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Are mangroves in the tropical Atlantic ripe for invasion? Exotic mangrove trees in the forests of South Florida

Introduction

Abstract
>Introduction
Methods
Results
Discussion
Acknowledgments
References
Tables and Figures
The human-aided dispersal of organisms among habitats on Earth often has led to greatly altered community structure and ecosystem function (see Mack et al. 2000 for review). Some of the species that arrive in new habitats proliferate, spread and persist; such plants that do so can alter fire regimes, nutrient cycling, ecohydrology and primary productivity and can affect the abundance and threaten the survival of native species. Identifying the suite of life history characteristics that determine whether a species has the potential to become invasive in habitats outside its native range has so far been elusive, but species with close relatives in non-native ecosystems and those that have become invasive elsewhere seem likely candidates. Among the factors contributing to the invasibility of biological communities, Elton (1958) proposed that communities with low species richness should be vulnerable to invasion. Further, ecosystem disturbance may promote rapid proliferation and invasiveness of newly naturalized species (Harper 1965).

Mangrove forests dominate about 75% of the tropical coastlines in the world (Odum et al. 1982). They are valued for both the goods that can be extracted from the forests, the ecosystem services they provide (Costanza et al. 1997) and the support of coastal food webs by the detritus produced in the forests (Odum and Heald 1975; Meziane et al. 2006; Abrantes and Sheaves 2009). In South Florida, there are over 170,000 ha of mangrove forests (Odum et al. 1982). These forests are dominated by four tree species that thrive in the saline, flooded soils of the coastal zone: red mangrove (Rhizophora mangle L.), black mangrove (Avicennia germinans L.), white mangrove (Laguncularia racemosa (L.) C.F. Gaertn.) and buttonwood (Conocarpus erectus L.). The South Florida mangrove species have close relatives that occur in the mangrove forests of the Indo-Pacific: R. mangle has congeners including R. stylosa, R. mucronata and R. apiculata; and in the same family are the genera Bruguiera, Ceriops and Kandelia. A. germinans has the congeners A. marina and A. alba, among others. Laguncularia racemosa is in the same family (Combretaceae) as C. erectus and Lumnitzera, with two species in the Indo-Pacific.

The mangrove forests of the Indo-Pacific are much more diverse than those of the tropical Atlantic region (Duke 1992). The general pattern of higher diversity of mangroves, coral reefs and seagrasses in the tropical Indo-Pacific in comparison to those of the tropical Atlantic is likely the result of extinction events following the tectonic separation of the smaller tropical Atlantic region from the larger tropical Indo-Pacific region (McCoy and Heck 1976). Other mangrove tree species, notably Bruguiera spp., did occur in the Atlantic region in the past. Bruguiera-type pollen has been found in early Eocene (ca. 50 MYA) deposits in France and England as well as in Oligocene (ca. 30 MYA) sediments from England. Fossil hypocotyls resembling Bruguiera, as well as Ceriops, another genus not currently known from the tropical Atlantic, also have been found in the early Eocene London Clay flora of England (reviewed in Graham 2006). When these lineages were extirpated from the tropical Atlantic is unclear.

The structure of mangrove forests in South Florida, as in most other regions, is strongly controlled by disturbance (Smith et al. 1994, 2009). Small scale, frequent disturbances such as lightning strikes open up gaps in the canopy of forests dominated by tall, late-successional species like R. mangle, allowing for smaller species with high dispersal abilities, like Laguncularia racemosa, to persist in the forests. Larger, less frequent disturbances such as hurricanes can remove the canopy from thousands of hectares of mangrove forest in a single event, opening up space for new trees to colonize formerly dense, closed canopy forests. Mangrove forests also are disturbed by human land clearing, dredging and filling. The pervasiveness of disturbances in mangrove forests could allow newly established species to rapidly proliferate across the landscape.

Lugo (1998) suggests that established mangrove forests resist invasion by exotic species because of the challenging physical environment of mangrove forests-but this contention is based on the idea that invaders will be non-mangroves. In the modern era of human mediated long-distance plant dispersal, there is potential for mangroves from different ocean basins to invade forests following their introduction. We know of no reasons why tropical Atlantic mangrove forests should support fewer ecological niches than Indo-Pacific forests, so the current species-depauperate nature of tropical Atlantic mangrove forests may be a result of increased rate of extinction in the smaller area of the tropical Atlantic compared to the Indo-Pacific. It is reasonable to assume that, once freed from dispersal limitations by human activities, species of mangroves from the more species-rich Indo-Pacific region could survive quite well in the tropical Atlantic. There are close relatives of all of the tropical Atlantic mangrove species in the Indo-Pacific. Extinctions over the last 50 M years have led to low species richness and consequently unfilled or underutilized niches (sensu, Walker and Valentine 1984). Also, disturbances are prevalent structuring forces in mangrove forests. For these reasons, Atlantic mangrove forests may be ripe for invasion by new mangrove tree species.

Humans have a long history of importing new trees-including mangroves-for food, timber, and as ornamentals; these new species have the potential to naturalize and invade new regions. Mangrove trees flourish when deliberately introduced to tropical islands that had no native mangroves. Likely owing to isolation and the limited dispersal ability of mangrove trees, there were no native mangroves in the Hawaiian archipelago or in French Polynesia in the Pacific Ocean. In 1902, R. mangle from South Florida was introduced to the Hawaiian island of Moloka'i to stabilize the shoreline and for honey production (see citations in Chimner et al. 2006). It is likely that these mangroves spread from Moloka'i to other Hawaiian islands, as R. mangle was recorded on the neighboring island of Oahu as early as 1917. In 1922, several species of mangroves were introduced to Oahu (Chimner et al. 2006), including R. mangle and C. erectus from South Florida and Bruguiera sexangula, Bruguiera parvifolia, Ceriops tagal and Rhizophora mucronata from the Philippines (Allen 1998). Of the Philippine species, only B. sexangula is known to persist in Hawaii; it has spread very little from its original planting sites, being known from only four sites on Oahu (Allen 1998). On the other hand, the species introduced from South Florida have been very successful. C. erectus is commonly used as an ornamental in Hawaii and has escaped cultivation. R. mangle has spread throughout the archipelago and has now colonized all but two of the Hawaiian Islands. On Oahu, the range of mangroves continues to expand 90 years after their introduction. The expanding mangrove forests have negatively impacted at least one endangered species, the Hawaiian stilt, a mudflatfeeding bird (Allen 1998). Rhizophora stylosa was introduced to Moorea, French Polynesia in 1937, with the intention of providing oyster culture habitat on the prop roots. A few propagules were introduced to one bay, but mangroves are now established around Moorea and on some nearby islands. These mangroves have replaced salt grass (Paspalum vaginatum) marshes and colonized mud flats, leading to efforts to control their spread (Langer and Lipps 2006).

Humans have introduced non-native mangrove species to areas with native mangroves as well. Nonnative Sonneratia caseolaris and S. apetala were introduced for timber production to a mangrove forest in Shenzen Bay, China in 1993. The species could sexually reproduce and individuals dispersed, but appeared to be inferior competitors to native species. As a result, Sonneratia spp. had limited impact on the structure of Shenzen Bay's mangrove forests (Zan et al. 2003). In Bangladesh, Biswas et al. (2007) documented five non-native mangrove species that have naturalized in the Sundarbans mangrove forest. Lumnitzera racemosa, R. mangle, Bruguiera gymnorrhiza and Xylocarpus granatum have been planted in Tonga as part of land reclamation/stabilization efforts. Lumnitzera racemosa has been reported to be well-established there (Clarke and Thaman 1993). These examples show that mangrove forests can indeed be invaded by newly introduced tree species.

As with the cases in Hawaii, China, Bangladesh and Tonga, South Florida has also experienced its share of exotic mangrove introductions. We focus on the introductions of B. gymnorrhiza (L.) Savigny and Lumnitzera racemosa Willd. as case studies. Members of Bruguiera have showy, ornamental flowers. In Hawaii, flowers of the introduced Bruguiera sexangula are used in the production of flower leis (Allen 1998). B. gymnorrhiza, native to the region ranging from eastern Africa to SE Asia and the Pacific Ocean islands, has attractive, large (ca. 2.5 cm diameter) red flowers, making it a candidate for planting as an ornamental tree. Indeed, the early twentieth century plant explorer David Fairchild sought out specimens of B. gymnorrhiza from Indonesia to plant in the intertidal zone at his house in Miami, Florida, USA. He wrote in his memoirs that he was anxious for the two trees he planted in 1940 to be successful and to spread throughout the region: "If they fruit, perhaps some day they will brighten our coasts with their flowers" (Fairchild 1945, p 94). His Miami house, known as "The Kampong," became a botanical garden in 1984, and as a result there is an historical record of the status of these introduced mangrove trees. Today, the progeny of the trees he planted have begun to expand and fulfill Fairchild's vision of red-flowered mangroves in Biscayne Bay, Florida. Further, during the twentieth century, many more mangrove specimens from around the world, including other B. gymnorrhiza, were planted a few kilometers from The Kampong at Fairchild Tropical Botanic Garden (FTBG) in Coral Gables, Florida. Lumnitzera racemosa was planted as part of the living collections at FTBG in 1966 and 1971. The intentional introduction of these species, with the carefully collected records about their status through the years, has provided us with an opportunity to assess the likelihood that these species would spread further in the region and become invasive, and to ask whether these populations may have exchanged gametes or received gametes from another as yet unidentified source population.


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