Coping with low nutrient availability and inundation: root growth responses of three halophytic grass species from different elevations along a flooding gradient

We describe the responses of three halophytic grass species that dominate the low (Spartina anglica), middle (Puccinellia maritima) and high (Elymus pycnanthus) parts of a salt marsh, to soil conditions that are believed to favour contrasting root-growth strategies. Our hypotheses were: (1) individual lateral root length is enhanced by N limitations in the soil but restricted by oxygen limitations, (2) the density of root branching within a species is inversely related to the length of the lateral roots, and (3) species from high elevations (i.e. the driest parts of a marsh) are the most responsive to changing soil conditions. Plant growth responses and soil parameters showed that the contrasting but uniformly applied soil treatments were effective. All three species showed a small but significant shift towards a finer root diameter distribution when N was limiting, partly because of the finer diameters of the laterals (Elymus and Spartina) and partly because of increased length of individual 1st-order laterals (Elymus and Puccinellia). The increased length of the 1st-order laterals of Elymus and Puccinellia grown under low N indicates that the first part of hypothesis 1 may be true. However, lack of effect of flooding and reduced soil conditions lead us to reject the second part of hypothesis 1. Hypothesis 2 was rejected for these three halophytes, as the branch density of 1st- and 2nd-order laterals appears to be controlled by other factors than length of individual laterals. Hypothesis 3 may be true for specific root characteristics (e.g. length of individual 1st-order laterals), but cannot be generalised (e.g. branch density and topological index). In conclusion, the present data on root growth in contrasting but homogeneous soil conditions indicate that morphological responsiveness of the root systems of these halophytic grass species is limited, regardless of their location along the elevational gradient.     

Transpiration and dry matter allocation in the angiosperm root parasiteCynomorium coccineum L. and two of its halophytic hosts

The angiosperm root parasiteCynomorium coccineum and the halophytic hostsLimonium delicatulum andArthrocnemum glaucum were invesrigated under natural conditions in a Mediterranean salt marsh in March 1992. The diurnal transpiration rate of the parasite was low and parallel to the climatic factors. The non-infected plants showed higher transpiration rates than the parasite and its hosts. Compared to the non-infected plants, it is apparent that the perennial herbL. delicatulum is more sensitive to infection since its reduction in the fresh and dry mass was higher than that found inA. glaucum.     

Variation in insect herbivory across a salt marsh tidal gradient influences plant survival and distribution

Herbivore damage and impact on plants often varies spatially across environmental gradients. Although such variation has been hypothesized to influence plant distribution, few quantitative evaluations exist. In this study I evaluated patterns of insect herbivory on an annual forb, Atriplex patula var. hastata, across a salt marsh tidal gradient, and performed experiments to examine potential causes and consequences of variation in herbivory. Damage to plants was generally twice as great at mid-tidal elevations, which are more frequently inundated, than at higher, less stressful, elevations at five of six surveyed sites. Field herbivore assays and herbivore preference experiments eliminated the hypothesis that plant damage was mediated by herbivore response to differences in host plants across the gradient. Alternately, greater herbivore densities in the mid-marsh, where densities of an alternate host plant (Salicornia europaea) were high, were associated with greater levels of herbivory on Atriplex, suggesting spillover effects. The effect of insect herbivores on host plant performance varied between the two sites studied more intensively. Where overall herbivore damage to plants was low, herbivory had no detectable effect on plant survival or seed production, and plant performance did not significantly differ between zones. However, where herbivore damage was high, herbivores dramatically reduced both plant survival (>50%) and fruit production (40-70%), and their effects were stronger in the harsher mid-marsh than the high marsh. Thus herbivores likely play a role in maintaining lower Atriplex densities in mid-marsh. Overall, these results suggest that variation in herbivore pressure can be an important determinant of patterns of plant abundance across environmental gradients.     

Nitrogen resorption from senescing leaves of three salt marsh plant species

Seasonalvariation in leaf nitrogen of mature green and senescent leaves and nitrogenresorption efficiency in three plants (Spartina maritima, Halimioneportulacoides and Arthrocnemum perenne) of aTagus estuary salt marsh are reported. Total nitrogen concentrations in greenand senescent leaves were higher during winter (December and March). Soilinorganic nitrogen availability showed an opposite pattern with higherconcentrations during summer (June and September) when total leaf biomass washigher. Nitrogen resorption efficiency ranged between 31 and 76% andH. portulacoides was the plant that better minimizednitrogen loss by this process. Nitrogen resorption occurred mainly from thesoluble protein pool, although other fractions must have been broken down duringthe resorption process. No significant seasonal variation in nitrogen resorptionefficiency and no relation to leaf total nitrogen or soil nitrogen availabilitywere found. This suggests that the efficiency of the resorption process is notdetermined by the plant nitrogen status nor by the availability of the nutrientin the soil. Nevertheless, resorption from senescing leaves may play animportant role in the nitrogen dynamics of salt marsh plants and reduce thenitrogen requirements for plant growth.     

Temporal dynamics of sediment bacterial communities in monospecific stands of Juncus maritimus and Spartina maritima

In the present study, we used 16S rRNA barcoded pyrosequencing to investigate to what extent monospecific stands of different salt marsh plant species (Juncus maritimus and Spartina maritima), sampling site and temporal variation affect sediment bacterial communities. We also used a bioinformatics tool, PICRUSt, to predict metagenome gene functional content. Our results showed that bacterial community composition from monospecific stands of both plant species varied temporally, but both host plant species maintained compositionally distinct communities of bacteria. Juncus sediment was characterised by higher abundances of Alphaproteobacteria, Myxococcales, Rhodospirillales, NB1–j and Ignavibacteriales, while Spartina sediment was characterised by higher abundances of Anaerolineae, Synechococcophycidae, Desulfobacterales, SHA–20 and Rhodobacterales. The differences in composition and higher taxon abundance between the sediment bacterial communities of stands of both plant species may be expected to affect overall metabolic diversity. In line with this expectation, there were also differences in the predicted enrichment of selected metabolic pathways. In particular, bacterial communities of Juncus sediment were predicted to be enriched for pathways related to the degradation of various (xenobiotic) compounds. Bacterial communities of Spartina sediment in turn were predicted to be enriched for pathways related to the biosynthesis of various bioactive compounds. Our study highlights the differences in composition and predicted functions of sediment‐associated bacterial communities from two different salt marsh plant species. Loss of salt marsh habitat may thus be expected to both adversely affect microbial diversity and ecosystem functioning and have consequences for environmental processes such as nutrient cycling and pollutant remediation.     

Arbuscular mycorrhizal fungal propagules in a salt marsh

The tolerance of indigenous arbuscular mycorrhizal fungi (AMF) to stressful soil conditions and the relative contribution of spores of these fungi to plant colonization were examined in a Portuguese salt marsh. Glomus geosporum is dominant in this salt marsh. Using tetrazolium as a vital stain, a high proportion of field-collected spores were found to be metabolically active at all sampling dates. Spore germination tests showed that salt marsh spores were not affected by increasing levels of salinity, in contrast to two non-marsh spore isolates, and had a significantly higher ability to germinate under increased levels of salinity (20) than in the absence of or at low salinity (10). Germination of salt marsh spores was not affected by soil water levels above field capacity, in contrast to one of the two non-marsh spore isolates. For the evaluation of infectivity, a bioassay was established with undisturbed soil cores (containing all types of AM fungal propagules) and soil cores containing only spores as AM fungal propagules. Different types of propagules were able to initiate and to expand the root colonization of a native plant species, but spores were slower than mycelium and/or root fragments in colonizing host roots. The AM fungal adaptation shown by this study may explain the maintenance of AMF in salt marshes.     

Effects of abiotic factors on the life span of the invasive cordgrass <Emphasis Type="Italic">Spartina densiflora</Emphasis> and the native <Emphasis Type="Italic">Spartina maritima</Emphasis> at low salt marshes

We analyzed variations in the life span of the invasive cordgrass Spartina densiflora at low marshes of SW Iberian Peninsula, and identified the abiotic factors limiting the plant in the absence of competition. With these objectives, clump survivorship, flowering, and growth of S. densiflora were studied in two natural populations at different low marsh elevations during more than three years, and at a transplant experiment in comparison with the native Spartina maritima. The life spans of both cordgrasses changed depending on small variations of a few centimeters in elevation. S. maritima, which tolerates better than S. densiflora the stressful abiotic environment of lower marshes, showed a significant lower distribution limit for its perennial habit, with survivorship longer than three years (from 1997 to 2000), than the neophyte (+1.57 m SHZ vs. +2.00 m SHZ). S. densiflora clumps flowered before dying at mostly all elevations, showing low relative growth rates. In contrast, clumps of S. maritima, with non-viable seeds, only flowered when they were three years old at higher elevations in the low marsh. Our results have applications for salt marshes bioengineering projects and to prevent S. densiflora from invading European marshes since our data improve the knowledge of its colonization mechanisms through salt marsh zonation and so identify those portions of restored and native marshes most susceptible to invasion due to the establishment of perennial populations.     

Effects of grazing and inundation on pasture quality and seed production in a salt marsh

During a six-year period, changes in the composition of dominant plant species of importance to foraging birds in a salt marsh on the Swedish west coast were followed inside and outside exclosures to document effects of grazing on herbage quality and seed production. Since marshes provide an important habitat for foraging geese and ducks, it was of interest to determine how cattle grazing would affect herbage production inAgrostis stolonifera andPuccinellia maritima and seed and root-tuber production inScirpus maritimus. Measurements of cover and height in permanent plots revealed that a wetter weather type favouredAgrostis, probably through reduced salinity, at the expense ofPuccinellia, which was the most favoured food of both cattle and birds.Agrostis out-competedPuccinellia when grazing pressure was low. Seed production inScirpus maritimus was reduced by cattle grazing, particularly whenPhragmites australis formed part of the vegetation. In the absence of cattle grazing, both herbage- and seed producing plants were gradually reduced, andPhragmites increased. Since high herbage consumption and high seed production are mutually exclusive, grazing rotation in combination with mowing is suggested as a management strategy.     

The importance of salt-marsh wetness for seed exploitation by dabbling ducks Anas sp.

The relationship between the inundation of a salt marsh in southeast Denmark not subject to lunar tides and the availability and predation of seeds of the annuals Salicornia spp. and Suaéda maritima by autumn staging dabbling ducks was studied by carrying out exclosure experiments over the course of 2 years. There was a marked difference in the wetness of the salt marsh between the two study years, which resulted in distinct temporal patterns of salt-marsh use by dabbling ducks. In both years, the depletion of seeds of both Salicornia spp. and S. maritima was initiated subsequent to the flooding of the sample transects, which also induced the gradual release of seeds from the plants within the exclosures. Nevertheless, seeds were removed more rapidly in plots visited by dabbling ducks than in the exclosures. The predation of seeds took place as soon as the individual plants had been fully submerged, but before the seeds were released from the plants. The timing of flooding events during early autumn may potentially affect the availability of the salt-marsh seed stock. Therefore, weather conditions may impose critical constraints on the feeding opportunities for dabbling ducks during autumn migration on non-tidal salt marshes.     

Periodicity of growth rings in some flood-prone trees of the Atlantic Rain Forest in Rio de Janeiro, Brazil

The periodicity of growth ring formation was studied in Tabebuia cassinoides (Lam.) DC, Tabebuia umbellata (Sond.) Sandwith, Symphonia globulifera L., and Alchornea sidifolia Müll. Arg. in a swamp forest within the Atlantic Rain Forest of the state of Rio de Janeiro, southeastern Brazil. Mechanical wounds of the vascular cambium allowed cyclic growth to be observed, and the position of latewood relative to the wounds was analysed. Radial growth was correlated with phenology, temperature, precipitation, photoperiod, flooding regime, and endogenous rhythms. All species showed annual growth rings; however, there were different patterns of radial growth. Phenology was an important factor influencing the activity of the vascular cambium. The period of leaf abscission was correlated with the formation of latewood in three of the species studied, but it occurred at different times for each species. Flooding was a determinant of periodic growth in T. cassinoides; photoperiod was indirectly responsible for radial growth rhythm in T. umbellata, and endogenous rhythms accounted for the radial growth rhythm of S. globulifera and A. sidifolia.     

Aggregative responses of brent geese on salt marsh and their impact on plant community dynamics

The aggregative responses and habitat preferences of a generalist herbivore, the dark-bellied brent goose Branta bernicla bernicla, feeding on salt marshes are examined in relation to vegetation community characteristics and the abundances of individual plant species. In the autumn, feeding was strongly concentrated on the low marsh, which had the highest biomass of the preferred food plant, Salicornia europaea. There was a strong aggregative response of the geese to the abundance of S. europaea. A decline in the availability of S. europaea led to an increase in the pattern of aggregation in relation to the two other major food plants on the low marsh, Aster tripolium and Puccinellia maritima. The availability of these food plants, however, reached critically low levels in mid-winter and the geese abandoned the low marsh for the high marsh. Within the high marsh, the plant communities selected tended to be dominated by the inedible species Limonium vulgare. The food plants selected were P. maritima in the winter and P. maritima and Triglochinmaritimum in the spring. On the high marsh, aggregative responses were shown to both P. maritima and T. maritimum, but in both cases, aggregation increased up to a critical level of biomass, and then declined. The prevention of grazing with exclosures for 3 years led to an increase in the abundance of P. maritima on both high and low marshes. This change was slight on high marsh but pronounced on low marsh, where S. europaea showed a decrease in abundance in the exclosures over this time. The implications of the aggregative responses for the population dynamics of P. maritima and S. europaea are discussed. Received: 11 September 1997 / Accepted: 12 December 1997     

Seasonal dynamics of arbuscular mycorrhizal fungi in differing wetland habitats

The dynamics and role of arbuscular mycorrhizal fungi (AMF) have been well described in terrestrial ecosystems; however, little is known about how the dynamics of AMF are related to the ecology of wetland ecosystems. The seasonal dynamics of arbuscular mycorrhizal (AM) colonization within different wetland habitats were examined in this study to determine the factors that influence AM associations and to further assess the ecological role of AMF in wetlands. Fen and marsh habitats of four wetlands in west central Ohio were sampled monthly from March to September. AMF were found at all four sites for each month sampled and were present in all of the dominant plant species. A significant effect of month (P<0.001) on AM colonization did occur and was attributable to maximum colonization levels in the spring and minimum levels in late summer. This trend existed in all four wetlands in both fen and marsh habitats, regardless of variation in water levels, percent soil moisture, or available phosphorus levels. Because abiotic factors had minimal influence on AM colonization variation and the level of AM colonization paralleled plant growth patterns, we conclude that the AM seasonal dynamic was in response to plant phenology. Our data suggest that AM associations in temperate fen and marsh habitats are prevalent in the spring during new root and vegetative growth, even for plants experiencing flooded conditions. Evidence of an overriding AM seasonal trend indicates that future studies should include a seasonal component to better assess the role and distribution of AMF in wetland ecosystems.     

Mycological studies on the angiosperm root parasiteCynomorium coccineum L. and two of its halophytic hosts

The fungal colonization of the angiosperm root parasiteCynomorium coccineum and the halophytic hostsLimonium delicatulum andArthrocnemum glaucum were investigated in a Mediterranean salt marsh in March 1992. The main fungal inhabitants on the leaves or shoot surface of the test plants wereAspergillus niger, Penicillium chrysogenum andCladosporium herbarum. The qualitative analysis of the fungal species associating the parasite, the hosts and the non-infected plants showed similar pattern. However, the total population exhibited quantitative differences coupled with the amount and the chemical composition of the exudates on plant surface and the quantity of transpired water. The fungal catch from the aerial shoot (inflorescence) of the parasite was higher than that collected from either the leaves or aerial shoots of non-infected or host plants. The fungal density on the leaves ofL. delicatulum was higher than those isolated from the aerial shoots ofA. glaucum. Infection byC. coccineum caused a marked drop in the total fungal population on leaves or shoot surfaces of the hosts as compared to the corresponding non-infected individuals. The stimulative effect of washings on spore germination of some isolated fungal species was matched with the density of fungi on the target plants.     

Structural characteristics of a diatom community epiphytic on Ruppia maritima

Epiphytic diatoms were collected from both the leaves and internodes of Ruppia maritima in a New Jersey salt marsh during the growing season of the host plant. Community diversity (H and the number of diatom taxa) values were initially high as Ruppia began its growth, but quickly dropped to sustained low levels as vegetative growth of the host ceased and new attachment sites were no longer available. A critical examination of all structural characteristics indicated that the leaves and internodes of Ruppia support a single, nearly homogeneous epiphytic diatom community. An analysis of variance indicated that differences between leaves and internodes were minimal, as did a comparison of the assemblages present on these two sites by a selected similarity index. A total of 57 taxa were encountered and the single dominant taxon was Navicula pavillardi, which accounted for one out of every three individuals counted. A comparison of the epiphytic diatom community with those inhabiting the sediments on the marsh proper revealed that the marsh sediments were the major source of individuals for Ruppia colonization.     

The effect of combined salinity and waterlogging on the halophyte Suaeda maritima: The role of antioxidants

Suaeda maritima is a halophytic plant and its habitat is salt marsh. In order to adapt to saline or waterlogged conditions, plants have evolved mechanisms that include antioxidant protection. However, the combined effect of salinity and waterlogging on antioxidants in S. maritima is unknown. The aim of this study was therefore to investigate the effect of saline-flooding on levels of glutathione and phenolic compounds (antioxidants) and the correlation between their concentration and activity in S. maritima shoots grown in their natural habitat and in a glasshouse.Shoots were collected from two different elevations (and so different degrees of flooding) of a salt marsh while other plants were grown in half strength seawater in the controlled conditions of a glasshouse for 8 weeks (drained and flooded). Shoot samples were used to measure dry weight, glutathione and its reduction state, malonyldialdehyde content (MDA), polyphenol content, superoxide anion and 2,2-diphenyl-1-picryl-hydrazyl-hydrate (DPPH) scavenging activity in the shoots of S. maritima.Growth of S. maritima was greater in plants growing on the high marsh than at a lower elevation and in drained medium as opposed to waterlogged conditions in the glasshouse. Waterlogging caused an increase in glutathione and its reduction state. The glutathione half-cell redox potential (E_GSSG/2GSH) was more negative in plant shoots grown under waterlogged conditions than in plants grown under normal conditions. Higher DPPH and superoxide anion scavenging activity was associated with high antioxidant concentrations (glutathione and polyphenols).Conclusions. Under saline-flooded conditions in the field and in the glasshouse, plants produced a higher concentration of antioxidants than under drained conditions. These result indicated that antioxidant molecules play an important role in S. maritima plants under combined salinity and waterlogging stress.     

Seasonal analyses of arbuscular mycorrhizae, nitrogen-fixing bacteria and growth performance of the salt marsh grass Spartina patens

Seasonal variation of arbuscular mycorrhizal fungi (AMF) in roots of the high salt marsh plant Spartina patens, the diversity of nitrogen-fixing bacteria in the rhizosphere and plant growth performance was studied at key stages of the growing season coinciding with major plant phenological stages, i.e., vegetative growth, reproduction and senescence. AMF colonization was highest during vegetative growth, with values declining during the growing season to the same level seen at plant dormancy. AMF colonization was reduced at lower depths in the sediments where anoxic conditions were observed and in plants treated with the systemic fungicide Benomyl. Only small changes in diversity of nitrogen-fixing bacteria in general and more specifically of those belonging to the ε-subdivision of Proteobacteria were detected during the season or between treatments by PCR-RFLP of nifH gene fragments with DNA as template for amplification; however, greater seasonal changes were displayed when cDNA was used as template for amplification as a proxy for gene expression and thus active bacteria. DGGE analyses of nifH gene fragments representing nitrogen-fixing bacteria of the ε-subdivision of Proteobacteria using both using DNA and cDNA as template showed highly diverse profiles that changed during the season and in response to treatment. Seasonal changes were observed for a suite of plant growth attributes and differences were observed between treatments, with higher values generally obtained on non-treated plants compared to Benomyl-treated plants. These differences were most pronounced during vegetative growth; however, differences between non-treated and Benomyl-treated plants were reduced seasonally and disappeared by the onset of senescence. This study demonstrates seasonal changes in AMF colonization on S. patens and in the community structure of nitrogen-fixing members of the ε-subdivision of Proteobacteria in the plant root zone. Plant growth performance changed seasonally with some effects of Benomyl-treatment.     

Effects of arbuscular mycorrhizal colonization and phosphorus application on nuclear ploidy in Allium porrum plants

Arbuscular mycorrhizal (AM) colonization can strongly affect the plant cell nucleus, causing displacement from the periphery to the center of the cell, hypertrophy and polyploidization. The hypertrophy response has been shown in a variety of AM plants whilst polyploidization has been reported only in Lycopersicon esculentum, a multiploid species with a small genome. In order to determine whether polyploidization is a general plant response to AM colonization, analyses were performed on Allium porrum, a plant with a large genome, which is much less subject to polyploidization than L. esculentum. The ploidy status of leaves, complete root systems and four zones of the adventitious roots was investigated in relation to phosphorus content, AM colonization and root differentiation in A. porrum plants grown under two different regimes of phosphate nutrition in order to distinguish direct effects of the fungus from those of improved nutrition. Results showed the presence of two nuclear populations (2C and 4C) in all treatments and samples. Linear regression analyses suggested a general negative correlation between phosphorus content and the proportion of 2C nuclei. The percentage of 2C nuclei (and consequently that of 4C nuclei), was also influenced by AM colonization, differentiation and ageing of the root cells, which resulted in earlier occurrence, in time and space, of polyploid nuclei.     

Variation in nutrient availability and plant species diversity across forb and graminoid zones of a Northern New England high salt marsh

Plant zonation patterns across New England salt marshes have been investigated for years, but how nutrient availability differs between zones has received little attention. We investigated how N availability, P availability, and plant N status varied across Juncus gerardii, Spartina patens, and mixed forb zones of a Northern New England high salt marsh. We also investigated relationships between several edaphic factors and community production and diversity across the high marsh. P availability, soil salinity, and soil moisture were higher in the mixed forb zone than in the two graminoid zones. NH⁺ ₄-N availability was highest in the J. gerardii zone, but NO^– ₃-N availability and mid season net N mineralization rates did not vary among zones. Plant tissue N concentrations were highest in the mixed forb zone and lowest in the S. patens zone, reflecting plant physiologies more so than soil N availability. Community production was highest in the J. gerardii zone and was positively correlated with N availability and negatively correlated with soil moisture. Plant species diversity was highest in the mixed forb zone and was positively correlated with P availability and soil salinity. Thus, nutrient availability, plant N status, and plant species diversity varied across zones of this high marsh. Further investigation is needed to ascertain if soil nutrient availability influences or is a result of the production and diversity differences that exist between vegetation zones of New England high salt marshes.     

Arbuscular mycorrhizal fungi enhance root cadmium and copper accumulation in the roots of the salt marsh plant Aster tripolium L.

It is known that vegetation plays an important role in the retention of heavy metals in salt marshes by taking up and accumulating the metals. In this study, we investigated whether arbuscular mycorrhizal fungi (AMF) increase Cd and Cu uptake and accumulation in the root system of the salt marsh species Aster tripolium L., and whether indigenous AMF isolated from polluted salt marshes have higher capacity to resist and alleviate metal stress in A. tripolium than isolates of the same species originated from non-polluted sites. Plants inoculated with Glomus geosporum, either isolated from a polluted salt marsh site (PL isolate) or from a non-polluted site (NP isolate), and non-mycorrhizal (NM) plants were compared in a pot experiment at four different Cd and Cu concentrations. Cd had no effect in root colonization, whereas high concentrations of Cu decreased colonization level in plants inoculated with the NP isolate. AM colonization did not increase plant dry weight or P concentration but influenced root Cd and Cu concentrations. Inoculation with PL and NP isolates enhanced root Cd and Cu concentrations, especially at highest metal addition levels, as compared to NM plants, without increasing shoot Cd and Cu concentrations. There was no evidence of intraspecific variation in the effects between AMF isolated from polluted and non-polluted sites, since there were no differences between plants inoculated with PL or NP isolate in any of the tested plant variables. The results of this study showed that AMF enhance metal accumulation in the root system of A. tripolium, suggesting a contribution of AMF to the sink of metals within vegetation in the salt marshes.