Termite Pests and Their Control in Taiwan ABSTRACT

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1 Termite Pests and Their Control in Taiwan by Hou-Feng Li 1*, Nan-Yao Su 1, Wen-Jer Wu 2, & Err-Lieh Hsu 2 ABSTRACT Of the 17 named termite species found in Taiwan, five are considered pests of wooden structures and wood products. In this study, two subterranean termites, Coptotermes formosanus Shiraki and Coptotermes gestroi (Wasmann), are the most destructive and are responsible for > 87% of termite infestations while another subterranean termite, Reticulitermes flaviceps (Oshima), occasionally attacked man made structures, resulting in < 1% infestations. The drywood termite, Cryptotermes domesticus (Haviland), and the fungus growing termite, Odontotermes formosanus (Shiraki), contributed 6% infestation each. The liquid termiticide chlorpyrifos, extensively used during the past two decades, has been replaced by another liquid pesticide, fipronil, which had 75% market share. Baiting has recently become more accepted and had 20% market share in Keywords: Coptotermes formosanus, Coptotermes gestroi, liquid termiticide, termite bait INTRODUCTION Taiwan lies across the Tropic of Cancer in the western Pacific Ocean with an average annual rainfall over 2,000 mm (Central Weather Bureau 2010). The warm and humid weather is suitable for termite habitation, and they have been recorded as severe pests in Taiwan for over 200 years (Su 2003). Traditionally, Taiwanese constructed their buildings of wood, and termite infestation is the major factor of biodegradation (Tsai 2007). Termite damage to other cellulose materials, such as papers, books, clothes, blankets, and mats, has been frequently reported (Oshima 1912, Yi 1954, Chao et al. 1989). Termites were also recorded as agricultural pests of fruit trees, sugar cane, 1 Department of Entomology and Nematology, Fort Lauderdale Research and Education Center, University of Florida, 3205 College Avenue, Ft. Lauderdale, FL Department of Entomology, National Taiwan University, 1, Roosevelt Road, Section 4, Taipei 106, Taiwan * Corresponding author, houfeng@ufl.edu 575

2 576 Sociobiology Vol. 57, No. 3, 2011 rice, vegetables, tea (Maki 1919, Yanagihara 1938, Yi 1954), and forestation (Chang and Hung 1986, Yang et al. 2002). More recent buildings were usually constructed of steel and concrete in order to survive frequent earthquakes and typhoons on the island. Today termites no longer cause damage to the frames of structures, but furniture, wooden floors, window frames, doors, ceiling, and other wooden decorations are seriously threatened (Tsai and Chen 2000, Tsai 2007). In addition, there is evidence that termites have chewed through the lead sheathing of electrical and telephone cables and caused short circuits (Yi 1954, Tsai et al. 2004), and damaged other transportation utilities including railroad sleepers, electric poles (Hwang 1962a, Yi 1965), and boats (Oshima 1919, Li et al. 2008). Due to severe termite damage to governmental buildings of the early Japanese colonial period, termite research efforts in Taiwan emerged in the early 1900s (Huang 2005). Government institutes including the Agricultural Experiment Station, the Bureau of Civil Engineering, and the Institute of Science were involved in termite control and prevention. Termite taxonomy, construction practices, termiticides, and wood preservation techniques were studied between 1904 and 1917 (Huang 2005). Most chemicals used in Taiwan during Japanese colonization were wood preservatives or termite repellent, such as coal tar, creosote oil, and camphor oil, spread on wood surface (Oshima 1909, 1911, 1912; Yi 1954). After World War II, termite research in Taiwan almost stopped, and control methods and chemicals used were adapted from United States and European countries. In the late 1940s, arsenical compounds were widely employed for soil and wood treatment for termite control (Yi 1954). The local manufacturer of organochlorides began in the mid-1950s (Yi 1954). Between 1950s and 1970s, organochlorides including DDT, hexachlorobenzene (BHC), aldrin, dieldrin, heptachlor, trichlorobenzene, and pentachlorophenol were suggested for treatment of soil, and sodium fluosilicate, arsenical compounds, DDT and BHC were recommended for remedial treatment of wood (Yi 1954, 1965; Chang 1962, Wang 1979). After most organochlorides were banned or phased out in the mid-1980s, organophosphates, particularly chlorpyrifos, became the major termiticides in Taiwan. Since concerns have arisen over its potential contamination of groundwater, the overall use of chlorpyrifos in termiticides was cancelled in the United States in Tsai and Lai (2004) predicted that

3 Li, H-.F. et al. Termite Pests in Taiwan chlorpyrifos will also be phased out from the market in Taiwan, and replaced by other available chemicals, including pyrethroids, neonicotinoids, fipronil, propoxur, and boric acid. No specific requirement to prevent termite damage is in construction codes and pre-treatment is not mandatory in Taiwan; hence, pest control operators (PCOs) primarily offer remedial control. Chemical treatment is generally considered the major tool for termite control in Taiwan, but no quantitative data on termiticide use has been reported so far. The objectives of the current study includes a verification of the economic status of termite pests in Taiwan, and a quantification of current termiticide use. MATERIALS AND METHODS A questionnaire was designed for licensed PCOs to quantify termite damage and the control measures used in Taiwan in Six questions were included: 1. How many termite-control services were offered by your company in each Taiwanese county in 2008? 2. Among these infested structures, of what percentages were residential, industrial, commercial, historical, and others? 3. What termiticides were used, and in what proportions? In cases where more than one was used for a single structure, indicate the combination used, and proportion of total cases that required two or more termiticides. 4. What was the proportion of each termiticide s cost to the corresponding service charge of treatment? 5. Was an effort made to identify termite species? 6. If termites were identified, what species were present and in what proportions? The questionnaires were delivered to PCOs through the Taiwan Environmental Pest Management Association (TEPMA) and then phone interviews were conducted to obtain further information. All reported cases from the valid questionnaires were lumped and used for calculating the proportions of control cases from each county, proportions of infested buildings by each termite species, proportions of infested buildings of each type, and percentage of each termiticide used by the user PCOs. The average cost of each termiticide was based on the data offered by the user PCOs. Posted information on the website of the Environmental Protection Administration of Taiwan (EPAT) regarding licensed pest control companies in each county (Anonymous 2009a) and permitted pesticides (Anonymous 2009b) were used for related analysis. The correlation between the number 577

4 578 Sociobiology Vol. 57, No. 3, 2011 of termite control cases in each county reported from questionnaires and the number of registered PCOs in each county from EPAT s database were tested by correlation analysis (SAS Institute 1985). RESULTS AND DISCUSSION Questionnaire and registered pest control companies Of the 107 questionnaires sent, 23 ( 21%) were returned and 17 ( 16%) were completed. Since some questions were related to commercial activities, many PCOs did not return the questionnaires. A total of 1,934 termite control cases were reported from the 17 valid questionnaires. The number of termite control cases in each county was strongly correlated to the number of registered pest control companies in each county (r = 0.95, p < , SAS Institute 1985) (Table 1) which indicated that these cases were representative for termite control business in Taiwan. There were 732 registered pest control companies in Taiwan (Anonymous 2009a), and they were primarily located in three densely populated counties, Taipei, Taichung and Kaohsiung (Table 1). Infested buildings Of the 1,934 termite control cases, 75% were conducted on residential premises, 8% on commercial buildings, 6% on industrial constructions, 5% on governmental buildings, 5% on historical constructions, and < 1% on trees. The results showed that termite infestations of residential premises remain, even though most modern buildings are constructed of steel and concrete. It is worth noting that 5% of control cases were conducted on historical buildings in the current survey. Termite damage is generally believed to be the major factor of biodegradation of historical buildings in Taiwan (Chao et al. 1989, Lin and Hong 2002, Tsai 2007). The annual budget for cultural property conservation and research of the central government increased from 2 to 28 million USD between 2004 and 2008 (Lin 2005, 2006, 2007, 2008, 2009). Termite pests Twelve of the 17 PCOs ( 70%) identified termite species when they offered termite control service. Of the total 1,638 termite control cases, >87% were caused by Coptotermes spp., 6% by Cryptotermes domesticus (Haviland), 6%

5 Li, H-.F. et al. Termite Pests in Taiwan 579 Table 1. Distribution of licensed PCOs and termite control cases in Taiwan. Area County No. of licensed PCOs (%) a No. of cases b Northern Taiwan Taipei c 315 (43.0%) 787 (40.7%) Taoyuan 55 (7.5%) 164 (8.5%) Hsinchu d 22 (3.0%) 133 (6.9%) Miaoli 1 (0.1%) 17 (0.9%) Central Taiwan Taichung e 94 (12.8%) 192 (9.9%) Changhua 25 (3.4%) 51 (2.6%) Yunlin 7 (1.0%) 5 (0.3%) Nantou 9 (1.2%) 12 (0.6%) Southern Taiwan Chiayi f 16 (2.2%) 25 (1.3%) Tainan g 60 (8.2%) 360 (18.6%) Kaohsiung h 92 (12.6%) 153 (7.9%) Pingtung 11 (1.5%) 21 (1.1%) Eastern Taiwan Yilan 2 (0.3%) 1 (0.1%) Hualien 10 (1.4%) 4 (0.2%) Taitung 8 (1.1%) 6 (0.3%) Islands Penghu 2 (0.3%) 2 (0.1%) Kinmen 2 (0.3%) 1 (0.1%) Lienchiang 1 (0.1%) 0 (0.0%) Total 732 (100.0%) 1,934 (100.0%) a Information obtained from the website of the Environmental Protection Administration of Taiwan (Anonymous 2009a). b Termite control cases of each county in 2008 reported in 17 valid questionnaires. c Taipei City and Keelung City were included; d Hsinchu City was included; e Taichung City was included; f Chiayi City was included; g Tainan City was included; h Kaohsiung City was included. by Odontotermes formosanus (Shiraki), and < 1% by Reticulitermes flaviceps (Oshima). Among the Taiwanese termites, Coptotermes spp., colloquially known as House Termites, were considered most destructive to wooden structures (Table 2), which matched the result of our current survey. Coptotermes formosanus Shiraki was believed to be the only Coptotermes species in Taiwan (Oshima 1912), but recent studies showed Coptotermes gestroi (Wasmann) were usually found in lowland areas of southern Taiwan and may have been introduced over a hundred years ago (Li 2009, Li et al. 2009a). To differentiate between the soldier castes of C. formosanus and C. gestroi, a microscopic examination is required; hence, the PCOs did not specify the species of Coptotermes in the questionnaires. The drywood termite, Cr. domesticus, was only mentioned few times in previous literature (Table 2), but our current survey showed that it is a common pest of wooden constructions including historical buildings. Cr. domesticus is distributed throughout the island, but most were found in southern Taiwan. The infestation of Cr. domes-

6 Table 2. Termite species and pest status in Taiwan based on previous literature. Taxon Urban Pest b Reference c Agricultural Pest b Reference c Termopsidae 1. Hodotermopsis sjoestedti (Holmgren) Kalotermitidae 2. Cryptotermes domesticus (Haviland) * 13, Glyptotermes fuscus Oshima 4. Glyptotermes satsumensis (Matsumura) 5. Incisitermes inamurae (Oshima) 6. Neotermes koshunensis (Shiraki) Rhinotermitidae 7. Coptotermes formosanus Shiraki ** 1, 2, 5, 7, 9, 10, 11, 12, 14, 15, 17, 20, * 1, 8, 9, 10, 12, 18 21, 22, 24, Coptotermes gestroi (Wasmann) ** Prorhinotermes japonicus (Holmgren) 10. Reticulitermes chinensis Snyder 11. Reticulitermes flaviceps (Oshima) a ** 1, 2, 5, 7, 9, 12, 14, 15, 17, 20, 21, * 8, 9, 11, 12, 14, 18 Termitidae 12. Nasutitermes kinoshitae (Hozawa) 13. Nasutitermes parvonasutus (Shiraki) 22, 25 * 8, 9, 11, Nasutitermes takasagoensis (Shiraki) * 1, Odontotermes formosanus (Shiraki) * 1, 5, 7, 9, 10, 15, 17, 20, 22, 25 ** 1, 3, 4, 6, 7, 8, 9, 10, 11, 14, 15, 16, 18, 19, 20, Pericapritermes nitobei (Shiraki) * 4, 6, 8, 9, 11, 14, Sinocapritermes mushae (Oshima et Maki) * 4, Sociobiology Vol. 57, No. 3, 2011 a R. flaviceps was identified as R. speratus in Taiwan in most of the early literature; b Pest status: **, major pest; *, minor pest. c 1. Oshima (1912); 2. Nawa (1913); 3. Maki (1917); 4. Maki (1919); 5. Oshima (1919); 6. Maki (1920); 7. Sonan (1930); 8. Yanagihara (1938); 9. Yi (1954); 10. Sun (1961); 11. Chang (1962); 12. Hwang (1962a); 13. Hwang (1962b); 14. Yi (1963); 15. Yi (1965); 16. Chang et al. (1978); 17. Wang (1979); 18. Chang and Hung (1986); 19. Chang (1989); 20. Chao et al. (1989); 21. Wu (1991); 22. Chang and Wang (1995); 23. Yang (2002); 24. Tsai et al. (2004); 25. Tsai (2007); 26. Li et al. (2008); 27. Li et al. (2009a).

7 Li, H-.F. et al. Termite Pests in Taiwan ticus was underestimated previously probably due to its cryptic behavior and slower wood-consumption rate than Coptotermes species. The fungus growing termite, O. formosanus, was the most common termite species found in both urban and natural environments below the altitude of 1,000 m throughout Taiwan (Huang 2004, Chiu et al. 2010). O. formosanus may occasionally enter houses from the yards and cause minor damages to wooden structures at points of wood-soil interface. The subterranean termite, R. flaviceps, was recorded as a major pest (Table 2), however, in the current survey, < 1% of termite control cases targeted this species. R. flaviceps was mostly found in either northern Taiwan or in mountainous areas of southern Taiwan. The infestation of R. flaviceps usually occurs at ground floors in moist wood. The reduction of soil-contacted wood use for modern buildings may have reduced infestation of R. flaviceps. So far, 17 named termite species of four families and 12 genera have been recorded in Taiwan (Chung & Chen 1994, Tsai & Chen 2003, Li et al. 2009b). Based on previous studies (Table 2) and the current survey, nine termite species were recorded as urban or agricultural pests. The rhinotermids include C. formosanus, C. gestroi, and R. flaviceps, and are mostly pests in urban environments. Termitids include Nasutitermes parvonasutus (Shiraki), N. takasagoensis (Shiraki), O. formosanus, Pericapritermes nitobei (Shiraki), and Sinocapritermes mushae (Oshima et Maki) and cause various degrees of damage to agriculture crops. The primitive termites, such as termopsids and kalotermitids, are neither urban pests nor agricultural pests, except for Cr. domesticus damaging wooden structures (Table 2). Termiticides Used Currently, 80 pesticide products are labeled for termite control and only seven of them were specialized for this purpose (Anonymous 2009b, Table 3). Four active ingredients, boric acid, hexaflumuron, fipronil, and cypermethrin, are used in the seven specialized termiticide products. Organophosphates and pyrethroids are used primarily in the non-termite-specific pesticides. Among the 80 pesticides, 56 (70%) were Restricted Use Pesticides (RUPs), which are purchased and used only by licensed PCOs. Based on the questionnaire survey, the liquid pesticide with fipronil as the active ingredient was used in 75% of all cases and termite bait containing hexaflumuron was employed in 20%. 581

8 582 Sociobiology Vol. 57, No. 3, 2011 Table 3. Type, cost, and use of termiticides in Taiwan. Registered termiticides a Termiticide use b Termiticide cost / service charge ± SE No. of cases (%) No. of products made in Taiwan No. of restricted use pesticides (%) No. of termiticides (specialized for termites) Active ingredient category Pyrethroids c 49 (3) 31 (63%) 45 (92%) 8 (0.39%) 20.00% Pyrethroids c + organophosphates d 7 (0) 6 (86%) 7 (100%) Organophosphates d 18 (0) 18 (100%) 16 (89%) 66 (3.39%) ± 1.25% Carbamate e 2 (0) 0 2 (100%) Boric acid 2 (2) 0 2 (100%) Benzoyl urea f 1 (1) (19.89%) ± 2.62% Phenylpyrazole g 1 (1) 1 (100%) (74.76%) ± 2.20% Total 80 (7) 56 (70%) 72 (90%) 1905 (98.44%) h a Information obtained from the website of the Environmental Protection Administration of Taiwan (Anonymous 2009b). b Data was generated from questionnaires; c Pyrethroids include alphacypermethrin, bifenthrin, cypermethrin, deltamethrin, d-tetramethrin, esbiothrin, etofenprox, imiprothrin, permethrin, phenothrin, pyrethrins, and tetramethrin; d Organophosphates include chlorpyrifos, pirimiphos-methyl, and fenitrothion; e Carbamate only includes propoxur; f Benzoyl urea only includes hexaflumuron; g Phenylpyrazole only includes fipronil; h Of 1,934 reported cases, no termiticide was used in 29 cases. Chlorpyrifos and pyrethroids only had 4% market share. Even though 90% of the 80 termiticide products were manufactured in Taiwan, 95% market share belonged to two imported products, Termidor, a liquid termiticide with fipronil, and the Sentricon Termite Colony Elimination System with hexaflumuron baits (Table 3). The cost of bait systems accounted for 26% of total service charges, but that of liquid pesticide accounted for 19% (Table 3). Termite bait systems were introduced into Taiwan around 1996, but their use was limited, probably due to their high cost. Due to the concern of potential impact of liquid pesticides on the environment, baiting has gained better acceptance for subterranean termite control, especially at culturally important sites (Su & Hsu 2003, Tsai 2007, Lou 2009). Most urban constructions in Taiwan are multi-story buildings without yards, requiring above-ground baiting systems to be used in 95% of cases instead of in-ground baiting stations. Since termite bait systems are not effective against drywood termites and higher termites, such as Cr. domesticus and O. formosanus, PCOs applied a combination of

9 Li, H-.F. et al. Termite Pests in Taiwan both bait systems and chemical treatment to control subterranean termites and drywood termites, in 2% of total cases in the current survey. In conclusion, C. formosanus and C. gestroi are the most serious termite pests in Taiwan and responsible for over 87% of termite control cases in Most of the infested buildings were residential premises (75%). Liquid termiticide with fipronil and termite bait with hexaflumuron were the two primary products used by PCOs, representing 75% and 20% market shares, respectively. ACKNOWLEDGMENTS The authors thank Prima Chien (Taiwan Environmental Pest Management Association) for delivering questionnaires, and Aaron Mullins and Paul Bardunias (University of Florida) for reviewing the manuscript. This study was supported in part by a grant from USDA-ARS under the grant agreement No REFERENCES Anonymous. 2009a. Information system of licensed pest control operator. gov.tw/mdc/search/search_permit.aspx?applykind=2&image=2b Anonymous. 2009b. Information system of permitted pesticide. mdc/search/search_license.aspx Center Weather Bureau Climate statistics. Chang, S.-S Life cycle and control method of termite. Farmer's Friend 13: 52. (in Chinese) Chang, S.-T Termite ecology and their control methods. Forest Products Industries 8: (in Chinese) Chang, S.-T., & S.-Y. Wang Wood preservative treatment and termite prevention treatment, pp In Y.-S. Wang (ed.), Wooden structure and housing conditions. Architectural Institute of Wooden Construction of the Republic of China, Taipei, Taiwan. (in Chinese) Chang, T.-L., S. Cheng, & C.-Y. Cheng A study on the chemical composition of the ant-hill of Odontotermes formosanus Shiraki. Taiwan Mushrooms 2: (in Chinese) Chang, Y.-C., & L.-M. Hung Isoptera, p. 7. In Y.-C. Chang & L.-M. Hung (eds.), A list of forest insect-pests and their host plants in Taiwan. Taiwan Forestry Research Institute, Taipei, Taiwan. (in Chinese) Chao, G.-D., H.-J. Wu, & Y.-S. Chow Investigation and ecological analysis of pests on historical buildings. Council for Cultural Affairs, Taipei, Taiwan. (in Chinese) 583

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