A Review of Leaf-mining Insects and Control Options for their Management, with Special Reference to Holocacista capensis (Lepidoptera: Heliozelidae) in Vineyards in South Africa

L.A.I. Steyn, H. Geertsema, A.P. Malan, P. Addison

Abstract


A leaf-mining pest occurring on commercial varieties of Vitis vinifera in South Africa was investigated due to the presence of cocoons on fruit. The leaf miner, Holocacista capensis, was reported on grapevines in 2012. Since its discovery on commercial grape varieties, control strategies have consisted solely of insecticide applications. Despite the fact that the leaf-mining habit is taxonomically diverse and considered ancient, little is generally known of leaf-mining larvae. A review was conducted in order to better understand the leaf-mining strategy and amalgamate the current knowledge of other leaf-mining insects.  The general evolutionary history within the full complement of taxa that display the leaf-mining habit is discussed. The review focuses on lepidopteran leaf-mining pests and discloses the known information associated with the first report and the impact of H. capensis in the Western Cape, South Africa. As no control methods have been identified for H. capensis in vineyards, various chemical, biological and cultural control strategies adopted for other leaf-mining pests were investigated. Control options, including the
use of entomopathogenic nematodes (EPNs), parasitoids, physical and cultural control measures, were considered and are discussed. Alternate control methods are pertinent for the grape-growing industry to avoid the development of the insecticide resistance that is common amongst leaf miners. This review aims to consolidate the available literature and therefore aid in the development of an integrated pest management strategy to effectively control H. capensis in infested vineyards in South Africa.

Keywords


integrated pest management, leaf miner, biological control, grapevine

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References


Allegrucci, N., Velazquez, M.S., Russo, M.L., Perez, E. & Scorsetti, A.C. 2017. Endophytic colonisation of tomato by the entomopathogenic fungus Beauveria bassiana: the use of different inoculation techniques and their effects on the tomato leafminer Tuta absoluta (Lepidoptera: Gelechiidae). J. Plant Protect. Res. 57, 205 – 211. doi: 10.1515/jppr-2017-0045

Allsopp, E., Barnes, B.N., Blomefield, T.L. & Pringle, K.L. 2015. Grapevine. In: Prinsloo, G.L. & Uys, V.M. (eds). Insects of cultivated plants and natural pastures in southern Africa, Entomological Society of Southern Africa, Cape Town. pp. 420 – 437.

Auerbach, M.J., Connor, E.F., & Mopper, S. 1995. Minor miners and major miners: Population dynamics of leaf-mining insects. In: Cappuccinco, N & Price, P.W. (eds). Population Dynamics: New Approaches and Synthesis. Chapter 5, Academic Press, San Diego. pp. 83 – 110.

Ayabe, Y. & Hijii, N. 2016. Avoidance of parasitoid attack is associated with the spatial use within a leaf by a lepidopteran leafminer. Entomol. Exp. Appl. 161, 39 – 49. doi: 10.1111/eea.12492

Batalla-Carrera, L., Morton, A. & García-del-Pino, F. 2010. Efficacy of entomopathogenic nematodes against the tomato leafminer Tuta absoluta in laboratory and greenhouse conditions. BioControl 55, 523 – 530. doi: 10.1007/s10526-010-9284-z

Beattie, G.A.C., Liu, Z.M., Watson, D.M., Clift, A.D. & Jiang, L. 1995a. Evaluation of petroleum spray oils and polysaccharides for control of Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae). Aust. J. Entomol. 34, 349 – 353. doi: 10.1111/j.1440-6055.1995.tb01353.x

Beattie, G.A.C., Somsook, V., Watson, D.M., Clift, A.D. & Jiang, L. 1995b. Field evaluation of Steinernema carpocapsae (Weiser) (Rhabditida: Steinernematidae) and selected pesticides and enhancers for control of Phyllocnistis citrella Stainton (Lepidoptera: Gracillariidae). Aust. J. Entomol. 34, 335 – 342. doi: 10.1111/j.1440-6055.1995.tb01351.x

Bennett, A. 2015. Cotton. In: Prinsloo, G.L. & Uys, V.M. (eds). Insects of cultivated plants and natural pastures in southern Africa, Entomological Society of Southern Africa, Cape Town. pp. 274 – 293.

Bernardo, U., van Nieukerken, E.J., Sasso, R., Gebiola, M., Gualtieri L. & Viggiani, G. 2015. Characterization, distribution, biology and impact on Italian walnut orchards of the invasive North-American leafminer Coptodisca lucifluella (Lepidoptera: Heliozelidae). Bull. Entomol. Res. 105, 210 – 224. doi: 10.1017/S0007485314000947

Biondi, A., Guedes, R.N.C., Wan, F.-H. & Desneux, N. 2018. Ecology, worldwide spread, and management of the invasive South American Tomato Pinworm, Tuta absoluta: Past, present and future. Annu. Rev. Entomol. 63, 239 – 258. doi: 10.1146/annurev-ento-031616-034933

Bourgogne, J. 1951. Ordre des Lepidopteres. In Traité de Zoologie. Masson Et Cie Éditeurs, Paris. pp. 300-448.

Boush, G.M. & Anderson, R.J. 1967. Coptodisca sp. (Lepidoptera: Heliozelidae) attacking cranberries in Wisconsin. J. Econ. Entomol. 60, 1472. doi: 10.1093/jee/60.5.1472

Buthelezi, N.M., Conlong, D.E. & Zharare, G.E. 2012. The groundnut leaf miner collected from South Africa is identified by mtDNA CO1 gene analysis as the Australian soybean moth (Aproaerema simplixella) (Walker) (Lepidoptera: Gelechiidae). Afr. J. Agric. Res. 7, 5285 – 5292. doi: 10.5897/AJAR12.986

Cardé, R.T. & Minks, A.K. 1995. Control of moth pests by mating disruption: successes and constraints. Annu. Rev. Entomol. 40, 559 – 585. doi: 10.1146/annurev.en.40.010195.003015

Cocco, A., Deliperi, S. & Delrio, G. 2013. Control of Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in greenhouse tomato crops using the mating disruption technique. J. Appl. Entomol. 137, 16 – 28. doi: 10.1111/j.1439-0418.2012.01735.x

Connor, E.F. & Taverner, M.P. 1997. The evolution and adaptive significance of the leaf-mining habit. Oikos 79, 6 – 25. doi: 10.2307/3546085

Cornell, H.V. 1989. Endophage-ectophage ratios and plant defence. Evol. Ecol. 3, 64 – 76. doi: 10.1007/BF02147932

Davis, D.R. 1998. The Monotrysian Heteroneura. In: Kristensen, N.P. (ed.). Lepidoptera, Moths and Butterflies. Volume 1. Part 35, Walter de Gruyter, Berlin. Handbook of Zoology. 4, 65 – 90.

Digweed, S.C., Macquarrie, C.J.K., Langor, D.W., Williams, D.J.M., Spence, J.R., Nystrom, K.L. & Morneau, L. 2009. Current status of invasive alien birch-leafmining sawflies (Hymenoptera: Tenthredinidae) in Canada, with keys to species. Can. Entomol. 141, 201 – 235. doi: 10.4039/n09-003

Dillman, A.R., Chaston, J.M., Adams, B.J., Ciche, T.A., Goodrich-Blair, H., Stock, S.P. & Sternberg, P.W. 2012. An entomopathogenic nematode by any other name. PLOS Pathog. 8, 1 – 4. doi: 10.1371/journal.ppat.1002527

Dos Santos, M.M., Soares, M.A., Silva, I.M., Fontes, P.C.R. & Zanuncio, J.C. 2018. First record of the sweet potato pest Bedellia somnulentella (Lepidoptera: Bedelliidae) in Brazil. Fla. Entomol. 101, 315 – 316. doi: 10.1653/024.101.0224

Du Plessis, H. 2015. Groundnut. In: Prinsloo, G.L. & Uys, V.M. (eds). Insects of cultivated plants and natural pastures in southern Africa, Entomological Society of Southern Africa, Cape Town. pp. 186 – 197.

El-Arnaouty, S.A., Pizzol, J., Galal, H.H., Kortam, M.N., Afifi, A.I., Beyssat, V., Desneux, N., Biondi, A. & Heikal, I.H. 2014. Assessment of two Trichogramma species for the control of Tuta absoluta in North African tomato greenhouses. Afr. Entomol. 22, 801 – 809. doi: 10.4001/003.022.0410

Feeny, P. 1970. Seasonal changes in oak leaf tannin and nutrients as a cause of spring feeding by winter moth caterpillars. Ecology 51, 565 – 581. doi: 10.2307/1934037

Ferguson, J.S. 2004. Development and stability of insecticide resistance in the leafminer Liriomyza trifolii (Diptera: Agromyzidae) to cyromazine, abamectin, and spinosad. J. Econ Entomol. 97, 112 – 119. doi: 10.1093/jee/97.1.112

Fragoso, D.B., Guedes, R.N.C., Picanço, M.C. & Zambolim, L. 2002. Insecticide use and organophosphate resistance in the coffee leaf miner Leucoptera coffeella (Lepidoptera: Lyonetiidae). Bull. Entomol. Res. 92, 203 – 212. doi: 10.1079/BER2002156

Garcia-Marí, F., Vercher, R., Costa-Comelles, J., Marzal, C. & Villalba, M. 2004. Establishment of Citrostichus phyllocnistoides (Hymenoptera: Eulophidae) as a biological control agent for the citrus leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae) in Spain. Biol. Control 29, 215 – 226. doi: 10.1016/S1049-9644(03)00155-5

Gilbert, M., Grégoire, J.C., Freise, J.F. & Heitland, W. 2004. Long‐distance dispersal and human population density allow the prediction of invasive patterns in the horse chestnut leafminer Cameraria ohridella. J. Anim. Ecol. 73, 459 – 468. doi: 10.1111/j.0021-8790.2004.00820.x

Gözel, Ç. & Kasap, İ. 2015. Efficacy of entomopathogenic nematodes against the tomato leafminer, Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) in tomato field. Turk. Entomol. Derg. 39, 229 – 237. doi: 10.16970/ted.84972

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

Grové, T., de Villiers, E.A. & Daneel, M.S. 2015. Mango. In: Prinsloo, G.L. & Uys, V.M. (eds). Insects of cultivated plants and natural pastures in southern Africa. Entomological Society of Southern Africa, Cape Town. pp. 574 – 588.

Haddi, K., Berger, M., Bielza, P., Rapisarda, C., Williamson, M.S. &

Bass, C. 2017. Mutation in the ace-1 gene of the tomato leaf miner (Tuta absoluta) associated with organophosphates resistance. J. Appl. Entomol. 141, 612 – 619. doi: 10.1111/jen.12386

Hara, A.H., Kaya, H.K., Gaugler, R., Lebeck, L.M. & Mello, C.L. 1993. Entomopathogenic nematodes for biological control of the leafminer, Liriomyza trifolii (Dipt.: Agromyzidae). Entomophaga 38, 359 – 369. doi: 10.1007/BF02374454

Head, J., Walters, K.F.A. & Langton, S. 2000. The compatibility of the entomopathogenic nematode, Steinernema feltiae, and chemical insecticides for the control of the South American leafminer, Liriomyza huidobrensis. BioControl 45, 345 – 353. doi: 10.1023/A:1009986217310

Heads, P.A. & Lawton, J.H. 1983. Studies on the natural enemy complex of the holly leaf-miner: the effects of scale on the detection of aggregative responses and the implications for biological control. Oikos 40, 267 – 276. doi: 10.2307/3544591

Hering, E.M. 1951. Biology of the leaf miners. W. Junk, Gravenhages, The Netherlands. 420 pp.

Holloway, J.D., Bradley, J.D. & Carter, D.J. 1987. CIE guides to insects of importance to man: 1. Lepidoptera. CAB International, Wallingford. 262 pp.

Hoy, M.A., Singh, R. & Rogers, M.E. 2007. Citrus leafminer, Phyllocnistis citrella (Lepidoptera: Gracillariidae), and natural enemy dynamics in central Florida during 2005. Fla. Entomol. 90, 358 – 359. doi: 10.1653/0015-4040(2007)90[358:CLPCLG]2.0.CO;2

Ingels, C.A. & Klonsky, K.M. 1998. Historical and current uses. In: Ingels, C.A., Bugg, R.L., McGourty, G.T. & Christensen, L.P. (eds). Cover Cropping in Vineyards: A Grower’s Handbook. Chapter 1, University of California, Oakland. pp. 3 – 7.

Isman, M.B. 2006. Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu. Rev. Entomol. 51, 45 - 66. doi: 10.1146/annurev.ento.51.110104.151146

Jacob, J.S. & Mathew, M.P. 2016. Laboratory evaluation of entomopathogenic nematodes against American serpentine leaf miner, Liriomyza trifolii (Burgess). J. Biopest. 9, 27 – 33.

Johns, C.V. & Hughes, L. 2002. Interactive effects of elevated CO2 and temperature on the leaf-miner Dialectica scalariella Zeller (Lepidoptera: Gracillariidae) in Paterson's Curse, Echium plantagineum (Boraginaceae). Glob. Chang. Biol. 8, 142 – 152. doi: 10.1046/j.1365-2486.2002.00462.x

Kamali, S., Karimi, J. & Koppenhöfer, A.M. 2017. New insight into the management of the tomato leaf miner, Tuta absoluta (Lepidoptera: Gelechiidae) with entomopathogenic nematodes. J. Econ. Entomol. 111, 112 – 119. doi: 10.1093/jee/tox332

Kaya, H.K., Bedding, R.A. & Akhurst, R.J. 1993. An overview of insect-parasitic and entomopathogenic nematodes. In: Bedding, R., Akhurst, R. & Kaya, H. (eds). Nematodes and the biological control of insect pests, CSIRO Publications, Australia. pp. 1 – 10.

Khan, I.A., Hussain, S., Akbar, R., Saeed, M., Farid, A., Ali, I., Alam, M. & Shah, B. 2015. Efficacy of bio- and synthetic pesticides against pea leaf miner, Phytomyza atricornis Goureau (Diptera: Agromyzidae), on pea in Peshawar. J. Entomol. Zool. Stud. 3, 368 – 370.

Kirichenko, N., Augustin, S. & Kenis, M. 2018. Invasive leafminers on woody plants: a global review of pathways, impact, and management. J. Pest Sci. 92, 93 – 106. doi: 10.1007/s10340-018-1009-6

Kroschel, J. & Zegarra, O. 2013. Attract-and-kill as a new strategy for the management of the potato tuber moths Phthorimaea operculella (Zeller) and Symmetrischema tangolias (Gyen) in potato: Evaluation of its efficacy under potato filed and storage conditions. Pest Manag. Sci. 69, 1205 – 1215. doi: 10.1002/ps.3483

Kuroko, H. 1987. Three new species of the genus Antispila (Lepidoptera: Heliozelidae) from Japan. Tinea 12, 109 – 117.

Langor, D.W., Digweed, S.C., Williams, D.J.M., Spence, J.R. & Saunders, C. 2000. Establishment and spread of two introduced parasitoids (Ichneumonidae) of the birch leafminer, Fenusa pusilla (Tenthredinidae). BioControl 45, 415 – 423. doi: 10.1023/A:1026598305752

Lebeck, L.M., Gaugler, R., Kaya, H.K., Hara, A.H. & Johnson, M.W. 1993. Host stage suitability of the leafminer Liriomyza trifolii (Diptera: Agromyzidae) to the entomopathogenic nematode Steinernema carpocapsae (Rhabditida: Steinernematidae). J. Invertebr. Pathol. 62, 58 – 63. doi: 10.1006/jipa.1993.1074

Lee, S., Hodges, R.W. & Brown, R.L. 2008. Checklist of Gelechiidae (Lepidoptera) in America north of Mexico. Zootaxa 2231, 1 – 39. doi: 10.11646/zootaxa.2231.1.1

Lees, D.C., Kawahara, A.Y., Rougerie, R., Ohshima, I., Kawakita, A., Bouteleux, O., de Prins, J. & Lopez-Vaamonde, C. 2014. DNA barcoding reveals a largely unknown fauna of Gracillariidae leaf-mining moths in the Neotropics. Mol. Ecol. Resour. 14, 286 – 296. doi: 10.1111/1755-0998.12178

Lewis, E.E., Hazir, S., Hodson, A. & Gulcu, B. 2015. Trophic relationships of entomopathogenic nematodes in agricultural habitats. In: Campos-Herrera, R. (ed.). Nematode pathogenesis of insects and other pests, Springer, Switzerland. pp. 139 – 163.

Lomelí-Flores, J.R., Barrera, J.F. & Bernal, J.S. 2010. Impacts of weather, shade cover and elevation on coffee leafminer Leucoptera coffeella (Lepidoptera: Lyonetiidae) population dynamics and natural enemies. Crop Prot. 29, 1039 – 1048. doi: 10.1016/j.cropro.2010.03.007

Low, C. 2012. Variable risk and the evolution of the defence repertoire of the Tupelo leafminer. In: Pontarotti. P. (ed.). Evolutionary Biology: Mechanisms and Trends, Springer, Berlin, Heidelberg. pp. 155 – 168.

Maharjan, R., Kwon, M., Kim. J. & Jung, C. 2017. Mass production of Diglyphus isaea (Hymenoptera: Eulophidae), a biological control agent of a Korean population of potato leaf miner Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae). Entomol. Res. 47, 94 – 100. doi: 10.1111/1748-5967.12205

Maier, C.T. 2001. Exotic lepidopteran leafminers in North American apple orchards: rise to prominence, management, and future threats. Biol. Invasions 3, 283 – 293. doi: 10.1023/A:1015289928950

Mey, W. 2011. Basic pattern of Lepidoptera diversity in southwestern Africa. In: Hacker, H.H. (ed.). Esperiana: Buchreihe zur Entomologie. Memoir 6. Wissenschaftlicher Verlag – Peks. Schwanfeld. pp. 1 – 316.

Migiro, L.N., Maniania, N.K., Chabi-Olaye, A. & Vandenberg, J. 2010. Pathogenicity of entomopathogenic fungi Metarhizium anisopliae and Beauveria bassiana (Hypocreales: Clavicipitaceae) isolates to the adult pea leafminer (Diptera: Agromyzidae) and prospects of an autoinoculation device for infection in the field. Environ. Entomol. 39, 468 – 475. doi: 10.1603/EN09359

Migiro, L.N., Maniania, N.K., Chabi-Olaye, A., Wanjoya, A. & Vandenberg, J. 2011. Effect of infection by Metarhizium anisopliae (Hypocreales: Clavicipitaceae) on the feeding and oviposition of the pea leafminer Liriomyza huidobrensis (Diptera: Agromyzidae) on different host plants. Biol. Control 56, 179 – 183. doi: 10.1016/j.biocontrol.2010.09.013

Milla, L., van Nieukerken, E.J., Vijverberg, R., Doorenweerd, C., Wilcox, S.A., Halsey, M.A., Young, D.A., Jones, T.M. & Kallies, A. 2018. A preliminary molecular phylogeny of shield-bearer moths (Lepidoptera: Adeloidea: Heliozelidae) highlights rich undescribed diversity. Mol. Phylogenetics Evol. 120, 129 – 143. doi: 10.1016/j.ympev.2017.12.004

Minkenberg, O.P.J.M. & van Lenteren, J.C. 1986. The leafminers Liriomyza bryoniae and L. trifolii (Diptera: Agromyzidae), their parasites and host plants: a review. Agricultural University of Wageningen Papers No. 86(2). 50 pp.

Muchemi, S.K., Zebitz, C.P.W., Borgemeister, C., Akutse, K.S., Foba, C.N., Ekesi, S. & Fiaboe, K.K.M. 2018. Interaction between Chrysocharis flacilla and Diglyphus isaea (Hymenoptera: Eulophidae), two parasitoids of Liriomyza leafminers. J. Econ. Entomol. 111, 556 – 563. doi: 10.1093/jee/toy007

Mutegi, D.M., Kilalo, D., Kimenju, J.W. & Waturu, C. 2017. Pathogenicity of selected native entomopathogenic nematodes against tomato leaf miner (Tuta absoluta) in Kenya. World. J. Agric. Res. 5, 233 – 239. doi: 10.12691/wjar-5-4-5

Nielsen, E.S. & Common, I.F.B. 1991. Lepidoptera (moths and butterflies). In: The Insects of Australia. 2nd Edition. Volume II, Melbourne University Press, Australia. pp. 817 – 915.

Noyes, J.S. 2003. Universal Chalcidoidea Database: About Chalcidoids. Natural History Museum. [Online]. Retrieved September 12, 2018:

http://www.nhm.ac.uk/our-science/data/chalcidoids/introduction.html

Parolin, P., Bresch, C., Desneux, N., Brun, R., Bout, A., Boll, R. & Poncet, C. 2012. Secondary plants used in biological control: a review. Int. J. Pest Manag. 58, 91 – 100. doi: 10.1080/09670874.2012.659229

Parra, J.R.P. & Zucchi, R.A. 2004. Trichogramma in Brazil: feasibility of use after twenty years of research. Neotrop. Entomol. 33, 271 – 81. doi: 10.1590/S1519-566X2004000300001

Patočka, J. & Turčáni, M. 2005. Lepidoptera Pupae: Central European Species. Text Volume. 542 pp. Plate Volume. Apollo Books, Denmark. 321 pp.

Percival, G.C. & Holmes, S.P. 2016. The influence of systematic inducing agents on horse chestnut leaf miner (Cameraria ohridella) severity in white flowering horse chestnut (Aesculus hoppicastanum L.). Urban For. Urban Green. 20, 97 – 102. doi: 10.1016/j.ufug.2016.08.009

Pereira, E.J.G., Picanço, M.C., Bacci, L., Crepso, A.L.B. & Guedes, R.N.C. 2007. Seasonal mortality factors of the coffee leafminer, Leucoptera coffeella. Bull. Entomol. Res. 97, 421 – 432. doi: 10.1017/S0007485307005202

Pereira, R.R., Picanço, M.C., Santana JR, P.A., Moreira, S.S., Guedes, R.N.C. & Corrêa, A.S. 2014. Insecticide toxicity and walking response of three pirate bug predators of the tomato leaf miner Tuta absoluta. Agric. Forest Entomol. 16, 293 – 301. doi: 10.1111/afe.12059

Potter, D.A. 1992. Abundance and mortality of a specialist leafminer in response to experimental shading and fertilization of American holly. Oecologia 91, 14 – 22. doi: 10.1007/BF00317235

Powell, J.A. 2003. Lepidoptera. In: Resh, V.H. & Cardé, R.T. (ed.). Encyclopaedia of insects, Academic Press, London. pp. 631 – 664.

Price, P.W., Fernandes, G.W. & Waring, G.L. 1987. Adaptive nature of insect galls. Environ. Entomol. 16, 15 – 24. doi: 10.1093/ee/16.1.15

Progar, R.A., Kruse, J.J., Lundquist, J.E., Zogas. K.P. & Rinella, M.J. 2014. An entomopathogenic fungus and nematode prove ineffective for biocontrol on an invasive leaf miner Profenusa thomsoni in Alaska. Biocontrol Sci. Techn. 25, 373 – 382. doi: 10.1080/09583157.2014.977224

Regier, J.C., Mitter, C., Kristensen, N.P., Davis, D.R., van Nieukerken, E.J., Rota, J., Simonsen, T.J., Mitter, K.T., Kawahara, A.Y., Yen, S.-H., Cummings, M.P. & Zwick, A. 2015. A molecular phylogeny for the oldest (nonditrysian) lineages of extant Lepidoptera, with implications for classification, comparative morphology and life-history evolution. Syst. Entomol. 40, 671 – 704. doi: 10.1111/syen.12129

Roditakis, E., Steinbach, D., Moritz, G., Vasakis, E., Stavrakaki, M., Ilias, A., García-Vidal, L., Martínez-Aguirre, M.D., Bielza, P., Morou, E., Silva, J.E., Silva, W.M., Siqueira, H.A.A., Iqbal, S., Troczka, B.J., Williamson, M.S., Bass, C., Tsagkarahou, A., Vontas, J. & Nauen, R. 2017. Ryanodine receptor point mutations confer diamide insecticide resistance in tomato leafminer, Tuta absoluta (Lepidoptera: Gelechiidae). Insect Biochem. Mol. Biol. 80, 11 – 20. doi: 10.1016/j.ibmb.2016.11.003

Roditakis, E., Vasakis, E., García-Vidal, L., Martínez-Aguirre, M.D., Rison, J.L., Haxaire-Lutun, M.O., Nauen, R., Tsagkarakou, A. & Bielza, P. 2018. A four-year survey on insecticide resistance and likelihood of chemical control failure for tomato leaf miner Tuta absoluta in the European/Asian region. J. Pest Sci. 91, 421 – 435. doi: 10.1007/s10340-017-0900-x

Rodríguez, S.M., Gerding, P.M. & France, I.A. 2006. Entomopathogenic fungi isolates selection for egg control of tomato moth Tuta absoluta Meyrick (Lepidoptera: Gelechiidae) eggs. Agricultura Técnica 66, 151 – 158.

Schoeman, P.S. 2015. Coffee. In: Prinsloo, G.L. & Uys, V.M. (eds). Insects of cultivated plants and natural pastures in southern Africa, Entomological Society of Southern Africa, Cape Town. pp. 530 – 541.

Scoble, M.J. 1992. The Lepidoptera: Form, Function and Diversity, Oxford University Press, New York. 404 pp.

Shah, P.A. & Pell, J.K. 2003. Entomopathogenic fungi as biological control agents. Appl. Microbiol. Biotechnol. 61, 413 – 423. doi: 10.1007/s00253-003-1240-8

Shanower, T.G., Wightman, J.A. & Gutierrez, A.P. 1993. Biology and control of the groundnut leafminer, Aproaerema modicella (Deventer) (Lepidoptera: Gelechiidae). Crop Prot. 12: 3 – 10. doi: 10.1016/0261-2194(93)90014-A

Sharma, R.R., Reddy, S.V.R. & Jhalegar, M.J. 2014. Pre-harvest fruit bagging: a useful approach for plant protection and improved post-harvest fruit quality – a review. J. Hortic. Sci. Biotechnol. 89, 101 – 113. doi: 10.1080/14620316.2014.11513055

Signes, A.J., Burló, F., Martínez Sánchez, F. & Carbonell-Barrachina, A.A. 2007. Effects of pre-harvest bagging on quality of black table grapes. World J. of Agric. Sci. 3, 32 – 38.

Siqueira, H.A.A., Guedes, R.N.C. & Picanço, M.C. 2001. Insecticide resistance in populations of Tuta absoluta (Lepidoptera: Gelechiidae). Agric. For. Entomol. 2, 147 – 153. doi: 10.1046/j.1461-9563.2000.00062.x

Soper, A.L., Macquarrie, C.J.L. & van Criesche, R. 2015. Introduction, establishment, and impact of Lathrolestes thomsoni (Hymenoptera: Ichneumonidae) for biological control of the ambermarked birch leafminer, Profenusa thomsoni (Hymenoptera: Tenthredinidae), in Alaska. Biol. Control 83, 13 – 19. doi: 10.1016/j.biocontrol.2014.12.018

Spencer, K.A. 1973. Agromyzidae (Diptera) of economic importance. In: Series Entomologica. Volume 9, Springer, Berlin. pp. 1 – 405.

Sporleder, M., Schaub, B., Aldana, G. & Kroschel, J. 2017. Temperature-dependent phenology and growth potential of the Andean potato tuber moth, Symmetrischema tangolias (Gyen) (Lep., Gelechiidae). J. Appl. Entomol. 141, 201 – 218. doi: 10.1111/jen.12321

Stehr, F.W. 1992. Lepidoptera. In: Immature Insects, Kendall/Hunt Publishing Company. Dubuque, Iowa. pp. 288 – 596.

Stelinski, L.L., Lapointe, S.L. & Meyer, W.L. 2010. Season-long mating disruption of citrus leafminer, Phyllocnistis citrella Stainton, with an emulsified wax formulation of pheromone. J. Appl. Entomol. 134, 512 – 520. doi: 10.1111/j.1439-0418.2009.01453.x

Stelinski, L.L., Miller, J.R. & Rogers, M.E. 2008. Mating disruption of citrus leafminer mediated by a noncompetitive mechanism at a remarkably low pheromone release rate. J. Chem. Ecol. 34, 1107 – 1113. doi: 10.1007/s10886-008-9501-8

Steyn, L.A.I., Addison, P. & Malan, A.P. 2019. Potential of South African entomopathegenic nematodes to control the leaf miner, Holocacista capensis (Lepidoptera: Heliozelidae). S. Afr. J. Enol. Vitic. 40, 301 – 307. doi: 10.21548/40-2-3420

Stock, S.P. 2015. Diversity, biology and evolutionary relationships. In: Campos-Herrera, R. (ed.). Nematode pathogenesis of insects and other pests, Springer International Publishing, Switzerland. pp. 3 – 27.

Stock, S.P. & Hunt, D.J. 2005. Morphology and systematics of nematodes used in biocontrol. In: Grewal, P.S., Ehlers, R-U. & Shapiro-Ilan, D.I. (eds). Nematodes as biocontrol agents, CABI Publishing, Oxfordshire pp. 3 – 63.

Suvočarev, K., Blanco, O., Faci, J.M., Medina, E.T. & Martínez-Cob, A. 2013. Transpiration of table grape (Vitis vinifera L.) trained on an overhead trellis system under netting. Irrig. Sci. 31, 1289 – 1302. doi: 10.1007/s00271-013-0404-2

Torrance, L.A.I. 2016. The bio-ecology of the Cape grapevine leafminer, Holocacista capensis (Lepidoptera: Heliozelidae), in the Western Cape. MSc thesis. Stellenbosch: Stellenbosch University. 120 pp.

Trumble, J.T. 1985. Integrated pest management of Liriomyza trifolii: influence of avermectin, cyromazine, and methomyl on leafminer ecology in celery. Agric. Ecosyst. Environ. 12, 181 – 188. doi: 10.1016/0167-8809(85)90109-4

Ueno, W., Hayasaka, T., Endo, S. & Shibahasi, T. 1987. Ecology and control of Antispila sp. (Lepidoptera: Heliozelidae) infesting grape leaves. Bull. Yamagata Prefectural Hortic. Exp, Station 6: 1 – 18.

Ureche, C. 2016. First record of a new alien invasive species in Romania: Phyllocnistis vitegenella Clemens (Lepidoptera: Gracillariidae). Acta Oecol. Carpatica IX, 133 – 138.

Vacas, S., Alfaro, C., Primo, J. & Navarro-Llopis, V. 2011. Studies on the development of a mating disruption system to control the tomato leafminer, Tuta absoluta Povolny (Lepidoptera: Gelechiidae). Pest Manag. Sci. 67, 1473 – 1480. doi: 10.1002/ps.2202

Van Damme, V.M., Beck, B.K.E.G., Berckmoes, E., Moerkens, R., Wittemans, L., de Vis, R., Nuyttens, D., Casteels, H.F., Maes, M., Tirry, L. & de Clercq, P. 2015. Efficacy of entomopathogenic nematodes against larvae of Tuta absoluta in the laboratory. Pest Manag. Sci. 72, 1702 – 1709. doi: 10.1002/ps.4195

Van Nieukerken, E.J. & Geertsema, H. 2015. A new leafminer on grapevine and Rhoicissus (Vitacea) in South Africa within an expanded generic concept of Holocacista (Insecta, Lepidoptera, Heliozelidae). ZooKeys 507, 41 – 97. doi: 10.3897/zookeys.507.9536

Van Nieukerken, E.J., Kaila, L., Kitching, I.J., Kristensen, N.P., Lees, D.C., Minet, J., et al. 2011. Order Lepidoptera Linnaeus, 1758 in: Zhang, Z.-Q. (ed.). Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa 3148, 212 – 221.

Van Nieukerken, E.J., Wagner, D.L., Baldessari, M., Mazzon, L., Angeli, G., Girolami, V., Duso, C. & Doorenweerd, C. 2012. Antispila oinophylla new species (Lepidoptera: Heliozelidae), a new North American grapevine leafminer invading Italian vineyards: taxonomy, DNA barcodes and life cycle. ZooKeys 170, 29 – 77. doi: 10.3897/zookeys.170.2617

Vári, L. 1961. South African Lepidoptera. Lithocolletidae, Transvaal Museum Memoir 12, Pretoria. 238 pp.

Visser, D. 2015a. Sweet potato. In: Prinsloo, G.L. & Uys, V.M. (eds). Insects of cultivated plants and natural pastures in southern Africa, Entomological Society of Southern Africa, Cape Town. pp. 74 – 85.

Visser, D. 2015b. Potato. In: Prinsloo, G.L. & Uys, V.M. (eds). Insects of cultivated plants and natural pastures in southern Africa, Entomological Society of Southern Africa, Cape Town. pp. 48 – 64.

Wang, H.-L., Geertsema, H., van Nieukerken, E.J. & Löfstedt, C. 2015. Identification of the female-produced sex pheromone of the leafminer Holocacista capensis infesting grapevine in South Africa. J. Chem. Ecol. 41, 724 – 731. doi: 10.1007/s10886-015-0611-9

Wei, J.N. & Kang, L. 2006. Electrophysiological and behavioral responses of a parasitic wasp to plant volatiles induced by two leaf miner species. Chem. Senses 31, 467 – 477. doi: 10.1093/chemse/bjj051

Weintraub, P.G. & Horowitz, A.R. 1998. Effects of translaminar versus conventional insecticides on Liriomyza huidobrensis (Diptera: Agromyzidae) and Diglyphus isaea (Hymenoptera: Eulophidae) populations in celery. J. Econ. Entomol. 91, 1180 – 1185. doi: 10.1093/jee/91.5.1180

Willett, D.S., Stelinski, L.L. & Lapointe, S.L. 2015. Using response surface methods to explore and optimize mating disruption of the leafminer Phyllocnistis citrella (Lepidoptera: Gracillariidae). Front. Ecol. Evol. 3, 1 – 11. doi: 10.3389/fevo.2015.00030

Williams, E.C. & Walters, K.F.A. 2000. Foliar Application of the entomopathogenic nematode Steinernema feltiae against leafminers on vegetables. Biocontrol Sci. Techn. 10, 61 – 70. doi: 10.1080/09583150029396

Wright, M.G. 2015. Proteas. In: Prinsloo, G.L. & Uys, V.M. (eds). Insects of cultivated plants and natural pastures in southern Africa, Entomological Society of Southern Africa, Cape Town. pp. 680 – 695.




DOI: https://doi.org/10.21548/41-2-4081

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