Advertisement

Root inoculation of strawberry with the entomopathogenic fungi Metarhizium robertsii and Beauveria bassiana reduces incidence of the twospotted spider mite and selected insect pests and plant diseases in the field

  • Fernanda Canassa
  • Fernanda C. N. Esteca
  • Rafael A. Moral
  • Nicolai V. Meyling
  • Ingeborg Klingen
  • Italo DelaliberaEmail author
Original Paper

Abstract

The effect of inoculation of strawberry roots by two entomopathogenic fungal isolates, Metarhizium robertsii (ESALQ 1622) and Beauveria bassiana (ESALQ 3375), on naturally occurring arthropod pests and plant diseases was investigated in four commercial strawberry fields during two growing seasons in Brazil. Three locations represented open-field production while strawberries were grown in low tunnels at the fourth location. Population responses of predatory mites to the fungal treatments were also assessed. Plants inoculated by the fungal isolates resulted in significantly fewer Tetranychus urticae adults compared to control plants at all four locations. The mean cumulative numbers ± SE of T. urticae per leaflet were: M. robertsii (225.6 ± 59.32), B. bassiana (206.5 ± 51.48) and control (534.1 ± 115.55) at the three open-field locations, while at the location with tunnels numbers were: M. robertsii (79.7 ± 10.02), B. bassiana (107.7 ± 26.85) and control (207.4 ± 49.90). Plants treated with B. bassiana had 50% fewer leaves damaged by Coleoptera, while there were no effects on numbers of whiteflies and thrips. Further, lower proportions of leaflets with symptoms of the foliar plant pathogenic fungi Mycosphaerella fragariae and Pestalotia longisetula were observed in the M. robertsii (4.6% and 1.3%)- and B. bassiana (6.1% and 1.3%)-treated plots compared to control plots (9.8% and 3.7%). No effect was seen on numbers of naturally occurring predatory mites. Our results suggest that both isolates tested may be used as root inoculants of strawberries to protect against foliar pests, particularly spider mites, and also against foliar plant pathogenic fungi without harming naturally occurring and beneficial predatory mites.

Keywords

Endophytic entomopathogenic fungi Microbial control Plant–microbe interactions Tetranychus urticae Integrated pest management (IPM) 

Notes

Acknowledgements

Daniela Milanez Silva and Vitor Isaias da Silva are thanked for technical assistance. We thank the strawberry producers Claudio Donizete dos Santos, Rafael Maziero, Mario Inui and Maurício dos Santos for letting us perform the experiments in their fields. We also thank Dr. Fagoni Fayer Calegario for helping to find the farmers and for introducing them to us. Dr. Geovanny Barroso is thanked for helping with the predatory mite identification.

Funding

This work was supported by the National Council for Scientific and Technological Development (CNPq) [Process No. 141373/2015-6] and by The Research Council of Norway through the SMARTCROP Project [Project Number 244526]. A 3-month student mission travel Grant to Norway was funded by CAPES (Project Number 88881.117865/2016-01) and SIU (Project Number UTF-2016-long-term-/10070).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Akello J, Sikora R (2012) Systemic acropedal influence of endophyte seed treatment on Acyrthosiphon pisum and Aphis fabae offspring development and reproductive fitness. Biol Control 61:215–221.  https://doi.org/10.1016/j.biocontrol.2012.02.007 CrossRefGoogle Scholar
  2. Akutse KS, Maniania NK, Fiaboe KKM, Van Den Berg J, Ekesi S (2013) Endophytic colonization of Vicia faba and Phaseolus vulgaris (Fabaceae) by fungal pathogens and their effects on the life-history parameters of Liriomyza huidobrensis (Diptera: Agromyzidae). Fungal Ecol 6:293–301.  https://doi.org/10.1016/j.funeco.2013.01.003 CrossRefGoogle Scholar
  3. Akutse KS, Fiaboe KKM, Van den Berg J, Ekesi S, Maniania NK (2014) Effects of endophyte colonization of Vicia faba (Fabaceae) plants on the life-history of leafminer parasitoids Phaedrotoma scabriventris (Hymenoptera: Braconidae) and Diglyphus isaea (Hymenoptera: Eulophidae). PLoS ONE 9:e109965.  https://doi.org/10.1371/journal.pone.0109965 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Andreazza F, Haddi K, Oliveira EE, Ferreira JAM (2016) Drosophila suzukii (Diptera: Drosophilidae) arrives at Minas Gerais State, a main strawberry production region in Brazil. Fla Entomol 99:796–798.  https://doi.org/10.1653/024.099.0439 CrossRefGoogle Scholar
  5. Ansari MA, Butt TM (2013) Influence of the application methods and doses on the susceptibility of black vine weevil larvae Otiorhynchus sulcatus to Metarhizium anisopliae in field-grown strawberries. Biocontrol 58:257–267.  https://doi.org/10.1007/s10526-012-9491-x CrossRefGoogle Scholar
  6. Attia S, Grissa KL, Lognay G, Bitume E, Hance T, Mailleux AC (2013) A review of the major biological approaches to control the worldwide pest Tetranychus urticae (Acari: Tetranychidae) with special reference to natural pesticides. J Pest Sci 86:361–386.  https://doi.org/10.1007/s10340-013-0503-0 CrossRefGoogle Scholar
  7. Barzman M, Bàrberi P, Birch ANE, Boonekamp P, Dachbrodt-Saaydeh S, Graf B, Hommel B, Jensen JE, Kiss J, Kudsk P, Lamichhane JR, Messéan A, Moonen AC, Ratnadass A, Ricci P, Sarah JL, Sattin M (2015) Eight principles of integrated pest management. Agron Sustain Dev 35:1199–1215.  https://doi.org/10.1007/s13593-015-0327-9 CrossRefGoogle Scholar
  8. Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–28.  https://doi.org/10.18637/jss.v067.i01 CrossRefGoogle Scholar
  9. Behie SW, Jones SJ, Bidochka MJ (2015) Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecol 13:112–119.  https://doi.org/10.1016/j.funeco.2014.08.001 CrossRefGoogle Scholar
  10. Bernardi D, Botton M, Nava DE, Zawadneak MAC (2015) Guia para a identificação e monitoramento de pragas e seus inimigos naturais em morangueiro. Embrapa Clima Temperado, BrasíliaGoogle Scholar
  11. Bing LA, Lewis LC (1991) Suppression of Ostrinia nubilalis (Hübner) (Lepidoptera: Pyralidae) by endophytic Beauveria bassiana (Balsamo) Vuillemin. Environ Entomol 20:1207–1211.  https://doi.org/10.1093/ee/20.4.1207 CrossRefGoogle Scholar
  12. Bixby-Brosi AJ, Potter DA (2012) Endophyte-mediated tritrophic interactions between a grass-feeding caterpillar and two parasitoid species with different life histories. Arthropod Plant Interact 6:27–34.  https://doi.org/10.1007/s11829-011-9163-2 CrossRefGoogle Scholar
  13. Brotman YL, Landau U, Cuadros-Inostroza A, Takayuki T, Fernie AR, Chet I, Viterbo A, Willmitzer L (2013) Trichoderma-plant root colonization: escaping early plant defense responses and activation of the antioxidant machinery for saline stress tolerance. PLoS Pathog 9:e1003221.  https://doi.org/10.1371/journal.ppat.1003221 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Canassa F, Tall S, Moral RA, Lara IAR, Delalibera I Jr, Meyling NV (2019) Effects of bean seed treatment by the entomopathogenic fungi Metarhizium robertsii and Beauveria bassiana on plant growth, spider mite populations and behavior of predatory mites. Biol Control 132:199–208.  https://doi.org/10.1016/j.biocontrol.2019.02.003 CrossRefGoogle Scholar
  15. Carroll G (1988) Fungal endophytes in stems and leaves—from latent pathogen to mutualistic symbiont. Ecology 69:2–9.  https://doi.org/10.2307/1943154 CrossRefGoogle Scholar
  16. Castillo-Lopez D, Zhu-Salzman K, Ek-Ramos MJ, Sword GA (2014) The entomopathogenic fungal endophytes Purpureocillium lilacinum (formerly Paecilomyces lilacinus) and Beauveria bassiana negatively affect cotton aphid reproduction under both greenhouse and field conditions. PLoS ONE 9:e103891.  https://doi.org/10.1371/journal.pone.0103891 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Castro TR, Wekesa VW, Moral RA, Demétrio CGB, Delalibera I Jr, Klingen I (2013) The effects of photoperiod and light intensity on the sporulation of Brazilian and Norwegian isolates of Neozygites floridana. J Invertebr Pathol 114:230–233.  https://doi.org/10.1016/j.jip.2013.08.004 CrossRefPubMedGoogle Scholar
  18. Castro T, Mayerhofer J, Enkerlib J, Eilenberg J, Meyling NV, Moral RA, Demétrio CGB, Delalibera I Jr (2016) Persistence of Brazilian isolates of the entomopathogenic fungi Metarhizium anisopliae and M. robertsii in strawberry crop soil after soil drench application. Agric Ecosyst Environ 233:361–369.  https://doi.org/10.1016/j.agee.2016.09.031 CrossRefGoogle Scholar
  19. Castro T, Eilenberg J, Delalibera I Jr (2018) Exploring virulence of new and less studied species of Metarhizium spp. from Brazil for two-spotted spider mite control. Exp Appl Acarol 74:139–146.  https://doi.org/10.1007/s10493-018-0222-6 CrossRefPubMedGoogle Scholar
  20. Chant DA, Yoshida-Shaul E (1991) Adult ventral setal patterns in the family Phytoseiidae (Acari: Gamasina). Int J Acarol 17(3):187–199.  https://doi.org/10.1080/01647959108683906 CrossRefGoogle Scholar
  21. Coll M, Shakya S, Shouster I, Nenner Y, Steinberg S (2007) Decision-making tools for Frankliniella occidentalis management in strawberry: consideration of target markets. Entomol Exp Appl 122:59–67.  https://doi.org/10.1111/j.1570-7458.2006.00488.x CrossRefGoogle Scholar
  22. Czaja K, Góralczyk K, Struciński P, Hernik A, Korcz W, Minorczyk M, Łyczewska M, Ludwicki JK (2015) Biopesticides—towards increased consumer safety in the European Union. Pest Manag Sci 71:3–6.  https://doi.org/10.1002/ps.3829 CrossRefPubMedGoogle Scholar
  23. Dara SK (2016) Managing strawberry pests with chemical pesticides and non-chemical alternatives. Int J Fruit Sci 16:1–13.  https://doi.org/10.1080/15538362.2016.1195311 CrossRefGoogle Scholar
  24. Demétrio CGB, Hinde J, Moral RA (2014) Models for overdispersed data in entomology. In: Ferreira CP, Godoy WAC (eds) Ecological modelling applied to entomology, 1st edn. Springer, New York, pp 219–259Google Scholar
  25. Easterbrook MA, Fitzgerald JD, Solomon MG (2001) Biological control of strawberry tarsonemid mite Phytonemus pallidus and two-spotted spider mite Tetranychus urticae on strawberry in the UK using species of Neoseiulus (Amblyseius) (Acari: Phytoseiidae). Exp Appl Acarol 25:25–36.  https://doi.org/10.1023/A:1010685903130 CrossRefPubMedGoogle Scholar
  26. Eilenberg J, Hajek A, Lomer C (2001) Suggestions for unifying the terminology in biological control. Biocontrol 46:387–400.  https://doi.org/10.1023/A:1014193329979 CrossRefGoogle Scholar
  27. FAOSTAT (2018) Food and Agriculture Organization of the United Nations Statistics. http://faostat.org/. Accessed 10 Oct 2018
  28. Fatoretto MB, Moral RA, Demétrio CGB, de Pádua CS, Menarin V, Rojas VMA, D’Alessandro CP, Delalibera I Jr (2018) Overdispersed fungus germination data: statistical analysis using R. Biocontrol Sci Technol 28:1034–1053.  https://doi.org/10.1080/09583157.2018.1504888 CrossRefGoogle Scholar
  29. Garcia R, Caltagirone LE, Gutierrez AP (1988) Comments on a redefinition of biological control. Bioscience 38:692–694.  https://doi.org/10.2307/1310871 CrossRefGoogle Scholar
  30. Garrido C, Carbú M, Fernández-Acero FJ, González-Rodríguez VE, Cantoral JM (2011) New insights in the study of strawberry fungal pathogens. In: Husaini AM, Mercado JA (eds) Genes, genomes and genomics, 1st edn. Global Science Books, Takamatsu, pp 24–39Google Scholar
  31. Garrido-Jurado I, Resquín-Romero G, Amarilla SP, Ríos-Moreno A, Carrasco L, Quesada-Moraga E (2017) Transient endophytic colonization of melon plants by entomopathogenic fungi after foliar application for the control of Bemisia tabaci Gennadius (Hemiptera: Aleyrodidae). J Pest Sci 90:319–330.  https://doi.org/10.1007/s10340-016-0767-2 CrossRefGoogle Scholar
  32. Gathage JW, Lagat ZO, Fiaboe KKM, Akutse KS, Ekesi S, Maniania NK (2016) Prospects of fungal endophytes in the control of Liriomyza leafminer flies in common bean Phaseolus vulgaris under field conditions. Biocontrol 61:741–753.  https://doi.org/10.1007/s10526-016-9761-0 CrossRefGoogle Scholar
  33. Goettel MS, Poprawski TJ, Vandenverg JD, Li Z, Roberts DW (1990) Safety to nontarget invertebrates of fungal biocontrol agents. In: Laird M, Lacey LA, Davison EW (eds) Safety of microbial insecticides, 1st edn. CRC Press, Flórida, pp 209–232Google Scholar
  34. González-Mas N, Cuenca-Medina M, Gutierrez-Sanchez F, Quesada-Moraga E (2019) Bottom-up effects of endophytic Beauveria bassiana on multitrophic interactions between the cotton aphid, Aphis gossypii, and its natural enemies in melon. J Pest Sci 92:1271–1281.  https://doi.org/10.1007/s10340-019-01098-5 CrossRefGoogle Scholar
  35. Greco NM, Pereyra PC, Guillade A (2005) Host-plant acceptance and performance of Tetranychus urticae (Acari: Tetranychidae). J Appl Entomol 130:32–36.  https://doi.org/10.1111/j.1439-0418.2005.01018.x CrossRefGoogle Scholar
  36. Greenfield M, Gomez-Jimenez MI, Ortiz V, Vega FE, Kramer M, Parsa S (2016) Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation. Biol Control 95:40–48.  https://doi.org/10.1016/j.biocontrol.2016.01.002 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Hajek AE, Delalibera I Jr (2010) Fungal pathogens as classical biological control agents against arthropods. Biocontrol 55:147–158.  https://doi.org/10.1007/s10526-009-9253-6 CrossRefGoogle Scholar
  38. Hoffmann D, Vierheilig H, Schausberger P (2011) Arbuscular mycorrhiza enhances preference of ovipositing predatory mites for direct prey-related cues. Physiol Entomol 36:90–95.  https://doi.org/10.1111/j.1365-3032.2010.00751.x CrossRefGoogle Scholar
  39. Jaber LR, Alananbeh KM (2018) Fungal entomopathogens as endophytes reduce several species of Fusarium causing crown and root rot in sweet pepper (Capsicum annuum L.). Biol Control 126:117–126.  https://doi.org/10.1016/j.biocontrol.2018.08.007 CrossRefGoogle Scholar
  40. Jaber LR, Araj SE (2018) Interactions among endophytic fungal entomopathogens (Ascomycota: Hypocreales), the green peach aphid Myzus persicae Sulzer (Homoptera: Aphididae), and the aphid endoparasitoid Aphidius colemani Viereck (Hymenoptera: Braconidae). Biol Control 116:53–61.  https://doi.org/10.1016/j.biocontrol.2017.04.005 CrossRefGoogle Scholar
  41. Jaber LR, Ownley BH (2018) Can we use entomopathogenic fungi as endophytes for dual biological control of insect pests and plant pathogens? Biol Control 116:36–45.  https://doi.org/10.1016/j.biocontrol.2017.01.018 CrossRefGoogle Scholar
  42. Keyser CA, Jensen B, Meyling NV (2016) Dual effects of Metarhizium spp. and Clonostachys rosea against an insect and a seed-borne pathogen in wheat. Pest Manag Sci 72:517–526.  https://doi.org/10.1002/ps.4015 CrossRefPubMedGoogle Scholar
  43. Klingen I, Haukeland S (2006) The soil as a reservoir for natural enemies of pest insects and mites with emphasis on fungi and nematodes. In: Eilenberg J, Hokkanen HMT (eds) An ecological and societal approach to biological control, 1st edn. Springer, Dordrecht, pp 145–211CrossRefGoogle Scholar
  44. Klingen I, Westrum K (2007) The effect of pesticides used in strawberries on the phytophagous mite Tetranychus urticae (Acari: Tetranychidae) and its fungal natural enemy Neozygites floridana (Zygomycetes: Entomophthorales). Biol Control 43:222–230.  https://doi.org/10.1016/j.biocontrol.2007.07.013 CrossRefGoogle Scholar
  45. Klingen I, Westrum K, Meyling N (2015) Effect of Norwegian entomopathogenic fungal isolates against Otiorhynchus sulcatus larvae at low temperatures and persistence in strawberry rhizospheres. Biol Control 81:1–7.  https://doi.org/10.1016/j.biocontrol.2014.10.006 CrossRefGoogle Scholar
  46. Kuhn TMA, Loeck AE, Zawadneak MAC, Garcia MS, Botton M (2014) Parâmetros biológicos e tabela de vida de fertilidade de Neopamera bilobata (Hemiptera: Rhyparochromidae) em morangueiro. Pesq Agropec Bras 49:422–427.  https://doi.org/10.1590/S0100-204X2014000600003 CrossRefGoogle Scholar
  47. Lacey LA, Grzywacz D, Shapiro-Ilan DI, Frutos R, Brownbridge M, Goettel MS (2015) Insect pathogens as biological control agents: back to the future. J Invertebr Pathol 132:1–41.  https://doi.org/10.1016/j.jip.2015.07.009 CrossRefGoogle Scholar
  48. Mantzoukas S, Chondrogiannis C, Grammatikopoulos G (2015) Effects of three endophytic entomopathogens on sweet sorghum and on the larvae of the stalk borer Sesamia nonagrioides. Entomol Exp Appl 154:78–87.  https://doi.org/10.1111/eea.12262 CrossRefGoogle Scholar
  49. McKinnon AC, Saari S, Moran-Diez ME, Meyling NV, Raad M, Glare TR (2017) Beauveria bassiana as an endophyte: a critical review on associated methodology and biocontrol potential. Biocontrol 62:1–17.  https://doi.org/10.1007/s10526-016-9769-5 CrossRefGoogle Scholar
  50. Meyling NV, Eilenberg J (2007) Ecology of the entomopathogenic fungi Beauveria bassiana and Metarhizium anisopliae in temperate agroecosystems: potential for conservation biological control. Biol Control 43:145–155.  https://doi.org/10.1016/j.biocontrol.2007.07.007 CrossRefGoogle Scholar
  51. Meyling N, Hajek A (2010) Principles from community and metapopulation ecology: application to fungal entomopathogens. Biol Control 55:39–54.  https://doi.org/10.1007/s10526-009-9246-5 CrossRefGoogle Scholar
  52. Moraes GJ, McMurtry JA, Denmark HA, Campos CB (2004) A revised catalogue of the mite family Phytoseiidae. Zootaxa 434:1–494.  https://doi.org/10.11646/zootaxa.434.1.1 CrossRefGoogle Scholar
  53. Moral RA, Hinde J, Demétrio CGB (2017) Half-normal plots and overdispersed models in R: the hnp package. J Stat Softw 81:1–23.  https://doi.org/10.18637/jss.v081.i10 CrossRefGoogle Scholar
  54. Oliveira DGP, Pauli G, Mascarin GM, Delalibera I (2015) A protocol for determination of conidial viability of the fungal entomopathogens Beauveria bassiana and Metarhizium anisopliae from commercial products. J Microbiol Methods 119:44–52.  https://doi.org/10.1016/j.mimet.2015.09.021 CrossRefPubMedGoogle Scholar
  55. Ownley BH, Griffin MR, Klingeman WE, Gwinn KD, Moulton JK, Pereira RM (2008) Beauveria bassiana: endophytic colonization and plant disease control. J Invertebr Pathol 3:267–270.  https://doi.org/10.1016/j.jip.2008.01.010 CrossRefGoogle Scholar
  56. Ownley B, Gwinn K, Vega F (2010) Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. Biocontrol 55:113–128.  https://doi.org/10.1007/s10526-009-9241-x CrossRefGoogle Scholar
  57. Parsa S, Ortiz V, Vega FE (2013) Establishing fungal entomopathogens as endophytes: towards endophytic biological control. J Vis Exp 74:e50360.  https://doi.org/10.3791/50360 CrossRefGoogle Scholar
  58. Parsa S, Ortiz V, Gómez-Jiménez MI, Kramer M, Vega FE (2018) Root environment is a key determinant of fungal entomopathogen endophytism following seed treatment in the common bean, Phaseolus vulgaris. Biol Control 116:74–81.  https://doi.org/10.1016/j.biocontrol.2016.09.001 CrossRefPubMedPubMedCentralGoogle Scholar
  59. Patiño-Ruiz JD, Schausberger P (2014) Spider mites adaptively learn recognizing mycorrhiza-induced changes in host plant volatiles. Exp Appl Acarol 64:455–463.  https://doi.org/10.1007/s10493-014-9845-4 CrossRefPubMedGoogle Scholar
  60. Quesada-Moraga E, Muñoz-Ledesma F, Santiago-Alvarez C (2009) Systemic protection of Papaver somniferum L. against Iraella luteipes (Hymenoptera: Cynipidae) by an endophytic strain of Beauveria bassiana (Ascomycota: Hypocreales). Environ Entomol 38:723–730.  https://doi.org/10.1603/022.038.0324 CrossRefPubMedGoogle Scholar
  61. Raworth DA (1986) An economic threshold function for the twospotted spider mite, Tetranychus urticae (Acari: Tetranychidae), on strawberries. Can Entomol 118:9–16.  https://doi.org/10.4039/Ent1189-1 CrossRefGoogle Scholar
  62. Rehner SA (2005) Phylogenetics of the insect pathogenic genus Beauveria. In: Vega FE, Blackwell M (eds) Insect fungal associations: ecology and evolution, 1st edn. University Press, New York, pp 3–27Google Scholar
  63. Rehner SA, Buckley EP (2005) A Beauveria phylogeny inferred from ITS and EF1-a sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. Mycologia 97:84–98.  https://doi.org/10.3852/mycologia.97.1.84 CrossRefPubMedGoogle Scholar
  64. Rezende JM, Zanardo ABR, Lopes MD, Delalibera I Jr, Rehner SA (2015) Phylogenetic diversity of Brazilian Metarhizium associated with sugarcane agriculture. Biocontrol 60:495–505.  https://doi.org/10.1007/s10526-015-9656-5 CrossRefGoogle Scholar
  65. Rhodes EM, Liburd OE, Kelts C, Rondon SI, Francis RR (2006) Comparison of single and combination treatments of Phytoseiulus persimilis, Neoseiulus californicus, and Acramite (bifenazate) for control of twospotted spider mites in strawberries. Exp Appl Acarol 39:213–225.  https://doi.org/10.1007/s10493-006-9005-6 CrossRefPubMedGoogle Scholar
  66. Rowell HJ, Chant DA, Hansell R (1978) The determination of setal homologies and setal patterns on the dorsal shield in the family Phytoseiidae (Acarina: Mesostigmata). Can Entomol 110(8):859–876.  https://doi.org/10.4039/Ent110859-8 CrossRefGoogle Scholar
  67. Sabbahi R, Merzouki A, Guertin C (2008) Efficacy of Beauveria bassiana against the strawberry pests, Lygus lineolaris, Anthonomus signatus and Otiorhynchus ovatus. J Appl Entomol 132:151–160.  https://doi.org/10.1111/j.1439-0418.2007.01248.x CrossRefGoogle Scholar
  68. Sances FV, Wyman JA, Ting IP (1979) Physiological responses to spider mite infestation on strawberries. Environ Entomol 8:711–714.  https://doi.org/10.1093/ee/8.4.711 CrossRefGoogle Scholar
  69. Sances FV, Toscano NC, Oatman ER, Lapre LF, Johnson MW, Voth V (1982) Reductions in plant processes by Tetranychus urticae (Acari: Tetranychidae) feeding on strawberry. Environ Entomol 11:733–737.  https://doi.org/10.1093/ee/11.3.733 CrossRefGoogle Scholar
  70. Sánchez-Rodríguez AR, Raya-Díaz S, Zamarreño ÁM, García-Mina JM, Campillo MC, Quesada-Moraga E (2018) An endophytic Beauveria bassiana strain increases spike production in bread and durum wheat plants and effectively controls cotton leafworm (Spodoptera littoralis) larvae. Biol Control 116:90–102.  https://doi.org/10.1016/j.biocontrol.2017.01.012 CrossRefGoogle Scholar
  71. Sasan RK, Bidochka MJ (2013) Antagonism of the endophytic insect pathogenic fungus Metarhizium robertsii against the bean plant pathogen Fusarium solani f. sp. phaseoli. Can J Plant Pathol 35:288–293.  https://doi.org/10.1080/07060661.2013.823114 CrossRefGoogle Scholar
  72. Sato ME, Da Silva MZ, Raga A, De Souza Filho MF (2005) Abamectin resistance in Tetranychus urticae Koch (Acari Tetranychidae): selection, cross-resistance and stability of resistance. Neotrop Entomol 34:991–998.  https://doi.org/10.1590/S1519-566X2005000600016 CrossRefGoogle Scholar
  73. Schausberger P, Peneder S, Juerschik S, Hoffmann D (2012) Mycorrhiza changes plant volatiles to attract spider mite enemies. Funct Ecol 26:441–449.  https://doi.org/10.1111/j.1365-2435.2011.01947.x CrossRefGoogle Scholar
  74. Solomon MG, Jay CN, Innocenzi PJ, Fitzgerald JD, Crook D, Crook AM, Easterbrook MA, Cross JV (2001) Review: natural enemies and biocontrol of pests of strawberry in Northern and Central Europe. Biocontrol Sci Technol 11:165–216.  https://doi.org/10.1080/09583150120035639 CrossRefGoogle Scholar
  75. Stone JK, Polishook JD, White JRJ (2004) Endophytic fungi. In: Mueller G, Bills GF, Foster MS (eds) Biodiversity of fungi: inventory and monitoring method, 1st edn. Elsevier, USA, pp 241–270CrossRefGoogle Scholar
  76. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 2 Nov 2018
  77. Tixier M-S, Guichou S, Kreiter S (2008) Morphological variation in the biological control agent Neoseiulus californicus (McGregor) (Acari: Phytoseiidae): consequences for diagnostic reliability and synonymies. Invertebr Syst 22:453–469.  https://doi.org/10.1071/IS07052 CrossRefGoogle Scholar
  78. Van Leeuwen T, Vontas J, Tsagkarakou A (2009) Mechanisms of acaricide resistance in the two spotted spider mite Tetranychus urticae. In: Ishaaya I, Horowitz AR (eds) Biorational control of arthropod pests, 1st edn. Springer, The Netherlands, pp 347–393CrossRefGoogle Scholar
  79. Van Leeuwen T, Vontas J, Tsagkarakou A, Dermauwa W, Tirry L (2010) Acaricide resistance mechanisms in the two-spotted spider mite Tetranychus urticae and other important Acari: a review. Insect Biochem Mol Biol 40:563–572.  https://doi.org/10.1016/j.ibmb.2010.05.008 CrossRefPubMedGoogle Scholar
  80. Vega FE (2008) Insect pathology and fungal endophytes. J Invertebr Pathol 98:277–279.  https://doi.org/10.1016/j.jip.2008.01.008 CrossRefPubMedGoogle Scholar
  81. Vega FE (2018) The use of fungal entomopathogens as endophytes in biological control: a review. Mycologia 110:4–30.  https://doi.org/10.1080/00275514.2017.1418578 CrossRefPubMedGoogle Scholar
  82. Vega FE, Goettel MS, Blackwell M, Chandler D, Jackson MA, Keller S, Koike M, Maniania NK, Monzón A, Ownley BH, Pell JK, Rangel DEN, Roy HE (2009) Fungal entomopathogens: new insights on their ecology. Fungal Ecol 2:149–159.  https://doi.org/10.1016/j.funeco.2009.05.001 CrossRefGoogle Scholar
  83. Vidal S, Jaber LR (2015) Entomopathogenic fungi as endophytes: plant-endophyte-herbivore interactions and prospects for use in biological control. Curr Sci 109:46–54Google Scholar
  84. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New YorkCrossRefGoogle Scholar
  85. Yan J, Broughton S, Yang S, Gange A (2015) Do endophytic fungi grow through their hosts systemically? Fungal Ecol 13:53–59.  https://doi.org/10.1016/j.funeco.2014.07.005 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Entomology and Acarology“Luiz de Queiroz” College of Agriculture/University of São Paulo (ESALQ/USP)PiracicabaBrazil
  2. 2.Department of Plant and Environmental SciencesUniversity of CopenhagenFrederiksberg CDenmark
  3. 3.Biotechnology and Plant Health DivisionNorwegian Institute of Bioeconomy (NIBIO)ÅsNorway
  4. 4.Department of Mathematics and StatisticsMaynooth UniversityMaynoothIreland

Personalised recommendations