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Invasion of Japan by exotic leafminers Liriomyza spp. (Diptera: Agromyzidae) and its consequences

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Abstract

Identifying patterns and causes of species displacement is important from the viewpoints of ecology and evolutionary biology as this phenomenon affects community structure. Here I review the species displacement between Liriomyza trifolii (Burgess) and Liriomyza sativae Blanchard (Diptera: Agromyzidae) in Japan. These two species and Liriomyza huidobrensis (Blanchard) originated from the New World and are considered to have invaded Japan from around 1990 to the early 2000s. During this period, L. trifolii was apparently displaced by L. sativae, but the direction of displacement in Japan has been contrary to that observed between the same two species in the USA and China. While the displacement of L. sativae by L. trifolii in these two countries can be attributed to the lower insecticide susceptibility of L. trifolii there, species displacement in the opposite direction in Japan is probably due to the relatively high fecundity of L. sativae and differential effects of the introduced parasitoid Dacnusa sibirica Telenga (Hymenoptera: Braconidae) on both Liriomyza species, except in the south of the country.

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References

  • Abe Y (2015) Discovery and progress in the study of the vegetable leafminer Liriomyza sativae in Japan. Plant Protect 69:793–796 (in Japanese)

    Google Scholar 

  • 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. Appl Entomol Zool 36:277–281

    Article  Google Scholar 

  • Abe Y, Tokumaru S (2008) Displacement in two invasive species of leafminer fly in different localities. Biol Invasions 10:951–953

    Article  Google Scholar 

  • 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). Eur J Entomol 102:805–807

    Article  Google Scholar 

  • Amano K, Suzuki A, Hiromori H, Saito T (2008) Relative abundance of parasitoids reared during field exposure of sentinel larvae of the leafminers Liriomyza trifolii (Burgess), L. sativae Blanchard, and Chromatomyia horticola (Goureau) (Diptera: Agromyzidae). Appl Entomol Zool 43:625–630

    Article  Google Scholar 

  • Chen B, Kang L (2004) Variation in cold hardiness of Liriomyza huidobrensis (Diptera: Agromyzidae) along latitudinal gradients. Environ Entomol 33:155–164

    Article  Google Scholar 

  • Editorial board (2009) Newly recognized plant diseases and insect pests. Ann Rept Kanto-Tosan Plant Prot Soc 56:147–150 (in Japanese)

    Google Scholar 

  • Gao Y, Lei Z, Abe Y, Reitz SR (2011) Species displacements are common to two invasive species of leafminer fly in China, Japan, and the United States. J Econ Entomol 104:1771–1773

    Article  PubMed  Google Scholar 

  • Gao Y, Reitz SR, Wei Q, Yu W, Lei Z (2012) Insecticide-mediated apparent displacement between two invasive species of leafminer fly. PLoS One 7(5):e36622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hada H, Sato M (2010) Occurrence of the pea leafminer, Liriomyza huidobrensis (Blanchard) and the vegetable leafminer, Liriomyza sativae Blanchard in Iwate Prefecture. Ann Rept Plant Prot North Japan 61:165–167 (in Japanese)

    Google Scholar 

  • Hayashi K, Kondou M, Ando S, Masuda T, Tokumaru S (2005) Occurrences and overwintering of Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae) in Miyagi Prefecture. Ann Rept Plant Prot North Japan 56:149–151 (in Japanese)

    Google Scholar 

  • Higuchi S, Koga M, Tsuruta S, Gyoutoku Y, Koga S (2002) Preference of the vegetable leaf miner, Liriomysa sativae (Blanchard) for host plants. Kyushu Plant Prot Res 48:72–75 (in Japanese)

    Article  Google Scholar 

  • Imura T (2005) Geographic distribution, seasonal prevalence of occurrence and parasitoid complex of vegetable leafminer, Liriomyza sativae Blanchard in Nara Prefecture. Bull Nara Agric Exp Stn 36:29–39 (in Japanese with English summary)

    Google Scholar 

  • Iwasaki A, Kasugai K, Iwaizumi R, Sasakawa M (2000) A newly recorded pest, Liriomyza sativae Blanchard in Japan. Plant Prot 54:142–147 (in Japanese)

    Google Scholar 

  • Iwasaki A, Iwaizumi R, Takano S (2004) A newly recorded pest, Liriomyza huidobrensis (Blanchard) in Japan. Plant Prot 58:13–19 (in Japanese)

    Google Scholar 

  • Kanmiya K (2011) Communication by vibratory signals in dipteran insects. In: Miyatake Y (ed) Insect communication by sounds and vibrations. Hokuryukan, Tokyo, pp 104–127 (in Japanese)

    Google Scholar 

  • Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170

    Article  Google Scholar 

  • Kiritani K (2013) Different effects of climate change on the population dynamics of insects. Appl Entomol Zool 48:97–104

    Article  Google Scholar 

  • Maharjan R, Oh HW, Jung C (2014) Morphological and genetic characteristics of Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae) infesting potato crops in Korea. J Asia-Pac Entomol 17:281–286

    Article  Google Scholar 

  • Malais M, Ravensberg WJ (1991) The biology of glasshouse pests and their natural enemies, knowing and recognizing (Yano E et al. translated 1995). Nosan-gyoson-bunka-kyokai, Tokyo (in Japanese)

    Google Scholar 

  • Minkenberg OPJM (1990) Reproduction of Dacnusa sibirica (Hymenoptera: Braconidae), an endoparasitoid of leafminer Liriomyza bryoniae (Diptera: Agromyzidae) on tomatoes, at constant temperatures. Environ Entomol 19:625–629

    Article  Google Scholar 

  • Mitsunaga T, Yano E (2004) The effect of multiple parasitism by an endoparasitoid on several life history traits of leafminer ectoparasitoids. Appl Entomol Zool 39:315–320

    Article  Google Scholar 

  • Miura K, Tagami Y, Ohtaishi M, Iwasaki A (2004) Application of molecular techniques to distinguish Liriomyza trifolii from L. sativae (Diptera: Agromyzidae) on tomato cultivation in Japan. J Econ Entomol 97:964–969

    Article  CAS  PubMed  Google Scholar 

  • Murphy ST, LaSalle J (1999) Balancing biological control strategies in the IPM of New World invasive Liriomyza leafminers in field vegetable Crops. Biocontr News Info 20:91–104

    Google Scholar 

  • Nishino S, Uchida Y (1999) Occurrence of parasitic wasps of Liriomyza trifolii (Burgess) and influence on the harvested amount of crops of the eggplant. Bull Nara Agric Exp Stn 30:11–16 (in Japanese with English summary)

    Google Scholar 

  • Ozawa A, Saito T, Ikeda F (1999) Effect of host plant and temperature on reproduction of American serpentine leafminer, Liriomyza trifolii (Burgess). Jpn J Appl Entomol Zool 43:41–48 (in Japanese with English summary)

    Article  Google Scholar 

  • Ozawa A, Ota M, Saito T (2004) Biological control of the American serpentine leafminer, Liriomyza trifolii (Burgess), on cherry tomato in greenhouse by the parasitoids, Hemiptarsenus varicornis (Girault). Annu Rep Kanto-Tosan Plant Prot Soc 51:123–128 (in Japanese)

    Google Scholar 

  • Palumbo JC, Mullis CH Jr, Reyes FJ (1994) Composition, seasonal abundance, and parasitism of Liriomyza (Diptera: Agromyzidae) species on lettuce in Arizona. J Econ Entomol 87:1070–1077

    Article  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–666

    Article  Google Scholar 

  • Perrings C, Dehnen-Schmutz K, Touza J, Williamson M (2005) How to manage biological invasions under globalization. Trends Ecol Evol 20:212–215

    Article  PubMed  Google Scholar 

  • Reitz SR, Trumble JT (2002a) Competitive displacement among insects and arachnids. Annu Rev Entomol 47:435–465

    Article  CAS  PubMed  Google Scholar 

  • Reitz SR, Trumble JT (2002b) Interspecific and intraspecific differences in two Liriomyza leafminer species in California. Entomol Exp Appl 102:101–113

    Article  Google Scholar 

  • Reitz SR, Gao Y, Lei Z (2013) Insecticide use and the ecology of invasive Liriomyza leafminer management. In: Trdan S (ed) Insecticides-development of safer and more effective technologies. In Tech, Rijeka, pp 235–255

    Google Scholar 

  • Saito T (1992) Outbreak of Liriomyza trifolii Burgess in Japan and its control. Plant Prot 46:103–106 (in Japanese)

    Google Scholar 

  • Saito T (1997) Mamehamoguribae. Nosan-gyoson-bunka-kyokai, Tokyo (in Japanese)

    Google Scholar 

  • Saito T (2004) Insecticide susceptibility of the leafminer, Chromatomyia horticola (Goureau) (Diptera: Agromyzidae). Appl Entomol Zool 39:203–208

    Article  CAS  Google Scholar 

  • Saito T (2006) Glasshouse pests and microbial control. Annu Rep Plant Prot North Japan 57:1–9 (in Japanese)

    Google Scholar 

  • Saito T, Oishi T, Ikeda F, Sawaki T (1992) Effect of insecticides on the serpentine leafminer, Liriomyza trifolii (Burgess) (Diptera: Agromyzidae). Jpn J Appl Entomol Zool 36:183–191 (in Japanese with English summary)

    Article  Google Scholar 

  • Saito T, Oishi T, Ozawa A, Ikeda F (1995) Effects of temperature, photoperiod, and host plants on development and oviposition of Liriomyza trifolii (Burgess) (Diptera: Agromyzidae). Jpn J Appl Entomol Zool 39:127–134 (in Japanese with English summary)

    Article  Google Scholar 

  • Saito T, Doi M, Tagami Y, Sugiyama K (2008) Hymenopterous parasitoids of the exotic leafminers Liriomyza trifolii (Burgess) and Liriomyza sativae Blanchard (Diptera: Agromyzidae) in Shizuoka Prefecture, Japan. Jpn J Appl Entomol Zool 52:225–229 (in Japanese with English summary)

    Article  Google Scholar 

  • Sakamaki Y, Miura K, Chi Y (2005) Interspecific hybridization between Liriomyza trifolii and Liriomyza sativae. Ann Entomol Soc Am 98:470–474

    Article  Google Scholar 

  • Scheffer SJ (2000) Molecular evidence of cryptic species within the Liriomyza huidobrensis (Diptera: Agromyzidae). J Econ Entomol 93:1146–1151

    Article  CAS  PubMed  Google Scholar 

  • Scheffer SJ, Lewis ML (2001) Two nuclear genes confirm mitochondrial evidence of cryptic species within Liriomyza huidobrensis (Diptera: Agromyzidae). Ann Entomol Soc Am 94:648–653

    Article  CAS  Google Scholar 

  • Scheffer SJ, Lewis ML (2005) Mitochondrial phylogeography of vegetable pest Liriomyza sativae (Diptera: Agromyzidae): divergent clades and invasive populations. Ann Entomol Soc Am 98:181–186

    Article  CAS  Google Scholar 

  • Scheffer SJ, Lewis ML (2006) Mitochondrial phylogeography of the vegetable pest Liriomyza trifolii (Diptera: Agromyzidae): diverged clades and invasive populations. Ann Entomol Soc Am 99:991–998

    Article  Google Scholar 

  • Scheffer SJ, Wijesekara A, Visser D, Hallett RH (2001) Polymerase chain reaction-restriction fragment-length polymorphism method to distinguish Liriomyza huidobrensis from L. langei (Diptera: Agromyzidae) applied to three recent leafminer invasions. J Econ Entomol 94:1177–1182

    Article  CAS  PubMed  Google Scholar 

  • Shepard BM, Braun SAR (1998) Seasonal incidence of Liriomyza huidobrensis (Diptera: Agromyzidae) and its parasitoids on vegetables in Indonesia. Int J Pest Manage 44:43–47

    Article  Google Scholar 

  • Shindo J, Kinota M, Inokuchi S, Kimura Y, Fujimura T (2005) Occurrence of pea leafminer, Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae), in Aomori Prefecture. Ann Rept Plant Prot North Jpn 56:145–148 (in Japanese with English summary)

    Google Scholar 

  • Spencer KA (1973) Agromyzidae (Diptera) of economic importance. Junk, Hague

    Book  Google Scholar 

  • Takafuji A, Ozawa A, Nemoto H, Gotoh T (2000) Spider mites of Japan: their biology and control. Exp Appl Acarol 24:319–335

    Article  CAS  PubMed  Google Scholar 

  • Takano S, Iwaizumi R, Nakanishi Y, Someya H, Iwasaki A (2005) Genetic differentiation and morphological comparison between two clades of Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae). Res Bull Pl Prot Jpn 41:43–46 (in Japanese with English summary)

    Google Scholar 

  • Takano S, Iwaizumi R, Nakanishi Y, Someya H (2008) Laboratory hybridization between the two clades of Liriomyza huidobrensis (Diptera: Agromyzidae). Appl Entomol Zool 43:397–402

    Article  CAS  Google Scholar 

  • Tian YF, Sakamaki Y, Tsuda K, Kusigemati K (2008a) Species composition of Liriomyza bryoniae, L. trifolii and L. sativae infesting vegetables and flowers in Kagoshima Prefecture. Kyushu Plant Prot Res 54:112–117 (in Japanese with English summary)

    Article  Google Scholar 

  • Tian Y-F, Sakamaki Y, Tsuda K, Kusigemati K (2008b) Species composition and hostplants for Liriomyza trifolii and L. sativae inside and outside of plastic greenhouses in the southern part of the Satsuma peninsula in Kagoshima Prefecture. J Jpn Soc Agric Tech Manage 15:35–43 (in Japanese with English summary)

    Google Scholar 

  • Tokumaru S (2008) The current situation and problems of the studies on biology and control of leafminer flies. Ann Rept Kansai Plant Prot 50:55–59 (in Japanese)

    Article  Google Scholar 

  • Tokumaru S, Abe Y (2001) Biology of the vegetable leafminer, Liriomyza sativae Blanchard, in Kyoto Prefecture. Plant Protect 55:64–66 (in Japanese)

    Google Scholar 

  • 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). Jpn J Appl Entomol Zool 47:143–152 (in Japanese with English summary)

    Article  Google Scholar 

  • Tokumaru S, Abe Y (2005a) Interspecific hybridization between Liriomyza sativae Blanchard and L. trifolii (Burgess) (Diptera: Agromyzidae). Appl Entomol Zool 40:551–555

    Article  Google Scholar 

  • Tokumaru S, Abe Y (2005b) Effects of host plants on the development and host preference of Liriomyza sativae, L. trifolii, and L. bryoniae (Diptera: Agromyzidae). Jpn J Appl Entomol Zool 49:135–142 (in Japanese with English summary)

    Article  Google Scholar 

  • Tokumaru S, Kurita H, Fukui M, Abe Y (2005) Insecticide susceptibility of Liriomyza sativae, L. trifolii, and L. bryoniae (Diptera: Agromyzidae). Jpn J Appl Entomol Zool 49:1–10 (in Japanese with English summary)

    Article  CAS  Google Scholar 

  • Tokumaru S, Ando Y, Kurita H, Hayashida Y, Ishiyama M, Abe Y (2007) Seasonal prevalence and species composition of Liriomyza sativae Blanchard, L. trifolii (Burgess), and L. bryoniae (Kaltenbach) (Diptera: Agromyzidae) in Kyoto Prefecture. Appl Entomol Zool 42:317–327

    Article  Google Scholar 

  • Torchin ME, Lafferty KD, Dobson AP, McKenzie VJ, Kuris AM (2003) Introduced species and their missing parasites. Nature 421:628–630

    Article  CAS  PubMed  Google Scholar 

  • Trumble JT, Nakakihara H (1983) Occurrence, parasitization, and sampling of Liriomyza species (Diptera: Agromyzidae) infesting celery in California. Environ Entomol 12:810–814

    Article  Google Scholar 

  • Tsuruta S, Gyoutoku Y, Iwamoto E, Koga S (2001) Trapping tests for vegetable leaf miner, Liriomyza sativae (Blanchard), using several sticky traps. Kyushu Plant Prot Res 47:103–107 (in Japanese)

    Article  Google Scholar 

  • Wang H, Reitz SR, Xiang J, Smagghe G, Lei Z (2014) Does temperature-mediated reproductive success drive the direction of species displacement in two invasive species of leafminer fly? PLoS One 9(6):e98761

    Article  PubMed  PubMed Central  Google Scholar 

  • Yamamoto K, Ookubo T, Morishige H, Tonogouchi H, Honda Y, Izumi K (2007) Study on the occurrence and chemical tolerance of tomato leaf miner (Liriomyza sativa Blanchard) emerged in Yamaguchi Prefecture. Bull Yamaguchi Agric Exp Stn 56:71–78 (in Japanese with English summary)

    CAS  Google Scholar 

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Acknowledgements

I am very grateful to have been invited by the Japanese Society of Applied Entomology and Zoology to write this review on exotic leafminer flies in recognition of the society’s award of a fellowship. Thanks are also due to the chief editor, Prof. T. Gotoh, for his encouragement, and all my colleagues, especially entomologists in Kyoto Prefectural University and Kyushu University, for their support of this study. Comments by anonymous reviewers improved the manuscript. I thank Dr. T. Ide for drawing the figures.

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  1. Biosystematics Laboratory, Faculty of Social and Cultural Studies, Kyushu University, Motooka, Nishi-Ku, Fukuoka, 819-0395, Japan

    Yoshihisa Abe

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Abe, Y. Invasion of Japan by exotic leafminers Liriomyza spp. (Diptera: Agromyzidae) and its consequences. Appl Entomol Zool 52, 175–182 (2017). https://doi.org/10.1007/s13355-017-0486-z

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