History and success of plant pathogens for biological control of introduced weeds in Hawaii

The economic value of biological control of introduced, invasive weeds in Hawaii with fungi is estimated to surpass $100 million. The history of biological control of invasive introduced weed species with fugal pathogens in Hawaii began in 1967 motivated by the request of a Kauai rancher whose pastures were infested with 'Kolomona,” Senna surattensis. A disease of unknown origin present in his ranch was studied. This led to the first successful control of an invasive species in the Islands by wound-inoculating the isolated pathogen, an Acremonium sp., on the weed in 1968, which killed 'Kolomona' in more than 10 ha of land. Hamakua 'Pa-makani,' Ageratina riparia, was the most serious invasive weed of range and forests of Hawaii in 1973. The release of the white smut Entyloma compositarum from Jamaica in 1975 induced spectacular disease epidemics in the late 1970s, “wiping out the weed.” This specific pathogen cleared 'Pa-makani' from more than 200,000 ha of infested rangeland, and kikuyu grass (Pennisetum clandestinum) pastures were rehabilitated in less than 6 years, saving the ranchers millions of dollars. These results convinced the Hawaii Department of Agriculture that fungi were a valuable tool in the management of invasive weeds. Koster's curse, Clidemia hirta, was considered by environmentalists the most serious introduced species in 1984. The specific fungal pathogen, Colletotrichum gloeosporioides f. sp. clidemiae, was introduced in 1985 from Panama, and approved for field inoculations by the Hawaii Board of Agriculture in 1986. Repeated inoculations with this fungus have caused striking decline of the weed in Aiea State Park and Palolo Valley, Oahu. This fungus becomes airborne only during extended windy and rainy periods, which limits its natural distribution. Therefore, repeated applications are required to enhance it as a bioherbicide. Banana poka (Passiflora tarminiana), from the Andean region between Colombia and Ecuador, was the most serious invasive species of high-elevation (800-2200 m) forests of Hawaii in 1983. This climbing vine threatened the pristine koa forests of Hawaii, Maui, and Kauai and the numerous endangered species of Hawaii's flora in the undergrowth. In 1991, Septoria passiflorae was found on infected banana poka seedlings at Ipiales, Colombia. The pathogen was introduced to Hawaii in 1993 for host-range study in a containment laboratory. Host-range studies showed the fungus to be specific only to banana poka. Inoculations by spraying spore suspensions on adaxial leaf surfaces during 1996-1997 in the Hilo Forest Reserve resulted in major epidemics that severely defoliated the vines. One year after inoculations, the weed biomass was reduced from 40 to 60% and by more than 95% five years later. By 2003, banana poka had been eliminated from most forests, except from north Kona, Hawaii where acid rain killed the fungus. Bush lantana (Lantana camara) has been in Hawaii since 1858, and the only pathogen that affects the Hawaiian accessions is a Septoria sp., which was introduced from Ecuador in 1984. The US Department of Agriculture, Animal and Plant Health Inspection Service (APHIS) granted permission to use this pathogen for field inoculations at Kokee State Park in 1996. Sites inoculated in 1989-1999 are showing significant decline in the lantana population, and it is expected that effective control of the weed will occur in time.