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Are mangroves in the tropical Atlantic ripe for invasion? Exotic mangrove trees in the forests of South Florida
Two individuals of B. gymnorrhiza, originally collected from Dago Bay, Sangihe Island, Sulawesi, Indonesia (ca. 3.38°N, 125.55°E), were planted on the edge of a 100 m long dredged canal at The Kampong in 1940 (Fairchild 1945, p 94; Sweeney 1967). These prized plants were nurtured by gardening staff. A survey in 1971 showed that one of the original trees was still alive, and six saplings were growing near the original plantings (Gillis 1971). During surveys conducted in August 2008 we identified 86 individuals of B. gymnorrhiza growing along the canal at The Kampong where the original individuals were planted in 1940 (Fig. 1c). Assuming that we identified all of the individuals in the population, the three estimates of population size from 1940, 1971 and 2008 fit to an exponential population growth model (Nt = Noert) yield a population growth rate (r) of 5.6% year-1 (R2 = 0.98).
We counted 40 B. gymnorrhiza trees and saplings at The Kampong, of which 37 were in the core plot (Fig. 2). Two B. gymnorrhiza trees were growing at the mouth of the canal where it meets Biscayne Bay, some 65 m from the core plot and another tree was at the head of the canal, 40 mdistant (Fig. 1c). There were 45 B. gymnorrhiza seedlings in the plot. The plot also contained 6 A. germinans, 27 Laguncularia racemosa and 115 R. mangle trees and saplings (Fig. 2). The majority of the B. gymnorrhiza adults and saplings were concentrated near the canal. B. gymnorrhiza seedlings, however, have spread well away from this core. Laguncularia racemosa was concentrated near the upland border of the plot whereas R. mangle was found throughout (Fig. 2). The few A. germinans were concentrated in the center of the plot along a small path that meanders through it.
Seedlings and saplings of B. gymnorrhiza and three of the native species (R. mangle, A. germinans and L. racemosa) were very abundant, with densities of 3,184 ha-1 for B. gymnorrhiza and > 5,000 ha-1 for each of the native species (Fig. 3). B. gymnorrhiza saplings (2.5 cm dbh) were more numerous than saplings of the native species in our permanent plot (Fig. 3) whereas R. mangle had the highest density in the next four larger size classes. The largest B. gymnorrhiza stem we measured was 15.1 cm dbh. The two largest stems in the plot were A. germinans, each of which was > 25.0 cm dbh (Fig. 3). Mangrove seedling densities were highly variable (Fig. 4) ranging between 0 and 9 m-2. There were no significant differences among species in density (F3, 20 = 2.09, P = 0.10). Lowest seedling densities were recorded under the B. gymnorrhiza clump and only B. gymnorrhiza seedlings were found there.
We observed prolific flowering of B. gymnorrhiza, but no fruit set or new seedlings, over the period May- October 2008. On our first surveys in May 2008, there were many B. gymnorrhiza seedlings, some with as few as two pairs of leaves above still-visible hypocotyls, evidence of seedling establishment from the previous year's reproduction, as well as numerous individuals with developing, unopened flowers. Seedlings as short as 1 m were observed with flower buds. By June 16, most of the trees in the population displayed crimson, open flowers; those flowers were concentrated on the portions of the trees receiving direct sunlight. On August 1, 2008, we carefully examined a subset of 44 individual saplings and trees for signs of flowering; 14 of the 44 examined individuals, as small as 1.4 m tall, were in flower, but we did not observe fruit or developing propagules. Flowering continued to be concentrated on trees and parts of trees exposed to direct sunlight. R. mangle individuals growing amongst the B. gymnorrhiza supported numerous 10 cm long propagules. By the time of our last survey on October 16, 2008, there were no more B. gymnorrhiza in flower, and we saw no evidence that there had been any fruit set during the entire reproductive season.
Mangroves at Fairchild Tropical Botanic Garden
Fairchild Tropical Botanic Garden (FTBG) is located near the coastline of Biscayne Bay (Fig. 1d) and the garden includes both intertidal wetland and upland plant communities. Records indicate that 129 individual members of 14 non-native species considered as true mangroves (sensu Tomlinson 1986) have been planted at FTBG since the garden opened to the public in 1938 (Table 1). Two of these taxa were only identified to the level of genus. Garden records indicate that during the last complete survey of mangrove collections in 1998, six of the original 14 taxa were still alive (Table 1). By 2008, surveys by the authors and FTBG staff revealed that five of the fourteen non-native mangrove taxa survived (Table 1). The B. gymnorrhiza individual died in the 1998-2008 interim, as evidenced by a single standing dead specimen.
Of the five non-native mangrove species that remain in the collections of FTBG, two apparently have not reproduced: Dolichandrone spathacea and Nypa fruticans. One adult specimen of R. stylosa had a dbh of 5.6 cm and had flower buds and immature fruit on the tree, while a specimen ~ 4 m from the flowering tree had a dbh of 5.1 cm and was not bearing fruit or flowers. We found no evidence of seedling or sapling R. stylosa near the two adult trees, and on a subsequent visit determined that no fruit had been produced by the one tree in flower. We found numerous seedlings under a Heritiera littoralis during our survey, but we did not observe seedlings of that species dispersing away from the adult, as the seedlings seemed to be kept in check by mowing of the lawn surrounding the parent tree.
In contrast to the other introduced species, Lumnitzera racemosa had reproduced repeatedly since introduction at FTBG. A total of fourteen Lumnitzera racemosa were planted in three different locations in FTBG's lowlands in the late 1960s to early 1970s. By 2009, at least one of the original plants still remained. At each of the three planting locations, Lumnitzera racemosa naturalized and began expanding its range and was found in densities far greater than the native mangrove species (Fig. 5). The densities of Lumnitzera racemosa saplings and trees we found were extremely high for mangrove stands, with 24,735 ha-1. However, the weighted (by density) average stem diameter was quite small, only 1.63 cm. A few larger individuals (10-20 cm dbh) were encountered but not within our plots. These stems were located along an interior pond at FTBG and were eradicated before we could quantify densities. The size frequency distributions clearly show Lumnitzera racemosa dominating the mangrove forests at this location (Fig. 1d).
Assuming exponential growth of this population, we conservatively estimate the population growth rate (r) to be between 17 and 23% year-1. The population was in flower and fruit during our first survey in November 2008, and the preponderance of seedlings and saplings (Fig. 5) in the population suggest copious reproduction. The total geographic extent of the invasion from the original locations now reaches beyond FTBG's borders into a neighboring county park. We estimate that within a span of 38- 43 years, the population expanded to dominate about 60,500 m2 of mangrove forest.
Molecular genetics of B. gymnorrhiza population at The Kampong
We genotyped 33 individuals from the Kampong population for ten microsatellite loci. Three loci were monomorphic. The remaining loci were polymorphic, six with two alleles per locus, and one with three alleles (Table 2). Observed heterozygosity for the polymorphic loci ranged from 0.000 to 0.455. Three of the seven polymorphic loci exhibited significant departure from the Hardy-Weinberg expectation. In each case the departure involved significant heterozygote deficiency (Table 2). No pairs of loci showed evidence of significant linkage disequilibrium at the level of P < 0.01. These are characteristics of a genetically depauperate population.
U.S. Department of the Interior, U.S. Geological Survey
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Last updated: 04 September, 2013 @ 02:04 PM (KP)
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