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Bemisia tabaci MED (Q biotype) (Hemiptera: Aleyrodidae) in Florida is on the move to residential landscapes and may impact open-field agriculture.

Q biotype whiteflies, more properly known as Bemisia tabaci Mediterranean (MED) and classified as B. tabaci (Gennadius) (Hemiptera: Aleyrodiae) (Dennehy et al. 2005; McKenzie et al. 2009, 2012), have been in the United States for approximately a dozen years. First found on poinsettia during fall 2004 in a retail outlet in Arizona (Dennehy et al. 2005), B. tabaci MED has since been identified from greenhousegrown ornamental horticulture plants in 26 states (McKenzie et al. 2012), including Florida (McKenzie et al. 2009). Indistinguishable morphologically from silverleaf whitefly (B. tabaci Middle Eastern Asia Minor 1 [MEAM1]), B. tabaci MED is extremely problematic to agricultural production because it has a high propensity to develop resistance to insect growth regulators (Horowitz et al. 2003) and neonicotinoid insecticides (Elbert & Nauen 2000; Horowitz et al. 2004). Both of these insecticide classes play crucial roles in controlling whiteflies in many different cropping systems including cotton (Ellsworth & Martinez-Carrillo 2001), vegetables (Palumbo et al. 2001), and ornamentals (McKenzie et al. 2014). Associated with the appearance of B. tabaci MED in the United States were reports of increasing problems in controlling whitefly infestations, primarily from ornamental growers. Population studies indicate B. tabaci MED was introduced into the United States on at least 3 separate occasions, and both eastern and western B. tabaci MED are found throughout the continental United States including Florida (Dickey et al. 2013). Previously, B. tabaci MED had been detected in North America only on ornamental plants and herbs in greenhouses and nurseries. This, however, changed in the spring of 2016, and the first detections of B. tabaci MED in residential landscapes and open field agricultural production are reported here.

Adults or immature stages of whiteflies collected were immediately placed in 95% ethanol for molecular analysis. If available, at least 12 whiteflies from each sample were used for species determination following the protocol developed by Shatters et al. (2009). DNA was extracted from individual whiteflies by placing a single whitefly in a 1.5 mL microcentrifuge tube, adding 50 [micro]l DNA lysis buffer, and grinding with a pestle. The pestle was rinsed with an additional 50 [micro]l DNA lysis buffer that was collected in the same tube. Tubes were placed in a metal boiling rack and boiled at 95 [degrees]C for 5 min and then placed in crushed ice for 5 min. Tubes were then centrifuged at 8,000 g for 30 s, and the supernatant (crude DNA lysate) was transferred to a new tube and stored at -80 [degrees]C for future processing.

We used species (biotype) specific polymerase chain reaction (PCR) primers that had been designed by Shatters et al. (2009) to recognize unique mtCOI gene regions within the MEAM1 (B biotype), NW biotype, and MED (Q biotype) species; these primers produce different-sized products depending on the source of the isolated template DNA and do not require DNA sequencing. The chosen mtCOI primer pairs amplified fragments of 303, 405, and 478 bp from DNA of the MED, NEW WORLD, and MEAM1 species, respectively. The 30 [micro]l final volume PCRs were run using a PTC-0200 DNA Engine[R] Peltier thermal cycler (MJ Research, Inc., Waltham, Massachusetts) under the conditions described by Shatters et al. (2009).

PCR amplifications for the mtCOI gene were also performed using the Btab-Uni primer set described by Shatters et al. (2009) for whiteflies determined to be B. tabaci NW biotype in any environment or B. tabaci MED in unique environments (residential landscapes and open field agriculture) by the species specific primer cocktail. An mtCOI sequence analysis was performed first by PCR amplifying an approximately 700 to 800 bp mtCOI DNA fragment and then sequencing the PCR amplified DNA. The 30 [micro]l PCRs were run using a T100 (TM) Thermal Cycler (BIO-RAD Laboratories, Inc., Hercules, California) under the conditions described by Shatters et al. (2009). Prior to sequencing, the amplified products were cleaned using Montage ([R]) PCR cleanup filters (Millipore, Billerica, Massachusetts). Fifty ng of total whitefly genomic DNA were used in BigDye[R] (Applied Biosystems, Foster City, California) sequencing reactions. All sequencing was performed bidirectionally with the amplification primers and BigDye ([R])Terminator v3.1 Cycle Sequencing Kits (Applied Biosystems, Foster City, California). Sequence reactions were analyzed on an Applied Biosystems[R] 3730XL DNA Analyzer (Applied Biosystems, Foster City, California) and were then compared and edited using Sequencher software (Gene Codes, Ann Arbor, Michigan). Biotype determination was based on direct sequence comparisons using the web based National Center for Biotechnology Information BLAST sequence comparison application (http://blast.ncbi.nlm.nih.gov/Blast.cgi), and sequences were deposited in GenBank.

Since the previous B. tabaci distribution surveys were done in Florida statewide (McKenzie et al. 2009) and in North America (McKenzie et al. 2012), B. tabaci MED was detected in Florida in 2011 (7 detections), 2013 (2), and 2014 (3) primarily on poinsettia (11) with a single detection on hibiscus. All B. tabaci MED detections were from nursery or greenhouse environments (McKenzie unpublished data). In 2016, landscapers and pest control operators in Palm Beach County, Florida, began experiencing problems controlling extremely high populations of Bemisia whiteflies on hibiscus plantings in multiple residential neighborhoods. In total, 10 residential landscapes were identified and subsequently determined to be infested by eastern B. tabaci MED (Table 1). Bemisia tabaci MED detected at 1 location was traced back to a wholesale nursery, and the infestation was the direct result of a new planting of hibiscus. Before it was contained, this infestation spread to lantana and a ficus hedge located on 2 neighboring properties. Bemisia tabaci MED was also detected on single family residences with established hibiscus (not new plantings), firecracker flower or mixed ficus hedges that did not have any apparent connection and were kilometers apart from one another. The original source of these infestations remains unknown. Bemisia tabaci MED was detected in Florida as far north as Tequesta, as far east as Palm Beach Island, as far south as Boca Raton, and as far west as Boynton Beach with a few detections in the center of Palm Beach County. In all of these residential landscape collections, B. tabaci MED comprised the entire sample. Three residential landscape collections resulted in 100% B. tabaci MEAM1 (data not shown). All residential detections were in very affluent well-manicured landscapes.

Florida vegetable fields have been heavily sampled to determine B. tabaci species composition for well over a decade and especially in tomato (McKenzie et al. 2004, 2009, 2012; Schuster et al. 2010; Caballero et al. 2014; Smith et al. 2016) with only B. tabaci MEAM1 being detected. In 2016, we processed 551 whiteflies from 28 vegetable field samples including tomato (9), cucumber (2), potato (1), watermelon (6), eggplant (3), and sweet potato (7); all were B. tabaci MEAM1. In Aug 2016, B. tabaci MED was detected in a field of sweet potato in Elkton, St. John County (Table 1), at a very low ratio (15:1 MEAM1: MED). This collection was totally comprised of immature nymphs removed from a sweet potato leaf from an isolated open field planted 90 d prior indicating that, because whitefly immatures are not mobile after the 1st instar, B. tabaci MED had oviposited on sweet potato in the field. However, approximately 1 wk after the initial collection, additional whitefly samples were taken from the same field, and only B. tabaci MEAM1 was detected (138:0 MEAM1: MED). Bemisia tabaci MED was also detected (1:16 MEAM1: MED) on morning glory weeds growing on the border of a fallow vegetable field ready to go into production in Palm Beach County and was confirmed 3 wk later with another sample (2:3 MEAM1: MED). This field was 800 m west of a wholesale nursery known to have B. tabaci MED.

In addition to the residential and open field detections, B. tabaci MED has been detected in 8 wholesale nurseries from 4 counties and 17 retail nurseries from 8 counties in Florida (Table 2). Bemisia tabaci MED was detected on multiple sampling dates from several of the nurseries. Hibiscus was the driving host plant in nursery (wholesale and retail) infestations and accounted for 78% of B. tabaci MED detections followed by firecracker flower and eggplant each with 9% and a single lantana detection. Sixty-five percent of the B. tabaci MED positive samples (21) were 100% B. tabaci MED and 35% (11) were mixed populations of B. tabaci MEAM1 and MED. One hundred samples from retail and wholesale nurseries were 100% B. tabaci MEAM1 and 1 sample from a retail nursery sampled from mint was 5:1 MEAM1:NW (National Center for Biotechnology Information accession number: KY131961) and represents the first detection of B. tabaci NW in Florida since it was displaced by B. tabaci MEAM1 in the mid-1980s (McKenzie et al. 2004, 2009, 2012).

We do not know why B. tabaci MED (Q biotype) emerged as a pest in Florida landscapes in 2016. Bemisia tabaci is not usually a problem in the landscape due to the multiple host plants and the presence of a complex of natural enemies that keep whiteflies in check. In addition, commercial producers of ornamental plants have successfully managed B. tabaci MED since its first detection in Florida years ago.

Several factors may explain the detection of B. tabaci MED in Florida landscapes in 2016. First, environmental conditions may have been favorable for the buildup of B. tabaci in the landscape. It is also possible that growers have gotten complacent and less vigilant in implementing solid whitefly management strategies. In addition, due to recent publicity about potential impacts on pollinators, some large retail garden centers have been pressuring ornamental producers to stop using neonicotinoid insecticides. Certain neonicotinoids are among the few insecticides that are highly effective against B. tabaci MED. As a result, some growers may have relied on older, less effective chemistries to which B. tabaci MED is resistant. These include pyrethroids, organo-phosphates, carbamates, insect growth regulators, and some neonicotinoids (Nauen et al. 2002, Horowitz et al. 2005, Nauen & Denholm, 2005).

Because we have detected B. tabaci MED in open field crops in the United States for the first time, and this pest is known to attack vegetables and cotton in other countries, there is a risk that unmanaged populations of B. tabaci MED could move from protected ornamental greenhouse production to open agriculture. In some cases, vegetable transplants and an array of ornamental plants are grown together in a greenhouse, which further increases the risk of introducing B. tabaci MED to field plantings of vegetables. There is also a concern that increased pesticide resistance will evolve in B. tabaci MEAM1.

To decrease the risk of B. tabaci MED and insecticide resistant B. tabaci MEAM1 spreading from ornamentals to field-grown vegetables and cotton, it is critical for producers and managers of ornamental plants to practice sound integrated pest management. This includes the use of cultural control, biopesticides, natural products (oils, soaps), and biological control. These management practices can provide some control of whiteflies under low pest pressure. However, under higher pest pressure, it is critical for growers to select targeted chemistry with known activity against B. tabaci MED and, if necessary, destroy infested crops.

This research was partially funded by the Floriculture and Nursery Research Initiative of the United States Department of Agriculture, Agricultural Research Service.

References Cited

Caballero R, Cyman S, Schuster DJ. 2014. Monitoring insecticide resistance in biotype B of Bemisia tabaci (Hemiptera: Aleyrodidae) in Florida. Florida Entomologist 96: 1243-1256.

Dennehy TJ, Degain BA, Harpold VS, Brown JK, Morin S, Fabrick JA, Byrne F, Nichols RL. 2005. New challenges to management of whitefly resistance to insecticides in Arizona. The University of Arizona-Cooperative Extension, Vegetable Report Series P-144, https://extension.arizona.edu/pubs/az1382_2.pdf (last accessed 28 Feb 2017).

Dickey A, Osborne LS, Shatters Jr RG, Hall P, McKenzie CL. 2013. Population genetics of invasive Bemisia tabaci cryptic species in the United States based on microsatellite markers. Journal of Economic Entomology 106: 1355-1364.

Elbert A, Nauen R. 2000. Resistance of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides in southern Spain with special reference to neonicotinoids. Pest Management Science 56: 60-64.

Ellsworth PC, Martinez-Carrillo JL. 2001. IPM for Bemisia tabaci: a case study from North America. Crop Protection 20: 853-869.

Horowitz AR, Gorman K, Ross G, Denholm I. 2003. Inheritance of pyriproxyfen resistance in the whitefly, Bemisia tabaci (Q biotype). Archives of Insect Biochemistry and Physiology 54: 177-186.

Horowitz AR, Kontsedalov S, Ishaaya I. 2004. Dynamics of resistance to the neonicotinoids acetamiprid and thiamethoxam in Bemisia tabaci (Homoptera: Aleyrodidae). Journal of Economic Entomology 97: 2051-2056.

Horowitz AR, Kontsedalov S, Khasdan V, Ishaaya I. 2005. Biotypes B and Q of Bemisia tabaci and their relevance to neonicotinoid and pyriproxyfen resistance. Archives of Insect Biochemistry and Physiology 58: 216-225.

McKenzie CL, Anderson PK, Villarreal N. 2004. An extensive survey of Bemisia tabaci (Homoptera: Aleyrodidae) in agricultural ecosystems in Florida. Florida Entomologist 87: 403-407.

McKenzie CL, Hodges G, Osborne LS, Byrne FJ, Shatters RG. 2009. Distribution of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in Florida--investigating the "Q" invasion. Journal of Economic Entomology 102: 670-676.

McKenzie CL, Bethke JA, Byrne FJ, Chamberlin JR, Dennehy TJ, Dickey AM, Gilrein D, Hall PM, Ludwig S, Oetting RD, Osborne LS, Schmale L, Shatters Jr RG. 2012. Distribution of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in North America following the Q invasion. Journal of Economic Entomology 105: 753-766.

McKenzie CL, Kumar V, Palmer CL, Oetting RD, Osborne LS. 2014. Chemical class rotations for control of Bemisia tabaci (Hemiptera: Aleyrodidae) on poinsettia and their effect on cryptic species population composition. Pesticide Management Science 70: 1573-1587.

Nauen R, Denholm I. 2005. Resistance of insect pests to neonicotinoid insecticides: current status and future prospects. Archives of Insect Biochemistry and Physiology 58: 200-215.

Nauen R, Stumpf N, Elbert A. 2002. Toxicological and mechanistic studies on neonicotinoid cross resistance in Q-type Bemisia tabaci (Hemiptera: Aleyrodidae). Pest Management Science 58: 868-875.

Palumbo J, Horowitz AR, Prabhaker N. 2001. Insecticidal control and resistance management for Bemisia tabaci. Crop Protection 20: 739-765.

Schuster DJ, Mann RS, Toapanta M, Cordero R, Thompson S, Cyman S, Shurtleff A, Morris RF. 2010. Monitoring neonicotinoid resistance in biotype B of Bemisia tabaci in Florida. Pest Management Science 66: 186-195.

Smith HA, Nagle CA, MacVean CA, McKenzie CL. 2016. Susceptibility of Bemisia tabaci MEAM1 (Hemiptera: Aleyrodidae) to imidacloprid, thiamethoxam, dinotefuran and flupyradifurone in south Florida. Insects 7: 57.

Shatters Jr RG, Powell CA, Boykin LM, Sheng HL, McKenzie CL. 2009. Improved DNA barcoding method for Bemisia tabaci and related Aleyrodidae: development of universal and Bemisa tabaci biotype-specific mitochondrial cytochrome c oxidase I polymerase chain reaction primers. Journal of Economic Entomology 102: 750-758.

Cindy L. McKenzie (1,*) and Lance S. Osborne (2)

(1) United States Department of Agriculture, Agricultural Research Service, United States Horticultural Research Laboratory, Fort Pierce, FL 34945, USA; E-mail: cindy.mckenzie@ars.usda.gov (C. L. M.)

(2) University of Florida, Entomology and Nematology Department, Mid-Florida Research & Education Center, Apopka, FL 32703, USA; E-mail: lsosborn@ufl.edu (L. S. O.)

Please Note: Illustration(s) are not available due to copyright restrictions.
Table 1. Sample date, location by city and zip code, host plant,
electrophoresis and sequencing results, and National Center for
Biotechnology Information (NCBI) accession number for residential
landscape and open field detections of Bemisia tabaci Mediterranean
(MED).

Sample date    Location by city             Host plant
               and zip code

25 Apr 2016    North Palm Beach, FL 33408   Hibiscus
 4 May 2016    North Palm Beach, FL 33408   Hibiscus
 4 May 2016    North Palm Beach, FL 33408   Lantana
 4 May 2016    North Palm Beach, FL 33408   Ficus / Hibiscus
12 May 2016    Palm Beach, FL 33480         Hibiscus
13 May 2016    Boca Raton, FL 33496         Hibiscus
20 May 2016    Boynton Beach, FL 33437      Hibiscus
24 May 2016    Palm Beach, FL 33480         Hibiscus
 7 Jun 2016    Boca Raton, FL 33496         Firecracker flower
25 Jul 2016    Tequesta, FL 33469           Porterweed
25 Jul 2016    Tequesta, FL 33469           Hibiscus
               Field Detections
17 Aug 2016    Elkton, FL 32033             Sweet Potato
23 Aug 2016    Elkton, FL 32033             Sweet Potato
25 Aug 2016    Boynton Beach, FL 33472      Morning glory on fallow
                                            vegetable field border
16 Sept 2016   Boynton Beach, FL 33472      Morning glory on fallow
                                            vegetable field border

               Electrophoresis   Uni-tab MED   NCBI
               results           sequence      accession
Sample date    MEAM1:MED (a)     results       number

25 Apr 2016      0:44            Eastern MED   KY073617
 4 May 2016      0:4             Eastern MED   KY073618
 4 May 2016      0:20            Eastern MED   KY073619
 4 May 2016      0:12            Eastern MED   KY073620
12 May 2016      0:20            Eastern MED   KY073621
13 May 2016      0:20            Eastern MED   KY073622
20 May 2016      0:20            Eastern MED   KY073623
24 May 2016      0:1             Eastern MED   KY073624
 7 Jun 2016      0:14            Eastern MED   KY073625
25 Jul 2016      0:18            Eastern MED   KY073626
25 Jul 2016      0:18            Eastern MED   KY073627

17 Aug 2016     15:1             Eastern MED   KY073628
23 Aug 2016    138:0             no MED data   Not applicable
25 Aug 2016      1:16            Eastern MED   KY073629
16 Sept 2016     2:3             Eastern MED   KY131960

(a) MEAM1 = Middle Eastern Asia Minor 1.

Table 2. Sample date, host plant, nursery environment, Florida county,
and biotype specific primer results for wholesale and retail nursery
detections of Bemisia tabaci Middle Eastern Asia Minor 1 (MEAM1;
biotype B) and Mediterranean (MED; biotype Q).

Date received   Host plant           Nursery environment  Florida county

11 May 2016     Hibiscus             Wholesale (1)        Palm Beach
 1 Jun 2016     Hibiscus             Wholesale (2)        Highlands
12 Jun 2016     Hibiscus             Retail (1)           Martin
13 Jun 2016     Hibiscus             Wholesale (2)        Highlands
13 Jun 2016     Hibiscus             Wholesale (3)        Palm Beach
14 Jun 2016     Hibiscus             Retail (2)           Seminole
14 Jun 2016     Hibiscus             Retail (2)           Seminole
17 Jun 2016     Hibiscus             Retail (3)           Palm Beach
17 Jun 2016     Hibiscus             Retail (3)           Palm Beach
17 Jun 2016     Hibiscus             Retail (4)           Duval
22 Jun 2016     Hibiscus             Retail (5)           Broward
22 Jun 2016     Firecracker flower   Retail (6)           Pinellas
23 Jun 2016     Hibiscus             Retail (7)           Palm Beach
23 Jun 2016     Hibiscus             Retail (8)           Martin
27 Jun 2016     Eggplant             Retail (9)           Hillsborough
27 Jun 2016     Hibiscus             Retail (10)          Palm Beach
 6 Jul 2016     Eggplant             Retail (11)          Seminole
 6 Jul 2016     Hibiscus             Wholesale (4)        Miami-Dade
 6 Jul 2016     Hibiscus             Retail (12)          Palm Beach
18 Jul 2016     Hibiscus             Wholesale (5)        Palm Beach
18 Jul 2016     Hibiscus             Retail (13)          Palm Beach
18 Jul 2016     Lantana              Wholesale (6)        Hillsborough
18 Jul 2016     Hibiscus             Wholesale (1)        Palm Beach
18 Jul 2016     Hibiscus             Wholesale (1)        Palm Beach
22 Jul 2016     Hibiscus             Retail (14)          Palm Beach
27 Jul 2016     Firecracker flower   Wholesale (7)        Hillsborough
27 Jul 2016     Hibiscus             Wholesale (8)        Miami-Dade
29 Jul 2016     Firecracker flower   Wholesale (7)        Hillsborough
12 Aug 2016     Eggplant             Retail (15)          St. Lucie
22 Aug 2016     Hibiscus             Retail (16)          Martin
 8 Sept 2016    Hibiscus             Retail (17)          Palm Beach
 8 Sept 2016    Hibiscus             Wholesale (8)        Miami Dade

                Biotype specific primer
Date received   MEAM1 (B)   MED (Q)

11 May 2016      0          16
 1 Jun 2016      0          23
12 Jun 2016      1           1
13 Jun 2016      1           7
13 Jun 2016      0           1
14 Jun 2016      0           5
14 Jun 2016      0          16
17 Jun 2016      0          20
17 Jun 2016      1           8
17 Jun 2016      0          20
22 Jun 2016      0           2
22 Jun 2016      0           6
23 Jun 2016      0           1
23 Jun 2016      0           2
27 Jun 2016     14           1
27 Jun 2016      0           1
 6 Jul 2016     10           1
 6 Jul 2016      6           1
 6 Jul 2016      0          18
18 Jul 2016      0           6
18 Jul 2016      0           4
18 Jul 2016     15           2
18 Jul 2016      0          13
18 Jul 2016      1           3
22 Jul 2016      0           7
27 Jul 2016     13           3
27 Jul 2016      0          16
29 Jul 2016      0           8
12 Aug 2016     15           1
22 Aug 2016      0           3
 8 Sept 2016     0           3
 8 Sept 2016     6          10

(a) Samples under nursery environment with the same superscript number
are confirmatory (2 or more collections at the same wholesale or retail
nursery from different sampling dates).
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Author:McKenzie, Cindy L.; Osborne, Lance S.
Publication:Florida Entomologist
Article Type:Report
Geographic Code:1U5FL
Date:Jun 1, 2017
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