Abstract

The objective of this study was to evaluate the potential of the pioneer plant species Bellucia grossularioides (L.) Triana (Melastomataceae) to act as a reservoir for parasitoids of fruit flies in the Brazilian Amazon. We collected 48 samples of fruits (total of 4,012 fruits, 43.98 kg) during the months of July, August and September of 2013, in 15 of the 16 municipalities of Amapá State, Brazil. All samples showed infestation by fruit flies, with rates varying from 60.6 to 239.1 puparia/kg of fruit (mean of 106.8 puparia/kg of fruit). The percentage of emergence varied 18.6 to 64.3% (mean of 39.9%). Specimens of Anastrepha coronilli Carrejo & González (Diptera: Tephritidae) were obtained from all samples collected. Specimens of Neosilba (Diptera: Lonchaeidae) were obtained from five samples, where they were represented by Neosilba bella Strikis & Prado and Neosilba glaberrima (Wiedemann). The mean percentage of parasitism was 12.8%, varying 4.7 to 26.7%. Four species of parasitoids were obtained: Doryctobracon areolatus (Szépligeti), Doryctobracon sp.2, Opius bellus Gahan (Braconidae) and Aganaspis pelleranoi (Brèthes) (Figitidae). Doryctobracon areolatus, present in all municipalities sampled, was the most abundant species. Considering that B. grossularioides is a plant species that is abundant in the area sampled, its relevance with respect to the maintenance of the population of parasitoids is discussed in the context of the integrated management of fruit flies in the Amazon.

Keywords:
Biological control; Natural enemies; Anastrepha coronilli; Doryctobracon areolatus

Resumo

O objetivo deste trabalho foi avaliar o potencial da espécie vegetal pioneira Bellucia grossularioides (L.) Triana (Melastomataceae) para atuar como reservatório de parasitoides de moscas-das-frutas na Amazônia brasileira. Foram realizadas coletas de 48 amostras de frutos (4.012 frutos, 43,98 kg) durante os meses de julho, agosto e setembro de 2013, em 15 dos 16 municípios do estado do Amapá, Brasil. Todas as amostras apresentaram infestação por dípteros, com índices que variaram de 60,6 a 239,1 pupários/kg de fruto (média de 106,8 pupários/kg de fruto). O percentual de emergência variou de 18,6% a 64,3% (média de 39,9%). Exemplares de Anastrepha coronilli Carrejo & González (Diptera: Tephritidae) foram obtidos de todas as amostras coletadas. Exemplares de Neosilba (Diptera: Lonchaeidae) foram obtidos de cinco amostras, sendo representadas por Neosilba bella Strikis & Prado e Neosilba glaberrima (Wiedemann). O percentual médio de parasitismo foi de 12,8%, variando de 4,7% a 26,7%. Quatro espécies de parasitoides foram obtidas: Doryctobracon areolatus (Szépligeti), Doryctobracon sp.2, Opius bellus Gahan (Braconidae) e Aganaspis pelleranoi (Brèthes) (Figitidae). Doryctobracon areolatus, presente em todos os municípios amostrados, foi a espécie mais abundante. Considerando-se que B. grossularioides é uma espécie vegetal abundante na área amostrada, sua relevância quanto à manutenção da população de parasitoides é discutida no contexto do manejo integrado de moscas-das-frutas na Amazônia.

Palavras-chave:
Controle biológico; Inimigos naturais; Anastrepha coronilli; Doryctobracon areolatus

Introduction

Fruit flies (Diptera: Tephritidae) are among the most important pests worldwide due to their economic impacts and the severe quarantine restrictions imposed by many countries to prevent their entry (Aluja 1994ALUJA, M. 1994. Bionomics and management of Anastrepha. Annu. Rev. Entomol. 39 (1): 155-178., Follett & Neven 2006FOLLETT, PA. & NEVEN, LG 2006. Current trends in quarantine entomology. Annu. Rev. Entomol. 51: 359-385., Aluja & Mangan 2008ALUJA, M. & MANGAN, RL. 2008. Fruit fly (Diptera: Tephritidae) host status determination: critical conceptual, methodological, and regulatory considerations. Annu. Rev. Entomol. 53: 473-502.). The information needed to understand the biology, ecology and evolution of these insects should be determined in areas of practically unchanged native vegetation, especially when one considers that the rapid deforestation of the tropics may be causing the disappearance or even extinction of many species of fruit flies, consequently threatening the associated native parasitoid species (Hymenoptera) (Aluja 1999ALUJA, M. 1999. Fruit fly (Diptera: Tephritidae) research in Latin America: myths, realities and dreams. An. Soc. Entomol. Brasil. 28 (4): 565-594., Aluja et al., 2003ALUJA, M., RULL, J., SIVINSKI, J., NORRBOM, AL., WHARTON, RA., MACÍAS-ORDÓÑEZ, R., DÍAZ-FLEISCHER, F. & LÓPEZ, M. 2003. Fruit flies of the genus Anastrepha (Diptera: Tephritidae) and associated native parasitoids (Hymenoptera) in the Tropical Rainforest Biosphere Reserve of Montes Azules, Chiapas, Mexico. Environ. Entomol. 32 (6): 1377-1385.). These insects, especially those belonging to the family Braconidae, play an important role in the natural biological control of fruit flies, considered as pests (López et al., 1999LÓPEZ, M., ALUJA, M. & SIVINSKI, J. 1999. Hymenopterous larval-pupal and pupal parasitoids of Anastrepha flies (Diptera: Tephritidae) in Mexico. Biolog. Control. 15: 119-129., Ovruski et al., 2000OVRUSKI, SM., ALUJA, M., SIVINSKI, J., WHARTON, RA 2000. Hymenopteran parasitoids on fruit-infesting Tephritidae (Diptera) in Latin America and the Southern United States: diversity, distribution, taxonomic status and their use in fruit fly biological control. Integrated Pest Manag Rev.5 (2): 81-107.).

In a study carried out in the state of Veracruz, Mexico, López et al. (1999)LÓPEZ, M., ALUJA, M. & SIVINSKI, J. 1999. Hymenopterous larval-pupal and pupal parasitoids of Anastrepha flies (Diptera: Tephritidae) in Mexico. Biolog. Control. 15: 119-129. demonstrated the need to protect native vegetation due to its important role as a reservoir of fruit flies parasitoids. The authors reported that native plants in the wild harbor significantly more parasitoids per fruit than do cultivated plants, corroborating the work of Sivinski (1991)SIVINSKI, J 1991.The influence of host fruit morphology on parasitization rates in the Caribbean fruit fly, Anastrepha suspensa. Entomophaga. 36 (3): 447-454. and Hernández-Ortíz et al. (1994)HERNÁNDEZ-ORTÍZ, V., PÉREZ-ALONSO, R. & WHARTON, RA 1994. Native parasitoids associated with the genus Anastrepha (Dipt.: Tephritidae) in Los Tuxtlas, Veracruz, Mexico. Entomophaga. 39 (2): 171-178..

López et al. (1999)LÓPEZ, M., ALUJA, M. & SIVINSKI, J. 1999. Hymenopterous larval-pupal and pupal parasitoids of Anastrepha flies (Diptera: Tephritidae) in Mexico. Biolog. Control. 15: 119-129., in summarizing studies with parasitoids in various countries, indicated that: 1) Doryctobracon areolatus (Szépligeti) (Hymenoptera: Braconidae) is the most abundant and widespread native parasitoid of Anastrepha; 2) most parasitoid species are generalists (they attack many Anastrepha species); and 3) many native species are found preferentially parasitizing Anastrepha larvae in wild native fruit trees.

Aluja (1999)ALUJA, M. 1999. Fruit fly (Diptera: Tephritidae) research in Latin America: myths, realities and dreams. An. Soc. Entomol. Brasil. 28 (4): 565-594. suggested that in regions where producers have few resources, the following actions can be promoted as alternatives to the wide use of insecticides: 1) the preservation of habitats where parasitoids develop; 2) artificial increase of certain reservoirs of parasitoids and species of trees promoting and multiplying biodiversity. More recently, Aluja et al. (2014)ALUJA, M., SIVINSKI, J., VAN DRIESCHE, R., ANZURES-DADDA, A. & GUILLÉN, L. 2014. Pest management through tropical tree conservation. Biodivers. Conserv. 23 (4): 831-853. proposed three categories of fruit plants of interest for the conservative biological control of fruit flies: 1) parasitoid multiplier plants: species that serve as alternative hosts for fruit flies pests when their commercial hosts are not available, in which they are exceptionally vulnerable to parasitism; 2) parasitoid reservoir plants: native or introduced trees in whose fruits non-pest fruit flies serve as hosts of generalist parasitoids that are capable of attacking tephritid pests on other commercially grown fruit species; and 3) pest-based parasitoid reservoir plants: native or introduced species that are not economically important locally but harbor fruit flies that would otherwise be pests and serve as hosts for parasites of major pests in the vicinity.

Bellucia is a Neotropical plant genus comprising seven species (Renner 1986RENNER, SS. 1986. Reproductive biology of Bellucia (Melastomataceae). Acta Amaz. 16: 197-208., 1987). In general, activities such as timber extraction, road construction and pasture formation have provided excellent habitats for species of this genus. Bellucia grossularioides (L.) Triana (Figure 1) occurs from Mexico to the Brazilian Amazon. It grows in areas of altered and unchanged vegetation, being adapted to a variety of soil types. It is among the most important pioneer species in terms of number of individuals per area in the Central Amazon. It flowers and bears fruit for long periods or continuously throughout the year. Eventually, fruits are consumed by animal species (especially mammals) and, less frequently, by humans. They usually reach a maximum height of 20 to 25 m. The minimum diameter for the beginning of the reproductive phase is 7.8 cm. The main dispersants are birds and monkeys (Bentos et al., 2008BENTOS, TV., MESQUITA, RCG. & WILLIAMSON, GB 2008. Reproductive phenology of Central Amazon pioneer trees. Trop. Conserv. Sci. 1 (3): 186-203., Santos et al., 2012SANTOS, GGA, SANTOS, BA & NASCIMENTO, HEM 2012. Contrasting demographic structure of short- and long-lived pioneer tree species on Amazonian forest edges. Biotropica. 44 (6): 771-778.).

Anastrepha coronilli Carrejo & González (Diptera: Tephritidae) is a species of the fraterculus group, considered to be of no economic importance, especially associated with Melastomataceae species (Norrbom et al., 2013NORRBOM, A.L., KORYTKOWSKI, C.A., ZUCCHI, R.A., URAMOTO, K., VENABLE, G.L., MCCORMICK, J. & DALLWITZ, M.J. 2012. Anastrepha and Toxotrypana: descriptions, illustrations, and interactive keys. Version: 28th September 2013. http://delta-intkey.com.
http://delta-intkey.com... ). In the Brazilian Amazon, some surveys were carried out to determine the infestation rates of B. grossularioides by A. coronilli and associated parasitoids. Parasitism of up to 28% of puparia was recorded in samples from Ferreira Gomes, Amapá State (Deus et al., 2013DEUS, EG., PINHEIRO, LS., LIMA, CR., SOUSA, MSM., GUIMARÃES, JA., STRIKIS, PC. & ADAIME, R 2013. Wild hosts of frugivorous dipteran (Tephritidae and Lonchaeidae) and associated parasitoids in the Brazilian Amazon. Fla. Entomol. 96 (4): 1621-1625.). The species of parasitoids recorded were: 1) Braconidae - Asobara anastrephae (Muesebeck) (Deus et al., 2009DEUS, EG., SILVA, RA., NASCIMENTO, DB., MARINHO, CF. & ZUCCHI, RA 2009. Hospedeiros e parasitóides de espécies de Anastrepha (Diptera, Tephritidae) em dois municípios do Estado do Amapá. Rev. Agric. 84 (3): 194-203.), Doryctobracon areolatus (Bomfim et al., 2007BOMFIM, DA., UCHÔA-FERNANDES, MA. & BRAGANÇA, MAL 2007. Hosts and Parasitoids of Fruit Flies (Diptera: Tephritoidea) in the State of Tocantins, Brazil. Neotrop. Entomol. 36 (6): 984-986., Deus et al., 2009DEUS, EG., SILVA, RA., NASCIMENTO, DB., MARINHO, CF. & ZUCCHI, RA 2009. Hospedeiros e parasitóides de espécies de Anastrepha (Diptera, Tephritidae) em dois municípios do Estado do Amapá. Rev. Agric. 84 (3): 194-203., Pereira 2009PEREIRA, JDB. 2009. Contribuição ao conhecimento de moscas-das-frutas (Tephritidae e Lonchaeidae) no Pará: diversidade, hospedeiros e parasitóides associados. Dissertação de Mestrado. Universidade Federal do Amapá, Macapá., Pereira et al., 2010PEREIRA, JDB, BURITI, DP, LEMOS, WP, SILVA, WR, SILVA, RA Espécies de Anastrepha Schiner (Diptera, Tephritidae), seus hospedeiros e parasitoides nos estados do Acre e Rondônia, Brasil. Biota Neotropica. 10 (3): http://www.biotaneotropica.org.br/v10n3/pt/abstract?short-communication+bn00410032010. (last access on 31/07/2017)
http://www.biotaneotropica.org.br/v10n3/... ,Marsaro Júnior et al., 2011MARSARO JUNIOR, AL., SOUZA-FILHO, MF., ADAIME, R. & STRIKIS, PC 2011. First report of natural infestation of Pereskia aculeata Mill. (Cactaceae) by Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) in Brazil. Rev. Agric. 86 (2): 151-154., Ronchi-Teles et al., 2011RONCHI-TELES, B, DUTRA, VS, TREGUE-COSTA, AP, AGUIAR-MENEZES, EL, MESQUITA, ACA & SILVA, JG 2011. Natural host plants and native parasitoids associated with Anastrepha pulchra and other Anastrepha species (Diptera: Tephritidae) in Central Amazon, Brazil. Fla. Entomol. 94 (2): 347-349, Silva et al., 2011a, Deus et al., 2013DEUS, EG., PINHEIRO, LS., LIMA, CR., SOUSA, MSM., GUIMARÃES, JA., STRIKIS, PC. & ADAIME, R 2013. Wild hosts of frugivorous dipteran (Tephritidae and Lonchaeidae) and associated parasitoids in the Brazilian Amazon. Fla. Entomol. 96 (4): 1621-1625., Dutra et al., 2013DUTRA, VS., RONCHI-TELES, B., GARCIA, MVB, ADAIME, R. & SILVA, JG 2013. Native hosts and parasitoids associated with Anastrepha fractura and other Anastrepha species (Diptera: Tephritidae) in the Brazilian Amazon. Fla. Entomol. 96 (1): 270-273.), Doryctobracon crawfordi (Viereck) (Deus et al., 2013DEUS, EG., PINHEIRO, LS., LIMA, CR., SOUSA, MSM., GUIMARÃES, JA., STRIKIS, PC. & ADAIME, R 2013. Wild hosts of frugivorous dipteran (Tephritidae and Lonchaeidae) and associated parasitoids in the Brazilian Amazon. Fla. Entomol. 96 (4): 1621-1625.), Doryctobracon sp. (Bomfim et al., 2007BOMFIM, DA., UCHÔA-FERNANDES, MA. & BRAGANÇA, MAL 2007. Hosts and Parasitoids of Fruit Flies (Diptera: Tephritoidea) in the State of Tocantins, Brazil. Neotrop. Entomol. 36 (6): 984-986.), Opius bellus Gahan (Dutra et al., 2013DUTRA, VS., RONCHI-TELES, B., GARCIA, MVB, ADAIME, R. & SILVA, JG 2013. Native hosts and parasitoids associated with Anastrepha fractura and other Anastrepha species (Diptera: Tephritidae) in the Brazilian Amazon. Fla. Entomol. 96 (1): 270-273., Adaime et al. 2017ADAIME, R., SOUSA, MSM., JESUS BARROS, CR., DEUS, EG., PEREIRA, JF., STRIKIS, PC. & SOUZA-FILHO, MF. 2017. Frugivorous Flies (Diptera: Tephritidae, Lonchaeidae), their host plants, and associated parasitoids in the extreme north of Amapá State, Brazil. Fla. Entomol. 100 (2): 316-324.) and Utetes anastrephae (Viereck) (Dutra et al., 2013DUTRA, VS., RONCHI-TELES, B., GARCIA, MVB, ADAIME, R. & SILVA, JG 2013. Native hosts and parasitoids associated with Anastrepha fractura and other Anastrepha species (Diptera: Tephritidae) in the Brazilian Amazon. Fla. Entomol. 96 (1): 270-273.); 2) Figitidae - Aganaspis nordlanderi Wharton (Ronchi-Teles et al., 2011RONCHI-TELES, B, DUTRA, VS, TREGUE-COSTA, AP, AGUIAR-MENEZES, EL, MESQUITA, ACA & SILVA, JG 2011. Natural host plants and native parasitoids associated with Anastrepha pulchra and other Anastrepha species (Diptera: Tephritidae) in Central Amazon, Brazil. Fla. Entomol. 94 (2): 347-349) and Aganaspis pelleranoi (Brèthes) (Deus et al., 2013DEUS, EG., PINHEIRO, LS., LIMA, CR., SOUSA, MSM., GUIMARÃES, JA., STRIKIS, PC. & ADAIME, R 2013. Wild hosts of frugivorous dipteran (Tephritidae and Lonchaeidae) and associated parasitoids in the Brazilian Amazon. Fla. Entomol. 96 (4): 1621-1625., Dutra et al., 2013DUTRA, VS., RONCHI-TELES, B., GARCIA, MVB, ADAIME, R. & SILVA, JG 2013. Native hosts and parasitoids associated with Anastrepha fractura and other Anastrepha species (Diptera: Tephritidae) in the Brazilian Amazon. Fla. Entomol. 96 (1): 270-273.). In all studies carried out in the region, D. areolatus was the predominant species.

This work was carried out to determine the potential of B. grossularioides to act as a reservoir of fruit flies parasitoids in the Amapá State in the Brazilian Amazon.

Material and Methods

1. Geographic area covered

The Amapá State (area of 143,453.70 km²) is situated in Eastern Amazon and is considered the most preserved of the country. It is bordered to the south and west by Pará State, to the east by the Atlantic Ocean, to the north by French Guiana and to the northwest by Suriname (Figure 2) (Porto 2007PORTO, J. 2007. Amapá: principais transformações econômicas e institucionais – 1943 a 2000. Edição do autor, Macapá, Amapá.). The climate in the region, according to the Koëppen-Geiger classification, is Aw (tropical savanna) and Am (tropical monsoon) types, with mean annual precipitation between 2,300 and 2,400 mm (Pell et al., 2007PEEL, MC., FINLAYSON, BL. & McMAHON, TA. 2007. Updated world map of the Köoppen-Geiger climate classification. Hydrol. Earth Syst. Sci. 11: 1633-1644.). The rainy season occurs from January to June and a characteristically dry period is more frequent from September to November. The mean annual temperature is 26ºC (IBGE 2011IBGE - INSTITUTO BRASILEIRO DE GEOGRAFIA E ESTATÍSTICA. http://www.ibge.gov.br/cidadesat/topwindow.htm?1 (last access in 07/08/2011.)
http://www.ibge.gov.br/cidadesat/topwind... ). The region is composed of domains of cerrado, floodplain forest, upland forest and the transition forests cerrado/forest and cerrado/floodplain forest (IEPA 2002IEPA - INSTITUTO DE PESQUISAS CIENTÍFICAS E TECNOLÓGICAS DO ESTADO DO AMAPÁ. 2002. Macrodiagnóstico do Estado do Amapá: primeira aproximação do ZEE. Macapá: IEPA. 140 p.).

2. Collection and processing of samples

Samples of B. grossularioides fruits were collected during July, August and September of 2013 in 15 of the 16 municipalities of Amapá State (Table 1 and Figure 2). The collections were made especially in the side of vicinal roads, locating plants with a good amount of fruits. Each sample was composed of fruits of the same plant, whose size depended on the availability of fruits. The fruits were collected directly from the plant and ground (intact fruits, freshly fallen), weighed on a digital balance and placed in plastic jars (14 cm in diameter), under on a thin layer of moistened sand, covered with organza and an open lid. The geographical coordinates of the sampling points were determined with the aid of a GPS.

In the laboratory of Plant Protection at Embrapa Amapá, the fruits were transferred to plastic trays, under a layer of moistened sand, covered with organza and fastened in place with rubber bands. Every seven days the samples were examined. The puparia obtained from each sample were packed in plastic bottles (6.5 cm in diameter) containing a thin layer of moist vermiculite. The bottles were kept in climatized chambers under controlled conditions of temperature (26±0.5ºC), relative humidity (70 ± 10%) and photophase (12 hours) and observed daily to determine the number of fruit flies and parasitoids. The emerged adults were preserved in 70% ethanol for later identification.

3. Identification of insects

The insects were identified using the keys of Zucchi (2000)ZUCCHI, R.A. 2000. Taxonomia. In Moscas-das-frutas de importância econômica no Brasil: conhecimento básico e aplicado (A. MALAVASI & R.A. ZUCCHI, eds.). Holos, Ribeirão Preto, p. 13-24., Canal and Zucchi (2000)CANAL, NA & ZUCCHI, RA. 2000. Parasitóides – Braconidae. In Moscas-das-frutas de importância econômica no Brasil: conhecimento básico e aplicado (A. MALAVASI & R.A. ZUCCHI, eds.). Holos, Ribeirão Preto, p.119-126., Marinho et al. (2011)MARINHO, CF, SILVA, RA & ZUCCHI, RA. 2011. Chave de identificação de Braconidae (Alysiinae e Opiinae) parasitoides de larvas frugívoras na região Amazônica. In Moscas-das-frutas na Amazônia brasileira: diversidade, hospedeiros e inimigos naturais (R.A. SILVA, W.P. LEMOS & R.A. ZUCCHI, eds.). Embrapa Amapá, Macapá, p. 91-102., Strikis (2011)STRIKIS, PC 2011. Description of 11 new species of genus Neosilba (Diptera: Lonchaeidae) from Brazil, its hosts and geographical distribution. Trends in Entomol. 7: 67-79. and Zucchi et al. (2011)ZUCCHI, R.A., URAMOTO, K. & SOUZA-FILHO, M.F. 2011. Chave ilustrada para as espécies de Anastrepha da Região Amazônica. In Moscas-das-frutas na Amazônia brasileira: diversidade, hospedeiros e inimigos naturais (R.A. SILVA, W.P. LEMOS & R.A. ZUCCHI, eds.). Embrapa Amapá, Macapá, p. 71-90.. Voucher specimens were deposited in the Plant Protection Laboratory of Embrapa Amapá.

4. Data analysis

We calculated: 1) infestation rate (number of puparia obtained in the sample ÷ weight of the sample), expressed as number of puparia/kg of fruit; 2) emergence percentage [(number of emerged adults ÷ number of puparia obtained in the fruit) x 100], expressed as a percentage; and 3) percentage of parasitism in pupae [(number of emerged parasitoids ÷ number of puparia obtained) x 100], expressed as a percentage.

Results

Forty-eight samples of B. grossularioides fruits (4,012 fruits, 43.98 kg) were collected, covering an extensive area of Amapá State (Table 2, Figure 1). All samples showed infestation by fruit flies (Table 2). A total of 4,307 puparia were obtained, with infestation rates varying from 60.6 to 239.1 puparia/kg of fruit (mean of 106.8 puparia/kg of fruit).

The emergence percentage ranged 18.6 to 64.3%, with a mean of 39.9% (Table 2). Specimens of A. coronilli Carrejo & González, 1993 (Diptera: Tephritidae) were obtained from all collected samples, totaling 571♀ and 548♂. Specimens of Neosilba (Diptera: Lonchaeidae) were obtained from five samples, represented by Neosilba bella Strikis & Prado (14♂) and N. glaberrima (Wiedemann) (1♂).

The mean percentage of parasitism was 12.8%, ranging 4.7 to 26.7% (Table 2). Only three samples (6.3% of the total of 48) did not show parasitism. Four species of parasitoids were obtained: Doryctobracon areolatus (582 specimens), Doryctobracon sp.2 (1), Opius bellus (3) (Braconidae) and Aganaspis pelleranoi (3) (Figitidae). Doryctobracon areolatus, present in all municipalities sampled, was the most abundant species

Discussion

1. Infestion rate and percentage of parasitism

In the state of Amapá, some other surveys had been carried out to determine the infestation rates of B. grossularioides by fruit flies and associated parasitoids. Table 3 shows data for 11 municipalities, with 97.8% of the samples being infested (the highest infestation rate was 242.5 puparia/kg, in samples from Mazagão). Only A. coronilli specimens were obtained.

Additionally, Jesus-Barros et al. (2012)JESUS-BARROS, CR., ADAIME, R., OLIVEIRA, MN., SILVA, WR., COSTA-NETO, SV. & SOUZA-FILHO, MF 2012. Anastrepha (Diptera: Tephritidae) species, their hosts and parasitoids (Hymenoptera: Braconidae) in five municipalities of the state of Amapá, Brazil. Fla. Entomol. 95 (3): 694-705. carried out extensive fruit sampling in five municipalities of Amapá (Cutias do Araguari, Itaubal do Piririm, Ferreira Gomes, Pracuúba and Tartarugalzinho). Thirty samples (1,892 fruits, 21.16 kg) of B. grossularioides were collected, and 28 of them were infested by fruit flies. A total of 636 puparia (infestation rate of 30.06 puparia/kg) were obtained, from which A. coronilli (225), A. striata Schiner (24) and A. antunesi Lima (3) emerged. The fact that A. striata and A. antunesi specimens were found is noteworthy in the present study. However, in relation to the total number of females obtained, the species corresponded to only 9.5 and 1.19%, respectively. In the state of Rondônia, Pereira et al. (2010)PEREIRA, JDB, BURITI, DP, LEMOS, WP, SILVA, WR, SILVA, RA Espécies de Anastrepha Schiner (Diptera, Tephritidae), seus hospedeiros e parasitoides nos estados do Acre e Rondônia, Brasil. Biota Neotropica. 10 (3): http://www.biotaneotropica.org.br/v10n3/pt/abstract?short-communication+bn00410032010. (last access on 31/07/2017)
http://www.biotaneotropica.org.br/v10n3/... obtained only one specimen of A. striata in fruits of B. grossularioides.

In other states of the Brazilian Amazon, few samples of B. grossularioides were collected (Table 4). The highest infestation rate recorded was 141.2 puparia/kg, in fruits from the state of Rondônia (Pereira et al., 2010)PEREIRA, JDB, BURITI, DP, LEMOS, WP, SILVA, WR, SILVA, RA Espécies de Anastrepha Schiner (Diptera, Tephritidae), seus hospedeiros e parasitoides nos estados do Acre e Rondônia, Brasil. Biota Neotropica. 10 (3): http://www.biotaneotropica.org.br/v10n3/pt/abstract?short-communication+bn00410032010. (last access on 31/07/2017)
http://www.biotaneotropica.org.br/v10n3/... .

The most frequent host of A. coronilli is actually B. grossularioides, and it is also found in Bellucia dichotoma Cogn. (Table 5). Four other hosts were also recorded for the species in the Brazilian Amazon, and of them, only guava (Psidium guajava L.) is of commercial importance. However, it should be noted that the frequency and abundance of A. coronilli in guava is very low. In intensive work in Amapá, Jesus-Barros et al. (2012)JESUS-BARROS, CR., ADAIME, R., OLIVEIRA, MN., SILVA, WR., COSTA-NETO, SV. & SOUZA-FILHO, MF 2012. Anastrepha (Diptera: Tephritidae) species, their hosts and parasitoids (Hymenoptera: Braconidae) in five municipalities of the state of Amapá, Brazil. Fla. Entomol. 95 (3): 694-705. collected 255 guava samples (9,657 fruits, 425.97 kg), of which 222 showed infestation by fruit flies. A total of 17,531 puparia were obtained (infestation rate of 41.16 puparia/kg), from which six species of Anastrepha emerged: A. striata (4176♀), A. fraterculus (Wiedemann) (95♀), A. coronilli (16♀), A. parishi Stone (15♀), A. distincta Greene (13♀) and A. zenildae Zucchi (2♀). It can be seen that only 0.37% of females obtained from guava in that study were A. coronilli. In a survey in Rondônia, Pereira et al. (2010)PEREIRA, JDB, BURITI, DP, LEMOS, WP, SILVA, WR, SILVA, RA Espécies de Anastrepha Schiner (Diptera, Tephritidae), seus hospedeiros e parasitoides nos estados do Acre e Rondônia, Brasil. Biota Neotropica. 10 (3): http://www.biotaneotropica.org.br/v10n3/pt/abstract?short-communication+bn00410032010. (last access on 31/07/2017)
http://www.biotaneotropica.org.br/v10n3/... obtained only one specimen of A. coronilli in guava.

In Brazil, records of species of lance flies associated with fruit species are scarce, because in many studies their presence is neglected. However, the classification of some species as pests has recently attracted the attention of researchers (Veloso et al., 1994VELOSO, VRS, FERNANDES, PM, ROCHA, MR, QUEIROZ, MV & SILVA, RMR 1994. Armadilhas para o monitoramento e controle das moscas-das-frutas Anastrepha spp. e Ceratitis capitata (Wied.). An. Soc. Entomol. Brasil. 23 (3): 487–493., Uchôa-Fernandes & Zucchi 1999UCHÔA-FERNANDES, MA & ZUCCHI, RA 1999. Metodología de colecta de Tephritidae y Lonchaeidae frugívoros (Diptera: Tephritoidea) y sus parasitoides (Hymenoptera). An. Soc. Entomol. Brasil. 28 (4): 601-610., Uchôa-Fernandes et al., 2002UCHÔA-FERNANDES, M.A., OLIVEIRA, I., MOLINA, R.M.S. & ZUCCHI, R.A. 2002. Species diversity of frugivorous flies (Diptera: Tephritoidea) from hosts in the Cerrado of the State of Mato Grosso do Sul, Brazil. Neotrop. Entomol. 31 (4): 515-524., Bittencourt et al., 2006BITTENCOURT, MAL., SILVA, ACM., BOMFIM, ZV., SILVA, VES., ARAÚJO, EL. & STRIKIS, PC 2006. Novos Registros de Espécies de Neosilba (Diptera: Lonchaeidae) na Bahia. Neotrop. Entomol. 2 (35): 282-283.). Recent studies indicate that larvae of some species of Lonchaeidae colonize a larger number of fruit species than larvae of flies of the family Tephritidae (Ferreira et al., 2003FERREIRA, HJ., VELOSO, VRS., NAVES, RV. & BRAGA-FILHO, JR. 2003. Infestação de moscas-das-frutas em variedades de manga (Mangifera indica L.) no estado de Goiás. Pesqui. Agropecu. Trop. 33 (1): 43-48.).

Recently, Strikis et al. (2011)STRIKIS, P.C., DEUS, E.G., SILVA, R.A., PEREIRA, J.D.B., JESUS, C.R. & MARSARO JÚNIOR, A.L. 2011. Conhecimento sobre Lonchaeidae na Amazônia brasileira. In Moscas-das-frutas na Amazônia brasileira: diversidade, hospedeiros e inimigos naturais (R.A. SILVA, W.P. LEMOS & R.A. ZUCCHI, eds.). Embrapa Amapá, Macapá, p. 205-216. collected available information on Lonchaeidae in the Brazilian Amazon and published new records of lance flies obtained from wild and cultivated fruit species. So far, only N. pendula (Bezzi) had been reported in fruits of B. grossularioides in Cantá, Roraima. In the present work the species N. bella and N. glaberrima are reported for the first time in this plant species (Table 5). Therefore, it is possible that these species use fruits of B. grossularioides as an alternative host.

The results indicated considerable parasitism (mean of 12.8% of parasitized puparia) (Table 2). In addition, 93.7% of the samples had parasitized puparia (43 of 48 samples). Four species of parasitoids were obtained, where Doryctobracon sp.2 was recorded for the first time in larvae of A. coronilli in fruits of B. grossularioides. It is a species that has been recently collected in Brazil but not yet formally described (Marinho et al., 2011MARINHO, CF, SILVA, RA & ZUCCHI, RA. 2011. Chave de identificação de Braconidae (Alysiinae e Opiinae) parasitoides de larvas frugívoras na região Amazônica. In Moscas-das-frutas na Amazônia brasileira: diversidade, hospedeiros e inimigos naturais (R.A. SILVA, W.P. LEMOS & R.A. ZUCCHI, eds.). Embrapa Amapá, Macapá, p. 91-102.). In other studies carried out in Amapá, the highest rate of parasitism of A. coronilli puparia was 28.0%, obtained in Ferreira Gomes. In most samples, the rate obtained has been greater than 10% (Table 3). Jesus-Barros et al. (2012)JESUS-BARROS, CR., ADAIME, R., OLIVEIRA, MN., SILVA, WR., COSTA-NETO, SV. & SOUZA-FILHO, MF 2012. Anastrepha (Diptera: Tephritidae) species, their hosts and parasitoids (Hymenoptera: Braconidae) in five municipalities of the state of Amapá, Brazil. Fla. Entomol. 95 (3): 694-705. found parasitism of 5.97%, with D. areolatus (37 specimens) and A. anastrephae (1) being collected in five municipalities of Amapá. In other places in the Brazilian Amazon, the highest parasitism rate observed was 12.5% in Roraima (Table 4) (Marsaro Júnior et al., 2011MARSARO JUNIOR, AL., SOUZA-FILHO, MF., ADAIME, R. & STRIKIS, PC 2011. First report of natural infestation of Pereskia aculeata Mill. (Cactaceae) by Ceratitis capitata (Wiedemann) (Diptera: Tephritidae) in Brazil. Rev. Agric. 86 (2): 151-154.).

It should be considered that the rates of parasitism found in studies in which fruits were collected in the field and placed under laboratory conditions are not real because the fruits were removed from the natural environment, possibly with eggs and larvae of first and second instars of fruit flies. Thus, when immatures are removed from the field, they are no longer likely to be parasitized (Uchôa-Fernandes et al., 2003UCHÔA-FERNANDES, MA, MOLINA, RMS, OLIVEIRA, I, ZUCCHI, RA, CANAL, NA & DÍAZ, NB 2003. Larval endoparasitoids (Hymenoptera) of frugivorous flies (Diptera, Tephritoidea) reared from fruits of the cerrado of the State of Mato Grosso do Sul, Brazil. Rev. Bras. entomol. 47 (2): 181-186.). Therefore, it is estimated that the actual parasitism rate in A. coronilli larvae infesting B. grossularioides fruits is even higher.

In the present work, nine species of fruit fly parasitoids (two from Figitidae and seven from Braconidae) have been found on B. grossularioides in the Brazilian Amazon (Table 6).

2. Implications for the integrated management of fruit flies

The results demonstrate the capacity of B. grossularioides to act as a fruit fly parasitoid reservoir (as proposed by Aluja et al., 2014ALUJA, M., SIVINSKI, J., VAN DRIESCHE, R., ANZURES-DADDA, A. & GUILLÉN, L. 2014. Pest management through tropical tree conservation. Biodivers. Conserv. 23 (4): 831-853.) in the state of Amapá and, therefore, in the Brazilian Amazon. The collections have been more extensive than in any other state in the region. The plant species clearly plays a fundamental role in the maintenance of the fruit fly parasitoid population. It is a pioneer species that is widely distributed and adapted to various soil conditions. Because it is not a species of economic interest, the biological control of fruit flies is favored, since the possibility of removal of the plants due to some commercial interest therefore does not seem to be a threat. Although fruits are consumed by animals, especially mammals, there does not seem to be considerable reduction in the amount of fruits on the ground, which potentially contains parasitoids. In general, when the infested fruits fall, the larvae abandon it and enter the soil, to proceed to the pupa phase. Thus, even if a certain amount of fruit is consumed, the parasitoids that infested fly larvae would be preserved, since they would already be in the pupa stage, in the soil.

In summary, the results suggest that B. grossularioides is a species that can be conserved in its environments of occurrence for maintenance of the parasitoid population. Another possibility that presents itself is to cultivate this plants species around orchards. The plants would act as reservoirs of parasitoids, which, being generalists, can help to reduce populations of pest species.

Another important point is that B. grossularioides hosts almost exclusively A. coronilli, a species of no economic importance. Thus, when considering the amount of fruits sampled and the total number of A. coronilli specimens obtained, the number of adults of other species becomes very small. Still, it is suggested that further, intensive surveys be conducted for a whole year to substantiate this notion.

It is therefore possible to attempt to develop systems through which parasitoid reservoirs can be managed to naturally increase the number of parasitoids in areas of native vegetation (López et al., 1999LÓPEZ, M., ALUJA, M. & SIVINSKI, J. 1999. Hymenopterous larval-pupal and pupal parasitoids of Anastrepha flies (Diptera: Tephritidae) in Mexico. Biolog. Control. 15: 119-129.). Thus, cultivation or maintenance of the natural populations of B. grossularioides could contribute to increasing the community of fruit flies parasitoids without the risk of increasing the population of pest species.

3. Research demands

The results obtained open new perspectives of research for the better understanding of the tritrophic interaction between B. grossularioides, A. coronilli and associated parasitoids. Studies based on individualized fruits could help considerably in this regard, as detailed by Silva et al. (2011b)SILVA, R.A., DEUS, E.G., RAGA, A., PEREIRA, J.D.B., SOUZA FILHO, M.F. & COSTA NETO, S.V. 2011b. Monitoramento de moscas-das-frutas na Amazônia: amostragem de frutos e uso de armadilhas. In Moscas-das-frutas na Amazônia brasileira: diversidade, hospedeiros e inimigos naturais (R.A. SILVA, W.P. LEMOS & R.A. ZUCCHI, eds.). Embrapa Amapá, Macapá, p. 33-50.. Undoubtedly, it is essential to study the phenology of B. grossularioides in local conditions of natural occurrence, detailing the fruiting period, the consequent infestation by fruit flies and the corresponding parasitism rate throughout the year. To quantify the fruits produced per plant per year is a determinant for estimating the contribution of each individual as parasitoid reservoir.

Moreover, it is also important to study the biology of A. coronilli and its behavioral aspects. In general, studies on species of no economic importance have been neglected. The main aspects to be studied are feeding and reproduction behaviors, as well as biological aspects, especially reproductive potential, immature development time and adult longevity.

Acknowledgments

We thank Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the Research Productivity grant awarded to Ricardo Adaime, Carlos Alberto Morais for his help with fieldwork, and the student Orimax Monteiro Cruz for help with laboratory work. Dr. A. Leyva (USA) provided English translation and editing of the manuscript.

References

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