Abstract
Rhizoglyphus robini Claparède (Acari: Acaridae) is a pest of bulbs, corms and tubers of several economically important crops. The biological control of R. robini has yet to be fully explored as an alternative to chemical pesticides. Entomopathogenic fungi in the genera Metarhizium (Hypocreales: Clavicipitaceae) are used for the biological control of several agricultural pests. The soil-dwelling predatory mite, Stratiolaelaps scimitus (Womersley) (Acari: Acaridae) is also frequently used alone or in combination with other biological control agents. There are few reports on the use of M. brunneum or S. scimutus against R. robini. The objectives of this research were to investigate the in vitro effect of different predatory mite ratios of S. scimitus on R. robini mortality and the combined use of a M. brunneum-based granule with S. scimitus as potential strategies to manage this pest. Mortality of R. robini in Petri dishes containing predators was significantly higher than without predators. When soil-filled containers containing R. robini were treated with both M. brunneum granules and S. scimitus, the lower densities of the bulb mite were obtained with the highest ratio of predator/prey mites. The number of bulb mites in the containers treated with only M. brunneum was significantly lower than the untreated control. These results demonstrate the potential for releasing of S. scimitus alone and in combination with M. brunneum granules to manage R. robini.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data that support this study findings are available from the corresponding author, upon reasonable request.
Code availability
Not applicable.
References
Acharya R, Hwang HS, Shim JK, Yu YS, Lee KY (2019) Control efficacy of fungus gnat, Bradysia impatiens, enhanced by a combination of entomopathogenic nematodes and predatory mites. Biol Control 138:1–6. https://doi.org/10.1016/j.biocontrol.2019.104071
Ali W, George DR, Shiel RS, Sparagano OA, Guy JH (2012) Laboratory screening of potential predators of the poultry red mite (Dermanyssus gallinae) and assessment of Hypoaspis miles performance under varying biotic and abiotic conditions. Vet Parasitol 187:341–344. https://doi.org/10.1016/j.vetpar.2012.01.014
Behle RW, Goett EJ (2016) Dosage response mortality of Japanese beetle, masked chafer, and june beetle (Coleoptera: Scarabaeidae) adults when exposed to experimental and commercially available granules containing Metarhizium brunneum. J Econ Entomol 109:1109–1115. https://doi.org/10.1093/jee/tov176
Bayram S, Çobanoglu S (2006) Astigmata and Prostigmata (Acari) of bulbaceous ornamental plants in Ankara, Turkey. Acta Phytopathol Entomol Hung 41:367–381. https://doi.org/10.1556/aphyt.41.2006.3-4.19
Chandler D, Davidson G, Pell JK, Ball BV, Shaw K, Sunderland KD (2000) Fungal biocontrol of acari. Biocontrol Sci Technol 10:357–384. https://doi.org/10.1080/09583150050114972
Díaz A, Okabe K, Eckenrode C et al (2000) Biology, ecology, and management of the bulb mites of the genus Rhizoglyphus (Acari: Acaridae). Exp Appl Acarol 24:85–113. https://doi.org/10.1023/A:1006304300657
Faria MR, Wraight SP (2007) Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256. https://doi.org/10.1016/j.biocontrol.2007.08.001
Flor-Weiler LB, Behle RW, Johnson ET, Strickman DA, Rooney AP (2019) Evaluation of a granular formulation containing Metarhizium brunneum F52 (Hypocreales: Clavicipitaceae) microsclerotia in controlling eggs of Aedes aegypti (Diptera: Culicidae). Biocontrol Sci Technol 29:68–82. https://doi.org/10.1080/09583157.2018.1530342
Gerson U, Weintraub PG (2007) Mites for the control of pests in protected cultivation. Pest Manag Sci 63:658–676. https://doi.org/10.1002/ps.1380
Ghalehgolabbehbahani A, Skinner M, Parker BL et al (2021) A standardized method for rearing Rhizoglyphus robini (Astigmata: Acaridae). J Plant Dis Prot 128:623–626. https://doi.org/10.1007/s41348-020-00381-3
Goettel MS, Inglis DG (1997) Fungi: Hyphomycetes. In: Lacey L (ed) Manual of Techniques in Insect Pathology. Academic Press, London, UK, pp 213–249
Hoda EM, Taha HA, Ibrahim GA, E-Beheri MM (1986) Biological observations on the predatory mite Hypoaspis miles Berlese (Acarina: Laelapidae). Bull Soc Entomol D’egypte 66:103–106
Jaronski ST, Jackson MA (2008) Efficacy of Metarhizium anisopliae microsclerotial granules. Biocontrol Sci Technol 18:849–863. https://doi.org/10.1080/09583150802381144
Kim S, Kim JC, Lee SJ, Lee MR, Park SE, Li D, Baek S, Shin TY, Gasmi L, Kim JS (2020) Soil application of Metarhizium anisopliae JEF-314 granules to control, flower chafer beetle, Protaetia brevitarsis seulensis. Mycobiology 48:139–147. https://doi.org/10.1080/12298093.2020.1735765
Knapp M, van Houten Y, van Baal E, Groot T (2018) Use of predatory mites in commercial biocontrol: current status and future prospects. Acarologia 58:72–82. https://doi.org/10.24349/acarologia/20184275
Kasuga S, Honda KI (2006) Suitability of organic matter, fungi and vegetables as food for Tyrophagus similis (Acari: Acaridae). Appl Entomol Zool 41:227–231. https://doi.org/10.1303/aez.2006.227
Lesna IKA, Sabelis MW, Bolland HR, Conijn CGM (1995) Candidate natural enemies for control of Rhizoglyphus robini Claparede (Acari: Astigmata) in lily bulbs: exploration in the field and preselection in the laboratory. Exp Appl Acarol 19:655–669. https://doi.org/10.1007/BF00145254
Lesna I, Sabelis M, Conijn C (1996) Biological Control of the Bulb Mite, Rhizoglyphus robini, by the Predatory Mite, Hypoaspis aculeifer, on lilies: predator-prey interactions at various spatial scales. J Appl Ecol 33:369–376. https://doi.org/10.2307/2404758
Lesna I, Conijn CGM, Sabelis MW, van Straalen NM (2000) Biological control of the bulb mite, Rhyzoglyphus robini, by the predatory mite, Hypoaspis aculeifer, on lilies: predator-prey dynamics in soil, under greenhouse and field conditions. Biocontrol Sci Technol 10:179–193. https://doi.org/10.1080/09583150029314
Ment D, Raman S, Gal S, Ezra D, Palevsky E (2020) Interactions of Metarhizium brunneum-7 with phytophagous mites following different application strategies. Insects 11:1–15. https://doi.org/10.3390/insects11060330
Midthassel A, Leather SR, Wright DJ, Baxter IH (2016) Compatibility of Amblyseius swirskii with Beauveria bassiana: two potentially complimentary biocontrol agents. Biocontrol 61:437–447. https://doi.org/10.1007/s10526-016-9718-3
Okabe K, Amano H (1990) Attractancy of alcohols isolated from culture filtrates of Fusarium fungi for the robine bulb mite, Rhizoglyphus robini Claparede (Acari: Acaridae), in sand. Appl Entomol Zool 25:397–404
Okabe K, Amano H (1991) Penetration and population growth of the robine bulb mite, Rhizoglyphus robini Claparede (Acari: Acaridae), on healthy and Fusarium-infected rakkyo bulbs. Appl Entomol Zool 26:129–136. https://doi.org/10.1303/aez.26.129
Rahimi H, Arbabi M (2006) Effect of corm and soil Acaricide treatment on the control of bulb mites (Rhizoglyphus robini Claparede; Acari: Acaridae) in saffron fields of Khorassan, IRAN. 2nd International Symposium on Saffron and Technology, Mashhad, Iran.
Rondeau S, Giovenazzo P, Fournier V (2018) Risk assessment and predation potential of Stratiolaelaps scimitus (Acari: Laelapidae) to control Varroa destructor (Acari: Varroidae) in honey bees. PLoS ONE 13:e0208812. https://doi.org/10.1371/journal.pone.0208812
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. https://doi.org/10.1016/j.biocontrol.2015.10.003
Saito T, Brownbridge M (2018) Compatibility of foliage-dwelling predatory mites and mycoinsecticides, and their combined efficacy against western flower thrips Frankliniella occidentalis. J Pest Sci 91:1291–1300. https://doi.org/10.1007/s10340-018-0991-z
Shereef GM, Soliman ZR, Atifi AM (1981) Economic importance of the mite Hypoaspis miles (Mesostigmata: Laelapidae) and its life history. Zool Soe Egypt Bull 30:103–108
Shipp L, Kapongo JP, Park HH, Kevan P (2012) Effect of bee-vectored Beauveria bassiana on greenhouse beneficials under greenhouse cage conditions. Biol Control 63:135–142. https://doi.org/10.1016/j.biocontrol.2012.07.008
Skinner M, Gouli S, Frank CE, Parker BL, Kim JS (2012) Management of Frankliniella occidentalis (Thysanoptera: Thripidae) with granular formulations of entomopathogenic fungi. Biol Control 63:246–252. https://doi.org/10.1016/j.biocontrol.2012.08.004
Sullivan CF, Kim PBL, M, Skinner (2021) Effectiveness of granular formulations of Metarhizium anisopliae and Metarhizium brunneum (Hypocreales: Clavicipitaceae) on off-host larvae of Dermacentor albipictus (Acari: Ixodidae). Biocontrol Sci Tech 31:1113–1127. https://doi.org/10.1080/09583157.2021.1926428
Sullivan CF, Parker BL, Davari A, Lee MR, Kim JS, Skinner M (2020) Pathogenicity of Metarhizium anisopliae and Metarhizium brunneum isolates and efficacy of Met52 G against winter tick larvae, 2019. Arthropod Manag Tests 45:1–3. https://doi.org/10.1093/amt/tsaa100
Summerell BA (2019) Resolving Fusarium: Current status of the genus. Annu Rev Phytopathol 57:323–339. https://doi.org/10.1146/annurev-phyto-082718-100204
Sun W, Sarkar SC, Xu X, Lei Z, Wu S, Meng R (2018) The entomopathogenic fungus Beauveria bassiana used as granules has no impact on the soil-dwelling predatory mite Stratiolaelaps scimitus. Syst Appl Acarol 23:2165–2172
Walter DE, Campbell NJH (2003) Exotic vs endemic biocontrol agents: would the real Stratiolaelaps miles (Berlese) (Acari: Mesostigmata: Laelapidae), please stand up? Biol Control 26:253–269. https://doi.org/10.1016/s1049-9644(02)00171-8
Wang J, Lei ZR, Xu HF, Gao YL (2011) Virulence of Beauveria bassiana isolates against the first instar nymphs of Frankliniella occidentalis and effects on natural enemy Amblyseius barkeri. Chin J Biol Control 27:479–484
Wright EM, Chambers RJ (1994) The biology of the predatory mite Hypoaspis miles (Acari: Laelapidae), a potential biological control agent of Bradysia paupera (Dipt.: Sciaridae). Entomophaga 39:225–235. https://doi.org/10.1007/BF02372360
Yang SH, Wang D, Chen C, Xu CL, Xie H (2020) Evaluation of Stratiolaelaps scimitus (Acari: Laelapidae) for controlling the root-knot nematode, Meloidogyne incognita (Tylenchida: Heteroderidae). Sci Rep. https://doi.org/10.1038/s41598-020-62643-2
Zhang XR, Wu SY, Reitz SR, Gao YL (2021) Simultaneous application of entomopathogenic Beauveria bassiana granules and predatory mites Stratiolaelaps scimitus for control of western flower thrips, Frankliniella occidentalis. J Pest Sci 94:119–127. https://doi.org/10.1007/s10340-020-01227-5
Acknowledgements
This research was supported with funds from the University of Vermont College of Agriculture and Life Sciences through a US Department of Agriculture, National Institute of Food and Agriculture, multi-state Hatch project (#W4185, VT-H02405MS). The authors thank Brian Spencer from Applied Bio-nomics, Ltd. for providing the predatory mites and the anonymous reviewers for their helpful comments and suggestions on this manuscript. Any findings, opinions, conclusions or recommendations expressed herein are those of the authors and do not necessarily reflect the views of the US Department of Agriculture.
Funding
This research was supported with funds from the US Department of Agriculture Hatch program (Project VT-HO2405MS) and the University of Vermont Experiment Station. It is part of the USDA Regional Project W4185, Biological Control in Pest Management Systems of Plants.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Ghalehgolabbehbahani, A., Sullivan, C.F., Davari, A. et al. Evaluation of the entomopathogenic fungus Metarhizium brunneum and the predatory mite Stratiolaelaps scimitus against Rhizoglyphus robini under laboratory conditions. Exp Appl Acarol 87, 19–29 (2022). https://doi.org/10.1007/s10493-022-00719-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10493-022-00719-6