Proc. Fla. State Hort. Soc. 119:417-421. 2006. UPDATE AND MANAGEMENT OF THE ASIAN PSYLLID, (: ) ON ORANGE JASMINE

CATHARINE MANNION* AND JORGE PEÑA ing pathogen; however, at this time, there needs to be further University of Florida, IFAS confirmation that it will host the disease organism. Tropical Research and Education Center Although orange jasmine could play an important role in 18905 SW 280th Street maintaining high populations of this pest, management in Homestead, FL 33031 the landscape may not always be warranted. The severity of damage witnessed on citrus is not usually as drastic on orange Additional index words. Murraya piniculata, citrus greening, jasmine. High populations of the psyllid on orange jasmine Huanglongbing can cause some leaf distortion and discoloration. Typically in the landscape in south Florida, populations of the psyllid on Abstract. The Asian citrus psyllid, Diaphorina citri Kuwayama orange jasmine rise and fall throughout the year, are com- (Sternorrhyncha: Psyllidae) is a pest of citrus and its close rel- monly preyed upon, and are not reported as a pest of concern atives. This psyllid is an efficient vector of the bacterium that to the homeowner. causes citrus greening. Orange jasmine, Murraya paniculata, Previous to the identification of the greening disease in is a common landscape and production plant in south and Florida, nursery growers did not report the Asian citrus psyl- central Florida, and also a host of the psyllid. High populations lid as a pest of concern on orange jasmine. Currently, there of the psyllid can be found on orange jasmine in the south are federal and state restrictions on the movement of host Florida landscape. There has been increased interest in man- agement of this pest with the recent confirmation of citrus plants of the greening disease and the Asian citrus psyllid. A greening in Florida. Currently, there is a compliance agree- state quarantine has been placed on several Florida counties ment for growers shipping orange jasmine from infested ar- and areas. Nursery growers shipping orange jasmine outside eas. Studies were conducted to determine the efficacy of the quarantine area must follow a compliance agreement that pesticides on psyllid populations on orange jasmine. All prod- specifies the necessary insecticide treatments required before ucts tested provided good to excellent control with the neon- the plants can be shipped. No plants can be shipped to citrus- ictinoids and pyrethroids providing the best control. These producing states. data provide more options to growers for insecticide manage- Currently there is little information on insecticides la- ment of the Asian citrus psyllid. beled for use on ornamental plants (production or land- scape) and the required options for control are limited. The Asian citrus psyllid, Diaphorina citri Kuwayama (Ster- There is a need for efficacy data of commercially available in- norrhyncha: Psyllidae) is a pest of citrus and its close relatives, secticides for use on ornamental plants. Studies were con- and first identified in Florida in 1998 (Halbert, 1998). The ducted to evaluate commercial products for control of Asian psyllid is currently established throughout the state. Although citrus psyllid on orange jasmine. it can damage plants directly through its feeding activities, the greater concern is that the psyllid is a primary vector of the Materials and Methods bacterium that causes the citrus greening or “Huanglong- bing” disease. Citrus greening disease is one of the most seri- Three insecticide efficacy tests were conducted at the ous citrus diseases in the world, and was found for the first Tropical Research and Education Center, Homestead, Fla. time in the U.S. in Miami-Dade County in August 2005. All tests were conducted on 3-gal orange jasmine standards in The life cycle of the Asian citrus psyllid takes 15-47 d de- containers which were obtained from a local grower. In tests pending on temperature (Mead, 1977; Tsai and Liu, 2000). 1 and 2, foliar treatment applications were applied with a CO2 The females lay their eggs on new flush, laying as many as 800 backpack sprayer (18 lb psi; TeeJet 3vs nozzle) at a volume of eggs in a lifetime. The nymphal stages produce waxy tubules 250 mL per plant. Drench treatments were poured over the and copious amounts of honeydew. Adults are small (3-4 soil surface at a volume of 385 mL per plant. In test 3, treat- mm), brownish that feed with their head down and ment applications were applied with a manual single cone their abdomen raised at about a 45° angle. nozzle sprayer at approximately 50 psi at a volume of 500 mL Orange jasmine, Murraya paniculata (Family Rutaceae), is per plant. Treatments and rates for all three tests are listed in a common landscape plant in central and south Florida (US- Table 1. DA hardiness zone 9B-11) and is also commercially produced The plants were initially infested with Asian citrus psyllid in south Florida (Gilman, 1999). Orange jasmine is a com- by placing them in the vicinity of an infested orange jasmine mon hedge plant but nursery growers have been encouraged hedge. Additional efforts to infest the plants were done for to grow it as a small tree for planting along streets under pow- the first test only which was conducted inside a greenhouse. er lines or as an accent or specimen tree anywhere in the trop- Adult psyllids were collected from an infested orange jasmine ical landscape. Orange jasmine is one of the preferred hosts hedge with a small vacuum, released into a cage, and then as- of the Asian citrus psyllid (Halbert and Manjunath, 2004; Tsai pirated from the cage for release in the greenhouse. Approx- and Liu, 2000). It is also suspected to be a host for the green- imately 100 adult psyllids were released weekly for 6 weeks prior to treatment application. In test 1, there were 8 replications (plants) per treatment. Two terminals per plant were randomly selected and re- *Corresponding author; e-mail: [email protected] moved from the plant by cutting just below the first full leaf.

Proc. Fla. State Hort. Soc. 119: 2006. 417

Table 1. Treatments, rates, and application methods for control of Asian cit- Table 2. The mean number of eggs of Asian citrus psyllid per orange jas- rus psyllid on orange jasmine. mine terminal in Test 1.

Treatment Mean number of eggs per terminal Test Trade name (active ingredient) Rate Application (days after treatment)

1 Marathon II (imidacloprid) 6 ml/cm diam drench Treatment 062034 Discus (imidacloprid + cyfluthrin) 25 oz/100 gal foliar Marathon II (drench) 0.69 az TriStar * (acetameprid) 96 g/100 gal foliar 8.94 a 0.00 a 0.69 a Yielder* (acetameprid) 224 g/100 gal foliar Discus 2.44 a 1.06 a 0.00 a 0.00 a Safari (dinotefuran) 8 oz/100 gal foliar TriStar 2.31 a 1.31 a 0.00 a 0.00 a Safari (dinotefuran) 24 oz/100 gal drench Yielder 5.06 a 1.12 a 0.00 a 1.81 a Flagship (thiamethoxam) 8 oz/100 gal foliar Safari 0.44 a 0.31 a 0.00 a 0.00 a Talstar (bifenthrin) 20 oz/100gal foliar Safari (drench) 1.44 a 0.75 a 2.34 a 6.75 a Azatin (azadirachtin) 14 oz/100 gal foliar Flagship 1.12 a 1.50 a 0.06 a 0.00 a Untreated control — — Talstar 6.94 a 0.75 a 0.06 a 0.00 a Azatin XL 0.69 a 1.38 a 0.81 a 0.81 a 2 Marathon II (imidacloprid) 1.7 oz/100 gal foliar Control 1.75 a 8.69 a 5.00 a 1.25 a Marathon II (imidacloprid) 6 ml/cm diam drench Discus (imidacloprid + cyfluthrin) 25 oz/100 gal foliar P value 0.0617 0.0774 0.4740 0.4285 Allectus (imidacloprid + bifenthrin) 10.7 oz/100 gal foliar zWithin columns, means followed by the same letter are not different. TriStar * (acetameprid) 96 g/100 gal foliar Yielder* (acetameprid) 224 g/100 gal foliar Safari (dinotefuran) 8 oz/100 gal foliar mean number of eggs in the control treatment ranged from Safari (dinotefuran) 12 oz/100 gal drench 1.25 to 8.69 per terminal. Twenty days after treatment appli- Safari (dinotefuran) 24 oz/100 gal drench cation, the mean number of eggs was less than one for all Flagship (thiamethoxam) 8 oz/100 gal foliar Talstar (bifenthrin) 20 oz/100gal foliar treatments except the drench application of Safari (2.3 eggs) Deltagard T&O (deltamethrin) 8 oz/100 gal foliar and the control (5.0 eggs). The mean number of nymphs per Tempo Ultra (cyfluthrin) 5.4 oz/100 gal foliar terminal prior to treatment (day 0) ranged from 5.5 to 18.2 Azatin (azadirachtin) 14 oz/100 gal foliar (Table 3). Regardless of treatment, the number of nymphs Judo (spiromesifen) 2 oz/100 gal foliar dropped to less than one in all treatments including the con- Judo (spiromesifen) 4 oz/100 gal foliar trol on the last two evaluations. There were no significant dif- Untreated control — — ferences among treatments on all evaluation dates except on 3 Actara 25WG (thiamethoxam) 4 oz/100 gal foliar day 6 (Table 3). On day 6, there were significantly fewer Carzol SP (formetanate hydrochloride) 20 oz/100 gal foliar nymphs in the Flagship, Yielder, Discus, and Safari (drench Danitol 2.4 EC (fenpropathrin) 51 oz/100 gal foliar and foliar applications). Fury 1.5 EC (zeta-cypermethrin) 8 oz/100 gal foliar Test 2. Overall the population was initially higher than in Prev-Am (sodium tetraborohydrate) 64 oz/100 gal foliar Test 1. The mean number of eggs per terminal did not signif- Venom 20 SG (dinotefuran) 14 oz/100 gal foliar icantly differ among treatments until 10 d after treatment and Experimental product + Citrus Oil 6 oz/100 gal foliar again on the final evaluation (Table 4). However, 10 and 17 d Untreated control — — after treatment, none of the insecticide treatments egg counts *Plus Capsil—2 oz/100 gal. were significantly lower than those for the control; and at 24 d after treatment, one treatment had significantly more eggs than the control. Each terminal was examined under a dissecting microscope On average, there were 48 nymphs per terminal on day 0. to determine the number of live eggs and nymphs. Evalua- Four days after treatment, all treatments except Yielder, Sa- tions were conducted 0, 6, 20, and 34 d after treatment. In test fari (low drench rate), and Judo (low rate) had significantly 2, there were also eight replications. The number of adults per plant was counted and then one terminal per plant was randomly selected and removed as described above. The Table 3. The mean number of nymphs of Asian citrus psyllid per orange jas- mine terminal in Test 1. number of eggs and nymphs were counted under a dissecting microscope. Evaluations were conducted 0, 4, 10, 17, 24 and Mean number of nymphs per terminal 31 d after the first application. In this test, a second applica- (days after treatment) tion of foliar treatments only was applied on day 21. In test 3, there were 7 replications (plants) per treatment. Two 5 cm Treatment 062034 terminals from each plant were randomly selected and re- Marathon II (drench) 9.00 a 1.19 ab 0.00 a 0.19 a moved from the plant. Each terminal was examined under a Discus 10.75 a 0.00 b 0.00 a 0.00 a dissecting microscope for live eggs, nymphs and adults. TriStar 13.06 a 0.62 ab 0.00 a 0.00 a All tests were analyzed using PROC GLM and significant Yielder 7.44 a 0.00 b 0.00 a 0.56 a means differences were determined using with the Student- Safari 12.06 a 0.12 b 0.00 a 0.44 a Newman-Keuls’ test at P ≤ 0.05. Safari (drench) 18.19 a 0.19 b 0.62 a 0.31 a Flagship 15.18 a 0.00 b 0.00 a 0.00 a Talstar 8.06 a 0.62 ab 0.00 a 0.00 a Results and Discussion Azatin XL 11.69 a 1.06 ab 0.25 a 0.75 a Control 5.56 a 2.12 a 0.38 a 0.06 a Test 1. The number of eggs did not significantly differ among treatments on all evaluation dates (Table 2). The P value 0.2830 0.0260 0.2515 0.7178

418 Proc. Fla. State Hort. Soc. 119: 2006.

Table 4. The mean number of eggs of Asian citrus psyllid per orange jasmine terminal in Test 2.

Mean number of eggs per terminal (days after treatment)

Treatment 041017 24 31 Marathon 16.00 a 4.12 a 28.12 ab 12.25 ab 0.87 b 0.12 a Marathon (Drench) 8.50 a 11.62 a 2.75 b 0.12 b 1.00 b 0.00 a Discus 21.50 a 10.50 a 2.75 b 0.00 b 3.37 b 0.00 a Allectus 14.37 a 13.12 a 2.00 b 0.50 b 4.00 b 0.00 a TriStar 17.87 a 8.87 a 13.87 ab 9.87 ab 0.62 b 0.25 a Yielder 12.87 a 5.25 a 51.87 a 52.25 a 1.12 b 2.25 a Safari Foliar 14.87 a 5.12 a 30.37 ab 17.25 ab 5.50 b 0.12 a Safari Low (Drench) 24.00 a 15.62 a 7.75 b 12.25 b 15.37 a 0.00 a Safari High (Drench) 28.62 a 9.25 a 0.00 b 8.87 b 8.75 ab 0.00 a Flagship 40.50 a 13.25 a 7.37 b 13.25 b 1.37 b 0.00 a Talstar 21.12 a 1.25 a 0.37 b 0.00 b 4.25 b 0.00 a Deltagard 10.87 a 4.87 a 1.50 b 0.00 b 0.00 b 0.00 a Tempo 16.00 a 12.00 a 2.50 b 0.62 b 0.00 b 0.00 a Azatin 14.50 a 1.75 a 24.37 ab 25.87 ab 1.25 b 0.87 a Judo Low 28.00 a 15.00 a 37.00 ab 25.75 ab 1.00 b 0.00 a Judo High 15.25 a 17.62 a 54.37 a 7.25 b 6.62 b 0.62 a Control 29.00 a 15.00 a 38.25 ab 37.37 ab 0.50 b 0.12 a P value 0.5404 0.7032 0.0001 0.0005 0.0009 0.6006 lower numbers of nymphs compared to the control (Table 5). among treatments 24 and 31 d after treatment. Those prod- All treatments were significantly lower than the control 24 d ucts that ultimately provided 100 percent control of adults in- after treatment. Those treatments that ultimately provided cluded Discus, Yielder, Safari (foliar and both drench rates), 100 percent control of the nymphs included Marathon Flagship, Talstar, Deltagard, Tempo and Judo (high rate) but (drench), Discus, Allectus, Safari (foliar), Flagship, Talstar, the number of adults in the control was very low. The highest Deltagard, and Tempo. number of adults in the control, after treatment, was on day The average number of adults before treatment (day 0) 4. The treatments that provided 100 percent control on day 4 was 3 per terminal. Four days after treatment, there were sig- included Discus, Allectus, Talstar, and Tempo. nificantly fewer adults in the Marathon (drench), Discus, Test 3. The average number of eggs per terminal was high- Allectus, Flagship, Talstar, Deltagard, Tempo and Azatin ly variable at the initiation of this test. Six days after treat- treatments compared to the control (Table 6). None of the ment, all treatments significantly reduced the number of insecticide treatments were significantly different from the eggs per terminal compared to the control (Table 7). How- control 10 d after application. However, by 17 d, Marathon ever, in the two subsequent evaluations the number of eggs (drench), Discus, Allectus, Yielder, Safari (foliar), Talstar, in the control decreased and there were no significant differ- Deltagard, and Tempo provided significantly fewer adults ences among treatments. None of the treatments provided than the control. There were no significant differences 100 percent control.

Table 5. The mean number of nymphs of Asian citrus psyllid per orange jasmine terminal in Test 2.

Mean number of nymphs per terminal (days after treatment)

Treatment 041017 24 31 Marathon 45.62 0.37 b 4.62 ab 13.00 ab 0.62 b 0.12 b Marathon (Drench) 39.12 2.00 b 0.12 b 0.50 b 0.25 b 0.00 b Discus 54.37 0.12 b 0.37 b 2.37 b 0.25 b 0.00 b Allectus 47.25 0.12 b 0.12 b 1.75 b 1.50 b 0.00 b TriStar 47.75 2.25 b 7.25 ab 16.50 ab 0.00 b 0.75 b Yielder 35.00 7.87 ab 2.37 b 22.37 ab 0.00 b 0.87 b Safari Foliar 28.50 0.37 b 2.75 ab 34.50 a 0.00 b 0.00 b Safari Low (Drench) 50.87 7.62 ab 1.62 b 2.12 b 12.62 b 13.25 a Safari High (Drench) 55.62 1.87 b 0.00 b 0.87 b 6.62 b 5.25 b Flagship 68.12 2.00 b 0.12 b 2.50 b 0.37 b 0.00 b Talstar 63.37 0.12 b 0.00 b 0.25 b 1.00 b 0.00 b Deltagard 32.75 3.12 b 0.37 b 0.00 b 0.25 b 0.00 b Tempo 45.12 0.87 b 13.62 a 0.00 b 0.00 b 0.00 b Azatin 18.50 2.50 b 11.87 ab 25.25 ab 9.37 b 1.50 b Judo Low 46.12 7.25 ab 5.75 ab 17.00 ab 1.75 b 0.87 b Judo High 35.12 1.75 b 5.62 ab 24.00 ab 7.25 b 1.37 b Control 57.25 13.62 a 13.62 a 37.62 a 33.37 a 8.25 ab P value 0.1923 0.0001 0.0001 0.0001 0.0001 0.0008

Proc. Fla. State Hort. Soc. 119: 2006. 419

Table 6. The mean number of adults of Asian citrus psyllid per orange jasmine terminal in Test 2.

Mean number of adults per terminal (days after treatment)

Treatment 041017 24 31 Marathon 2.50 a 0.62 bc 0.62 ab 0.12 ab 0.00 a 0.12 a Marathon (Drench) 3.12 a 0.25 c 0.00 b 0.00 b 0.00 a 2.00 a Discus 2.50 a 0.00 c 0.00 b 0.00 b 0.00 a 0.00 a Allectus 3.25 a 0.00 c 0.25 b 0.00 b 0.00 a 0.12 a TriStar 2.50 a 0.75 bc 0.25 b 0.62 a 0.00 a 0.12 a Yielder 2.62 a 1.12 bc 0.75 ab 0.00 b 0.12 a 0.00 a Safari Foliar 3.75 a 0.87 bc 0.50 b 0.00 b 0.00 a 0.00 a Safari Low (Drench) 2.75 a 2.62 a 0.25 b 0.62 a 0.12 a 0.00 a Safari High (Drench) 2.62 a 0.75 bc 0.00 b 0.25 a 0.12 a 0.00 a Flagship 4.50 a 0.12 c 0.25 b 0.12 ab 0.00 a 0.00 a Talstar 3.75 a 0.00 c 0.00 b 0.00 b 0.00 a 0.00 a Deltagard 1.75 a 0.12 c 0.00 b 0.00 b 0.00 a 0.00 a Tempo 2.50 a 0.00 c 0.00 b 0.00 b 0.00 a 0.00 a Azatin 2.50 a 0.12 c 0.62 ab 0.12 ab 0.12 a 0.12 a Judo Low 3.00 a 1.87 ab 1.50 a 0.37 a 0.00 a 0.37 a Judo High 3.50 a 0.62 bc 0.75 ab 0.12 ab 0.12 a 0.00 a Control 4.00 a 1.87 ab 1.00 ab 0.62 a 0.12 a 0.25 a P value 0.8054 0.0001 0.0001 0.0045 0.8015 0.4147

At the initiation of this test, there were on average 39 the pyrethroids and neonicotinoids provided the best and nymphs per terminal. All treatments caused a significant re- most consistent control. Ultimately, 100 percent control of duction in the number of nymphs compared to the control the nymphs with foliar applications was achieved with Allec- on both 6 and 20 d after treatment (Table 8). Danitol, Fury, tus, Discus, Talstar, Deltagard, Tempo, TriStar, and Flagship and the Experimental Product provided 100 percent control. or drench applications of Marathon (Tables 3 and 5). On the last evaluation (34 d after application) all the treat- The products used in Test 3 are labeled for use in a broad ments, except Carzol and Venom, continued to provide ex- list of agricultural crops. In general, products with the same cellent control of the nymphs which was significantly lower active ingredient as the ornamental products tested similarly. than the control. All products provided good to excellent control with the pyre- The mean number of adults averaged less than one per throids (Danitol and Fury) providing 100 percent control. terminal at the beginning of the test. The number of adults In all the tests, the psyllid population decreased with time was significantly reduced compared to the control 6 d after in the control treatments to the point of not being significant- treatment only (Table 9). Those products that provided this ly different from the insecticide treatments. It is unknown control included Actara, Carzol, Danitol, Fury and the Exper- why this occurred, however, it is speculated that the adults are imental Product. Fury was the only product to ultimately pro- quite mobile and moved around to feed on plants within the vide 100 percent control of adults. test vicinity which all were treated with insecticides. As a re- Overall, the products tested in all three tests provided sult, the population slowly decreased, even on the controls. good to excellent control. In the first two tests, the products These data provide more options to growers to manage tested are labeled for use on ornamental plants in production the Asian citrus psyllid. Additionally, there are a least four or in the landscape. Although there was some variability mode-of-action groups represented among these pesticides among effectiveness on life stages among the products, all of which will allow selection of products to alternate within a these products could be used for psyllid control. Generally, management program to reduce the chance of insecticide

Table 7. The mean number of eggs of Asian citrus psyllid per orange jas- Table 8. The mean number of nymphs of Asian citrus psyllid per orange jas- mine terminal in Test 3. mine terminal in Test 3.

Mean number of eggs per terminal Mean number of nymphs per terminal (days after treatment) (days after treatment)

Treatment 062034 Treatment 062034 Actara 25WG 0.71 a 2.21 b 2.14 a 7.21 a Actara 25WG 32.6 a 0.86 b 1.14 b 0.64 b Carzol SP 2.93 a 4.64 b 10.00 a 1.21 a Carzol SP 43.5 a 1.57 b 11.50 b 10.07 ab Danitol 2.4 EC 0.07 a 0.57 b 1.36 a 3.14 a Danitol 2.4 EC 35.1 a 0.50 b 0.00 b 0.57 b Fury 1.5 EC 0.21 a 3.36 b 0.07 a 2.14 a Fury 1.5 EC 50.9 a 0.00 b 0.00 b 0.79 b Prev-Am 17.00 a 2.50 b 8.00 a 7.50 a Prev-Am 43.6 a 4.21 b 3.86 b 4.79 b Venom 20 SG 2.36 a 1.86 b 8.21 a 3.00 a Venom 20 SG 41.5 a 0.00 b 0.07 b 8.36 ab Experimental + Oil 0.86 a 7.36 b 2.79 a 2.64 a Experimental + Oil 38.7 a 0.00 b 0.00 b 0.50 b Control 1.29 a 22.36 a 10.21 a 1.36 a Control 29.0 a 42.57 a 38.93 a 15.50 a P value 0.3620 0.0001 0.3549 0.2415 P value 0.8133 0.0001 0.0003 0.0083

420 Proc. Fla. State Hort. Soc. 119: 2006.

Table 9. The mean number of adults of Asian citrus psyllid per orange jas- resistance. Additionally, some of these products may be now mine terminal in Test 3. considered for use as part of the requirement for certification to ship orange jasmine outside the quarantine areas. Mean number of adults per terminal (days after treatment)

Treatment 062034 Literature Cited

Actara 25WG 0.07 a 0.07 b 0.14 a 0.36 a Gilman, E. F. 1999. Murraya paniculata. Florida Coop. Ext. Ser. EDIS Fact Carzol SP 0.43 a 0.00 b 0.00 a 0.07 a Sheet FPS-416. Danitol 2.4 EC 0.71 a 0.00 b 0.14 a 0.07 a Halbert, S. E. 1998. Entomology Section. Tri-ology (May-June 1998) 37(3):6-7. Fury 1.5 EC 0.43 a 0.00 b 0.00 a 0.00 a Halbert, S. E. and K. L. Manjunath. 2004. Asian citrus psyllids (Sternorrhyn- Prev-Am 0.64 a 0.50 ab 0.07 a 0.07 a cha: Psyllidae) and greening disease of citrus: a literature review and as- sessment of risk in Florida). Fla. Entomol. 87(3):330-353. Venom 20 SG 0.07 a 0.21 ab 0.14 a 0.36 a Mead, F. W. 1977. The Asiatic citrus psyllid, Diaphorina citri Kuwayama Experimental + Oil 0.71 a 0.00 b 0.00 a 0.21 a (Homoptera: Psyllidae). Entomology Circular 180. FDACS, DPI. 4pp. Control 1.00 a 0.57 a 0.00 a 1.14 a Tsai, J. H. and Y. H. Liu. 2000. Biology of Diaphorina citri (Homoptera: Psyl- P value 0.2445 0.0114 0.6432 0.0534 lidae) on four host plants. J. Econ. Entomol. 93(6):1721-1725.

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