Cutaneous chytrid infection was detected during an investigation into mass deaths in farmed North American bullfrogs. Although chytridiomycosis has been reported as an important cause of mass deaths in wild amphibians, whether chytrid infection was the cause of deaths in the disease outbreak described in this paper is unclear. First, while no examinations for B. dendrobatidis had been performed before the deaths, this organism has been repeatedly observed in skin examinations of healthy frogs in follow-up studies. Second, although not proved efficacious against cutaneous chytridiomycosis, the use of benzalkonium chloride, a recognized therapy for infections with nonhyphal fungi, failed to reduce mortality rates.
Possible causative agents include an infectious pathogen, which could not be detected by the examinations used, such as a ranavirus (2
) or adverse environmental factors. Alternatively, chytridiomycosis could be the cause of the outbreak if the current chytrid is a different strain from that causing the outbreak or became attenuated, if the farmed bullfrogs had immunity to the pathogen, or if a change in the environment before the die-off allowed a normally benign infection to become pathogenic. For example, increased temperatures reversibly inhibit both growth of B. dendrobatidis
in culture (3
) and the progress of disease outbreaks (D. Nichols, Smithsonian Institute, pers. commun.). Also, chytridiomycosis epizootics in wild U.S. amphibians often coincide with late-winter breeding (2
). The deaths we describe occurred at the beginning of winter and may have been precipitated by lowered environmental temperatures.
The mortality rates reported here were dramatic and costly. The rearing of bullfrogs is a growth industry in South America, particularly Brazil, Uruguay, and Argentina. Anecdotal reports of similar loss of stock in a number of farms in Uruguay (R. Mazzoni, unpub. data) suggest that disease is a major economic threat to this industry in South America. This situation is exacerbated by a lack of veterinary diagnostic capacity, management protocols, and treatment or prophylaxis.
Regardless of the cause of the deaths, the North American bullfrog may be relatively resistant to chytridiomycosis, at least under the environmental conditions in the current study. Unpublished data suggest that metamorph bullfrogs can be experimentally infected by B. dendrobatidis
without developing signs of disease (12
), and others have noted differential susceptibility to this disease among amphibian species (1
Nonclinical (silent) infections in farmed bullfrogs suggest that this species may act as a carrier of chytridiomycosis, which has serious implications for conservation of biodiversity. B. dendrobatidis
has been implicated in the complete removal of multiple species amphibian populations over large geographic areas in the wild (1
). Farmed bullfrogs originate in North America and have been introduced to South America during the last few decades for the lucrative restaurant trade. Live, farmed South American frogs are exported to other South American countries and to the United States. The trade in bullfrogs is large in scale and global in scope. According to the U.S. Fish and Wildlife Service, over 1 million bullfrogs are imported into the United States each year from South America alone (9
), with others shipped in from Asia. In the United States, animals are usually imported live at U.S. ports of entry and undergo veterinary inspections that are inadequate for identifying chytrid infection.
Recently, guidelines for amphibian translocations have been published that include specific quarantine and testing recommendations for chytridiomycosis (13
). These procedures, however, are intended for animal movements for International Union for Conservation of Nature and Natural Resources programs and are not legally binding. In the United States, the U.S. Department of Agriculture (USDA) may be the most suitable regulatory body for the bullfrog trade since these animals are a commercial agricultural product. No current USDA regulations exist for the identification of infectious agents in amphibians.
The farm we studied was opened in October 1998 with stock that originated from Brazil. The Brazilian farmers originally imported 300 pairs of frogs from Canada to set up the first South American farms approximately 30 years ago. The pathogen has been present in bullfrogs in North America since at least the 1970s (14
). B. dendrobatidis
in this outbreak may have been imported with breeding stock from North America. Alternatively, wild South American amphibians may be the source of infection. The Uruguay farm in our study is enclosed by concrete walls, but outdoor ponds have open access to wildlife, and wild amphibians (tree frogs) have been observed in the greenhouses where indoor rearing tanks are located. Whatever the origins of B. dendrobatidis
in farmed bullfrogs in Uruguay, such open-plan farms are likely sources of infection and disease for wild amphibian species. In view of this risk, surveillance for chytrid infection and for unusual levels of deaths in endemic amphibian species should be established in the vicinity of frog farms in Uruguay and elsewhere in the world.
Global trade and commerce are regularly cited as drivers of disease emergence in humans, domestic animals, wildlife, and plants (6
). For wildlife emerging infectious diseases, quantitative analyses demonstrate that this process is the most important driving factor (8
). For example, the (unknown) causative agent of the bullfrog deaths we describe may be spread by such trade. Also, the identification of B. dendrobatidis
in an international food animal trade has implications for amphibian conservation and for disease emergence in general. Our study adds to reports of chytridiomycosis in the international pet trade (19
), amphibians for outdoor pond stocking in the United States (2
), importation for zoo collections (5
), trade in laboratory animals (21
), and species known to have recently been introduced into new geographic regions (e.g., cane toads in Australia) (1
With a continued rise in the international air transport volume (22
), we predict a growing impact of trade and commerce on disease emergence within all populations, including wildlife. For this reason, we urge a revision of national and international veterinary guidelines for the inspection and quarantine of imported animals and animal products.