Key words: agricultural invasive pests, biological control agents, natural enemy, risk assessment
Insects invading from foreign environments have been steadily increasing in recent years because of global trade. Moreover, many exotic species have been imported as pets. Some of them have settled and caused some problems. For example, living exotic stag beetles and rhinoceros beetles have been imported since 1999. About 600 species from all parts of the world have been brought into Japan and sold as pets. Many of them did not settle long in Japan but many species of the exotic stag beetles have potential to be naturalized in the country (Araya 2002). Including these pet species, natural enemies and pollinators, alien species in Japan are now over 1,000 species. Morimoto and Kiritani (1995) defined exotic insect species as "those species reproducing naturally in a designated area where they were brought by unusual means, such as air, ocean current and accidental or intentional introduction". The Invasive Species Advisory Committee (ISAC) in USA defines invasive species as "alien species whose introduction does or is likely to cause harm to human health, economy, and environment." The Handbook of Alien Species in Japan (2002) lists 415 insects as exotic species, which are defined as species from foreign countries, and which were established in Japan after the Meiji era (1868). New invasive species were found or some disappeared after the publication of The Handbook of Alien Species in Japan. Missing records were also found. This study re-calculated 304 exotic species that now inhabit the country. Of the 304 species, 217 are agricultural pests species, corresponding to 71.6% of all alien species, and to about 7% of Japanese agricultural pests (The Japanese Society of Applied Entomology and Zoology 2006); 85 species are non-pest species and 10 of them are intentionally introduced insects such as honeybee for pollination and natural enemies for pest control. Countermeasures and risk assessment vary from each category of risks by exotic species. This paper discusses invasive insect problem and risk assessment separately from agricultural pests, biological control agents, and other species.
The most formidable invasive insects are agricultural pests. Invasive agricultural pests are majority alien insects, because their damages can be easily found in the farm. The Plant Protection Station in Japan quarantines plants to prevent invasion of agricultural pest insects and diseases at every port. Species prohibiting to be imported by the Plant Quarantine Law are listed (http://www.pps.go.jp/insect/index.html). In spite of the effort, however, many agricultural pests have invaded and caused damage to crops. The Ministry of Agriculture, Forestry and Fisheries (MAFF) has taken urgent countermeasures and makers of agricultural chemicals have searched for effective pesticides. Invasive pests that severely damage crops are exterminated For example, the melon fly, Bactrocera cucurbitae, and oriental fruit fly, B. dorsolis, were exterminated by sterile insect release method. The national government (MAFF) has provided both financial and technical support for the control projects implemented by the Fruit Fly Eradication Project Office, Okinawa Prefectural Government (OPFFEPO). The project spent 17 billion yen and over 20 years in total. Extermination project of West Indian sweet potato weevil ( Euscepes postfasciatus) and sweet potato weevil ( Cylas formicarius) continues in Okinawa Prefecture and the transport of live sweet potatoes from Okinawa to other prefecture within Japan is prohibited.
One of the important problems in pest control is resistance against chemical pesticides. Many invasive insects already have resistance to some pesticides in their native countries. For example, the legume leafminer, Liriomyza trifolii, having a resistance against many pesticides, has invaded Japan. The brown plant hopper, Nilaparvata lugens, and the whitebacked rice planthopper, Sogatella furcifera, which are not treated as invasive species, fly from overseas every year to Japan, and the damage of rice plants is sometimes severe. For the past three years, the brown plant hopper, which invaded Japan has largely become resistant against imidacloprid and the whitebacked rice planthopper against fipronil (Matsumura et al. 2007). Monitoring and early discovering of the planthoppers are carried out to prevent their heavy damages. Prediction of pest outbreak is conducted as a governmental enterprise and the MAFF in Japan pays about one million dollar a year to all prefectures to entrust monitoring of pests. Invasion of insects, which mediate plant disease, such as viruses is also serious problem. For invasive pest control, use of natural enemies has been tried.
Classical biological control had been done since 1911 mainly for invasive pests control. This involves importing natural enemies from the invasive pests' country of origin. Twenty-nine (29) natural enemies have been imported and released but only 9 species (28%) are established and succeeded as pest control. Recently, classical biological control method has not been used in Japan, because of the high cost in looking for effective natural enemies. Since 2002, all natural enemies have to be registered as biological pesticides. Now, 16 natural enemies are registered as biological pesticides, 11 of them are exotic natural enemies. Potential natural enemies now used in Japan are shown in Table 1.
Biological Control Agents
About 2,000 species of exotic arthropods have been introduced to control arthropod pests in 196 countries or islands during the past 120 years (Lenteren et al. 2006). Though beneficial for pest control, introduction of biological control agents from foreign countries may disturb native ecosystems. Non-target effects of the introduction of biological control agent on local communities and indigenous species have been widely discussed (e.g., Howarth 1983, 1991, Simberloff and Stiling 1996). Adverse effects are possible global extinction of non-target species, reduction in distribution range, reduction in population levels and partial displacement of natural enemies. Many non-target effects of biological control agents have been reported (Lynch and Thomas 2000). One of the famous examples is the introduced lady beetles, which have partially displaced native lady beetles in North America (Obrycki et al. 2000).
Holt and Hochberg (2001) categorized mechanism of non-target impacts of exotic biological control agents into: (a) shared predation; (b) mixed predation and competition; (c) exploitative competition; (d) enrichment; and (e) intra-guild predation. Shared predation means impacts on non-target species reflect interactions between introduced natural enemies and the target pest species. Mixed predation and competition are impacts on non-target species, increased by the presence of competing species. Exploitative competition is that the introduced natural enemies exploit non-target species, attacked by another non-target consumer. Enrichment means that the introduced natural enemies become the diet of native natural enemies and an increase of the native natural enemies results in impacts on non-target prey. Intra-guild predation is that the introduced natural enemies both compete with and attack non-target natural enemies within the same habitat. Studying these non-target impacts of introduced natural enemies determines whether the natural enemies can continue to be used or not.
Other Alien Species
Conservation biologists have been concerned with ecological impacts of all alien species, including plants and animals, on native ecosystem. In 2004, "The Invasive Alien Species Act" was promulgated to prevent adverse effects of alien species on ecosystems. The Cabinet Ordinance of the Ministry of the Environment specifies alien species which cause or likely cause severe adverse effects on ecosystems, as Invasive Alien Species (IAS), and prohibits rearing, planting, storing, carrying, importing, or other handling of IAS. Nineteen (19) insect species are now registered as IAS (http://www.env.go.jp/nature/intro/1outline/list/index.html#kon), which include: 14 species of long armed chafer (Coleoptera: Scarabaeidae); any species of the genus Cheirotonus (without C. jambar), Euchirus, and Propomacrus; a pollinator, Bombus terrestris; and 4 species of ants, namely, red imported fire ant (Solenopsis invicta), fire ant (S. geminata), Argentine ant (Linepithema humile), and little fire ant (Wasmannia auropunctata).
Risk Assessment As Risk Management of Alien Species
Pest risk analysis and assessment are performed to determine whether a pest should be regulated and the strength of any phytosanitary measures to be taken against it. The assessment is the evaluation of the likelihood of entry, establishment or spread of a pest or disease within the territory of an importing country, and of the associated potential biological and economic consequences. It is also the evaluation of the potential for adverse effects on human or animal health arising from the presence of additives, contaminants, toxins or disease-causing organisms in food, beverages or feedstuffs. The Plant Protection Office in Japan plans to apply pest risk analysis to all pests and strengthen the prevention of pests invading from oversea.
To prevent undesirable non-target impacts of introduced biological control agents on Japanese ecosystems, the Ministry of the Environment announced "Guidelines on Introduction of Environmental Impact Assessment of Biological Control Agents" in 1999. The detail of the guideline was summarized at international workshop on material circulation through agro-ecosystems in East Asian and assessment of its environmental impact at Tsukuba in 2003 (Mochizuki 2004). The guideline shows the stepwise procedure for environmental (=ecological) impact assessment of exotic biological control agents. Agricultural Chemicals Inspection Station performs the ecological risk assessment of exotic biological control agents following the guideline and decides their import and use. But this guideline is qualitative and not objective.
For four years since 1998, the evaluating environmental risks of biological control (ERBIC) project has been done in Europe to: (1) determine the negative and positive effects of the introduction and use of biological control agents for pest control on non-target species; (2) develop rapid and reliable methods to assess the potential risk of import and release of the biological control agents in Europe; and (3) design specific European guidelines to ensure that biological control agents which are to be introduced as environmentally safe (Lenteren et al. 2003). They proposed a risk assessment methodology for import and release of exotic biological control agents. They modified the system of Hickson et al. (2000). Their method is a quantitative method using risk index, which is calculated by multiplying value of likelihood (probability) of the impact and magnitude (consequence) of the impact. Assessment elements are composed of the five ecological determinants; the potential of an agent to establish in its novel environment, its abilities to disperse, its host range, and its direct and indirect effects on non-target species.
Mochizuki (2008) modified their methodology and proposed a new assessment procedure consisting of six elements: (1) establishment; (2) dispersal; (3) host range; (4) direct effect on rare or endemic species; (5) competition with native species; and (6) hybridization with native species. Tables 2 and 3 show the criteria of likelihood and magnitude of the impact. A numerical value (1-5) is assigned to the likelihood (L) and magnitude (M) of each element, and risk index must be calculated by multiplying values for L and M (L x M) for each element and adding the values of all six elements.
Since some cases need immediate importation of biological control agents, Mochizuki proposed a short-cut decision making procedure for permission to avoid unnecessary research time and costs. The first step is risk assessment by adding the values (risk index-1; RI-1= S Ln x Mn, n = 1 - 3) of the first three elements; establishment, dispersal and host range based on the first criteria ( Table 2). If the value does not exceed a standard value for RI-1, the risk is low and introduction is permitted and no more studies are necessary for the rest of the three elements, and if it exceeds the standard value, the risk is unclear and risk assessment should be performed by total values (total risk index: TRI= S Ln x Mn, n = 1 - 6) of all six elements based on the first and second criteria ( Table 2 and Table 3).
If TRI does not exceed a standard value for TRI, the introduction should be permitted but carefully. If it exceeds the standard value, the introduction should be prohibited or permitted with some conditions, such as use only in closed green house.
The standard values for each index are determined by examples in Japan and other countries. The risk indices for all natural enemies intentionally introduced in Japan since 1911 are calculated ( Table 4). Non-target effects of introduced natural enemies have not been reported in classical biological control agents and RI-1 does not exceed 40. RI-1 of Rodolia cardinalis is 39, but no non-target effects have been reported for 100 years from introduction. On the other hand, biological control agents such as Coccinella septempunctata have been reported on a large non-target effect in North America (e.g., Elliot et al. 1996, Obrycki et al. 2000). In this case, the RI-1 corresponds to 65 and TRI is 98. Mochizuki determined the threshold of decision making of introduction as RI-1 = 40 and TRI = 80. Fortunately, Coccinella septempunctata is an indigenous lady beetle and there is no problem using it for biological control in Japan. This proposal shows a method of decision making of importation only by risk. For beneficial insects such as biological control agents and pollinators, risk-benefit analysis will supply a well-balanced decision making, though risk-benefit analysis is a very difficult procedure.
For the other alien species, an environmental risk assessment is done. But quantitative risk analysis has not been conducted sufficiently. Any environmental risk assessment first identifies the hazards (intended as potential to cause harm), subsequently estimates the risk (intended as the likelihood of that potential being realized) of environmental importance (intended to refer to the routes of exposure for both humans and animals) (Calow, 1997). It is difficult to identify hazards of environmental importance for non-pest species. However, the risk assessment methods of pest and biological control agents serve as reference.
Prevention of entry is the first and most important line of defense against invasive species (Baker et al. 2005, Wittenberg and Cock 2001). If precaution and quarantine are performed, invasions by typhoon and westerlies are unavoidable. Early discovery of new invasive species is necessary. In the precaution list, photos, discrimination keys, habitat information should be included, because there are many similar insect species. An exact identification through DNA barcoding will be helpful (http://www.barcoding.si.edu/INBIPS.htm).
Collecting biological information of alien insects is very important to prevent ecological impact. A web-based global invasive species database (GISD) is a good database for this purpose. In Japan, the National Institute for Environmental Studies maintains an invasive species database (http://www.nies.go.jp/biodiversity/invasive/), but it is written in Japanese only. The National Institute for Agro-Environmental Sciences also developed the "Asian-Pacific Alien Species Database (APASD)" via the Internet since 2004 (http://apasd-niaes.dc.affrc.go.jp/). This database is written in English. The GISD and APASD are useful in knowing the biology of alien species and in making a precautions list. All native species in some countries have a possibility to become invasive species in other countries. Native species must be studied, especially agricultural pests and the information must be shared with other countries.
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Index of Images
Table 1 Natural Enemies Being Used or Promising in Japan
Table 2 The 1ST Criteria of Non-Target Impact of Introduced Biological Control Agents
Table 3 The 2ND Criteria of Non-Target Impact of Introduced Biological Control Agents
Table 4 Example of Index Value for Risk Assessment of Introduced Natural Enemies
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