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The evaluation of species interactions is fundamental to an adequate understanding of plant community structure and ecosystem functioning. Species interactions have been shown to be important factors in determining spatial patterns of plant distribution and dominance (Grace & Wetzel 1981; Grace & Tilman 1990; Keddy 2001). A plant population, however, is comprised of an array of individual genets that can differ in their responses to environmental factors, one another and other species. Our understanding of the contribution of the different plant genotypes within a population to responses to other organisms, such as competitors, herbivores and disease organisms, as well as to disturbance and environmental gradients, lags behind basic studies of species–species interactions, in which it is often assumed that all individuals are homogeneous or that the law-of-large numbers will ‘average out’ individual variation. It is possible that the number and relative magnitudes of biotic interactions will increase as the genotypic and genetic diversity in dominant, or foundation, plant species increases. Booth & Grime (2003) reported that experimental calcareous grassland plots containing greater within-species genetic diversity lost species more slowly than did plots with low genetic diversity. This suggests that genetic diversity of dominant plant species can mediate important biological interactions.
Salt marsh zonation results from a combination of species-specific differences in response to stress gradients and resource regimes, recovery following disturbance and competition among species (Bertness & Ellison 1987; Ellison 1987; Bertness 1991a,b; Levine et al. 1998a,b; Costa et al. 2003; Ewanchuk & Bertness 2004; Pennings et al. 2005). In the low intertidal, S. alterniflora is often the dominant species because of its high tolerance of frequently flooded, hypoxic conditions (Valiela & Teal 1974; Mendelssohn & Seneca 1980; Gleason & Zieman 1981; Mendelssohn et al. 1981). Although S. alterniflora can grow over a wide elevation range, its distribution and dominance at higher marsh elevations is limited by competition (Bertness 1991a,b; Crane et al. 2004). Competitive outcomes, however, can be affected by nutrient conditions (Covin & Zedler 1988; Levine et al. 1998a,b). Its various genotypes show different responses to elevation in terms of growth rates and reproductive patterns (Proffitt et al. 2003), and thus it is possible that genotypes, and their diversity, density, and distribution within the population, may also influence the outcomes of competitive and facilitative interactions.
Phenotypic variation in clone growth and morphology of S. alterniflora is, in part, genetically based (Seneca 1974; Gallagher et al. 1988; Seliskar et al. 2002; Proffitt et al. 2003). Variation in plant architecture can influence spatial heterogeneity within the marsh, which affects ecosystem function properties such as microbial respiration, edaphic chlorophyll and larval fish use (Seliskar et al. 2002), as well as interactions among plant species (Boyer & Zedler 1999). The interaction between genotype and microenvironmental conditions may lead to a variety of plastic growth and morphology responses that greatly increase the effects of this plant on salt marsh structure and function (Seliskar et al. 2002). Thus the wide-ranging S. alterniflora can be described as a foundation species, modifying the environment and providing resources for other species (Bruno & Bertness 2001).
Populations of S. alterniflora become established by both vegetative means (fragmentation and tidal transport followed by clonal growth) and seedling recruitment (Proffitt & Young 1999; Proffitt et al. 2003; Travis et al. 2004). Clonal and genetic diversity increases in young, rapidly expanding populations and later declines, possibly through interclone competition or genet loss through stochastic processes (Travis et al. 2002; Travis et al. 2004; Travis & Hester 2005). It is possible that the diversity of plant–environment interactions follows a similar pattern as interactions in an increasingly heterogeneous habitat may vary with differences in phenotype and clone morphology. Temporal as well as spatial heterogeneity would translate into variation in the ecological functions affected by S. alterniflora populations.
One form of habitat heterogeneity is produced by the variable extent to which S. alterniflora clonal patches show senescence in their centres (Stiller & Denton 1995; Proffitt et al. 2003). This aspect of clonal morphology can vary with plant genotype and environmental gradients such as elevation (Proffitt et al. 2003), but its effects on other species is poorly understood. Habitat heterogeneity may also be produced by among-clone variation in plant size or density.
We posed the following research questions. (i) Does the transplantation of S. alterniflora clones into an area of marsh dominated by the annual Salicornia bigelovii Torr. alter plant species composition and the rate of assemblage development in a young salt marsh? (ii) Do differences in S. alterniflora morphology (such as clone area, clone centre senescent area, stem density and height) among clonal genotypes produce additional variation in heterogeneity in soil and light variables? (iii) Does the strength or nature of facilitation or suppressive interactions vary with S. alterniflora genotype?
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Biotic interactions such as competition and facilitation play an important role in determining the mixture of species, diversity and dominance in ecological systems (Connell & Slatyer 1977; Chesson & Huntly 1997; Day & Young 2004; Pennings et al. 2005). In many systems, such as forests, grasslands and coral reefs, some species may exert strong influences on others by imposing physical structure and new suites of environmental conditions that do not exist in their absence (Bruno & Bertness 2001). We suggest that in such foundation or matrix or keystone species, differences in morphology or growth among clonal genotypes will increase the type and/or magnitude of effects on other species.
The presence or absence of the grass Spartina alterniflora has strong influences on other species in a young, developing marsh. The prior dominant species, the annual Salicornia bigelovii, is displaced by S. alterniflora, probably due to reduction in light penetration of the grass canopy, and is possibly further inhibited by reduction in water-borne seed transport to clone centres because of blockage by the dense clone edges. However, a number of other high marsh species recruited better into S. alterniflora experimental clones than non-grassed areas. Similar interactions among salt marsh plants have been reported in a number of studies. For example, Bertness & Ellison (1987) found that interspecific competition and disturbance were primary agents structuring a salt marsh community. Bertness & Ewanchuk (2002) reported greater survival and growth of certain fugitive salt marsh species when growing with dominant or matrix plant species than when grown in non-vegetated surroundings. Levine et al. (1998a) reported that nutrients could reverse competitive outcomes among salt marsh plants. Huckle et al. (2002) found that competitive interactions between salt marsh plant species were primarily above ground rather than below ground, and that competition was reduced under conditions of increased environmental stress.
Our study is the first to document differences in species–species plant interactions due to varying effects of different genotypes of S. alterniflora, both in terms of numbers of species recruiting and size and density of some of the more abundant species. Different shade regimes may be one of the mechanisms behind the biological effects of the genotypes, and contribute to the patchiness often observed for some less abundant or fugitive salt marsh species, but soil moisture, salinity and nutrients were unaffected. Thus, our findings agree with Seliskar et al. (2002), who reported that different genotypes of S. alterniflora produced changes in the marsh environment and exerted strong control on certain ecological functions.
The extent and ecological importance of these types of effects may be related to genotypic and possibly genetic diversity of the population of the dominant species. Genetic diversity tends to be relatively high in this species (Travis et al. 2002) and the diversity of clonal genets first increases then decreases with marsh age (Travis et al. 2004). However, despite some reduction, considerable genetic and genotypic diversity remains in populations over 1000 years old (Travis & Hester 2005). Genotypic variation in S. alterniflora results in variation in stem density, height and clonal morphology (Proffitt et al. 2003, present study). The high clonal and genetic diversities in S. alterniflora populations of the northern Gulf of Mexico marshes are maintained by high levels of outcrossing coupled with severe inbreeding depression (Travis et al. 2004). Clones in natural marshes of this region range considerably in size (maximum diameter < 20 to > 500 m) depending in part on marsh age (Travis & Hester 2005). This suggests that many marshes will consist of populations of many more different clonal genotypes than the five tested here, and their substantial variation in morphology, size, onset of senescence, etc., will greatly increase the potential for genotypic and genotype × environment effects in S. alterniflora-dominated marshes.
Here, we show that genet-specific differences in S. alterniflora plant size, density and degree of senescence of clone centres introduce heterogeneity that results in increases in the rate recruitment of a number of high marsh plant species at mid-tidal elevations and in size and/or density of the fugitive annual plant species Aster subulatus, as well as affecting replacement of Salicornia bigelovii. Some authors have suggested that higher order properties arising from such interactions may themselves be heritable, thus constituting a discipline of community genetics (Antonovics 1992; Whitham et al. 2003; but see Ricklefs 2003). If true, then genetic and genotypic variation in dominant species would have even greater, higher order, consequences for marsh ecology.
Senescence in the centre of S. alterniflora clones may be a function of age-related ramet mortality but, unlike some plant species (Bell 1974; Harper 1977), it is probably not related to directional growth of rhizomes (Metcalfe et al. 1986). Some grass patches senesce in the centre because they have vertical orientation of crowns and tend to grow themselves out of the ground (Dahl 1995); however, this is not known to be the case for S. alterniflora. Nutrient values measured in clones were similar to those in natural marshes in the area (Edwards & Proffitt 2003; K. R. Edwards & K. Mills, unpublished data). Also, fertilization of clone centres and edges produced no response in this marsh (A. B. Owens & C. E. Proffitt, unpublished data). This suggests that nutrient depletion is unlikely to be responsible for central senescence of the S. alterniflora clones or the different effects of its genets on other plant species. However, manipulative experiments on nutrients and senescence need to be done to support this contention.
Falinska (1995) reported that senescence of the upland plant Filipendula ulmaria influenced succession by giving rise to open space that was subsequently colonized by other plants. McConnaughay & Bazzaz (1990) found that there was greater plant performance in larger gaps and that plant–plant interactions were independent of gap size in a herbaceous old field community. Their work showed the species-specific nature of interactions, as indicated here by competition and facilitation among plants colonizing the senescent centres of S. alterniflora.
The patterns of colonization and seedling growth noted here are important in the development of community structure at mid and higher elevations. Several of the more abundant colonizers, such as Atriplex, Aster and Baccharis, have seeds that are adapted for wind dispersal, although in these tidal marshes they are probably also secondarily moved by water (Huiskes et al. 1995). Iva and Salicornia produce large numbers of very small seeds that are water dispersed. The substantially larger caryopsis of S. alterniflora is also dispersed by water movement. Dispersal of Salicornia europaea (an annual prevalent in the north-eastern United States) appears to be generally limited to a few metres (Ellison 1987) and, at our site, S. bigelovii seeds occurred on the soil surface mainly within a metre or two of parent plants. However, longer distance dispersal of seeds and/or seedlings clearly occurs because three to five successive years of seed set and colonization leads to a dense population of S. bigelovii across essentially the entire area of the sites (Proffitt & Young 1999; C. E. Proffitt, field observations). Whether the S. alterniflora clonal genotypes have direct effects on the other plant species or mediate plant responses through effects on microenvironmental parameters, or both, is not discernable from our study. Nor can we tell whether colonization per se is different in different S. alterniflora clonal types, or whether seedling survival and growth are different, or both. However, Egerova et al. (2003), working in this same marsh, did not find that S. alterniflora clones trapped greater numbers of seeds of Baccharis, but that they did enhance survival and growth of that woody high-marsh species.
Huckle et al. (2002) reported that Spartina anglica facilitated the growth of Puccinellia maritima at low nutrient concentrations, and that P. maritima outcompeted S. anglica. Bertness & Hacker (1994) and Bertness & Ewanchuk (2002) reported that in years with higher soil salinities, interactions among plant species tended to be facilitative because some species could ameliorate soil conditions that could adversely affect more sensitive plant species. However, Levine et al. (1998b) noted that for one salt-intolerant marsh species this effect was eliminated by fertilization. We found similar reductions in temperature to those reported by Bertness & Ewanchuk (2002) but, unlike Bertness & Ewanchuk (2002) and Bertness & Hacker (1994), we did not find significant effects of higher vegetation cover on soil pore water salinity. It is possible that, as the assemblage is developing on a newly deposited mud flat, nutrients are not limiting and consequently that the effects of salinity are somewhat reduced.
As noted, Spartina alterniflora clonal genotypes played a role in the extent of suppression of the annual dominant Salicornia bigelovii. Despite higher light levels, the very low densities and small plant sizes of S. bigelovii indicate that senescent clone centres did not serve as effective refugia for this species. In New England, Salicornia europaea, which occurs in non-grassed patches produced through wrack disturbance, is similarly competitively inferior to the marsh grasses (Bertness & Ellison 1987; Ellison 1987), and is suppressed by other marsh matrix species (Bertness & Ewanchuk 2002). However, in a cobble beach system, Bruno (2000) found that the presence of S. alterniflora facilitated establishment of S. europaea immediately landward by reducing water velocity and thus stabilizing the substrate. S. bigelovii remained a dominant in areas throughout our 200-ha created marsh site and was especially tall and abundant in interior, higher elevation regions. However, S. bigelovii, coming up new from seed each growing season, suffered greatly reduced densities after encountering expanding S. alterniflora clones. Boyer & Zedler (1999) found different outcomes when S. bigelovii was grown in competition with Spartina foliosa in a fertilizer experiment. Their results showed that S. foliosa, which is much shorter than S. alterniflora, only responded with increased growth to nutrient addition in the absence of S. bigelovii, while S. bigelovi grew to the size of S. foliosa when fertilized and produced > 1 × 106 seeds m−2. Salicornia virginica has also been reported to out-compete S. foliosa for nitrogen in California (Covin & Zedler 1988). Such experiments have not yet been done in our young, clay-soil marshes, although available data suggest that nutrients are not generally limiting (Edwards & Proffitt 2003; K. R. Edwards & K. Mills, unpublished data).
Bertness & Ewanchuk (2002) found more facilitative species–species interactions in New England salt marshes south of Cape Cod and more competitive interactions northwards. This was linked to warmer conditions in the more southern sites and in both sites in warm years. Our study included some of the same marsh genera and species as Bertness & Ewanchuk (2002) in a much more southerly locale (coastal Louisiana). Similar to their results for S. europaea, we found that S. alterniflora suppressed Salicornia bigelovii, but facilitated colonization and/or growth of a number of other species.
Numerous species are colonizing the large, initially vacant, mudflats created from dredged sediment at the Sabine National Wildlife Refuge (Proffitt & Young 1999; Edwards & Proffitt 2003; Egerova et al. 2003; Proffitt et al. 2003). However, the development of the dominant perennial S. alterniflora is an important agent of other changes within the vegetation assemblage. S. alterniflora colonizes essentially the entire elevation range of these sites when not in competition with other perennials (Proffitt & Young 1999; Proffitt et al. 2003) and enhances the recruitment and growth of a number of annual and woody plant species (Egerova et al. 2003; present study). A recent model suggests that S. alterniflora will become dominant over a large elevation range when nutrients are not limiting (Bertness 1991a,b; Huckle et al. 2002). Our results on the interactions between S. alterniflora and S. bigelovii tend to support this model although we found a substantial lag time because of the time necessary for S. alterniflora colonization and clonal growth in this young site (Proffitt et al. 2003; present study). However, our results also show that differences in clonal genets and central senescence lead to patchiness that can promote the recruitment and growth of some plant species. Whether or not long-term changes will result in the loss of some of these colonizing species through interspecific competition with the dominant grass will depend on the long-term clonal population dynamics of existing S. alterniflora clones and on the colonization of senescent centres by S. alterniflora seedlings and the ensuing establishment of new clones (Travis et al. 2004).
Spartina alterniflora has been described as a keystone species (Seliskar et al. 2002), a keystone or ecosystem engineer (Bruno 2000), and a foundation species (Pennings & Bertness 2001), because of the profound roles that it plays in creating habitat for other species, providing considerable productivity for marsh and nearshore food webs, buffering storm surges, and sequestering organic matter in the sediment. Despite decades of ecological studies in salt marshes, the importance of population biology, genetics and morphological variation for ecological function has only recently begun to be established (Seliskar et al. 2002; Proffitt et al. 2003; Travis et al. 2004; present study). Not only is an adequate understanding of the effects of genotypic and genetic variation on ecologically important plant traits critical to a full understanding of basic salt marsh ecology, it may also be fundamental to the conservation and restoration of fully functional populations of this dominant plant species.
Crane et al. (2004) stated that plants are not just ‘found in habitats where they grow best’, but rather that biotic interactions in association with environmental factors are important in producing plant assemblages. We suggest that populations of foundation species, such as S. alterniflora, that have greater clonal diversity will also have a broader array of ecologically important interactions with other plant species. This certainly appears to be the case in young marshes developing on mudflats. Further work will be required to determine if clonal diversity is important in biological interactions in very old marshes.