Printer Friendly

Frugivorous flies (Diptera: Tephritidae, Lonchaeidae), their host plants, and associated parasitoids in the extreme north of Amapa State, Brazil.

Fruit flies (Diptera: Tephritidae) are globally known as pests of fruit crops, due to the direct and indirect damage they cause to production (Aluja 1994). The family Tephritidae is comprised of over 5,000 species grouped into 500 genera. Approximately 70 species are confirmed pests, whereas others may potentially cause damage to crops (White & Elson-Harris 1992; Uchoa 2012). The Anastrepha Schiner species, Ceratitis capitata (Wiedemann) and Bactrocera carambolae Drew & Hancock, cause considerable damage to both commercial and noncommercial fruit trees in South America (Zucchi 2001; Vayssieres et al. 2013; Lemos et al. 2014).

In recent years, particularly in Brazil, frugivorous dipterans in the family Lonchaeidae have been reported to be primary invaders of commercial plant species. Neosilba zadolicha McAlpine & Steyskal, Neosilba pendula (Bezzi), Neosilba glaberrima (Wiedemann), and Neosilba perezi Romero & Ruppel, are currently viewed as pests due to the damage they cause to fruits or other structures of different plant species (Lourencao et al. 1996; Uchoa 2012; Lemos et al. 2015).

To date, 120 species of Anastrepha have been reported in Brazil. Among these, only 61 have known host plants, with Anastrepha fraterculus (Wiedemann) (110 hosts) and Anastrepha obliqua (Macquart) (48 hosts) as the most polyphagous species (Zucchi 2008). Ceratitis capitata and B. carambolae are the sole representatives of their genera in Brazil (Zucchi 2001). With regards to richness of Neosilba McAlpine, 25 species have been reported in the country.

In the Brazilian Amazon, multiple studies on frugivorous dipterans have been conducted in the past 10 yr, advancing knowledge on the biology and ecology of Tephritidae and Lonchaeidae (Silva et al. 2011). Seventy six species of Anastrepha and 14 species of Neosilba have been reported in the region to date (Adaime et al. 2016a; Pereira & Adaime 2016). Twenty-one host plants have been reported for B. carambolae, which has a distribution restricted to the states of Amapa and Roraima (Adaime et al. 2016b).

Although knowledge on frugivorous flies in the Amazon has increased significantly, some strategic areas in the region have not yet been duly studied. Among them is the extreme north of Amapa, Brazil, which includes the municipalities of Oiapoque and Calcoene, at the border with French Guiana. This region is extremely important to Brazil, as the flow of people and supplies crossing the border could facilitate the introduction of undesirable insect species. The introduction of the exotic species B. carambolae into Brazil exemplifies the vulnerability of this border area. Detected in 1989 in French Guiana, the species has been under official control in Oiapoque since 1996, when it was reported for the first time (Godoy et al. 2011).

Sugayama et al. (2015) stated that the risk of new pests being introduced through the Brazilian border is imminent. In Brazil, a constant concern exists regarding the potential introduction of Anastrepha suspensa (Loew), a quarantine pest that is absent in the country, but which is reported to occur in French Guiana. The introduction of this pest into Brazil would entail a closure of foreign markets, particularly for growers of mango (Mangifera indica L.; Anacardiaceae). Studies aiming to unveil the richness of fruit fly species and their host plants and natural enemies in this region are essential, as they will permit early detection of invading exotic species and offer supporting data for pest management.

In Oiapoque, although 20 species of Anastrepha, B. carambolae, and 5 species of parasitoids have been reported, knowledge of the associated hosts is minimal. In Calcoene, there have been reports only of B. carambolae and 4 species of Anastrepha, without any record of a parasitoid. In both municipalities, no species of Lonchaeidae have been reported to date.

Thus, we conducted a survey of frugivorous fly species (Tephritidae and Lonchaeidae), their host plants, and associated parasitoids, in the extreme north of Amapa State, Brazil.

Materials and Methods

CHARACTERIZATION OF STUDY AREA

The study area is located in the extreme north of the state of Amapa, at the Brazil-French Guiana border, and includes the municipalities of Calcoene and Oiapoque (Fig. 1). Together, these 2 municipalities occupy 25.88% of the total area of Amapa, which is 143,453.7 [km.sup.2]. Natural domains in the region include dense terra firme forest, floodable areas and savannas (Weiss 2011). The predominant climate in the region, as classified by Koppen, is Af (tropical rainforest), i.e., hot and wet, with a mean temperature of 25 [degrees]C, mean annual precipitation of 2,284 mm, and 60 mm or more of precipitation on the driest month. The rainy period is observed from Dec to Jul and the dry period is from Aug to Nov (SUDAM 1984; Diniz 1986).

SAMPLING PROCEDURES

Fruit were collected in the period from May 2011 to Jul 2013. Sampling was conducted at random, with the collection of intact fruits recently fallen to the ground. Geographic coordinates of each sampling site were recorded via a global positioning system device (GPSMAP[R]78s; Garmin, Schaffhausen, Switzerland). Each sample, comprised of multiple fruits, was stored in a plastic container, wrapped in a fine mesh bag, labeled and subsequently transported to the Plant Protection Laboratory at Embrapa Amapa, in the city of Macapa, Brazil.

ACQUISITION OF PUPARIA AND ADULT INSECTS

In the laboratory, the fruit were counted, weighed and arranged on plastic trays over a thin layer of moistened sand. The trays were covered with fine mesh, which was fastened in place with rubber bands. The fruit and sand were examined every 3 d, and any puparia found were removed and transferred into transparent plastic vials containing a thin layer of moistened vermiculite. The vials were covered with fine mesh and a vented lid before being placed in climate-controlled chambers (27 [+ or -] 0.5 [degrees]C; 70 [+ or -] 10% relative humidity (RH); 12:12 h L:D photoperiod). Fruit flies and parasitoids that emerged were stored in glass vials containing 70% ethanol, for subsequent identification.

IDENTIFICATION OF BIOLOGICAL MATERIAL

Specimens of Anastrepha were identified using the illustrated identification key published by Zucchi et al. (2011a). Identification of parasitoids (Braconidae) was based on the Canal & Zucchi (2000) and Marinho et al. (2011). Specimens of Neosilba were identified according to McAlpine & Steyskal (1982) and Strikis (2011).

To identify species of forest plants, we collected branches containing their reproductive structures (i.e., flowers and fruits), which were later processed into herbarium specimens using the mounting and preservation techniques described by Fidalgo and Bononi (1984). Plant species were identified through identification keys and comparison with specimens available at the Amapaense Herbarium (HAMAB), the herbarium at the Amapa Institute for Scientific and Technological Research (IEPA) in Macapa, Amapa, Brazil.

DATA ANALYSES

The data obtained were analyzed based on the following calculations: 1) infestation index = puparia obtained / mass of fruits collected, 2) emergence = (number of emerged flies + number of emerged parasitoids) / total number of puparia x 100, and 3) % parasitism = (number of emerged parasitoids / number of puparia) x 100.

Results

In total, 218 fruit samples were collected, a total of 3,915 fruits weighing 115.6 kg, belonging to 33 plant species (i.e., 12 native and 21 introduced) from 22 families (Tables 1 and 2). Infestation by fruit flies was observed in 69 samples (31.7%), belonging to 17 plant species from 13 families (Tables 1 and 2).

In total, 3,480 puparia were obtained, from which emerged specimens of Anastrepha (6 species), Neosilba (4 species), B. carambolae, and wasp parasitoids (3 species; Braconidae).

OIAPOQUE

In total, 126 samples were collected, consisting of 2,754 fruits (84.36 kg) of 29 plant species in 18 families. Infestation by fruit flies was observed in 45 samples (13 plant species in 10 families), from which 2,667 puparia were obtained (Table 1).

The species of Tephritidae obtained were: Anastrepha coronilli Carrejo & Gonzalez, Anastrepha distincta Greene, A. fraterculus, Anastrepha leptozona Hendel, A. obliqua, Anastrepha striata Schiner, and B. carambolae (Table 1).

Anastrepha obliqua was obtained from Spondias mombin Jacq. (Anacardiaceae) and Averrhoa carambola L. (Oxalidaceae). Anastrepha striata occurred in Psidium guajava L. (Myrtaceae) and Syzygium malaccense (L.) Merr. & L.M. Perry (Myrtaceae). Anastrepha coronilli was obtained from Bellucia grossularioides (L.) Triana (Melastomataceae), A. distincta from Inga edulis Mart. (Fabaceae), A. leptozona from Pouteria caimito (Ruiz & Pav.) Radlk. (Sapotaceae), and A. fraterculus from P guajava. Bactrocera carambolae was found in fruits of 4 plant species: A. carambola, Malpighia emarginata [Moc. & Sesse] ex DC. (Malpighiaceae), P. guajava, and S. malaccense (Table 1).

Anastrepha represented 61.3% of all tephritids obtained, followed by Bactrocera (38.7%). The greatest abundance of tephritids was observed in P. guajava, with A. striata as the predominant species (Table 1).

Neosilba represented 15.7% of all frugivorous flies obtained in Oiapoque. The species obtained were: Neosilba bella Strikis & Prado, N. glaberrima, Neosilba pseudozadolicha Strikis, and N. zadolicha (Table 1).

Neosilba glaberrima was obtained from 5 host species. Neosilba bella, N. pseudozadolicha, and N. zadolicha occurred in 3 hosts (Table 1). Only females were obtained from Byrsonima crassifolia (L.) Kunth (Malpighiaceae), I. edulis, and Moutabea cho datiana Huber (Polygalaceae), making species identification unfeasible.

Specimens of the parasitoid Doryctobracon areolatus (Szepligeti) (Hymenoptera: Braconidae) were obtained from fruits of B. grossularioides, P. guajava, and S. malaccense infested by frugivorous flies. The highest percentage of parasitism was observed in B. grossularioides (11.4%) (Table 1).

CALCOENE

In total, 92 samples were collected, consisting of 1,161 fruits (31.24 kg) of 19 plant species in 12 families. Infestation by fruit flies was observed in 24 samples (9 plant species in 7 families), from which 813 puparia were obtained (Table 2).

The species of Tephritidae obtained were: A. coronilli, A. fraterculus, A. obliqua, A. striata, and B. carambolae (Table 2).

Anastrepha coronilli was obtained from B. grossularioides, A. fraterculus from P. guajava, A. obliqua from S. mombin, and A. striata from P. guajava. Bactrocera carambolae was found in fruits of 3 plant species: A. carambola, P. guajava, and S. malaccense (Table 2).

Species of Anastrepha represented 83.7% of all tephritids obtained, followed by B. carambolae (16.3%). The highest abundance of tephritids was observed in P. guajava, with A. striata as the predominant species (Table 2).

Species of Neosilba represented 5.0% of all frugivorous flies obtained. The species obtained were N. glaberrima and N. pseudozadolicha (Table 2).

Neosilba glaberrima was found in Anacardium occidentale L. (Anacardiaceae) and Capsicum chinense Jacq. (Solanaceae). Neosilba pseudozadolicha was obtained from A. occidentale, C. chinense, Cucumis anguria L. (Cucurbitaceae), and S. malaccense (Table 2). Only females were obtained from A. carambola, Persea americana Mill. (Lauraceae) and P. guajava, making species identification unfeasible.

Specimens of the parasitoids D. areolatus, Opius bellus Gahan, and Utetes anastrephae (Viereck) (Hymenoptera: Braconidae) were obtained from fruits of B. grossularioides, P. guajava, and S. mombin infested by frugivorous flies. The highest percentage of parasitism was observed in B. grossularioides (16.3%) (Table 2).

Discussion

Anastrepha striata was the predominant species in both municipalities, due to its association with P. guajava, an abundantly sampled plant species (Tables 1 and 2). This strong association between A. striata and P. guajava already has been reported in the Brazilian Amazon (Silva et al. 2011; Marsaro Junior et al. 2013). Anastrepha striata also infested S. malaccense in Oiapoque, an unprecedented observation in the Brazilian Amazon.

Bactrocera carambolae was abundant, especially in Oiapoque. The species infested 4 hosts (A. carambola, M. emarginata, P. guajava, and S. malaccense) (Tables 1 and 2), all of which have already been reported in Amapa (Morais et al. 2016). Anastrepha obliqua was associated exclusively sampled with fruits of S. mombin, infesting all samples collected (Tables 1 and 2). Anastrepha obliqua is viewed as the main pest of this plant (Deus et al. 2016). This species also was found in A. carambola, an association already reported in Amapa (Zucchi et al. 2011b). Anastrepha fraterculus was obtained from guava fruits in both municipalities (Tables 1 and 2), always with a low abundance of specimens, confirming the results of other studies conducted in Amapa (Deus & Adaime 2013). Anastrepha coronilli was obtained only from fruits of B. grossularioides, in both municipalities (Tables 1 and 2). This association has been observed frequently in the Brazilian Amazon (Zucchi et al. 2011b). Anastrepha leptozona and A. distincta were observed only in Oiapoque (Table 1), associated with their most typical hosts in the region, namely P. caimito and I. edulis, respectively (Zucchi et al. 2011b). Among the Lonchaeidae obtained, N. glaberrima and N. zadolicha are the most polyphagous species in the Amazon region (Strikis et al. 2011; Lemos et al. 2015).

The highest infestation rates were observed in Myrtaceae host plants (Tables 1 and 2). Psidium guajava was infested especially by A. striata, and S. malaccense by B. carambolae. In Oiapoque, there was significant infestation of Annona muricata L. (Annonaceae), exclusively by species of Neosilba (Table 1).

Vayssieres et al. (2013) conducted a survey using McPhail traps (1994-2003) and fruit sampling (2001-2003) in French Guiana, from the border with Brazil to the border with Suriname. The authors did not report the presence of A. suspensa, but obtained 21 species of Anastrepha, in addition to B. carambolae. It should be noted that all species of Tephritidae (Anastrepha and Bactrocera) obtained in the present work already have been reported in French Guiana. Also relevant is the fact that we did not detect A. suspensa in the studied area (extreme north of Amapa, Brazil) and all 4 hosts we reported for B. carambolae in Amapa are among those reported by Vayssieres et al. (2013) in French Guiana.

Tables 3 and 4 show updated lists of frugivorous fly species already reported in Oiapoque and Calcoene, respectively. This work adds 5 new reports of frugivorous flies in the municipality of Oiapoque (A. leptozona, N. bella, N. glaberrima, N. pseudozadolicha, and N. zadolicha) and 3 in Calcoene (A. obliqua, N. glaberrima, and N. pseudozadolicha). In addition, 6 new associations between frugivorous fly species and their hosts were established for the Brazilian Amazon (Tables 3 and 4). This work also presents the first reports of parasitoids (D. areolatus, O. bellus, and U. anastrephae) in the municipality of Calcoene (Table 4).

This research contributes to the advance of knowledge on frugivorous flies, their host plants, and associated parasitoids in the extreme north of Amapa State, Brazil.

Acknowledgments

To our colleague Carlos Alberto Moraes, for support during sampling expeditions. To the Brazilian Council for Scientific and Technological Development (CNPq), for the Research Productivity Fellowships granted to R Adaime and MF de Souza-Filho. To the Ministry of Agriculture and Food Supply for authorizing publication of data pertaining to the carambola fruit fly, as provided in Normative Rule No. 52/2007.

References Cited

Adaime R, Sousa MSM, Pereira JF. 2016a. Anastrepha species and their hosts in the Brazilian Amazon. Amazon Network for Research on Fruit flies, last updated 3 Oct 2016, http://anastrepha.cpafap.embrapa.br (last accessed 18 Feb 2017).

Adaime R, Jesus-Barros CR, Bariani A, Lima AL, Cruz KR, Carvalho JP. 2016b. Novos registros de hospedeiros da mosca-da-carambola (Bactrocera carambolae) no estado do Amapa, Brasil. Comunicado Tecnico 146. Embrapa Amapa, Macapa, Brazil.

Aluja M. 1994. Bionomics and management of Anastrepha. Annual Review of Entomology 39: 155-178.

Canal NA, Zucchi RA. 2000. Parasitoides--Braconidae, pp. 119-126 In Malavasi A, Zucchi RA [eds.], Moscas-das-frutas de importancia economica no Brasil: conhecimento basico e aplicado. Holos, Ribeirao Preto, Sao Paulo, Brazil.

Creao MIP. 2003. Moscas-das-frutas (Diptera: Tephritidae): especies, distribuicao, medidas da fauna e seus parasitoides (Hymenoptera: Braconidae) no Estado do Amapa. MS Dissertation, Instituto Nacional de Pesquisas da Amazonia, Universidade do Amazonas, Manaus, Brazil.

Deus EG, Adaime R. 2013. Dez anos de pesquisas sobre moscas-das-frutas (Diptera: Tephritidae) no estado do Amapa: avancos obtidos e desafios futuros. Biota Amazonia 3: 157-168.

Deus EG, Pinheiro LS, Lima CR, Sousa MSM, Guimaraes JA, Strikis PC, Adaime R. 2013. Wild hosts of frugivorous dipterans (Tephritidae and Lonchaeidae) and associated parasitoids in the Brazilian Amazon. Florida Entomologist 96: 1621-1625.

Deus EG, Sousa MSM, Adaime R. 2016. Tapereba, pp. 260-265 In Silva NM, Adaime R, Zucchi RA [eds.], Pragas Agrfcolas e Florestais na Amazonia. Embrapa, Brasilia, Distrito Federal, Brazil.

De AS Diniz TD. 1986. Caracterizacao climatica da Amazonia Oriental. In Burger DM [ed.], Pesquisas sobre a utilizacao e conservacao do solo na Amazonia Oriental. Centro de Pesquisa Agropecuaria do Tropico Umido, documento 40, EMBRAPA, Belem, Brazil.

Fidalgo O, Bononi VLR. 1984. Tecnicas de coleta, preservacao e herborizacao de material botanico. Institute de Botanica, Sao Paulo, Brazil.

Godoy MJS, Pacheco WSP, Portal RR, Pires Filho JM, Moraes LMM. 2011. Programa Nacional de Erradicacao da Mosca-da-Carambola, pp. 134-158 In Silva RA, Lemos WP, Zucchi RA [eds.], Moscas-das-frutas na Amazonia Brasileira: Diversidade, Hospedeiros e Inimigos Naturais. Embrapa Amapa, Macapa, Amapa, Brazil.

Lemos LN, Adaime R, Jesus-Barros CR, Deus EG. 2014. New Hosts of Bactrocera carambolae (Diptera: Tephritidae) in Brazil. Florida Entomologist 97: 841-847.

Lemos LN, Lima CR, Adaime R, Costa-Neto R, Jesus CR; Strikis PC. 2015. New findings on Lonchaeidae (Diptera: Tephritoidea) in the Brazilian Amazon. Florida Entomologist 98:1227-1237.

Lourencao AL, Lorenzi JO, Ambrosano GMB. 1996. Comportamento de clones de mandioca em relacao a infestacao por Neosilba perezi (Romero & Rupell) (Diptera: Lonchaeidae). Scientia Agricola 53: 304-308.

Marinho CF, Silva RA, Zucchi RA. 2011. Chave de identificacao de Braconidae (Alysiinae e Opiinae) parasitoides de larvas frugfvoras na regiao Amazonica, pp. 91-101 In Silva RA, Lemos WP, Zucchi RA [eds.], Moscas-das-frutas na Amazonia Brasileira: Diversidade, Hospedeiros e Inimigos Naturais. Embrapa Amapa, Macapa, Amapa, Brazil.

Marsaro Junior AL, Deus EG, Ronchi-Teles B, Adaime R, Silva Junior RJ. 2013. Species of Anastrepha (Diptera: Tephritidae) captured in a guava orchard (Psidium guajava L., Myrtaceae) in Boa Vista, Roraima, Brazil. Brazilian Journal of Biology 73: 879-886.

McAlpine JF, Steyskal GC. 1982. A revision of Neosilba McAlpine with a key to the world genera of Lonchaeidae (Diptera). The Canadian Entomologist 114: 105-137.

Morais EGF, Jesus-Barros CR, Adaime R, Lima AL, Navia D. 2016. Pragas de expressao quarentenaria na Amazonia, pp. 521-559 In Silva NM, Adaime R, Zucchi RA [eds.], Pragas Agrfcolas e Florestais na Amazonia. Embrapa, Brasilia, Distrito Federal, Brazil.

Norrbom AL, Uchoa MA. 2011. New species and records of Anastrepha (Diptera: Tephritidae) from Brazil. Zootaxa 2835: 61-67.

Pereira JF, Adaime R. 2016. Lonchaeidae from Brazilian Amazon. Amazon Network for Research on Fruit flies, last updated 7 Jan 2016, http://lonchaeidae.cpafap.embrapa.br (last accessed on 18 Feb 2017)

Ronchi-Teles B. 2000. Ocorrencia e flutuacao populacional de especies de moscas-das-frutas e parasitoides com enfase para o genero Anastrepha (Diptera: Tephritidae) na Amazonia Brasileira. PhD Thesis, Institute Nacional de Pesquisas da Amazonia, Universidade do Amazonas, Manaus, Brazil.

Ronchi-Teles B, Silva NM, Norrbom AL. 1996. New records of Anastrepha spp. (Diptera: Tephritidae) and their host in Rondonia and Amapa States--Brazilian Amazonia, pp. 32-33 In Proceedings of the 2nd meeting of the Working Group on Fruit Flies of the Western Hemisphere, Vina Del Mar, Chile.

Silva RA, Lemos WP, Zucchi RA. [eds.]. 2011. Moscas-das-frutas na Amazonia Brasileira: Diversidade, Hospedeiros e Inimigos Naturais. Embrapa Amapa, Macapa, Amapa, Brazil.

Strikis PC. 2011. Description of 11 new species of genus Neosilba (Diptera: Lonchaeidae) from Brazil, its hosts and geographical distribution. Trends in Entomology 7: 67-79.

Strikis PC, Deus EG, Silva RA, Pereira JDB, Jesus CR, Marsaro Junior AL. 2011. Conhecimento sobre Lonchaeidae na Amazonia Brasileira, pp. 205-215 In Silva RA, Lemos WP, Zucchi RA [eds.], Moscas-das-frutas na Amazonia Brasileira: Diversidade, Hospedeiros e Inimigos Naturais. Embrapa Amapa, Macapa, Amapa, Brazil.

SUDAM (Superintendency for the Development of Amazonia). 1984. Atlas Climatologico da Amazonia Brasileira. Projecto de Hidrologia e Climatologia da Amazonia, publication number 39, Belem, Brazil.

Sugayama RL, lede ET, Stancioli AR, Alves GA, Oliveira IM, Dias JA. 2015. Ameacas fitossanitarias, pp. 449-471 In Sugayama RL, Silva ML, Silva SXB, Rangel LEP [eds.], Defesa Vegetal: Fundamentos, Ferramentas, Polfticas e Perspectivas. Sociedade Brasileira de Defesa Agropecuaria, Belo Horizonte, Minas Gerais, Brazil.

Trindade RBR, Uchoa MA. 2011. Species of fruit flies (Diptera: Tephritidae) in a transect of the Amazonian Rainforest in Oiapoque, Amapa, Brazil. Revista Zoologia 28: 653-657.

Uchoa MA. 2012. Fruit flies (Diptera: Tephritoidea): biology, host plants, natural enemies, and the implications to their natural control, pp. 271-300 In Larramendy ML, Soloneski S [eds.], Integrated Pest Management and Pest Control: Current and Future Tactics. InTech, Rijeka, Croatia.

Vayssieres JF, Cayol JP, Caplong P, Seguret J, Midgarden D, Sauers-Muller A van, Zucchi R, Uramoto K, Malavasi A. 2013. Diversity of fruit fly (Diptera: Tephritidae) species in French Guiana: their main host plants and associated parasitoids during the period 1994-2003 and prospects for management. Fruits 68: 219-243.

Weiss BM. 2011. Plano Territorial de Desenvolvimento Rural Sustentavel (PT-DRS) Extremo Norte do Amapa. Programa Integrado de Acoes Socioambientais da Amazonia Oriental, Macapa, Brazil, http://sit.mda.gov.br/download/ptdrs/ptdrs_qua_territorio154.pdf (last accessed 18 Feb 2017).

White IM, Elson-Harris M. 1992. Fruit Flies of Economic Significance: Their Identification and Bionomics. CAB International, Redwork Press Ltd, Melksham, UK.

Zucchi RA. 2001. Mosca-do-mediterraneo, Ceratitis capitata (Diptera: Tephritidae) pp. 15-22 In Vilela EF, Zucchi RA, Cantor F [eds.], Historico e Impacto das Pragas Introduzidas no Brasil. Holos, Ribeirao Preto, Sao Paulo, Brazil.

Zucchi RA. 2008. Anastrepha species their host plants and parasitoids. Fruit flies (Diptera: Tephritidae) in Brazil, updated 1 Dec 2016, www.lea.esalq.usp.br/anastrepha/ (last accessed 18 Feb 2017).

Zucchi RA, Uramoto K, Souza-Filho MF. 2011a. Chave ilustrada para as especies de Anastrepha da regiao Amazonica, pp. 71-90 In Silva RA, Lemos WP, Zucchi RA [eds.], Moscas-das-frutas na Amazonia Brasileira: Diversidade, Hospedeiros e Inimigos Naturais. Embrapa Amapa, Macapa, Amapa, Brazil.

Zucchi RA, Silva RA, Deus EG. 2011b. Especies de Anastrepha e seus hospedeiros na Amazonia Brasileira, pp. 51-70 In Silva RA, Lemos WP, Zucchi RA [eds.], Moscas-das-frutas na Amazonia Brasileira: Diversidade, Hospedeiros e Inimigos Naturais. Embrapa Amapa, Macapa, Amapa, Brazil.

Ricardo Adaim.e (1,2,3,*), Maria do Socorro Miranda de Sousa (2), Cristiane Ramos de Jesus-Barros (1), Ezequiel da Gloria de Deus (3), Jose Francisco Pereira (1), Pedro Carlos Strikis (4), and Miguel Francisco de Souza-Filho (5)

(1) Embrapa Amapa, Macapa, Amapa, 68903-419, Brazil; E-mail: ricardo.adaime@embrapa.br (R. A.), cristiane.jesus@embrapa.br (C. R. J.-B.), jose-francisco.pereira@embrapa.br (J. F. P.)

(2) Universidade Federal do Amapa, Programa de Pos-graduacao em Desenvolvimento Regional, Macapa, Amapa, 68902-280, Brazil; E-mail: socorro-ap@hotmail.com (M. S. M. S.)

(3) Universidade Federal do Amapa, Programa de Pos-graduacao em Biodiversidade Tropical, Macapa, Amapa, 68902-280, Brazil; E-mail: egd_bio@hotmail.com (E. G. D.)

(4) Independent Researcher, Av. Paschoal Ardito, No. 886, Americana, Sao Paulo, 13473-010, Brazil; E-mail: pcstrikis@gmail.com (P. C. S.)

(5) Instituto Biologico, Caixa Postal 70, Campinas, Sao Paulo, 13001-970, Brazil; E-mail: miguelf@biologico.sp.gov.br (M. F. S.-F.)

(*) Corresponding author; E-mail: ricardo.adaime@embrapa.br (R. A.)

Caption: Fig. 1. Fruit sampling sites in extreme north of Amapa State, Brazil (May 2011-Jul 2013).

Please Note: Illustration(s) are not available due to copyright restrictions.
Table 1. Rates of infestation of various plant species by frugivorous
flies (Tephritidae and Lonchaeidae) in Oiapoque, Amapa, Brazil. May
2011 to Jul 2013.

FAMILY                     Origin in         Fruits    Mass    PP
Species                    N/I         I/c   (n)       (kg)    (n)

ANACARDIACEAE
Anacardium occidentale L.  I           0/10    69       3.60
Mangifera indica L.        I           2/3     11       2.81    5
Spondias dulcis Soland.    I           0/3     36       2.10
Ex Forst. fil.
Spondias mombin Jacq.      N           2/2     76       0.90    37
ANNONACEAE
Annona muricata L.         I           1/2      2       0.91    117
APOCYNACEAE
Ambelania acida Aubl.      N           0/2     20       0.71
CARICACEAE                             0/7
Carica papaya L.           I           0/7     18       9.99
CUCURBITACEAE
Cucumis anguria L.         N           0/8     93       2.26
Cucumis sativus L.         I           0/3     15       2.11
Cucurbita sp.              N           0/2      2       1.83
EUPHORBIACEAE
Manihot esculenta Crantz   N           0/2     12       0.05
FABACEAE
Inga edulis Mart.          N           1/2      6       2.14    62
MALPIGHIACEAE
Byrsonima crassifolia      N           1/5    552       0.84    1
(L.) Kunth
Malpighia emarginata       I           6/12   969       4.13    185
[Moc. & Sesse] ex DC.
MELASTOMATACEAE
Bellucia grossularioides   N           3/3    142       1.70    88
(L.) Triana
MORACEAE
Artocarpus heterophyllus   I           0/4      4      12.54
Lam.
MYRTACEAE
Psidium guajava L.         I           17/18  359      12.83   1,591
Syzygium malaccense (L.)   I           3/3     58       1.34    183
Merr. & L.M. Perry
OXALIDACEAE
Averrhoa bilimbi L.        I           0/1     11       0.16
Averrhoa carambola L.      I           5/5     56       3.13    315
PASSIFLORACEAE
Passiflora edulis          N           0/4     20       1.32
Sims (fruit)
Passiflora edulis          N           0/2     37       0.09
Sims (flower bud)
POLYGALACEAE
Moutabea chodatiana Huber  N           1/1     21       0.12    9
RUBIACEAE
Coffea arabica L.          I           0/1     30       0.02
RUTACEAE
Citrus aurantium L.        I           0/2      9       5.33
Citrus reticulata Blanco   I           0/3     28       1.27
Citrus sinensis (L.)       I           1/10    69       7.86    10
Osbeck
SAPINDACEAE
Nephelium lappaceum L.     I           0/1     10       0.17
SAPOTACEAE
Pouteria caimito           N           2/3      9       1.94    64
(Ruiz & Pav.) Radlk.
Solanum gilo Raddi         I           0/2     10       0.16
Total                      --          45/126   2.754   84.36   2,667

FAMILY                         I         E      Tephritidae
Species                     (PP/kg)     (%)         (n)

ANACARDIACEAE
Anacardium occidentale L.
Mangifera indica L.          1.8       0.0
Spondias dulcis Soland.
Ex Forst. fil.
Spondias mombin Jacq.       41.1      75.7   Ao (12), 16 [male]
ANNONACEAE
Annona muricata L.         128.6      41.0
APOCYNACEAE
Ambelania acida Aubl.
CARICACEAE
Carica papaya L.
CUCURBITACEAE
Cucumis anguria L.
Cucumis sativus L.
Cucurbita sp.
EUPHORBIACEAE
Manihot esculenta Crantz
FABACEAE
Inga edulis Mart.           29.0      83.9   Ad (40), 11 [male]
MALPIGHIACEAE
Byrsonima crassifolia        1.2     100
(L.) Kunth
Malpighia emarginata        44.8      33.5        Bc (51)
[Moc. & Sesse] ex DC.
MELASTOMATACEAE
Bellucia grossularioides    51.8      52.3   Ac (19), 17 [male]
(L.) Triana
MORACEAE
Artocarpus heterophyllus
Lam.
MYRTACEAE
Psidium guajava L.         124.0     45.8      As (192), Af (9),
                                             238 [male] + Be (75)
Syzygium malaccense (L.)   136.6     45.9   As (3), 3 [male] + Bc (77)
Merr. & L.M. Perry
OXALIDACEAE
Averrhoa bilimbi L.
Averrhoa carambola L.      100.6     59.0   Ao (5), 5 [male] + Bc (162)
PASSIFLORACEAE
Passiflora edulis
Sims (fruit)
Passiflora edulis
Sims (flower bud)
POLYGALACEAE
Moutabea chodatiana Huber   75.0     77.8
RUBIACEAE
Coffea arabica L.
RUTACEAE
Citrus aurantium L.
Citrus reticulata Blanco
Citrus sinensis (L.)         1.3   100
Osbeck
SAPINDACEAE
Nephelium lappaceum L.
SAPOTACEAE
Pouteria caimito            33.0     20.3       Al (4), 4 [male]
(Ruiz & Pav.) Radlk.
Solanum gilo Raddi
Total                        --       --       As (195 [female]), Ad
                                               (40 [female]), Ac (19
                                            [female]), Ao (17 [female]),
                                              Af (9 [female]), Al (4
                                            [female]), 294 [male]+ Bc
                                                      (365)


FAMILY                         Lonchaeidae             Hymenoptera    P
Species                            (n)                     (n)       (%)

ANACARDIACEAE
Anacardium occidentale L.
Mangifera indica L.
Spondias dulcis Soland.
Ex Forst. fil.
Spondias mombin Jacq.
ANNONACEAE
Annona muricata L.            Nz (26), Ng(4),
                            Np (1), 17 [female]
APOCYNACEAE
Ambelania acida Aubl.
CARICACEAE
Carica papaya L.
CUCURBITACEAE
Cucumis anguria L.
Cucumis sativus L.
Cucurbita sp.
EUPHORBIACEAE
Manihot esculenta Crantz
FABACEAE
Inga edulis Mart.              1 [female]
MALPIGHIACEAE
Byrsonima crassifolia          1 [female]
(L.) Kunth
Malpighia emarginata          Nb (5), Ng(2),
                             Np (1), 3[female]
[Moc. & Sesse] ex DC.
MELASTOMATACEAE
Bellucia grossularioides                              Da(10)        11.4
(L.) Triana
MORACEAE
Artocarpus heterophyllus
Lam.
MYRTACEAE
Psidium guajava L.           Nz (25), Nb (5),        Da(134)        8.4
                            Ng(5), 44 [female]
Syzygium malaccense (L.)                               Da(1)        0.5
Merr. & L.M. Perry
OXALIDACEAE
Averrhoa bilimbi L.
Averrhoa carambola L.        Ng (5), Nb (1),
                             Nz (1), 7 [female]
PASSIFLORACEAE
Passiflora edulis
Sims (fruit)
Passiflora edulis
Sims (flower bud)
POLYGALACEAE
Moutabea chodatiana Huber     7 [female]
RUBIACEAE
Coffea arabica L.
RUTACEAE
Citrus aurantium L.
Citrus reticulata Blanco
Citrus sinensis (L.)          Np (4), 6 [female]
Osbeck
SAPINDACEAE
Nephelium lappaceum L.
SAPOTACEAE
Pouteria caimito             Ng(2), 3[female]
(Ruiz & Pav.) Radlk.
Solanum gilo Raddi
Total                      Nz (52), Ng (18), Nb (11), Np  Da(145)  --
                                (6), 89 [female]

N: native; I: introduced; I: samples infested; C: samples collected;
PP: puparia; I: infestation; E: emergence; P: percentage of parasitism;
Ac: Anastrepha coronilli Carrejo & Gonzalez; Ad: Anastrepha distincta
Greene; Af: Anastrepha fraterculus (Wiedemann); Al: Anastrepha
leptozona Hendel; Ao: Anastrepha obliqua (Macquart); As: Anastrepha
striata (Schiner); Bc: Bactrocera carambolae Drew & Hancock
([female],[male]); Nb: Neosilba bella Strikis & Prado; Ng: Neosilba
glaberrima (Wiedemann); Np: Neosilba pseudozadolicha Strikis; Nz:
Neosilba zadolicha McAlpine & Steyskal; Da: Doryctobracon areolatus
(Szepligeti) ([female] ,[male]).

Table 2. Rates of infestation of various plant species by frugivorous
flies (Tephritidae and Lonchaeidae) in Calcoene, Amapa, Brazil. May
2011 to Jul 2013.

FAMILY                     Origin          Fruits    Mass    PP     I
Species                     N/I     I/c     (n)      (kg)   (n)  (PP/kg)
ANACARDIACEAE
Anacardium occidentale L.  I       1/11     45       3.28     4     1.2
Mangifera indica L.        I       0/2       5       1.32
Spondias mombin Jacq.      N       3/3      51       0.67    41    61.2
CHRYSOBALANACEAE
Chrysobalanus icaco L.     N       0/2      77       0.21
COMBRETACEAE
Terminalia catappa L.              0/1      20       0.31
CUCURBITACEAE
Cucumis anguria L.         N       1/11    131       2.49     2     0.8
Cucumis sativus L.         I       0/9      32       4.32
LAURACEAE
Persea americana Mill.     I       1/1      5        0.39     1     2.6
MALPIGHIACEAE
Byrsonima crassifolia      N       0/1      30       0.05
(L.) Kunth
Malpighia emarginata       I       0/4      70       0.16
[Moc. & Sesse] ex DC.
MELASTOMATACEAE
Bellucia grossularioides   N       4/4     140       1.89    80    42.3
(L.) Triana
MYRTACEAE
Psidium guajava L.         I       9/10    132       4.77   525   110.0
Syzygium malaccense (L.)   I       2/2      20       0.60    81   135.0
Merr. & L.M. Perry
OXALIDACEAE
Averrhoa carambola L.      I       1/3      17       0.74    74   100.0
RUBIACEAE
Coffea arabica L.          I       0/2      81       0.05
RUTACEAE
Citrus aurantium L.        I       0/3      14       1.79
Citrus reticulata Blanco   I       0/3      22       2.59
Citrus sinensis (L.)       I       0/6      39       5.05
Osbeck
SOLANACEAE
Capsicum chinense Jacq.    I       2/14    230      0.54      5     9.3
Total                      --     24/92  1,161     31.24    813      --

FAMILY                           E                    Tephritidae
Species                         (%)                       (n)
ANACARDIACEAE
Anacardium occidentale L.       100
Mangifera indica L.
Spondias mombin Jacq.            53.7              Ao (8), 12 [male]
CHRYSOBALANACEAE
Chrysobalanus icaco L.
COMBRETACEAE
Terminalia catappa L.
CUCURBITACEAE
Cucumis anguria L.              100
Cucumis sativus L.
LAURACEAE
Persea americana Mill.          100
MALPIGHIACEAE
Byrsonima crassifolia
(L.) Kunth
Malpighia emarginata
[Moc. & Sesse] ex DC.
MELASTOMATACEAE
Bellucia grossularioides         65.0             Ac (15), 24 [male]
(L.) Triana
MYRTACEAE
Psidium guajava L.               66.9              As (160), Af (2),
                                                 173 [male] + Bc (8)
Syzygium malaccense (L.)         29.6                Bc (16)
Merr. & L.M. Perry
OXALIDACEAE
Averrhoa carambola L.            87.8                Bc (61)
RUBIACEAE
Coffea arabica L.
RUTACEAE
Citrus aurantium L.
Citrus reticulata Blanco
Citrus sinensis (L.) Osbeck
SOLANACEAE
Capsicum chinense Jacq.         100
Total                           --           As (160 [female]), Ac (15
                                             [female]), Ao (8 [female]),
                                             Af(2 [female]), 209
                                             ([male] + Bc (77)

FAMILY                        Lonchaeidae          Hymenoptera
Species                           (n)                  (n)         P (%)
ANACARDIACEAE
Anacardium occidentale L.     Ng(2), Np(l),
                              1 [female]
Mangifera indica L.
Spondias mombin Jacq.                              Ua (2)            4.9
CHRYSOBALANACEAE
Chrysobalanus icaco L.
COMBRETACEAE
Terminalia catappa L.
CUCURBITACEAE
Cucumis anguria L.            Np (1), 1 [female]
Cucumis sativus L.
LAURACEAE
Persea americana Mill.        1 [female]
MALPIGHIACEAE
Byrsonima crassifolia
(L.) Kunth
Malpighia emarginata
[Moc. & Sesse] ex DC.
MELASTOMATACEAE
Bellucia grossularioides                           Da (11), Ob (2)  16.3
(L.) Triana
MYRTACEAE
Psidium guajava L.            1 [female]           Da (7)            1.3
Syzygium malaccense (L.)      Np(3), 5 [female]
Merr. & L.M. Perry
OXALIDACEAE
Averrhoa carambola L.         4 [female]
RUBIACEAE
Coffea arabica L.
RUTACEAE
Citrus aurantium L.
Citrus reticulata Blanco
Citrus sinensis (L.) Osbeck
SOLANACEAE
Capsicum chinense Jacq.       Ng(l), Np(l),
                              3 [female]
Total                         Np (6), Ng(3), 169   Da (18), Ob (2), --
                                                   Ua(2)

N: native; I: introduced; I: samples infested; C: samples collected;
PP: puparia; I: infestation; E: emergence; P: percentage of parasitism;
Ac: Anastrepha coronilli Carrejo & Gonzalez; Af: Anastrepha fraterculus
(Wiedemann); Ao: Anastrepha obliqua (Macquart); As: Anastrepha striata
(Schiner); Be: Bactrocera carambolae Drew & Hancock ([female], [male]);
Ng: Neosilba glaberrima (Wiedemann); Np: Neosilba pseudozadolicha
Strikis; Da: Doryctobracon areolatus (Szepligeti) ([female], [male]);
Ob: Opius bellus Gahan ([female], [male]); Ua: Utetes anastrephae
(Viereck)([female], [male]).

Table 3. List of frugivorous flies (Tephritidae and Lonchaeidae) and
their host plants recorded in the municipality of Oiapoque, Amapa,
Brazil.

                       Sampling
Species                Method   Host                    Reference

Anastrepha             McPhail  --                      Trindade &
amita Zucchi                                            Uchoa (2011)
Anastrepha             McPhail  --                      Trindade &
binodosa Stone                                          Uchoa (2011)
Anastrepha coronilli   Fruit    Bellucia                Ronchi-Teles
Carrejo & Gonzalez              grossularioides         et al. (1996),
                                (L.) Triana             Trindade & Uchoa
                                                        (2011),
                                                        present paper
Anastrepha             McPhail  --                      Trindade &
dissimilis Stone                                        Uchoa (2011)
Anastrepha             McPhail  --                      Trindade &
distincta Greene                                        Uchoa (2011)
                       Fruit    Inga edulis Mart.       present paper
Anastrepha duckei      McPhail  --                      Trindade &
Lima                                                    Uchoa (2011)
Anastrepha             McPhail  --                      Trindade &
flavipennis Greene                                      Uchoa (2011)
Anastrepha             McPhail  --                      Trindade &
fraterculus                                             Uchoa (2011)
(Wiedemann)
                       Fruit    Psidium guajava L.      present paper
Anastrepha furcata     McPhail  --                      Trindade &
Lima                                                    Uchoa (2011)
Anastrepha             Fruit    Pouteria caimito (Ruiz  present paper
leptozona Hendel (*)            & Pav.) Radlk.
Anastrepha minensis    McPhail  --                      Trindade &
Lima                                                    Uchoa (2011)
Anastrepha mixta       McPhail  --                      Trindade &
Zucchi                                                  Uchoa (2011)
Anastrepha obliqua     McPhail  --                      Trindade &
(Macquart)                                              Uchoa (2011)
                       Fruit    Averrhoa carambola L.   present paper
                       Fruit    Spondias mombin Jacq.   present paper
Anastrepha             McPhail  --                      Trindade &
oiapoquensis                                            Uchoa (2011),
Norrbom & Uchoa                                         Norrbom &
                                                        Uchoa (2011)
Anastrepha             McPhail  --                      Trindade &
pseudoparallela                                         Uchoa (2011)
(Loew)
Anastrepha rafaeli     McPhail  --                      Trindade &
Norrbom &                                               Uchoa (2011)
Korytkowski
Anastrepha siculigera  McPhail  --                      Trindade &
Norrbom & Uchoa                                         Uchoa (2011)
Anastrepha             McPhail  --                      Trindade &
sororcula Zucchi                                        Uchoa (2011)
Anastrepha             Fruit    Psidium guajava L.      Ronchi-Teles
striata Schiner                                         (2000), Creao
                                                        (2003), present
                                                        paper
                       Fruit    Syzygium malaccense     present paper
                                (L.) Merr. &
                                L.M. Perry (**)
Anastrepha             McPhail  --                      Trindade &
submunda Lima                                           Uchoa (2011)
Anastrepha             Fruit    Spondias                Creao (2003)
turpiniae Stone                 mombin Jacq.
Bactrocera carambolae  --       --                      Ronchi-Teles
Drew & Hancock                                          (2000)
                       Fruit    Averrhoa carambola L.   Creao (2003),
                                                        present paper
                       Fruit    Malpighia emarginata    present paper
                                [Moc. & Sesse] ex DC.
                       Fruit    Psidium guajava L.      present paper
                       Fruit    Syzygium malaccense     present paper
                                (L.) Merr. &
                                L.M. Perry
Neosilba bella         Fruit    Malpighia emarginata    present paper
Strikis & Prado (*)             [Moc & Sesse] ex DC.
                       Fruit    Psidium guajava L.      present paper
                       Fruit    Averrhoa carambola L.   present paper
Neosilba glaberrima    Fruit    Annona muricata L.      present paper
(Wiedemann) (*)
                       Fruit    Averrhoa carambola L.   present paper
                       Fruit    Malpighia emarginata    present paper
                                [Moc & Sesse] ex DC.
                       Fruit    Pouteria caimito        present paper
                                (Ruiz & Pav.) Radlk.
                       Fruit    Psidium guajava L.      present paper
Neosilba               Fruit    Annona muricata L.      present paper
pseudozadolicha
Strikis (*)                     (**)
                       Fruit    Citrus sinensis (L.)    present paper
                                Osbeck.
                       Fruit    Malpighia emarginata    present paper
                                [Moc. & Sesse] ex DC.
Neosilba zadolicha     Fruit    Annona muricata L.      present paper
cAlpine & Steyskal
(*)
                       Fruit    Averrhoa carambola L.   present paper
                       Fruit    Psidium guajava L.      present paper

(*) First report of occurrence in this municipality.
(**) New association between this fly and host in the Brazilian Amazon.

Table 4. List of frugivorous flies (Tephritidae and Lonchaeidae) and
their host plants reported in the municipality of Calcoene, Amapa,
Brazil.

Species              Sampling   Host                     Reference
                     Method

Anastrepha           Fruit      Bellucia                 Deus et al.
                                grossularioides          (2013),
coronilli                       (L.) Triana              present paper
Carrejo & Gonzalez   Fruit      Bellucia imperialis      Deus et al.
                                Saldanha & Cogn          (2013)
Anastrepha           Fruit      Simaba guianensis Aubl.  Deus et al.
fraterculus                                              (2013)
(Wiedemann)
                     Fruit      Psidium guajava L.       present paper
Anastrepha obliqua   Fruit      Spondias mombin Jacq.    present paper
Macquart) (*)
Anastrepha parishi   Fruit      Simaba guianensis Aubl.  Deus et al.
Stone                                                    (2013)
Anastrepha striata   Fruit      Inga edulis Mart.        Creao (2003)
Schiner
                     Fruit      Psidium guajava L.       Creao (2003),
                                                         present paper
Bactrocera           Fruit      Psidium guajava L.       present paper
carambolae
Drew & Hancock
                     Fruit      Syzygium malaccense      present paper
                                (L.) Merr. & L.M. Perry
                     Fruit      Averrhoa carambola L.    present paper
Neosilba glaberrima  Fruit      Anacardium               present paper
(Wiedemann) (*)                 occidentale L. (**)
                     Fruit      Capsicum chinense        present paper
                                Jacq. (**)
Neosilba             Fruit      Anacardium               present paper
pseudozadolicha                 occidentale L. (**)
Strikis (*)
                     Fruit      Cucumis anguria L. (**)  present paper
                     Fruit      Syzygium malaccense      present paper
                                (L.) Merr. & L.M. Perry
                     Fruit      Capsicum chinense Jacq.  present paper

(*) First report of occurrence in this municipality.
(**) New association between this fly and host in the Brazilian Amazon.
COPYRIGHT 2017 Florida Entomological Society
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2017 Gale, Cengage Learning. All rights reserved.

 
Article Details
Printer friendly Cite/link Email Feedback
Author:Adaime, Ricardo; de Sousa, Maria do Socorro Miranda; de Jesus-Barros, Cristiane Ramos; de Deus, Ezeq
Publication:Florida Entomologist
Article Type:Report
Geographic Code:3BRAZ
Date:Jun 1, 2017
Words:5879
Previous Article:Two new species of Americanura (Collembola: Neanuridae) from Belize, Central America.
Next Article:Diptilomiopus floridanus (Acari: Eriophyoidea: Diptilomiopidae): its distribution and relative abundance with other eriophyoid species on dooryard,...
Topics:

Terms of use | Privacy policy | Copyright © 2018 Farlex, Inc. | Feedback | For webmasters