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First record of the association of banana (Musa sp.) and Ceratitis capitata (Widemann, 1824) in Brazil/ Primeiro registro da associacao de banana (Musa sp.) e Ceratitis capitata (Widemann,1824) no Brasil.

Brazil stands out as the fourth world's largest banana producer and largest consumer, with production of approximately 7 million tons in 2017, representing 6% of the world production (DOSSA; FUCHS, 2017). Bahia is the second largest banana producer state, with production of 802,000 tons in 2018, occupying an area of 84,000 ha (LSPA, 2018).

Several phytosanitary problems can lead to banana production and post-harvest losses, represented by some species of insects and mites, and mainly by phytopathogenic microorganisms (LICHTERBERG; LICHTERBERG, 2011). Unlike many other economically important fruit species, fruit flies (Diptera: Tephritidae) are not currently considered as insects with potential to reach banana crop pest status or to present quarantine importance when it comes to banana exports. However, the concern about the possible quarantine importance of the Mediterranean fruit fly, Ceratitis capitata (Wiedemann, 1824) on banana exports is not recent. According to Back and Pemberton (1916), bananas (Musa cavendishii L.) produced in the Hawaiian Islands for export were monitored for a period of three years at the beginning of the 20th century, and no fruit infestation was observed. Fruits of other varieties "Brazilian" Musa acuminata (Hybrid AAB), "Valery" (=Taiwan) M. acuminata (AAA Robusta) and "William's" M. acuminata (AAA 'Giant Cavendish') were not confirmed as natural C. capitata hosts in Hawaii (ARMSTRONG, 1983). In Hawaii, Krainacker et al. (1987) confirmed the development of C. capitata in thirty hosts under laboratory conditions, including banana (M. acuminata). In Brazil, Raga et al. (2011) observed four Tephritoidea puparia in banana samples (Musa paradisiaca L.), variety Prata, collected in Sao Paulo, but all of them non-viable, preventing identification of associated fly species.

Since its introduction in Brazil in 1901, C. capitata has expanded its geographic distribution and adapted to the most diverse host fruits and edaphoclimatic conditions, reinforcing its characteristic of generalist and of high ecological plasticity. Current data reveal that 96 plant species have already been registered as C. capitata hosts (ZUCCHI; MORAES, 2012). Several records of new C. capitata hosts are recent, such as the cactaceae Pereskia bahiensis Gurke, and forage palm, Opuntia ficus indica (L.) Mill, in Bahia (LEITE et al., 2017).

Considering the importance of banana farming in Bahia and Brazil, as well as the possibilities of expanding the export of fresh fruits, it was hypothesized that banana fruits are hosts of fruit flies and, therefore, contribute to the maintenance of tefritid populations in fruit growing regions, being able to assume pest status. The aim of the present work was to increase the knowledge about interactions between fruit flies and their hosts, with an emphasis on banana, aiming at the management of these insects.

The selection of sampling points was performed adapting the concept of landscape epidemiology (BERGAMIN FILHO et al., 2016) for fruit flies. This concept considers factors that contribute to the spatial dispersion of organisms, particularly landscape characteristics that increase the risk of occurrence of a particular pest. Thus, fruit sampling were carried out in nine properties of fruit growing regions of the Submedio Sao Francisco valley, inserted in the irrigation projects of Salitre, Manicoba and Mandacaru, in the municipality of Juazeiro, Bahia, Brazil. Properties were composed of banana (Musa sp.) plantations close to acerola (Malpighia emarginata DC), guava (Psidium guajava L.), mango (Mangifera indica L.) and papaya (Carica papaya L.) orchards or consortia of banana with guava or mango (Table 1). Ten samplings were carried out, one in November 2017 and the other in March 2018, with 1.5 to 4.0 kg of banana fruits being collected from each orchard at the maturation scales of Von Loesecke: 3 (more green than yellow), 5 (yellow with green tip) and 6 (yellow) (PBMH; PIF, 2006), according to the availability. Fruits were duly identified, including the cultivar, date of collection and geographical coordinates (Table 1), packed in plastic trays and transported to the Laboratory of Fruit Flies--State University of Southwestern Bahia, UESB, Vitoria da Conquista, BA. In the laboratory, samples were counted and their mass was determined. Then, fruits were packed in plastic trays containing vermiculite to obtain larvae and / or puparia of fruit flies. Trays remained covered with voile fabric to avoid contamination and after 15 days, they were searched for the location of puparia, which were transferred to plastic containers containing vermiculite for the emergence of fruit fly adults. Infestation rates in puparia kg [fruit.sup.-1] and puparia [fruit.sup.-1] were calculated (Table 1).

A total of 251 banana fruits were collected, with total mass of23,765.4 g. Fruit fly infestation was confirmed in banana variety Prata Ana (Musa sp.) at maturation scale 5 from Lots 286 from Santa Clara farm (collected in November 2017) and 301 from Salitre lot, obtaining 172 and 5 puparia, respectively, totaling 177 puparia. Of these, 106 C. capitata adults emerged, with total pupal viability of 59.89%, varying from 59.30% (Santa Clara) to 80.0% (Salitre). The highest infestation rates occurred in fruits from Santa Clara farm, reaching 146.08 puparia kg of [fruit.sup.-1] and 9.56 puparia [fruit.sup.-1] (Table 1).

Data confirm the hypothesis that banana fruits with predominantly yellow coloration (yellow with green tip--scale 5) can act as C. capitata hosts. Banana is harvested before reaching scale 5; however, the inadequate harvest management, considered the most delicate operation of the fruit production activity, can result in the permanence of fruits of different ages in orchards and, therefore, of different maturation stages. The maintenance of fruits at maturation scales 5 (yellow with green tip), 6 (yellow) and 7 (yellow with brown areas), i.e., those that have exceeded the harvesting point, should be avoided in order to reduce the risks of maintenance of C. capitata populations in the orchard. The infestation symptoms of banana at maturation scale 5 were characterized by blackened spots in puncture sites. However, little is known about the fruit maturation stage preferred for oviposition and that at the same time allows the larval development of flies for the main cultivars planted in Brazil. According to Armstrong (1983), based on works conducted in Hawaii, USA, more mature bananas (stages 3 to 6) of the "Brazilian", "Valery" and "William's" varieties are preferred for oviposition by C. capitata, with no infestation occurring at initial stages (1 and 2), considered green. Suberization of the bark at the puncture site and the release of latex around the eggs were pointed out by the author as the main causes of egg infeasibility and mortality of first-instar larvae. No similar data for varieties cultivated in Brazil were found in the available literature.

In Bahia, there are currently 12 banana production regions, with total of 2,836 Production Units (PUs), distributed in all regions of the state, and Nanica (AAA), Prata (AAB), Terra (AAB) and Maca (AAB) cultivars stand out as the most important (ADAB, 2018). There is a need to expand larval monitoring to other banana production regions and units, covering different varieties, soil and climatic conditions and associated landscapes.

Data corroborate recent studies on the great capacity of C. capitata adaptation to the most varied native and exotic hosts (ARAUJO et al., 2016; CUSTODIO et al., 2016; LEITE et al., 2017; NEUTZLING et al., 2016). This species is classified as a successful generalist frugivore due to its capacity to compensate for a host characteristic that tends to decrease the population growth rate (r) with another that tends to increase it, resulting in high growth rate (KRAINACKER et al., 1987).

Considering the general infestation index of 7.45 puparia kg [fruit.sup.-1], banana would not fit as primary C. capitata host, since the minimum limit of 30 puparia kg [fruit.sup.-1] can be used to consider the host as primary (ARAUJO, 2002). However, the infestation observed in the first sample from Santa Clara farm (146.08 puparia kg [fruit.sup.-1]) was high and may indicate higher pest pressure than the other collection points, due to the presence of hosts in the vicinity, like mango orchards in production.

The association between banana and C. capitata was recorded for the first time in Brazil.

DOI: http://dx.doi.org/10.1590/0100-29452019091

Acknowledgments

To Zenobia Cardoso dos Santos and Suzany Aguiar Leite, from the Graduate Program in Agronomy (Plant Technology), State University of Southwestern Bahia, for the collaboration in the processing of samples.

References

ADAB--Agencia Estadual de Defesa Agropecuaria da Bahia. Relatorio de unidades de producao por municipios. Salvador, 2018. 762 p.

ARAUJO, EL. Dipteros frugivoros (Tephritidae e Lonchaeidae) na Regiao de Mossoro/Assu, Estado do Rio Grande do Norte. 2002. 112f. Tese (Doutorado em Agronomia)--Escola Superior de Agricultura Luiz de Queiroz, Universidade de Sao Paulo, Piracicaba, 2002.

ARAUJO, M.R.; LEMOS, W.P.; SILVA, L.C., FRANCA; L.P.N.; ADAIME, R. New host records for Ceratitis capitata (Diptera:Tephritidae) in the state of Para, Brazil. Florida Entomologist, Lutz, v.99, n.2, p.327-328, 2016.

ARMSTRONG, J. W. Infestation biology of three fruit fly (Diptera: Tephritidae)s on 'Brazilian,' 'Valery,' and 'William's' cultivars of banana in Hawai. Journal of Economic Entomology, Oxford, v.76, p.539-543, 1983.

BACK, E.A.; PEMBERTON, C.E. Banana as a host fruit of the Mediterranean fruit fly. Journal of Agricultural Research, Washington, v.5, n.17, p. 793-812, 1916.

BERGAMIN FILHO, A.; INOUE-NAGATA, A.K.; BASSANEZI, R.B.; BELASQUE Jr., J.; AMORIM, L.; MACEDO, M.A.; BARBOSA, J.C.; WILLOCQUET, L.; SAVARY, S. The importance of primary inoculum and area-wide management to crop health and food security. Food Security, New York, v.8, p.221-238, 2016.

CUSTODIO, AC.; DONNARUMA, T.L.; SOUZAFILHO, M.F.; LOUZEIRO, L.R.F.; RAGA, A. Novo registro de hospedeiro associado a Ceratitis capitata (Diptera: Tephritidae). Biologico, Sao Paulo, v.78, n.2, p.141, 2016.

DOSSA, D.; FUCHS, F. Banana: producao, mercado e precos na CEASA-PR. Curitiba: CEASA, 2017. 3p. (Boletim Tecnico, 6).

KRAINACKER, D.A.; CAREY, J.R.; VARGAS; R.I. Effect of larval host on life history traits of the mediterranean fruit fly, Ceratitis capitata. Oecologia, Berlin, v.73, p.583-590, 1987.

LEITE, S.A.; CASTELLANI, M.A.; RIBEIRO, A.E.L.; COSTA, D.R.; BITTENCOURT, M.A.L.; MOREIRA, A.A. Fruit flies and their parasitoids in the fruit growing region of Livramento de Nossa Senhora, Bahia, with records of unprecedented interactions. Revista Brasileira de Fruticultura, Jaboticabal, v.39, n.4, p.592-602, 2017.

LICHTEMBERG, LA; LICHTEMBERG, P.S.F. Avancos na bananicultura brasileira. Revista Brasileira de Fruticultura, Jaboticabal, v.33, n.1, p.29-36, 2011. Volume especial

LSPA--Levantamento Sistematico da Producao Agricola. Banco de tabelas estatisticas. 2018. Disponivel em: <https://sidra.ibge.gov.br/home/lspa/bahia>. Acesso em: 20 jul. 2018.

NEUTZLING, A.S.; NUNES, A.M.; KRUGER, A.P.; GARCIA, F.R.M. Interacao entre moscas-das-frutas (Diptera: Tephritidae) e a planta hospedeira Sorocea bonplandii. Interciencia, Caracas, v.41, n.10, p.686-690, 2016.

PBMH/PIF--Programa Brasileiro para a Modernizacao da Horticultura & Producao Integrada de Frutas. Normas de classificacao de banana. Sao Paulo: CEAGESP, 2006. 7 p. (Documentos, 29).

RAGA, A.; SOUZA-FILHO, M.F.; MACHADO, R A.; SATO, M.E.; SILOTO, R.C. Host ranges and infestation indices of fruit flies (Tephritidae) and lance flies (Lonchaeidae) in Sao Paulo state, Brazil. Florida Entomologist, Lutz, v.94, n.4, p.787-794, 2011.

ZUCCHI, R.A; MORAES, R.C.B. Fruit flies in Brazil--hosts and parasitoids of the Mediterranean fruit fly. 2012. Disponivel em: <www.lea.esalq.usp.br/ceratitis/>. Acesso em: 15 out. 2018.

Ricardo Falcao de Sa (1), Alessandra da Silva Oliveira (1), Rita de Cassia Costa de Oliveira (2), Jose Carlos Marques dos Santos (3), Aldenise Alves Moreira (4), Maria Aparecida Castellani (4)

Corresponding author: castellani@uesb.edu.br

Received: August 03, 2018

Accepted: October 30, 2018

(1) Master in Agronomy, State Agricultural and Livestock Supervisor, State Agency of Agricultural Defense of Bahia, Salvador-BA, Brazil. Emails: ricardo.sa@adab.ba.gov.br, alessandro.oliveira1@adab.ba.gov.br

(2) Master in Agronomy, State Agricultural and Livestock Supervisor, Coordinator of the ADAB Fruit Flies Control Project, Salvador-BA, Brazil. Email: ritadecassia.oliveira@adab.ba.gov.br

(3) Agricultural Engineer, Agricultural Surveillance Technician, Agricultural Defense Agency of the State of Bahia, Salvador-BA, Brazil. Email:jose.santos4@adab.ba.gov.br

(4) PhD in Agronomy (Plant Protection), Professor at the Graduate Program in Agronomy (Plant Technology), State University of Southwest of Bahia, Vitoria da Conquista-BA, Brazil. Emails: aldenise.moreira@gmail.com; castellani@uesb.edu.br
Table 1. Sampling location of banana fruits (Musa sp.) as a
function of the landscape, total area and banana (ha), fruit
variety and maturation, geographical coordinates, number (no.) and
mass (g) of fruits, puparia and emerged Ceratitis capitata adults
(EA) (no.), pupal viability (PV) (%) and infestation rates (puparia
kg [fruit.sup.-1] and puparia [fruit.sup.-1]). Juazeiro, Bahia,
Brazil, 2018.

Sampling                              Area (ha)
                                                          Variety/
Site              Landscape **     Total     Banana    Maturation ***

Lot 286 Santa      Banana x        147.2       27       Prata Ana/ 5
Clara farm *         Mango
                     Mango
Lot 75 Salitre    Acerola and       6.0        6        Prata Ana/ 3
                     Guava
Lot 32             Banana x         0.1        6         Prata BRS
Manicoba             Mango                              Princesa/ 5
Lot 302              Guava          7.0        7        Prata Ana/ 5
Salitre
Lot 279            Banana x         7.0        7        Prata Ana/ 5
Salitre              Guava
Lot 136              Banana         7.0        7        Prata Ana/ 5
Salitre
Lot 301            Mango and        6.0        6        Prata Ana/ 5
Salitre              Guava
Lot 286 Santa      Banana x        147.2       27       Prata Ana/ 5
Clara farm           Mango
Lot 29             Mango and        4.0        4      Prata Pacovan/ 5
Mandacaru            Guava
Lot 78 Salitre      Acerola         6.0        6        Prata Ana/ 6

TOTAL                  --           --         --            --

Sampling                                        Fruit
                  Geographic                                  Puparia
Site              Coordinates             (no.)      (g)       (no.)

Lot 286 Santa     09[degrees]14" 54"S      18      1,177.4      172
Clara farm*       40[degrees]15" 10"W

Lot 75 Salitre    09[degrees]32" 25"S      24      2,447.0       0
                  40[degrees]36" 56"W
Lot 32            09[degrees]19" 06"S      22      1,661.0       0
Manicoba          40[degrees]17" 48"W
Lot 302           09[degrees]35"33,7"S     28      3,101.0       0
Salitre           40[degrees]35" 27"W
Lot 279           09[degrees]35" 05"S      34      3,890.0       0
Salitre           40[degrees]35" 57"W
Lot 136           09[degrees]34" 17"S      23      1,823.0       0
Salitre           40[degrees]37" 53"W
Lot 301           09[degrees]34" 31"S      24      1,636.0       5
Salitre           40[degrees]36" 15"W
Lot 286 Santa     09[degrees]14" 54"S      36      3,405.0       0
Clara farm        40[degrees]15" 10"W
Lot 29            09[degrees]23" 48"S       4       829.0        0
Mandacaru         40[degrees]24" 14"W
Lot 78 Salitre    9[degrees]32"26" S       38      3,796.0       0
                  40[degrees]37"9.1"W

TOTAL             --                       251    23,765.40     177

Sampling                          Infestation Rates
                   EA      PV
Site              (no.)    (%)     puparia kg         puparia
                                  [fruit.sup.-1]   [fruit.sup.-1]

Lot 286 Santa      102    59.30       146.08            9.56
Clara farm*

Lot 75 Salitre      0      --           --               --

Lot 32              0      --           --               --
Manicoba
Lot 302             0      --           --               --
Salitre
Lot 279             0      --           --               --
Salitre
Lot 136             0      --           --               --
Salitre
Lot 301             4     80.00        3.06             0.17
Salitre
Lot 286 Santa       0      --           --               --
Clara farm
Lot 29              0      --           --               --
Mandacaru
Lot 78 Salitre      0      --           --               --

TOTAL              106    59.89        7.45             0.70

* Samples were collected in November 2017. The other samples were
collected in March 2018. ** Data in column indicate banana
cultivations in Consortia (Banana x Mango, Banana x Guava) or close
to other fruit trees (Acerola, Guava and Mango). Maturation:
3--more green than yellow, 5--yellow with green tip and 6--yellow
(PBMW; PIF, 2006).
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Title Annotation:Plant Protection
Author:de Sa, Ricardo Falcao; Oliveira, Alessandra da Silva; de Oliveira, Rita de Cassia Costa; dos Santos,
Publication:Revista Brasileira de Fruticultura
Date:Mar 1, 2019
Words:2581
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