1. Introduction
Leafmining flies in the genus
Crop plants are damaged by
In addition to the direct damage inflicted to crop plants, producers may suffer further economic losses because of quarantine restrictions that constrain international trade (Gitonga et al., 2010). Producers lose export markets when importing countries ban products because of the actual or potential presence of leafminer infestations in the country of origin. Even without complete bans, phytosanitary measures (e.g., fumigation or irradiation (Hallman et al., 2011)) required by importing countries may make exports cost prohibitive for producers in the country of origin.
2. Taxonomy, origins and invasiveness
One of the great challenges in understanding the pest status of
Among the three major pest species, there have been considerable historical problems with their taxonomy and identification.
The endemic range of
Adding to the taxonomic complexity regarding
In addition to our evolving understanding of the taxonomy of
Although
In the mid 1970s, as more frequent and severe outbreaks of
Invasions of these
The introduction of
Whereas
3. Biological influences on pest status
The pest status of
4. Response to insecticides
One of the most important factors in leading to
Intense insecticide use is the most common strategy used to eradicate newly discovered outbreaks of
Cross resistance to multiple classes of insecticides is also likely in
At present, two of the most effective insecticides for
Another class of insecticide with efficacy against
Selection of appropriate insecticides and rates for use in the field also depends upon proper identification of leafminer species. Parrella and Keil (1985) found that
5. Management trends
The premise that leafminers are secondary pests, which are released from natural control when their enemies are eliminated (Luckmann & Metcalf, 1994), has a long history, even if it has not always been fully appreciated. Studies dating back to the 1940s have shown the importance of parasitoids in maintaining
In every geographic region where
Parasitoids associated with native non-pest
Whereas parasitoids are valuable control agents, making effective use of them in practice can be challenging. Parasitoid populations, by their nature, will lag behind the development of their host populations (Hofsvang et al., 2005; Trumble & Nakakihara, 1983; Weintraub, 2001a). In these types of situations, growers may need to apply insecticides to keep growing leafminer populations below economically damaging levels. In a similar vein, growers may need to use insecticides to treat other pest problems, which then may have detrimental effects on leafminer management (Getzin, 1960). The outcome of either situation is that leafminer populations are released from their natural control and rapidly increase because many of the insecticides used against leafminers or other pests are highly toxic to their parasitoids. Should such a rapid increase occur growers are likely to believe that further insecticide treatments are warranted. This then becomes the very definition of the pesticide treadmill.
Most broad spectrum synthetic insecticides developed since the 1940s are highly toxic to parasitoids of
Of the three most effective insecticides for use against
Results of various studies provide conflicting results for the effect of abamectin on leafminer parasitoids (reviewed in Kaspi & Parrella, 2005). In general, field studies have demonstrated that abamectin and spinosyns are not as detrimental to parasitoid populations as carbamates, organophosphate or pyrethroids, but they are more deleterious than cyromazine (Prijono et al., 2004; Schuster, 1994; Trumble, 1985). The greater toxicity of abamectin and spinosyns compared with cyromazine to
In recognition of the importance that parasitoids play in managing leafminers, Trumble and colleagues initiated development of IPM programs for field grown vegetables in California and Mexico. One of the first aspects addressed in the research program was to establish realistic economic thresholds in these agroecosystems for the key insect pests,
In commercial scale trials conducted in celery (
These trials consistently showed that the IPM programs had consistently lower populations of
Despite the lower insecticide use, growers were not sacrificing the amount of crop harvested or its quality. Ultimately, these IPM programs based on economic thresholds with the goal of conserving
Despite these constraints, there have been successful demonstrations of integrated management of
An ideal insecticide for incorporation into a greenhouse IPM program is one that is pest specific and not harmful to biological control agents of that pest, or those of other pests in the system (Kaspi & Parrella, 2005). Although not harmless to parasitoids, the use of abamectin can be successfully integrated with augmentative releases of the parasitoid
6. Conclusions
Growers around the world have experienced significant problems from
In a similar vein, when other pests reach economic threshold levels and require therapeutic insecticide treatments, growers are encouraged to consider the effect of those insecticide treatments on leafminer management. Proactive management decisions will reduce the likelihood of inducing severe outbreaks of leafminers. It is possible to produce a crop with few, if any insecticide treatments for leafminers, but this will best be realized if all growers in a community adopt similar IPM programs so that any one grower does not adversely affect neighboring growers. Continuing forward, the basic strategies for leafminer management are clear. However, the practical implementation of such strategies will remain a challenge. There is an ongoing need for development of selective, reduced risk insecticides to incorporate into leafminer management programs and to ensure that appropriate resistance management programs are developed. Further, there is a clear need for improved diagnostic methods and characterization of biological variation among biotypes and cryptic species of pest
Because invasions are most likely to continue into the future, it will be critical to accurately identify new invasive species and populations, and to monitor changes in leafminer population dynamics following invasions. As these leafminers will continue to be important pests of high value crops, insecticides will continue to be an important component of leafminer management. Therefore, it is imperative to continue to refine the use of insecticides that target leafminers. Improving application timing and methods will help to conserve insecticide susceptibility and maintain efficacy by mitigating the evolution of resistance. Insecticide resistance management must remain as a critical component of IPM. Furthermore, improving strategies for the conservation and augmentation of leafminer parasitoids will help reduce the need for insecticide applications. Knowledge gaps in regard to the effects of insecticides on various leafminer parasitoids should continue to be addressed. Leafminer management will best be accomplished through research on, and implementation of, comprehensive IPM strategies.
References
- 1.
Abe Y. & Kawahara T. (2001). Coexistence of the vegetable leafminer; Liriomyza sativae (Diptera: Agromyzidae), with L. trifolii and L. bryoniae on commercially grown tomato plants. Applied Entomology and Zoology 36: 277 - 281. - 2.
Abe Y.; Takeuchi T.; Tokumaru S. & Kamata J. (2005). Comparison of the suitability of three pest leafminers (Diptera: Agromyzidae) as hosts for the parasitoid Dacnusa sibirica (Hymenoptera: Braconidae). European Journal of Entomology 102: 805-807. - 3.
Abe Y. & Tokumaru S. (2008). Displacement in two invasive species of leafminer fly in different localities. Biological Invasions 10: 951–995. - 4.
Al-Khateeb S.A. & Al-Jabr A.M. (2006). Effect of leafminer Liriomyza trifolii (Burgess) (Diptera: Agromyzidae) on gas exchange capacity of cucumber, Cucumis sativus L. grown under greenhouse conditions. Acta Horticulturae 710: 423-428. - 5.
Andersen A.; Tran T.T.A. & Nordhus E. (2008). Distribution and importance of polyphagous Liriomyza-species (Diptera, Agromyzidae) in vegetables in Vietnam. Norwegian Journal of Entomology 55: 149-164. - 6.
Babul Hossain M. & Poehling H.M. (2006). Non-target effects of three biorationale insecticides on two endolarval parasitoids of Liriomyza sativae (Dipt., Agromyzidae). Journal of Applied Entomology 130: 360-367. - 7.
Bartlett P.W. & Powell D.F. (1981). Introduction of American serpentine leaf miner, Liriomyza trifolii, into England and Wales and its eradication from commerical nurseries, 1977-81. Plant Pathology 30: 185-193. - 8.
Bethke J.A. & Parrella M.P. (1985). Leaf puncturing, feeding and oviposition behavior of Liriomyza trifolii. Entomologia Experimentalis et Applicata 39: 149-154. - 9.
Bjorksten T.A. & Robinson M. (2005). Juvenile and sublethal effects of selected pesticides on the leafminer parasitoids Hemiptarsenus varicornis and Diglyphus isaea (Hymenoptera : Eulophidae) from Australia. Journal of Economic Entomology 98: 1831-1838. - 10.
Bjorksten T.A.; Robinson M. & La Salle J. (2005). Species composition and population dynamics of leafmining flies and their parasitoids in Victoria. Australian Journal of Entomology 44: 186-191. - 11.
Blanchard E.E. (1926). A dipterous leaf-miner on Cineraria, new to science. Revista de la Sociedad Entomologica Argentina 1: 10-11. - 12.
Blanchard E.E. (1938). Descripciones y anotaciones de dipteros argentinos Agromyzidae Anales de la Sociedad Cientifica Argentina 126: 352-359. - 13.
Broadbent A.B. & Pree D.J. (1989). Resistance to pyrazophos in the serpentine leafminer Liriomyza trifolii (Burgess) (Diptera: Agromyzidae) in Ontario greenhouse [Canada]. Canadian Entomologist 121: 47-54. - 14.
Bueno F.; Santos C.; Tofoli R.; Pavan A. & Bueno C. (2007). Reduction of spinosad rate for controlling Liriomyza huidobrensis (Diptera: Agromyzidae) in dry beans (Phaseolus vulgaris L.) and its impact on Frankliniella schultzei (Thysanoptera: Thripidae) and Diabrotica speciosa (Coleoptera: Chrysomelidae). BioAssay 2: 3. - 15.
CABI (2004) Liriomyza huidobrensis Datasheet: Crop Protection Compendium CD (ed. CAB International, Wallingford, Oxon, UK. - 16.
Chavez G.L. & Raman K.V. (1987). Evaluation of trapping and trap types to reduce damage to potatoes by the leafminer, Liriomyza huidobrensis (Diptera, Agromyzidae). Insect Science and its Application 8: 369-372. - 17.
Chen X.-X.; Lang F.-Y.; Xu Z.-H.; He J.-H. & Ma Y. (2003). The occurrence of leafminers and their parasitoids on vegetables and weeds in Hangzhou area, Southeast China. BioControl 48: 515-527. - 18.
Chow A. & Heinz K.M. (2006). Control of Liriomyza langei on chrysanthemum by Diglyphus isaea produced with a standard or modified parasitoid rearing technique. Journal of Applied Entomology 130: 113-121. - 19.
Demirozera O.; Tyler-Julian K.; Funderburk J.; Leppla N. & Reitz S. (2012). Frankliniella occidentalis (Pergande) integrated pest management programs for fruiting vegetables in Florida. Pest Management Science DOI: 10.1002/ps.3389. - 20.
Elmore J.C. & Ranney C.A., Jr. (1954). Injury to pepper plants by the pea leafminer. Journal of Economic Entomology 47: 357-358. - 21.
Ferguson J.S. (2004). Development and stability of insecticide resistance in the leafminer Liriomyza trifolii (Diptera: Agromyzidae) to Cyromazine, Abamectin, and Spinosad. Journal of Economic Entomology 97: 112-119. - 22.
Frick K.E. (1951). Liriomyza langei, a new species of leaf miner of economic importance in California. Pan-Pacific Entomologist 27: 81-88. - 23.
Frick K.E. (1957). Nearctic species in the Liriomyza pusilla complex no. 2 L. munda and two other species attacking crops in California (Diptera: Agromyzidae). Pan-Pacific Entomologist 33: 59-70. - 24.
Frick K.E. (1958). Liriomyza dianthi n. sp., a new pest of carnations in California (Diptera: Agromyzidae). Proceedings of the Entomological Society of Washington 60: 1-5. - 25.
Frick K.E. (1959). Synopsis of the species of agromyzid leaf miners described from North America. Proceedings of the United States National Museum 108: 347-465. - 26.
Gao Y.; Lei Z.; Abe Y. & Reitz S.R. (2011). Species displacements are common to two invasive species of leafminer fly in China, Japan, and the United States. Journal of Economic Entomology 104: 1771-1773. - 27.
Gao Y.; Reitz S.R.; Wei Q.; Yu W. & Lei Z. (2012). Insecticide-mediated apparent displacement between two invasive species of leafminer fly. PLoS ONE 7: e36622, doi:36610.31371/journal.pone.0036622. - 28.
Getzin L.W. (1960). Selective insecticides for vegetable leaf-miner control and parasite survival. Journal of Economic Entomology 53: 872-875. - 29.
Gitonga Z.M.; Chabi-Olaye A.; Mithöfer D.; Okello J.J. & Ritho C.N. (2010). Control of invasive Liriomyza leafminer species and compliance with food safety standards by small scale snow pea farmers in Kenya. Crop Protection 29: 1472-1477. - 30.
Hallman G.J.; Guo K. & Liu T.X. (2011). Phytosanitary irradiation of Liriomyza trifolii (Diptera: Agromyzidae). Journal of Economic Entomology 104: 1851-1855. - 31.
Hara A.H. (1986). Effects of certain insecticides on Liriomyza trifolii (Burgess) (Diptera: Agromyzidae) and its parasitoids on chrysanthemums in Hawaii. Proceedings of the Hawaiian Entomological Society 26: 65-70. - 32.
Hayslip N. (1961). Leafminer control on tomatoes in the Indian River area. Proceedings of the Florida State Horticultural Society 74. - 33.
He L.; Zhang Y.; Xiao N.; Wei J. & Kuang R. (2002). Liriomyza huidobrensis in Yunnan, China: Current distribution and genetic structure of a recently established population. Entomologia Experimentalis et Applicata 102: 213-219. - 34.
Heinz K.M. & Chaney W.E. (1995). Sampling for Liriomyza huidobrensis (Diptera: Agromyzidae) larvae and damage in celery. Environmental Entomology 24: 204-211. - 35.
Hidrayani; Purnomo; Rauf A.; Ridland P.M. & Hoffmann A.A. (2005). Pesticide applications on Java potato fields are ineffective in controlling leafminers, and have antagonistic effects on natural enemies of leafminers. International Journal of Pest Management 51: 181-187. - 36.
Hills O.A. & Taylor E.A. (1951). Parasitization of dipterous leafminers in cantaloups and lettuce in the Salt River Valley, Arizona. Journal of Economic Entomology 44: 759-762. - 37.
Hofsvang T.; Snøan B.; Andersen A.; Heggen H. & Anh L.N. (2005). Liriomyza sativae (Diptera: Agromyzidae), an invasive species in South-East Asia: Studies on its biology in northern Vietnam. International Journal of Pest Management 51: 71-80. - 38.
Huang S.W. (2004) Global Trade Patterns in Fruits and Vegetables: by USDA Economic Research Service) USDA-ERS, Washington, DC, p. 83. - 39.
IRAC International MoA Working Group (2011) IRAC MoA (Insecticide Resistance Action Committee Mode of Action) Classification Scheme, version 7.1, June 2011. - 40.
Jones V.P. & Parrella M.P. (1986). The movement and dispersal of Liriomyza trifolii (Diptera: Agromyzidae) in a chrysanthemum greenhouse. Annals of Applied Biology 109: 33-39. - 41.
Kaspi R. & Parrella M.P. (2005). Abamectin compatibility with the leafminer parasitoid Diglyphus isaea. Biological Control 35: 172-179. - 42.
Lange W.H. (1949). Notes on the occurrence of agromyzid flies during 1948, and a new record of two unreported species in California. Pan-Pacific Entomologist 25: 91-92. - 43.
Lange W.H.; Grigarick A.A. & Carlson E.C. (1957). Serpentine leaf miner damage. California Agriculture 12: 3-5. - 44.
Lanzoni A.; Bazzocchi G.G.; Burgio G. & Fiacconi M.R. (2002). Comparative life history of Liriomyza trifolii and Liriomyza huidobrensis (Diptera: Agromyzidae) on beans: Effect of temperature on development. Environmental Entomology 31: 797-803. - 45.
Lei Z.R.; Wen J.Z. & Wang Y. (1997). Research progress of the vegetable leafminer in China and suggestion in the future control. Annals of Agricultural Science of China Youth. Beijing: China Agricultural Press 495-499. - 46.
Leibee G.L. (1981) Insecticidal control of Liriomyza spp. on vegetables: Proceedings of the IFAS-Industry Conference on BioIogical Control of Liriomyza Leafminers II (ed. by D Schuster) University of Florida / IFAS, Lake Buena Vista, FL, pp. 216- 220. - 47.
Leibee G.L. & Capinera J.L. (1995). Pesticide resistance in Florida insects limits management options. Florida Entomologist 78: 386-399. - 48.
Levins R.A.; Poe S.L.; Littell R.C. & Jones J.P. (1975). Effectiveness of a leafminer [Liriomyza sativae] control program for Florida tomato production. Journal of Economic Entomology 68: 772-774. - 49.
Liu T.X.; Kang L.; Heinz K.M. & Trumble J. (2009). Biological control of Liriomyza leafminers: Progress and perspective. CAB Reviews: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources 4: 4: doi: 10.1079/PAVSNNR20094004. - 50.
Lonsdale O. (2011). The Liriomyza (Agromyzidae: Schizophora: Diptera) of California. Zootaxa: 1-123. - 51.
Luck R.F.; van den Bosch R. & Garcia R. (1977). Chemical insect control: A troubled pest management strategy. BioScience 27: 606-611. - 52.
Luckmann W.H. & Metcalf R.L. (1994) The pest-management concept: Introduction to Insect Pest Management (ed. by RL Metcalf & WH Luckmann) Wiley, New York, pp. 1-34. - 53.
MacDonald O.C. (1991). Responses of the alien leaf miners Liriomyza trifolii and Liriomyza huidobrensis (Diptera: Agromyzidae) to some pesticides scheduled for their control in the UK. Crop Protection 10: 509-513. - 54.
Mason G.A.; Johnson M.W. & Tabashnik B.E. (1987). Susceptibility of Liriomyza sativae and Liriomyza trifolii (Diptera: Agromyzidae) to permethrin and fenvalerate. Journal of Economic Entomology 80: 1262-1266. - 55.
Minkenberg O.P.J.M. (1988a). Dispersal of Liriomyza trifolii. Bulletin OEPP 18: 173-182. - 56.
Minkenberg O.P.J.M. (1988b). Life history of the agromyzid fly Liriomyza trifolii on tomato at different temperatures. Entomologia Experimentalis et Applicata 48: 73-84. - 57.
Morgan D.J.W.; Reitz S.R.; Atkinson P.W. & Trumble J.T. (2000). The resolution of Californian populations of Liriomyza huidobrensis and Liriomyza trifolii (Diptera: Agromyzidae) using PCR. Heredity 85: 53-61. - 58.
Mujica N. & Kroschel J. (2011). Leafminer fly (Diptera: Agromyzidae) occurrence, distribution, and parasitoid associations in field and vegetable crops along the Peruvian coast. Environmental Entomology 40: 217-230. - 59.
Nicoli G. (1997). Biological control of exotic pests in Italy: Recent experiences and perspectives. Bulletin OEPP 27: 69-75. - 60.
Oatman E.R. (1959). Natural control studies of the melon leaf miner, Liriomyza pictella (Thomson). Journal of Economic Entomology 52: 895-898. - 61.
Oatman E.R. (1960). Parasitism of the overwintering pupae of the melon leaf miner, Liriomyza pictella. Journal of Economic Entomology 53: 682. - 62.
Oatman E.R. & Kennedy G.G. (1976). Methomyl induced outbreak of Liriomyza sativae on tomato. Journal of Economic Entomology 69: 667-668. - 63.
Oatman E.R. & Michelbacher A.E. (1958). The melon leaf miner, Liriomyza pictella (Thompson) (Diptera: Agromyzidae) I. Life history studies. Annals of the Entomological Society of America 51: 557-566. - 64.
Oatman E.R. & Michelbacher A.E. (1959). The melon leaf miner, Liriomyza pictella (Thompson) (Diptera: Agromyzidae) II. Ecological studies. Annals of the Entomological Society of America 52: 83-89. - 65.
Ohno K.; Ohmori T. & Takemoto H. (1999). Effect of insecticide applications and indigenous parasitoids on population trends of Liriomyza trifolii in gerbera greenhouses. Japanese Journal of Applied Entomology and Zoology 43: 81-86. - 66.
Ozawa A.; Saito T. & Ota M. (2001). Biological control of the American Serpentine leafminer, Liriomyza trifolii (Burgess), on tomato in greenhouses by parasitoids. II. Evaluation of biological control by Diglyphus isaea (Walker) and Dacnusa sibirica Telenga in commercial greenhouses. Japanese Journal of Applied Entomology and Zoology 45: 61-74. - 67.
Palumbo J.C.; Mullis C.H., Jr. & Reyes F.J. (1994). Composition, seasonal abundance, and parasitism of Liriomyza (Diptera: Agromyzidae) species on lettuce in Arizona. Journal of Economic Entomology 87: 1070-1077. - 68.
Parkman P.; Dusky J.A. & Waddill V.H. (1989). Biological studies of Liriomyza sativae (Diptera: Agromyzidae) on castor bean. Environmental Entomology 18: 768-772. - 69.
Parrella M.P. (1982). A review of the history and taxonomy of economically important serpentine leafminers (Liriomyza spp.) in California (Diptera: Agromyzidae). Pan Pacific Entomologist 58: 302-308. - 70.
Parrella M.P. (1987). Biology of Liriomyza. Annual Review of Entomology 32: 201-224. - 71.
Parrella M.P. & Jones V.P. (1987). Development of integrated pest management strategies in floricultural crops. Bulletin of the Entomological Society of America 33: 28-34. - 72.
Parrella M.P.; Jones V.P.; Youngman R.R. & Lebeck L.M. (1985). Effect of leaf mining and leaf stippling of Liriomyza spp. on photosynthetic rates of chrysanthemum. Annals of the Entomological Society of America 78: 90-93. - 73.
Parrella M.P. & Keil C.B. (1984). Insect pest management: the lesson of Liriomyza. Bulletin of the Entomological Society of America 30: 22-25. - 74.
Parrella M.P. & Keil C.B. (1985). Toxicity of methamidophos to four species of Agromyzidae. Journal of Agricultural Entomology 2: 234-237. - 75.
Parrella M.P. & Trumble J.T. (1989). Decline of resistance in Liriomyza trifolii (Diptera: Agromyzidae) in the absence of insecticide selection pressure. Journal of Economic Entomology 82: 365-368. - 76.
Prijono D.; Rauf A.; Robinson M.; Bjorksten T. & Hoffmann A.A. (2004). Toxicity of chemicals commonly used in Indonesian vegetable crops to Liriomyza huidobrensis populations and the Indonesian parasitoids Hemiptarsenus varicornis, Opius sp., and Gronotoma micromorpha, as well as the Australian parasitoids Hemiptarsenus varicornis and Diglyphus isaea. Journal of Economic Entomology 97: 1191-1197. - 77.
Rathman R.J.; Johnson M.W.; Rosenheim J.A. & Tabashnik B.E. (1990). Carbamate and pyrethroid resistance in the leafminer parasitoid Diglyphus begini (Hymenoptera: Eulophidae). Journal of Economic Entomology 83: 2153-2158. - 78.
Reitz S.R. & Funderburk J. (2012) Management strategies for western flower thrips and the role of insecticides: Insecticides - Pest Engineering (ed. by F Perveen) InTech, Rijeka, Croatia, pp. 355 - 384. - 79.
Reitz S.R.; Kund G.S.; Carson W.G.; Phillips P.A. & Trumble J.T. (1999). Economics of reducing insecticide use on celery through low-input pest management strategies. Agriculture, Ecosystems, and Environment 73: 185-197. - 80.
Reitz S.R. & Trumble J.T. (2002a). Competitive displacement among insects and arachnids. Annual Review of Entomology 47: 435-465. - 81.
Reitz S.R. & Trumble J.T. (2002b). Interspecific and intraspecific differences in two Liriomyza leafminer species in California. Entomologia Experimentalis et Applicata 102: 101-113. - 82.
Rosen D. (1978) The importance of cryptic species and specific identifications as related to biological control: Biosystematics in Agriculture (ed. by JA Romberger) Allanheld, Osmun & Co., Montclair, NJ. - 83.
Saito T.; Ikeda F. & Ozawa A. (1996). Effect of pesticides on parasitoid complex of serpentine leafminer Liriomyza trifolii (Burgess) in Shizuoka Prefecture. Japanese Journal of Applied Entomology and Zoology 40: 127-133. - 84.
Salgado V.L. (1998). Studies on the mode of action of spinosad: Insect symptoms and physiological correlates. Pesticide Biochemistry and Physiology 60: 91-102. - 85.
Scheffer S.J. (2000). Molecular evidence of cryptic species within the Liriomyza huidobrensis (Diptera: Agromyzidae). Journal of Economic Entomology 93: 1146-1151. - 86.
Scheffer S.J. & Lewis M.L. (2001). Two nuclear genes confirm mitochondrial evidence of cryptic species within Liriomyza huidobrensis (Diptera: Agromyzidae). Annals of the Entomological Society of America 94: 648-653. - 87.
Scheffer S.J. & Lewis M.L. (2005). Mitochondrial phylogeography of vegetable pest Liriomyza sativae (Diptera: Agromyzidae): Divergent clades and invasive populations. Annals of the Entomological Society of America 98: 181-186. - 88.
Scheffer S.J. & Lewis M.L. (2006). Mitochondrial phylogeography of the vegetable pest Liriomyza trifolii (Diptera: Agromyzidae): Diverged clades and invasive populations. Annals of the Entomological Society of America 99: 991-998. - 89.
Scheffer S.J.; Lewis M.L. & Joshi R.C. (2006). DNA barcoding applied to invasive leafminers (Diptera: Agromyzidae) in the Philippines. Annals of the Entomological Society of America 99: 204-210. - 90.
Scheffer S.J.; Wijesekara A.; Visser D. & Hallett R.H. (2001). Polymerase chain reaction-restriction fragment-length polymorphism method to distinguish Liriomyza huidobrensis from L. langei (Diptera: Agromyzidae) applied to three recent leafminer invasions. Journal of Economic Entomology 94: 1177-1182. - 91.
Schuster D.J. (1994). Life-stage specific toxicity of insecticides to parasitoids of Liriomyza trifolii (Burgess) (Diptera: Agromyzidae). International Journal of Pest Management 40: 191-194. - 92.
Schuster D.J. & Everett P.H. (1983). Response of Liriomyza trifolii (Diptera:Agromyzidae) to insecticides on tomato. Journal of Economic Entomology 76: 1170-1174. - 93.
Shepard B.M.; Samsudin & Braun A.R. (1998). Seasonal incidence of Liriomyza huidobrensis (Diptera: Agromyzidae) and its parasitoids on vegetables in Indonesia. International Journal of Pest Management 44: 43-47. - 94.
Shipp J.L.; Boland G.J. & Shaw L.A. (1991). Integrated pest management of disease and arthropod pests of greenhouse vegetable crops in Ontario: Current status and future possibilities. Canadian Journal of Plant Science 71: 887-914. - 95.
Smith I.M. (1999). Review of the status of glasshouse quarantine pests in EPPO countries. Bulletin OEPP 29: 91-93. - 96.
Spencer K.A. (1965). A clarification of the status of Liriomyza trifolii (Burgess) and some related species. Proceedings of the Entomological Society of Washington 67: 32-40. - 97.
Spencer K.A. (1973) Agromyzidae (Diptera) of Economic Importance. Series Entomologica 9, I–XI. Dr. W. Junk B.V., The Hague. - 98.
Spencer K.A. (1990) Host Specialization in the World Agromyzidae (Diptera). Kluwer, Dordrecht, Netherlands. - 99.
Spollen K.M.; Johnson M.W. & Tabashnik B.E. (1995). Stability of fenvalerate resistance in the leafminer parasitoid Diglyphus begini (Hymenoptera: Eulophidae). Journal of Economic Entomology 88: 192-197. - 100.
Tagami Y.; Doi M.; Sugiyama K.; Tatara A. & Saito T. (2006). Survey of leafminers and their parasitoids to find endosymbionts for improvement of biological control. Biological Control 38: 210-216. - 101.
Tantowijoyo W. & Hoffmann A.A. (2010). Identifying factors determining the altitudinal distribution of the invasive pest leafminers Liriomyza huidobrensis and Liriomyza sativae. Entomologia Experimentalis et Applicata 135: 141-153. - 102.
Tokumaru S. & Abe Y. (2003). Effects of temperature and photoperiod on development and reproductive potential of Liriomyza sativae, L. trifolii, and L. bryoniae (Diptera: Agromyzidae). Japanese Journal of Applied Entomology and Zoology 47: 143-152. - 103.
Tokumaru S.; Kurita H.; Fukui M. & Abe Y. (2005). Insecticide susceptibility of Liriomyza sativae, L. trifolii, and L. bryoniae (Diptera: Agromyzidae). Japanese Journal of Applied Entomology and Zoology 49: 1-10. - 104.
Tran D.H.; Tran T.T.A.; Konishi K. & Takagi M. (2006). Abundance of the parasitoid complex associated with Liriomyza spp. (Diptera: Agromyzidae) on vegetable crops in central and southern Vietnam. Journal of the Faculty of Agriculture, Kyushu University 51: 115-120. - 105.
Trumble J.T. (1981). Liriomyza trifolii could become a problem on celery. California Agriculture 35: 30-31. - 106.
Trumble J.T. (1985). Integrated pest management of Liriomyza trifolii: influence of avermectin, cyromazine, and methomyl on leafminer ecology in celery. Agriculture, Ecosystems, and Environment 12: 181-188. - 107.
Trumble J.T. & Alvarado-Rodriguez B. (1993). Development and economic evaluation of an IPM program for fresh market tomato production in Mexico. Agriculture Ecosystems and Environment 43: 267-284. - 108.
Trumble J.T.; Carson W.G. & Kund G.S. (1997). Economics and environmental impact of a sustainable integrated pest management program in celery. Journal of Economic Entomology 90: 139-146. - 109.
Trumble J.T. & Nakakihara H. (1983). Occurrence, parasitization, and sampling of Liriomyza species (Diptera: Agromyzidae) infesting celery in California. Environmental Entomology 12: 810-814. - 110.
Trumble J.T.; Ting I.P. & Bates L. (1985). Analysis of physiological, growth, and yield responses of celery to Liriomyza trifolii. Entomologia Experimentalis et Applicata 38: 15-21. - 111.
Tryon E.H., Jr.; Poe S.L. & Cromroy H.L. (1980). Dispersal of vegetable leafminer Liriomyza sativae onto a transplant production range. Florida Entomologist 63: 292-296. - 112.
van Lenteren J.C. (2000). A greenhouse without pesticides: Fact or fantasy? Crop Protection 19: 375-384. - 113.
Waddill V.; Schuster D. & Sonoda R. (1986). Integrated pest management for Florida tomatoes. Plant Disease 70: 96-102. - 114.
Weintraub P.G. (2001a). Changes in the dynamics of the leafminer, Liriomyza huidobrensis, in Israeli potato fields. International Journal of Pest Management 47: 95-102. - 115.
Weintraub P.G. (2001b). Effects of cyromazine and abamectin on the pea leafminer Liriomyza huidobrensis (Diptera: Agromyzidae) and its parasitoid Diglyphus isaea (Hymenoptera: Eulophidae) in potatoes. Crop Protection 20: 207-213. - 116.
Weintraub P.G. & Horowitz A.R. (1995). The newest leafminer pest in Israel, Liriomyza huidobrensis. Phytoparasitica 23: 177-184. - 117.
Wene G.P. (1953). Control of the serpentine leaf miner on peppers. Journal of Economic Entomology 46: 789-793. - 118.
Wolfenbarger D. (1954). Potato yields associated with control of aphids and the serpentine leaf miner. Florida Entomologist 37: 7-12. - 119.
Yano E. (2004). Recent development of biological control and IPM in greenhouses in Japan. Journal of Asian-Pacific Entomology 7: 5-11.