Open Access Open Access  Restricted Access Subscription Access


DOI: http://dx.doi.org/10.11158/saa.23.11.10

The pathogenicity of entomopathogenic fungus Acremonium hansfordii to two-spotted spider mite, Tetranychus urticae and predatory mite Neoseiulus barkeri

Su-Qin Shang, Yao-Nian Chen, Ying-Lu Bai

Abstract


The two-spotted spider mite, Tetranychus urticae, is an important mite pest worldwide. It often leads to reduced crop yields or poor marketability of the produce and has already developed resistance to many acaricides. In this study, the pathogenicity of the entomopathogenic fungus (EPF), Acremonium hansfordii, to T. urticae and its side effects on the predatory mite Neoseiulus barkeri were compared. The toxicity of A. hansfordii was evaluated on T. urticae at 1.0×104, 1.0×106, 1.0×108 conidia/mL concentrations and predatory mite N. barkeri at 1.0×108 conidia/mL under experimental conditions at 25±1°C, 75±5% RH and 16L: 8D photoperiod. The effects of EPF on the development of the F0 and F1 generation of predatory mites were also assessed at 1.0×108 conidia/mL concentration. The results showed that the corrected mortality of T. urticae at three tested concentrations were 36.67%, 53.67% and 66.33% within 11d, and the median lethal time were 14.39 d, 9.84d and 7.99d, respectively. The corrected mortality of N. barkeri was only 3.9% after 11d at 1×108 conidia/mL concentration. Some hyphae of A. hansfordii were detected on the surface of treated T. urticae but not on N. barkeri body after 7d. After N. barkeri females were treated with 1.0×108 conidia/mL, the preoviposition period of the F0 generation was prolonged 1.56 times and the other life history parameters have no significant differences; similar patterns were also shown in the F1 generation. A. hansfordii showed strong pathogenicity against T. urticae but did not significantly adversely influence N. barkeri. Therefore, the combination of A. hansfordii and N. barkeri has the potential to be used for the control of T. urticae in the future. 


Keywords


Acremonium hansfordii, Neoseiulus barkeri, Tetranychus urticae, corrected mortality, median lethal time, life history parameters, biocontrol

References


Afifi, A.M., Ali, F.S., El-Saiedy, E.M.A. & Ahmed, M.M. (2015) Compatibility and integration of some control methods for controlling Tetranychus urticae Koch infesting tomato plants in Egypt. Egyptian Journal of Biological Pest Control, 25, 75–82.

Ahn, J.J., Kim, K.W. & Lee, J.H. (2010) Functional response of Neoseiulus californicus (Acari: Phytoseiidae) to Tetranychus urticae (Acari: Tetranychidae) on strawberry leaves. Journal of Applied Entomology, 134, 98–104.

https://doi.org/10.1111/j.1439-0418.2009.01440.x

Alzoubi, S. & Çobanoǧlu, S. (2010) Integrated control possibilities for two-spotted spider mite Tetranychus urticae Koch (Acarina: Tetranychidae) on greenhouse cucumber. International Journal of Acarology, 36, 259–266.

https://doi.org/10.1080/01647951003669000

Ambikadevi, D. & Samarjit, R. (1997) Chemical control of red spider mite Tetranychus cinnabarinus (Boisduval) on okra. Journal of Tropical Agriculture, 35, 38–40.

Bugeme, D.M., Knapp, M., Ekesi, S., Chabi-Olaye, A., Boga, H.I. & Maniania, N.K. (2015) Efficacy of Metarhizium anisopliae in controlling the two-spotted spider mite. Insect Science, 22, 121–128.

https://doi.org/10.1111/1744-7917.12111

Bugeme, D.M., Knapp, M., Boga, H.I., Ekesi, S. & Maniania, N.K. (2014) Susceptibility of developmental stages of Tetranychus urticae (Acari: Tetranychidae) to infection by Beauveria bassiana and Metarhizium anisopliae (Hypocreales: Clavicipitaceae). International Journal of Tropical Insect Science 34, 190–196.

https://doi.org/10.1007/s11046-008-9164-6

Bugeme, D.M., Knapp, M., Boga, H.I., Wanjoya, A.K. & Maniania, N.K. (2009) Influence of temperature on virulence of fungal isolates of Metarhizium anisopliae and Beauveria bassiana to the two-spotted spider mite Tetranychus urticae. Mycopathologia, 167, 221–227.

Butt, T., Coates, C., Dubovskiy, I. & Ratcliffe, N. (2016) Chapter nine-entomopathogenic fungi: new insights into host-pathogen interactions. Advances Genetics. 94, 307–364.

https://doi.org/10.1016/bs.adgen.2016.01.006

Çakmak, I., Başpınar, H. & Madanlar, N. (2003) Aydin ilinde örtü altı çilek alanlannda zararlı kırmızıörümcekler ve doğal duşmanlarının populasyon yoğunlukları. Türkiye Entomoloji Dergisi, 27, 191–205.

Çakmak, I., Başpinar, H. & Madanlar, N. (2005) Control of the carmine spider mite Tetranychus cinnabarinus boisduval by the predatory mite Phytoseiulus persimilis (Athias-Henriot) in protected strawberries in Aydin, Tukey. Turkish Journal of Agriculture and Forestry, 29, 259–265.

Chen, Y.N., Ru, Y. & Shang, S.Q. (2016) Predatory functional response of Neoseiulus barkeri on mixture resistance strain and susceptible strain of Tetranychus urticae Koch. Chinese Journal of Biological Control, 32, 428–433.

Chandler, D., Davidson, G. & Jacobson, R.J. (2005) Laboratory and glasshouse evaluation of entomopathogenic fungi against the two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae), on tomato, Lycopersicon esculentum. Biocontrol Science and Technology, 15, 37–54.

https://doi.org/10.1080/09583150410001720617

Dogan, Y.O., Hazir, S., Yildiz, A., Butt, T.M. & 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). Biological Control, 111, 6–12.

https://doi.org/10.1016/j.biocontrol.2017.05.001

Döker, İ., Kazak, C. & Karut, K. (2016) Functional response and fecundity of a native Neoseiulus californicus population to Tetranychus urticae (Acari: Phytoseiidae, Tetranychidae) at extreme humidity conditions. Systematic and Applied Acarology, 21(11), 1463–1472.

https://doi.org/10.11158/saa.21.11.3

Erler, F., Ates, A.O. & Bahar, Y. (2013) Evaluation of two entomopathogenic fungi, Beauveria bassiana and Metarhizium anisopliae, for the control of carmine spider mite, Tetranychus cinnabarinus (Boisduval) under greenhouse conditions. Egyptian Journal of Biological Pest Control, 23, 233–240.

Faria, M. & Wraight, S.P. (2001) Biological control of Bemisia tabaci with fungi. Crop Protection, 20, 767–778.

https://doi.org/10.1016/S0261-2194(01)00110-7

Farish, D.J. (1972) The evolutionary implications of qualitative variation in the grooming behaviour of the Hymenoptera (Insecta). Animal Behaviour, 20, 662–676.

https://doi.org/10.1016/S0003-3472(72)80139-8

Fathipour, Y., Karimi, M., Farazmand, A. & Talebi, A.A. (2017) Age-specific functional response and predation rate of Amblyseius swirskii (Phytoseiidae) on two-spotted spider mite. Systematic and Applied Acarology, 22(2), 159–169.

https://doi.org/10.11158/saa.22.2.1

Gao, Y.L., Reitz, S.R., Wang, J., Tamez-Guerra, P., Wang, E.G., Xu, X.N. & Lei, Z.R. (2012) Potential use of the fungus Beauveria bassiana against the western flower thrips Frankliniella occidentalis without reducing the effectiveness of its natural predator Orius sauteri (Hemiptera: Anthocoridae). Biocontrol Science and Technology, 22, 803–812.

https://doi.org/10.1080/09583157.2012.691158

Gatarayiha, M.C., Laing, M.D. & Miller, R.M. (2010a) Effects of adjuvant and conidial concentration on the efficacy of Beauveria bassiana for the control of the two spotted spider mite, Tetranychus urticae. Experimental and Applied Acarology, 50, 217–229.

https://doi.org/10.1007/s10493-009-9307-6

Gatarayiha, M.C., Laing, M.D. & Miller, R.M. (2010b) In vitro effects of flutriafol and azoxystrobin on Beauvaria bassiana and its efficacy against Tetranychus urticae. Pest Management Science, 66, 773–778.

https://doi.org/10.1002/ps.1941

Glockemann, B. (1992) Biological controll of Frankhiella occidentais on ornamental plants using predatory mites. 102, 1995–2002.

Hountondji, F.C.C., Yaninek, J.S., De Moraes, G.J. & Oduor, G.I. (2002) Host specificity of the cassava green mite pathogen Neozygites floridana. BioControl, 47, 61–66.

https://doi.org/10.1023/A:1014438220511

Inglis, G.D., Goettel, M.S., Butt, T.M. & Strasser, H. (2001) Use of Hyphomycetous fungi for managing insect pests. In: Butt, T.M., Jachsonand, C. & Magan, N. (eds) Fungi as biocontrol agents: Progress problems and potential. Wallingford, CABI Publishing, pp. 23–69.

Jacobson, R.J., Chandler, D., Fenlon, J. & Russell, K.M. (2001) Compatibility of Beauveria bassiana (Balsamo) Vuillemin with Amblyseius cucumeris Oudemans (Acarina: Phytoseiidae) to control Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) on cucumber plants. Biocontrol Science and Technology, 11, 391–400.

https://doi.org/10.1080/09583150120055808

Jarosik, V. & Pliva, J. (1995) Assessment of Amblyseius barkeri (Acarina: Phytoseiidae) as a control agent for thrips on greenhouse cucumbers. Acta Societatis Zoologicae Bohemicae, 59, 177–186.

Jiang, L.B., Zhao, Y.D., Zhou, X.L. & Shen, H.M. (2012) Biocompatibility between Acremonium hansrordii and common acaricides and the synergistic effect. Plant Protection, 38, 73–77.

Khaliq, A., Afzal, M., Raza, A.M., Kamran, M., Khan, A.A., Aqeel, M.A., Ullah, M.I., Khan, B.S. & Kanwal, H. (2018) Suitability of Thrips tabaci L. (Thysonaptera: Thripidae) as prey for the phytoseiid mite, Neoseiulus barkeri Hughes (Acari: Phytoseiidae). African Entomology, 26, 131–135.

Khanamani, M., Fathipour, Y., Asghar Talebi, A. & Mehrabadi, M. (2017) How pollen supplementary diet affect life table and predation capacity of Neoseiulus californicus on two-spotted spider mite. Systematic and Applied Acarology, 22(1), 135–147.

https://doi.org/10.11158/saa.22.1.14

Khodayari, S., Fathipour, Y. & Sedaratian, A. (2016) Prey stage preference, switching and mutual interference of Phytoseius plumifer (Acari: Phytoseiidae) on Tetranychus urticae (Acari: Tetranychidae). Systematic and applied acarology, 21(3), 347–355.

https://doi.org/10.11158/saa.21.3.9

Knapp, M. & Kashenge, S.S. (2003) Effects of different neem formulations on the two spotted spider mite, Tetranychus urticae Koch, ontomato (Lycopersicon esculentum Mill.). Insect Science and Its Application, 23, 1–7.

Lahai, M.T., Ekanayake, I.J. & George, J.B. (1998) Leaf harvesting effects on leaf retention and pest and disease incidence of cassava (Manihot esculenta Crantz). African Crop Science Journal, 11,107–117.

Li, Y.Y., Fan, X., Zhang, G.H., Liu, Y.Q., Chen, H.Q., Liu, H. & Wang, J.J. (2017) Sublethal effects of bifenazate on life history and population parameters of Tetranychus urticae (Acari: Tetranychidae). Systematic and Applied Acarology, 22(1), 148–158.

https://doi.org/10.11158/saa.22.1.15

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. Biological Control, 115, 105–111.

https://doi.org/10.1016/j.biocontrol.2017.09.012

Liu, P., Shang, S.Q. & Zhang, X.H. (2014) Virulence and selective toxicity of nine kinds of acaricides to Neoseiulus barkeri Hughes and Tetranychus urticae Koch. Plant Protection, 40, 181–184.

Ludwig, S.W. & Oetting, R.D. (2001) Susceptibility of natural enemies to infection by Beauveria bassiana and impact of insecticides on Ipheseius degenerans (Acari : Phytoseiidae). Journal of Agricultural and Urban Entomology, 18, 169–178.

Maniania, N.K., Bugeme, D.M., Wekesa, V.W., Delalibera, I. Jr. & Knapp, M. (2008) Role of entomopathogenic fungi in the control of Tetranychus evansi and Tetranychus urticae (Acari: Tetranychidae) pests of horticultural crops. Experimental and Applied Acarology, 46, 256–274.

https://doi.org/10.1007/s10493-008-9180-8

Međo, I., Stojnić, B. & Marčić, D. (2017) Acaricidal activity and sublethal effects of the microbial pesticide spinosad on Tetranychus urticae (Acari: Tetranychidae). Systematic and Applied Acarology, 22(10), 1748–1762.

https://doi.org/10.11158/saa.22.10.14

Meyling, N.V. & Pell, J.K. (2006) Detection and avoidance of an entomopathogenic fungus by a generalist insect predator. Ecological Entomology, 31, 162–171.

http://dx.doi.org/10. 1111/j.0307-6946.2006.00781.x

Mortazavi, N., Fathipour, Y. & Talebi, A.A. (2017) Interactions between two-spotted spider mite, Tetranychus urticae and greenhouse whitefly, Trialeurodes vaporariorum on strawberry. Systematic and Applied Acarology, 22(12), 2083–2092.

https://doi.org/10.11158/saa.22.12.5

Numa Vergel, S.J., Bustos, R.A., Rodríguez, C.D. & Cantor, R.F. (2011) Laboratory and greenhouse evaluation of the entomopathogenic fungi and garlic-pepp er extract on the predatory mites, Phytoseiulus persimilis and Neoseiulus californicus and their effect on the spider mite Tetranychus urticae. Biological Control, 57, 143–149.

https://doi.org/10.1016/j.biocontrol.2011.02.007

Onzo, A., Bello, I.A. & Hanna, R. (2013) Effects of the entomopathogenic fungus Neozygites tanajoae and the predatory mite Typhlodromalus aripo on cassava green mite densities: Screenhouse experiments. BioControl, 58, 397–405.

https://doi.org/10.1007/s10526-013-9508-0

Parsad, R. (2010) Some statistical techniques for bio-efficacy trials. 16, 62–76.

Pozzebon, A., Boaria, A. & Duso, C. (2015) Single and combined releases of biological control agents against canopy- and soil-dwelling stages of Frankliniella occidentalis in cyclamen. BioControl, 60, 341–350.

https://doi.org/10.1007/s10526-014-9641-4

Reichert, M.B., Toldi, M. & Ferla, N.J. (2016) Feeding preference and predation rate of Neoseiulus idaeus (Acari: Phytotseiidae) feeding on different preys. Systematic and Applied Acarology, 21(12), 1631–1640.

https://doi.org/10.11158/saa.21.12.4

Riahi, E., Fathipour, Y., Talebi, A.A. & Mehrabadi, M. (2017) Natural diets versus factitious prey: comparative effects on development, fecundity and life table of Amblyseius swirskii (Acari: Phytoseiidae). Systematic and Applied Acarology, 22(5), 711–723.

https://doi.org/10.11158/saa.22.5.10

Riahi, E., Fathipour, Y., Talebi, A.A. & Mehrabadi, M. (2016) Pollen quality and predator viability: life table of Typhlodromus bagdasarjani on seven different plant pollens and two-spotted spider mite. Systematic and Applied Acarology, 21(10), 1399–1412.

https://doi.org/10.11158/saa.21.10.10

Premachandra, W.T.S.D., Borgemeister, C., Berndt, O., Ehlers, R.-U. & Poehling, H.-M. (2003) Combined releases of entomopathogenic nematodes and the predatory mite Hypoaspis aculeifer to control soil-dwelling stages of western flower thrips Frankliniella occidentalis. BioControl, 48, 529–541.

https://doi.org/10.1023/A:1025703512113

Saber, M., Ahmadi, Z. & Mahdavinia, G. (2018) Sublethal effects of spirodiclofen, abamectin and pyridaben on life-history traits and life-table parameters of two-spotted spider mite, Tetranychus urticae (Acari: Tetranychidae). Experimental and Applied Acarology, 75, 55–67.

https://doi.org/10.1007/s10493-018-0226-2

Sáenz-de-Cabezón Irigaray, F.J., Marco-Mancebón, V. & Pérez-Moreno, I. (2003) The entomopathogenic fungus Beauveria bassiana and its compatibility with triflumuron: effects on the two spotted spider mite Tetranychus urticae. Biological Control, 26, 168–173.

https://doi.org/10.1016/S1049-9644(02)00123-8

Saemi, S., Rahmani, H., Kavousi, A. & Chi, H. (2017) Group-rearing did not affect the life table and predation rate of Phytoseiulus persimilis (Acari: Phytoseiidae) fed on Tetranychus urticae. Systematic and Applied Acarology, 22(10), 1698–1714.

https://doi.org/10.11158/saa.22.10.11

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 Science and Technology, 22, 873–882.

https://doi.org/10.1080/09583157.2012.695010

Seiedy, M., Saboori, A. & Zahedi-Golpayegani, A. (2013) Olfactory response of Phytoseiulus persimilis (Acari: Phytoseiidae) to untreated and Beauveria bassiana-treated Tetranychus urticae (Acari: Tetranychidae). Experimental and Applied Acarology, 60, 219–227.

https://doi.org/10.1007/s10493-012-9652-8

Seiedy, M. (2014) Feeding preference of Phytoseiulus persimilis Athias-Henriot (Acari: Phytoseiidae) towards untreated and Beauveria bassiana-treated Tetranychus urticae (Acari: Tetranychidae) on cucumber leaves. Persian Journal of Acarology, 3, 91–97.

Seiedy, M. (2015) Compatibility of Amblyseius swirskii (Acari: Phytoseiidae) and Beauveria bassiana for biological control of Trialeurodes vaporariorum (Hemiptera: Aleyrodidae). Systematics and Applied Acarology, 20, 731–738.

http://dx.doi.org/10.11158/saa.20.7.2.

Shang, S.Q., Liu, P., Chen, Y.N. & Zhang, X.H. (2017) Functional response and control potential of Neoseiulus barkeri to Tethanychus urticae. Plant Protection, 43, 118–121.

Shi, W.B. & Feng, M.G. (2004) Lethal effect of Beauveria bassiana, Metarhizium anisopliae, and Paecilomyces fumosoroseus on the eggs of Tetranychus cinnabarinus (Acari: Tetranychidae) with a description of a mite egg bioassay system. Biological Control, 30, 165–173.

https://doi.org/10.1016/j.biocontrol.2004.01.017

Song, L.W. (2006) Biological character and pathogenic mechanism of Acremonium hansfordii to aphid. Gansu Agriculture University. Dissertation, Gansu, Lanzhou.

Song, L.W., Yang, S.Y., Zhang, X.H. & Shen, H.M. (2007) A preliminary study on the nutritional conditions of Acremonium hansfordii. Plant Protection, 33, 67–70.

Song, Z.W., Zheng, Y., Zhang, B.X. & Li, D.S. (2016) Prey consumption and functional response of Neoseiulus californicus and Neoseiulus longispinosus (Acari: Phytoseiidae) on Tetranychus urticae and Tetranychus kanzawai (Acari: Tetranychidae). Systematic and Applied Acarology, 21(7), 936–946.

https://doi.org/10.11158/saa.21.7.7

St. Leger, R.J., Allee, L.L., Mai, B., Staples, R.C. & Roberts, D.W. (1992) Worldwide distribution of genetic variation among isolates of Beauveria spp. Mycological Research, 96, 1007–1115.

Ullah, M.S. & Lim, U.T. (2017a) Laboratory evaluation of the effect of Beauveria bassiana on the predatory mite Phytoseiulus persimilis (Acari: Phytoseiidae). Journal of Invertebrate Pathology, 148, 102–109.

https://doi.org/10.1016/j.jip.2017.06.006

Ullah, M.S. & Lim, U.T. (2017b) Synergism of Beauveria bassiana and Phytoseiulus persimilis in control of Tetranychus urticae on bean plants. Systematic and Applied Acarology, 22(11), 1924–1935.

https://doi.org/10.11158/saa.22.11.11

Wekesa, V.W., Moraes, G.J., Knapp, M. & Delalibera, I. (2007) Interactions of two natural enemies of Tetranychus evansi, the fungal pathogen Neozygites floridana (Zygomycetes: Entomophthorales) and the predatory mite, Phytoseiulus longipes (Acari: Phytoseiidae). Biological Control, 41, 408–414.

https://doi.org/10.1016/j.biocontrol.2007.03.003

Wu, S.Y., Gao, Y.L., Xu, X.N., Goettel, M.S. & Lei, Z.R. (2015) Compatibility of Beauveria bassiana with Neoseiulus barkeri for control of Frankliniella occidentalis. Journal of Integrative Agriculture, 14, 98–105.

https://doi.org/10.1016/S2095-3119(13)60731-5

Wu, S.Y., Gao, Y.L., Smagghe, G., Xu, X.N. & Lei, Z.R. (2016a) Interactions between the entomopathogenic fungus Beauveria bassiana and the predatory mite Neoseiulus barkeri and biological control of their shared prey/host Frankliniella occidentalis. Biological Control, 98, 43–51.

https://doi.org/10.1016/j.biocontrol.2016.04.001

Wu, S.Y., Gao, Y.L., Zhang, Y., Wang, E.G., Xu, X.N. & Lei, Z.R. (2014) An entomopathogenic strain of Beauveria bassiana against Frankliniella occidentalis with no detrimental effect on the predatory mite Neoseiulus barkeri: Evidence from laboratory bioassay and scanning electron microscopic observation. Plos One, 9, 1–8.

https://doi.org/10.1371/journal.pone.0084732

Wu, S.Y., He, Z., Wang, E.G., Xu, X.N. & Lei, Z.R. (2017) Application of Beauveria bassiana and Neoseiulus barkeri for improved control of Frankliniella occidentalis in greenhouse cucumber. Crop Protection, 96, 83–87.

https://doi.org/10.1016/j.cropro.2017.01.013

Wu, S.Y., Xie, H.C., Li, M.Y., Xu, X.N. & Lei, Z.R. (2016b) Highly virulent Beauveria bassiana strains against the two-spotted spider mite, Tetranychus urticae, show no pathogenicity against five phytoseiid mite species. Experimental and Applied Acarology, 70, 421–435.

https://doi.org/10.1007/s10493-016-0090-x

Zheng, Y., Clercq, P.D., Song, Z.W., Li, D.S. & Zhang, B.X. (2017) Functional response of two Neoseiulus species preying on Tetranychus urticae Koch. Systematic and Applied Acarology, 22(7), 1059–1068.

https://doi.org/10.11158/saa.22.7.13


Refbacks

  • There are currently no refbacks.


An international journal of the Systematic and Applied Acarology Society

ISSN 1362-1971