270 Florida Entomologist 96(1) March 2013

NATIVE HOSTS AND PARASITOIDS ASSOCIATED WITH ANASTREPHA FRACTURA AND OTHER ANASTREPHA SPECIES (DIPTERA: TEPHRITIDAE) IN THE BRAZILIAN AMAZON

Vivian Siqueira Dutra1, Beatriz Ronchi-Teles2, Marcos Vinicius Bastos Garcia3, Ricardo Adaime4, and Janisete Gomes Silva5* 1Graduate Program in Entomology, Instituto Nacional de Pesquisas da Amazônia, Caixa Postal 2223, 69080-971 Manaus, Amazonas, Brazil

2Coordenação de Biodiversidade, Instituto Nacional de Pesquisas da Amazônia, Caixa Postal 2223, 69080-971 Manaus, Amazonas, Brazil

3Embrapa Amazônia Ocidental, Rodovia AM 10 km 29, 69011-970 – Manaus, Amazonas, Brazil

4Embrapa Amapá, Rodovia Juscelino Kubitschek, km 5, 68903-419 – Macapá, Amapá, Brazil

5Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Rodovia Ilhéus-Itabuna km 16, 45650-000 - Ilhéus, Bahia, Brazil

*Corresponding author; E-mail: [email protected]

The Brazilian Amazon region comprises an ex- bellus Gahan parasitoids for the first time (Table ceptionally-high diversity of angiosperms, among 1). Previously, A. fractura had been reported solely which approximately 180 described species, both from Guyana (Stone 1942) and Amazonas, and the native and exotic that can be potential fruit fly hosts only known host and associated parasitoid were (Silva & Ronchi-Teles 2000). Currently, 60 Anastre- sclerophylla (Ducke) C.C. Berg (: pha species have been recorded in the Brazilian ) and Doryctobracon areolatus (Szépligeti) Amazon region, of which about 30 species are en- (Costa et al. 2009), respectively. We also report demic (Trindade & Uchôa 2011; Zucchi et al. 2011). Anastrepha distincta Greene infesting Inga cin- Here we report on new host/fruit fly/parasitoid namomea Spruce ex Benth (Fabales: Fabaceae: associations for some Anastrepha species for both Mimosoideae) in Brazil for the first time (Table Brazil and the Amazon region. A total of 4,137 1), but which was not attacked by any of the para- fruit (73.9 kg) from 40 different native and intro- sitoid species herein reported. The remaining 13 duced species in 19 families were collected Anastrepha species recovered during sampling from 2008 through 2011 in Manaus (S 03° 06' 07" (Table 1) had previously been reported infesting W 60° 01' 30"), Maués (S 03° 23' 01" W 57° 43' the hosts from which they were recovered here 07"), Presidente Figueiredo (S 02° 02' 04" W 60° (Zucchi et al. 2011). 01' 30"), and São Gabriel da Cachoeira (S 00° 07' We also report O. bellus and Utetes anastrephae 49" W 7° 05' 21") in the state of Amazonas; in Por- (Viereck) associated with Anastrepha coronilli to Velho (S 08° 45' 43" W 63° 54' 14") in the state Carrejo & González, and Aganaspis pelleranoi of Rondônia, and in Boa Vista (S 02° 49' 11" W (Brèthes) associated with A. coronilli and Anas- 60° 40' 24") in the state of Roraima. Fallen fruit, trepha striata Schiner for the first time in Brazil. both ripe and ripening, were collected randomly Our results indicate that native host in the from the ground under tree canopies within the Amazon forest in Brazil play an important role as forest. Cassava fruits were collected in an area reservoirs of native parasitoids and corroborate adjacent to the forest in Manaus (Amazonas) and previous studies in forested areas (López et al. Porto Velho (Rondônia). Adult flies and parasit- 1999; Aluja et al. 2003; Costa et al. 2009; Ronchi- oids were reared from collected fruits following Teles et al. 2011). methods described in Ronchi-Teles et al. (2011). We would like to thank Ana Claúdia Araújo, Voucher specimens were deposited at the Coleção Felipe Gomes, Mírian Santos, Neusa Hamada, Ta- de Invertebrados of the Instituto Nacional de Pes- tiana Senra, and Weber Novaes for their help with quisas da Amazônia. the collections. Thanks are also due to Carter R. A total of 3,470 fruit (63.3 kg) were infested yield- Miller, the anonymous reviewers and the editor for ing 7,662 puparia from which 3,073 Anastrepha comments on an earlier version of the manuscript. adults (1,469 males and 1,604 females), 669 braco- This study was supported by Conselho Nacional de nid parasitoids, and 17 figitid parasitoids emerged. Desenvolvimento Científico e Tecnológico (CNPq We report Anastrepha fractura Stone infesting fruit 575664/2008-8) and Rede Amazônica de Pesquisas of Salacia sp. (Celastrales: Celastraceae) in as- sobre Moscas-das-Frutas (EMBRAPA Chamada sociation with Asobara anastrephae (Muesebeck), 05/2006 Agrofuturo). V.S.D. was supported under Doryctobracon brasiliensis (Szépligeti), and Opius a CNPq fellowship during her Ph.D. Scientific Notes 271 Parasitoid species (n) 2 D. areolatus 5 D. areolatus 88 D. areolatus 43 O. bellus 6 U. anastrephae 0 92 O. bellus 72 A. anastrephae 9 D. areolatus 1 U. anastrephae 1 A. pelleranoi 1 A. nordlanderi 0 0 60 D. areolatus 3 A. anastrephae  1 D. brasiliensis  1 O. bellus  41 D. areolatus  128 D. areolatus 1 O. bellus 2 U. anastrephae 3 O. bellus  0 0 0 0 species (n) Anastrepha 27 A. obliqua 149 A. obliqua 9 A. antunesi 181 A. fractura 77 A. turpiniae 109 A. pickeli 1 A. manihoti 27 A. distincta 3 A. distincta 4 A. obliqua 104 A. obliqua 8 A. antunesi  122 A. obliqua 8 A. antunesi 108 A. distincta 3 A. pickeli

9 17 15 109 731 300 393 139 586 227 306 1,491 Number of pupae

9 8 11 15 14 28 27 85 162 213 232 1,038 of fruit Number 2.5 7.9 0.6 4.9 2.2 0.8 0.9 3.1 0.3 0.8 2.1 4.0 (kg) weight Sample . razil , B re g ion

Collection sites a m azon

Manaus Manaus Manaus Manaus Manaus Maués Presidente Figueiredo São Gabriel da Cachoeira Porto Velho Maués Manaus Manaus the

in

s itoi ds para

Hosts Introduced Native Native Introduced Native Native Native Native d a ss ociate

an d , ho s t , s pecie

n a streph 1. A New host record New Anastrepha parasitoid association Not possible to associate parasitoids with Anastrepha species    a b le Mangifera indica L. Spondias mombin L. CELASTRACEAE Salacia sp.  COMBRETACEAE catappa L. Terminalia EUPHORBIACEAE Manihot esculenta Crantz Inga cinnamomea Spruce ex Benth.  ANARCARDIACEAE Anacardium occidentale L. (MIMOSOIDEAE) FABACEAE Inga edulis Mart. T Plant Family and Species 272 Florida Entomologist 96(1) March 2013 Parasitoid species (n) 3 D. areolatus 0 0 0 1 D. areolatus 2 D. areolatus 0 0 10 Doryctobracon sp.2 8 A. pelleranoi 6 A. pelleranoi  0 0 0 0 0 9 D. areolatus 1 A. anastrephae 1 O. bellus  13 D. areolatus 11 D. areolatus 2 O. bellus  1 U. anastrephae  1 A. pelleranoi  21 D. areolatus 12 O. bellus species (n) Anastrepha 3 A. obliqua 19 A. obliqua 3 A. obliqua 1 A. striata 0 21 A. striata 51 A. striata 2 A. obliqua 7 A. striata 51 A. striata 5 A. turpiniae  6 A. striata 3 A. striata 20 A. striata 33 A. striata 4 A. obliqua 52 A. obliqua 35 A. bahiensis 41 A. coronilli 55 A. coronilli 17 A. obliqua

6 2 35 37 23 47 16 53 46 82 52 79 113 254 210 244 151 133 Number of pupae

3 8 11 11 65 50 15 47 15 73 49 16 12 31 43 304 219 226 of fruit Number . razil 0.7 0.5 0.1 0.3 0.4 0.3 0.7 0.5 2.7 0.9 0.8 1.2 3.3 0.3 4.6 2.2 1.5 1.3 , B (kg) weight Sample re g ion

a m azon

the

in

Collection sites São Gabriel da Cachoeira Manaus Manaus Manaus Porto Velho Manaus Maués Presidente Figueiredo Porto Velho São Gabriel da Cachoeira Manaus Manaus Maués Manaus Manaus Presidente Figueiredo Manaus Manaus s itoi ds para

d a ss ociate

Hosts an d Introduced Introduced Introduced Native Native Native Native Native Native Introduced , ho s t , s pecie

n a streph ) A ontinue d 1. ( C New host record New Anastrepha parasitoid association Not possible to associate parasitoids with Anastrepha species    a b le OXALIDACEAE carambola L. Averrhoa Syzygium jambolanum (Lam.) DC. Syzygium malaccense L. Psidium guineense Swart. Psidium guajava L. Psidium acutangulum D.C. MYRTACEAE Eugenia stipitata McVaugh MORACEAE Pouroma cecropiaefolia Mart. MELASTOMATACEAE Bellucia grossularioides (L.) Triana MALPIGHIACEAE Malpighia glabra L. T Plant Family and Species Scientific Notes 273

Summary

A new natural host for Anastrepha fractura Stone, Salacia sp., is reported for the first time in Brazil. Parasitoids attacking A. fractura are also reported. We also report Anastrepha distincta 0 0 23 D. areolatus 1 D. areolatus 0 0 Parasitoid species (n) Greene infesting Inga cinnamomea in Brazil for the first time. New associations betweenAnastre - pha species and parasitoids are also reported.

Resumo

Um novo hospedeiro natural de Anastrepha fractura Stone, Salacia sp., é relatado pela pri- A. serpentina

species (n) meira vez no Brasil. Parasitoides atacando A. Anastrepha 1 A. zenildae 105 60 A. leptozona 42 A. curitis 1 A. leptozona 13 A. serpentina 13 A. leptozona fractura são também relatados. Nós também re- latamos Anastrepha distincta Greene infestando

Inga cinnamomea no Brasil pela primeira vez. 4 6 Novas associações entre espécies de Anastrepha 57

205 e parasitoides também são relatadas. Number 1,484 of pupae

1

63 12 References Cited 194 160 of fruit Number . Aluja, M., Rull, J., Sivinski, J., Norrbom, A. L., Whar- ton, R. A., Macías-Ordoñez, R., Diaz-Fleischer, F., razil and López, M. 2003. Fruit flies of the Anas- 1.3 5.2 3.4 0.2 0.8 , B (kg)

weight trepha (Diptera: Tephritidae) and associated para- Sample sitoids (Hymenoptera) in the tropical rain forest bio- sphere reserve of Montes Azules, Chiapas, Mexico. re g ion Environ. Entomol. 32: 1377-1385. Costa, S. G. M, Querino, R. B., Ronchi-Teles, B., Pen- teado-Dias, A. M. M., and Zucchi, R. A. 2009. Para- a m azon sitoid diversity (Hymenoptera: Braconidae and Figi-

the tidae) on frugivorous larvae (Diptera: Tephritidae

in and Lonchaeidae) at Adolpho Ducke Forest Reserve,

Central Amazon Region, Manaus, Brazil. Braz. J. Biol. 69: 363-370. Collection sites López, M., Aluja, M., and Sivinski, J. 1999. Hymenop- Boa Vista Manaus Porto Velho São Gabriel da Cachoeira Manaus terous larval-pupal and pupal parasitoids of Anas- s itoi ds para trepha flies (Diptera: Tephritidae) in Mexico. Biol. Control 15: 119-129. Ronchi-Teles, B., Dutra, V. S., Tregue-Costa, A. P., Aguiar-Menezes, E. L., Mesquita, A. C. A., and Silva,

d a ss ociate J. G. 2011. Natural host plants and native parasit-

Hosts oids associated with Anastrepha pulchra and other Introduced Native Native an d Anastrepha species (Diptera: Tephritidae) in Central , Amazon, Brazil. Florida Entomol. 94(2): 347-349. Silva, N. M., and Ronchi-Teles, B. 2000. Amapá, Ama- ho s t

, zonas, Pará, Rondônia e Roraima. In Malavasi, A.; Zucchi, R. A. [eds.], Moscas-das-frutas de importância Econômica no Brasil. Conhecimento básico e aplicado. s pecie

Holos-Editora, Ribeirão Preto, São Paulo. pp. 203-209. Stone, A. 1942. The fruit flies of the genusAnastrepha . USDA Misc. Publ. 439: 1-112. Trindade, R. B. R., and Uchôa, M. A. 2011. Species of

n a streph fruit flies (Diptera: Tephritidae) in a transect of the Amazonian Rainforest in Oiapoque, Amapá, Brasil. ) A Zoologia 28: 653-657. Zucchi, R. A., Uramoto, K., and Souza-Filho, M. F. 2011. Chave ilustrada para as espécies de Anastrepha da

ontinue d região Amazônica. In R. A. Silva, W. P Lemos and R. A. Zucchi [eds.], Moscas-das-frutas na Amazônia

1. ( C Brasileira. Diversidade, Hospedeiros e Inimigos New host record New Anastrepha parasitoid association Not possible to associate parasitoids with Anastrepha species Naturais. Embrapá Amapá, Macapá, Amapá. pp.    a b le 73-90. RHAMNACEAE Ziziphus mauritiana Lam SAPOTACEAE Radlk. Pouteria caimito (Ruiz & Pav.) PASSIFLORACEAE Passiflora nitida Kunth T Plant Family and Species