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The status quo of invasive alien insect species and plant quarantine in Korea Ki Jeong Hong a Jong Ho Leeb Gwan Seok Leec Seunghwan Leed a Department of Animal and Plant Health Research Animal Plant and Fisheries Quarantine and Inspection Agency Suwon 443 400 Republic of Korea b Department of Plant Quarantine Animal Plant and Fisheries Quarantine and Inspection Agency Anyang 430 016 Republic of Korea c Department of Agricultural Biology National Academy of Agricultural Science RDA Suwon 441 707 Republic of Korea d School of Agricultural Biotechnology Seoul National University Seoul 151 742 Republic of Korea a b s t r a c ta r t i c l ei n f o Article history Received 18 July 2011 Revised 12 June 2012 Accepted 12 June 2012 Keywords Invasive alien insect species Plant quarantine Korea The recent increase in agricultural commodities from abroad and travelers due to the economic growth and globalization in Korea has resulted in an increase in invasive alien insect species establishing in Korea When alien is defi ned as species introduced after the beginning of the Greater Korean Empire Era 1897 171 in sect species are considered invasive alien species On average 0 85 alien insect species have become established each year for the last 40 years and 76 6 of the alien insect species are economic agricultural pests The annual invasion rate and the pest interceptions from imported cut fl owers planting material and vegetables have been increasing rapidly Traveler s baggage is an important pathway for fruit fl ies Most of the alien pests that were fi rst found in Japan were confi rmed in Korea at least 3 years later until the 1990s but the pattern has been reversed since the 2000s Thus continuous information sharing with neighboring countries such as Japan and China is needed to develop a system for early detection and prompt action against invading insect species Thus we introduce and summarize the present status of invasive alien insect species in Korea Korean Society of Applied Entomology Taiwan Entomological Society and Malaysian Plant Protection Society 2012 Published by Elsevier B V All rights reserved Introduction The Korean peninsula is surrounded on three sides by sea except for the northward land connection with the Manchurian plain of China and the Maritime Province of Russia This geographic connec tion has caused sharing of many indigenous insect species between Korea and neighboring areas for some time However the introduc tion of alien insects from other regions was restricted until the beginning of the Greater Korean Empire Era in 1897 Since then inter national trade with other continents has increased dramatically Plant quarantine aims to minimize economic damage to the agri cultural and forestry industries due to alien pests introduced from foreign countries Plant quarantine in Korea began in December 1912 by the Japanese colonial government The colonial government established the Regulations on the fruit trees and the cherry trees Since then the Korean government enacted the Plant Protection Act in December 1961 and amended it according to the WTO SPS Agree ment in December 1995 The Plant Protection Act 1995 has become the mother law harmonizing the quarantine pest concept which is a pest of potential economic importance to the area endangered thereby and not yet present there or present but not widely distrib uted and being offi cially controlled FAO 2010 In recent decades the world has entered a new phase for the mag nitude and diversity of biological invasions the Era of Globalization Globalization a result of economic growth and transport effi ciency has been examined in relation to its infl uence on biological invasions Hulme 2009 The increasing demand for foreign agricultural com modities a result of the recent economic growth in Korea increases the risk of biological invasion In particular consumer demand for fresh foods fruits and vegetables and ornamental products cut fl owers and plants for planting has been increasing rapidly Import ing these products has resulted in an increase in the number of inva sive alien insect species established in Korea For example 152 species were reported as possible or suspected alien insect species by Lee 1996 and many new invasive alien insects have been listed each year since then Despite stringent plant quarantine regulations alien species continue to enter accidently or intentionally and intrude on the insect fauna of Korea Moreover the invasion rate of alien in sect pests has tended to increase As described in the relevant international standards such as the Convention on Biological Diversity UN 2002 and the International Plant Protection Convention FAO 1997 each contracting party shall prevent the introduction of control or eradicate those alien spe cies that threaten plant human and animal health and the environ ment Thus Korea must improve its ability to predict invasions and to assess the potential agricultural or natural ecosystem impact of Journal of Asia Pacifi c Entomology 15 2012 521 532 Corresponding author at Plant Quarantine and Technology Center Department of Animal and Plant Health Research Animal Plant and Fisheries Quarantine and Inspec tion Agency Suwon 443 400 Republic of Korea Fax 82 31 204 0668 E mail address stpeters korea kr K J Hong 1226 8615 see front matter Korean Society of Applied Entomology Taiwan Entomological Society and Malaysian Plant Protection Society 2012 Published by Elsevier B V All rights reserved doi 10 1016 j aspen 2012 06 003 Contents lists available at SciVerse ScienceDirect Journal of Asia Pacifi c Entomology journal homepage introduced species Here we introduce and summarize the present status of invasive alien insect species in Korea Defi nition of invasive alien species An alien species is an individual or population at any life stage or a viable part of an organism that is non indigenous to an area and that has entered by human agency into the area An invasive alien species is also an alien species that has become injurious to plants or that by risk analysis is potentially injurious to plants FAO 2010 In other words the term invasive alien species applies when the abundance and distribution of a nonnative organism exceeds a defi ned and ac cepted environmental standard resulting in a net negative effect on social welfare Invasive alien species are one of the premier threats to the environment and food productivity Cook et al 2010 Kiritani 2003 enumerated three reasons that make the invasive alien species problem worse fi rst changes in environmental factors are incomparable in rate and dimensions with anytime in the past Second the consequences of biological invasions are very diffi cult to predict Finally biological invasions result in faunal homogenization and loss of biodiversity Establishing new pests can be costly due to increased crop dam age control programs and quarantine restrictions on trade Annual damage caused by alien insects and mites in the USA has been esti mated at more than 17 billion Pimental et al 2002 Invasive spe cies have also been identifi ed as a serious global threat to biological diversity and may cause disruption of ecological systems homogeni zation of biota and extinction SCOPE 1996 Current status of invasive alien insect species in Korea We defi ne alien with reference to a cut off date which is the be ginning of the Greater Korean Empire Era 1897 when Korea opened the door to foreign countries If a date further back in history is consid ered most species in Korea would be defi ned as alien Therefore we classify the species without any obvious record of introduction as in digenous including pre Great Korean Empire Era invasions While most alien mammals reptiles and fi shes such as nutria Myocastor coypus American bullfrog Rana catesbeiana and large mouth bass Micropterus salmoides have been intentionally intro duced into Korea Park et al 1998 alien insects except for intentionally introduced natural enemies have been introduced acci dentally or unintentionally As the Korean economy is strongly sustained by international trade it is thought that many alien insect species are unintentionally introduced into Korea via seaports air ports in imported cargo and via inanimate pathways Toy and Newfi eld 2010 such as passenger baggage containers used vehi cles or ships Many alien insect species have already been established in Korea through these various methods Here we propose that 171 species are alien insect species Appendix A based on a comparison of Japan e g Morimoto and Kiritani 1995 Kiritani 2002 with Korea e g Lee 1996 Lee 1996 listed up to 94 species as possible alien insects and 58 species as suspected alien species based on incomplete evidence The taxo nomic grouping of the 171 alien species is presented in Table 1 with their major pathway of invasion Of the 171 alien insect species shown in Table 1 and Appendix A Coleoptera and Hemiptera are represented by 67 species 39 2 and 35 species 20 5 respectively Thus Coleoptera and Hemiptera account for more than half of the alien insect species which is similar to their proportional representation in Japan Kiritani 1998 and the USA Sailer 1983 We examined the extent to which alien insect species contribute to the total number of species in any insect order The 11 species of benefi cial insects that were introduced intentionally were excluded from analysis Alien insect account for 0 6 1 8 0 4 1 8 1 1 9 0 and 1 4 within the largest insect orders of Lepidoptera Coleoptera Hy menoptera Hemiptera Diptera Thysanoptera and other orders re spectively Table 1 We have categorized the alien and native insect fauna in Korea in terms of the pest status of each species based on the List of Plant Dis eases InsectPestsandWeedsinKorea KSPP 1986 Similarly theeco nomic status of the 171 alien insects was examined after becoming established in Korea Of them 131 76 6 15 8 8 14 8 2 and 11 6 4 species are considered agricultural pests hygiene pests non pests and benefi cial insects respectively Table 2 In contrast agricul tural pest species comprise only 17 8 of the native insect fauna This means that alien insects are pestiferous at a rate 4 3 times higher than that among native insects However the pestiferous ratio 4 3 times of alien to native insects in Korea is much lower than the ratio 10 times in Japan Morimoto and Kiritani 1995 This may refl ect that the Japanese insect fauna about 30 000 species is more than twice greater than the Korean insect fauna about 14 000 species Table 1 Taxonomic grouping of the alien insect species in Korea including their major pathway OrderTotal species no a Alien species no Unintentional alien speciesb no Major pathway of invasion Coleoptera366567 39 2 65 1 8 Accidental Hemiptera188935 20 5 34 1 8 Accidental and spontaneous Lepidoptera370321 12 3 21 0 6 Accidental and spontaneous Hymenoptera279115 8 8 7 0 4 Mostly intentional Diptera136815 8 8 15 1 1 Accidental and spontaneous Thysanoptera898 4 7 8 9 0 Accidental Others69710 5 8 10 1 4 Accidental Total14 202171 100 160 1 1 a Paek et al 2010 Checklist of Korean Insects 14 188 spp new alien insects 14 spp listed in this report b Representing the alien insect species except for the intentionally introduced natu ral enemies Table 2 Ecological grouping of the alien insect species in Korea including the proportions of agricultural pest in the alien or native insect fauna OrderTotal species no a Agricultural pest no b Alien species no Sub totalAgricultural pestHygiene pestNon pest Benefi cial insect Coleoptera36655446760 52 Hemiptera18896993530131 Lepidoptera370310162121 Hymenoptera2791102151338 DipterThysanoptera895688 Others6973810451 Total14 2022528 17 8 171131 76 6 15 8 8 14 8 2 11 6 4 a Paek et al 2010 Checklist of Korean Insects 14 188 spp new alien insects 14 spp listed in this report in Appendix A b KSPP 1986 A List of Plant Diseases Insect Pests and Weeds in Korea 2477 spp invasive agricultural pests 51 spp in Appendix A 522 K J Hong et al Journal of Asia Pacifi c Entomology 15 2012 521 532 Insect pest detection from imported consignments The rate of alien species introduced is rising sharply with in creased transport trade travel and tourism between countries and continents Zahid et al 2008 Procedures to control the introduction of alien species tend to confl ict with policies promoting international trade and travel The most effective way to reduce entry of alien pests would be to reduce trade and travel but this approach is politically unacceptable If increased international trade and travel are encour aged as is the worldwide trend the movement vectors of alien spe cies will likely increase in number and variety Cox 1999 A fairly close relationship exists between the commodity type and the insect group represented The type of transportation also tends to be determined by the kind of commodity Table 3 Changes in the number of imported consignments entering Korea since the WTO SPS Agreement after 1996 are shown in Table 3 Among the agricul tural consignments excluding grain medicinal herbs and spices the amount of imported vegetables cut fl owers and seedlings shows the greatest increase It shows an increase of more than 160 times over the last 15 years in the case of vegetables The highest detection rates are on cut fl owers and planting materials seedlings Thus there is a strong positive relationship between the quantity of horti cultural items imported and the number of invading exotic species particularly greenhouse pests as discussed in the following sections Pathways and characteristics of the important alien insect species in Korea When invasive alien insect species were arranged in chronological orderbydecade beginningwiththeearliestknownyearsofoccurrence the representation of the various taxonomic groups has changed mark edlyduringthepast110 years Fig 1 Sixtyinvasivealieninsectspecies were recorded during that period Fig 1 The number of established alien insect species in Korea increased steeply after the Korean War in 1950 The maximum number 16 species in any one decade was recorded in the 1990s Alien insect pests associated with planting materials Many quarantine pests are external or surface feeders and these pests have equal status with internal pests for interrupting export shipments Infestations of surface pests may go undetected such as when individuals are protected within various plant parts in an exported commodity Most of the important fruit tree pests e g scale insects and aphids Table 4 were introduced in association with the importation of nursery trees during the Japanese colonial period 1910 1945 The sessile habit of scale insects increases their opportunity to invade when their host plants are imported from overseas If the host plants are then raised under conditions favorable for their growth this also tends to favor the scale insects Two alien insect pests of the superfamily Fulgoroidea have been recently introduced through planting material and are invading agri cultural and forestry ecosystems Table 4 They may have been intro duced as eggs laid between bark tissues of planting material This means that many economically important insect pests with similar habits have a high likelihood of being introduced For example the following pests are considered highly likely to be introduced Asian citrus psyllid Diaphorina citri vector of Huanglongbing disease on citrus and some species of leafhoppers and froghoppers such as Draeculacephala spp a vector of Pierce s disease on grape As shown in Table 3 the detection ratio of insect pests from plant ing materials particularly seedlings was quite higher than those from other items More precise inspection of planting materials at borders and strict control at post border facilities is needed to pre vent invasion and further spread of alien insect pests from imported plantings for propagation Alien insect pests associated with stored products During the Japanese colonial period 1910 1945 many cosmopoli tan stored grain pests including Dermestes vorax Trogoderma granarium Alphitobiusdiaperinus Tenebrio obscurus Triboliumcastaneum andPlodia interpunctella were introduced from Japan Table 5 Many new stored product pests invaded Korea during the period from the Korean War in 1950 to 1980 Korea imported a great quantity of rice wheat barley and livestock feed to cover the shortage of food through aid grains from foreign countries particularly the USA Most of the warehouses were fi rst established after the Korean War due to Table 3 Periodical changes in the inspection number of the whole imported consignment including hand carry and postal packages and the pestadetection ratio shown in parenthesis in entry points of Korea during 1996 2010 Data mining from Pest Information System QIA Items19961998200020022004200620082010 Planting materials7610 1 21 5507 1 85 9743 4 35 10 842 5 47 16 189 4 45 24 120 3 37 27 715 3 73 25 763 2 81 Seeds3677 0 19 3244 0 15 5276 0 17 5821 0 21 8809 0 31 10 162 0 49 10 356 0 17 10 808 0 09 Bulbs1451 0 00 714 1 26 928 4 42 569 9 14 673 22 14 822 8 03 1244 5 14 1913 2 67 Seedlings2482 3 42 1549 5 68 3539 10 57 4452 11 88 6707 8 11 13 136 5 30 16 115 5 91 13 042 5 09 Non planting materials78 560 11 62 77 637 3 29 223 729 2 01 809 989 0 59 2 099 499 0 33 3 599 397 0 21 3 486 545 0 27 3 765 704 0 22 Grains4333 10 20 8476 3 61 48 802 0 41 261 138 0 07 877 505 0 03 1 563 387 0 02 1 236 981 0 02 1 167 263 0 01 Fruits10 887 1 31 10 213 1 10 33 939 0 63 94 349 0 30 398 240 0 28 555 398 0 52 569 507 0 82 284 293 1 21 Vegetables5585 3 81 16 039 3 03 38 962 0 89 166 995 0 37 328 521 0 38 552 929 0 18 721 049 0 22 931 068 0 17 Cut fl owers987 2 03 904 1 00 1990 2 66 2022 2 23 1907 1 99 3890 2 44 3801 5 08 4427 7 79 Forages11 609 29 70 6048 11 09 14 794 10 72 29 830 4 36 26 211 6 26 28 961 4 17 28 331 3 75 30 518 4 04 Medicinal herbs andspices33 550 4 23 29 906 1 00 70 448 0 73 225 825 0 47 440 904 0 23 865 871 0 12 871 545 0
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