A baseline analysis of the distribution, host-range, and severity of the rust Puccinia Psidii in the Hawaiian islands, 2005-2010

Abstract

Puccinia psidii was first described by Winter (1884) on guava ( Psidium guajava L.) in Brazil. The rust is still a major pest of native guava in Brazil and is often referred to as “guava rust” internationally. It is unusual among rust fungi because of its broad and ever-expanding host-range within the Myrtaceae plant family (Simpson et al . 2006). The pathogen is regarded as a major threat to Eucalyptus plantations and other Myrtaceae worldwide (Coutinho et al . 1998, Grgurinovic et al . 2006, Glen et al . 2007). Infections of leaves and meristems are particularly severe on susceptible seedlings, cuttings, young trees, and coppice, causing plants to be stunted and multi-branched, inhibiting normal growth and development, and sometimes causing death to young seedlings (Booth et al . 2000, Rayachhetry et al . 2001). The fungus has expanded its host-range in Brazil, affecting both native and introduced Myrtaceae (Coutinho et al . 1998). Since its discovery in 1884, P. psidii has continually been discovered to have an expanding host-range within the Myrtaceae, affecting hosts throughout much of South and Central America and the Caribbean. Spreading out originally from Brazil in 1884, the fungus has been reported on hosts in the following countries (first record in parentheses): Paraguay (1884), Uruguay (1889), Ecuador (1891), Colombia (1913), Puerto Rico (1913), Cuba (1926), Dominican Republic (1933), Venezuela (1934), Jamaica (1936), Argentina (1946), Dominica (1948), Trinidad and Tobago (1951), Guatemala (1968), United States (Florida; 1977), Mexico (1981), El Salvador (1987), and Costa Rica (1998) (Simpson et al . 2006). It is possible that P. psidii was present in El Salvador and Costa Rica prior to 1980, but was not reported until 1987 and 1998, respectively. Until recently, Puccinia psidii was restricted to the Neotropics, Mexico, and the state of Florida in the United States. While the rust has been present in Florida for over 30 years, only recently has it spread westward. Although possibly present earlier, P. psidii was found in California in November 2005 in a nursery in San Diego County on Myrtus communis and documented by a report in a nursery newsletter (Mellano 2006). Puccinia psidii was first found in Hawai`i on a young plant of `ōhi`a ( Metrosideros polymorpha ) in April 2005, in a nursery on the island of O`ahu (Killgore and Heu 2005; Uchida et al . 2006). The fungus subsequently spread to most islands of the Hawaiian chain, infecting `ōhi`a and other myrtaceous hosts (Hauff 2006, Anderson et al . 2007). P. psidii was first found in Japan in May 2007 on cultivated `ōhi`a (Kawanishi et al . 2009). Most recently, a rust identified as Uredo rangelii was discovered in April 2010 in New South Wales, Australia (Carnegie et al . 2010). This rust is closely related to Puccinia psidii and is part of the guava rust complex described by Simpson et al . (2006). Although treated as a separate species by Simpson et al. (2006), many authors now consider U. rangelii a synonym for U. psidii , which is the anamorph (asexual stage) of P. psidii , and therefore, the same species (Glen et al . 2007, Carnegie et al . 2010). Because of the large diversity of native Myrtaceae present in Australia, the number of Myrtaceae hosts attacked by species of the guava rust complex will likely grow now that U. rangelii has arrived and is spreading in the country. As of this writing (June 2011), 94 species of Myrtaceae have been identified as hosts of U. rangelii in the states of New South Wales and Queensland. Damage is severe on nearly one-third of the species affected, and 16 of these species are threatened or endangered native species (Secretary of Australia, May 2011). The presence of Puccinia psidii in Hawai`i is particularly alarming for at least two reasons: (1) M. polymorpha is the dominant overstory tree of the native forest, and (2) P. psidii is now established in the Pacific region, where numerous Myrtaceae species are native. Native ecosystems in Hawai`i and the Pacific could be seriously affected by the spread of P. psidii , as both native and introduced Myrtaceae are significant components of many different plant communities throughout the region (Glen et al. 2007). Because the guava rust complex (i.e., P. psidii and U. rangelii ) now attacks well over 100 species of Myrtaceae worldwide, it is currently a priority for international quarantine and import restrictions in an effort to prevent further spread among Australasian and Pacific Myrtaceae. Several different studies have been done to determine what degree of genetic variation exists between isolates of Puccinia psidii from many different host plants and many different locations (Langrell et al . 2008, Kawanishi et al . 2009, Kadooka 2010, Graça et al . 2011). So far, all of these studies have shown that all of the Hawaiian samples tested so far have had the same genetic composition. Given that the P. psidii strain in Hawai`i has continually been shown for over five years to lack genetic variation at microsatellite marker sites (which are believed to undergo relatively rapid genetic change), a baseline evaluation of incidence and severity should be especially valuable to provide comparisons with future conditions. Worldwide, 23 Neotropical species in 11 genera and 59 Australasian and Pacific species in 13 genera had been recorded as hosts of Puccinia psidii before 2010 (Simpson et al . 2006, Anderson et al . 2007). Of those 82 species known to be hosts elsewhere, 42 are cultivated or naturalized in Hawai`i. Because of its wide host-range and aggressive pathogenicity, rust disease caused by P. psidii poses a considerable disease threat to many native and cultivated Myrtaceae throughout the world (Coutinho et al . 1998, Booth et al . 2000, Simpson et al . 2006). However, there are few reports comparing the severity of rust infection on native, introduced, and cultivated Myrtaceae (Rayachhetry et al . 2001, Perez et al . 2010). Since government agencies and the public are concerned about the extent of the rust movement within and to Hawai`i (Loope and La Rosa 2008, Loope 2010), there is a need to better understand the incidence, severity, and distribution of P. psidii in Hawai`i. To address that need, this research project was initiated to survey forests, surrounding plant communities, botanical gardens, and commercial nurseries to detect the presence and severity of P. psidii rust infections throughout Hawai`i on plants in the Myrtaceae family. This study provides a baseline on the host distribution and severity to compare current and future impacts of rust infections caused by P. psidii on native, naturalized, and cultivated Myrtaceae in Hawai`i.