ISSN 1387-3547, Volume 12, Number 8
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ISSN 1387-3547, Volume 12, Number 8 This article was published in the above mentioned Springer issue. The material, including all portions thereof, is protected by copyright; all rights are held exclusively by Springer Science + Business Media. The material is for personal use only; commercial use is not permitted. Unauthorized reproduction, transfer and/or use may be a violation of criminal as well as civil law. Biol Invasions (2010) 12:2509–2522 Author's personal copy DOI 10.1007/s10530-009-9660-8 ORIGINAL PAPER Are mangroves in the tropical Atlantic ripe for invasion? Exotic mangrove trees in the forests of South Florida James W. Fourqurean • Thomas J. Smith III • Jennifer Possley • Timothy M. Collins • David Lee • Sandra Namoff Received: 4 August 2009 / Accepted: 13 November 2009 / Published online: 28 November 2009 Ó Springer Science+Business Media B.V. 2009 Abstract Two species of mangrove trees of Indo- Molecular genetic analyses confirm very low genetic Pacific origin have naturalized in tropical Atlantic diversity, as expected from a population founded by mangrove forests in South Florida after they were two individuals. The maximum number of alleles at any planted and nurtured in botanic gardens. Two Brugui- locus was three, and we measured reduced heterozy- era gymnorrhiza trees that were planted in the intertidal gosity compared to native-range populations. Lumnitz- zone in 1940 have given rise to a population of at least era racemosa was introduced multiple times during the 86 trees growing interspersed with native mangrove 1960s and 1970s, it has spread rapidly into a forest species Rhizophora mangle, Avicennia germinans and composed of native R. mangle, A. germinans, Lag- Laguncularia racemosa along 100 m of shoreline; the uncularia racemosa and Conocarpus erectus and now population is expanding at a rate of 5.6% year-1. occupies 60,500 m2 of mangrove forest with stem densities of 24,735 ha-1. We estimate the population growth rate of Lumnitzera racemosa to be between 17 & J. W. Fourqurean ( ) Á T. M. Collins Á D. Lee Á and 23% year-1. Populations of both species of natu- S. Namoff Department of Biological Sciences, Florida International ralized mangroves are dominated by young individuals. University, Miami, FL 33199, USA Given the long life and water-dispersed nature of e-mail: jim.fourqurean@fiu.edu propagules of the two exotic species, it is likely that they have spread beyond our survey area. We argue that the J. W. Fourqurean Marine Science Program and Southeast Environmental species-depauperate nature of tropical Atlantic man- Research Center, Florida International University, grove forests and close taxonomic relatives in the more North Miami, FL 33181, USA species-rich Indo-Pacific region result in the suscepti- bility of tropical Atlantic mangrove forests to invasion J. W. Fourqurean Á J. Possley Á S. Namoff Center for Tropical Plant Conservation, Fairchild Tropical by Indo-Pacific mangrove species. Botanic Garden, 11935 Old Cutler Rd, Miami, FL 33156, USA Keywords Botanic gardens Á Bruguiera Á Lumnitzera Á Forest structure Á Population genetics T. J. Smith III Southeastern Ecological Science Center, United States Geological Survey, 600 4th St. S, St. Petersburg, FL 33701, USA Introduction T. M. Collins Division of Environmental Biology, National Science The human-aided dispersal of organisms among Foundation, Arlington, VA 22230, USA habitats on Earth often has led to greatly altered 123 2510 Author's personal copy J. W. Fourqurean et al. community structure and ecosystem function (see smaller tropical Atlantic region from the larger Mack et al. 2000 for review). Some of the species that tropical Indo-Pacific region (McCoy and Heck arrive in new habitats proliferate, spread and persist; 1976). Other mangrove tree species, notably Brugui- such plants that do so can alter fire regimes, nutrient era spp., did occur in the Atlantic region in the past. cycling, ecohydrology and primary productivity and Bruguiera-type pollen has been found in early can affect the abundance and threaten the survival of Eocene (ca. 50 MYA) deposits in France and England native species. Identifying the suite of life history as well as in Oligocene (ca. 30 MYA) sediments from characteristics that determine whether a species has the England. Fossil hypocotyls resembling Bruguiera,as potential to become invasive in habitats outside its well as Ceriops, another genus not currently known native range has so far been elusive, but species with from the tropical Atlantic, also have been found in close relatives in non-native ecosystems and those that the early Eocene London Clay flora of England have become invasive elsewhere seem likely candi- (reviewed in Graham 2006). When these lineages dates. Among the factors contributing to the invasibil- were extirpated from the tropical Atlantic is unclear. ity of biological communities, Elton (1958) proposed The structure of mangrove forests in South Flor- that communities with low species richness should be ida, as in most other regions, is strongly controlled by vulnerable to invasion. Further, ecosystem disturbance disturbance (Smith et al. 1994, 2009). Small scale, may promote rapid proliferation and invasiveness of frequent disturbances such as lightning strikes open newly naturalized species (Harper 1965). up gaps in the canopy of forests dominated by tall, Mangrove forests dominate about 75% of the late-successional species like R. mangle, allowing for tropical coastlines in the world (Odum et al. 1982). smaller species with high dispersal abilities, like They are valued for both the goods that can be Laguncularia racemosa, to persist in the forests. extracted from the forests, the ecosystem services Larger, less frequent disturbances such as hurricanes they provide (Costanza et al. 1997) and the support of can remove the canopy from thousands of hectares of coastal food webs by the detritus produced in the mangrove forest in a single event, opening up space forests (Odum and Heald 1975; Meziane et al. 2006; for new trees to colonize formerly dense, closed Abrantes and Sheaves 2009). In South Florida, there canopy forests. Mangrove forests also are disturbed are over 170,000 ha of mangrove forests (Odum et al. by human land clearing, dredging and filling. The 1982). These forests are dominated by four tree pervasiveness of disturbances in mangrove forests species that thrive in the saline, flooded soils of the could allow newly established species to rapidly coastal zone: red mangrove (Rhizophora mangle L.), proliferate across the landscape. black mangrove (Avicennia germinans L.), white Lugo (1998) suggests that established mangrove mangrove (Laguncularia racemosa (L.) C.F. Gaertn.) forests resist invasion by exotic species because of and buttonwood (Conocarpus erectus L.). The South the challenging physical environment of mangrove Florida mangrove species have close relatives that forests—but this contention is based on the idea that occur in the mangrove forests of the Indo-Pacific: invaders will be non-mangroves. In the modern era of R. mangle has congeners including R. stylosa, human mediated long-distance plant dispersal, there R. mucronata and R. apiculata; and in the same is potential for mangroves from different ocean family are the genera Bruguiera, Ceriops and Kand- basins to invade forests following their introduction. elia. A. germinans has the congeners A. marina and We know of no reasons why tropical Atlantic A. alba, among others. Laguncularia racemosa is in mangrove forests should support fewer ecological the same family (Combretaceae) as C. erectus and niches than Indo-Pacific forests, so the current Lumnitzera, with two species in the Indo-Pacific. species-depauperate nature of tropical Atlantic man- The mangrove forests of the Indo-Pacific are much grove forests may be a result of increased rate of more diverse than those of the tropical Atlantic extinction in the smaller area of the tropical Atlantic region (Duke 1992). The general pattern of higher compared to the Indo-Pacific. It is reasonable to diversity of mangroves, coral reefs and seagrasses in assume that, once freed from dispersal limitations by the tropical Indo-Pacific in comparison to those of the human activities, species of mangroves from the tropical Atlantic is likely the result of extinction more species-rich Indo-Pacific region could survive events following the tectonic separation of the quite well in the tropical Atlantic. There are close 123 Are mangroves in the tropical Atlantic ripe for Author's invasion? personal copy 2511 relatives of all of the tropical Atlantic mangrove marshes and colonized mud flats, leading to efforts to species in the Indo-Pacific. Extinctions over the last control their spread (Langer and Lipps 2006). 50 M years have led to low species richness and Humans have introduced non-native mangrove consequently unfilled or underutilized niches (sensu, species to areas with native mangroves as well. Non- Walker and Valentine 1984). Also, disturbances are native Sonneratia caseolaris and S. apetala were prevalent structuring forces in mangrove forests. For introduced for timber production to a mangrove forest these reasons, Atlantic mangrove forests may be ripe in Shenzen Bay, China in 1993. The species could for invasion by new mangrove tree species. sexually reproduce and individuals dispersed, but Humans have a long history of importing new appeared to be inferior competitors to native species. trees—including mangroves—for food, timber, and as As a result, Sonneratia spp. had limited