Current Status of Thrips (Thysanoptera: Thripidae) in Vidalia Onions in Georgia

Abstract The Vidalia onion crop in Georgia is grown in the winter, and the key insect pests in Georgia are thrips (Thysanoptera: Thripidae). The thrips complex consists predominantly of tobacco thrips, Frankliniella fusca (Hinds), with smaller percentages of western flower thrips, F. occidentalis Pergande, eastern flower thrips, F. tritici (Fitch) and onion thrips, Thrips tabaci Lindeman. Onion thrips has become a greater concern in the last 10 years likely due to the introduction of a more aggressive biotype of T. tabaci on onions coming from Peru into the Vidalia region. A preliminary laboratory bioassay at 25 °C suggested that this onion thrips biotype could out-compete tobacco thrips on onions. Surveys were conducted from 2004 through 2013 in commercial Vidalia onion fields to determine if this increase in the percentage of onion thrips would occur. Average seasonal temperatures were highly correlated (r = 0.811) with percent T. tabaci and negatively correlated (r = -0.807) with F. fusca. The results suggest that temperature might regulate the proportion of onion thrips to tobacco thrips in the field, with a higher percentage of tobacco thrips occurring during cool winters and more onion thrips occurring in warm winters. Nevertheless, F. fusca continues to be the dominant thrips species in the Vidalia onion winter growing region of Georgia averaging 78% of the adult thrips population from 2004 to 2013.

Significant damage to onions by thrips can range from 30% (Rueda et al. 2007), 35-43% (Fournier et al. 1995), to 60% yield loss (Waiganjo et al. 2008). Action and/or economic threshold calculations have been based on dollar yield response (Fournier et al. 1995) and onion leaf damage estimates (Nault & Shelton 2010). These thrips control action thresholds do not take into account the potential impact of Iris yellow spot virus (IYSV) transmission by thrips, which can significantly reduce yields of jumbo and colossal sizes of onion (Kritzman et al. 2001;Gent et al. 2004). Most thresholds are based on thrips per onion leaf (Fournier et al. 1995, Rueda et al. 2007, Nault & Shelton 2010. However, since most damage by thrips occurs at the beginning of the bulb formation stage (Kendall & Capinera 1987), which occurs during the 8-12 leaf stage (Schwartz & Cramer 2011), a simple estimate of an action threshold for thrips per plant during this critical onion development stage would be the thrips per leaf level of 0.9 (Fournier et al. 1995) multiplied by 8 to 12 = 7 to 11 thrips per plant. In Georgia's Vidalia onion production area, insecticide applications are recommended at an action threshold of 5 thrips per plant (Sparks & Riley 2008) as a slightly more conservative level.
During the last decade, greater numbers of T. tabaci have been found in the Vidalia onion region, presumably due to T. tabaci-contaminated onion bulbs imported from Peru to the Vidalia region beginning in 2003 . Sweet onions are grown in Peru during the spring and summer months and shipped to Georgia so that Vidalia onion processing/packing sheds can remain active in the fall of the year, after the Vidalia onion storage crop is exhausted. In 2004, the composition of thrips species from a major onion cull pile was compared to the composition of thrips species collected from surrounding commercial fields in the subsequent onion growing season to test this assertion. Subsequently, thrips competition studies were conducted in a laboratory bioassay in 2004 to determine if the Peruvian T. tabaci would reproduce at a greater rate on onion plants than F. fusca at 25 °C in single species populations or when multiple species are combined on the same onion plant. The hypothesis was that T. tabaci would out-compete F. fusca on onion. Based on the preliminary result reported in this paper, we hypothesized that the proportion of T. tabaci relative to F. fusca should increase in the Vidalia region. A 10-year survey was conducted to monitor the proportion of T. tabaci to other thrips species across multiple commercial fields within the Vidalia production region. Correlation analysis was conducted to determine if annual winter temperatures varied the same way as the proportion of thrips species.

Thrips Competition Study
Onion transplants (cultivar 'Savannah Sweet') of "pencil" thickness and at a 3-5 leaf stage free of thrips based on visual inspection were planted into soil media (Sunshine Mix, Sun Gro Horticulture, Bellevue, Washington) in a 1 quart (0.946 L) styrofoam cup and sprayed to run-off with 1% Safer® Soap solution. After 24 h on 8 Apr, 2004, thrips were placed on the plant with a fine paint brush, and a quart-cup plastic exclusion cage covered with a fine nylon screen top vent was placed over the styrofoam cup. The edge between the cups was sealed with a sticky clay strip (yellow Handitak, Pacer Technology, Cucamonga, California). All thrips were reared on onion plants in an established colony before collection, and both the T. tabaci colony and F. fusca colony were > 90% female at the time of the test. The treatments were: 1) ten T. tabaci pupae, 2) ten F. fusca pupae, and 3) ten F. fusca pupae + ten T. tabaci pupae. These were pupal stages so that the individuals would eclose as adults at approximately the same time. There were 4 replications, and the experiment was repeated twice. All of the cups were place into a Percival Growth Chamber, 2 replicates per each shelf, and the temperature was set to 27.5 °C and 12:12 h L:D. The cages were maintained undisturbed for 1 week, and then the top cup was removed. The entire plant and cup was inspected for adults (presumably from the introduced pupae) and any newly hatched immature thrips that might be present. All adult thrips were removed and placed into 70% ethanol in 7-mL vials with treatment and date labels. Only immature thrips were counted. The cages were sealed leaving immature thrips for another 2 weeks, and the above procedure was repeated. The above procedure was repeated 2 more times 1 week apart, and in the final inspection all thrips adults and larvae were counted and collected into 70% ethanol. All adult thrips were identified to species using identification keys (Oetting et al. 1993;Stannard 1968) at 70-140X magnification by a SZH10 Olympus® (Olympus America, Lake Success, New York) stereomicroscope. Analysis of variance and LSD tests for separation of treatment means (SAS Institute 1990) were performed by sample date and the means were summed over all dates. The com-petition experiments were combined because of similar treatment effects and PROC ANOVA was conducted over all 8 replicates.
Onion Cull Pile Survey Sprouted bulbs at a large cull pile of Peruvian onions near a major onion processing plant in Tattnall county were monitored for thrips species composition during the fall 2003 to spring 2004 season on 16 Dec, 3 Feb, 10 Mar, 7 Apr. Eight commercial onion production fields were sampled within Toombs and Tattnall counties from approximately 5 to 50 miles (8 to 80 km) from the cull pile site on 3 and 17 Mar and 7 Apr. At each site, on each sample date, plants were visually examined for thrips. Plants were randomly selected, and sampling was conducted for approximately 30 min in each field on each date (one person sampling for 30 min, or 2 sampling for 15 min). Thrips were aspirated off the plants and placed into alcohol. All thrips collected were examined to determine developmental stage (adult or immature) and species. The majority of thrips collected were adults, and only the adult data are presented. Adult thrips were examined under a dissecting scope for preliminary species identification. Subsamples were mounted on slides and examined under a compound microscope for species verification. A t test was used to describe the variation in percent T. tabaci of all adult thrips collected between cull pile and onion production field sites.

Commercial Onion Survey
Onion production fields were sampled within Toombs and Tattnall counties from spring 2004 through spring 2013 exactly as described by Sparks et al. (2011). The data for percent T. tabaci across all location was from the Sparks et al. (2011) study plus sample years 2011-2013. In each year, fields selected were scattered throughout these 2 counties. In 2004, 8 fields were sampled, with 4 in each county, with data from 3 dates (3 and 17 Mar, 7 Apr). In 2005, ten commercial fields were sampled, with 5 fields in each county, over 5 dates (11 and 22 Feb,14 Mar,4 and 27 Apr). In 2006, 9 fields were sampled, with 4 in Toombs County and 5 in Tattnall County. These fields were sampled 5 times (19 Jan, 7 and 27 Feb, 16 and 28 Mar). In 2007, eleven fields were sampled on 13 Mar. Based on the results from these fields, additional sampling of 18 fields from 2 through 10 Apr was conducted to further document an increase in T. tabaci. In 2008, 16 fields were sampled between 8 and 11 Apr. In 2009, 14 fields were sampled on 25 Mar. In 2010, 18 fields were sampled on 6 May. In 2011, 15 fields were sampled on 11 Apr. In 2012, 10 fields were sampled on 8 Mar, and in 2013, 23 fields were sampled between 13 Mar and 24 Apr. Percent T. tabaci and F. fusca per year was calculated based on adult thrips counts.
In each field on each sample date, plants were visually observed for thrips, and adults were aspirated into vials of 70% ethanol. Each field was sampled for 30 min when populations were low to moderate. If thrips populations were high and adequate numbers of adults were collected, sample time was reduced. All thrips were transported to the laboratory for identification. Thrips were preliminarily identified and counted under a dissecting microscope. Subsamples of each species were slide mounted for verification. Voucher specimens were sent to the University of Georgia-Museum of Natural History. While multiple species were collected during this monitoring program, only the common pest species, F. fusca and T. tabaci, were included in this report. These 2 species, F. fusca and T. tabaci, represented over 95% of all thrips collected each year.
Weather data, including the daily maximum and minimum temperatures and precipitation from Nov 1 to May 1 of each annual, oniongrowing season from transplant to harvest, were obtained from the Georgia Automated Weather Station at Vidalia, Toombs County, Georgia (http://www.griffin.uga.edu/aemn/cgi-bin/AEMN. pl?site=GAVI&report=hi accessed Nov 25, 2013). The average temperature calculated as the (daily high + daily low)/2 and total rainfall values from Nov 1 to May 1 for the years 2003-2013 were correlated with annual percentages of thrips species to see if temperature and/or rainfall during the growing season were related to the annual percentage of a given thrips species over years (n = 10) using PROC CORR (SAS Institute 1990).

Thrips Competition Study
Thrips tabaci and F. fusca reproduced similarly on onions based on numbers of larvae produced by each species (Table 1). Thrips tabaci produced 22% more adults overall. When combined (ten F. fusca pupae + ten T. tabaci pupae per plant), F. fusca produced significantly fewer adults than when F. fusca alone was present on the plant, whereas T. tabaci had no significant reduction in adults at date or overall (Table 1). There was a significant reduction in the overall number of nymphs (F = 6.73, df = 2, 14, P < 0.01, Table 1) on the plants where the 2 species were combined. This suggests that mortality of immature thrips was elevated when thrips species were combined possibly due to some direct competition. Given that the number of T. tabaci adults was unaffected after one generation and the number of F. fusca adults was significantly reduced in the combined treatment, the most likely scenario was that T.
tabaci interfered with the development of immature stages of F. fusca.

Commercial Onion Survey
The average thrips species composition in the multi-site, 10-year survey of commercial onion production fields was 78% tobacco thrips, F. fusca,  based on adult counts over all locations and years (Fig. 2). The flower thrips, F. occidentalis Pergande and F. tritici (Fitch), represented less than 2% over this 10-year survey. Thrips tabaci represented 20% of the adult thrips population (Fig. 2). This was a change from the less than 1% T. tabaci reported for onions in Georgia from 1998 to 2001 (Riley & Batal 1997, 1998Riley 2000, who also reported F. fusca as the dominant species, averaging 62% of the adult thrips population over the 4 years, followed by F. occidentalis 28% and F. tritici 10%. These reports were from Tift County which is south of the main Vidalia onion production region in Toombs and Tattnall Counties. During the first 3 years of this survey, the proportion of T. tabaci tended to decline, but in 2007 the population suddenly exceeded 50% of the adults collected (Fig. 2). The percentage of T. tabaci again declined from 2008 to 2011 and then again in 2012 spiked up to 64% of the adult thrips collected. This last increase coincided with one of the warmest years on record for Georgia, which suggested that temperature could be a factor in the relative proportion of thrips species in onion. The percentage of T. tabaci was positively correlated (r = 0.811, P < 0.01, n = 10) with the seasonal average temperature in the Vidalia onion growing region from 2004 to 2013. Conversely, the percentage of F. fusca was negatively correlated with the seasonal average temperature (r = -0.807, P < 0.01, n = 10). Over this same period, F. fusca was positively correlated with total adult thrips (r = 0.933, P < 0.001, n = 10), but T. tabaci was not (r = 0.090, P = 0.80, n = 10) suggesting that the peaks of T. tabaci were less indicative of overall thrips populations on onions in this specific winter production zone.
The results of this study indicate an obvious change in the pest thrips species complex over time, likely related to differences in temperature. In the 10 years of this study, flower thrips had declined to less than 2% of the adult population in commercial onion fields (compared to the previously reported 38% in 1997-2001). Thrips tabaci sporadically increased to a 2012 high of 64% (averaging 20% from 2004-2013), and F. fusca, the tobacco thrips, remained the dominant species for most years (averaging 78% from 2004-2013).
Several other factors likely contributed to the observed fluctuations in thrips species composition in Vidalia onion over the last decade. It is likely that a new biotype of the onion thrips established in this region . Genetic analyses of T. tabaci from the Vidalia region in recent years do not exclude Peru as a possible source of its introduction (Srinivasan et al. 2011). The competition studies conducted with the T. tabaci collected from Peruvian onion cull piles indicate that this species has the potential to successfully compete with the F. fusca under warm conditions (25 °C). However, F. fusca seems to be favored by cool temperatures, as indicated by the negative correlation with winter temperatures in this study, which is characteristic of the Vida- lia onion growing season between Nov and May each year. Insecticide resistance may have also played a role in the population shift. Lack of efficacy of organophosphate insecticides against the F. fusca and F. occidentalis in Georgia detected in the early 2000s  resulted in a shift in insecticide use toward pyrethroid insecticides. Onion thrips is well known for pyrethroid resistance in much of its range (Martin et al. 2003;MacIntyre-Allen et al. 2005;Shelton et al. 2006), and field trials conducted in the Vidalia region in 2007 verified poor performance against the onion thrips and continued good efficacy against tobacco thrips (Sparks 2008). Concerns over the potential impact of IYSV led to increased reliance on insecticides for control of the thrips vector in 2006 and 2007 (Sparks, personal observation). Thus, the increased use of pyrethroid insecticides in the region may be partially responsible for the observed shift. In 2008, a decline in pyrethroid efficacy against tobacco thrips was noted in field trials (Sparks unpublished data). This, in combination with reduced use of insecticides, may have removed part of the competitive advantage of the onion thrips and contributed to the shift back towards historical pest complex composition. Even so, the positive correlations with temperature suggest that T. tabaci may be favored in warmer years.