Development and Impact of the Spotted Wing Drosophila, Drosophila suzukii, in Florida Strawberries

Abstract

Drosophila suzukii (Diptera: Drosophilidae), an Asian pest of strawberries and other thin-skinned fruit, was first detected in the Americas in California in the fall of 2008, and its first discovery in Florida came on 4 August 2009 in Hillsborough Co. Although D. suzukii is now found throughout much of Florida, no commercially damaging larval infestations have been reported in fresh market strawberries. Although other drosophilids were present in surveys, only Drosophila melanogaster appears to be a formidable competitor for D. suzukii in strawberries and may prevent or even conceal economic damage in strawberries held for processing.

Keywords:

• Diptera
• Drosophilidae
• invasion
• non-native
• monitoring
• trapping
• Zaprionus indianus
• Drosophila melanogaster

INTRODUCTION

Strawberries, mostly for the fresh market, were produced in Florida on 3,601 ha (National Agric. Statistics Service, 2010a) and valued at about $362 million during 2010 (National Agric. Statistics Service, 2010b). There are numerous arthropod pests that affect strawberries in Florida, principally spider mites, thrips, sap beetles, aphids, and some moth larvae. The arrival of a new Asian fruit pest, Drosophila suzukii, in California in 2008 (Bolda, 2008) caused concern for its possible introduction and establishment in Florida. Various hosts of this pest are present in Florida, including commercially important strawberries, blueberries, and to a limited extent blackberries, and wine grapes. Female D. suzukii can attack undamaged fruit (Cline, 2009) unlike the relatively minor, long-resident (Keller, 2007) pest, D. melanogaster, that lays its eggs only in previously opened wounds (Price et al., 2006).

In anticipation of an introduction into Florida, aids for identification of adult male D. suzukii were distributed to each of the state and federal Cooperative Fruit Fly Detection Offices with requests for inspection personnel to look for D. suzukii.

On 4 August 2009, the first adult D. suzukii found in Florida were confirmed to be in Hillsborough Co. A pest alert was issued by the Florida Department of Agriculture and Consumer Services Division of Plant Industry (FDACS/DPI) (Steck et al., 2009). Suspect larvae also had been submitted by a homeowner for identification earlier in July from purchased fresh cherry fruit that originated from California; a definitive identification as D. suzukii could not be confirmed.

It is almost certain that this fly was not present in Florida prior to May 2007 and most likely not present before the summer of 2009. Between April 2006 and June 2007, a biodiversity survey comprising weekly servicing of 100 McPhail traps positioned on north–south transects throughout Florida was conducted by both state and federal fruit fly detection personnel. The entire preserved contents from these trap samples were examined for the presence of D. suzukii, and there were none present in any of the 5,200 collections. Additionally, the sequentially more distant detections of D. suzukii throughout peninsular Florida since the initial detection on 4 August 2009 (Dean, unpublished data), seem to fit a pattern of a newly expanding invasive population.

The original detections occurred in the routine servicing of adult tephritid fruit fly Multilure detection traps (Better World Manufacturing, Fresno, CA, USA) baited with BioLure synthetic lures containing ammonium acetate, putrescine, and trimethylamine (Suterra Inc., Bend, OR, USA). These traps, which were serviced biweekly, were located in a wild Prunus caroliniana in a high risk, high trap density area under a preventive sterile Mediterranean fruit fly release program.

Following the first discoveries in Hillsborough Co., fruit fly detection personnel placed supplemental McPhail traps at locations in the vicinity of the two initial discoveries and at two nearby open air fruit markets. These fruit fly traps were serviced weekly and baited with known Drosophila spp. attractants torula yeast, sugar, and banana. These supplemental fruit fly traps caught two additional female D. suzukii, one adjacent to the original detection sites and one at the nearby open air fruit market.

New D. suzukii captures continued to occur in the routine fruit fly detection program traps and survey traps. As additional specimens were detected in the area, tests were conducted to select a cleaner, easier to service, and more specific trap for detecting D. suzukii. Meanwhile, Geographic Information Systems (GIS)-enabled map updates of new D. suzukii discoveries were made available through FDACS/DPI and production-oriented educational materials and training programs were made available to stakeholders by the University of Florida Institute of Food and Agricultural Science (Price and Nagle, 2010).

MATERIALS AND METHODS

Adult Fly Survey Near Commercial Strawberry Farms

Because new detections of D. suzukii continued to occur within the strawberry production areas of Hillsborough Co., additional Drosophila specific traps baited with torula yeast and sugar were established to monitor the population dynamics of adult D. suzukii weekly in strawberries. These traps were designed and serviced by FDACS/DPI personnel and are described by Price and Nagle (2010). They were established as fixed traps in seven locations in the strawberry production areas selected for an abundance of multiple hosts in order to increase the probability of detecting D. suzukii throughout the season.

Adult Fly Survey at University of Florida, Gulf Coast Research and Education Center (GCREC)

In addition to FDACS/DPI weekly trap checking near commercial strawberry fields, GCREC personnel conducted weekly sweep net sampling for adult D. suzukii around discarded produce at the strawberry, vegetable, and ornamentals research site in Balm from August until December 2009, when Drosophila spp. traps (Price and Nagle, 2010) baited with torula yeast and sugar were placed as fixed traps near blueberry plots and strawberry plots. Weekly sampling of these adult traps has continued without interruption.

Survey of Adult Flies Reared from Fruit Collected at Commercial Farms

During the harvest season, fruit sampling from commercial strawberry farms was initiated at six locations selected for proximity to positive adult D. suzukii trap sites in the Hillsborough Co., Plant City production area. Within-field sampling locations were selected randomly, and samples included field edges and centers. Fruit were specifically selected for full ripeness and for possible fruit fly damage to increase the probability that D. suzukii infested fruit would be discovered. Six to 12 fruit from the appropriate category were sampled weekly from each field for 14 weeks (14 December 2009 until 22 March 2010), when most strawberry plants were destroyed. Sampled fruit were taken to the Fruit Fly Identification Laboratory, FDACS/DPI, in Palmetto where they were separated into groups of three to four fruits and held at room temperature (∼24°C) in 266 ml plastic cups containing a 2-cm layer of coarse Vermiculite^® (Verlite Co., Tampa, FL, USA). Cups were sealed inside clear 4-mil, 15 × 23-mm zip-sealed bags that had been perforated with ca. 50 pin holes to reduce condensation. The containers were held until any immature D. suzukii within the fruit developed to adults so that accurate identification could be performed.

RESULTS

Adult Fly Survey Near Commercial Strawberry Farms

Population dynamics of adult D. suzukii near commercial strawberry farms were characterized by wide fluctuations through the season (Fig. 1). The deep decline in average recovery of flies from the high of 6.2 flies per trap (Fig. 1, arrow A) coincided with a record 13 nights of sub-freezing weather that occurred in late December 2009 and early January 2010. However, warmer days that followed allowed a resurgence of the flies trapped by the end of January (Fig. 1, arrow B). High levels of D. suzukii captures occurred also in the summer, but they were not associated with strawberry production (Dean, unpublished data).

FIGURE 1 Average number of D. suzukii flies captured near selected strawberry fields weekly in traps (dotted line) and numbers of D. suzukii flies reared from strawberry fruit taken from row middles (solid line) and reared from strawberry fruit taken directly from plants (dash line). Arrow A at dotted line indicates the period of 13 continuous days of weather during which freezes occurred daily and few D. suzukii flies were trapped. Arrow B at dotted line indicates the warming period that followed when more D. suzukii flies were trapped. Arrow C at solid line indicates the period of increased rearing D. suzukii flies form cull fruit taken from row middles. Arrow D at the dash line indicates the initial occurrences of rearing D. suzukii flies from sound fruit taken from plants. Eastern Hillsborough Co., Fla. (color figure available online).

Adult Fly Survey at University of Florida, Gulf Coast Research and Education Center (GCREC)

No D. suzukii males were detected by sweep net sampling during the period from August to 14 December 2009. The most abundant drosophilids collected by this method during the sampling period were the recently introduced Zaprionus indianus (Steck, 2005) followed in abundance by D. melanogaster; the latter species predominated near the end of the sampling period.

Population fluctuations of D. suzukii at GCREC, as monitored by baited adult traps, are presented in Figure 2. Traps did not capture any D. suzukii males at the GCREC site during the strawberry fruiting period of December 2009 through mid-April 2010 and during the subsequent blueberry fruiting period April 2010. The first adult males were detected the last week of July 2010 and the latest were detected the last week of September 2010 (Fig. 2). D. melanogaster, however, were collected in numbers >100 during most weeks. During March through mid-April 2010, when some experimental strawberry plots had been abandoned in the field, it was common to discover up to about 9,000 D. melanogaster flies per trap.

FIGURE 2 Average number of male D. suzukii flies captured weekly in two traps at University of Florida GCREC, eastern Hillsborough Co., Florida (color figure available online).

Survey of Adult Flies Reared from Fruit Collected at Commercial Farms

There was no detectable damage to fruit attached to plants in any of the fields sampled during early harvest December 2009 through mid-February 2010. Therefore, initially only culls collected from row middles were available for sampling. As the season progressed, both culls from row middles and suspect fruit harvested directly from the plants were sampled. Once D. suzukii were first discovered in fruit taken directly from plants the first week of March (Fig. 1, arrow D), collections of cull fruit from row middles ceased and only suspect fruit taken directly from the plant were sampled. No flies were reared from strawberry fruit until the end of January, when the first D. suzukii and the first D. melanogaster were collected from cull fruits taken from row middles. Numbers of D. suzukii reared from cull fruit taken from row middles continued to increase through the second week of February (Fig. 1, arrow C) when sampling from row middles ceased. By the second week of April, no more strawberries remained to be sampled.

The ratio of D. suzukii to D. melanogaster over the entire sampling period was about 1 to 100 and all six sites yielded D. melanogaster, while only about one-third of those sites yielded D. suzukii (Table 1). There was a much greater number of both Drosophila species from cull fruit taken from row middles than from damaged fruit harvested from plants (Table 1).

TABLE 1 Number of Drosophila spp. Flies Reared from Strawberry Fruit Discarded to Row Middles and from Fruit Harvested Directly from Plants^z

	From fruit discarded to row middles		From damaged fruit taken from plants		Total from all fruit			Percent of total
	D. suzukii	D. melanogaster	D. suzukii	D. melanogaster	D. suzukii	D. melanogaster	Total flies	D. suzukii	D. melanogaster
Total flies reared from fruit	25.0	1,900.0	18.0	2,815.0	43.0	4,715.0	4,758.0	0.9	99.1
Avg/sample	0.6	43.2	0.6	90.8	0.8	85.7	86.5
SD/sample	1.8	110.1	2.4	241.7	2.3	233.8	234.8
No. samples taken	44.0	44.0	31.0	31.0	55.0	55.0	55.0
No. positive samples detected	6.0	18.0	3.0	8.0	9.0	26.0	35.0
Percent positive samples	13.6	40.9	9.7	25.8	16.4	47.3	63.6
No. sites sampled	6.0	6.0	6.0	6.0	6.0	6.0	6.0
No. positive sites sampled	2.0	6.0	1.0	4.0	3.0	6.0	9.0
Percent positive sites	33.3	100.0	16.7	66.7	50.0	100.0
^zData are from six to 12 fruit per sample, eastern Hillsborough Co., Florida.

DISCUSSION

D. suzukii has become established within the major strawberry production area of Florida and is known to infest strawberry fruits attached to plants and to infest the culls dropped in row middles. However, during the first strawberry harvest period after D. suzukii established in the strawberry production area (2009–2010), negligibly low infestations occurred and no economic damage was found. Again, during the following strawberry harvest period (2010–2011), the fly did not cause economic loss through this writing, 8 February 2011. Unlike the economic impact that D. suzukii caused on the west coast USA (Cline, 2009), D. suzukii remains only a modest nuisance in Florida strawberry crops. None-the-less, the ecology of this pest merits study in greater detail to understand any factors that could facilitate future outbreaks and threaten strawberry and other small fruit industries of Florida.

As with any newly introduced species, D. suzukii must compete with established organisms that may require some of the same resources. In this case, D. suzukii encountered a very successful, established competitor on strawberries, D. melanogaster, given the disproportionate numbers of the latter found both in fruit samples and trap samples. Through rearing D. suzukii from various host fruits and establishing a research colony on an artificial medium, it has been seen that D. melanogaster out-competes D. suzukii for the same resources under these laboratory conditions (Dean, unpublished data). More rigorous studies should be conducted; however, we speculate in those instances where D. suzukii successfully initially damaged the strawberry fruit by oviposition, D. melanogaster rapidly exploited the oviposition wound and displaced D. suzukii. Certainly, when rearing D. suzukii adults from field strawberries infested with both drosophilids, it was often found that the few adult D. suzukii to emerge had died quickly, while multiple very active D. melanogaster adults survived (Dean, unpublished data). Perhaps this dominance of D. melanogaster may reduce damage by D. suzukii or maybe its dominance will conceal earlier damage produced by D. suzukii.

Acknowledgments

We are very grateful for the contributions to this study by Kathleen Miller USDA/APHIS/PPQ who first detected D. suzukii in Florida and the personnel from the Hillsborough Co. Fruit Fly Detection Offices of Howard Wallace FDACS/DPI and Andre McCarroll USDA/APHIS/PPQ who helped with supplemental trapping. Also our thanks go to Donald Cones and Timothy Mader for performing weekly surveying, rearing, and counting Drosophila spp., Renae Snyder and Arnold Bailey for GIS and map support, and Alicia Whidden of the Hillsborough Co. Cooperative Extension Office for providing contacts with strawberry producers and industry information. University of Florida contributions to this study were funded by the Florida Strawberry Growers Association.