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New records of thrips species on mango and natural enemies associated

Novos registros de espécies de tripes em mangueira e inimigos naturais associados

Abstract

The mango tree (Mangifera indica L.), native to Asia, is expanding in Brazil. However, research related to phytophagous organisms and natural enemies associated with this fruit are scarce in the country. The aim of this work was to report new species of thrips-pest and natural enemies associated with mango tree inflorescence. The work was carried out in a Tommy Atkins mango orchard located in the municipality of Jardinópolis, São Paulo, Brazil. The arthropods found in malformed inflorescences were collected and identified. Frankliniella gemina Bagnall, Frankliniella distinguenda Bagnall (Thysanoptera: Thripidae) and Haplothrips gowdeyi (Franklin) (Thysanoptera: Phlaeothripidae) thrips-pest species were recorded for the first time associated with inflorescence in mango orchards. The predators were collected in association with the phytophagous thrips.

Index terms
Thysanoptera; pest; predators

Resumo

A mangueira (Mangifera indica L.), planta nativa da Ásia, encontra-se em expansão no Brasil. Entretanto, pesquisas relacionadas aos organismos fitófagos e aos inimigos naturais associados a essa frutífera são escassos no País. O objetivo deste trabalho foi relatar novas espécies de tripes e aos inimigos naturais associados às inflorescências de mangueira. O trabalho foi realizado em um pomar de mangueiras Tommy Atkins, localizado no município de Jardinópolis, São Paulo, Brasil. Os artrópodes encontrados nas inflorescências malformadas foram coletados e identificados. As espécies Frankliniella geminaBagnall, Frankliniella distinguenda Bagnall (Thysanoptera: Thripidae) e Haplothrips gowdeyi (Franklin) (Thysanóptera: Phlaeothripidae) foram registradas pela primeira vez associadas à inflorescência de mangueira. Os predadores foram coletados em associação com os tripes fitófagos.

Termos para indexação
Thysanoptera; praga; predadores

Introduction

Mango tree (Mangifera indica L.) (Anarcadiaceae) is native to Asia. Of pleasant aroma and flavor, fruits are consumed in natura or processed in the manufacture of sweets, juices or ice creams (PITCHAON, 2011 PITCHAON, M. Antioxidant capacity of extracts and fractions from mango (Mangifera indica Linn.) seed kernels. International Food Research Journal, Serdang, v.18, n.1, p.523-528, 2011. ). Brazil was the first country in the Americas to grow this plant, firstly introduced by the Portuguese in Rio de Janeiro in the 16th century, expanding to the whole country.

Brazil currently stands out as the seventh largest mango producers, and most of the production is concentrated in the states of Bahia (23%), Pernambuco (23%) and São Paulo (18%) (MAIA et al., 2016 MAIA, M.C.C.; ARAÚJO, L.B.; DIAS, C.T.S.; OLIVEIRA, L.C.; VASCONCELOS, L.F.L.; CARVALHO JÚNIOR, J.E.V.; SIMEÃO, M.; BASTOS, Y.G.M. Seleção de genótipos em uma população de melhoramento de manga rosa usando o método multivariado biplot. Ciência Rural, Santa Maria, v.46, n.10, p.1689-1694, 2016. ; IBGE, 2016 IBGE. Produção agrícola municipal. Rio de Janeiro, 2018, Disponível em: http://www.sidra.ibge.gov.br. Acesso em: 8 maio 2018.
http://www.sidra.ibge.gov.br...
).

In recent years, there has been a great increase in the consumption of mango in the domestic and foreign markets, which has contributed to an increase in the world fruit production. Thus, mango cultivation has gradually assumed a prominent position in the country, considerably increasing the number of planted trees (OLIVEIRA et al., 2002 OLIVEIRA, F.D.C.; COELHO, E.F.; VASCONCELOS, L.F.L.; ARAÚJO, E.C.E. Produção de manga sob diferentes regimes de irrigação, em condições subúmidas. Revista Brasileira de Engenharia Agrícola e Ambiental, Campina Grande,v.6, p.390-396, 2002. ; IBGE, 2016 IBGE. Produção agrícola municipal. Rio de Janeiro, 2018, Disponível em: http://www.sidra.ibge.gov.br. Acesso em: 8 maio 2018.
http://www.sidra.ibge.gov.br...
).

During their development, mango trees can be attacked by various pests, which can affect growth, development and productivity. Among pests, thrips (Thysanoptera) stand out among the most important pests associated with mango trees, attacking leaves, inflorescences and fruits (BARBOSA; PARANHOS, 2005 BARBOSA, F.R.; PARANHOS, B.A.J. Artrópodes-praga associados à cultura da mangueira no Brasil e seu contole. In: MENEZES, E.A.; BARBOSA, F.R. Pragas da mangueira: monitoramento, nível de ação e controle. Petrolina: Embrapa Semi-Árido, 2005. p.17-50. ). The tissues of plants with injuries caused by these organisms have silver coloration that can evolve to ferruginous appearance (PEÑA, 2004 PEÑA, J.E. Integrated pest management and monitoring techniques for mango pests. Acta Horticulturae, Wageningen, v.645, p.51-161, 2004. ). According to BRANDÃO and BOARETTO (2002) BRANDÃO, A.L.S.; BOARETTO, M.A.C. Pragas da mangueira. In: SÃO JOSÉ, A.R. (Org.). O agronegócio manga: produção e mercado. Vitória da Conquista: Universidade Estadual do Sudoeste da Bahia, DFZ, 2002. CD-ROM , both immatures and adults are “scraper-suckers” and can feed on pollen, sap of petals and ovaries of flowers, which cause the wilt of inflorescences and decrease fructification.

Several thrips species have been recorded in mango culture worldwide. In Malaysia, Thrips hawaiiensis (Morgan), Scirtothrips dorsalis (Capuz), Frankliniella schultzei (Trybom) and Megalurothrips usitatus (Bagnall) have been reported (ALIAKBARPOR;, RAWI, 2012 ALIAKBARPOUR, H.; RAWI, C.S.M. The species composition of thrips (Insecta: Thysanoptera) inhabiting mango orchards in Pulau Pinang, Malaysia. Tropical Life Sciences Research, Penang, v.23, n.1, 45–6, 2012. ); in Israel, Frankliniella occidentalis (Pergande) (WYSOKI et al., 1993 WYSOKI, M.; BEN-DOV, Y.; SWIRSKI, E.; IZHAR, Y. The arthropod pests of mango in Israel. Proceeding of the IV International Mango Symposium. Acta Horticulturae, Wageningen, v.341, p.452-466, 1993. ); in India, Thrips palmi Karny, Thrips hawaiensis (Morgan) and Thrips subnudula (Karny) (KRISHNAMOORTHY; VISALAKSHI, 2012 KRISHNAMOORTHY, A.; VISALAKSHI, P.N.G. Record of thrips on mango. Journal of Horticultural Science, Bangalore, v.7. n.1, p.110-111, 2012. ); Frankliniella bispinosa (Morgan) and Frankliniella kelliae Sakimura, in the United States (PEÑA, 1998 PEÑA, J.E.; MOHYUDDIN, A.I.; WYSOKI, M. review of the pest management situation in mango agroecosystems. Phytoparasitica, Rehovot, v.26, n.2, p.129148, 1998. ) and, in Australia, Selenothrips rubrocinctus Giard (PENG; KRISTIAN, 2004). In Brazil, S. rubrocinctus, F. schultzei, Frankliniella gardeniae Moulton and Frankliniella brevicaulis Hood species have been reported (BARBOSA et al., 2005 BARBOSA, F.R.; PARANHOS, B.A.J. Artrópodes-praga associados à cultura da mangueira no Brasil e seu contole. In: MENEZES, E.A.; BARBOSA, F.R. Pragas da mangueira: monitoramento, nível de ação e controle. Petrolina: Embrapa Semi-Árido, 2005. p.17-50. ).

In Brazil, information about thrips and natural enemies associated with this plant is still scarce (BARBOSA et al., 2005 BARBOSA, F.R.; PARANHOS, B.A.J. Artrópodes-praga associados à cultura da mangueira no Brasil e seu contole. In: MENEZES, E.A.; BARBOSA, F.R. Pragas da mangueira: monitoramento, nível de ação e controle. Petrolina: Embrapa Semi-Árido, 2005. p.17-50. ). The knowledge about the organisms that occur in the mango culture is of fundamental importance for the establishment of integrated pest management programs, as it enables the identification of pest insects and natural enemies, and contributes to the understanding of the relationships among species in the agroecosystem (DUARTE et al., 2013 DUARTE, R. T.; GALLI, J. C.; PAZINI, W. C. Levantamento populacional de predadores (Arthropoda) em cultivo orgânico de goiaba (Psidium guajava L.). Revista Agroambiente, Boa Vista, v.7, n.3, p.352-358, 2013. ). Therefore, this study aimed to report the occurrence of thrips species associated with inflorescence malformation in mango trees and their natural enemies.

The study was carried out in a mango orchard (Tommy Atkins cultivar) located at the municipality of Jardinópolis, São Paulo, Brazil (20°55’28”S, 47°55’45”W) in September 2017. The experimental area 1,552 mm annual average length and Dark Red Latosol soil. The climate of the region, according to classification of Köoeppen, is of type Cwa, subtropical, relatively dry in the winter, with rains in the summer. The orchard plants were 30 years old, approximately seven meters high and planted in 14 m x 12 m spacing. Sampling was performed by means of the collection of inflorescences in 30 randomly selected plants. Inflorescences were packed in paper bags and sent to laboratory belonging to the São Paulo State University - Faculty of Agrarian and Veterinary Sciences, Jaboticabal Campus (UNESP / FCAV).

The presence of thrips and natural enemies (mites and insects) in inflorescences was verified using a stereomicroscope. The organisms observed were collected with a single-wire brush. After this initial screening, inflorescences were shaken on white paper to verify the presence of other arthropods. Subsequently, the counting of thrips and other arthropods collected was carried out.

Specimens were later packed in vials containing 70% alcohol.

Thrips and mites found were slide-mounted for identification (MOUND; MARULLO, 1996 MOUND, L.A.; MARULLO, R. The thrips of Central and South America: an introduction (Insecta: Thysanoptera). Memoirs on Entomology International, Gainsvilee, v.6, p.1-488, 1996. ; KRANTZ; WALTER, 2009 KRANTZ, G. W.; WALTER, D. E. A. Manual of acarology. 3rd ed. Lubbock: Texas Tech University Press, 2009. 807 p. ). The other insects were mounted on entomological pins and identified under stereomicroscope.

Our work reports new records of three thrips species for mango in Brazil, namely Frankliniella gemina Bagnall, Frankliniella distinguenda Bagnall and Haplotrips gowdeyi (Franklin) (figure 1). In addition, F. gardeniae species (Table 1) was also found. The average of thrips found per inflorescence was 20 adults and 40 nymphs. In relation to natural enemies, Harmonia axyridis (Pallas), Cycloneda sanguinea (Linnaeus), Hippodamia convergens Guérin-Meneville (Coleoptera: Coccinellidae), Orius insidiosus (Say) (Hemiptera: Anthocoridae), Proctolaelaps bickleyi Bram and Iphiseiodes zuluagai Denmark e Muma (Acari: Phytoseiidae) were found in inflorescences (Table 1).

Figure 1
Thrips species and injuries on Tommy Atkins mango (Mangifera indica) trees in Jardinópolis, São Paulo state, Brazil. A. mango tree inflorescences with initial symptoms of floral malformation; B. highly infested by thrips and black color (advanced symptom) in the same mango orchard; C. Frankliniella distinguenda; D. Frankliniella gardeniae; E. Frankliniella gemina; F. Haplothrips gowdeyi.

Table 1
Thrips and natural enemies associated with floral malformation on Tommy Atkins mango trees. Jardinópolis-SP, Brazil, 2017.

The occurrence of F. gardeniae was reported in citrus, guava, soybean, grape and avocado (HODDLE et al., 2002 HODDLE, M.S.; MORSE, J.G.; PHILLIPS, P.P.; FABER, B.; JETTER, KAREN. Avocado thrips: new challenge for growers. California Agriculture, Los Angeles, v.56, n.3, p.103-107, 2002. ; CAVALLERI et al., 2006 CAVALLERI, A.; ROMANOWSKI, H.P.; REDAELLI, L.R. Thrips species (Insecta, Thysanoptera) inhabiting plants of the Parque Estadual de Itapuã, Rio Grande do Sul, Brazil. Revista Brasileira de Zoologia, Curitiba, v. 23, n. 2, p. 367-374, 2006. ; LIMA et al., 2013a LIMA, E.F.B.; FONTES, L.S.; PINENT, S.M.J.; REIS, A.S.; FREIRE FILHO, F.R.; LOPES, A.C.A. Thrips species (Insecta: Thysanoptera) associated to Cowpea in Piauí, Brazil. Biota Neotropica, Campinas, v.13, n.1, p. 383-386, 2013a. ; MOREIRA et., 2014 MOREIRA, A.N.; OLIVEIRA, V.J.; OLIVEIRA, J.E.M.;SOUZA, G.M.M.; BREDA, M.O. Injuries caused by frankliniella spp. (thysanoptera: thripidae) on seedless grapes. Ciência e Agrotecnologia, Lavras, v.38, n.4, p.328-334, 2014. ). Haplothrips gowdeyi was recorded in nectarine flower, bean, soybean, fava, rice, coffee and watermelon (HICKEL; DUCROQUET 1998 HICKEL, E.R.; DUCROQUET, J.H.J. Tripes associados à floração da nectarina em Santa Catarina. Anais da Sociedade Entomológica do Brasil, Jaboticabal, v.27, n.2, p.307-308, 1998. ; LIMA et al., 2013b LIMA, E.F.B.; MONTEIRO, R.C.; ZUCCHI, R.A. Thrips species (Insecta: Thysanoptera) associated to Fabaceae of agricultural importance in Cerrado and Amazon-Caatinga ecotone from Brazilian Mid-North. Biota Neotropica, Campinas v.13, n.2, p.283-289, 2013b. ; COSTA et al., 2015). Frankliniella gemina has already been reported in rose bush, grape and various ornamental plants (MOREIRA et al., 2014 MOREIRA, A.N.; OLIVEIRA, V.J.; OLIVEIRA, J.E.M.;SOUZA, G.M.M.; BREDA, M.O. Injuries caused by frankliniella spp. (thysanoptera: thripidae) on seedless grapes. Ciência e Agrotecnologia, Lavras, v.38, n.4, p.328-334, 2014. ). On the other hand, the species F. distinguenda is little reported in the literature.

In this mango orchard approximately 88.9% of the inflorescences presented malformation and high density of thrips (Figure 1). This resulted in a strong loss of production. Therefore, our study reports new records of three species of thrips for the mango tree, F. gemina, F. distinguenda and H. gowdeyi, and gathers information for future research, as damage potential and control measures, as well as their interactions with natural enemies.

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  • BARBOSA, F.R. Manejo integrado de pragas da mangueira In: SIMPÓSIO DE MANGA DO VALE DO SÃO FRANCISCO, 1., 2005, Juazeiro. Anais… Petrolina: Embrapa Semi-Árido, 2005. CD-ROM.
  • BARBOSA, F.R.; PARANHOS, B.A.J. Artrópodes-praga associados à cultura da mangueira no Brasil e seu contole. In: MENEZES, E.A.; BARBOSA, F.R. Pragas da mangueira: monitoramento, nível de ação e controle. Petrolina: Embrapa Semi-Árido, 2005. p.17-50.
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  • CAVALLERI, A.; ROMANOWSKI, H.P.; REDAELLI, L.R. Thrips species (Insecta, Thysanoptera) inhabiting plants of the Parque Estadual de Itapuã, Rio Grande do Sul, Brazil. Revista Brasileira de Zoologia, Curitiba, v. 23, n. 2, p. 367-374, 2006.
  • DUARTE, R. T.; GALLI, J. C.; PAZINI, W. C. Levantamento populacional de predadores (Arthropoda) em cultivo orgânico de goiaba (Psidium guajava L.). Revista Agroambiente, Boa Vista, v.7, n.3, p.352-358, 2013.
  • HICKEL, E.R.; DUCROQUET, J.H.J. Tripes associados à floração da nectarina em Santa Catarina. Anais da Sociedade Entomológica do Brasil, Jaboticabal, v.27, n.2, p.307-308, 1998.
  • HODDLE, M.S.; MORSE, J.G.; PHILLIPS, P.P.; FABER, B.; JETTER, KAREN. Avocado thrips: new challenge for growers. California Agriculture, Los Angeles, v.56, n.3, p.103-107, 2002.
  • IBGE. Produção agrícola municipal. Rio de Janeiro, 2018, Disponível em: http://www.sidra.ibge.gov.br Acesso em: 8 maio 2018.
    » http://www.sidra.ibge.gov.br
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  • LIMA, E.F.B.; FONTES, L.S.; PINENT, S.M.J.; REIS, A.S.; FREIRE FILHO, F.R.; LOPES, A.C.A. Thrips species (Insecta: Thysanoptera) associated to Cowpea in Piauí, Brazil. Biota Neotropica, Campinas, v.13, n.1, p. 383-386, 2013a.
  • LIMA, E.F.B.; MONTEIRO, R.C.; ZUCCHI, R.A. Thrips species (Insecta: Thysanoptera) associated to Fabaceae of agricultural importance in Cerrado and Amazon-Caatinga ecotone from Brazilian Mid-North. Biota Neotropica, Campinas v.13, n.2, p.283-289, 2013b.
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  • MOREIRA, A.N.; OLIVEIRA, V.J.; OLIVEIRA, J.E.M.;SOUZA, G.M.M.; BREDA, M.O. Injuries caused by frankliniella spp. (thysanoptera: thripidae) on seedless grapes. Ciência e Agrotecnologia, Lavras, v.38, n.4, p.328-334, 2014.
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  • OLIVEIRA, F.D.C.; COELHO, E.F.; VASCONCELOS, L.F.L.; ARAÚJO, E.C.E. Produção de manga sob diferentes regimes de irrigação, em condições subúmidas. Revista Brasileira de Engenharia Agrícola e Ambiental, Campina Grande,v.6, p.390-396, 2002.
  • PEÑA, J.E. Integrated pest management and monitoring techniques for mango pests. Acta Horticulturae, Wageningen, v.645, p.51-161, 2004.
  • PEÑA, J.E.; MOHYUDDIN, A.I.; WYSOKI, M. review of the pest management situation in mango agroecosystems. Phytoparasitica, Rehovot, v.26, n.2, p.129148, 1998.
  • PENG R.K.; CHRISTIAN. K. The weaver ant, Oecophylla smaragdina (Hymenoptera: Formicidae), an effective biological control agent of the red-banded thrips, Selenothrips rubrocinctus (Thysanoptera: Thripidae) in mango crops in the Northern Territory of Australia. International Journal of Pest Management, Abingdon, v.50, n.2, p.107-114, 2004.
  • PITCHAON, M. Antioxidant capacity of extracts and fractions from mango (Mangifera indica Linn.) seed kernels. International Food Research Journal, Serdang, v.18, n.1, p.523-528, 2011.
  • WYSOKI, M.; BEN-DOV, Y.; SWIRSKI, E.; IZHAR, Y. The arthropod pests of mango in Israel. Proceeding of the IV International Mango Symposium. Acta Horticulturae, Wageningen, v.341, p.452-466, 1993.

Publication Dates

  • Publication in this collection
    2019

History

  • Received
    08 July 2018
  • Accepted
    21 Sept 2018
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