Citrus Bacterial Canker: Outbreaks and Regulatory Response
Citrus bacterial canker (CBC), caused by Xanthomonas citri subsp. citri (syn. X. campestris pv. citri, X. axonopodis pv. citri) has been introduced into Florida several times. Below is a brief history of the detection of CBC in Florida and the responses mounted by the Florida Department of Agriculture and Consumer Services Division of Plant Industry (FDACS-DPI) and US Department of Agriculture Animal and Plant Health Inspection Service (USDA-APHIS).
1910: Trifoliate rootstock infected with the Asian or “A” strain of the bacterium were brought into Florida from Japan. The response to CBC detection included the implementation of a quarantine to prevent the movement of citrus plants, the destruction of over three million nursery plants, and the removal of over a quarter million field trees. Eradication was declared a success in 1933 and regulatory detection surveys have continued to the present day since this initial CBC outbreak.
1984: An outbreak of citrus bacterial spot, caused by a less virulent strain (“E” strain) (now X. alfalfae subsp. citrumelonis) was detected on nursery stock. Over twenty million citrus plants were destroyed.
1986 to 1994: The “A” strain was detected in residential citrus in the Tampa Bay area and in nearby commercial groves. For the first time, not only were infected trees destroyed but also all exposed host plants within 38 m (125 ft). Also for the first time, residential trees were eradicated. After the destruction of 600 residential trees and almost 90,000 production trees, and no further detections for a two-year period, an official declaration of successful eradication was made in 1994. Regulations were suspended.
1995: The “A” strain of the CBC agent was detected on residential citrus in the vicinity of the Miami International Airport. It is believed that the appearance of CBC in commercial citrus resulted from spread out of residential sources. An eradication program was initiated immediately, and quarantine regulations were re-instated. The protocol required removing or buckhorning (removal of all green aboveground tissue, also known as hat-racking) all potential hosts within 38 m (125 ft) of an infected tree. After one year, the infection level remained too high to continue with the buckhorn protocol and it was suspended. In late 1996, all exposed trees had to be removed. Resources were quickly depleted; the program was under-staffed, the quarantine area rapidly expanded to 93,499 ha (361 mi2). The situation was exacerbated by the detection of CBC in another area in west central Florida. The isolate from this area was found to be genetically identical to the isolate responsible for the 1984 outbreak, which indicated that CBC had not been successfully eradicated after all. In early 1998, the Florida Commissioner of Agriculture and the Citrus Canker Eradication Program (CCEP) declared a moratorium on the
removal of exposed citrus trees because a judge stopped tree removal in response to homeowner lawsuits using standards in effect at the time. Homeowners were opposed to removal of trees that were not infected without evidence that they could be sources of inoculum. During the moratorium, the bacteria quickly spread and additional sites were discovered in southwest Florida. During this 12-month study period, the 1,900 ft rule (580 meter radius) was created which expanded the quarantine to 129,500 h (500 mi2) with a program budget of $9.5 million. By 2000, the Persian lime industry in south Florida had been destroyed (Schubert et al., 2001).
2004: The three hurricanes and a tropical storm that crossed the Florida peninsula dispersed the pathogen even further across the state (Irey et al., 2006a; Gottwald and Irey, 2007); resulting in the establishment of new infections at substantial distances from the known existing infections. Survey and eradication efforts by the FDACS and USDA-APHIS became even more intense to eliminate new outbreaks before the next hurricane season.
The FDACS and USDA-APHIS simultaneously employed the following survey protocols: the sentinel grove survey (based on sentinel commercial blocks of susceptible cultivars), the targeted grove survey (based on meteorological data that used a GIS-weather model to predict the direction of disease spread due to hurricanes), the delimiting grove survey (which was performed once new infections were discovered) and the self survey (performed by the grower). Production managers and other workers that are in contact with commercial citrus on a daily basis were trained by a joint University of Florida and FDACS-DPI program to search for, recognize, and report suspicious symptoms to FDACS-DPI or USDA-APHIS inspectors for confirmation.
Not all citrus canker-infected trees detected in 2004 had been removed by the time the first hurricane (Hurricane Wilma) hit the Florida peninsula in October 2005. Of the 80,000 acres of commercial citrus identified as affected after the 2004 season, 32,000 acres remained even with the removal of 120,000 trees per week. It was estimated that an additional 168,000 to 220,000 acres of commercial citrus would have to be destroyed after the 2005 hurricane season under the 1900-foot protocol. At this point in time, the annual federal appropriation to maintain the program was $36 million. Eradication costs significantly increased from $10 million in 1996 to $50 million in 1999. In 2000, program costs escalated to $145 million. A panel of USDA scientists and global experts in citrus diseases conferred and concluded that the disease was now so widely distributed that eradication was not feasible.
On January 11, 2006 the USDA issued a press release stating that it would discontinue all efforts to eradicate canker. Subsequently, the Florida House of Representatives decided to halt the eradication campaign and repeal the 1900-foot protocol on May 3, 2006. However, because of the value of the fresh fruit industry and not every citrus production area in Florida was severely infected, there was still considerable support from the production industry to continue with a revised management program. Hence, the concept of a State-Federal-Commercial Industry Citrus Health Response Plan was launched. It is based on best management practices, living with the disease while minimizing production losses, and the implementation of a quarantine that prohibits the movement of fruit from known-infected areas of the state to non-infected areas and to other citrus-producing states. This plan has evolved into a National program, the Citrus Health Response Program, and is administered by the USDA-APHIS. USDA-APHIS has recently lifted the quarantine on Florida fresh fruit after findings that commercial fruit is not an important means of spread of the disease, thus allowing growers more flexibility in marketing their fruit.
Factors contributing to the failure of the Canker Eradication Program include:
Time required for tree removal: A few homeowners refused to comply with tree removal or provide access to residential properties, and initial resources (manpower, vehicles, and funding) were limited.
While legal battles for tree removal were being fought, inoculum sources remained during the declaration of moratorium in 1998 and the disease spread to new areas of the state through human movement.
Tropical storms and hurricanes were optimal for bacterial spread (bacterial cells blown long distances by wind and carried in rain drops).
Florida lacks geographical barriers such as mountains.
Lack of a positive public relations campaign especially in ethnic residential areas.
Lessons for huanglongbing (HLB) learned from the canker experience:
Importance of disease-free sources of citrus propagation material and nursery stock.
Eradication actions taken at the first detection of Asian citrus psyllid (ACP) in 1998 might possibly have slowed ACP spread and delayed HLB’s incursion (although ACP control efforts elsewhere have not been very successful).
Intensive surveys for the Candidatus Liberibacter asiaticus pathogen, if conducted in 1998, might have stimulated action to slow the spread of HLB.
Effective public outreach campaigns help to make the urban sector part of the solution to maintaining the commercial industry.
While plant pathogens and their vectors and insect pests are part of biology, their implications enter the realm of social and political arenas. The urban sector does not always trust scientists or regulatory personnel. These should be taken into consideration when developing a public outreach campaign.
Massive amounts of funding do not always solve the problem.