Brazilian Peppertree: a Poster Child for Which Is Known to Promote the Invasion of Invasive Plants in Florida Alien Species (Hobbs and Huenneke 1992)

Home , Calophya, Schinus terebinthifolia, Tecmessa (moth)

Brazilian peppertree: a poster child for which is known to promote the invasion of invasive plants in Florida alien species (Hobbs and Huenneke 1992). Secondly, Florida‟s depauperate native flora V. Manrique, University of Florida (Ewel 1986) may exert low „biotic J. P. Cuda, University of Florida resistance‟ - the ability of native W. A. Overholt, University of Florida communities to resist invasion (Lodge 1993; Maron and Vilà 2001). Finally, huge Invasive plants in Florida numbers of exotic plants are continually The growth in global trade has being brought into Florida, the vast majority resulted in unprecedented movement of of which are intentionally introduced plants and animals outside of their native through the ornamental plant trade ranges (di Castri 1989; Pimental 2011). The (Reichard and White 2001). Thus, majority of introductions of alien species opportunities for invasion into Florida may have little impact on native ecosystems, but simply be elevated due to constant, high a few species become established in natural propagule pressure (Simberloff 1997). areas and threaten native biodiversity, alter ecological processes, and often have severe Brazilian peppertree economic consequences (Mack et al. 2000). Schinus terebinthifolia Raddi Invasive plants are estimated to cost the (Anacardiaceae), commonly referred to as U. S. economy $123 billion per year (U.S. Brazilian peppertree, is a plant of South Department of Interior 2009). America origin characterized by having In the continental USA, Florida shiny alternate compound leaves and multi- stands out as the recipient of the most exotic stemmed branches that often form an plant invaders (U.S. Congress 1993; impenetrable tangle (Cuda et al. 2006). This Simberloff 1997), with 1421 non-native species is native to Brazil, Argentina and species growing outside of cultivation Paraguay (Barkley 1944; 1957). In the U.S., (Wunderlin and Hansen 2008), and infesting Brazilian peppertree occurs in Florida, an estimated 1.0 million acres (Lee et al. Texas, Alabama, California and Hawaii 2009). Florida‟s elevated susceptibility to (EDDMapS 2012). Records indicate that invasion likely stems from several factors, Brazilian peppertree was imported into including a highly disturbed environment, Miami in 1898 and 1899 (Morton 1978), and

1 later into Punta Gorda by Dr. George Stone followed by an exponential growth phase, or around 1926 (Nehrling 1944). Recent be a reflection of the time required for the molecular studies support the historical selection of genotypes adapted to novel record. Two genetic types of Brazilian environments encountered in an introduced peppertree have been identified in Florida range (Mack et al. 2000; Sakai et al. 2001; (referred to as A and B), and since their Crooks 2005). Mukherjee et al. (2012) arrival, they have extensively hybridized speculated that the lag period was due in (Williams et al. 2005; 2007). The western A part to genetic adaptations and evolution that haplotype was introduced into Punta Gorda followed hybridization of the two genetic from southeastern Brazil, and the eastern B types that invaded Florida. Ecological niche haplotype was introduced into Miami from modeling suggests that one trait which may northern Brazil near Salvador, Bahia have evolved since the introduction of (Williams et al. 2005; Mukherjee et al. Brazilian peppertree, is cold tolerance. This 2012). These two source populations of trait may be responsible for recent Florida‟s hybrid trees are separated by northward spread of Brazilian peppertree in approximately 800 km in Brazil, and thus, Florida and into southern Alabama have not had the opportunity to hybridize in (EDDmapS 2012; Mukherjee et al. 2012). the native range. Florida‟s hybrid trees are therefore genetically distinct from trees that Impacts in Florida occur in the native range. According to Brazilian peppertree is considered to Geiger et al. (2011), Florida hybrids have be one of the most serious invasive plants in higher survival, growth rates, and produce Florida (Schmitz et al. 1997) and is more biomass than the parental plants when classified as a Category I invasive plant grown together in a common garden. species by the Florida Exotic Plant Pest There was a long lag period, perhaps Council (FLEPPC 2011). Rodgers et al. 50-60 years, between the time that Brazilian (2012) estimate that ~283,000 hectares of peppertree was first introduced into Florida, south and central Florida are invaded by and the time it was recognized as invading Brazilian peppertree, including disturbed natural ecosystems (Morton 1978). Lag sites (e.g., canal banks, fallow farmlands), times may be caused by slow population and natural communities (e.g., pinelands, growth during initial stages of introduction hardwood hammocks and mangrove forests)

(Cuda et al. 2006). Several attributes may (Diaprepes abbreviatus), a serious pest of contribute to its invasiveness, including a citrus in Florida and California (McCoy et large number of fruits produced per female al. 2003). Furthermore, Brazilian peppertree plant, an effective mechanism of dispersal is contributing to and benefiting from the by birds (Panetta and McKee 1997), establishment of the black spiny-tailed tolerance to shade (Ewel 1978), fire (Doren iguana (Ctenosaura similis (Gray)) in et al. 1991), and drought (Nilson and Muller southwest Florida (Jackson and Jackson 1980a), allelopathic effects on neighboring 2007). plants (Gogue et al. 1974; Nilson and Muller In addition to the ecological impacts, 1980b; Morgan and Overholt 2005; Brazilian peppertree presents a health risk to Overholt et al. 2012), and tolerance to saline humans. Like most other members of the conditions (Ewe 2001; Ewe and Sternberg Anacardiaceae family, Brazilian peppertree 2002). The invasion and displacement of contains active alkenyl phenols (e.g. native species by Brazilian peppertree poses urushiol, cardol), which can cause contact a serious threat to biodiversity in many dermatitis and inflammation to sensitive ecosystems in Florida (Morton 1978; Cuda individuals (Tomlinson 1980). Moreover, et al. 2006). Several studies have shown individuals may experience respiratory that Brazilian peppertree contributes to other problems such as chest pains, acute invasive species problems, a phenomenon headaches, eye irritation, and flu-like referred to as „invasional meltdown‟ symptoms when in close proximity to the (Simberloff and Van Holle 1999). For plants. Direct contact with the plant sap may instance, Clouse (1999) showed that leaf- result in a rash followed by intense itching. litter under Brazilian peppertree plants Ingesting the bark, leaves, and fruits can be growing in the previously farmed land toxic to humans, mammals, and birds known as Hole-in-the-Donut area of the (Morton 1978). Thus, the continuous Florida Everglades serves as a safe refuge increase of Brazilian peppertree infestations for some exotic ants that would otherwise coupled with its allergenic properties could not have gained such a strong foothold in negatively affect the multi-billion dollar this native habitat. Brazilian peppertree has tourist industry in Florida (Smith and Brown also been reported as an alternate host and 1994). reservoir for the exotic root weevil

Management Biological control Mechanical methods, such as cutting, Classical biological control involves burning and flooding, and herbicide the introduction of host-specific natural application are commonly used in enemies from a weed‟s native range to combination for controlling Brazilian reduce populations in the introduced range, peppertree in Florida (Gioeli and Langeland under the premise that the invader became 1997; Langeland 2001). For example, cut- aggressive due to escape from its natural stump treatments or basal bark applications enemies (enemy release hypothesis) of triclopyr can effectively control Brazilian (Williams 1954; Harris 1998; van Driesche peppertree (Langeland and Stocker 2001). and Bellows 1996; Keane and Crawley However, these methods are unsuitable for 2002). Brazilian peppertree provides an some natural areas (e.g., mangrove forests) illustration of this concept. Surveys in because of their potential for negative Florida in the 1980s identified several effects to non-target species (Doren and generalist insect herbivores, but damage to Jones 1997). Both chemical and mechanical Brazilian peppertree was minimal (Cassani control measures have been used with some 1986; Cassani et al. 1989). In contrast, success, but maintenance programs are surveys conducted in South America have required to prevent regrowth (Koepp 1978). revealed a high diversity of specialized In addition, these methods are labor natural enemies (Bennett et al. 1990; intensive and costly, particularly for large Bennett and Habeck 1991; Habeck et al. infestations. A pilot restoration project to 1994; Cuda et al. 2006; McKay et al. 2009), remove 24.4 ha of Brazilian peppertree from several of which may have potential for Hole-in-the-Doughnut in the Everglades biological control. However, none have yet National Park was completed at a cost of been released. Research on a defoliating $640,000 (Doren et al. 1990). However, it sawfly that was shown to be highly host was calculated that it would cost $20 million specific to Brazilian peppertree (Medal et al. and take 20 years to restore the entire 2000 1999; Cuda et al. 2005), was halted after the ha parcel of the Hole-in-the-Doughnut larvae were found to contain compounds (Doren et al. 1990). toxic to mammals (Dittrich et al. 2004), and possibly birds. Other candidate agents performed poorly on Florida Brazilian

4 peppertree (Manrique et al. 2008; Cuda et al. competitive ability and reproduction of 2012) or were shown to feed on related non- Florida‟s Brazilian peppertrees, resulting in target plants during quarantine studies reduced weed populations in the field. (Davis et al. 2011; Oleiro et al. 2011; Wheeler et al. 2011; McKay et al. 2012). Lessons learned and future directions Despite the lack of success in biological control of Brazilian peppertree, Brazilian peppertree illustrates many the future appears promising. Research on of the general concepts of invasive plant two candidate agents, a defoliating tortricid ecology. Similar to the majority of invasive moth, Episimus unguiculus Clarke (Martin plants, Brazilian peppertree was introduced et al. 2004) and a stem boring weevil and popularized as an ornamental. The low Apocnemidophorus piptzi (Faust), has been level of insect herbivory of Brazilian completed and petitions for their field peppertree in Florida supports the „enemy release are pending approval of the United release hypothesis‟ (Williams 1954; Keane States Department of Agriculture. and Crawley 2002), and provides a Additionally, recent exploration in Brazil theoretical basis for the search for biological has identified promising new natural control agents in the native range. enemies, including a thrips, Hybridization has been implicated in the Pseudophilothrips ichini Hood, and a group aggressiveness of Brazilian peppertree in of gall forming psyllids in the genus Florida (Mukherjee et al. 2012), and appears Calophya (Burckhardt et al. 2011; Christ et to be a common thread in many plant al. 2012). The thrips feed gregariously on invasions (Ellstrand and Schierenbeck growing shoot tips and flowers, preventing 2000). The lag period between the new growth and causing flower abortion introduction of Brazilian peppertree, and its (Cuda et al. 2006; Mound et al. 2010). recognition as invasive, is also a common Psyllids in the genus Calophya are highly feature of invasion ecology (Kowarik 1995; host-specific (Burckhardt and Basset 2000), Crooks 2005), and likely is a result of and form pit-galls in plant foliage causing hybridization followed by natural selection growth abnormalities and eventual leaf drop of genetic types well-adapted to Florida‟s (Downer et al. 1988). If released, these environment (Mukherjee et al. 2012). natural enemies may decrease the Finally, growing evidence of positive

5 interactions between Brazilian peppertree weed risk assessment would go a long way and other exotic species (Clouse 1999; in decreasing future problems with invasive McCoy et al. 2003; Jackson and Jackson plants (Gordon et al. 2008). 2007) provides support for the invasional In addition to these regulatory meltdown hypothesis proposed by Simberoff measures, more effort should be directed and Van Holle (1999). towards educating the public about the threats of invasive plants, and invasive A practical question is: What lessons species in general. The demand for novel can be gained from the experiences with plants may decline if people were more Brazilian peppertree that could be applied to aware of the environmental and economic the management of other invasive species? costs associated with invasive species. It is One is certainly the difficulty of managing encouraging that a survey of consumers at an exotic plant once it becomes firmly the Philadelphia Flower Show in 2004 established over a large geographic area. revealed that a majority (>80%) of Thus, a primary objective of invasive plant respondents were aware that exotic plants management should be the avoidance of were used in landscapes, and that some future problems through regulatory methods exotic plants cause problems in natural that limit the arrival of new, potentially areas. In Minnesota, Yue et al. (2011) found invasive plants. Historically, with the that consumers would be willing to pay a exception of a few plants included on the premium for plants labeled as non-invasive Federal Noxious Plant List (the majority of or native, suggesting that new labeling which are already in the U.S.A), all that was regulations could curb the demand for required to introduce plants or seeds was invasive and potentially invasive plants. evidence that they were not infested with Finally, biological control provides plant pathogens or pest insects the only sustainable and economically (USDA/APHIS 2012). This has changed feasible solution to the Brazilian peppertree slightly with recently enacted NAPPRA problem in Florida. Biological control has a (Not Authorized Pending Pest Risk long history of success in the regulation of Analysis) regulations, which in 2011 invasive species worldwide (Hartley 1990; established a new category of plants which Julien and Griffith 1998; Grevstad 2006; cannot be imported prior to the completion Tipping et al. 2009), and in some of a risk analysis. Properly administered

6 ecosystems, such as natural areas and aquatic habitats, biological control may be the only viable management option. Even though no biological control agents have been released against Brazilian peppertree, much has been learned about its genetics, ecology, distribution and natural enemies, and the future is promising.

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