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

Discussion

Abstract
Introduction
Methods
Results
>Discussion
Acknowledgments
References
Tables and Figures
At least two species of Indo-Pacific mangroves (B. gymnorrhiza and Lumnitzera racemosa) have naturalized and spread in the mangrove forests of South Florida, showing that Atlantic mangrove forests are indeed susceptible to invasion. The two species we focus on were introduced and nurtured in botanic gardens, anthropogenically modified and disturbed environments in South Florida. These results emphasize the need for vigilance by those who may introduce and cultivate such species.

Bruguiera gymnorrhiza and Lumnitzera racemosa are likely to continue to invade mangrove forests if they are introduced to the tropical Atlantic region. In fact, both species have been recognized as having a high but unproven potential to become invasive (Allen and Duke 2006). The success of these particular species in South Florida, despite the presence of native mangrove competitors, is likely a consequence of the similar environments in tropical American and Indo-Pacific mangrove forests, the close taxonomic relationships between the invaders and native taxa, the species-depauperate flora of tropical American mangroves compared to the Indo-Pacific, and the prevalence of disturbance in the introduction sites. Further, given that these conditions are common to the entire tropical Atlantic coast, it is likely that the mangrove forests in the entire region are susceptible to invasion by Indo-Pacific mangroves.

It has been noted that plants with broad natural ranges that include both Africa and Asia are much more likely to naturalize in new areas compared to species with more limited distributions (Pemberton and Liu 2009). Both B. gymnorrhiza and Lumnitzera racemosa have quite extensive native ranges, suggesting that they have broad environmental tolerances and great dispersal abilities. B. gymnorrhiza has the broadest natural range of all mangrove species, from East Africa to Polynesia and as far north as Ryukyu Island (ca. 26°N, Tomlinson 1986). Lumnitzera racemosa is found from East Africa to the western Pacific islands of Fiji and Tonga, tropical Australia, and Indo-China (Tomlinson 1986). The broad native ranges lend further support to the idea that these species will do well in the mangrove habitats of tropical America if individuals disperse from their current restricted distributions.

In addition to having broad ranges, both B. gymnorrhiza and Lumnitzera racemosa are capable of establishing and growing in a wide range of environmental conditions. For example Bruguiera sp. are routinely found in both non-tidal, freshwater Melaleuca swamps and Eleocharis marshes found upstream in estuaries in northeastern Queensland, Australia (TJS, personal observation). Presumably storm surges carried propagules into these locations, and once there, they survived, and it is possible that this species could become established in the Eleocharis marshes of the Everglades. We also found Lumnitzera racemosa thriving in a non-tidal freshwater pond at FTBG and in a high salinity swale north of the garden.

Populations of both introduced species have sizefrequency distributions strongly skewed to very young individuals (Fig. 3, Fig. 5), consistent with rapidly expanding populations. The aggressiveness of the growth rate of the two exotic populations differed. The B. gymnorrhiza population was founded by only two individuals and therefore had very low genetic diversity. While we have not yet surveyed the genetic diversity of the Lumnitzera racemosa population, given that it was founded by many more individuals introduced over a 5 year period, it is likely to have greater genetic diversity than B. gymnorrhiza. Further, B. gymnorrhiza produces fewer, larger propagules per parent compared to Lumnitzera racemosa, which has more weedy life history characteristics.

Both Brugiuera gymnorrhiza and Lumnitzera racemosa have perfect flowers and are self-compatible (Tomlinson 1986), so that even a single individual of either species has the ability to produce seeds and fruit in isolation. The conspicuous red flowers of B. gymnorrhiza are pollinated mostly by birds in its native range (Tomlinson 1986). The lack of successful fruit set in B. gymnorrhiza during 2008 may have been due to lack of pollinators, or to some environmental condition not conducive to reproduction. The sporadic nature of successful reproduction in South Florida may have limited the rate of growth of this population. Seeds of B. gymnorrhiza, like those of the native R. mangle, germinate while still attached to the parent tree; these germinated propagules fall from the parent and are dispersed by water. The population of B. gymnorrhiza at The Kampong is adjacent to a short (100 m long) canal that opens into Biscayne Bay (Fig. 1c); we documented that B. gymnorrhiza seedlings dispersed ca. 50 m in either direction along the canal from the original planting location. We assume that propagules of this species have been released into the Bay for at least 50 years. Given that propagules of Bruguiera sp. are viable after floating for at least 60 days (Allen and Krauss 2006), it is very likely that B. gymnorrhiza is established in other mangrove stands in northern Biscayne Bay. In contrast to B. gymnorrhiza, the smaller white flowers of Lumnitzera racemosa are pollinated by a number of insects including wasps, bees, butterflies and moths (Tomlinson 1986). The smaller ungerminated seeds of Lumnitzera racemosa fall from the parent, and since they float, they can be dispersed by water (Tomlinson 1986). At FTBG, Lumnitzera racemosa was planted in areas with no regular connection to the open water of Biscayne Bay, and it appears that for now the expansion of Lumnitzera racemosa has been limited to the back mangrove environment of the network of mosquito control ditches surrounding FTBG (Fig. 1d). However, given the frequency of hurricanes in the region and importance of hurricanes in driving the dynamics of mangrove recruitment in South Florida (Smith et al. 1994, 2009), if left unchecked, it is likely that Lumnitzera racemosa seeds will soon spread beyond the back mangrove environment. And, given the small size of first reproduction and the numerous seeds produced by this species, its spread will likely be extremely rapid.

Both of the exotic mangrove populations we studied occur in areas supporting native mangrove species; the expansion of these populations suggests that the exotic mangroves can indeed compete with native species. Studies in Indo-Pacific countries where Bruguiera and Rhizophora co-occur suggest that species in these genera have similar environmental requirements, and that the competitive hierarchy between the genera changes depending on local conditions. In one case, Ye et al. (2004) found that B. gymnorrhiza seedlings grow faster in the lower intertidal than the high intertidal, but survivorship was lower in the lower intertidal because of physical disturbance. In another study, B. gymnorrhiza seedlings were found to have the lowest tolerance to flooding compared to three other mangrove species in China, which corresponds to the zonation of the mangrove forest there (He et al. 2007). In Hawaii, where both species are introduced, Bruguiera occurs higher in the intertidal than R. mangle, but the comparatively high shade tolerance of Bruguiera seedlings allows them to become established in R. mangle stands (Allen and Krauss 2006). Once established, R. mangle seedlings grow faster than Bruguiera sexangula seedlings under a wide variety of light and salinity conditions, but R. mangle is more tolerant of high salinity environments. Bruguiera seemed to have a slow-growth, tolerance strategy compared to R. mangle in Hawaii (Krauss and Allen 2003a).

The net effect of a change in disturbance regime on the success of B. gymnorrhiza populations is unclear. In a mixed-species mangrove forest in Micronesia, B. gymnorrhiza seedlings were more abundant than other species in both natural and anthropogenic light gaps as well as under the undisturbed canopy, despite the species composition of the canopy surrounding the gap, suggesting that species composition may shift towards B. gymnorrhiza if disturbance increases (Pinzon et al. 2003). Conversely, Imai et al. (2006) found that low levels of disturbance, and therefore low light levels reaching the forest floor, exclude seedlings of species that require high light levels, leading to dominance of the forest by B. gymnorrhiza, which has very shade-tolerant propagules.

Differences in herbivory and seed predation among native and introduced species may partially regulate competition among the species and help explain the distribution of mangrove species in the intertidal zone (Smith 1987). Seed predation can be high in mangroves and suppress seedling establishment, but seedlings of B. gymnorrhiza were less heavily predated than other common mangrove species in forests in Northern Australia (Clarke and Kerrigan 2002). In contrast, Bosire et al. (2005) found that Bruguiera propagules on the floor of a replanted Rhizophora forest were preyed upon at a greater rate than the propagules of the dominant canopy species. Krauss and Allen (2003b) found that seedling success of B. gymnorrhiza was high under a broad range of tidal, light and salinity conditions and herbivory did not exert control over seedling survivorship in Kosrae, part of Micronesia. The importance of seed predation in controlling seedling success rate may be determined by whether the species are in their native ranges, with specialized seedling predators, or not. Predation on propagules of R. mangle is lower on Hawaii than in areas with native mangrove forests, and the lower predation has been hypothesized to be a result of the lack of nonindigenous propagule predators and a facilitator of rapid spread of this species in the Hawaiian Islands (Steele et al. 1999). Similarly, we expect that seedling predation should be more severe for R. mangle than for introduced B. gymnorrhiza in South Florida, but this hypothesis remains to be tested. Such a difference in seed predators may partially explain why B. gymnorrhiza has been able to colonize the mangrove forest at The Kampong.

Outside of their native ranges, some plant species develop unusual stand structure and density compared to their native ranges (as observed for Schinus terebinthifolius and Melaleuca quinquenervia in South Florida, Gordon 1998). In Hawaii, R. mangle has very high rates of net production and very high stem density compared to that measured in its native range. This is attributed to lack of competition with other woody plants and lack of herbivory on trees and propagules (Cox and Allen 1999). It is possible that either B. gymnorrhiza or Lumnitzera racemosa could behave similarly in the tropical Atlantic because of release from native competitors and predators.

Mangrove distributions tend to have pole-ward limits set by wintertime low temperatures, with varying degrees of cold tolerance among species. In South Florida, severe cold fronts can cause widespread mortality of native mangroves (Lugo and Zucca 1977). And, planting records from the Kampong and FTBG suggest that South Florida may be a marginal environment for B. gymnorrhiza, since the death of cultivated specimens was recorded following abnormal cold periods (Gillis 1971). It may be that the relatively pole-ward, subtropical climate of South Florida has limited the longevity of individual B. gymnorrhiza trees and therefore the rate of population growth. However, in the current situation of increasing global temperatures, the pole-ward extent of mangroves in general (Stevens et al. 2006), and B. gymnorrhiza in Florida in particular, is likely to increase.

Despite the very low genetic diversity of the B. gymnorrhiza population at The Kampong, the population has expanded since its planting in 1940 and we found no evidence of pollen exchange between the population at The Kampong and the specimens cultivated a few kilometers away at FTBG. Planting records indicate that two trees may have founded the population of B. gymnorrhiza at The Kampong almost 70 years ago. If this is the case, we would expect to see a limited number of alleles per locus (maximum of 4). We would also expect reduced heterozygosity relative to natural populations as a result of this bottleneck. This reduction in heterozygosity would be intensified by genetic drift in this small founding population over time, and by inbreeding. Results from our analyses of ten microsatellite markers are consistent with this historical record. A single locus has three alleles; all remaining loci possess 1 or 2 alleles. This is consistent with a population founded by as few as two individuals. Four of the loci that are variable in the native-range populations are fixed in The Kampong population, and four more have reduced heterozygosity compared to native-range populations. For the three loci that significantly deviate from the Hardy-Weinberg expectation, the deviation is a heterozygote deficit, again consistent with inbreeding and drift in a small population. It is also possible that some of the deviation from Hardy-Weinberg expectations may result from the presence of null alleles for these loci (Islam et al. 2006). Inbreeding and self fertilization have been previously reported in mangrove species (Maguire et al. 2000; Chen et al. 1996; Nunez-Farfan et al. 2002), so this may prove to be an adaptation of mangroves for colonizing new habitats.

Given the recognized importance of the mangroves of the tropical Atlantic to the functioning of the coastal seascape, the ecosystem functioning of the region's mangrove forests may change as a consequence of invasive species. In the 1970s, Avicennia marina from the south Pacific was introduced into a salt marsh on Mission Bay, in San Diego, southern California, USA in order to provide specimens for plant physiology research (Jeff Crooks, personal communication, Tijuana River National Estuarine Research Reserve). Despite eradication attempts, this mangrove persists and its population is expanding. The invasion of the salt marsh by mangroves caused changes in nitrogen cycling in the sediments (Moseman et al. 2009). The cycling of the detrital material produced by mangrove forests, essential to coastal food webs in South Florida, may be altered by the presence of B. gymnorrhiza and Lumnitzera racemosa. An analysis of food web structure in the introduced R. mangle forest in Hawaii using stable isotopes suggests that mangrove detritus does not get assimilated in the food web, in contrast to a native R. mangle forest in Puerto Rico (Demopoulos et al. 2007). This suggests that the establishment of mangroves on the mudflats was not necessarily an enhancement of the ecosystem services provided by the previously existing mud flats of Hawaii, since the mangrove carbon was not efficiently taken up by Hawaiian marine food webs. Other introduced species in mangroves in South Florida have indeed caused changes in ecosystem functioning. S. terebinthifolius, the Brazilian pepper, was introduced to Florida in the 1840s, but it was not recognized as an aggressive invasive plant until surveys in the 1950s found it to be increasing in density in Everglades National Park. Today, it is found in both disturbed and undisturbed tropical hardwood forests, pine rocklands, sawgrass marshes and mangroves across South Florida (Jones and Doren 1997). S. terebinthifolius is not a true mangrove, but an opportunistic species that produces noxious secondary compounds that depress the growth rate of seedlings of R. mangle and A. germinans (Donnelly et al. 2008); it severely affects the habitat value of the systems it invades because of the dense tangle of vegetation and the toxic secondary compounds (Doren and Jones 1997, Gordon 1998).

The observations we report here may be cause for concern, both for managers of coastal environments in the tropical Atlantic, as well as for directors and staff of botanical gardens. Species of mangroves from the Indo-Pacific region have become established in South Florida, and these established populations are producing propagules and seeds that are capable of being widely distributed by nearshore currents to large parts of the tropical Atlantic. The consequences of the invasion of tropical Atlantic ecosystems by these species are unclear, but a precautionary approach may be in order, in light of the myriad examples of ecosystem disruption by introduced plant species. To be cautious, managers of botanical gardens could periodically revisit their collection policies, especially when collecting and planting exotic species in a matrix of related native species. Further, care could be taken to communicate with the managers of neighboring natural areas and to prevent the spread of propagules outside the confines of the botanic garden, either by normal conditions or by extreme weather events. In order to limit the spread of such invasive mangrove species, it would be necessary to conduct broader surveys of areas that could have potentially been reached by water-dispersed propagules.

Plant explorers and botanic gardens have long been aware of the problem of weediness and the importance of quarantining candidate plants prior to their introduction to ensure the new plantwould not become a pest in the new environment (Fairchild 1898). Yet, itwas not until the 1990s when policies truly began to change. In the case studies we discuss, both gardens are taking action to address the spread of non-native mangroves. FTBG has already removed Lumnitzera racemosa from its collections and is currently cooperating with other land management agencies to eradicate the species from garden's vicinity. Indeed, the Voluntary Codes of Conduct for Botanic Gardens and Arboreta (http://www.centerforplantconservation.org/invasives/gardensN.html), which both gardens have endorsed, lays out sound practices to help stem the spread of invasive plant species.


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