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Anastrepha (Diptera: Tephritidae) species, their hosts and parasitoids (Hymenoptera: Braconidae) in five municipalities of the state of Amapa, Brazil.

Fruit flies of the genus Anastrepha Schiner are distributed across the Neotropical Region, where more than 250 species are known. In addition to being the most diverse genus in the neotropics, Anastrepha also is the economically relevant group of Tephritidae in the region (Norrbom et al. 1999; Silva et al. 2010). A total of 112 species of Anastrepha have been reported in Brazil, placing the country in a prominent position regarding fruit fly diversity on the American continent (Zucchi 2007, 2008).

Fruit flies have a wide variety of native and exotic hosts, as their larvae necessarily develop inside fruits or other plant parts, the occurrence of such flies is intimately associated with the availability of host fruits (Malavasi et al. 2000). Despite the importance of host plant relationship for fruit fly ecology, at least one host is known for only 47% of Anastrepha species in Brazil (Zucchi2008).

Identifying the host plants of Tephritidae is a fundamental stepping stone for the adequate and efficient handling of pest species. The use of a given host by a species of tephritid may vary among populations, depending on host availability and regional fruiting phenology, and on other ecological factors that may modify the fitness of larvae on different plants, or such use may simply be the result of the existence of different hosts in different regions within the geographical range of the species (Bernays & Graham 1988; Nascimento et al. 2000; Selivon 2000; Hernandez-Ortiz & Aluja 2004). Knowing the wild hosts and infestation rates of pest species is also important in trying to control/regulate them.

The recent intensification of studies on native hosts of fruit flies in little-disturbed areas has been providing relevant information on fruit fly/ host associations. These works have been fundamentally important to the clarification of host use patterns and the ecological and evolutionary processes pertinent to these insects (Uramoto et al. 2008). These studies are also important for determining interactions among different species competing for different hosts.

In the Brazilian Amazon, the available knowledge on fruit flies and their hosts expanded considerably in recent years, with 60 species of Anastrepha recorded thus far (Trindade & Uchoa 2011; Zucchi et al. 2011). The state of Amapa, where 33 species of Anastrepha have been reported to date, has been making substantial contributions to knowledge on Anastrepha species richness and their hosts in Amazonian ecosystems (Zucchi2008; Trindade & Uchoa 2011); and the list of known hosts is constantly increasing (Jesus et al. 2008ab, 2010; Silva et al. 2009).

Aluja (1999) points out that native fruit flies may be at risk of extinction because of the rapid devastation of tropical forests. This makes it urgent and essential for conservation purposes to know not only the existing species of Anastrepha, but especially their relationship with native and/ or wild hosts and tritrophic interactions among wild tephritoids, their host plants and parasitoids in these environments.

The purpose of this work was to identify the species of Anastrepha, their natural and introduced hosts and the associated parasitoid species in 5 municipalities of the eastern zone of the Brazilian state of Amapa.

MATERIALS AND METHODS

The Brazilian state of Amapa is located in the Eastern Amazon, bordering the state of Para to the South and West, the Atlantic Ocean to the East, French Guiana to the North, and Suriname to the Northwest (Fig. 1) (Porto 2007). Fruits were collected from urban and rural areas of the municipalities of Cutias do Araguari, Itaubal do Piririm, Ferreira Gomes, Pracuuba, and Tartarugalzinho in eastern Amapa (Fig. 1). The sampled region is located between latitudes N 00[degrees] 30' 14.8" and N 01[degrees] 45' 37.2" and between longitudes W 50[degrees] 41' 51.4" and 51 14' 15.7". The climates prevailing in the region, according to the Koeppen-Geiger classification, are Aw (tropical savanna) and Am (tropical monsoon) with an average annual precipitation of 2,300 mm to 2,400 mm (Pell et al. 2007). The rainy period is from Jan to Jun, and a characteristically dry period occurs most often between Sep and Nov. The average annual temperature is 26[degrees]C (IBGE 2011). The vegetation in this region is comprised of "Cerrado", floodplain forest, dry-land forest, and cerrado/forest and cerrado/floodplain transition forests (IEPA 2002).

Fruits of native, subspontaneous or naturalized and exotic plant species were collected at monthly intervals between Feb 2006 and Aug 2007 in urban and rural areas of each of the 5 municipalities. At each collection event, fruits of potential fruit fly hosts were sampled at random from different ecosystems. The fruits were collected directly off the plants or from the ground (if recently fallen), from plants that bore abundant numbers of maturing or ripe fruits.

The fruits were stored in coolers or cotton sacks (depending on the characteristics of each fruit), then transported to the Laboratorio de Entomologia at Embrapa Amapa, in the city of Macapa. In the laboratory, fruit samples were processed to retrieve tephritid and parasitoid pupae, as per Silva et al. (2011a).

After adult emergence, tephritids and braconids were identified with identification keys (Zucchi 2000; Canal & Zucchi 2000). Voucher specimens were deposited in the Laboratorio de Entomologia at Embrapa Amapa (Macapa, Amapa, Brazil).

For those plants that could not be identified in the field botanical material consisting of dried pressed specimens was collected for later identification as per Fidalgo & Bononi (1984). Dried specimens were prepared and deposited at the Herbario Amapaense (HAMAB) of the Instituto de Pesquisas Cientificas e Tecnologicas do Amapa --IEPA (Macapa, Amapa, Brazil), where they were identified and added to the institute's collection. Taxonomic names were updated to match the List of Species of the Brazilian Flora by the Rio de Janeiro Botanical Garden (Forzza et al. 2010), and plant families were classified according to APGII (2003).

The rates of infestation by fruit flies were expressed as number of puparia per fruit ([I.sub.pp/f]) and number of puparia per kilogram of fruit ([I.sub.pp/kg]). Percentage of parasitism was calculated as the ratio of emerged parasitoids to known number of puparia (P = number of emerged parasitoids/total number of puparia x 100).

Results and Discussion

A total of 817 samples (1,094.36 kg) of potential fruit fly hosts were collected from 70 plant species across 29 families (Table 1). Among the sampled plant species, Psidium guajava L.; Myrtales: Myrtaceae (guava) and Anacardium occidentale L; Sapindales: Anacardiaceae (cashew) are the most widely known and commonly grown in other regions of Brazil. Most other species were native (some of them found in a wild state), obtained from backyards or small rural properties where these plants are used for household consumption.

Collection efforts were most strongly focused on Fabaceae (10 species), Myrtaceae (7), and Arecaceae (7) (Fig. 2). Most of the collected families (55.2%) were represented by 3 or more plant species.

Among the sampled species, 22 were infested by Anastrepha, and Fabaceae was the family with the highest number of infested species, all of them in the genus Inga. This may be a reflection of the locations where collections took place, as Inga spp. are frequently found in brushwood areas and forest remnants (Cavalcante 1991) which are more easily accessible and located closer to human dwellings. Myrtaceae was second in number of collected and infested species, followed by Anacardiaceae. It should also be noted that all sampled species of Sapotaceae and Melastomataceae were infested (Fig. 2). Other studies exploring wild fruits in Brazil have emphasized Myrtaceae as the plant family with the highest rates of infestation by Tephritidae. Uramoto et al. (2008) analyzed the associations of tephritids with native hosts in the state of Espirito Santo, where they collected fruit samples from 248 plant species (51 families). Among them, Myrtaceae was the most diversified family. Silva et al. (2010) studied the diversity of Anastrepha in native and exotic hosts in the state of Bahia. The authors collected fruits of 27 plant species (15 families), of which only 6 families were infested by Anastrepha of which the Myrtaceae had the highest infestation rate.

The tephritids obtained in this work all belonged to the genus Anastrepha. We did not collect any Bactrocera carambolae Drew & Hancock and Ceratitis capitata (Wiedemann). Bactrocera carambolae is found only in the state of Amapa where an eradication program is underway (Godoy et al. 2011). Ceratitis capitata has not been detected in the state (Silva et al. 2011).Twelve species of Anastrepha were identified (Table 2): Anastrepha striata Schiner (82.65%), Anastrepha coronilli Carrejo & Gonzalez (6.63%), Anastrepha obliqua (Macquart) (5.47%), Anastrepha distincta Greene (2.28%), Anastrepha fraterculus (Wiedemann) (2.10%), Anastrepha parishi Stone (0.30%), Anastrepha leptozona Hendel (0.22%), Anastrepha pickeli Lima (0.11%), Anastrepha antunesi Lima (0.07%), Anastrepha serpentina (Wiedemann) (0.07%), Anastrepha sororcula Zucchi (0.06%), and Anastrepha zenildae Zucchi (0.04%).

Anastrepha striata had by far the highest number of hosts (14 species of fruit belonging to 8 families) (Table 2). Anastrepha fraterculus was observed in 5 host species (4 families). Studies conducted in the Southeast and Northeast regions of Brazil have reported A. fraterculus as the most polyphagous species (Uramoto et al. 2008; Silva et al. 2010). However, in the Amazon region, this species has been reported on only 10 hosts, whereas A. striata has a higher number of known hosts: 28 species in 16 botanical families (Zucchi et al. 2011). Deus et al. (2009), while studying fruit flies in the municipalities of Pedra Branca do Amapari and Serra do Navio in the state of Amapa, indicated that A. striata has the highest number of hosts and is the most abundant species in guava fruits, confirming its supremacy in North Brazil in relation to A. fraterculus, which is the predominant tephritid in guava in Southeast Brazil. In fact, A. striata is seen as the bio-geographical opposite of A. fraterculus because it becomes gradually more common as one moves northward along its distribution in Brazil (Mala vasi et al. 2000).

Anastrepha distincta Greene was observed in 7 hosts, 5 of which belonged to Inga (Fabaceae), indicating that the species presents an intimate association with this plant genus (Table 2). Anastrepha distincta in Amapa showed a narrower spectrum of hosts than that reported in other studies, for among the 8 plant species where this tephritid has been reported in the Brazilian Amazon, 4 are Fabaceae, 2 Clusiaceae, 1 Myrtaceae, and 1 Anacardiaceae (Zucchi et al. 2011).

Some species were observed in only one host: A. serpentina in Pouteria sp.2; A. leptozona in Pouteria sp.1; A. zenildae in P. guajava, and A. pickeli in Manihot sp. (Table 2). The latter is the first record of a host of A. pickeli in the Brazilian Amazon, and this species is found in all regions of the country, where 2 host plant species have been reported to date (Zucchi 2008). However, only A. pickeli has been reported in the Amazon, and until now had been collected as adults with McPhail traps. Anastrepha pickeli belongs to the spatulata group, in which some species infest Manihot spp. and use a specialized mechanism to detoxify the glycosides present in these fruits (Selivon 2000).

The periods of occurrence of the different tephritid species were variable. Anastrepha striata was constantly present in P. guajava, with sporadic presence detected in other hosts (Table 2). It is a generalist species that occurs in 27 host species from 11 families, with a strong preference for hosts of the genus Psidium (Myrtaceae) (Selivon 2000; Norrbom 2005; Weems & Fasulo 2009).

Adult flies were obtained from 22 plant species, most of them wild (Table 3). Anastrepha striata was collected in greatest abundance (the highest number of individuals) in a single host species (4,176 specimens in P. guajava), followed by A. obliqua (282 in Spondias mombin), and A. coronilli (225 in Bellucia grossularioides L.) (Table 3). According to Silva et al. (2011), A. striata is not only the species with the highest number of hosts, it is also the most abundant and widely distributed Anastrepha species in the state of Amapa.

Anastrepha parishi was found in P. guajava and Bellucia imperialis, expanding its list of known hosts in Brazil after having been reported recently in fruits of Oenocarpus bacaba (Arecaceae) (Jesus et al. 2008a; Zucchi et al. 2011). Adaime et al. (2012) published the irst host record of A. parishi in Myrciaria dubia Mc Vaugh in the state of Roraima, Brazil.

Anastrepha striata and A. fraterculus were found in Anacardium occidentale (Table 3). Cashew has already been reported as a host of A. striata in Amapa, A. leptozona in Amazonas, and A. obliqua in Tocantins (Jesus et al. 2008b; Zucchi et al. 2011) but this is the irst report of A. occidentale as a host of A. fraterculus in Brazil.

Of all the collected fruits, 23 species were infested. In P. caimito was only recorded the emergence of adult braconid parasitoids but no tephritids, whereas the other infested plant species revealed the presence of both Anastrepha and parasitoids. All the collected samples of Inga sp. 4, Inga sp. 5, Manihot sp., Pouteria sp. 1, Pouteria sp. 2, and Psidium guineense were infested (Table 4). An analysis of infestation rates showed that wild fruits were more infested by Anastrepha than introduced plant species. In terms of puparia/kg of fruit, Pouteria sp.1 was the most infested (434.29 pp/kg), followed by Manihot sp. (130.43 pp/kg) and Inga sp.5 (120.62 pp/kg). In terms of puparia/fruit, Pouteria sp. 2 (2.5 pp/fruit) and C. utilis (1.99 pp/fruit) presented the highest rates. According to Silva et al. (2011b), the highest reported infestation rates in the state of Amapa occur in native fruits of the Amazon region, where usually only 1 species of Anastrepha is present or predominant. We also highlight the considerable infestation rates found in guava (41.16 pp/kg and 1.82 pp/fruit), which are similar to the ones already reported in other studies in the state of Amapa (from 13.3 to 58.3 pp/kg) (Silva et al. 2011b). Araujo & Zucchi (2003) reported that guava is one of the most tephritid-infested fruits in Brazil, with infestation rates varying across different regions of the country, and influenced mainly by rainfall and host availability. Infestation ranged from 35 to 118 pp/kg in their experiment in Northeast Brazil, which caused a 78-100% loss of guava crops.

The efficient control of fruit fly populations requires the integration of several methods, including cultural, mechanical, biological, and chemical. However, some basic pre-requisites are indispensable for the successful implementation of an integrated control system for fruit flies, such as knowledge of the bio-ecology of fruit infesting populations, as well as the phenology and distribution of their host plant species and natural enemies. Nevertheless, the use of Braconidae parasitoids has been intensiied in several countries of America (Ovruski et al. 2000).

The present work recorded a total of 652 specimens of parasitoids, all of them Braconidae: Doryctobracon areolatus (Szepligeti, 1911) (95.86%), Opius bellus Gahan, 1930 (2.76%), Asobara an astrephae (Muesebeck, 1958) (1.07%), and Utetes anastrephae (Viereck, 1913) (0.31%) (Fig. 3). Doryctobracon areolatus was the most abundant and was present in all plant species where parasitoid emergence was observed (Fig. 3). The predominance of D. areolatus in the state of Amapa had already been highlighted by Silva et al. (2011b). This species has been revealing itself to be an important parasitoid in Brazil and Latin America, both on account of its abundance and its widespread distribution (Canal & Zucchi 2000; Carvalho et al. 2010; Leonel Jr. et al. 1995; Ovruski et al. 2000).

Although guava presented the highest ratio of number of adult parasitoids to number of observed puparia, S. mombin (hog plum) was the plant species with the highest rate of parasitoid occurrence (8.45%) (Fig. 4), hog plum also contained the highest parasitoid species richness (Fig. 4b). In a study on parasitoids of tephritids in the state of Amazonas, Canal et al. (1995) also reported that the majority of parasitoids were obtained from hog plum. According to Leonel (1991), these fruits might be subject to intense parasitism because parasitoids can ind host larvae with more ease in fruits of small size, thin skin and shallow flesh, such as those of hog plum. According to Sivinski et al. (1997), smaller fruit attracts parasitoids with short ovipositors because it is easier to find fly larvae, whereas parasitoids with long ovipositors are able to seek larvae in fruits of varying flesh thicknesses. This means that parasitoids with long ovipositors (>6 mm) occur on fruits of all sizes, whereas parasitoids with smaller ovipositors (<3 mm) can only infest the larvae found in small fruits. Doryctobracon areolatus has a long ovipositor and this characteristic is a factor explaining to its predominant position as the most common parasitoid of fruit fly larvae in the braconid's natural distribution range. Other studies in the state of Amapa have shown the importance of hog plum as a "reservoir" of para sitoids (Silva et al. 2007; Cunha et al. 2011).

A parasitoid/fruit fly association can be established when a single species of fly and a single species of parasitoid are the only ones to emerge in the same rearing container (Leonel Jr. et al. 1996). We were able to conirm that D. areolatus is associated with 6 species of Anastrepha; the parasitoids A. anastrephae, O. bellus and U. anastrephae were associated with 3, 2, and 1 species respectively (Table 5). For the state of Amapa records of U. anastrephae infesting A. obliqua, D. areolatus infesting A. fraterculus and A. parishi, and A. anastrephae infesting A. fraterculus are irst-time reports.

In conclusion, based on fruit sampling in 5 municipalities in eastern Amapa, it is possible conclude that A. striata is the most abundant and polyphagous tephritid species in the region. The highest rates of infestation by Anastrepha were found in wild plant species. The highest parasitism levels occurred in fruits of S. mombin and D. areolatus was the most abundant parasitoid species.

ACKNOWLEDGMENTS

To Mr. Carlos Alberto Moraes for his assistance during fruit collection. To the anonymous reviewers and the editor for their contribution in this manuscript. Also, we thank the Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq) for granting a Regional Scientific Development Fellowship to CRJB, a Research Productivity Fellowship to RA and an Undergraduate Research Fellowship to MNO; and the Secretaria de Estado da Ciencia e Tecnologia do Amapa for financial aid to this research.

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TRINDADE, R. B. R., AND UCHOA, M. A. 2011. Species of fruit flies (Diptera: Tephritidae) in a transect of the amazonian rainforest in Oiapoque, Amapa, Brazil. Zoologia 28(5): 653-657.

URAMOTO, K, MARTINS, D. S., AND ZUCCHI, R. A. 2008. Fruit flies (Diptera, Tephritidae) and their associations with native host plants in a remnant area of the highly endangered Atlantic Rain Forest in the State of Espirito Santo, Brazil. Bull. Entomol. Res. 98: 457-466.

WEEMS JR, H. V., AND FASULO, T. R. 2009. Guava fruit fly, Anastrepha striata Schiner (Insecta: Diptera: Tephritidae). Available at: http://edis.ifas.ufl.edu/pdffiles/IN/IN54400.pdf. [revision date: 2009].

ZUCCHI, R. A. 2000. Taxonomia, pp. 13-24 In A. Malavasi and R. A. Zucchi [eds.], Moscas-das-frutas de importancia economica no Brasil: conhecimento basico e aplicado. Holos. Ribeirao Preto.

ZUCCHI, R. A. 2007. Diversidad, distribucion y hospedeiros del genero Anastrepha en Brasil, pp. 77-100 In V. Hernandez-Ortiz [ed.], Moscas de la fruta en Latinoamerica (Diptera: Tephritidae): diversidad, biologia y manejo. S y G editores: Mexico City, Mexico.

ZUCCHI, R. A. 2008. Fruit flies in Brazil-Anastrepha species and their hosts plants. Available at: www.lea. esalq.usp.br/anastrepha/.[revision date: 05/04/2011].

ZUCCHI, R. A., SILVA, R. A., AND DEUS, E. G. 2011. Especies de Anastrepha e seus hospedeiros na Amazonia brasileira, pp. 53-70 In R. A. Silva, W. P. Lemos and R. A. Zucchi [eds.], Moscas-das-frutas na Amazonia brasileira: diversidade, hospedeiros e inimigos naturais. Embrapa Amapa. Macapa.

CRISTIANE R. JESUS-BARROS (1), RICARDO ADAIME (1), MANOELA N. OLIVEIRA (2), WILSON R. SILVA (3), SALUSTIANO V. COSTA-NETO (4) AND MIGUEL F. SOUZA-FILHO (5)

(1) Embrapa Amapa, Rodovia Juscelino Kubitschek, km 5, No. 2600, Macapa, Amapa, Brasil

(2) Universidade Federal do Amapa (UNIFAP), Rodovia Juscelino Kubitschek, km 2, Macapa, Amapa, Brasil

(3) Secretaria de Estado da Educacao do Amapa, Avenida FAB, 96, Macapa, Amapa, Brasil

(4) Instituto de Pesquisas Cientificas e Tecnologicas do Amapa (IEPA), Rodovia Juscelino Kubitschek, km 10, Macapa, Amapa, Brasil

(5) Instituto Biologico, Rodovia Heitor Penteado, km 3, Campinas, Sao Paulo, Brasil

Corresponding author; E-mail: adaime@cpafap.embrapa.br

TABLE 1. PLANT SPECIES SAMPLED IN THE MUNICIPALITIES
OF CUTIAS DO ARAGUARI, ITAUBAL DO PIRIRIM, FERREIRA GOMES,
PRACUUBA, AND TARTARUGALZINHO IN AMAPA, BRAZIL,
FEB 2006 TO AUG 2007.

Family/Species             Origin *

Anacardiaceae

  Anacardium                  N
  occidentale L.
  Mangifera indica L.         SS

  Spondias mombin L.          N
  Spondias purpurea L.        E

Annonaceae

  Annona paludosa Aubl.       N
  Annona squamosa L.          E
  Annona muricata L.          E
  Annona mucosa               N
    (Jacq.) Bail.

Apocynaceae

  Ambelania acida Aubl.       N
  Couma utilis                N
    (Mart.) M. Arg.
  Parahancornia amapa         N
    (Huber) Ducke

Arecaceae

  Astrocaryum                 N
    vulgare L.
  Attalea maripa              N
    (Aubl.) Mart.
  Attalea phalerata           N
  Mart. ex Spring.
  Bactris maraja Mart.        N
  Bactris gasipaes            N
    Kunth.
  Oenocarpus bacaba           N
    Mart.
  Oenocarpus distichus        N
    Mart.

Bignoniaceae

  Jacaranda copaia            N
    (Aubl.) D. Don

Bromeliaceae

  Ananas ananassoides         N
    (Baker) L.B. Sm.
  Ananas comosus              N
    (L.) Merr.

Burseraceae

  Protium heptaphyllum        N
    (Aubl.) March.
  Trattinnickia               N
    burserifolia Mart.

Caricaceae

  Carica papaya L.            SS

Caryocaraceae

  Caryocar glabrum            N
    Pers.

Chrysobalanaceae

  Licania macrophylla         N
    Benth.
  Chrysobalanus icaco L.      N

Dilleniaceae

  Doliocarpus sp.             N

Dioscoreaceae

  Dioscorea alata L.          N

Euphorbiaceae

  Manihot sp.                 N

Celastraceae

  Cheiloclinium               N
    cognatum
    (Miers) A.C. Sm.

Humiriaceae

  Endopleura uchi             N
    (Huber) Cuatrec.

Lauraceae

  Licaria mahuba              N
    (A. Samp.) Kostern.
  Persea americana            SS
    Mill.

Malpighiaceae

  Byrsonima crassifolia       N
    (L.) Kunth
  Malpighia                   N
    punicifolia L.

Lamiaceae

  Gmelina arborea             N
    Roxb. ex Sm.

Melastomataceae

  Bellucia imperialis         N
    Saldanha & Cogn.
  Bellucia                    N
    grossularioides
   (L.) Triana.
  Mouriri acutiflora          N
    Naud.

Fabaceae

  Inga edulis Mart.           N
  Inga fagifolia G. Don       N
  Inga heterophylla           N
    Willd.
  Inga velutina Willd         N
  Inga sp. 1                  SS
  Inga sp. 2                  N
  Inga sp. 3                  N
  Inga sp. 4                  N
  Inga sp. 5                  N
  Inga sp. 6                  N

Moraceae

  Artocarpus                  SS
    heterophyllus Lam.
  Ficus sp.                   N

Myrtaceae

  Campomanesia                N
    xanthocarpa O. Berg.
  Eugenia cumini              SS
    (L.) Druce
  Eugenia luschnathiana       SS
    Klotzsch ex O. Berg
  Eugenia malaccensis L.      N
  Psidium guajava L.          N
  Psidium guineense SW        N
  Psidium sp. 2               N

Oxalidaceae

  Averrhoa bilimbi L.         SS
  Averrhoa carambola L.       SS

Passifloraceae

  Passiflora sp. 1            N
  Passiflora sp. 2            N

Rubiaceae

  Coffea arabica L.           SS

Rutaceae

  Citrus sinensis             SS
    (L.) Osbeck.
  Citrus sp.                  N

Sapotaceae

  Pouteria caimito            N
    (Ruiz & Pav.) Radlk.
  Pouteria sp. 1              N
  Pouteria sp. 2              N

Solanaceae

   Solanum paniculatum L.     N

N = native species, E = exotic species, SS = subspontaneous.

TABLE 2. ANASTREPHA SPECIES, HOSTS AND PERIOD OF OCCURRENCE IN
FRUITS COLLECTED IN CUTIAS DO ARAGUARI, ITAUBAL DO PIRIRIM,
FERREIRA GOMES, PRACUUBA, AND TARTARUGALZINHO IN AMAPA, BRAZIL,
FEB 2006 TO AUG 2007.

                                                   Period and site of
                                                     sampling *

Host plant                                         2006

Tephritidae     Family            Species          F      M      A

A. antunesi     Anacardiaceae     S. mombin
                Melastomataceae   B. imperialis
A. coronilli    Melastomataceae   B. imperialis
                Myrtaceae         P. guajava              T      CT
A. distincta    Fabaceae          Inga sp. 1       T      T      T
                                  Inga sp. 4
                                  Inga sp. 5
                                  I. edulis
                                  I. fagifolia
                Myrtaceae         P. guajava
                Oxalidaceae       A. carambola
A fraterculus   Anacardiaceae     A. occidentale
                                  S. mombin        T      I
                Malpighiaceae     B. crassifolia   C
                Melastomataceae   M. acutiflora
                Myrtaceae         P. guajava       T      T      T
A. leptozona    Sapotaceae        Pouteria sp. 1
A obliqua       Anacardiaceae     S. mombin        CT     CFIP   FP
                                  S. purpurea
A parishi       Melastomataceae   B. imperialis
                Myrtaceae         P. guajava
A pickeli       Euphorbiaceae     Manihot sp.
A. serpentina   Sapotaceae        Pouteria sp. 2
A. sororcula    Melastomataceae   B. grossu-
                                    larioides
                                  M. acutiflora
A. striata      Anacardiaceae     A. occidentale
                                  S. mombin
                Apocynaceae       C. utilis
                Arecaceae         O. bacaba
                Fabaceae          Inga sp.1               T
                                  Inga sp. 4
                                  Inga edulis
                Malpighiaceae     B. crassifolia
                Melastomataceae   B. grossu-
                                    larioides
                                  B. imperialis
                Myrtaceae         E. luschna-
                                  thiana
                                  P. guajava       CFIT   CIPT   CFIT
                                  P. guineense
                Oxalidaceae       A. carambola
A. zenildae     Myrtaceae         P. guajava

                                                   Period and site of
                                                      sampling *

Host plant                                         2006

Tephritidae     Family            Species          M      J      J

A. antunesi     Anacardiaceae     S. mombin
                Melastomataceae   B. imperialis           C
A. coronilli    Melastomataceae   B. imperialis           FT     CFT
                Myrtaceae         P. guajava              IT
A. distincta    Fabaceae          Inga sp. 1
                                  Inga sp. 4       T
                                  Inga sp. 5
                                  I. edulis        CFI    T      T
                                  I. fagifolia
                Myrtaceae         P. guajava
                Oxalidaceae       A. carambola
A fraterculus   Anacardiaceae     A. occidentale
                                  S. mombin
                Malpighiaceae     B. crassifolia
                Melastomataceae   M. acutiflora
                Myrtaceae         P. guajava       CP
A. leptozona    Sapotaceae        Pouteria sp. 1
A obliqua       Anacardiaceae     S. mombin        CFIP
                                  S. purpurea
A parishi       Melastomataceae   B. imperialis           T
                Myrtaceae         P. guajava
A pickeli       Euphorbiaceae     Manihot sp.
A. serpentina   Sapotaceae        Pouteria sp. 2
A. sororcula    Melastomataceae   B. grossu-
                                    larioides
                                  M. acutiflora
A. striata      Anacardiaceae     A. occidentale
                                  S. mombin        C
                Apocynaceae       C. utilis
                Arecaceae         O. bacaba
                Fabaceae          Inga sp.1
                                  Inga sp. 4       F
                                  Inga edulis      C
                Malpighiaceae     B. crassifolia
                Melastomataceae   B. grossu-
                                    larioides
                                  B. imperialis           FT
                Myrtaceae         E. luschna-
                                  thiana
                                  P. guajava       CFIPT  CFIPT  IFP
                                  P. guineense
                Oxalidaceae       A. carambola                   C
A. zenildae     Myrtaceae         P. guajava

                                                   Period and site of
                                                      sampling *

Host plant                                         2006

Tephritidae     Family            Species          A      S      O

A. antunesi     Anacardiaceae     S. mombin
                Melastomataceae   B. imperialis    C
A. coronilli    Melastomataceae   B. imperialis    T             T
                Myrtaceae         P. guajava
A. distincta    Fabaceae          Inga sp. 1                     T
                                  Inga sp. 4
                                  Inga sp. 5
                                  I. edulis        CI            FT
                                  I. fagifolia
                Myrtaceae         P. guajava
                Oxalidaceae       A. carambola
A fraterculus   Anacardiaceae     A. occidentale
                                  S. mombin
                Malpighiaceae     B. crassifolia
                Melastomataceae   M. acutiflora
                Myrtaceae         P. guajava
A. leptozona    Sapotaceae        Pouteria sp. 1
A obliqua       Anacardiaceae     S. mombin
                                  S. purpurea
A parishi       Melastomataceae   B. imperialis
                Myrtaceae         P. guajava
A pickeli       Euphorbiaceae     Manihot sp.
A. serpentina   Sapotaceae        Pouteria sp. 2
A. sororcula    Melastomataceae   B. grossu-
                                    larioides
                                  M. acutiflora
A. striata      Anacardiaceae     A. occidentale
                                  S. mombin
                Apocynaceae       C. utilis
                Arecaceae         O. bacaba
                Fabaceae          Inga sp.1
                                  Inga sp. 4
                                  Inga edulis      I             F
                Malpighiaceae     B. crassifolia
                Melastomataceae   B. grossu-
                                    larioides
                                  B. imperialis                  T
                Myrtaceae         E. luschna-
                                  thiana
                                  P. guajava       FITP   CFIPT  CFIPT
                                  P. guineense
                Oxalidaceae       A. carambola
A. zenildae     Myrtaceae         P. guajava       P

                                                   Period and site of
                                                      sampling *

Host plant                                         2006          2007

Tephritidae     Family            Species          N      D      J

A. antunesi     Anacardiaceae     S. mombin                      P
                Melastomataceae   B. imperialis
A. coronilli    Melastomataceae   B. imperialis           T
                Myrtaceae         P. guajava
A. distincta    Fabaceae          Inga sp. 1
                                  Inga sp. 4       F
                                  Inga sp. 5                     F
                                  I. edulis        TP     CIT    CFIP
                                  I. fagifolia                   T
                Myrtaceae         P. guajava       T      I
                Oxalidaceae       A. carambola     I
A fraterculus   Anacardiaceae     A. occidentale          P
                                  S. mombin                      P
                Malpighiaceae     B. crassifolia
                Melastomataceae   M. acutiflora
                Myrtaceae         P. guajava
A. leptozona    Sapotaceae        Pouteria sp. 1                 F
A obliqua       Anacardiaceae     S. mombin                      C
                                  S. purpurea      T
A parishi       Melastomataceae   B. imperialis
                Myrtaceae         P. guajava              P
A pickeli       Euphorbiaceae     Manihot sp.
A. serpentina   Sapotaceae        Pouteria sp. 2
A. sororcula    Melastomataceae   B. grossu-
                                    larioides
                                  M. acutiflora
A. striata      Anacardiaceae     A. occidentale          P
                                  S. mombin
                Apocynaceae       C. utilis                      F
                Arecaceae         O. bacaba
                Fabaceae          Inga sp.1
                                  Inga sp. 4
                                  Inga edulis      P             CFT
                Malpighiaceae     B. crassifolia                 C
                Melastomataceae   B. grossu-
                                    larioides
                                  B. imperialis
                Myrtaceae         E. luschna-      C
                                  thiana
                                  P. guajava       CFIPT  CFIPT  CFIPT
                                  P. guineense
                Oxalidaceae       A. carambola     C
A. zenildae     Myrtaceae         P. guajava

                                                   Period and site of
                                                     sampling *

Host plant                                         2007

Tephritidae     Family            Species          F      M      A

A. antunesi     Anacardiaceae     S. mombin
                Melastomataceae   B. imperialis
A. coronilli    Melastomataceae   B. imperialis    T
                Myrtaceae         P. guajava
A. distincta    Fabaceae          Inga sp. 1
                                  Inga sp. 4
                                  Inga sp. 5
                                  I. edulis        TP     FP     C
                                  I. fagifolia
                Myrtaceae         P. guajava                     F
                Oxalidaceae       A. carambola
A fraterculus   Anacardiaceae     A. occidentale
                                  S. mombin               I      P
                Malpighiaceae     B. crassifolia
                Melastomataceae   M. acutiflora    CT
                Myrtaceae         P. guajava       FPT    I      T
A. leptozona    Sapotaceae        Pouteria sp. 1   F
A obliqua       Anacardiaceae     S. mombin        FPT    FIP    FP
                                  S. purpurea
A parishi       Melastomataceae   B. imperialis
                Myrtaceae         P. guajava
A pickeli       Euphorbiaceae     Manihot sp.                    P
A. serpentina   Sapotaceae        Pouteria sp. 2
A. sororcula    Melastomataceae   B. grossu-
                                    larioides
                                  M. acutiflora           C
A. striata      Anacardiaceae     A. occidentale
                                  S. mombin               P
                Apocynaceae       C. utilis
                Arecaceae         O. bacaba        I      P
                Fabaceae          Inga sp.1
                                  Inga sp. 4
                                  Inga edulis      T
                Malpighiaceae     B. crassifolia
                Melastomataceae   B. grossu-
                                    larioides
                                  B. imperialis
                Myrtaceae         E. luschna-
                                  thiana
                                  P. guajava       CFIPT  CFIPT  CFIT
                                  P. guineense     P
                Oxalidaceae       A. carambola
A. zenildae     Myrtaceae         P. guajava

                                                   Period and site of
                                                       sampling *

Host plant                                         2007

Tephritidae     Family            Species          M      J      J

A. antunesi     Anacardiaceae     S. mombin
                Melastomataceae   B. imperialis
A. coronilli    Melastomataceae   B. imperialis    F      F      CFT
                Myrtaceae         P. guajava
A. distincta    Fabaceae          Inga sp. 1                     F
                                  Inga sp. 4
                                  Inga sp. 5
                                  I. edulis
                                  I. fagifolia
                Myrtaceae         P. guajava
                Oxalidaceae       A. carambola
A fraterculus   Anacardiaceae     A. occidentale
                                  S. mombin
                Malpighiaceae     B. crassifolia
                Melastomataceae   M. acutiflora
                Myrtaceae         P. guajava       CIT
A. leptozona    Sapotaceae        Pouteria sp. 1
A obliqua       Anacardiaceae     S. mombin        FP
                                  S. purpurea
A parishi       Melastomataceae   B. imperialis
                Myrtaceae         P. guajava
A pickeli       Euphorbiaceae     Manihot sp.
A. serpentina   Sapotaceae        Pouteria sp. 2
A. sororcula    Melastomataceae   B. grossu-
                                    larioides
                                  M. acutiflora
A. striata      Anacardiaceae     A. occidentale
                                  S. mombin        P
                Apocynaceae       C. utilis
                Arecaceae         O. bacaba
                Fabaceae          Inga sp.1
                                  Inga sp. 4
                                  Inga edulis
                Malpighiaceae     B. crassifolia
                Melastomataceae   B. grossu-                     F
                                    larioides
                                  B. imperialis
                Myrtaceae         E. luschna-
                                  thiana
                                  P. guajava       CFIPT  CFIPT  CIP
                                  P. guineense
                Oxalidaceae       A. carambola
A. zenildae     Myrtaceae         P. guajava

                                                   Period and site of
                                                    sampling *

Host plant                                         2007

Tephritidae     Family            Species          A

A. antunesi     Anacardiaceae     S. mombin
                Melastomataceae   B. imperialis
A. coronilli    Melastomataceae   B. imperialis    CF
                Myrtaceae         P. guajava
A. distincta    Fabaceae          Inga sp. 1       C
                                  Inga sp. 4
                                  Inga sp. 5
                                  I. edulis
                                  I. fagifolia
                Myrtaceae         P. guajava
                Oxalidaceae       A. carambola
A fraterculus   Anacardiaceae     A. occidentale
                                  S. mombin
                Malpighiaceae     B. crassifolia
                Melastomataceae   M. acutiflora
                Myrtaceae         P. guajava
A. leptozona    Sapotaceae        Pouteria sp. 1
A obliqua       Anacardiaceae     S. mombin
                                  S. purpurea
A parishi       Melastomataceae   B. imperialis
                Myrtaceae         P. guajava       IT
A pickeli       Euphorbiaceae     Manihot sp.
A. serpentina   Sapotaceae        Pouteria sp. 2   C
A. sororcula    Melastomataceae   B. grossu-
                                    larioides
                                  M. acutiflora
A. striata      Anacardiaceae     A. occidentale
                                  S. mombin
                Apocynaceae       C. utilis
                Arecaceae         O. bacaba
                Fabaceae          Inga sp.1
                                  Inga sp. 4
                                  Inga edulis
                Malpighiaceae     B. crassifolia
                Melastomataceae   B. grossu-
                                    larioides
                                  B. imperialis
                Myrtaceae         E. luschna-
                                  thiana
                                  P. guajava       CFIT
                                  P. guineense
                Oxalidaceae       A. carambola
A. zenildae     Myrtaceae         P. guajava

* C = Cutias do Araguari, F = Ferreira Gomes, I = Itaubal do Piririm,
T = Tartarugalzinho, P = Pracuuba.

TABLE 3. HOSTS AND NUMBER OF INDIVIDUALS OF ANASTREPHA
IN FRUITS COLLECTED IN CUTIAS DO ARAGUARI, ITAUBAL DO
PIRIRIM, FERREIRA GOMES, PRACUUBA, AND TARTARUGALZINHO
IN AMAPA, BRAZIL, FEB 2006 TO AUG 2007.

                      Host plant

Family           Species           Common name     Anastrepha
                                                   (number of females)

Anacardiaceae    A. occidentale    Cashew          A. striata (3)
                                                   A. fraterculus (1)
                 S. mombin         Hog plum        A. striata (33)
                                                   A. obliqua (282)
                                                   A. fraterculus (9)
                                                   A. antunesi (1)
                 S. purpurea       Jocote          A. obliqua (4)
Apocynaceae      C. utilis         Sorva           A. striata (48)
Arecaceae        O. bacaba         Bacaba          A. striata (24)
Euphorbiaceae    Manihot sp.       Cassava fruit   A. pickelli (6)
Fabaceae         I. edulis         Ice-cream-bean  A. striata (98)
                                                   A. distincta (157)
                 I. fagifolia      Sweet pea       A. distincta (3)
                 I. velutina       "Hairy inga"    A. striata (8)
                 Inga sp.1         Inga            A. striata (4)
                                                   A. distincta (103)
                 Inga sp.4         "Dwarf inga"    A. striata (8)
                                                   A. distincta (70)
                 Inga sp.5         Monkey inga     A. distincta (35)
Malpighiaceae    B. crassifolia    Nance           A. striata (1)
                                                   A. fraterculus (5)
Melastomataceae  B. grossul-       Goiaba-de-anta  A. striata (24)
                   arioides                        A. coronilli (225)
                                                   A. antunesi (3)
                 B. imperialis     Red goiaba-     A. striata (1)
                                     de-anta       A. sororcula (1)
                                                   A. coronilli (115)
                                                   A. parishi (1)
                 M. acutiflora     Mamuriballi     A. fraterculus (3)
                                                   A. sororcula (2)
Myrtaceae        E. luschnathiana  Pitomba         A. striata (3)
                 P. guajava        Guava           A. striata (4,176)
                                                   A. parishi (15)
                                                   A. coronilli (16)
                                                   A. fraterculus (95)
                                                   A. distincta (13)
                                                   A. zenildae (2)
                 P. guineense      Brazilian       A. striata (6)
                                     guava
Oxalidaceae      A. carambola      Star Fruit      A. striata (20)
                                                   A. distincta (1)
Sapotaceae       Pouteria sp. 1    Native abiu     A. leptozona (12)
                 Pouteria sp. 2    Wild abiu       A. serpentina (4)

TABLE 4. NUMBER OF SAMPLES, NUMBER OF FRUITS, HOST WEIGHT,
NUMBER OF TEPHRITIDAE PUPARIA, AND INFESTATION RATE OF
FRUITS COLLECTED IN CUTIAS DO ARAGUARI, ITAUBAL DO
PIRIRIM, FERREIRA GOMES, PRACUUBA, AND TARTARUGAL-ZINHO
IN AMAPA, BRAZIL, FEB 2006 TO AUG 2007.

Hosts                      Samples *                Mass
                                          Fruits    (kg)
                      C       I     %      (n)

A. occidentale        29      5    17.2      438    24.80
A. carambola          51      3     5.9      665    76.34
B. grossularioides    30     28    93.3    1,892    21.16
B. imperialis         32     26    81.3    2,199    32.15
B. crassifolia         7      1    14.3    3,044     6.37
C. utilis              5      2    40.0      163     4.12
E. luschnathiana       3      1    33.3      185     0.44
I. edulis             95     48    50.5      325    63.62
I. fagifolia           8      1    12.5      508     6.02
Inga sp. 1            17     10    58.8      313    24.75
Inga sp. 4             4      4   100.0      213     2.69
Inga sp. 5             1      1   100.0      130     0.97
I. velutina            6      2    33.3      115     2.92
Manihot sp.            3      3   100.0      126     0.23
M. acutiflora          2      1    50.0      225     0.59
O. bacaba             13      4    30.8    8,130    26.24
P. caimito            12      2    16.7      101     7.01
Pouteria sp. 1         2      2   100.0       51    0,175
Pouteria sp. 2         1      1   100.0        2     0.39
P. guajava           255    222    87.1    9,657   425.97
P. guineense           2      2   100.0      145     2.12
S. mombin             55     51    92.7    9,454   126.97
S. purpurea            3      1    33.3       75     0.86

Hosts                Puparia         Infestation rate
                       (n)
                               [I.sub.pp/kg]   [I.sub.pp/f]

A. occidentale           19            0.77           0.04
A. carambola             99            1.30           0.15
B. grossularioides      636           30.06           0.34
B. imperialis         1,533           47.68           0.70
B. crassifolia            7            1.10           0.00
C. utilis               324           78.64           1.99
E. luschnathiana          8           18.18           0.04
I. edulis               538            8.46           1.66
I. fagifolia             10            1.66           0.02
Inga sp. 1              466           18.83           1.49
Inga sp. 4              252           93.68           1.18
Inga sp. 5              117          120.62           0.90
I. velutina             156           53.42           1.36
Manihot sp.              30          130.43           0.24
M. acutiflora            40           67.80           0.18
O. bacaba               110            4.19           0.01
P. caimito               64            9.13           0.63
Pouteria sp. 1           76          434.29           1.49
Pouteria sp. 2            5           12.82           2.50
P. guajava           17,531           41.16           1.82
P. guineense             32           15.09           0.22
S. mombin             2,721           21.43           0.29
S. purpurea              26           30.23           0.35

* C: collected, I: infested, %: percentage of infested samples.

Table 5. Number of parasitoids observed in Anastrepha
species found in fruits collected in Cutias do Araguari, Itau-bal
do Piririm, Ferreira Gomes, Pracuuba, and Tartarugalzinho
in Amapa, Brazil, Feb 2006 to Aug 2007.

                Doryctobracon     Opius x     Asobara       Utetes
                   areolatus      areolatus  anastrephae  anastrephae
                     (n)            (n)          (n)          (n)

A. coronilli         136             0            0            0
A. distincta          7              0            0            0
A. fraterculus        78             0            2            0
A. obliqua            95            15            1            2
A. parishi            2              0            0            0
A. striata           307             3            4            0


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Author:Jesus-Barros, Cristiane R.; Adaime, Ricardo; Oliveira, Manoela N.; Silva, Wilson R.; Costa-Neto, Sal
Publication:Florida Entomologist
Article Type:Report
Geographic Code:3BRAZ
Date:Sep 1, 2012
Words:7160
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