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Interaction between predatory mites (Acari: Phytoseiidae) and entomopathogenic fungi in Tetranychus urticae populations

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Abstract

The mite Tetranychus urticae Koch is an important pest on several agricultural crops. Resistance to synthetic pesticides has encouraged evaluating more sustainable control strategies. We evaluated the predatory mites Phytoseiulus persimilis Athias Henriot and Neoseiulus californicus McGregor alone or as vectors of entomopathogenic fungi on the mortality of T. urticae. We estimated the susceptibility of the predatory mites and T. urticae to infection by Metarhizium anisopliaesensu stricto (s. str.) (Metchnikoff) Sorokin, Beauveria bassianas. str. Bals. Vuill, Akanthomyces lecanii (Zimm.) Spatafora, Kepler & B. Shrestha and Cordyceps fumosorosea (Wize) Kepler, B. Shrestha & Spatafora. Then, we determined the mortality of T. urticae due to the two predatory mites alone or in combination with the four fungal isolates. T. urticae was more susceptible to fungi than the predatory mites. B. bassiana and M. anisopliae isolates caused the greatest mortality. Greater mortality of T. urticae was achieved when predatory mites were vectoring B. bassiana or M. anisopliae conidia. Combining predatory mites and entomopathogenic fungi has potential for the control of T. urticae.

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source to force predatory mites to move into the arena

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References

  • Al-Mazra'Awi MS, Kevan PG, Shipp L (2007) Development of Beauveria bassiana dry formulation for vectoring by honey bees Apis mellifera (Hymenoptera: Apidae) to the flowers of crops for pest control. Biocontr Sci Technol 7:733–741

    Article  Google Scholar 

  • Barber A, Campbell CAM, Crane H, Lilley R, Tregidga E (2003) Biocontrol of two-spotted spider mite Tetranychus urticae on dwarf hops by the Phytoseiid mites Phytoseiulus persimilis and Neoseiulus californicus. Biocontr Sci Technol 3:275–284

    Article  Google Scholar 

  • Baverstock J, Roy HE, Pell JK (2010) Entomopathogenic fungi and insect behaviour: from unsuspecting hosts to targeted vectors. BioControl 55:89–102

    Article  Google Scholar 

  • Blümel S, Walzer A (2002) Efficacy of different release strategies of Neoseiulus californicus McGregor and Phytoseiulus persimilis Athias Henriot (Acari: Phytoseiidae) for the control of two-spotted spider mite (Tetranychus urticae Koch) on greenhouse cut roses. Syst Appl Acarol 7:35–48

    Google Scholar 

  • Bugeme DM, Knapp M, Ekesi S, Chabi-Olaye A, Boga HI, Maniania NK (2015) Efficacy of Metarhizium anisopliae in controlling the two-spotted spider mite Tetranychus urticae on common bean in screen house and field experiments. Insect Sci 22:121–128

    Article  Google Scholar 

  • Çağatay NS, Menault P, Riga M, Vontas J, Ay R (2018) Identification and characterization of abamectin resistance in Tetranychus urticae Koch populations from greenhouses in Turkey. Crop Prot 112:112–117

    Article  Google Scholar 

  • Chandler D, Davidson G, Pell JK, Ball BV, Shaw K, Sunderland KD (2000) Fungal biocontrol of Acari. Biocontr Sci Technol 10:357–384

    Article  Google Scholar 

  • Chandler D, Davidson G, Jacobson RJ (2005) Laboratory and glasshouse evaluation of entomopathogenic fungi against the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae), on tomato, Lycopersicon esculentum. Biocontr Sci Technol 15:37–54

    Article  Google Scholar 

  • Choh Y, Sabelis MW, Janssen A (2017) Predatory interactions between prey affect patch selection by predators. Behav Ecol Sociobiol 71:66. https://doi.org/10.1007/s00265-017-2288-2

    Article  PubMed  PubMed Central  Google Scholar 

  • Dogan YO, Hazir S, Yildiz A, Butt TM, Cakmak I (2017) Evaluation of entomopathogenic fungi for the control of Tetranychus urticae (Acari: Tetranychidae) and the effect of Metarhizium brunneum on the predatory mites (Acari: Phytoseiidae). Biol Control 111:6–12

    Article  Google Scholar 

  • Dromph KM (2001) Dispersal of entomopathogenic fungi by collembolans. Soil Biol Biochem 33:2047–2051

    Article  CAS  Google Scholar 

  • Duso C, Malagnini V, Pozzebon A, Castagnoli M, Liguori M, Simoni S (2008) Comparative toxicity of botanical and reduced-risk insecticides to Mediterranean populations of Tetranychus urticae and Phytoseiulus persimilis (Acari: Tetranychidae, Phytoseiidae). Biol Control 47:16–21

    Article  Google Scholar 

  • Fathipour Y, Karimi M, Farazmand A, Talebi AA (2018) Age-specific functional response and predation capacity of Phytoseiulus persimilis (Phytoseiidae) on the two-spotted spider mite. Acarologia 58:31–40

    Google Scholar 

  • Gerson U, Weintraub PG (2007) Review mites for the control of pests in protected cultivation. Pest Man Sci 63:658–676

    Article  CAS  Google Scholar 

  • Greco NM, Liljesthröm GG, Gugole Ottaviano MF, Cluigt N, Cingolani MF, Zembo JC, Sánchez NE (2011) Pest management plan for the two-spotted spider mite, Tetranychus urticae, based on the natural occurrence of the predatory mite Neoseiulus californicus in strawberries. Int J Pest Man 57:299–308

    Article  Google Scholar 

  • Ibarra-Cortés KH, Guzmán-Franco AW, González-Hernández H, Suarez-Espinosa J, Baverstock J (2013) Selection of a fungal isolate for the control of the pink hibiscus mealybug Maconellicoccus hirsutus. Pest Manag Sci 69:874–882

    Article  Google Scholar 

  • Inglis GD, Enkerli J, Goettel MS (2012) Laboratory techniques used for entomopathogenic fungi: Hypocreales. In: Lacey LA (ed) Manual of techniques in invertebrate pathology. Academic Press London, Second Edition, pp 189–253

    Chapter  Google Scholar 

  • Kamel MS, Afia SI, El Saiedy E (2018) Biological control of Tetranychus urticae (Acari: Tetranychidae) using four predatory mites (Acari: Phytoseiidae) on two sweet pea cultivars. Biosci Res 15:185–191

    Google Scholar 

  • Lin G, Tanguay A, Guertin C, Todorova S, Brodeur J (2017) A new method for loading predatory mites with entomopathogenic fungi for biological control of their prey. Biol Control 115:105–111

    Article  Google Scholar 

  • Márquez-Chávez A, Guzmán-Franco AW, Santillán-Galicia MT, Tamayo-Mejía F, Rodríguez-Maciel JC (2019) Effect of host plant on the genetic diversity of Tetranychus urticae Koch populations and their susceptibility to fungal infection. Biol Control 137:104015. https://doi.org/10.1016/j.biocontrol.2019.104015

    Article  Google Scholar 

  • McMurtry JA, De Moraes GJ, Sourassou NF (2013) Revision of the lifestyles of phytoseiid mites (Acari: Phytoseiidae) and implications for biological control strategies. Syst Appl Acarol 18:297–320

    Google Scholar 

  • Midthassel A, Leather SR, Wright DJ, Baxter IH (2016) Compatibility of Amblyseius swirskii with Beauveria bassiana: two potentially complementary biocontrol agents. BioControl 61:437–447

    Article  Google Scholar 

  • Mori K, Saito Y, Sakagami T (1999) Effects of the nest web and female attendance on survival of young in the subsocial spider mite Schizotetranychus longus (Acari: Tetranychidae). Exp Appl Acarol 23:411–418

    Article  Google Scholar 

  • Payne R, Murray D, Harding S, Baird D, Soutar D (2005) GenStat for Windows, 8th edn. Introduction. VSN International, Hemel Hempstead, UK

    Google Scholar 

  • Rivero-Borja M, Guzmán-Franco AW, Rodriguez-Leyva E, Santillán-Ortega C, Pérez-Panduro A (2018) Interaction of Beauveria bassiana and Metarhizium anisopliae with chlorpyrifos ethyl and spinosad in Spodoptera frugiperda larvae. Pest Manage Sci 74:2047–2052

    Article  CAS  Google Scholar 

  • Saito Y (1985) Life types of spider mites. In: Helle W, Sabelis MW (eds) Spider mites: their biology, natural enemies and control. Elsevier, Amsterdam, pp 253–264

    Google Scholar 

  • Saito T, Brownbridge M (2016) Compatibility of soil-dwelling predators and microbial agents and their efficacy in controlling soil-dwelling stages of western flower thrips Frankliniella occidentalis. Biol Control 92:92–100

    Article  Google Scholar 

  • Seiedy M, Saboori A, Allahyari H (2012) Interactions of two natural enemies of Tetranychus urticae, the fungal entomopathogen Beauveria bassiana and the predatory mite, Phytoseiulus persimilis. Biocontrol Sci Technol 22:873–882

    Article  Google Scholar 

  • Trandem N, Berdinesen R, Pell JK, Klingen I (2016) Interactions between natural enemies: Effect of a predatory mite on transmission of the fungus Neozygites floridana in two-spotted spider mite populations. J Invertebr Pathol 134:35–37

    Article  Google Scholar 

  • Ullah MS, Lim UT (2015) Laboratory bioassay of Beauveria bassiana against Tetranychus urticae (Acari: Tetranychidae) on leaf discs and potted bean plants. Exp Appl Acarol 65:307–318

    Article  CAS  Google Scholar 

  • Ullah MS, Lim UT (2017) Laboratory evaluation of the effect of Beauveria bassiana on the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae). J Invertebr Pathol 148:102–109

    Article  Google Scholar 

  • van Leeuwen T, Tirry L, Yamamoto A, Nauen R, Dermauw W (2015) The economic importance of acaricides in the control of phytophagous mites and an update on recent acaricide mode of action research. Pestic Biochem Phys 121:12–21

    Article  Google Scholar 

  • Vergel SJN, Bustos RA, Rodríguez CD, Cantor RF (2011) Laboratory and greenhouse evaluation of the entomopathogenic fungi and garlic–pepper extract on the predatory mites, Phytoseiulus persimilis and Neoseiulus californicus and their effect on the spider mite Tetranychus urticae. Biol Control 57:143–149

    Article  Google Scholar 

  • Welham SJ, Gezan SA, Clark SJ, Mead A (2015) Statistical methods in biology: design and analysis of experiments and regression. CRC Press (Taylor & Francis Group), Boca Raton, FL

    Google Scholar 

  • Wu SY, Gao YL, Xu XN, Wang DJ, Li J, Wang HH, Lei ZR (2015) Feeding on Beauveria bassiana-treated Frankliniella occidentalis causes negative effects on the predatory mite Neoseiulus barkeri. Sci Rep 5:12033. https://doi.org/10.1038/srep12033

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu SY, Xie HC, Li MY, Xu XN, Lei ZR (2016) Highly virulent Beauveria bassiana strains against the two-spotted spider mite, Tetranychus urticae, show no pathogenicity against five phytoseiid mite species. Exp Appl Acarol 70:421–435

    Article  Google Scholar 

  • Wu S, Guo J, Xing Z, Gao Y, Xu X, Lei Z (2017) Comparison of mechanical properties for mite cuticles in understanding passive defense of phytoseiid mite against fungal infection. Mater Des 140:241–248

    Article  Google Scholar 

  • Wu S, Xing Z, Sun W, Xu X, Meng R, Lei Z (2018) Effects of Beauveria bassiana on predation and behavior of the predatory mite Phytoseiulus persimilis. J Invertebr Pathol 153:51–56

    Article  Google Scholar 

  • Zhang YX, Sun L, Lin GY, Lin JZ, Chen X, Ji J, Zhang ZQ, Saito Y (2015) A novel use of predatory mites for dissemination of fungal pathogen for insect biocontrol: The case of Amblyseius swirskii and Neoseiulus cucumeris (Phytoseiidae) as vectors of Beauveria bassiana against Diaphorina citri (Psyllidae). Syst Appl Acarol 20:177–187

    Google Scholar 

  • Zheng Y, De Clercq P, Song ZW, Li DS, Zhang BX (2017) Functional response of two Neoseiulus species preying on Tetranychus urticae Koch. Syst Appl Acarol 22:1059–1068

    Google Scholar 

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Acknowledgements

ORC received a scholarship from Consejo Nacional de Ciencia y Tecnología (CONACYT) Mexico for his Master of Science. This research was partially funded by Servicio Nacional de Sanidad, Inocuidad y Calidad Agroalimentaria (SENASICA), Mexico, under the project PM17-4048 ‘Determinación de la acarofauna presente en berries de la principals zonas productoras de Mexico'.

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Correspondence to Ariel W. Guzmán-Franco.

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Castillo-Ramírez, O., Guzmán-Franco, A.W., Santillán-Galicia, M. et al. Interaction between predatory mites (Acari: Phytoseiidae) and entomopathogenic fungi in Tetranychus urticae populations. BioControl 65, 433–445 (2020). https://doi.org/10.1007/s10526-020-10004-3

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