Successional patterns of key genes and processes involved in the microbial nitrogen cycle in a salt marsh chronosequence

Here, we investigated the patterns of microbial nitrogen cycling communities along a chronosequence of soil development in a salt marsh. The focus was on the abundance and structure of genes involved in N fixation (nifH), bacterial and archaeal ammonium oxidation (amoA; AOB and AOA), and the abundances of genes involved in denitrification (nirS, nirK, nosZ). Potential nitrification and denitrification activities were also measured, and increases in nitrification were found in soils towards the end of succession, whereas denitrification became maximal in soils at the intermediate stages. The nifH, nirK and nirS gene markers revealed increases in the sizes of the respective functional groups towards the intermediate stage (35 years), remaining either constant (for nifH) or slightly declining towards the latest stage of succession (for nirK and nirS). Moreover, whereas the AOB abundance peaked in soils at the intermediate stage, that of AOA increased linearly along the chronosequence. The abundance of nosZ was roughly constant, with no significant regression. The drivers of changes in abundance and structure were identified using path analysis; whereas the ammonia oxidizers (AOA and AOB) showed patterns that followed mainly N availability, those of the nitrogen fixers followed plant diversity and soil structure. The patterns of denitrifiers were group-dependent, following the patterns of plant diversity (nirK and nirS) and belowground shifts (nosZ). The variation observed for the microbial groups associated with the same function highlights their differential contribution at different stages of soil development, revealing an interplay of changes in terms of niche complementarity and adaptation to the local environment.     

Methane production potential and methanogenic archaea community dynamics along the Spartina alterniflora invasion chronosequence in a coastal salt marsh

Invasion by the exotic species Spartina alterniflora, which has high net primary productivity and superior reproductive capacity compared with native plants, has led to rapid organic carbon accumulation and increased methane (CH₄) emission in the coastal salt marsh of China. To elucidate the mechanisms underlying this effect, the methanogen community structure and CH₄ production potential as well as soil organic carbon (SOC), dissolved organic carbon, dissolved organic acids, methylated amines, aboveground biomass, and litter mass were measured during the invasion chronosequence (0–16 years). The CH₄ production potential in the S. alterniflora marsh (range, 2.94–3.95 μg kg^?1 day^?1) was significantly higher than that in the bare tidal mudflat. CH₄ production potential correlated significantly with SOC, acetate, and trimethylamine concentrations in the 0–20 cm soil layer. The abundance of methanogenic archaea also correlated significantly with SOC, and the dominant species clearly varied with S. alterniflora-driven SOC accumulation. The acetotrophic Methanosaetaceae family members comprised a substantial proportion of the methanogenic archaea in the bare tidal mudflat while Methanosarcinaceae family members utilized methylated amines as substrates in the S. alterniflora marsh. Ordination analysis indicated that trimethylamine concentration was the primary factor inducing the shift in the methanogenic archaea composition, and regressive analysis indicated that the facultative family Methanosarcinaceae increased linearly with trimethylamine concentration in the increasingly sulfate-rich salt marsh. Our results indicate that increased CH₄ production during the S. alterniflora invasion chronosequence was due to increased levels of the non-competitive substrate trimethylamine and a shift in the methanogenic archaea community.     

Nitrogen fixation and nitrogen limitation of primary production along a natural marsh chronosequence

We experimentally tested the conditions where heterospecific attraction is more likely to occur. The heterospecific attraction hypothesis predicts that colonizing or migrant individuals use the presence of resident species as a cue for profitable breeding sites. In other words, increasing resident densities will result in increased migrant densities until the costs of interspecific competition override the benefits of heterospecific attraction. The experiment consisted of a reference and a manipulation year. In the reference year, resident titmice were permitted to breed at intermediate densities whilst in the manipulation year, resident densities were manipulated in nine study plots. Three treatments were performed as low, intermediate and high resident densities and migrant density responses were measured in both years. Relative between-year migrant and resident densities were analyzed by regression analysis. Migrant foliage gleaning guild densities responded linearly and positively, as did densities of habitat generalists, in particular Chaffinch ( Fringilla coelebs),. The ground-foraging guild did not show a response. This study provides support for predictions of the heterospecific attraction hypothesis and suggests that information on habitat quality with reference to both food availability and safe breeding sites are important in using heterospecifics as cues. Based on Chaffinch response data, artificially increased resident densities were not high enough for competitive effects between residents and migrants to decrease heterospecific attraction. It seems unlikely that in northern environments natural resident densities will reach high levels where competitive effects would occur, therefore heterospecific attraction will always be beneficial. This study again shows the importance of heterospecific attraction in migrant habitat selection and as a process promoting species diversity in northern breeding bird assemblages.     

Methane emissions along a salt marsh salinity gradient

The seasonal flux of methane to the atmosphere was measured at three salt marsh sites along a tidal creek. Average soil salinities at the sites ranged from 5 to 17 ppt and fluxes ranged from below detection limits (less than 0.3 mgCH₄ m^-2 d^-1) to 259 mgCH₄ m^-2 d^-1. Annual flux to the atmosphere was 5.6 gCH₄ m^-2 from the most saline site, 22.4 gCH₄ m^-2 from the intermediate site, and 18.2 gCH₄ m^-2 from the freshest of the three sites. Regression of the amount of methane in the soil with flux indicates that changes in this soil methane can account for 64% of the observed variation in flux. Data on pore water distributions of sulfate suggests that the activity of sulfate reducing bacteria is a primary control on methane flux in these transitional environments. Results indicate that relatively high emissions of methane from salt marshes can occur at soil salinities up to approximately 13 ppt. When these data are combined with other tidal marsh studies, annual CH₄ flux to the atmosphere shows a strong negative correlation with the long term average soil salinity over a range from essentially fresh water to 26 ppt.     

Dynamics of bacterial community succession in a salt marsh chronosequence: evidences for temporal niche partitioning

The mechanisms underlying community assembly and promoting temporal succession are often overlooked in microbial ecology. Here, we studied an undisturbed salt marsh chronosequence, spanning over a century of ecosystem development, to understand bacterial succession in soil. We used 16S rRNA gene-based quantitative PCR to determine bacterial abundance and multitag 454 pyrosequencing for community composition and diversity analyses. Despite 10-fold lower 16S rRNA gene abundances, the initial stages of soil development held higher phylogenetic diversities than the soil at late succession. Temporal variations in phylogenetic β-diversity were greater at initial stages of soil development, possibly as a result of the great dynamism imposed by the daily influence of the tide, promoting high immigration rates. Allogenic succession of bacterial communities was mostly driven by shifts in the soil physical structure, as well as variations in pH and salinity, which collectively explained 84.5% of the variation concerning community assemblage. The community assembly data for each successional stage were integrated into a network co-occurrence analysis, revealing higher complexity at initial stages, coinciding with great dynamism in turnover and environmental variability. Contrary to a spatial niche-based perspective of bacterial community assembly, we suggest temporal niche partitioning as the dominant mechanism of assembly (promoting more phylotype co-occurrence) in the initial stages of succession, where continuous environmental change results in the existence of multiple niches over short periods of time.     

Modulation of respiratory metabolism in response to nutrient changes along a soil chronosequence

Laboratory studies indicate that plant respiratory efficiency may decrease in response to low nutrient availability due to increased partitioning of electrons to the energy‐wasteful alternative oxidase (AOX); however, field confirmation of this hypothesis is lacking. We therefore investigated plant respiratory changes associated with succession and retrogression in soils aged from 10 to 120 000 years along the Franz Josef soil chronosequence, New Zealand. Respiration rates and electron partitioning were determined based on oxygen isotopic fractionation. Leaf structural traits, foliar nutrient status, carbohydrates and species composition were measured as explanatory variables. Although soil nutrient levels and species composition varied by site along the chronosequence, foliar respiration across all sites and species corresponded strongly with leaf nitrogen concentration (r² = 0.8). In contrast, electron partitioning declined with increasing nitrogen/phosphorus (r² = 0.23) and AOX activity correlated with phosphorus (r² = 0.64). Independently, total respiration was further associated with foliar Cu, possibly linked to its effect on AOX. Independent control of AOX and cytochrome pathway activities is also discussed. These responses of plant terminal respiratory oxidases – and therefore respiratory carbon efficiency – to multiple nutrient deficiencies demonstrate that modulation of respiratory metabolism may play an important role in plant responses to nutrient gradients.     

Trap color and placement affects estimates of insect family-level abundance and diversity in a Nebraska salt marsh

Sampling programs to establish baseline ecosystem information (e.g., species abundance and diversity) often fail to consider the potential influence of sampling techniques on results. Research on sampling economically important insects has demonstrated the possible influences of trap color and trap placement on results, but few data have been collected from natural environments. Consequently, we examined the effects of color (yellow and blue) and placement (exposed and shaded by plants) of sticky traps on insect captures and diversity estimates from a Nebraska inland salt marsh community. We identified 1913 specimens from 67 insect families collected during five trapping dates in July 1996. More Cicindelidae were collected on exposed traps, and more Staphylinidae, Dolichopodidae, Cicadellidae, and Thripidae were collected on shaded traps. More Dolichopodidae were collected on yellow traps, while more Syrphidae and Thripidae were collected on blue. Shannon and alpha diversity measures were significantly higher for shaded traps than exposed traps, but were not affected by trap color. Our results highlight the importance of characterizing sampling techniques when establishing diversity estimates. These data provide the first complete accounting of community-level insect response to colored sticky traps and provide new information for color preference of non-economic insect species.     

Clonal structure of Elytrigia atherica along different successional stages of a salt marsh

Elytrigia atherica is a tall clonal grass species typical of higher salt marshes, but is gradually invading to the lower marshes. At young successional stages of a salt marsh, E. atherica is found sparsely dispersed in small groups of ramets. These patches increase in size and ramet density over time, eventually forming extensive swards as succession proceeds. This study investigates the change in the clonal diversity of E. atherica stands during colonization as a result of its reproductive strategy. Clonal diversities of differently sized patches of E. atherica were investigated on two lower salt-marsh sites of different age, 25 years and 35 years, respectively. Microsatellite fingerprint patterns were used to determine genet identities and to estimate relatedness and genetic differentiation between the sites, between patches within sites and within patches. The majority of the patches on both sites contained more than one genet. On the older site, the clonal diversity was higher than on the younger site. However, the clonal diversity tended to decrease with increasing patch size. Low genetic differentiation was found between the two sites, indicating habitat differentiation, whereas differentiation between patches within sites was high. It is reasoned that different environmental conditions could have resulted in different clonal structures: On an older marsh, the increase of successful seedling recruitment, due to more suitable environmental conditions, leads to an increase in clonal diversity. Over time, with increasing ramet density, intraspecific competition is likely to increase, resulting in a decrease of clonal diversity.     

Nutrient changes in water flooding the high salt marsh

Summary Water samples were collected during inundation by the tides of the littoral Spartina patens vegetation. This grass is characterized by a more or less permanent inferior layer of dead grass which is thick and uniform enough to suggest a filtering system. Water analyses demonstrated clear variation with time in P, PO₄, and Mn; this variation corresponds with changes in the level of the water during high tide, as well as with the progressive inundation of the Spartina patens vegetation.

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Résumé Des échantillons d'eau ont été récoltés pendant l'inondation par la marée de la végétation littorale de Spartina patens. Cette graminée est caractérisée par une nappe plus ou moins permanente d'herbe morte suffisamment épaisse et uniforme pour suggérer un systéme de filtrage. Les analyses ont montré une variation nette dans le contenu de P, PO₄ et Mn, une variation qui correspond avec les changements dans le niveau d'eau pendant la marée haute, aussi avec l'inondation de la nappe d'herbe mentionnée.

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This work was carried out with the aid of funds from the National Science Foundation (Grant GB 568) and from the University of Wisconsin-Milwaukee Graduate School.

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Contribution No. 8 from the Center for Great Lakes Studies of the University of Wisconsin-Milwaukee.     

Soil seed bank and driftline composition along a successional gradient on a temperate salt marsh

Abstract. This study focuses on the relationship between vegetation succession and soil seed bank composition on the Schiermonnikoog (The Netherlands) salt marsh over 100 yr. The importance of driftline material in seed dispersal and the relationship with succession is also investigated. The results indicate that the majority of species have a transient or short‐term seed persistent bank. Seeds of most species are able to float over the salt marsh and become concentrated in the driftline higher up the marsh. After plants have established a seed bank forms, which disappears when vegetation is replaced by later‐successional species. Exceptions are Spergularia mar‐itima, which is still present in the seed bank of late successional stages, and Juncus gerardi and Glaux maritima, which appear in the seed bank of early successional stages, but are absent in the vegetation. Based on the results of this study constraints and possibilities for salt‐marsh restoration by de‐embankment are discussed.     

Long-term changes of salt marsh communities by cattle grazing

Over a period of 9 years a grazing experiment was carried out in the mainland salt marsh of the Leybucht (Niedersachsen) with three stocking rates, namely, 0.5 ha^-1, 1 ha^-1, and 2 cattle ha^-1. These were also compared with an abandoned area. The results are based on sampling of the invertebrates in 1980, 1981, 1982, and 1988, and of the vegetation in 1980 and 1988. The rate of sedimentation is highest in the Puccinellia maritima-zone and decreases with the increase of stocking rates. The Elymus pycnanthus vegetation type becomes dominant in the higher salt marsh in the abandoned site. The canopy height decreases with increasing stocking rate, whereas a gradient in the structure of the vegetation develops with the lowest stocking rate. The population densities, the species-richness and the community diversity of invertebrates increases after the cessation of grazing. The high rate of sedimentation in the abandoned site promotes the immigration of species from higher salt marsh levels and adjacent grasslands, and eventually halotopophilous species and communities may disappear. On the other hand grazing reduces numerous species living both in or on upper parts of the vegetation or being sensitive to trampling by cattle. The community structure shows that the salt marsh ecosystem changed from a food web dominated by plant feeding animals to a food web dominated by animals foraging on detritus. The salt marsh management has to be differentiated into both ungrazed and lightly grazed areas (each 50%) or an overall grazing in large areas with less than 0.5 cattle ha^-1.     

Compositional changes over space and time along an occurrence–abundance continuum: anthropogenic homogenization of the North American avifauna

Aim Changes in community attributes due to the influence of anthropogenic activities have been examined primarily using occurrence data with little consideration of associated changes in abundance. To determine how this influences our perception of biotic homogenization, we examined compositional patterns for avian assemblages over space and time along an occurrence–abundance continuum. Location The contiguous United States and southern Canada. Methods We examined avian assemblages at 951 Breeding Bird Survey (BBS) routes from 1970 to 2005 that contained a total of 443 species. We used five dissimilarity indices to estimate compositional patterns along an occurrence–abundance continuum of assemblage structure (from species occurrence to transformed abundance to raw abundance) for 396,925 unique combinations of BBS route pairs. We examined annual plots of dissimilarity by distance between BBS routes pairs to estimate spatial and temporal patterns for each index. Results Dissimilarity declined with increasing distance between route pairs for occurrence and transformed abundance, reaching an asymptote at approximately 2500 km. For raw abundance, dissimilarity peaked at intermediate distances (1000–2500 km) with no evidence of an asymptote. Avian assemblages became more similar over time at all points along the continuum. Occurrence and transformed abundance presented the weakest temporal trends, which were uniform or poorly delineated as a function of distance between routes. Raw abundance presented the strongest temporal trends, which declined in strength with increasing distance between routes. Main conclusions With the addition of abundance, there was a substantial and consistent pattern of degradation of β‐diversity for North American avifauna that differed considerably from that observed from occurrence data alone. The geographical expansion of a few species, which recently benefited from the direct and indirect consequences of anthropogenic activities, probably played a prominent role in these patterns. When broad‐scale expansions in occupancy are evident, minor gains in similarity based on species occurrence can mask more substantial gains in similarity based on local abundance. When abundance information is unavailable, its role can be estimated by how occupancy has responded geographically to anthropogenic activities and the expectations of the abundance–occupancy relationship. Our findings support previous work indicating that widespread and locally abundant species will tend to benefit more from anthropogenic activities, creating a possible synergism that enhances biotic homogenization.     

Modeling productivity of a salt marsh

A model of primary productivity in a salt marsh is developed and compared to a regression analysis study of data showing dependence of growth on growing season, mean tidal height, and average monthly temperatures for several grass species.     

Proximate nutritive value changes during decomposition of salt marsh plants

Recognition of salt marsh plant detritus as a nutritious source of food for estuarine consumers prompted investigation of in situ decomposition and proximate nutritive values of three plants and their detritus namely: Spartina cynosuroides and Distichlis spicata (Gramineae) and Scirpus americanus (Cyperaceae) growing abundantly in Mississippi tidal marshes. During decomposition to particulate detritus, these plants retain 60–70% organic content and the caloric value either remains the same or increases slightly. Crude fiber, carbohydrate, and fat contents decline but protein shows 96–300% increase from dead plants to particulate detritus stage.     

To identify impacts in variable systems using anomalous changes: a salt marsh example

A method is proposed to identify impacts of habitat modification in cases where it is difficult to site experimental and control samples. This problem occurs especially in heterogeneous systems, but may pose difficulties in any field experimental situation. The method is relevant to the situation where treated (modified) and untreated sites are spread over a range of habitat types. Types of change are identified and compared to treatments. If a specific change type is associated with a particular treatment then it is likely that the change is causally related to the treatment. There are five stages in the analysis. First, the classes or states of the sample sites, over a period of time, are identified (by numerical classification). Second, for each sample site, the sequence of states is listed. Third, transition matrices are made for each sample site to show the changes which have occurred. Fourth, the transition matrices are classified, to identify types of change. Finally, we use the Chisquared test to indicate whether the treated and untreated sites are associated with particular types of change. As an example, we refer to habitat modification to manage salt-marsh mosquitoes and we evaluate impacts on the environment mainly through changes to the vegetation. We consider that the method has potential to identify changes in heterogeneous systems even though little change was identified in the particular salt marsh studied.     

Decadal changes in vegetation of a subarctic salt marsh used by lesser snow and Canada geese

In the Hudson–James Bay system, grubbing and grazing by lesser snow geese have resulted in severe devegetation of coastal marshes. These changes likely represent an example of an alternative stable state; however, long-term datasets documenting whether revegetation is occurring are scarce. Here, we report results of a 10-year study investigating changes in the state of a degraded salt marsh system on the north coast of Akimiski Island, Nunavut. Four transects were intensively sampled in 1998 and 2008, two within the dense nesting and brood-rearing area of a snow geese colony, one on the colony edge, and one outside it; all of these sites were also used by broods of Canada geese. Key forage species (Puccinellia phryganodes, Festuca rubra, Carex subspathacea) were less common near the colony center than elsewhere; biomass of Puccinellia also tended to be lower in more central areas. Forage species often increased in abundance between samplings, but the magnitude of changes was small. In contrast, non-forage species (Salicornia, Spergularia, Glaux) often reached high abundance within the colony center; some (Salicornia) decreased while others (Spergularia) increased. We argue the degraded state was initiated by foraging damage from an exceptional stopover of 295,000 staging birds in 1972 and that the combined foraging pressure of relatively small numbers of nesting and migrant geese since then, coupled with soil changes, has been sufficient to maintain devegetated areas as a persistent alternative state. Whether or not this state is truly stable, further recovery is likely to be very slow.     

Seasonal changes in reflectance and standing crop biomass in three salt marsh communities

Reflectance of red (656-705 nm) and infrared (776-826 nm) solar radiation and standing crop biomass were measured in three salt marsh communities at intervals of approximately 2 weeks between February and August 1974. Red reflectance declined at the onset of greening in each community and was correlated with standing crop of green biomass. Infrared reflectance increased substantially in the shrub community but less in the grass and sedge communities. The inverse of red reflectance was found to be a reliable predictor of green biomass in sedge and grass communities, but not in a shrub community.