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Mite fauna on transgenic soybean in an experimental station in western Bahia, Brazil

ABSTRACT

The aim of this study was to identify mite fauna associated with soybean crops and to report new species of the Monsoy 8349 IPRO variety in the municipality of Luís Eduardo Magalhães, western region of Bahia. Samplings were performed in an area with transgenic soybeans, subdivided into three treatments: T01, with no use of agricultural pesticides; T02, complete package of pesticides, except for acaricides; and T03, complete package of pesticides including acaricides. Twenty plants were selected per treatment at each sampling; one apical, one median, and one basal leaf were collected from each plant, totaling 60 leaves per treatment. A total of 1,292 mites were found, belonging to three families, five genera, and six species. The major phytophagous mite species found were Mononychellus planki McGregor and Tetranychus urticae Koch, while the major predatory mites found were Neoseiulus transversus Denmark & Muma and Euseius concordis Chant.

Keywords
Glycine max ; Tetranychidae; Phytoseiidae; biological control

INTRODUCTION

Soybean is a major agricultural crop in Brazil, cultivated in 35 million hectares with a production of 114 million tons in the harvest of 2018/19 (EMBRAPA, 2019EMBRAPA. Soja em números (safra 2018/19). Londrina: Embrapa Soja, 2019. Available from: http://www.infoteca.cnptia.embrapa.br/infoteca/handle/doc/1136580. Acessed on: 08 August 2019.
http://www.infoteca.cnptia.embrapa.br/in...
). In the state of Bahia, the cultivated area is larger than 1.5 million hectares, with mean yield of 5.3 million tons, approximately 5% of national production and 58% of production in the Northeast (CONAB, 2017–2018CONAB. Conjuntura de Soja. Brasília: CONAB, 2017–2018. Available from: https://www.conab.gov.br/info-agro/analises-do-mercado-agropecuario-e-extrativista/analises-do-mercado/historico-de-conjunturas-de-soja. Acessed on: 25 Nov. 2022.
https://www.conab.gov.br/info-agro/anali...
). This crop had a higher expansion from 1990 to 2008 in the western region of the state, but exploited areas for this crop only increased in 2001 in the municipality of Luís Eduardo Magalhães. Over the last years, soybean crop yield has increased by reducing losses caused by limiting factors such as pest insects, especially mite species (ÁVILA; GRIGOLLI, 2014ÁVILA, C.J.; GRIGOLLI, J.F.J. Pragas da soja e seu controle. In: LOURENÇÃO, A.L.F. et al. (ed.). Tecnologia e produção: Soja 2013/2014. Curitiba: Midiograf, 2014. chap.6, p.109-168.).

Studies conducted in Brazil have identified a few phytophagous mite species as the most frequent and most damaging to soybean crops: Mononychellus planki McGregor, 1950, Tetranychus desertorum (BANKS, 1900BANKS, N. The red spiders of the United States (Tetranychus and Stigmaeus). U.S. Department of Agriculture Division of Entomology. Technical Series Bulletin, v.8, p.65-77, 1900.), Tetranychus gigas (PRITCHARD; BAKER, 1955PRITCHARD, A.E.; BAKER, E.W. A revision of the spider mite family Tetranychidae. v.2. San Francisco: Pacific Coast Entomological Society, 1955. 472p.), Tetranychus ludeni Zacher, 1913, Tetranychus urticae Koch, 1836 (Tetranychidae), and Polyphagotarsonemus latus (BANKS, 1904BANKS, N. A treatise on the Acarina or mites. Proceedings of the United States National Museum, Washington, D.C., v.28, n.1382, p.1-114, 1904. https://doi.org/10.5479/si.00963801.28-1382.1
https://doi.org/10.5479/si.00963801.28-1...
) (Tarsonemidae) (GUEDES et al., 2007GUEDES, J.V.C.; NAVIA, D.; LOFEGO, A.C.; DEQUECH, S.T.B. Ácaros associados à cultura da soja no Rio Grande do Sul, Brasil. Neotropical Entomology, Londrina, v.36, n.2, p.288-293, 2007. https://doi.org/10.1590/S1519-566X2007000200017
https://doi.org/10.1590/S1519-566X200700...
; ROGGIA et al., 2009ROGGIA, S.; GUEDES, J.V.C.; KUSS ROGGIA, R.C.R.; VASCONCELOS, G.J.N.; NAVIA, D.; DELALIBERA JUNIOR, I. Ácaros predadores e o fungo Neozygites floridana associados a tetraniquídeos em soja no Rio Grande do Sul. Pesquisa Agropecuária Brasileira, Brasília, v.44, p.107-110, 2009. https://doi.org/10.1590/S0100-204X2009000100015
https://doi.org/10.1590/S0100-204X200900...
; ÁVILA; GRIGOLLI, 2014ÁVILA, C.J.; GRIGOLLI, J.F.J. Pragas da soja e seu controle. In: LOURENÇÃO, A.L.F. et al. (ed.). Tecnologia e produção: Soja 2013/2014. Curitiba: Midiograf, 2014. chap.6, p.109-168.). Also, several predator species were reported in soybean crops, such as: Euseius alatus De Leon, 1966, Galendromus annectens, De Leon, 1958, Iphiseiodes zuluagai (DENMARK; MUMA, 1973DENMARK, H.A.; MUMA, M.H. Phytoseiid mites of Brazil (Acarina: Phytoseiidae). Revista Brasileira de Biologia, São Carlos, v.33, p.235-276, 1973.), Neoseiulus anonymus Chant & Baker, 1965, Neoseiulus benjamini Schica, 1981, Neoseiulus californicus McGregor, 1954, Neoseiulus idaeus (DENMARK; MUMA, 1973DENMARK, H.A.; MUMA, M.H. Phytoseiid mites of Brazil (Acarina: Phytoseiidae). Revista Brasileira de Biologia, São Carlos, v.33, p.235-276, 1973.), Neoseiulus transversus (DENMARK; MUMA, 1973DENMARK, H.A.; MUMA, M.H. Phytoseiid mites of Brazil (Acarina: Phytoseiidae). Revista Brasileira de Biologia, São Carlos, v.33, p.235-276, 1973.), Neoseiulus tunus De Leon, 1967, Phytoseiulus fragariae Denmark & Schicha, 1983, Phytoseiulus macropilis (BANKS, 1904BANKS, N. A treatise on the Acarina or mites. Proceedings of the United States National Museum, Washington, D.C., v.28, n.1382, p.1-114, 1904. https://doi.org/10.5479/si.00963801.28-1382.1
https://doi.org/10.5479/si.00963801.28-1...
), Proprioseiopsis cannaensis (MUMA, 1962MUMA, M.H. New Phytoseiidae (Acarina: Mesostigmata) from Florida. Florida Entomologist, Lutz, v.45, n.1, p.1-10, 1962.), Proprioseiopsis neotropicus Ehara, 1966 e Typhlodromalus aripo De Leon, 1967 (ROGGIA et al., 2009ROGGIA, S.; GUEDES, J.V.C.; KUSS ROGGIA, R.C.R.; VASCONCELOS, G.J.N.; NAVIA, D.; DELALIBERA JUNIOR, I. Ácaros predadores e o fungo Neozygites floridana associados a tetraniquídeos em soja no Rio Grande do Sul. Pesquisa Agropecuária Brasileira, Brasília, v.44, p.107-110, 2009. https://doi.org/10.1590/S0100-204X2009000100015
https://doi.org/10.1590/S0100-204X200900...
; REZENDE et al., 2012REZENDE, J.M.; LOFEGO, A.C.; NÁVIA, D.; ROGGIA, S. Mites (Acari: Mesostigmata, Sarcoptiformes and Trombidiformes) associated to soybean in Brazil, including new records from the Cerrado areas. Florida Entomologist, Lutz, v.95, n.3, p.683-693, 2012.; REICHERT et al., 2014REICHERT, M.B.; SILVA, G.L.; ROCHA, M. S.; JOHANN, L.; FERLA, N.J. Mite fauna (Acari) in soybean agroecosystem in the northwestern region of Rio Grande do Sul State, Brazil. Systematic and Applied Acarology, Auckland, v.19, n.2, p.123-136, 2014. https://doi.org/10.11158/saa.19.2.2
https://doi.org/10.11158/saa.19.2.2...
; CAVALCANTE et al., 2017CAVALCANTE, A.C.C.; FAMAH SOURASSOU, N.; MORAES, G.J. Potential predation of the exotic Amblyseiius swirskii on Euseius concordis (Acari Phytoseiiiae), a predatory mite commonly found in Brazil. Biocontrol Science of Technology, London, v.27, n.2, p.288-293, 2017. https://doi.org/10.1080/09583157.2016.1272096
https://doi.org/10.1080/09583157.2016.12...
, 2018CAVALCANTE, A.C.C.; DEMITE, P.R.; DA SILVA CARNEIRO, M.E.; NUNES, L. S.; DE AZEVEDO PEREIRA, A.I. Mites (Acari) associated with soybean culture (Glycine max), in the southeast region of Goiás state. Magistra, v.29, n.3/4, p.266-272, 2018.).

The aim of this study was to identify the mite fauna associated to soybean crops of the Monsoy 8349 IPRO variety in the municipality of Luís Eduardo Magalhães, western region of Bahia; and to report new predator species for this culture and analyze if phytophagous and predators species have any significant correlation.

MATERIAL AND METHODS

The investigation was conducted at the experimental station of Fundação de Apoio à Pesquisa e Desenvolvimento do Oeste Baiano (Fundação Bahia), 12°04’52.3”S 45°42’47.3”W, between November 2018 and March 2019 in the municipality of Luís Eduardo Magalhães located in the western region of Bahia. According to Köppen’s classification, the climate in the municipality is BSh, hot and dry with winter rains.

The experiment was carried out in an area with transgenic soybeans subdivided into three treatments: T01, with no use of agricultural pesticides; T02, with a complete package of pesticides, except for acaricides; and T03, with a complete package of pesticides including acaricides. Each treatment contained 15 rows with 0.5 m spacing, and covered an area of 336 m2. Sowing occurred on November 30, 2018, and the variety used was Monsoy 8349 IPRO. This genotype was chosen because it was the most frequently used variety both in previous harvests and in the region.

Seeds were treated with carbendazim + thiram (0.08 g), fipronil (0.02), inoculant (0.05), 4-indol-3-ylbutyric acid + gibberellic acid + kinetin (0.06). Products and dosages used in treatments T02 and T03 (Table 1) for phytosanitary management, as well as application dates, were defined according to soybean development stages and considering the protocols adopted by regional farmers.

Table 1
Agricultural pesticides used in the treatments “complete package of agricultural pesticides, except for acaricides” (T02) and “complete package of agricultural pesticides” (T03), in the municipality of Luís Eduardo Magalhães, Bahia, 2018/19 harvest.

Samplings were first conducted biweekly, and then became weekly when the presence of mites was confirmed. Samplings started in the V2 stage, according to the classification proposed by FEHR; CAVINESS (1977)FEHR, W.R.; CAVINESS, C.E. Stages of soybean development. Ames: lowa State University of Science and Technology, 1977. 11p. Available from: https://dr.lib.iastate.edu/handle/20.500.12876/90239. Acessed on: 20 June 2020.
https://dr.lib.iastate.edu/handle/20.500...
and ended at harvest. A total of 20 plants were randomly sampled in each treatment. Three leaves per plant were removed (apical, median, and basal), totaling 60 leaves per treatment.

Leaves were stored in plastic bags, which were labeled and transported in a thermal box to the Laboratório de Fisiopatologia of Universidade Estadual da Bahia (UNEB), where they were analyzed under a stereo microscope. Mites found were mounted on microscopy slides in Hoyer’s medium (FLECHTMANN, 1985FLECHTMANN, C.H.W. Ácaros de importância agrícola. São Paulo: Nobel, 1985. 189p.). Slides were settled in an oven (50–60 °C) for 10 days for fixation and diaphanization of specimens. After this period slides were identified using labels and stored in appropriate boxes in an acclimatized room with controlled relative air humidity. Mite identification was performed at the Laboratório de Acarologia of Universidade do Vale do Taquari, with the aid of a phase contrast microscope and dichotomous keys (LINDQUIST, 1986LINDQUIST, E.E. The world genera of Tarsonemidae (Acari: Heterostigmata): a morphological, phylogenetical, and systematic revision, with a reclassification family-group taxa in the Heterostigmata. The Memoirs of the Entomological Society of Canada, Cambridge, v.118, n.S136, p. 1-517, 1986. https://doi.org/10.4039/entm118136fv
https://doi.org/10.4039/entm118136fv...
; BAKER; TUTTLE, 1994BAKER, E.W.; TUTTLE D.M. (ed.) A guide to the spider mites (Tetranychidae) of the United States. West Bloomfield: Indira, 1994. 347p.; CHANT; MCMURTRY, 2007CHANT, D.A.; MCMURTRY J.A. Illustrated keys and diagnoses for the genera and subgenera of the Phytoseiidae of the World (Acari: Mesostigmata). Michigan: Indira, 2007. 220p.). Bioestat 5.0 was used for statistical analyses and the correlation coefficient (r) was performed to evaluate the mite preference in each treatment (AYRES et al., 2007AYRES, M.; AYRES JR., M.; AYRES, D.L.; SANTOS, A.A.S. BioEstat 5.0: aplicações estatísticas nas áreas das ciências biológicas e médicas. Sociedade Civil Mamirauá, 2007. 364p.).

RESULTS

A total of 1292 mites were found, belonging to three families, five genera, and six species (Table 2). The highest richness was found in treatment T01, with five species, followed by T02, with four species, and T03, with the lowest amount, three species. On the other hand, treatment T02 had the highest abundance, with 857 mites; T01 with 233 mites and T03 with 202 mites. No mites were found on the adaxial face of the leaves examined.

Table 2
Mite fauna found in area with transgenic soybeans subdivided into three treatments: T01, with no use of agricultural pesticides; T02, with a complete package of pesticides, except for acaricides; and T03, with a complete package of pesticides including acaricides, in the municipality of Luís Eduardo Magalhães, Bahia, 2018/19 harvest.

Tetranychus urticae and M. planki were present in all treatments, i.e., they accounted for 99% of specimens collected. M. planki had the highest abundance compared to the other species; during the study period, 846 specimens were found, of which 746 were present in T02.

In the present study, it is reported for the first time the presence of Euseius concordis (CHANT, 1959CHANT, D.A. Phytoseiid Mites (Acarina: Phytoseiidae). Memoirs of the Entomological Society of Canada, Winnipeg, v.91, n.S12, p.5-166, 1959. https://doi.org/10.4039/entm9112fv
https://doi.org/10.4039/entm9112fv...
) and Neoseiulus gracilis (MUMA, 1962MUMA, M.H. New Phytoseiidae (Acarina: Mesostigmata) from Florida. Florida Entomologist, Lutz, v.45, n.1, p.1-10, 1962.) on soybean crops. The highest number of predatory mites was observed in T01, with no chemicals applied. For this site was observed significant correlation between E. concordis and Tarsonemus sp. (r = 1; p < 0.0001), E. concordis and M. planki (r = 0.89; p = 0.0005), N. transversus and Tarsonemus sp. (r = 0.79; p = 0.0059), and N. transversus and M. planki(r = 0.93; p = 0.0001). Neoseiulus transversus may be an effective predator on the M. planki control in T01; a ratio of approximately four phytophagous per predatory mites were accounted for. These results may suggest the higher potential for biological control in this treatment without agrochemicals application, as also observed by ALI (1998)ALI, F.S. Life tables of Phytoseiulus macropilis (Banks) (Gamasida: Phytoseiidae) at different temperatures. Experimental and Applied Acarology, Basel, v.22, n.6, p.335-342, 1998. https://doi.org/10.1023/A:1024560924642
https://doi.org/10.1023/A:1024560924642...
. Studies have reported that insecticides/acaricides have a direct effect on predatory mite fauna in many agricultural crops (SATO et. al., 2009SATO, M.E.; SILVA, M.Z.; SILVA, R.B.; SOUZA FILHO, M.F.; RAGA, A. Monitoramento da resistência de Tetranychus urticae Koch (Acari: Tetranychidae) a abamectin e fenpyroximate em diversas culturas no estado de São Paulo. Arquivos do Instituto Biológico, São Paulo, v.76, n.2, p.217-223, 2021. https://doi.org/10.1590/1808-1657v76p2172009
https://doi.org/10.1590/1808-1657v76p217...
; 2016SATO, M. E.; VERONEZ, B.; STOCCO, R.S.M.; QUEIROZ, M.C.V.; GALLEGO, R. Spiromesifen resistance in Tetranychus urticae (Acari: Tetranychidae): Selection, stability, and monitoring. Crop Protection, v.89, p.278-283, 2016. https://doi.org/10.1016/j.cropro.2016.08.003
https://doi.org/10.1016/j.cropro.2016.08...
; FOUNTAIN; MEDD, 2015FOUNTAIN, M.T.; MEDD, N. Integrating pesticides and predatory mites in soft fruit crops. Phytoparasitica, Basel, v.43, n.5, p.657-667, 2015. https://doi.org/10.1007/s12600-015-0485-y
https://doi.org/10.1007/s12600-015-0485-...
; MAROUFPOOR et al., 2016MAROUFPOOR, M.; GHOOSTA, Y.; POURMIRZA, A.A.; LOTFALIZADEH, H. The effects of selected acaricides on life table parameters of the predatory mite, Neoseiulus californicus fed on European red mite. North-Western Journal of Zoology, Oradea, v.12, n.1, e151101, 2016.; SCHMIDT-JEFFRIS et al., 2021SCHMIDT-JEFFRIS, R.A.; COFFEY, J.L.; MILLER, G.; FARFAN, M.A. Residual activity of acaricides for controlling spider mites in watermelon and their impacts on resident predatory mites. Journal of Economic Entomology, v.114, n.2, p.818-827, 2021. https://doi.org/10.1093/jee/toaa320
https://doi.org/10.1093/jee/toaa320...
), and this is supported by the data obtained in the present study.

In T02, M. planki was more abundant species, showing not being directly affected by pesticides. However, pesticides seem to have affected populations of Phytoseiidae, as only one specimen of N. gracilis was found, which correlated with Tarsonemus sp. (r = 0.91; p = 0.0002).

The abundance of M. planki exposed to acaricides in T03 decreased in relation to T02; T. urticae seems to have benefited from the application of all pesticides (including acaricides) because in T03 it presented the highest abundance observed in the present study. No phytoseiids were collected in this experimental area.

According to BUENO et al. (2012)BUENO, A.D.F. et al. Inimigos naturais das pragas da soja. In: BUENO, A.D.F. et al. Soja: manejo integrado de insetos e outros artrópodes-praga. Brasília: EMBRAPA, 2012. p.493-629., increase in pest mite population under these conditions might be associated to: (1) predator inhibition, as only one phytoseiid specimen was found in T02 and none in T03; (2) improved plant conditions, derived from fertilization or from changes in plant physiology caused by pesticides (trophobiosis); and (3) the stimulation of mite reproduction provided by pyrethroid, neonicotinoid insecticides, and others (hormoligosis). CAMPBELL (1978)CAMPBELL, W.V. Effect of pesticide interactions on the twospotted spider mite on peanuts. Peanut Science, Alexandria, v.5, n.2, p.83-86, 1978. and BOYKIN; CAMPBELL (1982)BOYKIN, L.S.; CAMPBELL, W.V. Rate of population increase of the twospotted spider mite (Acari: Tetranychidae) on peanut leaves treated with pesticides. Journal of Economic Entomology, Oxford, v.75, n.6, p.966-971, 1982. https://doi.org/10.1093/jee/75.6.966
https://doi.org/10.1093/jee/75.6.966...
observed that some pesticides can contribute to increased mite populations in peanut fields by stimulation of the mite’s reproductive potential.

Further studies must be carried out to evaluate the potential of N. transversus in the control of M. planki; the effects of pesticides on M. planki and T. urticae in soybean in Brazil.

ACKNOWLEDGEMENTS

The authors thank the Fundação de Apoio à Pesquisa e Desenvolvimento do Oeste Baiano (Fundação Bahia) for providing the area for research and for the land preparation tools, also to the employees who worked in the application of pesticides. We also thank the Laboratório de Fisiopatologia of Universidade Estadual da Bahia (UNEB) and the Laboratório de Acarologia of Universidade do Vale do Taquari – Univates for providing space for sampling analysis and mite mounting and identification process during the study.

  • Peer Review History: Double-blind Peer Review.
  • AVAILABILITY OF DATA AND MATERIAL

    All data generated or analyzed during this study are included in this published article.
  • FUNDING

    This work did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
  • ETHICAL APPROVAL

    Not applicable.

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Edited by

Section Editor: Silvia Galleti

Publication Dates

  • Publication in this collection
    09 Jan 2023
  • Date of issue
    2022

History

  • Received
    13 July 2022
  • Accepted
    01 Nov 2022
Instituto Biológico Av. Conselheiro Rodrigues Alves, 1252 - Vila Mariana - São Paulo - SP, 04014-002 - São Paulo - SP - Brazil
E-mail: arquivos@biologico.sp.gov.br