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Species of Anastrepha (Diptera: Tephritidae), their host plants, and parasitoids in small fruit production areas in the state of Amapa, Brazil.

Fruit flies (Diptera: Tephritidae) are among the principal pests in agriculture (Malavasi 2009). In addition to the direct damage caused by the development of larvae inside the fruits, there are significant monetary losses caused by quarantine restrictions for certain species of fresh fruit destined for export (Carvalho et al. 2000). Among the Tephritidae, the genus Anastrepha Schiner, endemic to the Neotropical region, has greatest economic impact in the Americas. Anastrepha is quite diverse, with 235 species described, and is widely distributed in the American tropical and subtropical regions (Aluja 1994; Uramoto et al. 2008; Uchoa & Nicacio 2010). In Brazil, 120 species have already been reported (Zucchi 2008).

In the Brazilian Amazon, 76 Anastrepha species are known (Adaime et al. 2016). Of these, 5 are considered of economic importance: Anastrepha fraterculus (Wiedemann), Anastrepha obliqua (Macquart), Anastrepha pseudoparallela (Loew), Anastrepha striata Schiner, and Anastrepha zenildae Zucchi (Uramoto & Zucchi 2009; Dutra et al. 2013; Adaime et al. 2016). In Amapa, 37 species of Anastrepha are already documented, making this state the second one in species richness in the Amazon region (Zucchi 2008).

Despite the economic importance of Tephritidae, the association of fruit fly species with host plants has not been established for most of the known species in the Brazilian Amazon (Zucchi et al. 2011a). The identification of the host fruits is essential for the establishment of an adequate and efficient management program for the pest species (Jesus-Barros et al. 2012). From fruit collections, it is possible to determine the rates of fruit infestation by tephritids and the parasitism rates of the tephritids by parasitoids (Silva et al. 2011a). These relationships can also provide information on the life history of fruit fly species because the host plant, together with temperature, humidity and natural enemies, can affect larval development, adult fecundity, and survival rate. In addition, the understanding of these relationships provides information on the structure of the fruit fly community in the Brazilian Amazon, because the host plant may have a direct effect on the distribution and abundance of Anastrepha species. It is worth noting that tephritids show different degrees of specialization on species of plants native to the American continent, ranging from monophagy to polyphagy (Duyck et al. 2004; Aluja & Mangan 2008; Malavasi 2009; Hafsi et al. 2016).

Fruit production areas in the Brazilian Amazon, especially in the state of Amapa, are mostly characterized by the use of agroforestry systems and urban and rural backyards usually surrounded by native vegetation. This design can favor infestation by fruit flies because there are about 200 fruit species in the Brazilian Amazon, of which half are native and have the potential to host tephritid species. In addition, the availability of cultivated fruits, together with the high diversity of native plant species that fruit throughout the year, may allow the succession of hosts and the maintenance of fruit fly populations (Silva & Ronchi-Teles 2000).

Host availability is one of the main factors affecting the population dynamics of fruit flies. Jesus-Barros et al. (2012), in a study carried out in the state of Amapa, observed that the highest rates of infestation by Anastrepha were recorded in native fruits of the Amazon region. Lemos et al. (2015), in a study carried out in the southeast region of Brazil, found that the population dynamics of Anastrepha in guava orchards was influenced by the availability of alternative hosts in the areas adjacent to the orchard.

The action of natural enemies is another biotic factor, as well as host availability and phenology, which has a strong influence on the population regulation of tephritid species (Leal et al. 2009; Aluja et al. 2012). In the Neotropical region, the braconid parasitoids are among the principal mortality factors of Anastrepha (Carvalho et al. 2010). Doryctobracon areolatus (Szepligeti) (Hymenoptera: Braconidae) has been shown to be the most abundant and widely distributed parasitoid in Brazil (Jesus-Barros et al. 2012). Nonetheless, natural parasitism in the various fruit producing regions in Brazil is variable because it is influenced by the host plant species, by the host fly, and by the place and time of collection (Ovruski et al. 2000; Bittencourt et al. 2012).

The aim of this research was to identify species of Anastrepha and their host plants and associated parasitoids in fruit production areas of 3 municipalities in the state of Amapa in the Brazilian Amazon.

Materials and Methods

STUDY SITE

We conducted this study on 3 farms located in the municipalities of Mazagao, Porto Grande, and Santana, state of Amapa, Brazil. All 3 properties contained commercial orchards with adjoining areas of native forest.

The area in Mazagao (0.1[degrees]S, 51.25[degrees]W) exhibits native floodplain forest vegetation, which undergoes daily flooding due to tides. Common species include Platymiscium duckei Huber (Fabaceae), Virola surinamensis (Rol.) Warb. (Myristicaceae), Calycophyllum spruceanum (Benth.) Hook. f. ex K. Schum. (Rubiaceae), and Carapa guianensis Aubl. (Meliaceae). The commercial orchard area occupies an area of approximately 10 ha, with cultivated fruit trees including Tahiti lime (Citrus aurantifolia Swingle 'Tahiti'; Rutaceae), passionfruit (Passiflora edulis Sims; Passifloraceae), and soursop (Annona muricata L.; Annonaceae) grown to make fruit concentrate or to be sold fresh.

The area in Porto Grande (0.6[degrees]N, 1.45[degrees]W) exhibits dense forest vegetation with numerous tree species including Protium species (Burseraceae), Caryocar villosum (Aubl.) Pers. (Caryocaraceae), and Dipteryx odorata (Aubl.) Willd. (Fabaceae). The property covers approximatly 100 ha, of which 30% is used for the cultivation of fruit trees, mainly hog plum (Spondias mombin L.; Anacardiaceae), araza (Eugenia stipitata McVaugh; Myrtaceae), and soursop (A. muricata).

The area in Santana (0.03[degrees]S, 51.21[degrees]W) exhibits secondary forest vegetation with Eschweilera tenuifolia Miers (Lecythidaceae), Ficus pertusa L. f. (Moraceae), and Pourouma guianensis Aubl. (Urticaceae) as predominant species. The commercial orchard is approximately 20 ha, and the main species are acerola (Malpighia emarginata DC; Malpighiaceae), guava (Psidium guajava L.; Myrtaceae), and passionfruit (P. edulis).

As classified by Koppen, the climate type at the study sites is Am, characterized as hot and humid with a short dry season in the spring. Rainfall is distributed between 2 well-defined periods: a rainy season (Jan-Jul), which receives about 80% of all annual rainfall in the area, and a dry season (Aug-Dec). Temperatures are high throughout the year, with an annual average of 25 to 27 [degrees]C (low of 22 [degrees]C and high of 34 [degrees]C) (IBGE 2010).

EXPERIMENTAL PROCEDURES

Samples were obtained from fruit crops and adjacent areas of native vegetation. Once a month from Jan to Dec 2012, fruits were collected from various plant species either directly from the plant or by retrieving recently fallen fruit. Samples were transported in stackable plastic crates to the Entomology Laboratory at Embrapa Amapa, where the fruits were weighed on a digital scale. For preparation of the samples, the fruits were processed and individualized as per the sample size criterion established by Silva et al. (2011a): a) 15 units, for small fruits; b) 10 units, for medium-sized fruits; and c) 3 units, for large or elongated fruits. In each sample, each individual fruit was considered as 1 sub-sample.

The collected fruits were placed either individually in tubular, transparent plastic vials (8 x 6 cm DH) with vented lids lined with organza or, in the case of large or elongated fruits, on rectangular plastic trays (33 x 18 x 6 cm LWH) also covered with organza held in place by rubber bands. Both types of containers included a thin layer of sterilized sand as a substrate for pupation.

Every 3 d, the sand was examined, and tephritid puparia were removed with spatulas. The puparia were transferred to transparent plastic vials (8 cm diameter) with vented lids covered with organza and containing a thin layer of moistened vermiculite. The adult insects that emerged were killed, transferred to microcentrifuge tubes containing 70% ethanol, and labeled for subsequent identification.

The insects obtained were identified according to Zucchi et al. (2011b) and Marinho et al. (2011). Wild plant species were identified with identification keys and by comparison with specimens available at the Herbario Amapaense, the herbarium at the Amapa State Institute for Scientific and Technological Research (Macapa, Amapa, Brazil).

The following infestation rates were calculated: 1) percentage of fruits infested = (number of fruits infested / number of fruits collected) x 100; 2) number of puparia per fruit = number of puparia obtained 4 number of infested fruits in the sample.

Results

During the sampling period, 412 fruit samples (4,554 fruits; 323.4 kg) representing 78 plant species (51 native and 27 introduced) were obtained from 32 botanical families (Table 1). Infestation was observed in 107 (26.0%) collected samples, representing 20 plant species in 13 botanical families (Tables 1 and 2). In total, 5,252 puparia were obtained, from which emerged specimens of 11 species of Anastrepha and 5 species of parasitoids (4 Braconidae and 1 Figitidae species; both Hymenoptera). The species of Anastrepha obtained were: Anastrepha antunesi Lima, Anastrepha coronilli Carrejo & Gonzalez, Anastrepha distincta Greene, A. fraterculus, Anastrepha hastata Stone, Anastrephaleptozona Hendel, A. obliqua, Anastrephapickeli Lima, Anastrepha serpentina (Wiedemann), A. striata, and A. zenildae (Table 2).

The plant families Anacardiaceae, Myrtaceae, and Sapotaceae contained the greatest number of hosts of Anastrepha (3 species in each plant family). The plant families Annonaceae, Celastraceae, Euphorbiaceae, Fabaceae, Malpighiaceae, Malvaceae, and Melastomataceae each contained 1 host species (Table 2).

The highest percentages of infested fruits were recorded in Inga edulis Mart. (Fabaceae) (100%), P. guajava (94.4%), and E. stipitata (92.7%). In I. edulis, a high infestation rate was also obtained, as high as 30.6 puparia per fruit (Table 2). No adults emerged from the puparia of Tephritidae that were obtained from fruits of Oenocarpus bacaba Mart. (Arecaceae) and Persea americana Mill. (Lauraceae) (Table 2), whereas only the parasitoid Opius bellus Gahan (Hymenoptera: Braconidae) emerged from the puparia ontained from Licania laxiflora Fritsch (Chrysobalanaceae).

The most abundant species of Anastrepha were A. striata (5082), A. obliqua (376 2 ), and A. distincta (3012 ). The great majority of specimens of A. striata (98.2%) were from the infestation in P. guajava, but specimens were also obtained from Pouteriacaimito (Ruiz & Pav.) Radlk. (Sapotaceae) and S. mombin (Table 2). Anastrepha obliqua was recorded in 7 hosts, predominately in E. stipitata (1552) and S. mombin (1212). Anastrepha distincta had the greatest incidence in I. edulis (1842). Anastrepha fraterculus occurred in 2 species of Anacardiaceae, 2 of Myrtaceae and 1 of Fabaceae, being predominant in P. guajava (212 ). Anastrepha serpentina occurred in 2 species of Sapotaceae. Anastrepha antunesi occurred only in S. mombin. The species A. coronilli, A. hastata, A. leptozona, A. pickeli, and A. zenildae occurred in only 1 host each.

The species A. antunesi, A. fraterculus, A. obliqua, and A. striata were recorded in the 3 municipalities studied. Anastrepha distincta and A. hastata in 2 municipalities, and the others in only 1 (Table 3).

The species of parasitoids obtained were: Asobara anastrephae (Muesebeck) (Hymenoptera: Braconidae), D. areolatus, O. bellus, Utetes anastrephae (Viereck) (Hymenoptera: Braconidae), and Aganaspis pelleranoi (Brethes) (Hymenoptera: Figitidae) (Table 2). Opius bellus was the most abundant species; we recovered 101 individuals from Anastrepha infesting 4 host plant species. Doryctobracon areolatus also was obtained from 4 plant species, but in lower abundance (67 specimens) than O. bellus.

Discussion

In this study, it was possible to characterize the host utilization by Anastrepha in areas with high diversity of fruit plants by means of broad sampling (78 plant species) on 3 fruit producing properties in the state of Amapa. Although the diversity of fruit plants available in the area was high, not all species were used as hosts (Table 1). According to Querino et al. (2010) and Hernandez-Ortiz (1993), some species of fruit flies that occur in the Amazon have a high level of specificity in relation to hosts, with a strong preference for certain species or botanical families.

The percentages of infested fruits obtained from I. edulis, P. guajava, and E. stipitata are striking because they are high. However, it is not possible to compare them with most other studies carried out in Amapa because earlier studies were performed with pooled fruit samples, which prevents the estimation of the percentage of infested fruits. On the other hand, in relation to the number of puparia per fruit, the 3 species showed values similar to those already reported in Amapa (Silva et al. 2011b).

All recorded Anastrepha species had already been reported from the state of Amapa (Deus & Adaime 2013). In the present study, all 16 P. guajava samples collected were infested by A. striata (94.4% of the fruits). This close association of A. striata with P. guajava has been well documented in Amapa (Silva et al. 2011b) and elsewhere in the Brazilian Amazon (Silva et al. 2011c). It is a species widely distributed in Amapa, where 25 hosts (16 families) have already been registered (Silva et al. 2011b).

Anastrepha obliqua was obtained from 7 hosts, especially E. stipitata (41.1% of specimens) and S. mombin (32.6% of specimens). This species was also recorded from 4 other hosts, among them Quararibea guianensis Aubl. (Malvaceae). Infestation of Q. guianensis by an Anastrepha species has not previously been recorded.

Anastrepha distincta was the predominate fly infesting I. edulis (99.3% of the specimens), its main host in Amapa (Silva et al. 2011b). The species was also reared from A. muricata, which is a new association for Brazil.

Anastrepha fraterculus was recorded in 5 hosts, with 55.3% of its specimens being from P. guajava. The species is widely distributed in Amapa, although the population density is low (Deus & Adaime 2013).

Anastrepha antunesi was obtained only from S. mombin, a species with which it is frequently associated (Deus & Adaime 2013). In general, A. antunesi and A. obliqua are obtained from S. mombin fruits. Nascimento et al. (2015) collected 600 fruits of this plant and evaluated them individually. The authors recorded infestation by fruit flies in 151 fruits (25.2%) and obtained 298 puparia (mean of 1.97 puparia per fruit, with a maximum of 8 puparia per fruit). The simultaneous occurrence of A. obliqua and A. antunesi was recorded in only 2 of the 151 infested fruits (1.3%).

Anastrepha serpentina was obtained from fruits of Manilkara zapota (L.) P. Royen (Sapotaceae) and Pouteria gardneri (Mart. & Miq.) Baehni (Sapotaceae). The occurrence of A. serpentina in P. gardneri is not previosly reported for Brazil. It should be noted that A. serpentina has already been reported in Pouteria gardneriana (A. DC.) Radlk.( Sapotaceae) in the state of Goias (Zucchi 2008), but that plant species does not occur in the Amazon region.

The species A. coronilli, A. hastata, A. pickeli, and A. zenildae were represented by a single specimen each, in hosts already reported to support them (Deus & Adaime 2013). However, A. leptozona was recorded here for the first time in M. zapota in Brazil.

The action of parasitoids on Anastrepha species was also recorded in this study. Of the 179 specimens obtained, 56.4% were O. bellus, 38.0% D. areolatus, 3.9% A. anastrephae, 1.1% A. pelleranoi, and 0.6% U. anastrephae (Table 2). Together, O. bellus and D. areolatus accounted for 94.4% of the total specimens obtained. Due to their abundance, they are the species with the greatest potential to control the population of fruit flies under the conditions in Amapa (Deus & Adaime 2013). Opius bellus and D. areolatus occurred in the 3 municipalities studied. The other species occurred only in Porto Grande (Table 2). We obtained 81.0% of the parasitoid specimens reported in this study from S. mombin. This plant plays an important role as a natural reservoir of the fruit fly parasitoid populations in Amapa, which deserves further study (Sousa et al. 2016).

Acknowledgments

We thank our colleagues who helped with field work (Carlos Alberto Moraes, Manoel Jonas de Jesus Viana, and Marcelo Luiz de Oliveira) and laboratory work (Maria do Socorro Miranda de Sousa, Luana dos Santos Pinheiro, Francisco Andrew Pacheco, Oziel Barroso Baia, Sarron Feliphe, and Jonh Carlo Reis). We are grateful to Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq) for the Bolsa de Produtividade em Pesquisa (Productivity in Research Grant) awarded to R. Adaime. A. Leyva (USA) helped with English translation and editing of the manuscript.

References Cited

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Lailson do Nascimento Lemos (1), Ezequiel da Gloria de Deus (1), Danilo Baia do Nascimento (1), Cristiane Ramos de Jesus-Barros (2), Salustiano Vilar da Costa-Neto (3), and Ricardo Adaime (1,2,*)

(1) Universidade Federal do Amapa, Programa de Pos-Graduacao em Biodiversidade Tropical, Macapa, Amapa, 68902-280, Brazil; E-mail: l.n.lemos@hotmail.com (L. N. L.), egd_bio@hotmail.com (E. G. D.), danilo.baia@hotmail.com (D. B. N.)

(2) Embrapa Amapa, Macapa, Amapa, 68903-419, Brazil; E-mail: cristiane.jesus@embrapa.br (C. R. J.-B.), ricardo.adaime@embrapa.br (R. A.)

(3) Instituto de Pesquisas Cientificas e Tecnologicas do Amapa, Macapa, Amapa, 68900-000, Brazil; E-mail: salucostaneto@gmail.com (S. V. C.-N.)

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

Please Note: Illustration(s) are not available due to copyright restrictions.
Table 1. Number of fruit samples and individual fruits collected, and
number infested by Anastrepha species, from 3 municipalities in the
state of Amapa, Brazil (Jan-Dec 2012).

Scientific name                     Common name        Family
                                    [Portuguese]

Alibertia edulis (Rich.) A. Rich.   Purui              Rubiaceae
Anacardium occidentale L.           Caju               Anacardiaceae
Annona mucosa Jacq.                 Biriba             Annonaceae
Annona muricata L.                  Graviola           Annonaceae
Artocarpus altilis                  Fruta-pao          Moraceae
(Parkinson) Fosberg
Artocarpus heterophyllus            Jaca               Moraceae
Lam.
Astrocaryum aculeatum               Tucuma             Arecaceae
G. Mey.
Astrocaryum murumuru                Murumuru           Arecaceae
Mart.
Attalea maripa (Aubl.) Mart.        naja               Arecaceae
Attalea phalerata Mart,             Urucuri            Arecaceae
ex Spreng.
Averrhoa carambola L.               Carambola          Oxalidaceae
Bactris gasipaes Kunth              Pupunha            Arecaceae
Bactris maraja Mart.                Maraja             Arecaceae
Bellucia egensis (DC.) Penneys,     Verde-peludo       Melastomataceae
Michelangeli, Judd, Almeda
Bellucia grossularioides (L.)       Goiaba-de-anta     Melastomataceae
Triana
Byrsonima crassifolia (L.)          Muruci             Malpighiaceae
Kunth
Calophyllum brasiliensis            Jacareuba          Calophyllaceae
Cambess.
Capsicum chinense Jacq.             Pimentinha         Solanaceae
Carica papaya L.                    Mamao              Caricaceae
Caryocar glabrum (Aubl.)            Piquiarana         Caryocaraceae
Pers.
Cayaponia ferruginea                Fruta de cutia     Curcubitaceae
Gomes-Klein
Cheiloclinium cognatum              Bacupari           Celastraceae
(Miers) A.C. Sm.
Cissus amapaensis Lombardi          Uva-do-mato        Vitaceae
Citrus aurantifolia Swingle         Limao taiti        Rutaceae
'Tahiti'
Citrus aurantium L.                 Laranja-da-terra   Rutaceae
Citrus latifolia Tanaka             Limao galego       Rutaceae
Citrus limonia Osbeck               Limao-cravo        Rutaceae
Citrus reticulata Blanco            Tangerina          Rutaceae
Citrus sinensis (L.) Osbeck         Laranja            Rutaceae
Coffea arabica L.                   Cafe               Rubiaceae
Combretum laxum Jacq.               Pombeiral          Combretaceae
Conceveiba guianensis Aubl.         Arraieira          Euphorbiaceae
Cucumis anguria L.                  Maxixe             Curcubitaceae
Cucumis sativus L.                  Pepino             Curcubitaceae
Eschweilera tenuifolia              Mata-mata          Lecythidaceae
(O. Berg) Miers [flower bud]
Eugenia stipitata McVaugh           Araca-boi          Myrtaceae
Ficus pertusa L. f.                 Apui               Moraceae
Geissospermum sericeum              Quinarana          Apocynaceae
Miers
Guarea guidonia (L.) Sleumer        Jatauba            Meliaceae
Gustavia augusta L.                 Jenipaparana       Lecythidaceae
Inga edulis Mart.                   Inga-cipo          Fabaceae
Licania laxiflora Fritsch           Anoera             Chrysobalanaceae
Malpighia emarginata DC             Acerola            Malpighiaceae
Mammea americana L.                 Abrico             Clusiaceae
Mangifera indica L.                 Manga comum        Anacardiaceae
Mangifera indica L.                 Manga cavalo       Anacardiaceae
'Tommy Atkins'
Manicaria saccifera Gaertn          Bussu              Arecaceae
Manihot esculenta Crantz            Mandioca           Euphorbiaceae
Manilkara elata                     Macaranduba        Sapotaceae
(AlemAo ex Miq.) Monach
Manilkara zapota (L.) P.            Sapotilha          Sapotaceae
Royen
Metrodorea flavida K. Krause        Laranjinha         Rutaceae
Oenocarpus bacaba Mart.             Bacaba             Arecaceae
Parinari excelsa Sabine             Isqueira           Chrysobalanaceae
Passiflora edulis Sims              Maracuja           Passifloraceae
[flower bud]
Passiflora edulis Sims              Maracuja           Passifloraceae
Persea americana Mill.              Abacate            Lauraceae
Physalis angulata L.                Camapu             Solanaceae
Plinia cauliflora (Mart.)           Jaboti caba        Myrtaceae
Kausel
Pourouma guianensis Aubl.           Mapatirana         Urticaceae
Pouteria caimito (Ruiz & Pav.)      Abiu               Sapotaceae
Radlk.
Pouteria gardneri (Mart.            Aguai-una          Sapotaceae
& Miq.) Baehni
Pouteria macrophylla                Cutite             Sapotaceae
(Lam.) Eyma
Protium heptaphyllum (Aubl.)        Breu vermelho      Burseraceae
Marchand
Protium sp.                         Breu branco        Burseraceae
Psidium guajava L.                  Goiaba             Myrtaceae
Quararibea guianensis Aubl.         Inajarana          Malvaceae
Solanum aethiopicum L.              Jilo               Solanaceae
Solanum paniculatum L.              Jurubeba           Solanaceae
Spondias dulcis Forst.              Cajarana           Anacardiaceae
Spondias mombin L.                  Tapereba           Anacardiaceae
Spondias purpurea L.                Siriguela          Anacardiaceae
Strychnos asperula                  Gogo-de-guariba    Loganiaceae
Sprague & Sandwith
Symphonia globulifera L. f.         Anani              Clusiaceae
Syzygium cumini (L.) Skeels         Jambolao           Myrtaceae
Syzygium jambos (L.) Alston         Jambo vermelho     Myrtaceae
Tapirira obtusa (Benth.)            Fruto de pombo     Anacardiaceae
J. D. Mitch.
Theobroma cacao L.                  Cacau              Malvaceae
Trattinnickia rhoifolia Willd.      Amesclao           Burseraceae
Trichilia rubra C. DC.              Cachua             Meliaceae
Trymatococcus amazonicus            Inhare             Moraceae
Poepp. & Endl.
No. species = 78                                       No. families = 32

                                             Mazagao
Scientific name                     Origin   CS        CF       IS
                                    N/I

Alibertia edulis (Rich.) A. Rich.   N          0           0     0
Anacardium occidentale L.                      1          10     0
Annona mucosa Jacq.                 N          0           0     0
Annona muricata L.                             1           3     0
Artocarpus altilis                             0           0     0
(Parkinson) Fosberg
Artocarpus heterophyllus                       0           0     0
Lam.
Astrocaryum aculeatum               N          0           0     0
G. Mey.
Astrocaryum murumuru                N          6          60     0
Mart.
Attalea maripa (Aubl.) Mart.        N          0           0     0
Attalea phalerata Mart,             N          7          70     0
ex Spreng.
Averrhoa carambola L.                          0           0     0
Bactris gasipaes Kunth                         0           0     0
Bactris maraja Mart.                N          1          15     0
Bellucia egensis (DC.) Penneys,     N          0           0     0
Michelangeli, Judd, Almeda
Bellucia grossularioides (L.)       N          0           0     0
Triana
Byrsonima crassifolia (L.)          N          0           0     0
Kunth
Calophyllum brasiliensis            N          1          15     0
Cambess.
Capsicum chinense Jacq.                        8         120     0
Carica papaya L.                               1           3     0
Caryocar glabrum (Aubl.)            N          0           0     0
Pers.
Cayaponia ferruginea                N          0           0     0
Gomes-Klein
Cheiloclinium cognatum              N          2          30     1
(Miers) A.C. Sm.
Cissus amapaensis Lombardi          N          0           0     0
Citrus aurantifolia Swingle                    9          90     0
'Tahiti'
Citrus aurantium L.                            0           0     0
Citrus latifolia Tanaka                        0           0     0
Citrus limonia Osbeck                          8          80     0
Citrus reticulata Blanco                       2          20     0
Citrus sinensis (L.) Osbeck                    4          40     0
Coffea arabica L.                              0           0     0
Combretum laxum Jacq.               N          0           0     0
Conceveiba guianensis Aubl.         N          0           0     0
Cucumis anguria L.                  N          5          75     0
Cucumis sativus L.                             5          15     0
Eschweilera tenuifolia              N          0           0     0
(O. Berg) Miers [flower bud]
Eugenia stipitata McVaugh           N          0           0     0
Ficus pertusa L. f.                 N          2          30     0
Geissospermum sericeum              N          0           0     0
Miers
Guarea guidonia (L.) Sleumer        N          0           0     0
Gustavia augusta L.                 N          0           0     0
Inga edulis Mart.                   N          2           6     2
Licania laxiflora Fritsch           N          5          45     0
Malpighia emarginata DC                        1          15     1
Mammea americana L.                            0           0     0
Mangifera indica L.                            2          20     0
Mangifera indica L.                            0           0     0
'Tommy Atkins'
Manicaria saccifera Gaertn          N          1          15     0
Manihot esculenta Crantz            N          0           0     0
Manilkara elata                     N          2          30     0
(AlemAo ex Miq.) Monach
Manilkara zapota (L.) P.                       0           0     0
Royen
Metrodorea flavida K. Krause        N          4          60     0
Oenocarpus bacaba Mart.             N          1          15     0
Parinari excelsa Sabine             N          1          15     0
Passiflora edulis Sims              N          5          75     0
[flower bud]
Passiflora edulis Sims              N          8          80     0
Persea americana Mill.                         0           0     0
Physalis angulata L.                           1          15     0
Plinia cauliflora (Mart.)                      0           0     0
Kausel
Pourouma guianensis Aubl.           N          0           0     0
Pouteria caimito (Ruiz & Pav.)      N          1          10     0
Radlk.
Pouteria gardneri (Mart.            N          0           0     0
& Miq.) Baehni
Pouteria macrophylla                N          0           0     0
(Lam.) Eyma
Protium heptaphyllum (Aubl.)        N          1          15     0
Marchand
Protium sp.                         N          1          15     0
Psidium guajava L.                             4          40     4
Quararibea guianensis Aubl.         N          3          45     1
Solanum aethiopicum L.                         3          30     0
Solanum paniculatum L.              N          0           0     0
Spondias dulcis Forst.                         0           0     0
Spondias mombin L.                  N          3          45     3
Spondias purpurea L.                           7         105     4
Strychnos asperula                  N          0           0     0
Sprague & Sandwith
Symphonia globulifera L. f.         N          3          45     0
Syzygium cumini (L.) Skeels                    1          15     0
Syzygium jambos (L.) Alston                    3          30     0
Tapirira obtusa (Benth.)            N          0           0     0
J. D. Mitch.
Theobroma cacao L.                             1           3     0
Trattinnickia rhoifolia Willd.      N          0           0     0
Trichilia rubra C. DC.              N          1          15     0
Trymatococcus amazonicus            N          1          15     0
Poepp. & Endl.
No. species = 78                             129       1,495    17

                                          Porto Grande           Santana
Scientific name                     IF    CS    CF      IS  IF   CS

Alibertia edulis (Rich.) A. Rich.     0     2      30    0    0    0
Anacardium occidentale L.             0     0       0    0    0    2
Annona mucosa Jacq.                   0     3       9    0    0    0
Annona muricata L.                    0     4      12    0    0    2
Artocarpus altilis                    0     4      12    0    0    0
(Parkinson) Fosberg
Artocarpus heterophyllus              0     2       6    0    0    3
Lam.
Astrocaryum aculeatum                 0     0       0    0    0    1
G. Mey.
Astrocaryum murumuru                  0     0       0    0    0    0
Mart.
Attalea maripa (Aubl.) Mart.          0     1      15    0    0    0
Attalea phalerata Mart,               0     0       0    0    0    0
ex Spreng.
Averrhoa carambola L.                 0     9      90    0    0    0
Bactris gasipaes Kunth                0     2      30    0    0    0
Bactris maraja Mart.                  0     0       0    0    0    0
Bellucia egensis (DC.) Penneys,       0     3      45    0    0    4
Michelangeli, Judd, Almeda
Bellucia grossularioides (L.)         0     2      30    2    6    0
Triana
Byrsonima crassifolia (L.)            0     0       0    0    0    5
Kunth
Calophyllum brasiliensis              0     0       0    0    0    0
Cambess.
Capsicum chinense Jacq.               0     1      15    0    0    3
Carica papaya L.                      0     5      15    0    0    6
Caryocar glabrum (Aubl.)              0     1      10    0    0    0
Pers.
Cayaponia ferruginea                  0     0       0    0    0    1
Gomes-Klein
Cheiloclinium cognatum                1     0       0    0    0    3
(Miers) A.C. Sm.
Cissus amapaensis Lombardi            0     0       0    0    0    2
Citrus aurantifolia Swingle           0     0       0    0    0    3
'Tahiti'
Citrus aurantium L.                   0    10     100    0    0    0
Citrus latifolia Tanaka               0     0       0    0    0    2
Citrus limonia Osbeck                 0     8      80    0    0   11
Citrus reticulata Blanco              0     4      40    0    0    5
Citrus sinensis (L.) Osbeck           0     0       0    0    0    1
Coffea arabica L.                     0     0       0    0    0    3
Combretum laxum Jacq.                 0     2      30    0    0    0
Conceveiba guianensis Aubl.           0     0       0    0    0    1
Cucumis anguria L.                    0     1      15    0    0    1
Cucumis sativus L.                    0     0       0    0    0    1
Eschweilera tenuifolia                0     0       0    0    0    4
(O. Berg) Miers [flower bud]
Eugenia stipitata McVaugh             0    11     110   11  102    0
Ficus pertusa L. f.                   0     2      30    0    0    1
Geissospermum sericeum                0     2      20    0    0    0
Miers
Guarea guidonia (L.) Sleumer          0     1      15    0    0    0
Gustavia augusta L.                   0     0       0    0    0    1
Inga edulis Mart.                     6     0       0    0    0    5
Licania laxiflora Fritsch             0     0       0    0    0    1
Malpighia emarginata DC               4     4      60    4   15    9
Mammea americana L.                   0     3      30    0    0    0
Mangifera indica L.                   0     1      10    0    0    2
Mangifera indica L.                   0     7      21    0    0    0
'Tommy Atkins'
Manicaria saccifera Gaertn            0     0       0    0    0    0
Manihot esculenta Crantz              0     1      15    1    1    1
Manilkara elata                       0     0       0    0    0    0
(AlemAo ex Miq.) Monach
Manilkara zapota (L.) P.              0    12     120    6   38    0
Royen
Metrodorea flavida K. Krause          0     0       0    0    0    0
Oenocarpus bacaba Mart.               0     1      15    0    0    6
Parinari excelsa Sabine               0     0       0    0    0    0
Passiflora edulis Sims                0     0       0    0    0    3
[flower bud]
Passiflora edulis Sims                0     0       0    0    0    2
Persea americana Mill.                0     4      12    0    0    4
Physalis angulata L.                  0     0       0    0    0    0
Plinia cauliflora (Mart.)             0     1      15    1    6    0
Kausel
Pourouma guianensis Aubl.             0     1      15    1    6    0
Pouteria caimito (Ruiz & Pav.)        0     0       0    0    0    1
Radlk.
Pouteria gardneri (Mart.              0     1      15    1    1    0
& Miq.) Baehni
Pouteria macrophylla                  0     4      40    0    0    0
(Lam.) Eyma
Protium heptaphyllum (Aubl.)          0     0       0    0    0    0
Marchand
Protium sp.                           0     1      15    0    0    0
Psidium guajava L.                   33     0       0    0    0   12
Quararibea guianensis Aubl.           2     0       0    0    0    0
Solanum aethiopicum L.                0     0       0    0    0    0
Solanum paniculatum L.                0     1      15    0    0    4
Spondias dulcis Forst.                0    11     110   11    4    0
Spondias mombin L.                   24     6      90    6   77    5
Spondias purpurea L.                 48     9     135    7   99    0
Strychnos asperula                    0     0       0    0    0    1
Sprague & Sandwith
Symphonia globulifera L. f.           0     0       0    0    0    0
Syzygium cumini (L.) Skeels           0     0       0    0    0    1
Syzygium jambos (L.) Alston           0     2      20    0    0    2
Tapirira obtusa (Benth.)              0     0       0    0    0    3
J. D. Mitch.
Theobroma cacao L.                    0     4      12    0    0    0
Trattinnickia rhoifolia Willd.        0     0       0    0    0    1
Trichilia rubra C. DC.                0     0       0    0    0    0
Trymatococcus amazonicus              0     0       0    0    0    0
Poepp. & Endl.
No. species = 78                    126   154   1,524   51  356  129

                                    Santana
Scientific name                     CF      IS   IF

Alibertia edulis (Rich.) A. Rich.       0    0     0
Anacardium occidentale L.              20    0     0
Annona mucosa Jacq.                     0    0     0
Annona muricata L.                      6    1     1
Artocarpus altilis                      0    0     0
(Parkinson) Fosberg
Artocarpus heterophyllus                9    0     0
Lam.
Astrocaryum aculeatum                  15    0     0
G. Mey.
Astrocaryum murumuru                    0    0     0
Mart.
Attalea maripa (Aubl.) Mart.            0    0     0
Attalea phalerata Mart,                 0    0     0
ex Spreng.
Averrhoa carambola L.                   0    0     0
Bactris gasipaes Kunth                  0    0     0
Bactris maraja Mart.                    0    0     0
Bellucia egensis (DC.) Penneys,        60    0     0
Michelangeli, Judd, Almeda
Bellucia grossularioides (L.)           0    0     0
Triana
Byrsonima crassifolia (L.)             75    0     0
Kunth
Calophyllum brasiliensis                0    0     0
Cambess.
Capsicum chinense Jacq.                45    0     0
Carica papaya L.                       90    0     0
Caryocar glabrum (Aubl.)                0    0     0
Pers.
Cayaponia ferruginea                   15    0     0
Gomes-Klein
Cheiloclinium cognatum                 45    1     1
(Miers) A.C. Sm.
Cissus amapaensis Lombardi             30    0     0
Citrus aurantifolia Swingle            30    0     0
'Tahiti'
Citrus aurantium L.                     0    0     0
Citrus latifolia Tanaka                20    0     0
Citrus limonia Osbeck                 110    0     0
Citrus reticulata Blanco               50    0     0
Citrus sinensis (L.) Osbeck            10    0     0
Coffea arabica L.                      45    0     0
Combretum laxum Jacq.                   0    0     0
Conceveiba guianensis Aubl.            15    0     0
Cucumis anguria L.                     15    0     0
Cucumis sativus L.                      3    0     0
Eschweilera tenuifolia                 60    0     0
(O. Berg) Miers [flower bud]
Eugenia stipitata McVaugh               0    0     0
Ficus pertusa L. f.                    15    0     0
Geissospermum sericeum                  0    0     0
Miers
Guarea guidonia (L.) Sleumer            0    0     0
Gustavia augusta L.                    10    0     0
Inga edulis Mart.                      15    3    15
Licania laxiflora Fritsch              15    1     1
Malpighia emarginata DC               135    9    80
Mammea americana L.                     0    0     0
Mangifera indica L.                    20    0     0
Mangifera indica L.                     0    0     0
'Tommy Atkins'
Manicaria saccifera Gaertn              0    0     0
Manihot esculenta Crantz               15    0     0
Manilkara elata                         0    0     0
(AlemAo ex Miq.) Monach
Manilkara zapota (L.) P.                0    0     0
Royen
Metrodorea flavida K. Krause            0    0     0
Oenocarpus bacaba Mart.                90    1     1
Parinari excelsa Sabine                 0    0     0
Passiflora edulis Sims                 45    0     0
[flower bud]
Passiflora edulis Sims                 20    0     0
Persea americana Mill.                 12    1     1
Physalis angulata L.                    0    0     0
Plinia cauliflora (Mart.)               0    0     0
Kausel
Pourouma guianensis Aubl.               0    0     0
Pouteria caimito (Ruiz & Pav.)         10    1     2
Radlk.
Pouteria gardneri (Mart.                0    0     0
& Miq.) Baehni
Pouteria macrophylla                    0    0     0
(Lam.) Eyma
Protium heptaphyllum (Aubl.)            0    0     0
Marchand
Protium sp.                             0    0     0
Psidium guajava L.                    120   12   118
Quararibea guianensis Aubl.             0    0     0
Solanum aethiopicum L.                  0    0     0
Solanum paniculatum L.                 60    0     0
Spondias dulcis Forst.                  0    0     0
Spondias mombin L.                     75    5    43
Spondias purpurea L.                    0    0     0
Strychnos asperula                     15    0     0
Sprague & Sandwith
Symphonia globulifera L. f.             0    0     0
Syzygium cumini (L.) Skeels            15    0     0
Syzygium jambos (L.) Alston            20    0     0
Tapirira obtusa (Benth.)               45    0     0
J. D. Mitch.
Theobroma cacao L.                      0    0     0
Trattinnickia rhoifolia Willd.         15    0     0
Trichilia rubra C. DC.                  0    0     0
Trymatococcus amazonicus                0    0     0
Poepp. & Endl.
No. species = 78                    1,535   39   296

N = Native; I = Introduced; CS = collected samples; CF = collected
fruits; IS = infested samples; IF = infested fruits.

Table 2. Species of Anastrepha, host plants, and associated parasitoids
in 3 municipalities in the state of Amapa, Brazil (Jan-Dec 2012).

                                    Infestation (b)   Anastrepha species
                                                      (c) and parasitoid
                                                      species (d)
FAMILY                    Puparia
Species (a)                 (n)     % Fl     P/F      Mazagao (e)

ANACARDIACEAE
  Spondias dulcis (*)          45      4.0    11.3    --
  Spondias mombin (*)         918     60.0     6.4    Ao(9 [male]),
                                                      Aa(2 [male]),
                                                      11 [male] +
                                                      Ob(12), Da(7)
  Spondias purpurea (*)       243     61.3     1.7    Ao(4 [male]),
                                                      2 [male]
ANNONACEAE
  Annona muricata (*)           4      4.8     4      --
ARECACEAE
  Oenocarpus bacaba (**)        1      0,8     1      --
CELASTRACEAE
  Cheiloclinium                16      2.7     8      1 [male]
  cognatum (**)
CHRYSOBALANACEAE
  Licania laxiflora (**)        2      1.7     2      --
EUPHORBIACEAE
  Manihot esculenta (*)         1      3.3     1      --
FABACEAE
  Inga edulis (*)             643    100      30.6    Ad(184 [male]),
                                                      76 [male]
LAURACEAE
  Persea americana (*)          1      4.2       1    --
MALPIGHIACEAE
  Malpighia                    60     47.1     0.6    --
  emarginata (*)
MALVACEAE
  Quararibea                   11      4.4     5.5    Ao(5 [male])
  guianensis (**)
MELASTOMATACEAE
  Bellucia                     13     20.0     2.2    --
  grossularioides (**)
MYRTACEAE
  Eugenia stipitata (*)       885     92.7     8.7    --

  Plinia cauliflora (*)        15     40.0     2.5    --
  Psidium guajava (*)       2,242     94.4    14.8    Ast(45 [male]),
                                                      Af(3 [male]),
                                                      51 [male]

SAPOTACEAE
  Manilkara zapota (*)         86   31,7     2,3      --

  Pouteria caimito (*)         18   50,0     1,8      --
  Pouteria                      3    6,7       3      --
  gardneri (**)

                          Anastrepha species
                          (c) and parasitoid
                          species (d)
FAMILY
Species (a)               Porto Grande (e)               Santana (e)

ANACARDIACEAE
  Spondias dulcis (*)     Ao(7 [male]), 5 [male]         --
  Spondias mombin (*)     Ao(99 [male]), Aa(20 [male]),  Ao(13 [male]),
                          Af(1 [male]), Ast(1 [male]),   Aa(6 [male]),
                          96 [male] + Ob(60), Da(16),    18 [male] +
                          Asa(7), Agp(2), Ua(1)          Ob(22), Da(18)
  Spondias purpurea (*)   Ao(69 [male]), Af(4 [male]),   --
                          80 [male] + Da(5), Ob(4)
ANNONACEAE
  Annona muricata (*)     --                             Ad(1)
ARECACEAE
  Oenocarpus bacaba (**)  --                             0
CELASTRACEAE
  Cheiloclinium           --                             Ah(1 [male]),
  cognatum (**)                                          2 [male]
CHRYSOBALANACEAE
  Licania laxiflora (**)  --                             Ob(2)
EUPHORBIACEAE
  Manihot esculenta (*)   Ap(1)                          --
FABACEAE
  Inga edulis (*)         --                             Ad(115 [male]),
                                                         Af(2 [male]),
                                                         38 [male]
LAURACEAE
  Persea americana (*)    --                             0
MALPIGHIACEAE
  Malpighia               Ao(3 [male]), 1 [male]         Ao(5 [male]),
  emarginata (*)                                         3 [male]
MALVACEAE
  Quararibea              --                             --
  guianensis (**)
MELASTOMATACEAE
  Bellucia                Ac(1 [male]), 2 [male]         --
  grossularioides (**)
MYRTACEAE
  Eugenia stipitata (*)   Ao(155 [male]),   --
                          Af(10 [male]), 168 [male]
  Plinia cauliflora (*)   Ao(6 [male]), 8 [male]         --
  Psidium guajava (*)     --                             Ast(454 [male])
                                                         , Af(18 [male])
                                                         , Ad(1 [male]),
                                                         Ao(1 [male]),
                                                         Azn(1 [male]),
                                                         595 [male] +
                                                         Da(11), Ob(1)
SAPOTACEAE
  Manilkara zapota (*)    Asp(4 [male]),                 --
                          Alp(1 [male]), 8 [male]        Ast(8 [male]),
                                                         1 [male]
  Pouteria caimito (*)    --                             --
  Pouteria                Asp(1 [male]) + Da(1)
  gardneri (**)

(a) Symbols following species names indicate (**)= native host; (*) =
introduced host.
(b) Infestation calculated as % Fl = percentage of infested fruits; P/F
= puparia per fruit.
(c) Fruit flies = Aa: Anastrepha antunsesi, Ac: Anastrepha coronilli,
Ad: Anastrepha distincta, Af: Anastrepha fraterculus, Ah: Anastrepha
hastata, Alp: Anastrepha leptozona, Ao: Anastrepha obliqua, Ap:
Anastrepha pickeli, Asp: Anastrepha serpentina, Ast: Anastrepha
striata, Am: Anastrepha zenildae. Male flies ([male]) were not
identified to species.
(d) Parasitoids = Agp: Aganaspis pelleranoi, Asa: Asobara anastrephae,
Da: Doryctobracon areolatus, Ob: Opius bellus, Ua: Utetes anastrephae.
(e) A dash (--) indicates that no species was found.

Table 3. Species of Anastrepha and their hosts in 3 municipalities in
the state of Amapa, Brazil (Jan-Dec 2012).

Specie                                   Host
                          Family              Species

Anastrepha antunesi       Anacardiaceae       Spondias mombin
Anastrepha coronilli      Melastomataceae     Bellucia grossularioides
Anastrepha distincta      Annonaceae          Annona muricata (a)
                          Fabaceae            Inga edulis
                          Myrtaceae           Psidium guajava
Anastrepha fraterculus    Anacardiaceae       Spondias mombin
                          Anacardiaceae       Spondias purpurea
                          Fabaceae            Inga edulis
                          Myrtaceae           Eugenia stipitata
                          Myrtaceae           Psidium guajava
Anastrepha hastata        Celastraceae        Cheiloclinium cognatum
Anastrepha leptozona      Sapotaceae          Manilkara zapota (a)
Anastrepha obliqua        Anacardiaceae       Spondias dulcis
                          Anacardiaceae       Spondias mombin
                          Anacardiaceae       Spondias purpurea
                          Malpighiaceae       Malpighia emarginata
                          Malvaceae           Quararibea guianensis (a)
                          Myrtaceae           Eugenia stipitata
                          Myrtaceae           Plinia cauliflora
                          Myrtaceae           Psidium guajava
Anastrepha pickeli        Euphorbiaceae       Manihot esculenta
Anastrepha serpentina     Sapotaceae          Manilkara zapota
                          Sapotaceae          Pouteria gardneri (a)
Anastrepha striata        Anacardiaceae       Spondias mombin
                          Myrtaceae           Psidium guajava
                          Sapotaceae          Pouteria caimito
Anastrepha zenildae       Myrtaceae           Psidium guajava

Specie                             Municipality
                          Mazagao   Porto Grande   Santana

Anastrepha antunesi       x         x              x
Anastrepha coronilli                x
Anastrepha distincta                               x
                          x                        x
                                                   x
Anastrepha fraterculus              x
                                    x
                                                   x
                                    x
                          x                        x
Anastrepha hastata        x                        x
Anastrepha leptozona                x
Anastrepha obliqua                  x
                          x         x              x
                          x         x
                                    x              x
                          x
                                    x
                                    x
                                                   x
Anastrepha pickeli                  x
Anastrepha serpentina               x
                                    x
Anastrepha striata                  x
                          x                        x
                                                   x
Anastrepha zenildae                                x

(a) Unpublished association for Brazil (Anastrepha and host).
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Article Details
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Author:Lemos, Lailson do Nascimento; de Deus, Ezequiel da Gloria; do Nascimento, Danilo Baia; de Jesus-Barr
Publication:Florida Entomologist
Article Type:Report
Geographic Code:3BRAZ
Date:Jun 1, 2017
Words:7145
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