Our experiments show that environmental factors have significant effects on the growth of the two salt marsh species and that interactions occur between them at both an intra-and interspecific level. Of the three environmental factors studied, sediment and waterlogging affected biomass production of Spartina and all three factors affected the competitive interactions between the species. In all experiments where plant interactions were detected, the interspecific competition was found to be more intense than intraspecific competition.
Effects of salinity, sediment and waterlogging on plant response
When grown in monospecific combinations, Spartina biomass was reduced when grown in sand, a result that agrees with previous population studies on this species (Thompson et al. 1991). However, our study showed a differential response of Spartina’s biomass components to the type of sediment: Spartina’s below-ground biomass was reduced in sand, whilst its above-ground biomass was increased in loam. We suggest that this slight variation in the response of the two components of the biomass may arise from influences of different components of the sediment, the coarse-grained sandy sediments inhibiting root development and loam having a nutrient-related effect leading to an increase in above-ground biomass.
Above-ground biomass of Spartina was reduced by both intraspecific competition and interspecific competition from Puccinellia and the intensity of these interactions was greatest in loam sediments. Physical stress from environmental factors (such as coarse sediment composition and low nutrient availability) are less intense in the loam sediments and the results support the assertion that plant interactions will become more important as stress is reduced. Further insight into the interspecific interaction between Spartina and Puccinellia was obtained from the effects of Puccinellia on Spartina below-ground biomass, where a competitive effect was detected in the loam sediment and a facilitative effect detected in the mixed and sand sediments. We interpret these results as a sediment-dependent response to the presence of Puccinellia. In loam, alleviation of treatment-imposed stress is combined with more intense interspecific competition from Puccinellia, thus inhibiting both above- and below-ground Spartina biomass. However, in sandy sediments, competition is less intense and Spartina appears to respond to above-ground interference from Puccinellia by the production of below-ground structures, a response not seen when exposed to intraspecific competition. This suggestion is supported by the morphological data, which showed that the numbers of Spartina vegetative tillers parallel the increase in Spartina below-ground biomass. We suggest that, by investing in underground rhizomes that give rise to innumerable small vegetative tillers, Spartina may be able to avoid above-ground competition by spreading vegetatively into areas more favourable for growth.
In the waterlogging experiment, lack of immersion reduced the above-ground biomass of Spartina grown in monospecific combinations. This contrasts with investigations into the effects of waterlogging in field conditions which have shown reduced growth of Spartina species in waterlogged sediments (Groenendijk et al. 1987; Mendelssohn & McKee 1988), attributable to long-term exposure to a reducing environment and the associated accumulation of sulphide and oxygen deficient roots. The duration of this experiment may be too short to produce conditions that affect growth. This would explain the lack of waterlogging effects on biomass in Puccinellia, a species that is known to survive only short periods of exposure to sulphide in the latter part of the growing season (Havill et al. 1985).
Both intra- and interspecific competition affected the growth of above-ground Spartina in the waterlogging experiment. Intraspecific competition did not vary in intensity between waterlogging treatments, but above-ground interspecific competition was greater in non-waterlogged treatments compared to those experiencing full or half immersion. Spartina below-ground biomass was only affected when the stress of non-waterlogged soils was combined with the presence of Puccinellia. As in the sediment experiment, no effect of immersion was detected on the growth of Puccinellia. However, effects of waterlogged soils may have been obscured in the case of Puccinellia above-ground biomass. In full- and half-immersion treatments, increased stolon extension (not measured) may have resulted in above-ground biomass of Puccinellia being higher than would be expected in field conditions: stolons of Puccinellia were able to float on the water surface of immersed treatments and root into the water, thus spreading further than where the water level was beneath the base of the pots.
No effect of salinity on the growth of Spartina or Puccinellia was detected for either above- or below-ground components of biomass, despite the experimental treatments being set at comparable levels to those found to have significant effects on growth in other studies (Rozema & van Diggelen 1991) and reflecting the range of salinity experienced in field conditions. In this experiment, main-plots were individually established with species combination treatments immersed in a relatively shallow reservoir of saline water (10 cm). As a consequence, the species combination treatments may have been more exposed to the influences of rainfall, which would have had a diluting effect on the pots from above and counteracted the influences of saline water infiltrating into the soil from the base of the individual pots than if they had been fully immersed. This experiment may thus be more representative of high salt marsh elevations where rainfall has a greater influence than tidal water in determining soil salinity levels (de Leeuw et al. 1991). Intraspecific competition was, however, detected for Spartina and Puccinellia above-ground biomass, but not for below-ground biomass, suggesting an interference effect from conspecifics for each species.
Overall, both species generally showed intraspecific competition both above- and below-ground. Interspecific competition was asymmetric with Puccinellia competitively reducing above-ground production of Spartina to a greater degree than did intraspecific competition, but with Spartina having little or no effect of on Puccinellia biomass.
Comparison of experimental results with salt marsh conditions
Spartina colonizes bare mud-flats at lower marsh elevations in the Dee Estuary. Coarse-grained sediments and frequent tidal inundation impose environmental stress in these areas, and although Spartina is able to tolerate such conditions when experimentally imposed, it performs better in more nutrient-rich, loamy sediments, similar to those higher up the marsh. This finding corresponds well with previous studies where Spartina plants in pioneer zones were shorter than those from further up the marsh (Thompson 1990). This difference in growth of Spartina cannot be explained by phenotypic plasticity caused by age-related somatic variation of clones (Thompson et al. 1991; Thompson et al. 1993), as all plants in our study were collected from clones from the same area of pioneer marsh. However, the reduced biomass and tiller production of Spartina plants grown in coarse-grained sediment may reflect the greater degree of stress in these conditions.
The impact of the presence of Puccinellia on Spartina biomass, and the way that it changes across the sediment gradient is particularly interesting. In these experiments we have shown competition, as measured by the Relative Neighbour Effect index, to be most intense in loam sediments, resulting in Spartina biomass being inhibited both above- and below-ground. In coarse-grained sandy sediments, however, above-ground competition from Puccinellia is less intense. At this position along the environmental gradient, it appears that the stresses imposed by the environmental conditions play a more important role than the interactions between species. This finding supports the idea of an inverse relationship between stress tolerance and competitive ability (Grime 1979). Whilst above-ground competition becomes less intense in sandy sediments, at the below-ground level, Spartina biomass actually increases, suggesting a facilitative interaction. An investment in rhizomes could be interpreted as a response to nutrient-poor conditions and an attempt to migrate to more favourable patches; however, such a response would also be expected to occur in monospecific combinations. We suggest that this finding may be explained by the hypothesis that Spartina is able to respond to less intense levels of above-ground interspecific competition by investing in below-ground biomass.
In the waterlogging experiment, a similar trade-off occurs between the competitive ability of Puccinellia and the stress tolerance of Spartina. This experiment shows growth of Spartina to be highest in immersed treatments and Puccinellia to have a greater competitive effect in non-immersed treatments, suggesting that the stress imposed on Puccinellia by immersion has a debilitating effect on its competitive ability.
These factors may be strong forces in determining salt marsh structure and development. At lower elevations, Spartina may be able to evade competition by rhizome extension when above-ground interference hinders tiller development. As elevation increases, however, and environmental conditions become analogous to those experienced in the loam and non-waterlogged experimental treatments, the intensity of competition increases and results in competitive exclusion by Puccinellia.
Previous studies of the competitive interaction between these species have suggested that Puccinellia out-competes Spartina because it develops earlier in the year and reduces the competitive ability of Spartina by preventing light from reaching developing shoots (Scholten & Rozema 1990). The relatively late canopy development of Spartina is due to it being a C4 species, with very low photosynthetic efficiency at low temperatures resulting in the ability to grow and reproduce being limited to months where the average temperature rises above 9–10 °C (Long 1983). This experiment, where both species were planted simultaneously, suggests that the effects of earlier development of Puccinellia may be compounded by the direct physical interference of above-ground Puccinellia stolons on Spartina tillers in summer and autumn.
One interesting feature is the lack of environmental effects on the growth of Puccinellia, indicating that it grows equally well in all the experimental conditions and that other factors may be responsible for limiting growth in field conditions. One possible explanation is that Puccinellia development in the field is affected by physical stress imposed by the action of repetitive tidal inundation. In this experiment, no attempt was made to create tidal periodicity or the physical impact of tides. It can be postulated that in field conditions Spartina, being rhizomatous and relatively robust, would be more suited to withstand these physical stresses than the stoloniferous Puccinellia. Thus Spartina may facilitate the establishment of Puccinellia through provision of sheltered environments, in combination with enhanced accretion of silt sediments. Such facilitation has been shown to exist in salt marshes colonized by Spartina maritima (Castellanos et al. 1994) with subsequent suppression of S. maritima tillers by a more competitive invader.
Our study has shown how the interaction of abiotic and biotic factors, particularly competition, is fundamental to the generation of plant zonation patterns in salt marshes. In recent field-based studies in a North American salt marsh, it was found that competitive hierarchies could be reversed by nutrient-enhancement, leading to the domination of species usually displaced to physically stressful tidal elevations (Levine et al. 1998). In a long-term field study of a European coastal barrier salt marsh, it was found that nutrient enhancement led to an acceleration in successional change (van Wijnen & Bakker 1999). Our study, using an experimental pot-based approach, has demonstrated that the competitive interaction between Spartina and Puccinellia is asymmetric, with Puccinellia having a competitive effect on Spartina, but not vice versa. Furthermore, this competitive effect is intensified in less physically stressful environments, such as those found in fine-grained, nutrient-rich sediments exposed to less tidal inundation, allowing the more competitive species to become dominant. We suggest that this supports the findings of van Wijnen & Bakker (1999), and that the competitive hierarchy established may arise as a consequence of the different life strategies of the two species. Spartina is a rhizomatous perennial possessing a C4 physiology, whilst Puccinellia is a stoloniferous C3 perennial. In Northern Europe, Spartina is late to emerge, the temperature dependence of the C4 pathway causing its growing season to be delayed (Long 1983; Gray et al. 1991). Puccinellia, however, is able to start growing relatively early in the year. In this way, our findings support the idea that the competitive dominance exhibited by Puccinellia over Spartina is related to early emergence and driven by competition for light (Bertness 1991; Goldberg & Miller 1990). At latitudes lower than our study site, where the growing season of Spartina is unlikely to be delayed, the observed hierarchy may be diminished or even reversed.
The findings of these experiments have important implications for conservation and the prediction of salt marsh community development, particularly as these may interact with changes in climate. We have proposed a mechanism by which competitive displacement of species may occur, in that the displacement of Spartina in physically stressed environments is an active process. Where Spartina is affected by above-ground competition, increased production of below-ground vegetative rhizomes may allow vegetative spread of Spartina into areas with less competition. Further work is needed to elucidate the validity of this mechanism in field conditions.