The citrus canker epidemic in Florida: the scientific basis of regulatory eradication policy for an invasive species.

Increasing international travel and trade have rendered U.S. borders much more porous and dramatically increased the risk of introductions of invasive plant pests into agricultural crops (1). Nationally, the responsibility for safeguarding agriculture falls to the U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Plant Protection and Quarantine (USDA, APHIS, PPQ). However, the current system for protecting agricultural industries has broken down allowing for an unprecedented number of introductions of exotic pests, including plant pathogens. Such introductions threaten crops and can hinder national and international agricultural markets and trade. In 1999, President Clinton announced an initiative for invasive species to address these issues and introduced an Executive Order on Invasive Species (10). The order is intended to coordinate and enhance federal government efforts to prevent introduction of invasive species and to provide for their control. The Executive Order calls for the appointment of a council, chaired by the Secretaries of Agriculture, Commerce, and the Interior, and composed of key federal agencies charged with developing an invasive species management plan. In response, the National Plant Board initiated a “stakeholder” review of the USDA, APHIS, PPQ safeguarding system in order to identify means to improve pest exclusion and detection of and response to invasive pest introductions (1). Enter citrus canker. Currently in Florida, one such invasive species is Xanthomonas axonopodis pv. citri (Xac), a bacterial plant pathogen that causes Asiatic citrus canker. Citrus canker is an introduced plant disease that has received considerable press attention, has produced far-reaching political and socioeconomic impact in Florida, and has implications for national and international trade (3,4). Although Xac is mostly a leaf and fruit-blemishing pathogen, the disease triggers immediate quarantines of areas with outbreaks in Florida, disrupting movement of fresh fruit (3,11). The importance of citrus canker as a major invasive disease and the political forces that govern attempts to eradicate the disease were recently exemplified by the visit of the U.S. Secretary of Agriculture to the Homestead/Florida City area south of Miami on 22 March 2000 to view a major outbreak of the disease first hand. Secretary Glickman declared the South Florida canker outbreak area in Dade and Broward Counties a federal disaster area, opening the door for disaster relief funds and for U.S. Marshals to assist crews in expediting the cutting and removal of trees from homeowners’ residences in metropolitan Miami (26). South Florida was one stop on a national tour conducted by the Secretary of Agriculture to highlight non-native, invasive pests and diseases that threaten U.S. agriculture and natural resources (20). Citrus canker has a long history. The disease was first found spread throughout the southeastern United States on imported seedlings from Japan in the early 1910s and was declared eradicated from Florida and the adjacent states in 1933. Citrus canker was discovered again in Manatee County Florida, south of Tampa Bay in the late 1980s, and was thought to be eradicated by 1994. Two years thereafter, the disease re-emerged in the same area on the west coast of Florida where the 1980s outbreak had occurred. In the meantime, a new and separate infestation of citrus canker was discovered in urban Miami in 1995, that was estimated to have been introduced in 1992 or 1993 (17). Since that time the disease has spread from an initial area of 14 square miles near the Miami airport, to over 1,005 square miles in the metropolitan area plus an additional 260 square miles of urban and commercial citrus areas throughout the State. Genomic analysis of bacterial isolates from both time periods indicates that the latest Manatee County outbreak is a hold over from the 1980s outbreak that escaped the eradication program. However, the majority of current outbreaks of citrus canker are caused by the same genotype of Xac as in the Miami area. Thus, human-assisted movement of the bacterium from that source appears to have occurred several times. In early 2000, a third genomically distinct isolate of Asiatic citrus canker with an attenuated host range was identified in Palm Beach County on the east coast of Florida. Thus, there are presently at least three Xac genotypes that have been introduced into Florida in the recent two decades. Although this bacterial disease is mostly a leaf and fruit-spotting malady, it results in immediate quarantines, disrupting national and international trade (3,11). Although citrus canker can cause debilitation of trees and losses in fruit quality and yield, it is because of its socioeconomic and political impact that the disease is so devastating. If Xac should become endemic in Florida, it will effectively result in a prohibition of interstate commerce of fresh citrus fruit, which comprises approximately 20% of the State’s $8 billion commercial citrus industry (23). In addition, some cultivars of highly susceptible citrus species, such as grapefruit (Citrus paradisi), will have reduced economic viability due to the requirement for multiple bactericidal sprays per year to maintain yields and quality. The Florida citrus industry is concentrated predominantly in the southern half of the State, in close proximity to rapidly expanding urban population centers. Because the outbreaks originated in urban areas, response to citrus canker, therefore, affects not just the citrus industry. Hundreds of thousands of urban homeowners have citrus trees as ornamentals and for dooryard fruit production and have had or will have their trees destroyed. The Florida Department of Agriculture and Consumer Services, Division of Plant Industry (DPI) and USDA, APHIS responded to the 1995 Corresponding author: T. R. Gottwald; E-mail address: [email protected]