A summary of information on the rust Puccinia psidii Winter (guava rust) with emphasis on means to prevent introduction of additional strains to Hawaii

Abstract

The neotropical rust fungus Puccinia psidii ( P. psidii ) was originally described from the host common guava in its native Brazil but has been found since on hosts throughout the myrtle family (Myrtaceae), including a dramatic host jump to nonnative Eucalyptus plantations. Most rust fungi are able to live only on a very narrow range of host species. P. psidii is unusual both for having a broad host range and for the intensity of its damage to susceptible young growth. This rust first got a foothold in the United States in Florida more than three decades ago. The U.S. Department of Agriculture (USDA) has since considered it a nonactionable, nonreportable pest. Hawaii and Florida are the only two states with native species in the myrtle family. Over a period of 30 years, this rust has done little damage to any of the scattered native Myrtaceae in Florida, although the host range of the rust has gradually grown to about 30 mostly nonnative species in the family, apparently because of increasing genetic variety of the rust by repeated introductions. However, Florida’s native Myrtaceae are among the roughly 1,100 neotropical species that are largely resistant to P. psidii . The 3,000 species of non-neotropical Myrtaceae of the Pacific, Australia, Asia, and Africa are expected to prove much more vulnerable to P. psidii . Little is known about the genetics or genetic strains of P. psidii , although existing literature shows that there are numerous strains that have differential ability to infect suites of host plants. The rust was first recorded in the state of Hawaii on Oahu in April 2005 and quickly spread throughout the Hawaiian Islands. The main concern in Hawaii became the potential threat to ohia, Metrosideros polymorpha (Myrtaceae), the endemic forest tree species overwhelmingly important in Hawaii’s nature and culture. The potential ecological consequences of a virulent strain of rust on ohia forests are immense, due to its role as a foundation tree species and the diversity of niches it fills in Hawaii. A single genetic strain of the rust is established in Hawaii, apparently composed of a single genotype lacking sexual reproduction. P. psidii has been found statewide in Hawaii attacking Myrtaceae from near sea level to about 1,200 m elevation in areas with rainfall ranging from 750–5,000 mm. Five of eight native Myrtaceae and at least 15 nonnative species have been observed as hosts of P. psidii in Hawaii. The federally endangered Eugenia koolauensis (nioi) and the nonendangered indigenous species Eugenia reinwardtiana are severely damaged. The introduced (an Asian species) and invasive rose apple, Syzygium jambos , is severely affected at a landscape scale, with widespread crown dieback and many instances of complete tree death. In spite of billions of wind-dispersed rust spores produced from rose apple infestations during 2006 to 2008, adjacent ohia have been little affected to date by the rust strain in Hawaii. Within the elevation range of the rust, P. psidii is found on less than 5 percent of the ohia trees in the wild; on those ohia trees on which the rust is found, it is normally found on less than 5 percent of the leaves. The strain in Hawaii has not attacked many of the species known to be infected by the rust elsewhere, including common guava. On the basis of the very substantial genetic diversity of the much-studied, crop-damaging species of the genus Puccinia , there is good reason to believe that there are at minimum dozens and likely hundreds or thousands of genotypes of P. psidii , likely concentrated in the core range in Brazil but with potential for dispersal by globalization. Multiple genotypes are believed already present in the United States and certain to spread freely in the absence of restrictions. The U.S. Forest Service has initiated a major collaborative project in Brazil to investigate the genetics of susceptibility of Hawaii’s ohia to P. psidii , but initial results will likely not be available for several years. If just one more strain reaches Hawaii, the consequences could be dire for ohia, with each new genotype arriving having an unknown likelihood of increasing damage to ohia; possibilities for mutation and (or) genetic mixing, even with asexual strains, are apparently substantial, based on what is known about other Puccinia species. Investigations are needed to clarify rust-nioi relationships. However, it is likely that keeping out new strains of P. psidii may be important for long-term survival of nioi as well as for the health of ohia forest. The source of Hawaii’s initial invasion by P. psidii is uncertain but is strongly suspected to have been decorative foliage of species in the myrtle family from the mainland United States, most likely California, where there had been outbreaks of this rust on cultivated myrtle in 2005. In 2006–7, Maui’s Hawaii Department of Agriculture (HDOA) inspectors intercepted several P. psidii infected shipments of foliage myrtle, shipped from several California counties. Recognizing the huge threat of the rust to Hawaii’s one million acres of ohia forests, and consequently to Hawaii’s watersheds and biodiversity, Hawaii’s Board of Agriculture unanimously approved an interim rule in August 2007 banning importation of plants in the myrtle family from “infested areas,” specified as South America, Florida, and California. However, the interim rule has not been made permanent by HDOA, and the department has stated that it needs further information to formulate a long-term rule that imposes appropriate measures. Rust spores can survive for 2 to 3 months, and the pathogen can be transported to Hawaii on Myrtaceae from anywhere in the world through the United States mainland. There is much geographic reshuffling of flowers and foliage among the far-flung firms in the trade, especially for bouquet making. Because P. psidii is a nonactionable and nonreportable pest in the United States, foliage and flowers of the myrtle family can move freely into the country (usually but not necessarily always through the ports of Miami or Los Angeles), and from state to state. Currently, the State of Hawaii regulates incoming plant material in the family Myrtaceae by visual inspection. Inspection capacity and latent (asymptomatic) infections limit the ability to detect the rust. New molecular tests could improve detection efficiency, but the cost and the time required to process samples currently precludes their routine use in ports of entry. Interdiction, which has effectively kept coffee rust ( Hemileia vastatrix ) out of Hawaii for 120 years, offers the strongest protection for Hawaii’s native ecosystems from P. psidii . Interdiction of Myrtaceae from the continental United States could have the important supplementary benefit of preventing establishment in Hawaii of other very significant pests of multiple species of Myrtaceae that are already in the country, including: the Eugenia psyllid Trioza eugeniae (Hemiptera: Psyllidae); Chrysophtharta m-fuscum , the Eucalyptus tortoise beetle (Coleoptera: Chrysomelidae); Leptocybe invasa , the blue gum chalcid wasp (Hymenoptera: Chalcidae); and the fungal pathogens Mycosphaerella molleriana (Ascomycota: Mycosphaerelliaceae, crinkle leaf disease of Eucalyptus spp.) and Neofusicoccum parvum (Ascomycota: Botryosphaeriaceae), currently causing serious damage to Syzygium paniculatum in south Florida nurseries. Each of these pests would be likely to cause very significant damage to native and (or) cultivated Myrtaceae in Hawaii. Each of these pests is a prime candidate for transport by the foliage and (or) nursery stock pathways from Florida and California into Hawaii. Hawaii Department of Agriculture has a clear mandate to protect Hawaii’s natural environment, forestry and cultivated Myrtaceae. Principles of the World Trade Organization’s Treaty on Sanitary and Phytosanitary Measures and the International Plant Protection Convention are consistent with the right of Hawaii to take action. The current threat of P. psidii and the other five serious threats to Myrtaceae are primarily posed by the importation of infected plants from the continental United States; however, that may change in the future. If Hawaii were to decide to take a stand (through State regulation) to protect its native and introduced Myrtaceae, there is a possibility that USDA would consider Federal regulation of Myrtaceae from foreign countries.