae). their host plants and parasitoids (Hymenoptera) in the state of Roraima, Brazil: state of the art. Revista Biotemas, Florianópolis, v.30, n.1, p.13-23, 2017. https://doi.org/10.5007/2175-7925.2017v30n1p13
https://doi.org/10.5007/2175-7925.2017v3...
). Anastrepha manihoti has a registered distribution in some Brazilian regions: Amazonas and Rondônia (RONCHI-TELES, 2000RONCHI-TELES, B. Ocorrência e flutuação populacional de espécies de moscas-das-frutas e parasitoides. com ênfase para o gênero Anastrepha (Diptera: Tephritidae) na Amazônia brasileira. 2000. Thesis. (PhD in Biological Sciences). Instituto Nacional de Pesquisas da Amazônia, Universidade do Amazonas, Manaus, Brazil. Available from: https://repositorio.inpa.gov.br/handle/1/38756. Accessed on: 12 Apr. 2019.
https://repositorio.inpa.gov.br/handle/1...
), Pernambuco (HAJI; MIRANDA, 2000HAJI, F.N.P.; MIRANDA, I.G. In: Pernambuco. A. Malavasi & R.A. Zucchi (Eds.). Moscas-das-frutas de Importância econômica no Brasil: conhecimento básico e aplicado. Ribeirão Preto: Holos, 2000. p.229-233.), Santa Catarina (GARCIA et al., 2002GARCIA, F.R.M.; CAMPOS, J.V.; CORSEUIL, E. Lista documentada das moscas-das-frutas (Diptera. Tephritidae) de Santa Catarina, Brasil. Revista Biociências, Porto Alegre, v.10, n.1, p.139-148, 2002.), Rio de Janeiro (FERRARA et al., 2004FERRARA, F.A.; URAMOTO, K.; AGUIAR-MENEZES, E.L.; SOUZA, S.A.; CASSINO, P.C. Novos registros de moscas-das-frutas (Diptera: Tephritidae) no estado do Rio de Janeiro. Neotropical Entomology, Londrina, v.33, n.6, p.797-798, 2004. https://doi.org/10.1590/S1519-566X2004000600019
https://doi.org/10.1590/S1519-566X200400...
), Roraima (MARSARO JÚNIOR et al., 2011MARSARO JÚNIOR, A.L.; ADAIME, R.; RONCHI-TELES, B.; LIMA, C.R.; PEREIRA, P.R.V.D.S. Anastrepha species (Diptera: Tephritidae) their hosts and parasitoids in the extreme north of Brazil. Biota Neotropica, Campinas, v.11, n.4, p.117-124, 2011. https://doi.org/10.1590/S1676-06032011000400012
https://doi.org/10.1590/S1676-0603201100...
), Bahia (SANTOS et al., 2011SANTOS, M.S.; NAVACK, K.I.; ARAUJO, E.L.; SILVA, J.G. Análise faunística e flutuação populacional de moscas-das-frutas (Diptera: Tephritidae) em Belmonte, Bahia. Revista Caatinga, Mossoró, v.24, n.4, p.86-93, 2011. http://periodicos.ufersa.edu.br/index.php/sistema
http://periodicos.ufersa.edu.br/index.ph...
) and Minas Gerais (CAMARGOS et al., 2015CAMARGOS, M.G.; ALVARENGA, C.D.; GIUSTOLIN, T.A.; OLIVEIRA, P.C.D.C.; RABELO, M.M. Moscas-das-frutas (Diptera: Tephritidae) em cafezais irrigados no norte de Minas Gerais. Coffee Science, Viçosa, v.10, n.1, p.28-37, 2015. http://www.sbicafe.ufv.br:80/handle/123456789/8101
http://www.sbicafe.ufv.br:80/handle/1234...
). Among the six Anastrepha species obtained in the present study, A. manihoti is reported for the first time in the state of Piauí.

There was a significant difference in fruit fly communities by the diversity index (H) in the two study periods in which there was only one rare species (Table 1). The advantage of diversity lies in the survival of the community. For example, rare species (singleton species), apparently without economic importance, can contribute to the maintenance of community stability, exerting important indirect functions (ROSA DE OLIVEIRA, 2015ROSA DE OLIVEIRA, M.B. Análise comparativa das espécies de Anastrepha (Diptera. Tephritidae) em três agroecossistemas no estado de São Paulo. 2015. Dissertation. (Master’s in Entomology). Escola Superior de Agricultura “Luiz de Queiroz”, Universidade de São Paulo, São Paulo, Brazil.; SILVEIRA-NETO et al., 1976SILVEIRA-NETO, S.; NAKANO, O.; BARBIN, D.; NOVA, N.A.V. Manual de ecologia dos insetos. Agronômica Ceres. São Paulo, 1976.). Therefore, the presence of these species is indicative of the host diversity around the study area. The values of the diversity index, species richness index (Margalef) and uniformity index corroborate that the fruit fly community in south central Piauí has average species diversity and contributes to the equitable distribution of abundance and dominance of these species.

The greatest uniformity of species occurred in the cashew orchard in both periods evaluated (February 2016 to January 2017, scarce rains and February 2017 to April 2018, rainiest period), (Table 2). Therefore, with a more equitable distribution in the orchard compared to the native forest area, probably due to the presence of hosts in the orchard’s surroundings throughout the year, host succession of the fruit fly species was enabled.

Fruit sampling and climatic occurrences

The fruits of M. tomentosa (wild guava) were sampled in rainy periods. This Myrtaceae hosted A. zenildae, A. obliqua and A. fraterculus and contributes to the maintenance of the population in the two studied areas. Myrtaceae in the Neotropical Region are responsible for maintaining resources for fruit flies, and their fruits are suitable for the larval development of a great diversity of Tephritidae species (NICÁCIO; UCHOA, 2011NICÁCIO, J.; UCHOA, M.A. Diversity of frugivorous flies (Diptera: Tephritidae and Lonchaeidae) and their relationship with host plants (Angiospermae) in environments of South Pantanal Region, Brazil. Florida Entomologist, Gainesville, v.94, n.3, p.443-466, 2011. https://doi.org/10.1653/024.094.0309
https://doi.org/10.1653/024.094.0309...
; UCHOA et al., 2002; URAMOTO et al., 2008URAMOTO, K.; MARTINS., D.S.; ZUCCHI, R.A. Fruit flies (Diptera, Tephritidae) and their associations with native host plants in a remnant area of the highly endangered Atlantic Rainforest in the State of Espírito Santo, Brazil. Bulletin of Entomological Research, Cambridge, v.98, n.5, p.457-466, 2008. https://doi.org/10.1017/S0007485308005774
https://doi.org/10.1017/S000748530800577...
).

Several species of Anastrepha have a wide geographical distribution, such as A. obliqua observed in 25 Brazilian states, followed by A. fraterculus (23) and A. zenildae (18) (ZUCCHI; MORAES, 2021ZUCCHI, R.A.; MORAES, R.C.B. Fruit flies in Brazil - Anastrepha species their host plants and parasitoids. 2021. Available from: http://www.lea.esalq.usp.br/anastrepha. Acessed on: 18 May 2021.
http://www.lea.esalq.usp.br/anastrepha...
). All these three fly species were obtained from the fruits of M. tomentosa (wild-guava). Myrtaceae species are important host for fruit flies of the Anastrepha genus and C. capitata. In Brazil, only from this plant family, 74 host fruits have been for these Tephritidae flies have already been reported (LEITE et al., 2017LEITE, S.A.; CASTELLANI, M.A.; RIBEIRO, A.E.L.; COSTA, D.R.D.; BITTENCOURT, M.A.L.; MOREIRA, A.A. Fruit flies and their parasitoids in the fruit growing region of Livramento de Nossa Senhora, Bahia, with records of unprecedented interactions. Revista Brasileira de Fruticultura, Jaboticabal, v.39, n.4, p.1-10, 2017. https://doi.org/10.1590/0100-29452017592
https://doi.org/10.1590/0100-29452017592...
; ZUCCHI; MORAES, 2021ZUCCHI, R.A.; MORAES, R.C.B. Fruit flies in Brazil - Anastrepha species their host plants and parasitoids. 2021. Available from: http://www.lea.esalq.usp.br/anastrepha. Acessed on: 18 May 2021.
http://www.lea.esalq.usp.br/anastrepha...
).

Fruit collections took place in periods when there was a greater volume of precipitation (Fig. 2). This rainy season offered favorable conditions for flowering, and fruit ripening in that area of the Cerrado-Caatinga. With the incidence of rains and an increase in the relative humidity of the air in the region, populations of fruit fly species remained stable in the surveyed areas. It was observed that as rainfall increased, there was an increase in the abundance of fruit flies, mainly A. zenildae, A. obliqua, and A. fraterculus, with population peaks following the rainiest periods. Similar results were verified by AZEVEDO et al. (2010)AZEVEDO, F.R.; GUIMARÃES, J.A.; SIMPLÍCIO, A.A.F.; SANTOS, H.R. Análise faunística e flutuação populacional de moscas-das-frutas (Diptera: Tephritidae) em pomares comerciais de goiaba na região do Cariri cearense. Arquivos do Instituto Biológico, São Paulo, v.77, n.1, p.33-41, 2010. https://doi.org/10.1590/1808-1657v77p0332010
https://doi.org/10.1590/1808-1657v77p033...
in the state of Ceará, where they found that the gradual increase in precipitation rates was correlated with the increase in the capture of fruit flies. The results are also congruent with those of BATEMAN (1972)BATEMAN, M.A. The ecology of fruit flies. Annual Review of Entomology, Annapolis, v.17, n.1, p.493-518, 1972. https://doi.org/10.1146/annurev.en.17.010172.002425
https://doi.org/10.1146/annurev.en.17.01...
and ALUJA (1994)ALUJA, M. Bionomics and management of Anastrepha. Annual Review of Entomology, Annapolis, v.39, n.1, p.155-178, 1994. https://doi.org/10.1146/annurev.en.39.010194.001103
https://doi.org/10.1146/annurev.en.39.01...
carried out in commercial orchards. Therefore, the population fluctuations of adult tefritids are associated with the availability of host fruits and local climatic conditions.

CONCLUSIONS

Anastrepha zenildae, A. obliqua and A. fraterculus occur in an area of native forest and cashew orchard in the south of the state of Piauí; A. alveata, A. manihoti and A. dissimilis occurred only in the cashew orchard. Anastrepha manihoti is for the first time reported in the state of Piauí, collected in McPhil traps. Anastrepha zenildae, A. obliqua and A. fraterculus are new associations, infesting fruits of M. tomentosa (Myrtaceae) in Brazil.

The availability of host fruits influences the population fluctuation of fruit flies, mainly in the native forest area. Anastrepha zenildae was the most successful species (most abundant and dominant in the region, followed by A. obliqua, being the two most economically important pest species, in addition to A. fraterculus, in the two surveyed areas. The period of greatest abundance of fruit flies in the south-center of Piauí is the rainy season with mild temperatures (February to April).

ACKNOWLEDGEMENTS

We thank Mr. José Luiz Silva for allowing the collection of samples on his farm and Dr. Marcelo Lopes for the identification of plant species.

  • Peer Review History: Double-blind Peer Review.
  • AVAILABILITY OF DATA AND MATERIAL

    All data generated or analyzed during this study are included in this published article.
  • FUNDING

    Universidade Federal do Piauí
    Programa Institucional de Bolsas de Iniciação Científica
    Grant No. 007/2018 PROPESQ/UFPI
    Fundação de Amparo à Pesquisa do Estado do Piauí
    Grant No. 008/2018 – FAPEPI IC
    Conselho Nacional de Desenvolvimento Científico e Tecnológico
    Grant No. 301279/2015-2.
  • ETHICAL APPROVAL

    Not applicable.

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Edited by

Section Editor: Silvia Galleti

Publication Dates

  • Publication in this collection
    06 Jan 2023
  • Date of issue
    2022

History

  • Received
    10 Feb 2022
  • Accepted
    11 Oct 2022
Instituto Biológico Av. Conselheiro Rodrigues Alves, 1252 - Vila Mariana - São Paulo - SP, 04014-002 - São Paulo - SP - Brazil
E-mail: arquivos@biologico.sp.gov.br