1 For Submission to: 2 3 4 5 Jesusa C. Legaspi 6 USDA‐ARS‐CMAVE 7 FAMU‐Center for Biological Control 8 Tallahassee, FL 32308 9 Phone: (850) 656 9870 ext. 10 10 FAX: (850) 656‐9808 11 Email: [email protected] 12 13 14 15 16 17 Biology, Ecology and Control of the Ficus Whitefly, 18 Singhiella simplex (Hemiptera: Aleyrodidae) 19 20 Jesusa Crisostomo Legaspi1, Catharine Mannion2, Divina Amalin2 and Benjamin C. Legaspi, Jr.3 21 22 1U. S. Department of Agriculture, Agricultural Research Service, CMAVE / FAMU ‐ Center for 23 Biological Control, 6383 Mahan Dr., Tallahassee, FL 32308; 2Tropical Research and Education 24 Center, University of Florida, 18905 SW 280th Street, Homestead, FL 33031, 3 Employed by State 25 of Florida, contact through senior autho Legaspi et al.: The Ficus Whitefly Page 2 of 24

26 Table of Contents 27 28 Economic importance ...... 3 29 Geographic distribution ...... 3 30 Descriptive biology...... 4 31 Reproductive biology and life table analysis ...... 4 32 Controlling the Ficus whitefly ...... 5 33 References Cited...... 9 34 Figure Captions ...... 13 35 Legaspi et al.: The Ficus Whitefly Page 3 of 24

36 Economic importance 37 38 Whiteflies are small Homopteran that cause crop damage by extracting phloem 39 sap, excreting honeydew that serves as a medium for fungi, or acting as vectors of economically 40 important viral pathogens (Byrne and Bellows 1991). Crop loss can exceed 50% yield reduction 41 as their importance as economic pests appears to increase continually. The ficus whitefly, 42 Singhiella simplex (Singh) (Hemiptera: Aleyrodidae), is an economic pest of Ficus plant species 43 in India, Burma and China (Hodges 2007). The whitefly has been most commonly found 44 infesting weeping fig (Ficus benjamina L.) (Moraceae) (Fig. 1). However, it has also been 45 reported on F. altissima Blume (lofty fig, false banyan tree), F. bengalensis L. (“banyan tree”), F. 46 microcarpa L.f. (Cuban laurel), F. aurea Nutt. (strangler fig), F. lyrata Warb. (fiddle‐leaf fig), F. 47 racemosa L. (Cluster Fig, Indian Fig) and F. maclellandii King (banana‐leaf fig) (Mannion et al. 48 2008). When disturbed, small clouds of the tiny gnat‐like insects emerge from whitefly‐infested 49 foliage. Severe infestations result in leaf dropping or shedding and defoliation. Like other 50 whiteflies, the Ficus whitefly can cause serious injury to host plants by sucking sap, resulting in 51 wilting, yellowing, stunting, defoliation, or plant death (Osborne 2008). 52

53 Geographic distribution 54 55 Although S. simplex has historically been known as a pest of Ficus in India, Burma and 56 China, its arrival in the Continental United States is relatively recent. Possibly the earliest record 57 is that of the Florida Department of Agriculture and Consumer Services, Division of Plant 58 Industry (FDACS‐DPI) in South Florida on August 3, 2007 on F. benjamina (Hodges 2008). A 59 similar report was made by the Miami‐Dade County Extension, University of Florida – Institute 60 of Food and Agricultural Sciences. Since the initial report in south Florida in 2007, FDACS‐DPI 61 surveys have found the Ficus whitefly in the coastal counties towards central Florida (Fig. 2). 62 Recently, the whitefly was intercepted at entry points on Ficus plants imported into Korea from 63 China (Suh et al. 2008). The first US record of S. simplex was made on F. benjamina in Miami, 64 Florida on 3 August 2007 (Hodges 2007). Since then, geographic expansion has increased to Legaspi et al.: The Ficus Whitefly Page 4 of 24

65 include most of southern Florida, as well as along both coasts of Florida up to central Florida 66 (Hodges 2007). 67

68 Descriptive biology 69 70 Very little is known about the biology and life history of the Ficus whitefly. Eggs are 71 usually laid on leaf undersides (Fig. 3) and hatch into crawlers. The crawlers are mobile and 72 begin to feed. Early nymphal stages can be very difficult to detect. The nymphs become 73 immobile feeders, usually oval and flat in shape (Mannion et al. 2008). During the pupal stage, 74 the nymphs turn tan to light green with red eyes and measure about 1.3 mm in length. The 75 adult whitefly is yellow, and the wings are white with a faint grey band towards the middle 76 (Hodges 2007, Mannion et al. 2008). 77

78 Reproductive biology and life table analysis 79 80 Like other whiteflies in its genus, S. simplex is assumed to have at least three 81 generations per year in Florida (Hodges 2007) with a lifecycle completed within about one 82 month (Mannion et al. 2008). Detailed reproductive biology and life table studies at five 83 different constant temperatures were performed by Legaspi et al. (2011). In the laboratory, 84 development rates (reciprocal of duration times) were studied at 15, 20, 25, 27, 30 and 35 °C on 85 leaf cuttings of F. benjamina. No insects survived the 35°C treatment. Total duration of 86 immature stages varied from 97.11 d at 15°C to 25.23 d at 30°C (Table 1). Within each 87 immature lifestage, development rates increased linearly with temperature and were described 88 using linear equations. For the combined immature stages (eggs to pupae), the effect of 89 temperature on development was described adequately using both linear regressions and a

90 nonlinear model Briere model: r(T )  aT (T  T0 ) TL  T where a is an empirical constant, r is

91 development rate, T is temperature, T0 is the lower developmental threshold, and TL is lethal 92 temperature (Briere et al. 1999) (Fig. 4). The linear model estimated lower developmental

93 threshold temperature (T0) to be 10.6°C. By comparison, the Briere model estimated T0 of 7.3°C Legaspi et al.: The Ficus Whitefly Page 5 of 24

94 and upper lethal temperature of 45.9°C The thermal requirement for development from eggs to 95 pupae was calculated to be 487.8 degree‐days. Life table parameters for the whitefly at each

96 temperature are shown in Table 2. Ficus whitefly reproduction was highest at 27°C: R0, GRR, T, 97 r,  and DT were 23.114 &/&, 24.25&/&, 31.413 d, 0.0999&/ &/d, 1.105&/ &/d and 6.93 d, 98 respectively. The calculations assumed a 1:1 sex ratio which may have underestimated actual 99 reproductive potential because the sex ratio of immatures that successfully emerged was

100 female‐biased (79.4%; 15♂: 58&). 101 The combined effects of temperature and adult female age were analyzed using the 102 nonlinear regression model of Enkegaard (1993): eggmean = (p+qT) d exp(– wTd); where T is 103 temperature. The Enkegaard model did not provide a very good fit to the observed data (Fig. 5), 104 possibly because of high variability in fecundity and paucity of data points. Female adult 105 survivorship was plotted on a linear scale (Fig. 6). Duration of adulthood was significantly longer 106 at 15°C compared to all other temperatures tested, averaging 8.0 d, compared to 4.2, 2.8 and 107 2.5 at 25, 27, and 30 °C , respectively. 108 Temperature was not found to significantly affect lifetime fecundity. At 15, 25, 27 and 109 30 °C, lifetime fecundity per female averaged 27.0, 37.9, 46.2, and 27.7 eggs, respectively. The 110 temperature effect was not significant, probably due to high variability. Also, lower daily 111 fecundity at lower temperatures may have been compensated by longer ovipositional periods.

112 Controlling the Ficus whitefly 113 114 Chemical control. Mannion et al. (2008) recommend drenching soil around the bases of 115 trees or hedges with neonicotinid compounds such as imidacloprid or clothianidin. These 116 insecticides are widely known to attack the central nervous system while displaying 117 reduced toxicity to mammals. When applied properly, neonicotinids should provide adequate 118 whitefly control for 4 – 8 months, although monitoring after 3 months is suggested with 119 possible spot treatments where needed. Although soil application is the preferred control, 120 foliar treatments may be necessary during extreme infestations. In such cases, recommended 121 foliar insecticides include flonicamid (novel insecticide), abamectin (also an acaricide/ 122 nematicide), azadirachtin (insect growth regulator), Beauveria bassiana (entomopathogenic Legaspi et al.: The Ficus Whitefly Page 6 of 24

123 fungus), pyriproxyfen (juvenile hormone analogue), pymetrozine (novel antifeedant), 124 endosulfan (organochlorine), spiromesifen (lipid biosynthesis inhibitor), buprofezin (chitin 125 synthesis inhibitor), bifenthrin (pyrethroid) and acetamiprid (neonicotinoid). To prevent the 126 development of resistance, insecticides should be rotated based on differing modes of action. 127 Biological control. Biological control agents used against whiteflies typically include 128 parasitic Hymenoptera e.g. Encarsia formosa Gahan (Aphelinidae) (Hoddle et al. 1998) or 129 Eretmocerus spp. (van Lenteren and Martin 2006), predatory Coccinellid (Obrycki and 130 Kring 1998; Arnó et al. 2010), entomopathogenic fungi e.g., Beauveria bassiana (Balsamo) 131 Vuillemin and Paecilomyces fumosoroseus (Wize) Brown & Smith (Poprawski and Jones 2001), 132 or combinations of these agents (Labbé et al. 2009; Bardin et al. 2008). 133 Whitefly‐infested Ficus plants in Miami that were sampled for natural enemies (G. 134 Hodges, C. Mannion, unpublished data) yielded several species of parasitic wasps and predatory 135 beetles (Coleoptera: ). The wasps were identified to be Encarsia protransvena 136 Viggiani (Hymenoptera: Aphelinidae) and Amitus benetti Viggiani & Evans (Hymenoptera: 137 Platygasteridae) (Fig. 7). Encarsia protransvena is distributed worldwide and attacks whitefly 138 hosts such as the greenhouse whitefly, Trialeurodes vaporariorum (Westwood) (Homoptera: 139 Aleyrodidae) (Giorgini 2001). Amitus benetti is a parasitoid of the silverleaf whitefly, Bemisia 140 argentifolii Bellows & Perring (Homoptera: Aleyrodidae) (Ryckewaert and Alauzet 2002). The 141 beetles were the multi‐colored Asian lady , Harmonia axyridis Pallas; the ashy gray lady 142 beetle, Olla v‐nigrum (Mulsant); Exochomus childreni Mulsant, Chilocorus nigritus (F.), and the 143 dark blue lady beetle, Curinus coeruleus (Mulsant). Harmonia axyridis has been used as a 144 biological control agent against aphids and other species of Hemipteran pests (Yoon et al. 2010; 145 Koch 2003). Olla v‐nigrum is indigenous in arboreal habitats throughout much of the United 146 States, and is known to be a natural enemy of aphids and psyllids (Michaud 2001). Exochomus 147 childreni has been evaluated as a predator of mites in citrus (Villanueva et al. 2004). Chilocorus 148 nigritus has been used successfully as a biological control agent of scale pests throughout the 149 tropical and tropical environments (Ponsonby 2009). Curinus coeruleus is a predator of citrus 150 psyllids (Soemargono et al. 2008). Legaspi et al.: The Ficus Whitefly Page 7 of 24

151 The generalist predator Delphastus catalinae (Horn) (Coleoptera: Coccinellidae) was 152 evaluated as a potential biological control agent of Ficus whitefly (JCL unpublished data). 153 Delphastus is widely known as a whitefly predator (e.g., Heinz et al. 1999; Legaspi et al. 2006). 154 Female predators were starved for a 24‐h period, then allowed to feed for a 24‐h period on 155 Ficus whiteflies of different stages: eggs, small and large larvae. Initial prey numbered 200 eggs, 156 100 small larvae and 50 large larvae. Within the 24‐h feeding period, Delphastus adults 157 consumed about 150 eggs or 40 small larvae (Fig. 8). Predation on large larvae was minimal. 158 Therefore, Delphastus may be a useful control agent when the whiteflies are in the egg or small 159 larval stages, but unlikely to be successful against large larvae. 160 161 162 163 164 Legaspi et al.: The Ficus Whitefly Page 8 of 24

165 Acknowledgments 166 167 Technical assistance was provided by Neil Miller (USDA, ARS, CMAVE), Keith Marshall, Jr. 168 and William Zeigler (Florida A&M Univ.). Luis Bradshaw and Phellicia Perez (University of 169 Florida) assisted in the field collection of the ficus whitefly. We thank Ru Nguyen, Greg Hodges 170 (Division of Plant Industry, Gainesville, FL) and Jesse A. Logan (US Forest Service, retired) for 171 helpful discussions. 172 This article presents the results of research only. The use of trade, firm, or corporation 173 names in this publication is for the information and convenience of the reader. Such use does 174 not constitute an official endorsement or approval by the United States Department of 175 Agriculture or the Agricultural Research Service of any product or service to the exclusion of 176 others that may be suitable. 177 178 Legaspi et al.: The Ficus Whitefly Page 9 of 24

179 References Cited 180 181 Arnó, J. R., Gabarra, R., Liu, T.‐X., Simmons, A. M., and Gerling, D. (2010) Natural enemies of 182 Bemisia tabaci: predators and parasitoids. In Bemisia: bionomics and management of a 183 global pest. Stansly, P. A., and Naranjo, S. E. (eds.). Springer, Amsterdam, The 184 Netherlands. pp. 385–421. 185 Bardin, M., Fargues, J., and Nicot, P. C. (2008) Compatibility between biopesticides used to 186 control grey mould, powdery mildew and whitefly on tomato. Biological Control 46, 187 476–483 188 Bonato, O., Lurette, A., Vidal, C., Fargues, J. (2007). Modelling temperature‐dependent 189 bionomics of Bemisia tabaci (Q‐biotype). Physiological Entomology 32, 50–55. 190 Byrne, D. N., and Bellows, T. S. (1991) Whitefly biology. Annual Review of Entomology 36, 431– 191 457. 192 Briere, J.‐F., Pracros, P., Le Roux, A.‐Y., and Pierre, J.‐S. (1999) A novel rate model of 193 temperature‐dependent development for . Environmental Entomology 28, 194 22–29. 195 Enkegaard, A. (1993) The poinsettia strain of the cotton whitefly, Bemisia tabaci (Homoptera: 196 Aleyrodidae), biological and demographic parameters on poinsettia (Euphorbia 197 pulcherrima) in relation to temperature. Bulletin of Entomological Research 83, 535– 198 546. 199 Giorgini, M. (2001) Induction of males in thelytokous populations of Encarsia meritoria and 200 Encarsia protransvena: A systematic tool. BioControl 46, 427 – 438. 201 Greenberg, S. M., Legaspi, B. C. Jr., Jones, W. A., and Enkegaard, A. (2000) Temperature‐ 202 dependent life history of Eretmocerus eremicus (Hymenoptera: Aphelinidae) on two 203 whitefly hosts (Homoptera: Aleyrodidae). Environmental Entomology 29, 851–860. 204 Heinz, K. M., Brazzle, J. R., Parella, M. P., and Pickett, C. H. (1999) Field evaluations of 205 augmentative releases of Delphastus catalinae (Horn) (Coleoptera: Coccinellidae) for 206 suppression of Bemisia argentifolii Bellows & Perring (Homoptera: Aleyrodidae) 207 infesting cotton. Biological Control 16, 241–251. Legaspi et al.: The Ficus Whitefly Page 10 of 24

208 Hoddle, M. S., Van Driesche, R. G., and Sanderson, J. P. (1998) Biology and use of the whitefly 209 parasitoid Encarsia Formosa. Annual Review of Entomology 43, 645–669. 210 Hodges, G. (2007) The fig whitefly Singhiella simplex (Singh) (Hemiptera: Aleyrodidae): A new 211 exotic whitefly found on ficus species in south Florida. Div. of Plant Industry, Florida 212 Department of Agriculture and Consumer services 213 (http://doacs.state.fl.us/pi/enpp/ento/Singhiella%20simplex.html) 214 Koch, R. L. (2003). The multicolored Asian lady beetle, Harmonia axyridis: A review of its 215 biology, uses in biological control, and non‐target impacts. Journal of Insect Science 3, 1– 216 16. 217 Labbé, R. M., Gillespie, D. R., Cloutier, C. and Brodeur, J. (2009) Compatibility of an 218 entomopathogenic fungus with a predator and a parasitoid in the biological control of 219 greenhouse whitefly. Biocontrol Science and Technology 19, 429–446. 220 Legaspi, J. C., Mannion, C., Amalin, D., and Legaspi, B. C. Jr. (2011) Life table analysis and 221 development of the Ficus whitefly, Singhiella simplex (Hemiptera: Aleyrodidae) under 222 different constant temperatures. Annals of the Entomological Society of America. In 223 press. 224 Legaspi, J. C., Simmons, A. M., and Legaspi, B. C. Jr. (2006) Prey preference by Delphastus 225 catalinae (Coleoptera: Coccinellidae) on Bemisia argentifolii (Homoptera: Aleyrodidae): 226 effects of plant species and prey stages. The Florida Entomologist 89, 218–222. 227 Mannion, C., Osborne, L., Hunsberger, A., Mayer, H., and Hodges, G. (2008) Ficus whitefly: A 228 new pest in south Florida. The Institute of Food and Agricultural Sciences, University of 229 Florida. 230 Michaud, J. P. (2001) Numerical response of Olla v‐nigrum (Coleoptera: Coccinellidae) to 231 infestations of Asian citrus psyllid, (Hemiptera: Psyllidae) in Florida. The Florida 232 Entomologist 4, 608–612. 233 Obrycki, J. J., and Kring, T. J. (1998) Predaceous Coccinellidae in biological control. Annual 234 Review of Entomology 43, 295–321. Legaspi et al.: The Ficus Whitefly Page 11 of 24

235 Osborne, L. (2008) The "Ficus Whitefly": A new pest in south Florida. Invasive 236 Working Group. University of Florida. 237 (http://www.mrec.ifas.ufl.edu/lso/IAWG/FIG/default.asp) 238 Poprawski, T. J., and Jones, W. A. (2001) Host plant effects on activity of the mitosporic fungi 239 Beauveria bassiana and Paecilomyces fumosoroseus against two populations of Bemisia 240 whiteflies (Homoptera: Aleyrodidae). Mycopathologia 151, 11–20. 241 Ponsonby, D. J. 2009. Factors affecting utility of Chilocorus nigritus (F.) (Coleoptera: 242 Coccinellidae) as a biocontrol agent. CAB Reviews: Perspectives in Agriculture, 243 Veterinary Science, Nutrition and Natural Resources. 4. 20 pp. 244 Ryckewaert, P. and Alauzet, C. (2002) The natural enemies of Bemisia argentifolii in Martinique 245 BioControl 47, 115–126. 246 Soemargono, A., Ibrahim, Y. B., Ibrahim, R., and Osman, M. S. (2008) Life table and 247 demographic parameters of the metallic blue ladybeetle, Curinus coeruleus Mulsant, fed 248 with the asian citrus psyllid, Diaphorina citri Kuwayama. Pertanika Journal of Tropical 249 Agricultural Science. 31, 1–10. 250 Suh, S.‐J., Evans, G. A., and Oh, S.‐M. (2008) A checklist of intercepted whiteflies (Hemiptera: 251 Aleyrodidae) at the Republic of Korea ports of entry Journal of Asia‐Pacific Entomology 252 11, 37–43. 253 Van Lenteren, J. C., and Martin, N. A. (2006) Biological control of whiteflies. In Albajes, R., 254 Gullino, M. L., and van Lenteren, J. C. (eds.) Integrated pest and disease management in 255 greenhouse crops. Kluwer, Dordrecht, the Netherlands. pp. 202 – 216. 256 Villanueva, R. T., Michaud, J. P., and Childers, C. C. (2004). Ladybeetles as predators of pest and 257 predacious mites in citrus. Journal of Entomological Science 39, 23–29. 258 Wittmeyer, J. L., and Coudron. T. A. (2001) Life table parameters, reproductive rate, intrinsic 259 rate of increase, and estimated cost of rearing Podisus maculiventris (Heteroptera: 260 Pentatomidae) on an artificial diet. Environmental Entomology 94, 1344–1352. 261 Yoon, C., Seo, D.‐K., Yanga, J.‐O., Kang, S.‐H., and Kim, G.‐H. (2010) Attraction of the predator, 262 Harmonia axyridis (Coleoptera: Coccinellidae), to its prey, Myzus persicae (Hemiptera: 263 Aphididae), feeding on Chinese cabbage. Journal of Asia‐Pacific Entomology 4, 255–260. Legaspi et al.: The Ficus Whitefly Page 12 of 24

264 Legaspi et al.: The Ficus Whitefly Page 13 of 24

265 Figure Captions 266 267 Figure 1. Tree defoliation caused by Ficus whitefly. 268 269 Figure 2. Current Ficus whitefly distribution in the United States. Based on surveys by the 270 Florida Department of Agriculture and Consumer Services, Division of Plant Industry. 271 Counties in pink were positive for Ficus whitefly 272 (http://doacs.state.fl.us/pi/enpp/ento/Singhiella%20simplex.html) 273 274 Figure 3. Life stages of the Ficus whitefly. A) Eggs B) Nymphs C) red‐eyed nymph (pupa) D) adult 275 276 Figure 4. Effect of temperature on development rate (egg to pupae): linear model r(T)= ‐ 277 0.0216421 + 0.0020499T (SE of estimates = 0.0010686, and 0.0000435, respectively; F = 278 2216.8; df = 1, 71; P < 0.01; R2 = 0.97). Briere model (dashed line) estimates: a =

279 0.0000146, T0 = 7.3120084; TL = 45.9512202 (ASE = 0.0000020, 1.0080836, and 280 3.3177988, respectively; R2 = 0.97) (from Legaspi et al. 2011) 281 282 Figure 5. Enkegaard surface showing effects of temperature and time on numbers of eggs laid. 283 Model was: eggs = (‐30.2105187+2.6177368T) d exp(‐0.0342074Td) (ASE = 8.83, 0.556, 284 0.0038, respectively) R2 = 0.16; where T is temperature and d is time (Enkegaard 1993) 285 (Legaspi et al. 2011) 286 287 Figure 6. Female adult survivorship (plotted on linear scale) (Legaspi et al. 2011) 288 289 Figure 7. Encarsia protransvena adult and parasitized whitefly nymph. Harmonia axyridis and 290 Olla v‐nigrum adults. (Photographs courtesy H. Glenn, University of Florida) 291 Legaspi et al.: The Ficus Whitefly Page 14 of 24

292 Figure 8. Predation by Delphastus catalinae on different life stages of the Ficus whitefly (JCL 293 unpublished data). Female predators were starved for 24‐h, then given a feeding period 294 of 24 h. 295 Legaspi et al.: The Ficus Whitefly Page 15 of 24

296 Fig. 1 297

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299 Fig 2 300

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307 Fig. 4 308

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312 Fig. 6 313

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324 Table 1. Effect of temperature on immature survival (days) of the ficus whitefly, 325 Singhiella simplex (means ± SE) (Legaspi et al. 2011) 326 Life stage Temperature (oC) 15 20 25 27 30 Eggs 36.00 ± 21.00 ±0.26b 11.00 ± 0.00c 10.21 ±0.14cd 8.00 ± 0.00e 0.82a First 1.56 ± 1.00 ± 0.00b 2.19 ±0.32a 1.00 ± 0.00b 1.00 ± 0.00b 0.18ab Second 18.78 ± 11.12 ± 0.18b 6.06 ± 0.28c 6.05 ± 0.26c 4.38 ± 0.33c 1.34a Third 11.67 ± 0.5a 6.18 ± 0.30b 3.06 ± 0.25c 6.21 ± 0.36b 3.38 ± 0.21c Fourth 22.56 12.88 ± 0.34b 8.56 ± 0.39c 4.05 ± 0.38d 5.54 ± 0.37d ±0.62a Pre‐pupae 3.67 ±0.64a 1.75 ± 0.25b 1.00 ± 0.00b 1.05 ± 0.05b 1.23 ± 0.12b Pupae 3.67 ±0.71a 2.38 ± 0.39b 1.06 ±0.06c 1.10 ±0.07c 1.23 ±0.17c Total 97.11 ± 56.31 ± 0.69b 32.81 ± 0.68c 29.74 ± 0.26d 25.23 ± 0.17e immatures 2.11a (16) (16) (19) (13) (9) 327 328 Insects in 35°C treatment did not survive and are excluded from analysis; each stage analyzed 329 separately for effects of temperature on life stage duration (means ± SE); Numbers in 330 parentheses indicates sample size; within each row, means followed by different letters are 331 significantly different Tukey HSD; P < 0.05) Legaspi et al.: The Ficus Whitefly Page 24 of 24

332 Table 2. Life history parameters for S. simplex (Legaspi et al. 2011) 333 Parameter Temperature (oC) 15 25 27 30 1 Net Reproductive Rate (R0) 13.055 21.464 23.114 13.834 Gross Reproductive Rate (GRR)2 19.495 29.415 24.25 16.62.0 Generation Time (T)3 99.3 35.48 31.413 26.86 Intrinsic Rate of Increase (r)4 0.0258 0.0864 0.0999 0.0978 Finite Rate of Increase ()5 1.0262 1.0902 1.105 1.103 Doubling Time (DT)6 26.87 8.022 6.93 7.087 334 335

1 R0 = lxmx summation of survivorship multiplied by age‐specific fecundity per female, expressed in units of &/&; egg numbers divided by 2 assuming 1:1 sex ratio 2 GRR =  mx ; summation of age‐specific fecundity per female in &/ & 3 T = ( xlxmx) / R0 in days 4 r ≈ (ln R0) / T in &/ &/day 5  = er in &/ &/day 6 DT = ln (2)/ r in days