The Brazilian peppertree seed-borne pathogen, Neofusicoccum batangarum, a potential biocontrol agent

Abstract

The invasive exotic Brazilian peppertree, Schinus terebinthifolius Raddi (Sapindales: Anacardiaceae) has become a serious threat to the delicate ecosystem of Everglades National Park in Florida, USA. More than 4000 ha in the Hole-in-the-Donut (HID) area within the park have been infested with Brazilian peppertree. Brazilian peppertree is a prolific seed producer, which enhances its invasive potential. Native phytopathogens can be a viable tool in the management of exotic species; no prior studies have reported on the occurrence of native seed-borne pathogens of Brazilian peppertree in Florida. This study showed that drupes of Brazilian peppertree are affected by seed-borne fungal pathogens. These fungal pathogens either cause germination failure or attack seedlings after germination, which results in reduced vigor or seedling death. The seed-borne fungal isolate BPSPF-1 was found to be virulent, and when inoculated it was able to kill Brazilian peppertree seedlings in seedling assays, and 1 year old saplings in greenhouse trials. Field inoculation of Brazilian peppertree branches with BPSPF-1 resulted in dieback symptoms. Host range studies on one related native species (winged sumac, Rhus copallinum) and one non-native species (mango, Mangifera indica) showed that neither was affected by girdle inoculation of stems. The BPSPF-1 isolate produced dark melanized mycelium on agar media and did not produce conidia or other fruiting structures. Based on ITS DNA sequence analyses, the isolate was identified as Neofusicoccum batangarum.

Introduction

Florida along with Gulf Lowlands is second only to Hawaii in the USA in the magnitude of invasion by non-indigenous species (Cox, 1999). Brazilian peppertree, Schinus terebinthifolius Raddi (Sapindales: Anacardiaceae) is an invasive exotic evergreen, dioecious, insect-pollinated hardwood tree species (Loope and Dunevitz, 1981, Loope, 1992) native to Argentina, Brazil, and Paraguay (Mytinger and Williamson, 1987). Introduced to the United States in the mid-1800s as an ornamental, Brazilian peppertree is currently established in California, Florida, Hawaii, Louisiana, and Texas (Hight et al., 2003, Williams et al., 2005, Cuda et al., 2006).

Brazilian peppertree is a pioneer of disturbed sites, but is also successful in undisturbed natural environments (tropical hardwood forests, pine rocklands, sawgrass marshes, and mangrove swamps) in Florida (Jones and Doren, 1997). It can be an aggressive weed that displaces native vegetation. Brazilian peppertree now covers large areas in south and central Florida, as well as many of the islands on the east and west coasts of the state. Biannual surveys of exotic organisms conducted by the South Florida Water Management District indicate that Brazilian peppertree is the most widespread exotic plant in the state – occupying more than 283,279 ha (Ferriter, 1997). It has been placed in the Category-1 of Florida’s Most Invasive Species list by the Florida Exotic Plant Pest Council because of its ability to alter the structure of terrestrial habitats and negatively impact biodiversity of native ecosystems.

A single Brazilian peppertree produces tens of thousands of single-seeded, small, fleshy, red fruits (drupes) annually between November and February, which are consumed by native birds and mammals (Ewel et al., 1982, Jones and Doren, 1997). The germination rates of seeds increase when consumed by frugivores (Panetta and McKee, 1997). Seed germination is also increased if the seed is released from the exocarps (Panetta and McKee, 1997, Tassin et al., 2007). Invasive success of Brazilian peppertree is attributed to its broad range of environmental eurytolerance (Snyder, 1999, Spector and Putz, 2006, Ewe and Sternberg, 2007) and allelopathic activity (Bennett and Habeck, 1991, Morgan and Overholt, 2005).

A significant infestation of Everglades National Park by Brazilian peppertree has occurred. Perhaps the largest and most infamous of the Everglades National Park Brazilian peppertree infestation involves an area of over 4000 ha of abandoned agricultural lands in the midst of natural subtropical ecosystems, hence the name “Hole-in-the-Donut”, (HID). Since the whole of Everglades National Park has over 40,000 ha that are affected by Brazilian peppertree, the infestation within the “Hole-in-the-Donut” is only part of a much larger issue. However, the “Hole-in-the-Donut” site has reached an almost monospecific stand stage of succession where change occurs very slowly (Loope and Dunevitz, 1981, NPS, 1998).

Eradication and management of Brazilian peppertree involves herbicides and mechanical methods (Dalrymple et al., 2003, Cuda et al., 2006). These are labor intensive and expensive (Manrique et al., 2009), and additional concerns include pollution and the effects on non-target species in the natural areas (Jones and Doren, 1997). Alternative possibilities mostly include classical insect biological control agents (Hight et al., 2003, Cuda et al., 2005, Manrique et al., 2009).

Propagule pressure (i.e. the number of propagules and the frequency of introduction events) is an important determinant of habitat invasibility of natural systems (Lockwood et al., 2005, Von Holle and Simberloff, 2005). The invasiveness of Brazilian peppertree is largely driven by its enormous reproductive potential. For management and eradication, identifying and understanding recruitment and dispersal pathways of non-native plants is critical (Davies and Sheley, 2007, Tassin et al., 2007). Evidence from various systems demonstrates that fungal pathogens can severely limit seed survival for species that recruit from persistent seed banks, and may play an important role in structuring plant populations and restricting host distributions within communities. During the course of our studies on Brazilian peppertree in Everglades National Park – “Hole-in-the-donut”, we came across the persistent occurrence of seeds infected with fungi. This contamination was observed even after following strict surface sterilization procedures. It was presumed that the fungi originated from within the seed. These results were the impetus for an effort to study Brazilian peppertree seed-borne pathogens in the Everglades National Park – “Hole-in-the-Donut”. If a large collection of seed-borne pathogens were made available, some of the selected pathogens may have the potential to be developed further as a bioherbicide system to control Brazilian peppertree.

The objectives of our study were to isolate and characterize indigenous seed-borne pathogens of Brazilian peppertree in Everglades National Park – “Hole-in-the-Donut”, Florida, screen and evaluate the pathogenicity of seed-borne pathogens in greenhouses and field, and determine the host range of seed-borne pathogen on selected non-target plant species.