oriental fruit fly eradication · nvasive insect pests and the pathogens they vector are a chronic...

108 American Entomologist • Summer 2019

Invasive insect pests and the pathogens they vector are a chronic concern for human, animal, and plant health worldwide. For the agricultural community, fruit

flies (Diptera: Tephritidae) are among the top threats. Many regulatory agencies monitor fruit fly incursions using various survey activities and protocols and com-monly undertake expensive eradication programs using approved phytosanitary measures to eliminate them when they occur (FAO 2010). Numerous incursions and ensuing eradication efforts worldwide have been summa-rized in the Global Eradication and Response Database (GERDA; Kean et al. 2018), which includes reports of 1,025 eradication programs in 107 countries against terrestrial arthropod pests and plant pathogens. They recorded 259 eradication programs directed against tephritids, with

117 directed against the Mediterranean fruit fly, Cerati-tis capitata (Wiedemann) and 126 directed against eight species of Bactrocera/Zeugodacus. Of the 55 eradication programs directed against the oriental fruit fly, Bactroc-era dorsalis (Hendel), including its synonyms Bactrocera invadens Drew, Tsuruta & White, Bactrocera papayae Drew & Hancock, and Bactrocera philippinensis Drew & Hancock (Schutze et al. 2015a, 2015b; Fig. 1), 40 were declared successful. Carey et al. (2017) noted that GERDA accepted a regulatory definition of eradication: apparent local extirpation of a species based on its absence under surveillance for at least three times the normal gener-ation time. This may or may not equate to a complete extirpation over a broader area. As eradication programs have become routine in many areas and for many pests, the scientific and programmatic details that might help distinguish between successful outcomes and eradica-tion failures are published infrequently in the scientific literature or in public outlets.

The United States Department of Agriculture safeguards U.S. agriculture through the efforts of the Animal and Plant Health Inspection Service, Plant Protection and Quarantine (USDA-APHIS-PPQ) program, working in partnership with regions of the U.S. that are susceptible to invasive fruit flies (especially Florida, California, and Texas) to develop surveillance programs designed for those regions (IPRFFSP 2006). The protocols for these programs include maintaining a network of detection traps, initiating delimitation surveys to determine numbers and spread of the invasive pest upon initial fly capture, and, if additional flies are captured, initiating eradica-tion programs to prevent establishment (IAEA 2003). In

Oriental Fruit Fly Eradication

in Florida 2015–2016Program Implementation, Unique Aspects,

and Lessons LearnedGARY J. STECK, ABBIE J. FOX, DANIEL CARRILLO, DAVID DEAN, AMY

RODA, NANCY D. EPSKY, AND TREVOR R. SMITH

Fig. 1. Oriental fruit fly female.

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niversity of Florida user on 28 June 2019

American Entomologist • Volume 65, Number 2 109

Florida, the Florida Department of Agriculture and Con-sumer Services, Division of Plant Industry (FDACS-DPI) partners with USDA-APHIS-PPQ to oversee the fruit fly program in accordance with state and federal trapping guidelines (USDA 2015). Regulatory personnel work with research and university extension personnel as needed for these programs.

Florida has a long history of invasive fruit fly detections, delimitations, and eradication programs that began with the first appearance of C. capitata in the continental U.S. in 1929, which led to the first successful large-scale erad-ication of a tephritid fruit fly population in history (Clark et al. 1996). Of the 21 fruit fly eradication programs con-ducted in Florida before 2015, 16 were directed against C. capitata, four were conducted against B. dorsalis, and one was the successful eradication of Anastrepha obliqua

(Macquart) in 1936 (Steck 2001). The first detection of B. dorsalis in Florida was in 1964 (Clark et al. 1996; Table 1). From 1964 to 2014, B. dorsalis incursions were detected another 15 times in 10 different counties. Most detections were of one to three males, with the single exception of detection of 12 males and four females in 1999 in Tampa. Similarly, B. correcta (Bezzi), B. carambolae (Drew and Hancock), and B. zonata (Saunders) have been detect-ed in Florida a collective 13 times, but they were never trapped in numbers sufficient to trigger an eradication program (Table 1). In contrast, 2,266 male and 1,558 female B. dorsalis were detected in California from 1960 to 2012, with 1,558 detection events in 244 cities (Papadopoulos et al. 2013). Thus, Florida has been relatively free from B. dorsalis invasion, with most incursions known from the detection of only a single fly. However, this changed

Fig. 2. Fruit fly detection trapping array in Florida. Trap densities based on risk criteria 1, 2, 3 (high, medium, and low, respectively).

ALACHUA

BAKERBAY

BRADFORD

BREVARD

BROWARD

CALHOUN

CHARLOTTE

CITRUS

CLAY

COLLIER

COLUMBIA

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DIXIE

DUVAL

ESCAMBIA

FLAGLER

FRANKLIN

GADSDEN

GILCHRIST

GLADES

GULF

HAMILTON

HARDEE

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HIGHLANDS

HILLSBOROUGH

HOLMES

INDIANRIVER

JACKSON

JEFFERSON

LAFAYETTE

LAKE

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LIBERTY

MADISON

MANATEE

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MARTIN

MIAMI-DADEMONROE

NASSAUOKALOOSA

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ORANGE

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PINELLAS

POLK

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SARASOTA

SEMINOLE

ST. JOHNS

ST. LUCIE

SUMTER

SUWANNEE

TAYLOR UNION

VOLUSIA

WAKULLA

WALTON WASHINGTON

United States Department of Agriculture

ÜThese data, and all the information contained therein, have been collected by the U.S. Department of Agriculture'sAnimal and Plant Health Inspection Service (APHIS), or by its cooperators on APHIS’ behalf, for restricted governmentpurposes only and is the sole property of APHIS. Data may be disseminated on a need-to-know basis only andmust be used for their intended government purpose(s). All information contained within these data are subject torequired Federal safeguards and shall only be shared and/or used consistent with the Trade Secrets Act [18 U.S.C.1905], the Privacy Act of 1974, as amended [5 U.S.C. 552a], the Freedom of Information Act [5 U.S.C. 552], theconfidentiality provisions of the Food Security Act of 1985 [7 U.S.C. 2276], Section 1619 of the Food, Conservation,and Energy Act of 2008 [7 U.S.C. 8791], and other applicable Federal laws and implementing regulations, as well aswith the confidentiality or non-disclosure provisions of any other agreement entered into between APHIS and a cooperator.

USDA-APHIS-PPQ Gainesville, FL 32606 Author: Courtney HartMap Projection: GCS North American 1983 HARNDocument Path: H:\Work\GIS\FFED\TrappedSections_120116.mxd

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Date Created: 3/14/2017 Data Source: eTRAP

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MIAMI-DADE

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MiamiEvergladesNational

ParkPalmetto Bay

Oriental fruit fly detections 2015

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in the summer of 2015, when B. dorsalis was found in southern Florida in Miami-Dade County.

The event began with the detection of a single male B. dorsalis in Palmetto Bay, a residential area in Miami-Dade County, on 17 August 2015 (Fig. 2 inset). This detection appeared no different from previous Florida detections of a single male in a trap; however, it was a harbinger of what was to follow. After discovery of another single male in a trap west of the initial detection, there was an alarming discovery of 45 male B. dorsalis in a trap (Fig. 3) located near the second fly detection. This was unprecedented in Florida; the number of flies in this single trap exceeded the sum of all previous detections in the state. To make matters worse, this location was deep in the Redland agricultural area of Miami-Dade County, the heartland of tropical fruit production in southern Florida. The detec-tion of larvae in mango, Mangifera indica L., at the same site on 28 August 2015 confirmed a breeding population. This location was designated the apparent outbreak epi-center, and program activities changed from delimitation surveys to establishment of a large quarantine area and initiation of an eradication program.

In this paper, we describe the major eradication pro-gram conducted successfully against B. dorsalis in Flor-ida during 2015–2016. In addition to describing the stan-dard detection systems that are in place continuously, we describe the delimitation surveys triggered by initial detection of an invasive fruit fly and the eradication and quarantine activities started when threshold population indicators were met. Additionally, we provide insight into new approaches and methods employed, as well as les-sons learned that will be useful should it be necessary to implement similar programs in the future.

Fruit Fly Detection TrappingMuch of peninsular Florida is monitored year-round with an array of traps: the invasive fruit fly detection system. Approximately 56,000 traps are deployed over ≈20,720 km2 (≈8,000 square miles) and serviced throughout the year (Fig. 2). Jackson traps (Harris et al. 1971) are baited with male-targeted parapheromone lures (Cunningham 1989a). Glass McPhail traps (Steyskal 1977) and plastic McPhail-type traps (“Multilure”; IAEA 2003) are baited with female-biased protein-based torula yeast (McP/TYB) or a three-component (3C) lure comprised of putrescine, ammonia acetate, and trimethylamine (ML/3C), respec-tively. Jackson traps baited with methyl eugenol (JT/ME) are used to detect male B. dorsalis (Steiner 1952) and other ME-responding Bactrocera species. The types of traps and their densities and frequency of inspection are based on criteria of perceived risk of introduction. High-risk areas (Criterion 1) surround ports of entry (i.e., immediate vicinity of air- and seaports); moderate-risk areas (Criterion 2) correspond to urban areas; and low-risk areas (Criterion 3) correspond to rural residential and crop production areas (Fig. 2). The detection of one male or a non-gravid female triggers a delimitation survey to determine the extent of the incursion. Core and buffer areas are designated and trap densities are increased over baseline levels according to the species-specific action plan. The detection of two or more nearby males or the discovery of gravid females or immature stages indicate a breeding population. This triggers an eradication pro-gram to prevent establishment of the species. Detailed national guidelines regarding fruit fly traps, trap densi-ties, triggers, and time requirements are followed (USDA 2015, USDA 2016b, Suppl. file).

Fig. 3. Forty-five male oriental fruit flies on Jackson trap in Redland.

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Table 1. History of Bactrocera spp. detections in Florida through 2018, including costs and durations and information on delimitation surveys and eradication programs triggered by those detections.

Year Species City County Males Females Larvae ≈ CostDuration (months)

1964 dorsalis St. Petersburg Pinellas 1 0 0 $20,000 2

1969 dorsalis Miami Miami-Dade 1 0 0 $33,000 3

1994 dorsalis Ft. Lauderdale Broward 1 0 0 $100,000 4

1995 dorsalis St. Petersburg Pinellas 3 0 0 $530,000 3*

1999 dorsalis Tampa Hillsborough 12 4 0 $100,000 3*

1999 dorsalis Deltona Volusia 1 0 0 N/A 3

1999 correcta Titusville Brevard 2 0 0 N/A 3

2000 dorsalis Bradenton Manatee 1 0 0 N/A 3

2001 correcta Apopka Orange 1 0 0 N/A 3

2001 correcta Oviedo Seminole 1 0 0 N/A 3

2001 dorsalis Kissimmee Osceola 1 0 0 N/A 3

2001 dorsalis Sarasota Sarasota 2 0 0 $100,000 3*

2002 correcta Homestead Miami-Dade 1 0 0 N/A 3

2002 correcta Pinellas Park Pinellas 3 0 0 N/A 3

2002 correcta Miami Miami-Dade 1 0 0 N/A 3

2002 correcta Apopka Orange 1 0 0 N/A 3

2002 dorsalis Orlando Orange 2 0 0 N/A 3

2002 dorsalis Pompano Beach Broward 1 0 0 N/A 3

2007 dorsalis Valrico Hillsborough 1 0 0 N/A 3



2008 correcta Orlando Orange 1 0 0 N/A 3

2008 carambolae Orlando Orange 2 0 0 N/A 3

2010 dorsalis Safety Harbor Pinellas 2 0 0 N/A 3

2010 zonata Miami Miami-Dade 1 0 0 N/A 5

2011 correcta Windermere Orange 1 0 0 N/A 4

2013 correcta Sarasota Sarasota 1 0 0 N/A 4

2014 dorsalis Plantation Broward 1 0 0 N/A 2

2015 correcta Boynton Beach Palm Beach 2 0 0 N/A 3

2015 dorsalis Palmetto Bay, Redland, Miami

Miami-Dade 140 18 8 $3,500,000 6*

2016 dorsalis St. Petersburg Pinellas 1 0 0 N/A 2

2017 dorsalis Mt. Dora Lake 1 0 0 N/A 4

2017 dorsalis Clearwater Pinellas 1 0 0 N/A 3

2017 dorsalis Weston Broward 1 0 0 N/A 3

2017 correcta St. Petersburg Pinellas 1 0 0 N/A 4

2018 zonata Lake Worth Palm Beach 2 0 0 N/A 2

2018 dorsalis Redland Miami-Dade 4 0 0 $625,000 4*

*Eradication campaigns

N/A = information not available

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Bactrocera dorsalis Delimitation Survey TimelineOn 17 August 2015, a male B. dorsalis was found in a detection trap (JT/ME) located in a Criterion 2 area of Miami-Dade County, specifically in the town of Palmetto Bay (Fig. 2, inset). This detection triggered the establish-ment of the first delimitation survey area, with the dis-covery site designated as the core area (Fig. 4, Table 2). The deployed trapping grid was 134.7 km2 (52 mi2), as Biscayne Bay covered the area to the southeast less than 1.6 km away from the detection site.

Nine days later, on 26 August, a single male B. dorsalis was found in a detection trap (JT/ME) in Miami-Dade County located 22.5 km west of the first find. This trap was located in the Redland agricultural area in Home-stead, a Criterion 3 area, and a second delimitation sur-vey area was initiated (Fig. 4). On the following day, we were shocked to encounter 45 males in a single JT/ME trap in a section (approximately 2.6 km2) adjoining the second core area. This second detection site in the Red-land agricultural area became a new core area with a cor-responding higher density of traps, and the surrounding delimitation survey buffer area expanded accordingly (Fig. 4, Table 2). The next day, 28 August, two live and six dead larvae were found in mango on the same property. These discoveries were immediate evidence of a breeding population, which triggered an eradication program and initiated a quarantine of the affected area.

During the next six weeks, 133 males were detected in JT/ME traps and six males and five females were detected in McP/TYB traps over five contiguous sections and one disconnected section in the Redland agricultural area (Fig. 4, Table 2). An additional 13 females were hand-caught on 10 September at a site about 300 m from the outbreak epicenter. Although a few escaped capture,

Fig. 5. Timeline of oriental fruit fly (OFF) detections and control activities. MAT=male annihilation treatment; ME=methyl eugenol.

Fig. 4. Delimitation trapping areas. Flies were detected in each of the 1-square-mile core areas. Trap densities correspond to distance from the core.

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12 of the females were netted over a 30-minute period from a loose aggregation on the undersides of banana foliage, Musa acuminata Colla. A single female was cap-tured nearby on the foliage of a longan tree, Dimocarpus longan Lour. Many of these females were gravid. The last fly detection occurred on 10 October. In total, 158 adults and eight larvae were found in the area of the eradication program (Table 2). A timeline of detections is shown in Fig. 5, and relative numbers of flies captured and their locations are shown in Fig. 6. Three weeks into the event, on 8 September, another single male B. dorsalis was found in a detection trap (JT/ME) located in Miami but outside of the two existing delimitation survey areas. This site was a Criterion 1 area located near the Miami International Airport, approximately 32.2 km northeast of the Redland agricultural area. A third delimitation survey area was established here (Fig. 4, Table 2).

No additional flies were found in the delimitation sur-veys established after the detections in Palmetto Bay and Miami, and surveys ended in October and November 2015, respectively (Table 2).

Eradication MeasuresWhen the eradication trigger was met, FDACS-DPI and USDA-APHIS-PPQ formed response teams that were mobilized and sent to the impacted area. A state and federal cooperative program was organized according to Incident Command System (ICS) using a unified com-mand structure, a standard and mandated protocol for such programs throughout the U.S. (Suppl. file).

Methyl eugenol is the key, not only to early detection of B. dorsalis, but also to its eradication. It is a powerful feeding cue that can be combined with pesticide to kill attracted flies (Steiner and Lee 1955). This approach is called male annihilation (Cunningham 1989b) and is the basis for the male annihilation technique (MAT), which is used to break the reproduction cycle of the wild flies and to eradicate the population. MAT has proven effective for eradicating B. dorsalis from islands (Steiner et al. 1965) and when used in area-wide population management (Vargas et al. 2014). The early-age-related response of B. dorsalis males to ME before sexual maturity is one of the reasons MAT has been so successful. Forty to fifty percent of all males can be eliminated from the wild population before they attain sexual maturity (Wong et al. 1989, Shelly et al. 2008). MAT consisted of applying a small amount of

a thickened spray containing ME (≈8.8 ml), naled (≈1.2 ml), and Min-U-Gel 400 (Active Minerals International, LLC, Sparks, MD) from a slow-moving vehicle to objects such as utility poles (Fig. 7) and street-side trees within a minimum 2.4 km radius around any fly detection site in the Redland agricultural area. The total MAT treatment area was 67.35 km2. Approximately 600 spot treatments were applied per 2.6 km2. MAT treatments were contin-ued weekly for one life cycle past the last detection, and were then applied every other week during the second life cycle for a total of 13 rounds of treatments. Life cycle estimates ranged from 32 to 44 days during the Septem-ber–October period.

Additional control actions were conducted within the 200 m radius around sites in which gravid females or larvae were found. Soil drench (Warrior II [a.i. lamb-da-cyhalothrin, Syngenta Crop Protection, LLC, Greens-boro, NC]) was applied under the drip-line of B. dorsalis fruit-bearing host plants on all included properties. This treatment targeted third instars and pupae in the soil and was the first time that Warrior II was used for soil drench in a regulatory quarantine program. After exten-sive research and field testing in Hawaii, Warrior II was approved as a soil drench in February 2015, replacing

Fig. 6. Quarantine and treatment areas.

Table 2. Details of the delimitation surveys during the 2015–2016 B. dorsalis outbreak in Florida. Delimitation surveys included male-targeted Jackson traps baited with methyl eugenol (JT/ME) and female-biased McPhail traps baited with the liquid protein bait torula yeast plus borax (McP/TYB).

Location Detection date Fly finds Area Trap numbers Survey end datePalmetto Bay 17 August 2015 1 male 163 km2 330 JT/ME

60 McP/TYB20 October 2015

Redland 26 August 2015 138 males18 females

8 larvae

357 km2 604 JT/ME 245 McP/TYB

12 February 2016

Miami 8 September 2015 1 male 192 km2 390 JT/ME 60 McP/TYB

12 November 2015

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diazinon, which lost U.S. EPA registration in December 2014 (Stark et al. 2014).

Foliar bait spray using a ground-based treatment with GF-120 Naturalyte (GF-120, Dow AgroSciences LLC, Indi-anapolis, IN) was applied to individual host and non-host trees and plants, targeting the underside of foliage. GF-120, a formulation of the pesticide spinosad and the food bait protein hydrolysate, is certified for use in organic production systems. Fruit flies are attracted to the protein hydrolysate and ingest it, thereby receiving a lethal dose of the pesticide. Protein hydrolysate increases the efficacy of chemical applications and reduces the area requiring treatment with pesticides for control (Prokopy et al. 1992).

All treatments were potentially compromised on sev-eral occasions by heavy rain (several inches each time) on 10, 16–17, and 24–27 September, and on 8–9 October 2015. One limitation of MAT application was that it could be applied only once every seven days per label, whereas GF-120 could be reapplied daily, if needed, according to the Special Local Need (SLN) 24 (c) label.

More than 100,000 kg of fruit from regulated B. dor-salis host species were removed from the 200 m radius areas to eliminate eggs and/or infested fruit. By volume and weight, the primary host materials removed were banana, avocado (Persea americana Mill.), and mamey sapote [Pouteria sapota (Jacq.) H. E. Moore & Stearn], all of which were collected and transported to a Miami-Dade County landfill for burial.

In addition to the ground applications, one aerial bait spray application of GF-120 was implemented by the Florida

Department of Agriculture and Consumer Services (FDACS) and Miami-Dade County at the request of the local agri-cultural community. The application occurred during the nights of 2 and 3 October 2015 to minimize exposure to non-target insects. The treatment area was 41.4 km2 of predominantly agricultural land. No applications were made over named water bodies, and there was a 91.4 m setback buffer for aquaculture farms. Extensive outreach was conducted before aerial application, and an FDACS helpline was operational throughout nights and week-ends. Eradication treatments are summarized in Table 3.

Standard eradication protocol specifies that traps should be serviced daily for seven days after the date of the last fly detection, and weekly thereafter. However, due to the value of highly diversified specialty crops and the asso-ciated risks in the area of infestation, the daily trapping period was extended to ensure earliest possible detec-tion of any remaining B. dorsalis. Therefore, traps were serviced daily for one full life cycle after the last B. dor-salis detection and weekly thereafter for a period of two additional life cycles.

A small team of entomologists was in the core areas on most days, coordinating their activities with detection and control personnel to examine likely host fruits for larval infestation. The host list for B. dorsalis includes more than 400 plant species, most of which are grown in southern Florida. In total, the entomologists cut more than 4,400 pieces of fruit, representing at least 54 differ-ent host species, to check for infestation. The potential hosts most thoroughly checked were avocado, banana,

Fig. 7. Male annihilation treatment applied to utility pole.

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carambola (Averrhoa carambola L.), various types of citrus, guava (Psidium guajava L.), mamey sapote, and papaya (Carica papaya L.). As previously noted, only a few larvae were found in mango, and no other hosts were found to be infested.

Regulatory MeasuresThe Regulatory Branch of ICS was responsible for all regulatory actions and enforcement in the 255.5 km2 quarantine area in the Redland agricultural area. The quarantine boundaries were established using a radius of 7.2 km around all fly detection sites. Any recognized B. dorsalis host plant within this area was regulated to prevent the potential spread of B. dorsalis through move-ment of infested material. There were three distinct areas within the quarantine. The first area (2.07 km2) was a 200 m radius around larval or female fly detections. No host material was allowed to be removed from this area, except by program personnel for burial at the approved landfill. The second area (9.9 km2) was outside the 200 m zone but within a 1.6 km radius around fly finds (any life stage or sex), where harvest was allowed only if a post-harvest treatment procedure was followed. The third area was the remaining 243.5 km2, where harvest was allowed if a 30-day pre-harvest treatment or a post-harvest treat-ment was applied. FDACS-DPI and USDA-APHIS-PPQ implemented and enforced compliance agreements, which prescribed specific requirements for growers, pack-inghouses, and plant nurseries in the quarantine area. These measures allowed growers and packers to move commodities out of the quarantine area for post-harvest treatments or after completing a 30-day pre-harvest bait treatment. Pre-harvest treatment for growers required the use of bait sprays of either technical-grade malathion combined with the protein bait Nulure (Miller Chemical & Fertilizer LLC, Hanover, PA) or GF-120 (Code of Federal Regulations: 7 CFR 301.32-10). The Control Branch of ICS conducted control activities in the defined 200 m radius and 1.5 mile (3.88 km) radius treatment areas around fly detections. Stakeholders were responsible for pre- and post-harvest commodity certification treatments.

The Regulatory Branch of ICS performed site visits to confirm that regulatory compliance requirements were met. They either provided growers with a limited permit, allowing them to ship their crops for approved post-harvest treatments, or they issued a temporary certificate for movement of commodities after 30-day pre-harvest treatments were verified. The magnitude of the regulatory effort was unprecedented: more than 800 nurseries, more than 800 growers, almost 800 harvesters and transporters, and 121 packinghouses were affected (Table 4). For producers who chose not to comply with quarantine regulations, FDACS Office of Agricultural Law Enforcement deployed personnel to enforce compliance.

Table 3. Control Branch methods used during the 2015–2016 B. dorsalis eradication program in the Redland agricultural area in Homestead, FL.

Method Material used Amount applied Area treated (ha) RateMAT1 Dibrom/ME/Min-U-Gel mix2 820.7 L 6,734 1.5-2.9 L/km2

Soil drench3 Warrior II mix 118,458.4 L 14.9 0.795 L/m2

Foliar bait spray4 GF-120 1,794.3 L 45.7 88.7 ml/host

Aerial bait spray5 GF-120 4,345.7 L 4,144 73 L/km2

Bait stations Jackson traps without sticky insert, with ME/Dibrom or GF-120

1,199 bait stations

Fruit removal6 100,438.9 kg removed 45.7

1 75,135 spot treatments applied in 13 applications (rate = 1–2 gal. per mile2)2 Mix includes 96.5 L Dibrom concentrate (87.4%), 723.8 L ME, and 127.9 kg Min-U-Gel3 26.5 L Warrior II concentrate, 99 properties treated (rate = 0.56 fl. oz. in 15.5 gal. water/1,000 ft2)4 52,784 foliar bait sprays (444.8 L of mix)5 Rate = 10 fl. oz. per acre6 Fruit removed from areas within 200 m of sites with detections of females and/or larvae

Table 4. Summary of regulated entities during the 2015–2016 B. dorsalis eradication program in the Redland agricultural area in Homestead, FL.

Types of regulated entities by compliance agreement section Number

Fruit and Produce Dealers 259

Growers 823

Harvesters and Transporting 758

Processing Facility 31

Packinghouses Inside Quarantine Area 65

Packinghouses Outside Quarantine Area 56

Nurseries and/or Stock Dealers 830

Gift Fruit Shippers 5

Lawn/Property Maintenance 110

Airport/Bus Stations/Ocean Vessel/Train Stations 3

Charitable Organizations and/or Gleaners 47

A total of 1,804 compliance agreements was issued. Compliance agreements were vetted and reclassified into different sections to better identify the activities that the regulated entities perform. One compliance agreement may include multiple regulated sections; thus, total of compliance agreements issued does not equal the sum total of the individual sections.

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The officers actively patrolled the quarantine area daily and nightly to deter illegal movement of hosts. They confiscated approximately 75,000 kg of non-compliant commodities being illegally transported out of the quar-antine area. All of the confiscated host material was taken to an approved landfill for proper disposal. The regula-tory components of this program were monumental and would have been impossible to manage without a highly trained and well-seasoned state inspector team.

Smuggling, Interdiction, and Trade Compliance Investigations (SITC). The mission of USDA-APHIS-PPQ’s SITC Program is to detect and prevent the unlawful entry and distribution of prohibited and/or non-compli-ant products that may harbor exotic plant and animal pests, disease, or invasive species. The SITC Program also provides investigatory support during various emer-gency programs that arise within the state. The Florida SITC personnel immediately responded to the oriental fruit fly incursion to determine the associated pathway of its entry. To this end, SITC visited 694 commercial and residential sites, surveyed commercial locations for non-compliant imports, and visited door-to-door in residential settings. As part of this sweep, 53 face-to-face interviews took place in the immediate vicinity of the various fly finds. No admissions or proof of smuggling activity were obtained.

Economic impact. Direct federal, state, and county expenditures to eradicate B. dorsalis from Miami-Dade County were approximately $3.5 million. Throughout much of the program period, nearly 100 state and federal personnel were on-site and dedicated to eradication and compliance activities daily. In total, approximately 450 different state and federal personnel participated in the eradication program, typically working two-week rotations.

The University of Florida–Institute of Food and Agri-cultural Sciences (UF–IFAS) and FDACS estimated that there were approximately 6,943 ha of 22 different crops with high economic value and more than 800 nurseries directly affected by the quarantine. Alvarez et al. (2016) further estimated production losses and other economic losses due to the eradication program. They considered three scenarios that estimated direct losses resulting from the quarantine plus a potential non-planting response by growers in Miami-Dade County. The mid-range estimate of growers’ losses was approximately $10.7 million, and the associated total economic impacts to the county, including indirect and induced multiplier effects, were estimated at approximately 334 full- and part-time jobs lost and a loss of $27 million in industry output.

Unique Aspects of the Eradication ProgramHost plant issues. The Redland agricultural area is unique in the U. S. for its diversity and density of tropical fruits and vegetables. At least 186 plants on the oriental fruit fly host list (USDA 2016c) occur in the Redland area, and at least 52 of these are of commercial value.

At the onset of the eradication program, the B. dorsalis host list in the action plan included approximately 130 species. On 18 September 2015, a new Federal Order was published with the host list greatly expanded to 432 plant

species (USDA 2016c). All cultivars, varieties, and hybrids of the plant species in this list are considered suitable hosts of B. dorsalis. The timing of the host list update could not have been worse from the perspective of stakeholders, and it caused a great deal of confusion and consternation about regulated commodities! The host list expansion was due to the recent taxonomic synonymization of key pest species within the B. dorsalis species complex (Schutze et al. 2015a, 2015b). Bactrocera invadens, B. papayae, and B. philippinensis are currently recognized as junior syn-onyms of B. dorsalis, and therefore their geographical and host plant ranges were combined.

By acreage, the most significant hosts present in the Redland area were avocado, mango, carambola, guava, papaya, banana, longan, and litchi (Litchi chinensis Sonn.). More details on these crops are provided in the supple-mental file available with this paper on the American Entomologist website..

Commodity treatment issues. Multiple problems with commodity treatments were encountered at the beginning of the program. For example, malathion labels did not list many of the crops grown in the quarantine area, nor did they list the application frequency that the program mandated. In addition, supplies of GF-120 were limited on the U.S. East Coast. Thus, Dow AgroSciences transported product from the U.S. West Coast, delaying treatments by more than a week in many cases. To facilitate pre-har-vest bait treatments for growers, USDA, FDACS-Agricul-ture Environmental Services, and DPI worked with U.S. EPA to register SLN 24(c) labels for malathion (Gowan, Yuma, AZ; Loveland Products, Loveland, CO) and GF-120. GF-120 was registered as a SLN due to the application limitations of the Section 3 label. Aerial application over urban areas also was included in this GF-120 SLN label.

There were limited options for growers within the half-mile radius around fly finds to move their products. Post-harvest treatments, such as processing, irradiation, cold treatments, and fumigation with methyl bromide, would have allowed some regulated crops to be mar-keted outside the quarantined area. Various approved post-harvest treatments specific for B. dorsalis included in the USDA treatment manual (USDA 2016a) were accept-able for immediate certification and movement of host plants from the quarantine area—avocado, bell pepper (Capsicum annuum L.), Citrus spp., eggplant (Solanum melongena L.), litchi, longan, mango, papaya, squash (Cucurbita spp.), tomato (Solanum lycopersicum L.), and zucchini (Cucurbita pepo L.). Despite the multiple alternatives, however, these treatments were used in very few instances because of a lack of local certified facilities and equipment (i.e., hydrothermal and irradiation treat-ments) and not knowing whether the specific crops and cultivars grown in Florida tolerated the treatments. Exist-ing phytosanitary post-harvest treatments were designed and tested in areas where B. dorsalis is established and infests local cultivars. For instance, avocado treatments were designed for hard-skinned varieties (Guatemalan and Mexican races) imported from Hawaii, Israel, or the Philippines into the continental U.S., whereas Florida avocados (West Indian and West Indian-Guatemalan

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hybrids) with thinner and softer skin were not included in these tests. Tests conducted during the eradication program revealed that six Florida avocado cultivars do not tolerate fumigation or cold treatments specified in the USDA treatment manual (Carrillo et al. 2017).

Southern Florida is a major vegetable production area during the fall and winter months. Except for sweet corn, Zea mays L., and okra, Abelmoschus esculentus (L.) Moench, all other major vegetable crops grown in the area, including green beans (Phaseolus vulgaris L.), tomato, pepper, eggplant, and squash, are included in the official B. dorsalis host list (USDA 2016c). The B. dorsalis detection occurred at the onset of the vegetable planting season and induced major changes in production plans of commercial vegetable growers, who opted to delay planting and avoid the quarantined area.

One approved treatment that could have been used for all of the B. dorsalis host material was irradiation, but there were no facilities conducting phytosanitary irradiation in Florida. A work plan was developed to allow for move-ment of commodities to the nearest irradiation facility in Gulfport, Mississippi. Although this was an expensive solution, phytosanitary irradiation treatments were used a few times for high-value crops, such as dragon fruit, Hylocereus spp. (three truckloads; Fig. 8) and mamey sapote (two truckloads).

Outreach activities and coordination. Outreach efforts were critical to the success of the eradication campaign. The program faced the challenge of communicating basic and technical information about the pest and regulations to the agricultural industry, elected officials, and an eth-nically diverse general public. The outreach component also had an educational role by raising the awareness of existing services through stakeholder workshops. Import-ant components of outreach activities were an interac-tive website to facilitate decision-making by commodity growers and homeowners; a toll-free helpline; a dedicated regulatory information telephone line; an information tent centrally located within the quarantine area; 12 mobile road signs in English and Spanish strategically placed around and within the quarantine area; and centrally located compliance agreement sign-up at the UF–IFAS facility in Homestead, which was staffed by program personnel (Figs. 9–10; Suppl. file). In addition, multiple media events and town hall meetings were organized for growers, public officials, and interested citizens. Targeted outreach allowed program staff to address the specific needs of each stakeholder group.

Partnering with other agencies and institutions was essential for communicating timely information. At the onset and throughout the program, Incident Command worked closely with the University of Florida–Tropical Research and Education Center and Miami–Dade County Extension personnel. As known members of the commu-nity, they were essential in communicating and explaining the quarantine and corresponding regulations associated with treatment and movement of regulated commodities. Similarly, FDACS Office of Agricultural Law Enforcement personnel, although primarily deployed to support com-pliance and deter illegal movement of B. dorsalis hosts

Fig. 8. Dragon fruit in quarantine area could not be moved off of the property without treatment or processing.

Fig. 9. Road signage at entrance to quarantine area.

Fig. 10. Information tent for local stakeholders.

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out of the quarantine area, reinforced the urgency of the quarantine, answered questions, addressed stakeholders’ concerns, and directed industry stakeholders to program personnel for compliance information. In addition, local government officials involved in outreach helped commu-nicate the needs of their constituents and the resources available to help with the eradication effort.

The success of outreach efforts was attributable to the use of multiple formats and delivery of consistent and straightforward messages about the pest, regulations, control measures, and quarantine area. Also, the outreach effort adjusted and added communication tools to meet the specific needs of industry stakeholders. Adding the online interactive maps and daily group e-mail updates allowed industry stakeholders to get timely answers to specific questions to aid in their decision-making pro-cess. The open and responsive format of the outreach effort, built in partnership with grower and community associations, university extension, and county govern-ment, helped forge a united effort to achieve eradication.

Speculation on the Outbreak and Its OriginsCommercial movement of fruit fly host material is highly regulated. Interception records at U.S. ports of entry show that only a small fraction of all arriving fruit fly-infest-ed commodities is sourced as “permit cargo” (1.2%). In contrast, approximately 97% of all infested commodities arrive via passenger baggage (S. Bullington, USDA-APHIS-PPQ, pers. comm., 1 June 2016). For this reason, routine fruit fly detection traps are most heavily concentrated in population centers (≈1–2 JT/ME traps per km2), whereas rural areas have low trap densities (≈0.6 JT/ME trap per km2). When the first B. dorsalis was found in the Redland agricultural area on a delimitation survey trap, there were only five JT/ME traps distributed in the five contiguous core sections as part of the regular detection program. Although an exact date of introduction is unknown, an approximate latest date of arrival can be estimated based on backward extrapolation of life cycles. Given the low density of JT/ME traps in the Redland agricultural area and the number of flies trapped and their dispersion, it is likely that the founder population went through at least one generation before the detection event. Polyph-agous fruit flies, such as B. dorsalis, are strong fliers and often disperse over tens of kilometers before reproduc-tive maturity (Fletcher 1987, Vargas et al. 1989, Froerer et al. 2010). Males respond strongly to ME upon attain-ing sexual maturity at about 10 days (Karunaratne and

Karunaratne 2012). If the first B. dorsalis male detected in Palmetto Bay on 17 August was a dispersing fly that originated in the Redland agricultural area, it could have emerged from host fruit that had been infested as early as 7 July 2015. This speculation is based on the number of day-degrees required at temperatures at that time to complete development from egg to adult, plus 10 days for reaching the age to respond to ME. Likewise, presuming that the larvae found in mango on 28 August were the beginning of a new cohort of B. dorsalis, the degree-day model suggests a cohort of females that started about 3 July 2015. If additional generations went undetected, B. dorsalis may have arrived a month or more earlier. A higher density of traps in the Redland agricultural area might have detected the infestation even earlier. How-ever, a density of only 0.4 JT/ME traps per km2 or fewer was sufficient in this case to detect the population while it was relatively small and manageable in size.

Molecular analysis of 114 of the B. dorsalis specimens captured in the program, including each of the single flies trapped in Palmetto Bay and Miami, support a novel introduction of the pest into Florida in 2015, most likely from Southeast Asia. Three cytochrome oxidase I (COI) haplotypes were present in this population. COI hap-lotypes from one previous (2014) and five subsequent oriental fruit fly detections in Florida (2016–2018; Table 1) were all different from those seen in 2015 and from each other (Norman Barr, USDA-APHIS, pers. comm.).

Concluding RemarksThe procedures for conducting a fruit fly eradication program, however large the area involved, are straight-forward, science-based, time-tested, and readily imple-mented with sufficient resources and a well-trained team. Detection and control activities such as MAT, soil drenches, bait sprays, and fruit removal may lead directly to eradication. The accompanying quarantine and regu-latory actions, however, are in many ways unpredictable and more challenging, as they involve interactions with numerous groups of stakeholders, who often have con-flicting agendas. For example, some producers in the Redland agricultural area, without any requirement to do so, voluntarily plowed their crops under to eliminate potential breeding habitats for the flies. In contrast, some producers in the mandatory fruit-removal zones refused access to their properties, relenting only after being served a legal warrant. Other challenges included the unexpected and large expansion of the regulated host plant list two weeks into the campaign, leading to complaints about the validity of the regulations. Chemical control actions led to unfounded charges of harm to livestock or pets. Additionally, both the agricultural production community and the public at large have endured a seemingly endless rash of high-impact invasive insects and their vectored plant pathogens, e.g., citrus greening that has devastat-ed citrus production in Florida (Singerman and Useche 2016) and laurel wilt that kills native redbay along with avocado, its commercial relative (Mayfield et al. 2008). The resulting fatigue, complacency, and uncooperative responses by producers and consumers alike are palpable.

Although an exact date of introduction is unknown, an approximate latest date of arrival can be estimated based on backward extrapolation of life cycles. Given the low density of JT/ME traps in the Redland agricultural area and the number

of flies trapped and their dispersion, it is likely that the founder population went through at least

one generation before the detection event.

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Ultimately, the best response to a pest quarantine is to eliminate the causative agent as quickly as possible. In the 2015–2016 B. dorsalis invasion, a well-coordinated, multi-agency program with experienced personnel and good resources enabled a successful and rapid eradica-tion. The survey crews began the Redland agricultural area delimitation activities on the same day that the first male was detected. The full trap array was in place within four days, despite multiple detections in the surrounding areas, requiring additional trap deployment. Fruit remov-al from the property where larvae were detected began the day after that detection. Although public notification was required 24 hours before any chemical control could begin, the first round of MAT (4,900 spot applications) was completed within 10 days. The total time from first detection of B. dorsalis in the Redland agricultural area to last detection was 45 days. Unfortunately, the last detec-tion did not end the quarantine, which depended on the weather and its impact on attainment of degree-days corresponding to three life cycles. The quarantine was lifted on 13 February 2016, fewer than six months after it was imposed. Although this could be considered quick in terms of a B. dorsalis eradication program, it represents a long time relative to the narrow market windows of many specialty crops grown in southern Florida.

Every crisis of this nature is subject to hotwash (debrief-ing) analysis that reveals correctable deficiencies. As a result, several program improvements have been inau-gurated. For example, the large rural land area of Miami-Dade County classified as Criterion 3 for detection trap-ping purposes has been reassessed and now specifies a higher trapping density. Also, chemical registration labels that did not exist at the start of the eradication program are now in place and are available, if needed, for the next fruit fly quarantine event. And now, of course, state and federal personnel have gained additional experience with eradication and regulation, and new and improved lines of communications have been established.

Emphasis on specific research and development needs may lead to improved responses to future eradication and quarantine events. The perennial search for a “better mousetrap” is one. Detection of B. dorsalis is based on male attraction to ME. However, male dispersal biology frequently takes them many kilometers away from the females and sites of larval infestation. The mobility and invasion capabilities of these flies are truly frightening. In this case, even though we eventually discovered the infestation center and saturated the area with McP/TYB traps, the traps performed very poorly in attracting and capturing females; sharp-eyed entomologists did a much better job of catching females! A new or improved female attractant for B. dorsalis could significantly improve early detection of core outbreak sites for these fruit flies. The development of systems approaches for regulated hosts is another research need. Quarantine treatments may be reduced or replaced by a system of mitigating factors, such as selection of green fruits or resistant cultivars or special packing house procedures. Both tomato and avocado are amenable to protocols that allow commer-cial production to proceed even in areas where fruit flies

are established, such as C. capitata in Hawaii (Jang et al. 2014, USDA 2013).

When a quarantine is enacted, growers and the pub-lic are affected immediately and desire relief. Research solutions, however, typically require years of development time. Something as “simple” as replacing diazinon as a soil drench, a problem identified during the C. capitata eradication programs in Florida during 1997–1998, took 15 years to enact (Stark et al. 2014). Similarly, public concerns arose over the use of malathion bait sprays in California fruit fly eradication programs in 1981 (Kahn et al. 1990), but it took more than 17 years (1984–2001) to develop and register spinosad for insect control. Its efficacy against tephritids was demonstrated (King and Hennessey 1996), and GF-120 bait spray was developed (Mangan et al. 2006) and subsequently approved for use in fruit fly programs (Code of Federal Regulations 7 CFR 301.32-10). Thus, replacing malathion with GF-120 as tox-icant in bait sprays took more than 20 years.

There is perhaps no solution for some of the problems experienced in this event (e.g., the lack of post-harvest treatment options available to growers). It may not be commercially viable for local irradiation and hot-water treatment facilities to exist in mothballed status until such a crisis and need arises. Likewise, how do we reduce the strong monetary incentives for producers to transport regulated commodities in violation of quarantine restric-tions? Presently, producers in quarantined areas are potentially subject to total monetary loss of their crops. Perhaps compensation to cover grower losses could mit-igate cheating and the associated risk of spreading the pest outbreak.

There were numerous challenges for the 2015–2016 B. dorsalis eradication program in Florida, due primarily to the size and location of this infestation. However, with the infrastructure and experienced personnel already in place as a result of long-term, ongoing regulatory pro-grams for tephritid fruit fly detection, the incursion was detected in time to initiate a B. dorsalis eradication pro-gram that prevented establishment of this pest species. Quarantine activities prevented spread of the infestation to areas outside of the delimitation survey areas. Despite the challenges, however, strong communication and coop-eration among state and federal regulatory agencies, the university, county, and federal research and extension personnel, the growers, and other community members facilitated implementation and successful completion of the eradication effort.

AcknowledgmentsWe thank the Florida Department of Agriculture and Consumer Services–Division of Plant Industry for their support on this contribution; Courtney Hart (USDA-APHIS-PPQ, Gainesville, FL) and Matthew Albritton (FDACS-DPI, Gainesville, FL) for providing the maps; and Georgia Keene (USDA-APHIS-PPQ, Palmetto, FL) for help with editing the manuscript. We appreciate the insightful comments provided by reviewers Todd Shel-ley, Cathy Marzolf, Sarah Marnell, Ken Bloem, Susan Halbert, Bryan Benson, Matt Brodie, and Paul Kendra.

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Mention of trade names or commercial products in this publication is solely for the purpose of providing spe-cific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture. USDA is an equal opportunity provider and employer.

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Gary J. Steck, Division of Plant Industry, Florida Department of Agriculture and Consumer Services, Gainesville, FL, [email protected]; Abbie J. Fox, U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine (USDA APHIS PPQ), Fruit Fly Exclusion and Detection Program, Palmetto, FL; Daniel Carrillo, University of Florida, Tropical Research and Education Center, Homestead, FL; David Dean (retired), USDA APHIS PPQ, Center for Plant Health Science and Technology, Palmetto, FL; Amy Roda, USDA APHIS PPQ, Center for Plant Health Science and Technology, Miami; Nancy D. Epsky (retired), USDA, Agricultural Research Service, Miami, FL; and Trevor R. Smith, Division of Plant Industry, Florida Department of Agriculture and Consumer Services, Gainesville, FL.

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