Phytosanitary Treatments Against Bactrocera Dorsalis (Diptera: Tephriti- Dae): Current Situation and Future Prospects

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Dohino, Toshiyuki, Hallman, Guy, Grout, Timothy, Clarke, Anthony, Follett, Peter, Cugala, Domingos, Minh Tu, Duong, Murdita, Wayan, Hernandez, Emilio, Pereira, Rui, & Myers, Scott (2017) Phytosanitary treatments against Bactrocera dorsalis (Diptera: Tephriti- dae): Current situation and future prospects. Journal of Economic Entomology, 110(1), pp. 67-79.

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Notice: Please note that this document may not be the Version of Record (i.e. published version) of the work. Author manuscript versions (as Sub- mitted for peer review or as Accepted for publication after peer review) can be identiﬁed by an absence of publisher branding and/or typeset appear- ance. If there is any doubt, please refer to the published source. https://doi.org/10.1093/jee/tow247 1 Dohino et al.: Phytosanitary Treatments Toshiyuki Dohino 2 for Bactrocera dorsalis Yokohama Plant Protection Station 3 Ministry of Agriculture, Forestry, 4 Journal of Economic Entomology and Fisheries 5 Forum Section Yokohama, Kanagawa 231-0801, 6 Japan 7 Phone: +81-45-622-8893 8 Fax: +81-45-621-7560 9 E-mail: [email protected]

11 Phytosanitary Treatments against Bactrocera dorsalis (Diptera: Tephritidae):

12 Current Situation and Future Prospects

14 Toshiyuki Dohino, Guy J. Hallman,1 Timothy G. Grout,2 Anthony R. Clarke,3 Peter A.

15 Follett,4 Domingos R. Cugala,5 Duong Minh Tu,6 Wayan Murdita,7 Emilio Hernandez,8

16 Rui Pereira,1 and Scott W. Myers9

18 Yokohama Plant Protection Station, Ministry of Agriculture, Forestry, and Fisheries,

19 Yokohama, Japan.

20 1Insect Pest Control Section, Joint FAO/IAEA Division of Nuclear Techniques in Food

21 and Agriculture, International Atomic Energy Agency, Vienna, Austria.

22 2Citrus Research International, Nelspruit, South Africa.

23 3School of Earth, Environmental, and Biological Sciences, Faculty of Science and

24 Technology, Queensland University of Technology (QUT), Brisbane, Qld., Australia.

25 4USDA-ARS, Daniel K. Inouye U. S. Pacific Basin Agricultural Research Center, Hilo,

26 HI, USA.

27 5Faculty of Agronomy and Forest Engineering, Universidade Eduardo Mondlane,

28 Maputo, Mozambique.

29 6Plant Quarantine Diagnostic Center, Plant Protection Department, Ministry of

30 Agriculture and Rural Development, Hanoi, Viet Nam.

31 7Pest Forecasting Institute, Ministry of Agriculture, Karawang, Indonesia.

32 8Programa Moscafrut (SAGARPA-SENASICA), Tapachula, Mexico.

33 9USDA-APHIS Center for Plant Health Science and Technology, Otis Laboratory,

34 Buzzards Bay, MA, USA.

36 Abstract

37 Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) is arguably the most important

38 tephritid attacking fruits after Ceratitis capitata (Wiedemann) (Diptera: Tephritidae). In

39 2003 it was found in Africa and quickly spread to most of the sub-Saharan part of the

40 continent destroying fruits and creating regulatory barriers to their export. The insect is

41 causing new nutritional and economic losses across Africa, as well as the losses it has

42 caused for decades in infested areas of Asia, New Guinea, and Hawaii. This new

43 panorama represents a challenge for fruit exportation from Africa. Phytosanitary

44 treatments are required to export quarantined commodities out of infested areas to areas

45 where the pest does not exist and could become established. This paper describes

46 current phytosanitary treatments against B. dorsalis and their use throughout the world,

47 the development of new treatments based on existing research, and recommendations

48 for further research to provide phytosanitary solutions to the problem.

50 Keywords: Bactrocera invadens, cold treatment, heat treatment, oriental fruit fly,

51 quarantine treatment

52 Bactrocera dorsalis (Hendel) (Diptera: Tephritidae), the oriental fruit fly, is

53 one of the world’s worst fruit fly pests and certainly the most pestiferous within the

54 genus Bactrocera. As with all frugivorous tephritids, the damage is done when the

55 female deposits her eggs into fruit where the larvae hatch and feed. Direct crop loss is

56 caused by this feeding and induced fruit drop, but significant indirect loss results when

57 market access opportunities are lost due to quarantine restrictions on potentially infested

58 fruit (Heather and Hallman 2008). The United States, Department of

59 Agriculture-Animal and Plant Health Inspection Service (USDA-APHIS) lists

60 approximately 450 plant species that are considered regulated hosts of B. dorsalis

61 (USDA-APHIS 2015).

62 The invasion and spread of B. dorsalis throughout Africa in the last decade

63 (under the junior synonym B. invadens Drew, Tsuruta and White), has significantly

64 raised the pest profile of B. dorsalis, both as a field and market access problem (Lux et

65 al. 2003, Ekesi et al. 2011). It has also highlighted the operational fact that developing,

66 approving, and implementing new phytosanitary treatments to gain commodity market

67 access in the presence of B. dorsalis has become increasingly complex, but also

68 potentially repetitive depending on commodities, countries, and treatments.

69 The objective of this paper, stemming from an International Plant Protection

70 Convention (IPPC) Secretariat meeting (IPPC 2014), is to summarize the current status

71 of B. dorsalis from a phytosanitary perspective. Aspects of the taxonomy of B. dorsalis

72 and related species are discussed, followed by a summary of the invasion of Africa by B.

73 dorsalis and subsequent impact on market access of host commodities. The core of the

74 paper is a listing and description of approved phytosanitary treatment schedules for B.

75 dorsalis and a summary by region or country of current phytosanitary research and

76 regulatory activities directed at the pest. The paper concludes with suggestions for

77 future research directed toward the development of additional phytosanitary treatments

78 and globally coordinated actions to lessen the economic impact of this invasive species.

79 Taxonomic History and Status of Bactrocera dorsalis

80 Bactrocera dorsalis has a long and complicated taxonomic history which

81 significantly impacts market access and pest management (Clarke and Schutze 2014,

82 Schutze et al. 2015a). The species was first described by Fabricius in 1794 as Musca

83 ferruginea from specimens with red-brown thoraces most likely collected in eastern

84 India. Over the next 200 yr several changes were proposed for the taxonomic status of

85 the species. Hardy (1969) first used the term “complex” with B. dorsalis and noted that

86 it had a predominantly black thorax.

87 Drew and Hancock (1994) described several new species which were

88 morphologically similar to B. dorsalis and which previously were considered to be B.

89 dorsalis. These new species included the Asian papaya fruit fly, B. papayae Drew &

90 Hancock, and the Philippine fruit fly, B. philippinensis Drew & Hancock. Bactrocera

91 invadens was thought to be B. dorsalis when collected for the first time in Kenya (Lux

92 et al. 2003), but was later described as a separate species by Drew et al. (2005).

93 Critically for trade and control, each of these proposed species has a different

94 geographic distribution. Bactrocera dorsalis occurs from India across to eastern Asia

95 and south-eastern China, B. papayae occurs in southern Thailand, Malaysia, and

96 Indonesia, B. philippinensis in the Philippines, and B. invadens in Africa and Sri Lanka

97 (Schutze et al. 2015a).

98 Bactrocera papayae, B. philippinensis, and B. invadens have proven very

99 difficult to separate morphologically from B. dorsalis (Clarke et al. 2005, Drew et al.

100 2005). This has prompted several authors to suggest that they are all one biological

101 species (Tan et al. 2011, 2013, Schutze et al. 2012). Drew and Romig (2013)

102 subsequently made B. philippinensis a synonym of B. papayae based on morphology.

103 They also reported that B. dorsalis, B. papayae, and B. invadens were separate species

104 and that B. invadens was excluded from the “B. dorsalis species complex” due to its

105 thoracic color. A recent large, international project coordinated by the Joint Food and

106 Agriculture Organization/International Atomic Energy Agency (FAO/IAEA)

107 Programme of Nuclear Techniques in Food and Agriculture has applied a suite of

108 independent tools to determine if these are the same biological species (De Meyer et al.

109 2015a). These tools include mating compatibility studies (Schutze et al. 2013, Bo et al.

110 2014), multiple genetic tests (San Jose et al. 2013), pheromone analysis (Tan et al. 2011,

111 2013), cytogenetics (Augustinos et al. 2014), and morphological and morphometric

112 analysis (Krosch et al. 2012, Schutze et al. 2012, 2015b). This work has been

113 summarized in Schutze et al. (2015a) and Hendrichs et al. (2015), with the conclusion

114 that there are no consistent differences in any of these characteristics to justify the

115 species remaining separate. As a result, the species B. dorsalis, B. philippinensis, B.

116 papayae, and B. invadens have been formally synonymized (Drew and Romig 2013,

117 Schutze et al. 2015a), meaning that of the four only B. dorsalis should now be

118 recognized as a taxonomically and biologically valid species. This synonymization is

119 recognized by a growing number of plant protection organizations.

120 In another taxonomic change, recent revision elevates the subgenus Bactrocera

121 (Zeugodacus) to genus status; this new genus would include important economic

122 species such as B. (Zeugodacus) cucurbitae (Coquillett) and B. (Zeugodacus) tau

123 (Walker) (De Myer 2015b; Virgilio et al. 2015). Because B. dorsalis and B. cucurbitae

124 co-occur across much of their respective geographic ranges, treatments for B. dorsalis

125 are often developed in conjunction with treatments for B. cucurbitae and both are

126 discussed in this paper. While recognizing the status change of Zeugodacus, until more

127 national plant protection organizations accept this taxonomic change, we treat

128 Zeugodacus as a subgenus of Bactrocera in this paper.

129 Origin and Spread of Bactrocera dorsalis

130 Bactrocera dorsalis has a long history of invasion and range expansion

131 throughout Asia and the Pacific (Stephens et al. 2007, Wan et al. 2012). This has

132 contributed to its significance as a global pest and barrier to trade in a wide range of

133 fruit and vegetable commodities. Additionally, its tolerance to a relatively wide range of

134 environmental conditions has aided its ability to colonize new environments, and many

135 warm climate regions throughout the world remain at risk for establishment (Stephens

136 et al. 2007, De Villers et al. 2016). In the United States B. dorsalis has been intercepted

137 in Florida and in California more than 50 times since the 1980s and established

138 populations have been eradicated on multiple occasions (USDA-APHIS 2014).

139 Research suggests detections in California are the result of multiple introductions from

140 various sources, which indicates there is a constant threat of establishment of this

141 species in North America (Barr et al. 2014). Most recently, detections of B. dorsalis in

142 Florida in 2015 triggered establishment of a quarantine that required host commodities

143 to undergo a postharvest phytosanitary treatment before they would be allowed to

144 transit until the pest was eradicated (Alvarez et al. 2016).

145 Bactrocera dorsalis in Africa. Bactrocera dorsalis was recorded in Africa for

146 the first time in 2003 in Kenya (Lux et al. 2003) and within a year in the neighboring

147 countries of Tanzania (Mwatawala et al. 2004) and Uganda (Drew et al. 2005). It was

148 subsequently described in Africa as B. invadens (Drew et al. 2005) and was thought to

149 have originated from Sri Lanka. Subsequent genetic work (Khamis et al. 2009)

150 confirmed that the fly seemed to have first invaded eastern Africa and dispersed from

151 there to the rest of mainland Africa south of the Sahara, with the exception of parts of

152 South Africa where it is still absent. The most economically important host for B.

153 dorsalis in Africa is mango, followed by guava, (Mwatawala et al. 2006, 2009, Goergen

154 et al. 2011, Vayssieres et al. 2014). The fact that these hosts are common in all

155 inhabited regions of tropical and subtropical Africa may explain why the fly has

156 dispersed so rapidly. Furthermore, there have been a number of other commercial hosts

157 listed for B. dorsalis in Africa (Goergen et al. 2011, Vayssieres et al. 2014). The host

158 list in Africa is expected to increase, as hundreds of hosts are recorded for B. dorsalis in

159 other parts of the world (CABI 2016, USDA-APHIS 2015).

160 Initially there were few coordinated attempts to monitor and control the pest in

161 the field (Ekesi et al. 2011, Vayssieres et al. 2009). Later an intensive, coordinated

162 surveillance network with an early detection response action plan was implemented for

163 B. dorsalis in South Africa (Manrakhan et al. 2011a). Field research involving protein

164 baits and male annihilation was conducted by South Africans in eastern Africa to gain

165 experience controlling the pest before it arrived in South Africa (Grout and Stephen

166 2013) and early incursions in South Africa were successfully eradicated using these

167 techniques (Manrakhan et al. 2011b).

168 Importation into South Africa of 300 tons of avocado per annum from Kenya

169 (Waitathu 2010) and banana worth US$20 million per annum from Mozambique

170 (Cugala et al. 2014) was suspended in 2008 due to the presence of B. dorsalis in the

171 exporting countries. Around this time, Mauritius and Seychelles also stopped the

172 importation of banana, mango, avocado, and citrus from some African countries where

173 B. dorsalis was present (Ekesi 2010).

174 Phytosanitary Treatments

175 Bactrocera dorsalis is the most studied tephritid regarding phytosanitary

176 treatments after C. capitata and its recent invasion of Africa has increased its

177 importance significantly. It was the first tephritid studied for phytosanitary irradiation

178 (Koidsumi 1930), and a few years later vapor heat treatments against the pest were

179 being researched (Koidsumi 1936).

180 In the United States nearly annual detections of B. dorsalis in urban areas and

181 periodically in fruit-production areas trigger treatment requirements and/or host removal

182 for host commodities in newly established quarantine areas. Impacted growers may

183 have little time to prepare for mandatory treatments to move their produce, and in some

184 cases efficacy data are not available to support a treatment. Therefore, as in other areas

185 under threat by B. dorsalis, proactive phytosanitary treatment solutions are a necessity.

186 Heat Treatments. Heat is currently used as a commercial phytosanitary

187 treatment in two basic forms: immersion in water at 46-49°C or exposure to air at

188 43-50°C. Sometimes a distinction is made between “high-temperature, forced air”

189 treatments and “vapor heat” treatments with the distinction being that the former keeps

190 the dew point of the air below the surface temperature resulting in no condensation of

191 water of the fruit surface while the latter results in condensation (Hallman and

192 Armstrong 1994). However, that distinction does not hold up in commercial application,

193 and Heather and Hallman (2008) argue that there is much overlap among the two

194 designations and they should all be referred to as heated air treatments. In this

195 publication we combine them and call those all vapor heat treatments (VHT) in keeping

196 with IPPC (2015) designations. Table 1 lists the currently approved heat treatment

197 schedules against B. dorsalis.

198 The major importing countries using VHT are Australia, South Korea, Japan,

199 and New Zealand. Although the United States has several vapor heat treatments

200 approved, they are mostly lengthy treatments developed >70 yr ago that have not been

201 used commercially in decades (USDA-APHIS 2016). More than half of the VHT were

202 developed and are used in Asia to disinfest mangoes of B. cucurbitae as well as B.

203 dorsalis and range in severity from heating the seed surface to 46.0°C for 10 min to

204 48.0°C for 20 min (Table 1).

205 Treatment severity varies with country of origin; the most severe treatments are

206 done in India and the mildest ones in the Philippines. The range of VHT schedules

207 suggest that there may be differences among fruit hosts that influence the efficacy of

208 VHT. For example, while Philippine mangoes require 10 min at 46.0°C, papayas

209 require 70 min at the same temperature and Thai longans, pomelos, and mangosteens

210 require 20, 30, and 58 min, respectively, at 46.0°C. Some VHT schedules use lower

211 humidity than saturated air (< 90% RH) in the first part of the heat treatment in order to

212 preserve fruit quality (e.g., Philippine papayas, Thai mangoes, pomelos, and

213 mangosteens).

214 Two treatments for lychees combine VHT (46.2 or 46.5°C for 20 min)

215 followed by short (40 or 42 h at 2°C) cold treatment (Table 1); they are designed to

216 preserve lychee quality which may suffer from the 47°C, 20 min VHT.

217 Two hot water immersion treatments are approved against B. dorsalis: one for

218 lychees and longans from Hawaii to the United States mainland and one for mangoes

219 from Pakistan to Australia (Table 1).

220 Cold Treatments. There are several cold treatment schedules for host fruits of

221 B. dorsalis (Table 2). Cold treatments at 1.0°C vary from 12-17 d, and differ depending

222 on importing country and perhaps fruit species; however, there are insufficient

223 schedules to arrive at general recommendations.

224 Ionizing Radiation. There are only two accepted schedules for ionizing

225 radiation against B. dorsalis and these both involve the same dose of 150 Gy (Table 3),

226 which is the generic dose for Tephritidae accepted by the USDA-APHIS (2006) and

227 IPPC (2009).

228 Methyl Bromide Fumigation. Methyl bromide fumigation treatments and the

229 fumigation followed by cold treatments for B. dorsalis are only accepted by the United

230 States (Table 3). Although methyl bromide may still be used for phytosanitary

231 treatments under the quarantine and pre-shipment use exemption in the Montreal

232 Protocol on Substances that Deplete the Ozone Layer, its continued use for that purpose

233 is not guaranteed and alternatives should be sought (UNEP 2006).

234 Research, Development, and Application

235 The following section, divided by geographical areas, describes the status of

236 the use of phytosanitary measures against B. dorsalis and research completed or

237 underway that could lead to further treatment schedules.

238 Africa. As a new invader to the continent, B. dorsalis is receiving much

239 attention. However, other damaging tephritids also exist; e.g., the most widely

240 distributed fruit fly of commercial importance in South Africa is C. capitata. In the

241 eastern and coastal regions of the country, Ceratitis rosa Karsch is often as abundant as

242 C. capitata, particularly during the summer months (De Villiers et al. 2013). The males

243 of both of these species can be monitored with trimedlure (Grout et al. 2011b), and cold

244 treatments for C. capitata are effective against C. rosa (Ware et al. 2004). Both species

245 have a broad host range, and most cold treatments used on exported host plant material

246 need to be effective against C. capitata. A third species, C. cosyra (Walker), is

247 primarily a pest of mango (Grout and Stoltz 2007) and does not respond to trimedlure,

248 but is attracted to terpinyl-acetate. No heat treatments are being used against the above

249 fruit flies in produce that is being exported from South Africa.

250 Although B. dorsalis was at first successfully eradicated along the northern

251 borders of South Africa it eventually established in the subtropical Vhembe region of

252 the northern Limpopo Province inhabited by many subsistence farmers growing mango,

253 banana, guava, and papaya (Manrakhan et al. 2011a). Fruit flies in South Africa are

254 controlled in commercial orchards by protein baits, either as sprays or in bait stations.

255 Male annihilation techniques are used against B. dorsalis because of the potent

256 attractiveness of methyl eugenol to males of this species.

257 Most of the cold treatments used on export produce are intended to kill

258 lepidopteran species which are more difficult to kill with cold than fruit flies. This

259 means that many of the bilateral agreements require a treatment of temperatures < 0°C

260 for 22 d. Treatments T107-e and T107-k (Table 2) have this requirement for the control

261 of Thaumatotibia leucotreta (Meyrick) and it is considered adequate for C. capitata and

262 C. rosa, and in citrus it is considered adequate against B. dorsalis. The same treatment

263 is used for the export of grapes and persimmons to Israel and grapes to China. An even

264 more severe treatment, 0°C for 40 d, is required for the export of apples to Mexico to

265 disinfest them from Grapholita molesta (Busck). This treatment is also considered

266 adequate for B. dorsalis, C. capitata and C. rosa. South Africa exports several kinds of

267 citrus, such as lemons, grapefruits, and Clementine mandarins, to Japan using cold

268 treatments (≤ -0.6°C for 12 d or 14 d). The efficacy of cold treatment for 16 d at

269 temperatures < 1.4°C for exportations was validated in large scale trials (Grout et al.

270 2011c) for C. capitata.

271 Collaborative work on B. dorsalis between South Africa and Kenya resulted in

272 the validation of a cold treatment at ≤ 0.9°C for 16 d for citrus (Grout et al. 2011a) and

273 ≤ 1.5°C for 18 d for avocado (Ware et al. 2012).

274 Without control, direct damage to mango by B. dorsalis in sub-Saharan Africa

275 has been reported to range from 30-80% depending on the cultivar, locality, and season

276 (Ekesi et al. 2006, Rwomushana et al. 2008, Vayssières et al. 2009). In addition to the

277 direct losses, indirect losses attributed to quarantine restrictions have been enormous,

278 and both losses have wide reaching socio-economic implications for millions of rural

279 and urban populations involved in the mango value chain across Africa (Ekesi et al.

280 2011, Vayssières et al. 2014).

281 Kenya has continued to lose US$2 million annually since 2008 due to the B.

282 dorsalis quarantine restriction on Kenyan avocado import by South Africa (Otieno

283 2011). In Uganda, the mango industry alone is threatened to lose > US$116 million

284 annually because of B. dorsalis (Nankinga et al. 2010). The European Union

285 interception rates of African fruits and vegetables due to exotic Tephritidae continue to

286 rise (Guichard 2009). While no study has been made of the losses due to fruit flies

287 across the entire African continent, sections of the industry believe that export trade

288 bans are causing the continent ~ US$2 billion losses annually (Malavasi 2014).

289 In Mozambique B. dorsalis was first recorded in 2007 in Cuamba district in the

290 Northern Province of Niassa (Correia et al. 2008). The occurrence of the pest has led to

291 the suspension of fruit and vegetable exports to Mozambique’s major trading partners,

292 with domestic quarantine measures causing severe financial losses to producers and a

293 virtual cessation of investment, as well as severely compromising food security and

294 internal trade (Cugala et al. 2011).

295 The current export volume for banana in Mozambique is estimated at 35,000

296 tons per year with a foreign exchange value of US$17.5 million. A temporary closure of

297 market access for 3 wk during October 2008 resulted in a loss of US$2.5 million

298 (Cugala et al. 2011, Jose et al. 2013). In the Central province of Manica ~US$ 1.5

299 million has been lost due to quarantine restrictions on the presence of B. dorsalis

300 (Cugala et al. 2011). Collaborative research between Kenya and Mozambique has

301 shown that mature green ‘Cavendish dwarf’ bananas are not hosts of B. dorsalis

302 (although ripe, yellow bananas are) (Cugala et al. 2014), so exports of this crop in the

303 mature green stage from Mozambique to South Africa have resumed.

304 To overcome other restrictions in trade, postharvest phytosanitary treatments

305 are researched. Hot water immersion (12 min at a minimum core temperature of 47°C)

306 is currently used at farmer packing houses in the central Province of Manica,

307 Mozambique, to disinfest mature green mangoes of B. dorsalis for export to South

308 Africa where they are used for processing into juices. In addition to the hot-water

309 treatment, fruit fly preventative action is based on a series of pre-harvest management

310 measures and a bait spraying program with protein hydrolysate and spinosad. The B.

311 dorsalis population is systematically monitored at the production site.

312 There has been no apparent negative impact of hot-water treatment on mango

313 fruit quality, but there is need for a scientific assessment of quality. Also, because the

314 treatment is limited to two cultivars for juicing, further development of the hot water

315 treatment for fresh mangoes and other cultivars is being done. Experience from Kenya

316 has shown that disinfestation of ‘Apple’ mangoes of B. dorsalis could be achieved in 70

317 min at 46.1°C.

318 Research on hot-water treatment for mango has been conducted in Africa

319 (Ducamp-Collin et al. 2008, Self et al. 2012) but has not yet been accepted by importing

320 countries. Ideally, a broadly applicable heat treatment acceptable for all trading partners

321 would be more useful than specific treatments for each country in Africa. Self et al.

322 (2012) suggest that a hot water treatment resulting in a core temperature of 46.5°C

323 could be the basis of a fruit fly quarantine treatment for African mangoes.

324 Asia. Bactrocera dorsalis is native to Asia and has been widespread in many

325 countries there since it was first described.

326 Several species of tephritids besides B. dorsalis infest commercial fruit in

327 China. Novel disinfestation research was done some years ago with B. dorsalis. The

328 efficacy of a combination VHT – cold treatment for lychees was confirmed with > 113

329 thousand eggs (most tolerant stage) while fruit quality was maintained (Liang et al.

330 1994). This combination treatment may reduce damage to lychees compared with VHT

331 or cold alone. A hot water immersion treatment for mangoes was developed by basing

332 the treatment end point on seed surface temperature instead of time; hot water mango

333 treatments have traditionally been based on time (USDA-APHIS 2016). Mangoes were

334 immersed in 46.1°C water until the seed surface was at ≥ 46.0°C for 10 min (Liang et al.

335 1993). Modern heated air treatments are based on a like temperature endpoint, and this

336 approach is more amenable to the development of heat treatments that are effective

337 against broad groups of insects than heat treatments based entirely on time (Heather and

338 Hallman 2008). Storage at 2.0 ± 0.1°C for 14 d disinfested oranges of eggs and larvae of

339 B. dorsalis without harm to the fruit (Liang et al. 1992).

340 In Indonesia there are six known species of Bactrocera of economic

341 importance: B. albistrigata (Meijere), B. carambolae Drew & Hancock, B. cucurbitae,

342 B. dorsalis, B. occipitalis (Bezzi), and B. umbrosa (F.). VHT research is being

343 conducted with B. carambolae, B. dorsalis, and B. cucurbitae. Heating mangoes to a

344 seed-surface temperature of 47.0°C and holding them for 30 min provides mortality of

345 all three flies. Indonesian mangoes have been exported to Persian Gulf countries, Hong

346 Kong, Singapore, and Malaysia without treatment, while export to Japan, Taiwan, South

347 Korea, and China is sought. To maintain quality, mangoes of medium size (250-300 g)

348 and 75-80% maturity are used for VHT, and cool storage must be maintained after

349 treatment. Even distribution of heat in the chamber is critical to efficacy. There is

350 commercial interest in VHT for export of melons and ‘Arumanis’ mangoes, and

351 evaluations are underway for this opportunity.

352 Bactrocera dorsalis and B. cucurbitae had caused serious damage to

353 agricultural products in the southwestern islands of Japan. Bactrocera dorsalis was

354 eradicated in 1986 by the use of the male annihilation technique (MAT) over 18 yr, and

355 B. cucurbitae was eradicated in 1993 by the use of sterile insect technique (SIT) over 22

356 yr (Yoshizawa 1997). Both MAT for B. dorsalis and SIT for B. cucurbitae continue to

357 be employed to prevent fruit fly re-invasion because the eradication area is exposed to a

358 constant risk of fruit fly invasion from neighboring countries.

359 The Ministry of Agriculture, Forestry and Fisheries (MAFF) in Japan approves

360 imports of host plant products when an appropriate quarantine treatment for B. dorsalis

361 has been established by the exporting country and the commercial treatment operation

362 meets the approved treatment protocol. MAFF requires large-scale disinfestation tests

363 after determination of the most tolerant stage of the target fruit fly to the treatment in

364 exporting countries. The disinfestation and temperature data submitted by exporting

365 countries are evaluated, and MAFF also asks exporting countries to confirm that the

366 treatment will not have unacceptable effects on the fruit quality.

367 In 2013 the following fresh fruits treated by phytosanitary treatments against B.

368 dorsalis were imported into Japan according to the annual plant quarantine statistics

369 report (MAFF PPS 2015): Ponkan oranges (85 t), pomelos (2 t), and grapes (17 t) were

370 imported from Taiwan with cold treatment (Table 2); mangoes (3,947 t) from the

371 Philippines, Thailand, Taiwan, Pakistan, Malaysia, and Hawaii, papayas (2,844 t) from

372 the Philippines, Hawaii, and Taiwan, dragon fruits (1,064 t) from Viet Nam and Taiwan,

373 and mangosteens (100 t) and pomelos (1 t) from Thailand were imported with VHT

374 (Table 1), and lychees (392 t) were imported from China and Taiwan with a

375 combination treatment of VHT and cold treatment (Table 1).

376 Based on import inspection in 2002, live larvae of the “B. dorsalis species

377 complex” were found in papaya from the Philippines treated by VHT. This treatment

378 failure resulted in MAFF reviewing the procedure for certifying commercial VHT

379 facilities in exporting countries by conducting performance tests at least once a year and

380 specifying cold spots in the chamber, among other reforms.

381 Japan has been conducting research on factors that affect fruit fly mortality.

382 The results of several in vitro studies are reported below. Dohino et al. (2014) found

383 that eggs generally increased in heat tolerance (44-47°C in vitro) as they aged. For

384 example, 3 h-old eggs of B. dorsalis immersed in hot-water of 46°C for 5 min all died,

385 while a mean of 80% of 30 h-old eggs so treated hatched. Egg age had a much lesser

386 impact on cold treatment. At 3°C for 5 d, 3-18 h-old eggs all died while 25% of 24-30

387 h-old eggs hatched. Kaneyuki et al. (2014) found that in vitro heat (45°C) tolerance of

388 the first instar also varied by age, with early- and mid-aged first instars being more

389 tolerant than late-aged. Further in vitro hot-water (45°C) research by Kaneyuki et al.

390 (2016) found that heat tolerance decreased with increasing age of 1st and 2nd instar B.

391 dorsalis, but increased with increasing age of 3rd instars, with 1st instars being the most

392 tolerant. Third instar B. dorsalis were more tolerant to in vitro immersion in hot-water

393 at 43°C when reared at higher temperatures between 20-35°C (Miyazaki and Dohino

394 2000). A high density of larvae in artificial diet resulted in metabolic heat and a higher

395 rearing temperature than low density and enhanced heat tolerance of 3rd instars to hot

396 water at 46°C (Yamamoto et al. 2008). The results of in vitro testing, however, should

397 be confirmed by testing in infested fruits.

398 A series of VHT tests was conducted on mango infested with eggs of B.

399 dorsalis to clarify the effect of the fruit size/weight, shape, and variety on the mortality

400 of B. dorsalis eggs. Yoshinaga et al. (2009) reported that larger fruit provided higher

401 mortality due to longer exposure time when ‘Carabao’ mangoes in 3 different sizes

402 infested with eggs were heated to raise fruit core temperature to 44-47°C inside a VHT

403 chamber set at 49°C and 95% RH. Yamamoto et al. (2011) reported that when two

404 cultivars, ‘Irwin’ (366 g) and ‘Keitt’ (762 g) of mango infested with B. dorsalis eggs

405 were subjected to VHT at 50°C, the seed-surface temperatures to achieve 100%

406 mortality of eggs were 47°C for Irwin and 45°C for ‘Keitt’, respectively, although the

407 fruit temperature under the peel of both cultivars increased similarly during heating. In

408 addition, Omura et al. (2014) reported that when the same weight (428-481 g) of

409 different shaped ‘Nam Doc Mai’ (flat/elongated) and ‘Kent’ (oval/round) mangoes were

410 heated to 45°C, the rate of temperature change in ‘Nam Doc Mai’ mangoes was greater

411 and mortality of eggs was lower than in ‘Kent’ mangoes; these results indicate that fruit

412 shape may affect mortality in VHT.

413 Ishige et al. (2013) preheated papayas infested with B. dorsalis eggs at 38°C

414 for 30-120 min inside a VHT chamber, then heated them at 47°C and reported that

415 mortality was inversely proportional to exposure time of preheating. They suggested

416 that preheating in VHT might reduce fruit fly mortality when preheating was applied to

417 avoid heat injury of fruit.

418 Kawai et al. (2013) found that relative humidity and cooling method slightly

419 affected the mortality of B. dorsalis eggs in mangoes treated with VHT. At 95% RH

420 mortality when the seed surface reached 46°C was 99.89%, while when the humidity

421 temporarily fell below 90% RH, mortality was 98.23%. After VHT, mortality was

422 99.98% by air cooling but 99.53% by shower cooling.

423 Six tephritid species, B. carambolae, B. correcta (Bezzi), B. dorsalis, B.

424 malaysiensis (Drew & Hancock), B. cucurbitae, and B. tau represent the greatest

425 obstacle to exports of fresh fruits and vegetables from Viet Nam. VHT and irradiation

426 phytosanitary treatments against these tephritids are approved for export of tropical

427 fresh fruits to the United States, South Korea, Japan, New Zealand, Chile, and Australia

428 (PPD 2013).

429 VHT at 46.5°C for 40 min is used to export dragon fruits to Japan, South Korea,

430 New Zealand, and Chile (Table 1). Mangoes exported to New Zealand are vapor

431 heat-treated at 46.5°C for 30 min.

432 Dragon fruits, longans, lychees, and rambutans are exported to the United

433 States with an irradiation treatment of 400 Gy against mealybugs and tephritids.

434 Recently research was conducted to lower the dose for the three species of mealybugs of

435 quarantine concern to the United States to 231 Gy (Doan et al. 2016). Because the

436 radiation dose for B. dorsalis and the other quarantine pest tephritids is 150 Gy, this

437 research should allow the treatment dose for these fruits to be reduced to 231 Gy.

438 Europe. Although B. dorsalis does not occur in the wild in Europe,

439 phytosanitary treatment research is being conducted at the FAO/IAEA laboratories in

440 Seibersdorf, Austria taking advantage of the B. dorsalis populations from many parts of

441 the world maintained there for research on the sterile insect technique and related

442 technologies. Phytosanitary treatment research was initiated at Seibersdorf to develop

443 treatments against the species when it was considered B. invadens.

444 Hallman et al. (2013) showed that the susceptibility of B. dorsalis from Kenya

445 was not greater than that of Ceratitis capitata (Wiedemann) at 0.94°C and suggested

446 that cold treatment schedules used for the latter species would be effective for B.

447 dorsalis. This led to the inclusion of B. dorsalis (under the name B. invadens) in the

448 treatment schedule T107-k for citrus (USDA-APHIS 2016). Furthermore, Hallman et al.

449 (2011) found that the estimated time to achieve 99.9% mortality of 3rd instars in cold

450 treatment at 0.94°C was identical (7.7 d) between the African population and a

451 Thai-sourced population of B. dorsalis. Similarly, mortality estimates were not

452 significantly different between these populations in hot-water treatments at 44.7°C.

453 Myers et al. (2016) found that B. dorsalis populations from Kenya, Malaysia, the

454 Philippines, and Thailand did not differ in cold tolerance when the 3rd instars were

455 reared in navel oranges and subjected to cold treatment at 2.0°C.

456 Oceania. Bactrocera dorsalis is established in Hawaii, having been first found

457 there in the mid-1940s. It is part of a tephritid complex with three other species of

458 economic concern: C. capitata, B. cucurbitae, and B. latifrons (Hendel). Together they

459 represent the greatest obstacle to the export of fresh fruits and vegetables from Hawaii,

460 followed by a variety of other quarantine insect pests. Papayas, dragon fruits, longans,

461 bananas, rambutans, and mangoes are exported to the United States mainland with

462 irradiation at 150 Gy for fruit flies or 400 Gy if surface pests are present (Follett and

463 Armstrong 2004, Follett and Weinert 2012). Irradiation is approved for an additional 15

464 fruit and vegetable crops that are not exported such as carambola, breadfruit, and

465 tomato.

466 Papayas are exported from Hawaii to the United States mainland and Japan

467 using VHT (Table 1); papayas exported from Hawaii were about 3,855 tons in 2012,

468 and 16% were to Japan. Mangoes (‘Haden’ or ‘Keitt’) can be exported to Japan using

469 the same VHT, but thus far shipments have been limited to a total of 864 kg from

470 2004-2013.

471 Other approved heat treatments such as hot water immersion for lychee and

472 longan (Armstrong and Follett 2007) and vapor heat for rambutan (Table 1) are not

473 currently used. Heat treatments may cause undesirable darkening of the pericarp in

474 lychee and rambutan (Follett and Sanxter 2000, 2003). Fresh pineapple cultivars of 50%

475 or more ‘smooth cayenne’ parentage are exported to the United States mainland as a

476 non-host for fruit flies (Armstrong 1994), and irradiation and heat treatments are

477 available for other pineapple cultivars.

478 A phytosanitary system is approved for export of ‘Sharwil’ avocados to the

479 United States mainland based on poor host status, low pest prevalence, sanitation,

480 trapping, bait sprays, and limited distribution (northern tier states during winter months

481 only) to minimize the risk of B. dorsalis infestation (Follett 2009, Follett and Vargas

482 2010). Current citrus cold treatment research is focused on B. cucurbitae which is more

483 cold tolerant than B. dorsalis and similar in cold tolerance to C. capitata (Follett and

484 Snook 2013).

485 Future Research and Application

486 This section suggests future research that may be needed and the possibility of

487 developing more broadly applicable treatments. A newly formed international group

488 (Phytosanitary Measures Research Group) examines phytosanitary treatment issues with

489 an objective of making treatments more broadly applicable (IPPC 2016). Heather and

490 Hallman (2008) discuss a variety of treatment possibilities, their advantages and

491 disadvantages, research done, and commercial potential. The most promising ones are

492 briefly discussed below.

493 Heat treatments. The VHT schedules of eight areas producing mango (Table

494 1) are shown by target temperature in Table 4. The treatment temperatures at the seed

495 surface range from 46°C to 48°C, and theoretically, higher temperatures require shorter

496 holding times; however, such a trend is not always substantiated. For example, mangoes

497 from Taiwan require 30 minutes holding regardless if the temperature is 46.5 or 47.5°C.

498 Research is needed to determine if factors such as host species, cultivar, or fly

499 population significantly affect efficacy. Similarly, research is needed to determine if

500 different laboratory fruit infestation techniques affect the efficacy of the treatment. In

501 addition, the consideration of plant quarantine security by researchers in exporting

502 countries and evaluation of disinfestation data by importing countries might have

503 influenced determination of the schedules. In order to make the most suitable heat

504 treatment for each fruit commodity, research collaboration between many countries

505 might be needed. Furthermore, research is needed to clarify the role of factors affecting

506 the efficacy of phytosanitary treatment between experiments in developing the treatment

507 and commercial applications.

508 Hot water immersion has been a viable treatment for mangoes infested with C.

509 capitata and Anastrepha spp. (Heather and Hallman 2008) and should also continue to

510 be amenable against B. dorsalis. However, in vitro studies by Armstrong et al. (2009)

511 indicate that heat treatments against B. dorsalis may need to be more severe than those

512 against C. capitata, which may challenge mango quality. A hot water treatment that is

513 broadly effective against fruit flies should be based on temperature inside the mango

514 instead of time of immersion, given that time of treatment is currently based on shape

515 and size of the fruit (Heather and Hallman 2008). More research for developing hot

516 water treatment schedules in many countries is needed to develop effective hot water

517 treatments against B. dorsalis.

518 Cold Treatment. More research is needed to develop cold treatments against

519 B. dorsalis for fruits that tolerate the low temperatures required, which tend to not

520 include many tropical fruits. On the other hand, combination treatment (VHT + cold

521 treatment) designed to preserve fruit quality are used for lychee. This provides the

522 possibility of developing phytosanitary treatments for heat susceptible fruit such as

523 longan and rambutan. The major disadvantage to cold treatments, long treatment

524 durations, might be alleviated by combining with other treatments.

525 Irradiation. The potentially most widely applicable treatment is ionizing

526 radiation at 150 Gy, the generic dose approved for all Tephritidae (USDA-APHIS 2016;

527 IPPC 2009). This dose is tolerated by more fresh fruits than any other treatment applied

528 on a commercial scale (Heather and Hallman 2008). However, some markets do not yet

529 accept phytosanitary irradiation (Follett 2014, Hallman and Loaharanu 2016). Zhao et al.

530 (2016) conducted research with > 100,000 3rd instars reared in guava that supports

531 lowering the dose for B. dorsalis to 116 Gy. Previously Follett and Armstrong (2004)

532 demonstrated the efficacy of 124 Gy in large-scale testing of 55,743 late third instars of

533 B. dorsalis reared on diet or fruit and inserted into papayas with no emergence of adults.

534 Facilities for irradiation may be lacking. The United States allows

535 phytosanitary irradiation at several ports of entry, allowing for treatment application

536 when facilities are not available in the exporting country (Bustos-Griffin et al. 2015).

537 The use of irradiation in combination with other technologies could be beneficial

538 (Lacroix and Follett 2015). Particularly, irradiation in combination with cold may

539 reduce the duration and cost of cold treatment protocols and allow use of higher

540 temperatures that do not cause chilling injury in sensitive fruits. Additional research is

541 needed to demonstrate the efficacy of irradiation plus cold combination treatments

542 while assessing commodity quality.

543 Fumigants. Research with sulphuryl fluoride, carbonyl sulphide, and gaseous

544 formulations of phosphine against tephritids infesting fruit are considered promising

545 (Heather and Hallman 2008). As methyl bromide fumigation is still allowed for

546 postharvest phytosanitary uses but only some markets still accept fruits so treated,

547 development of new applications for it might be warranted. Liu et al. (2012) concluded

548 that phosphine fumigation at a concentration of 1.5 g/L at 5°C for 5 d could serve as a

549 phytosanitary treatment against B. dorsalis in navel oranges with negligible harm to the

550 fruit. A total of 2,467 3rd instars (most tolerant stage) were tested in fruit under these

551 conditions with no survivors resulting.

552 Modified Atmospheres. Atmospheres with low concentrations of oxygen

553 and/or high concentrations of carbon dioxide have been extensively studied although

554 applied commercially as a phytosanitary treatment in only one instance against surface

555 pests (Carpenter and Potter 1994). Heather and Hallman (2008) discuss various

556 applications of modified atmospheres with other factors, highlighting that combination

557 with heat is synergistic. However, little research has been done with tephritids, and the

558 potential reduction in treatment severity may not be as favourable as with other insects

559 (Hallman 2010), possibly because tephritids are already in a reduced oxygen

560 environment inside fruit.

561

562 Acknowledgements

563 We are grateful to Saluckjit Phankum, Sunyanee Srikachar (Department of

564 Agriculture, Thailand), Watchreeporn Orankanok (Department of Agricultural

565 Extension, Thailand), Mingoo Park, Deuk-Soo Choi (Animal and Plant Quarantine

566 Agency, Republic of Korea), Isao Miyazaki (Ministry of Agriculture, Forestry and

567 Fisheries, Japan), and Joanne Wilson (New Zealand Ministry for Primary Industries) for

568 reviewing related information of treatment schedules and suggestions. The IPPC is

569 thanked for organizing a meeting on phytosanitary treatments of B. dorsalis from which

570 this paper was one result. A.R.C is the recipient of grant PBCRC4127 from the Plant

571 Biosecurity Cooperative Research Centre which has helped fund his involvement in this

572 activity. A.R.C would like to acknowledge the support of the Australian Government’s

573 Cooperative Research Centres programme.

574

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963 Table 1. Existing phytosanitary heat treatment schedules against Bactrocera dorsalis.

Origin Importing Commodity Treatment schedule Target pests Reference or source1 (Export) country (Fruit core temperature) Vapor heat Not specified United States Bell pepper, To 44.4°C for 8.75 h B. dorsalis, B. cucurbitae, USDA 2016, T106-b eggplant, Ceratitis capitata mountain papaya, papaya, pineapple, squash, tomato, zucchini Papaya To 47.2°C in 4 h B. dorsalis, B. cucurbitae, USDA 2016, T106-c C. capitata Belize, Chile, United States Papaya To 47.2°C in 4 h, hold 5 B. dorsalis, B. cucurbitae, USDA 2016, T103-d-1, Hawaii min C. capitata 2 Hawaii Japan Mango, papaya To 47.2°C B. dorsalis complex2, MAFF Japan 2015 B. cucurbitae, C. capitata New Zealand Papaya To 47.2°C B. dorsalis, B. cucurbitae, MPI NZ 2014 C. capitata in ≥ 4 h United States Citrus To 47.2°C in 4 h, hold 5 B. dorsalis, B. cucurbitae, USDA 2016, T103-b-1 min C. capitata Longan, lychee, To 47.2°C in 1 h, hold B. dorsalis, C. capitata USDA 2016, T106-f, g rambutan for 20 min

Origin Importing Commodity Treatment schedule Target pests Reference or source1 (Export) country (Fruit core temperature) Hawaii United States Rambutan To 47.2°C in 1 h, hold 20 B. dorsalis, B. cucurbitae, USDA 2016, T103-e min C. capitata India Australia Mango To 46.5°C and hold for B. dorsalis, B. cucurbitae DAFF Australia 2014 30 min or to 47.5°C and hold for 20 min (Minimum treatment time 2 h) Japan Mango To 47.5°C and hold for B. dorsalis complex2, MAFF Japan 2015 20 min B. cucurbitae New Zealand Mango To 48°C and hold for 20 B. caryeae, B. correcta, MPI NZ 2014 min B. dorsalis, B. zonata, B. cucurbitae, B. tau, Malaysia Japan Mango To 46.5°C and hold for B. dorsalis complex2, MAFF Japan 2015 20 min; Air cooling only B. cucurbitae

Pakistan Japan Mango To 47.0°C and hold for B. dorsalis complex2, MAFF Japan 2015 25 min; Air cooling only B. cucurbitae

Philippines United States Mango To 46.0°C in 4 h, hold B. occipitalis, B. dorsalis, USDA 2016, T106-d-1 (Guimaras only) for 10 min B. cucurbitae

Origin Importing Commodity Treatment schedule Target pests Reference or source1 (Export) country (Fruit core temperature) Philippines Australia Mango To 46.0°C and hold for B. dorsalis, B. cucurbitae DAFF Australia 2014 (Guimaras, 10 min Samal, and Davao del Sur) Philippines Japan Mango To 46.0°C and hold for B. dorsalis complex2, MAFF Japan 2015 10 min B. cucurbitae Papaya To 46.0°C and hold for 70 min New Zealand Mango To 46°C and hold for10 B. dorsalis, B. cucurbitae MPI NZ 2014 min Papaya To 46°C and hold for 70 min South Korea Mango To 46.0°C and hold for B. dorsalis complex2 QIA Korea 2015 10 min Papaya To 46.0°C and hold for 70 min Taiwan Australia Mango To 46.5°C and hold for B. dorsalis, B. cucurbitae DAFF Australia 2014 30 min Japan Dragon fruit To 46.5°C and hold for B. dorsalis complex2, MAFF Japan 2015 (Hylocereus 30 min; air cooling only B. cucurbitae undatus)

Origin Importing Commodity Treatment schedule Target pests Reference or source1 (Export) country (Fruit core temperature) Taiwan Japan Mango To 46.5°C and hold for B. dorsalis complex2, MAFF Japan 2015 30 min B. cucurbitae Papaya To 47.2°C New Zealand Lychee To 47°C and hold for 20 B. dorsalis, B. cucurbitae MPI NZ 2014 min Mango To 46.5°C and hold for 30 min South Korea Mango To 46.5°C and hold for B. dorsalis QIA Korea 2015 30 min Papaya To 47.2°C and hold for B. dorsalis, etc 5 min United States Mango To 47.5°C and hold for B. dorsalis, B. cucurbitae USDA 2016, T106-d 30 min, cooling required Thailand Australia Longan To 46°C and hold for 20 B. dorsalis DAFF Australia 2014 min or to 47°C and hold for 15 min Japan Mango To 47.0°C and hold for B. dorsalis complex2, MAFF Japan 2015 20 min B. cucurbitae

Origin Importing Commodity Treatment schedule Target pests Reference or source1 (Export) country (Fruit core temperature) Thailand Japan Mangosteen To 46.0°C and hold for B. dorsalis complex2 MAFF Japan 2015 58 min; air cooling only

Pomelo To 46.0°C and hold for 30 min; air cooling only

New Zealand Longan, lychee To 47°C and hold for 20 B. dorsalis, B. correcta, MPI NZ 2014 min B. cucurbitae Mango B. dorsalis, B. cucurbitae South Korea Mango To 47.0°C and hold for B. dorsalis QIA Korea 2015 20 min Viet Nam Chile Dragon fruit To 46.5°C and hold for B. dorsalis, B. cucurbitae IPPC ECBD Meeting 40 min Dec. 2014 Japan Dragon fruit To 46.5°C and hold for B. dorsalis complex2, MAFF Japan 2015 (Hylocereus 40 min B. cucurbitae undatus) Mango To 47.0°C and hold for B. dorsalis complex2, 20 min B. correcta, B. cucurbitae New Zealand Dragon fruit To 46.5°C and hold for B. dorsalis, B. cucurbitae MPI NZ 2014 40 min

Origin Importing Commodity Treatment schedule Target pests Reference or source1 (Export) country (Fruit core temperature) Viet Nam New Zealand Mango To 46.5°C and hold for B. carambolae, MPI NZ 2014 30 min or 47°C and hold B. dorsalis, B. correcta, for 20 min B. cucurbitae, B. tau, B. tuberculata, B. zonata South Korea Dragon fruit To 46.5°C and hold for B. dorsalis, B. cucurbitae IPPC ECBD Meeting 40 min Dec. 2014 Mango To 47.0°C and hold for B. dorsalis etc. QIA Korea 2015 20 min Vapor heat plus cold China Japan Lychee To 46.5°C, hold for 10 B. dorsalis complex2 MAFF Japan 2015 min, followed by 2°C for 40 h Taiwan Japan Lychee To 46.2°C, hold for 20 B. dorsalis complex2 MAFF Japan 2015 min, followed by 2°C for 42 h South Korea Lychee To 46.2°C, hold for 20 B. dorsalis QIA Korea 2015 min, followed by 2°C for 42 h Hot water immersion Hawaii United States Longan, lychee ≥ 49°C water for 20 min B. dorsalis, C. capitata USDA 2016, T102-d-1, 2

Origin Importing Commodity Treatment schedule Target pests Reference or source1 (Export) country (Fruit core temperature) Pakistan Australia Mango 48°C water: B. dorsalis, B. correcta, DAFF Australia 2014 to 500 g, 60 min, B. zonata 501-700 g, 75 min, 701-900 g, 90 min

964 1DAFF: Australia: http://www.agriculture.gov.au/, http://apps.daff.gov.au/; IPPC: International Plant Protection Convention; IPPC

965 ECBD: IPPC, Expert Consultation on Phytosanitary Treatments in Bactrocera dorsalis complex in Okinawa, Japan, Dec.1-5, 2014;

966 IPPC ECCT: IPPC, Expert Consultation on Cold Treatments in Buenos Aires, Argentina, Dec.2-6, 2013; USDA:

967 http://www.aphis.usda.gov/; MAFF: Japan: http://www.maff.go.jp/pps/; MPI: NZ: http://www.mpi.govt.nz/,

968 http://www.biosecurity.govt.nz/; QIA: Korea: http://www.qia.go.kr/

969 2 Mainly 6 species of economic importance（B. carambolae, B. caryeae, B. dorsalis, B. kandiensis, B. occipitalis, B. pyrifoliae）among

970 B. dorsalis complex based on Drew & Hancock (1994).

971 Table 2. Existing phytosanitary cold treatment schedules against Bactrocera dorsalis.

Origin Importing Commodity Treatment schedule Target pests Reference or source1 (Export) country (Fruit core temperature) Not specified United States Apricot, citrus ≤ -0.55°C for 22 d B. dorsalis, USDA 2016, T107-e (only to 3 ports), Ceratitis capitata, grape, nectarine, C. quinaria, C. rosa, peach, plum Thaumatotibia leucotreta Citrus (only for ≤ -0.55°C for 24 d B. dorsalis, C. rosa, USDA 2016, T107-k port of Houston) T. leucotreta (interim measure) Carambola, ≤ 0.99°C for 15 d B. dorsalis USDA 2016, T107-j lychee, longan, ≤ 1.38°C for 18 d sand pear Taiwan Japan Grape, pomelo ≤ 1.0°C for 12 d B. dorsalis complex2 MAFF Japan 2015

Ponkan ≤ 1.0°C for 14 d New Zealand Lychee ≤ 1°C for 13 d B. dorsalis, B. cucurbitae MPI NZ 2014

South Korea Ponkan ≤ 1.0°C for 14 d B. dorsalis, B. cucurbitae, IPPC ECCT Meeting B. tsuneonsis, B. caudatus, Dec. 2013 B. latifrons, B. tau Thailand Australia Longan, lychee 0.99°C for 17 d B. dorsalis, B. cucurbitae, IPPC ECBD Meeting 1.38°C for 20 d Conopomorpha sinensis Dec. 2014

Origin Importing Commodity Treatment schedule Target pests Reference or source1 (Export) country (Fruit core temperature) Thailand New Zealand Longan 0.99°C for 13 d B. dorsalis, B. correcta MPI NZ 2014 1.38°C for 18 d Lychee 0°C for 10 d B. dorsalis, B. cucurbitae 0.56°C for 11 d 1.11°C for 12 d 1.67°C for 14 d

972 1,2Same as notes of Table 1

973 Table 3. Existing phytosanitary treatment schedules against Bactrocera dorsalis other than heat and cold treatment.

Origin Importing Commodity Treatment schedule Target pests Reference or (Export) country source1 Ionizing radiation Not specified Not specified Fruits, vegetables 150 Gy All Tephritidae IPPC 2009 Not specified United States Fruits, vegetables 150 Gy All Tephritidae USDA 2016, T105 Hawaii New Zealand Papaya 150 Gy B. dorsalis, B. cucurbitae, MPI NZ 2014 Ceratitis capitata Methyl bromide fumigation Hawaii, Israel, United States Avocado ≥ 21.1°C, 32 g/m3 for 4 h B. dorsalis, B. cucurbitae, USDA 2016, Philippines C. capitata T101-c-1 Methyl bromide fumigation plus cold treatment Not specified United States Apple, apricot, ≥ 21.1°C, 32 g/m3 for 2 h B. dorsalis, B. cucurbitae, USDA 2016, avocado, cherry, followed by 0.6-2.8°C for 4 d or B. tryoni, C. capitata, T108-a-1, 2, 3 grape, kiwi, 3.3-8.3°C for 11 d Brevipalpus chilensis nectarine, peach, or pear, plum, ≥ 21.1°C, 32 g/m3 for 2.5 h quince followed by 1.1-4.4°C for 4 d or 5.0-8.3°C for 6 d or 8.9-13.3°C for 10 d

Origin Importing Commodity Treatment schedule Target pests Reference or (Export) country source1 or ≥ 21.1°C, 32 g/m3 for 3 h followed by 6.1-8.3°C for 3 d or 8.9-13.3°C for 6 d

974 1 Same as notes of Table 1

975 Table 4. Existing VHT schedules against Bactrocera dorsalis for mango.

Target temperature at Holding time Area of origin 976 seed surface

46 °C 10 min Philippines

46.5 °C 20 min Malaysia

30 min India, Taiwan, Viet Nam

47 °C 20 min Thailand, Viet Nam

25 min Pakistan

47.2 °C 0 min Hawaii

47.5 °C 20 min India

30 min Taiwan

48 °C 20 min India