1 2 3 4 Jesusa C. Legaspi 5 USDA-ARS-CMAVE 6 FAMU

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 insects 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 insect 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

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