Grapevine Leaf Application of Steinernema yirgalemense to Control Planococcus ficus in Semi-field Conditions

T. Platt, N.F Stokwe, A.P. Malan


The vine mealybug, Planococcus ficus Signoret (Hemiptera: Pseudococcidae), is a key insect pest of South African grapevine. The ability of mealybugs to avoid or resist the action of chemical pesticides has led to the investigation of alternative control methods, such as the application of entomopathogenic nematodes (EPNs). However, EPN application faces challenges, due to the maladaptation of EPN species to aboveground conditions. In this study, the ability of adjuvants to improve the control of P. ficus in grapevine using an indigenous nematode species, Steinernema yirgalemense, was investigated. A trial was performed to assess EPN survival on grapevine foliage, when applied in the morning (high humidity / low temperature) compared with in the afternoon (high temperature / low humidity). In a semi-field trial, the combination of
adjuvants Zeba® and Nu-Film-P® resulted in 66% control of P. ficus after 48 h, compared to the use of Zeba® alone (43%), and EPNs alone (28%). Additionally, lower concentrations of EPNs showed predictably lower mortality rates of P. ficus. Significantly, higher EPN survival was recorded at each time interval in the morning, compared with the corresponding interval in the afternoon. This study demonstrates the ability of S. yirgalemense, when applied with adjuvants and at an appropriate time of day, to control P. ficus on grapevine, under semi-field conditions.


above ground; adjuvants, grapevine, Nu-Film-P®, Planococcus ficus, Steinernema yirgalemense, Zeba®

Full Text:



Adams, B.J. & Nguyen, K.B., 2002. Taxonomy and systematics. In:

Gaugler, R. (ed). Entomopathogenic nematology. CAB International, Wallingford. pp. 1 – 34.

Annecke, D.P. & Moran, V.C., 1982. Insects and Mites of Cultivated Plants in South Africa. Butterworths, Durban.

Arthurs, S., Heinz, K.M. & Prasifka, J.R., 2004. An analysis of using entomopathogenic nematodes against above-ground pests. Bul. Entomol. Res. 94, 297-306. doi: 10.1079/BER2003309

Beck, B., Brusselman, E., Nuyttens, D., Moens, M., Temmerman, F., Pollet, S., Van Weyenberg, S. & Spanoghe, P., 2014. Improving the biocontrol potential of entomopathogenic nematodes against Mamestra brassicae: Effect of spray application technique, adjuvants and an attractant. Pest Manag. Sci. 70, 103-112. doi: 10.1002/ps.3533

Berlinger, M.J., 1977. The Mediterranean vine mealybug and its natural enemies in southern Israel. Phytoparasitica 5, 3-14. doi: 10.1007/BF03179429

Cabaleiro, C. & Segura, A., 1997. Some characteristics of the transmission of grapevine leafroll associated virus 3 by Planococcus citri Risso. Eur. J. Plant. Pathol. 103, 373-378. doi: 10.1023/A:1008619523666

Caravia, L., Collins, C., Petrie, P.R. & Tyerman, S.D., 2016. Applications of shade treatments during Shiraz berry ripening to reduce the impact of high temperature. Aust. J. Grape Wine Res. 22, 422-437. doi: 10.1111/ajgw.12248

Cartechini, A. & Palliotti, A., 1995. Effects of shading on vine morphology and productivity and leaf gas exchange characteristics in grapevines in the field. Am. J. Enol. Vitic. 46, 227-234.

Daane, K.M., Cooper, M.L., Triapitsyn, S.V., Walton, V.M., Yokota, G.Y., Haviland, D.R., Bentley, W.J., Godfrey, K.E. & Wunderlich, L.R., 2008. Vineyard managers and researchers seek sustainable solutions for mealybugs, a changing pest complex. Calif. Agr. 62, 167-176. Doi: 10.3733/ca.v062n04p167

Daane, K.M., Malakar-Kuenen, R., Guillen, M., Bentley, W.J., Bianchi, M. & Gonzalez, D., 2003. Abiotic and biotic pest refuges hamper biological control of mealybugs in California vineyards. In: 1st Intern. Symp. on Biological Control of Arthropods, Honolulu. pp. 389 – 398.

De Villiers, M. & Pringle, K.L., 2007. Seasonal occurrence of vine pests in commercially treated vineyards in the Hex River Valley in the Western Cape Province, South Africa. Afr. Entomol. 15, 241. doi: 10.4001/1021-3589-15.2.241

De Waal, J.Y., 2008. Entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) for the control of the codling moth Cydia pomonella (L.) under South African conditions. Thesis, Stellenbosch University, Private Bag X1, 7602 Matieland (Stellenbosch), South Africa.

De Waal, J.Y., Addison, M.F. & Malan, A.P., 2017. Potential of Heterorhabditis zealandica (Rhabditida: Heterorhabditidae) for the control of codling moth, Cydia pomonella (Lepidoptera: Tortricidae) in semi-field trials under South African conditions. Int. J. Pest. Manag. 63, 1-9. doi: 10.1080/09670874.2017.1342149

De Waal, J.Y., Malan, A.P. & Addison, M.F., 2013. Effect of humidity and a superabsorbent polymer formulation on the efficacy of Heterorhabditis zealandica (Rhabditida: Heterorhabditidae) to control codling moth, Cydia pomonella (L.) (Lepidoptera: Tortricidae). Biocontrol. Sci. Techn. 23, 62-78. doi: 10.1080/09583157.2012.736472

Downie, D.A. & Gullan, P.J., 2004. Phylogenetic analysis of mealybugs (Hemiptera: Coccoidea: Pseudococcidae) based on DNA sequences from three nuclear genes, and a review of the higher classification. Syst. Entomol. 29, 238-259. doi: 10.1111/j.0307-6970.2004.00241.x

Downing, A.S., 1994. Efficacy of entomopathogenic nematodes (Rhabditida: Heterorhabditidae) against white grubs (Coleoptera: Scarabaeidae). J. Econ. Entomol. 83, 643-646. doi: 10.1093/jee/87.3.643

Forst, S. & Clarke, D., 2002. Bacteria-nematode symbiosis. In: Gaugler, R. (ed). Entomopathogenic nematology. CAB International, Wallingford. pp. 57 – 78.

Gaugler, R., Bednarek, A. & Campbell, J.F., 1992. Ultraviolet inactivation of heterorhabditid and steinernematid nematodes. J. Invertebr. Pathol. 160, 155-160. doi: 10.1016/0022-2011(92)90026-Z

Gaugler, R. & Boush, G.M., 1978. Effects of ultraviolet radiation and sunlight on the entomogenous nematode, Neoaplectana carpocapsae. J. Invertebr. Pathol. 32, 291-296. doi: 10.1016/0022-2011(78)90191-X

Georgis, R., 1990. Formulation and application technology. In: Gaugler, R. & Kaya, H.K. (eds). Entomopathogenic nematodes in biological control. CRC Press Inc., Boca Raton. pp. 173 – 191.

Glazer, I., 1992. Survival and efficacy of Steinernema carpocapsae in an exposed environment. Biocontrol Sci. Techn. 2, 101-107. doi: 10.1080/09583159209355223

Glazer, I., 2002. Survival biology. In: Gaugler, R. (ed). Entomopathogenic nematology. CAB International, Wallingford. pp. 169 – 188.

Glazer, I., Klein, M., Navon, A., & Nakache, Y., 1992a. Comparison of efficacy of entomopathogenic nematodes combined with antidesiccants applied by canopy sprays against three cotton pests (Lepidoptera: Noctuidae). J. Econ. Entomol. 85, 1636-1641. doi: 10.1093/jee/85.5.1636

Glazer, I., Nakache, Y. & Klein, M., 1992b. Use of entomopathogenic nematodes against foliage pests. Hassadeh 72, 626-630.

Greer, D.H. & Weston, C., 2010. Heat stress affects flowering, berry growth, sugar accumulation and photosynthesis in Vitis vinifera cv. Semillon grapevines grown in a controlled environment. Funct. Plant Biol. 37, 206-214. doi: 10.1071/FP09209

Grewal, P.S., Selvan, S. & Gaugler, R., 1994. Thermal adaptation of entomopathogenic nematodes: Niche breadth for infection, establishment, and reproduction. J. Therm. Biol. 19, 245-253. doi: 10.1016/0306-4565(94)90047-7

Griffin, C.T., Boemare, N.E. & Lewis, E.E., 2005. Biology and behaviours. In: Grewal, P.S., Ehlers, R.-U. & Shapiro-Ilan, D.I. (eds). Nematodes as biocontrol agents. CAB International, Wallingford. pp. 47 – 64.

Hattingh, V., Cilliers, C.J. & Bedford, E.C.G., 1998 (2nd ed). Citrus mealybugs. In: Bedford, E.C.G., Van den Berg, M.A. & De Villiers, E.A. (eds). Citrus pests in the Republic of South Africa. Institute for Tropical and Subtropical Crops, Nelspruit. pp. 112 – 120.

Head, J., Lawrence, A.J. & Walters, K.F.A., 2004. Efficacy of the entomopathogenic nematode, Steinernema feltiae, against Bemisia tabaci in relation to plant species. J. Appl. Entomol. 128, 543-547. doi: 10.1111/j.1439-0418.2004.00882.x

Kaya, H.K. & Stock, S.P., 1997. Techniques in insect nematology. In: Lacey, L.A. (ed). Manual of Techniques in Insect Pathology. Academic Press, San Diego, C.A. pp. 281¬ ¬– 324.

Le Vieux, P.D. & Malan, A.P., 2013b. The potential use of entomopathogenic nematodes to control Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae). S. Afr. J. Enol. Vitic. 34, 296-306.

Le Vieux, P.D. & Malan, A.P., 2015. Prospects for using entomopathogenic nematodes to control the vine mealybug, Planococcus ficus, in South African vineyards. S. Afr. J. Enol. Vitic. 36, 59-70.

Lello, E.R., Patel, M.N., Matthews, G.A. & Wright, D.J., 1996. Application technology for entomopathogenic nematodes against foliar pests. Crop Prot. 15, 567-574. Doi: 10.1016/0261-2194(96)00026-9

MacVean, C.M., Brewer, J.W. & Capinera, J.L., 1982. Field tests of antidesiccants to extend the infection period of an entomogenous nematode, Neoaplectana carpocapsae, against the Colorado potato beetle. J. Econ. Entomol 75, 97-101. doi: 10.1093/jee/75.1.97

Mason, J.M., Matthews, G.A. & Wright, D.J., 1998. Screening and election of adjuvants for the spray application of entomopathogenic nematodes against a foliar pest. Crop Prot. 17, 463-470. doi: 10.1016/S0261-2194(98)00043-X

Millar, I.M., 2002. Mealybug genera (Hemiptera: Pseudococcidae) of South Africa: Identification and review. Afr. Entomol. 10, 185-233.

Mráček, Z., 2002. Use of entomoparasitic nematodes (EPANs) in biological control. In: Upadhyay, R.K. (ed). Advances in microbial control of insect pests. Springer, Boston, MA. pp. 235 – 264.

Norton, D.C., 1978. Ecology of Plant-Parasitic Nematodes. Wiley, New York. pp. 128 – 132.

Odendaal, D., Addison, M.F. & Malan, A.P., 2016. Evaluation of above-ground application of entomopathogenic nematodes for the control of diapausing codling moth (Cydia pomonella L.) under natural conditions. Afr. Entomol. 24, 61-74. doi: 10.4001/003.024.0061

Platt, T., Malan, A.P & Stokwe, N.F., 2018a. A review of the potential use of entomopathogenic nematodes to control above-ground South African pest insects. Afr. J. Enol. Vitic. (Submitted).

Platt, T., Stokwe, N.F. & Malan, A.P., 2018b. Potential of local entomopathogenic nematodes for control of the vine mealybug,

Planococcus ficus. Afr. J. Enol. Vitic. (In Press).

Platt, T., Malan, A.P & Stokwe, N.F., 2018c. Foliar application of Steinernema yirgalemense to control Planococcus ficus: Assessing adjuvants to improve application in the glasshouse. S. Afr. J. Enol. Vitic. (In Press).

Prinsloo, G.H & Uys, V.M., 2015. Insects of Cultivated Plants and Natural Pastures in Southern Africa. Entomological Society of Southern Africa, Pretoria, South Africa.

Schroer, S. & Ehlers, R.-U., 2004. Foliar application of the entomopathogenic nematode Steinernema carpocapsae for biological control of diamondback moth larvae (Plutella xylostella). Biol. Control. 33, 81-86. doi: 10.1016/j.biocontrol.2004.12.009

Shapiro, M., Mclane, W. & Bell, R., 1985. Laboratory evaluation of selected chemicals as antidesiccants for the protection of the entomogenous nematode, Steinernema feltiae (Rhabditidae, Steinernematidae) against Lymantria dispar (Lepidoptera, Lymantriidae). J. Econ. Entomol. 78, 1437-1441.

Shapiro-Ilan, D.I., Gouge, D.H., Piggott, S.J. & Fife, J.P., 2006. Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. Biol. Control 38, 124-133. doi: 10.1093/jee/78.6.1437

TIBCO Inc., 2017. STATISTICA (data analysis software system), version 13.

Van Niekerk, S. & Malan, A.P., 2012. Potential of South African entomopathogenic nematodes (Heterorhabditidae and Steinernematidae) for control of the citrus mealybug Planococcus citri (Pseudococcidae). J. Invertebr. Pathol. 111, 166-174. doi: 10.1016/j.jip.2012.07.023

Van Niekerk & Malan, A.P. 2013. Adjuvants to improve aerial control of the citrus mealybug Planococcus citri (Hemiptera: Pseudococcidae) using entomopathogenic. J. Helminth. 98, 189-195. doi:10.1017/S0022149X13000771

Van Niekerk, S. & Malan, A.P., 2014a. Compatibility of Heterorhabditis zealandica and Steinernema yirgalemense with agrochemicals and biological control agents. African Entomology 22, 49-56.

Van Niekerk, S. & Malan, A.P., 2014b. Evaluating the efficacy of a polymer-surfactant formulation to improve control of Planococcus citri (Risso) (Hemiptera: Pseudococcidae) under simulated natural conditions. Afr. Pl. Prot. 17, 1-9

Van Zyl, S.A., Brink, J-C., Calitz, F.J. & Fourie, P.H., 2010. Effects of adjuvants on deposition efficiency of fenhexamid sprays applied to Chardonnay grapevine foliage. Crop. Prot. 29, 843-852. doi: 10.1016/j.cropro.2010.04.017

Wakgari, W.M. & Giliomee, J.H, 2004. Mealybugs and their parasitoids in apple and pear orchards in the Western Cape Province, South Africa. Afr. Plant Prot. 10, 7-11.

Walton, V.M., 2003. Development of an integrated pest management system for vine mealybug, Planococcus ficus (Signoret), in vineyards in the Western Cape Province, South Africa. Thesis, Stellenbosch University, Private Bag X1, 7602 Matieland (Stellenbosch), South Africa.

Walton, V.M. & Pringle, K.L., 2004b. Vine mealybug, Planococcus ficus (Signoret) (Hemiptera: Pseudococcidae), a key pest in South African vineyards. A review. S. Afr. J. Enol. Vitic. 25, 54-62. doi: 10.21548/25-2-2140

Webster, J.M. & Bronskill, J.F., 1968. Use of Gelgard M and an evaporation retardant to facilitate control of larch sawfly by a nematode-bacterium complex 1. J. Econ. Entomol. 61, 1370-1373. doi: 10.1093/jee/61.5.1370

Woodring, J.L., Kaya, H.K., 1988. Steinernematid and heterorhabditid nematodes: a handbook of techniques. Fayetteville: Arkansas Agricultural Experimental Station. (Southern Cooperative Series Bulletin 331).

Wilson, M. & Gaugler, R., 2004. Factors limiting short-term persistence of entomopathogenic nematodes. J. Appl. Entomol. 128, 250-253. doi: 10.1111/j.1439-0418.2004.00814.x

Wright, D.J., Peters, A., Schroer, S, & Fife, J.P., 2005. Application technology. In: Grewal, P.S., Ehlers, R.U. & Shapiro-Ilan, D.I. (eds). Nematodes as biocontrol agents. CAB International, Wallingford. pp. 91 – 106.



  • There are currently no refbacks.