A.J.P. Smolders

Sulfide as a soil phytotoxin—a review

In wetland soils and underwater sediments of marine, brackish and freshwater systems, the strong phytotoxin sulfide may accumulate as a result of microbial reduction of sulfate during anaerobiosis, its level depending on prevailing edaphic conditions. In this review, we compare an extensive body of literature on phytotoxic effects of this reduced sulfur compound in different ecosystem types, and review the effects of sulfide at multiple ecosystem levels: the ecophysiological functioning of individual plants, plant-microbe associations, and community effects including competition and facilitation interactions. Recent publications on multi-species interactions in the rhizosphere show even more complex mechanisms explaining sulfide resistance. It is concluded that sulfide is a potent phytotoxin, profoundly affecting plant fitness and ecosystem functioning in the full range of wetland types including coastal systems, and at several levels. Traditional toxicity testing including hydroponic approaches generally neglect rhizospheric effects, which makes it difficult to extrapolate results to real ecosystem processes. To explain the differential effects of sulfide at the different organizational levels, profound knowledge about the biogeochemical, plant physiological and ecological rhizosphere processes is vital. This information is even more important, as anthropogenic inputs of sulfur into freshwater ecosystems and organic loads into freshwater and marine systems are still much higher than natural levels, and are steeply increasing in Asia. In addition, higher temperatures as a result of global climate change may lead to higher sulfide production rates in shallow waters.

A Three-Stage Symbiosis Forms the Foundation of Seagrass Ecosystems

Ancient Associations Submarine seagrass meadows are critical to fisheries and coastline protection and provide feeding grounds for many endangered species, including dugongs and turtles, and serve as a nursery for coral reef fish. The persistence and maintenance of seagrass ecosystems have been mysterious, because accumulation of organic matter in the beds should rapidly lead to toxic sulphide levels in the sediment. Using a meta-analysis and a field study, van der Heide et al. (p. 1432) atttribute the 100-million-year success of seagrasses to a three-stage symbiosis. Seagrass beds worldwide contain high densities of small lucinid bivalves that have symbiotic sulphide-oxidizing bacteria in their gills. This association appears to relieve any sulphide stress for seagrasses, while the lucinids and their symbionts profit from the accumulation of degradable organic matter and oxygen release from seagrass roots. A marine plant, small molluscs, and their resident sulfide-oxidizing bacteria survive together. Seagrasses evolved from terrestrial plants into marine foundation species around 100 million years ago. Their ecological success, however, remains a mystery because natural organic matter accumulation within the beds should result in toxic sediment sulfide levels. Using a meta-analysis, a field study, and a laboratory experiment, we reveal how an ancient three-stage symbiosis between seagrass, lucinid bivalves, and their sulfide-oxidizing gill bacteria reduces sulfide stress for seagrasses. We found that the bivalve–sulfide-oxidizer symbiosis reduced sulfide levels and enhanced seagrass production as measured in biomass. In turn, the bivalves and their endosymbionts profit from organic matter accumulation and radial oxygen release from the seagrass roots. These findings elucidate the long-term success of seagrasses in warm waters and offer new prospects for seagrass ecosystem conservation.

Anaerobic oxidization of methane in a minerotrophic peatland: Enrichment of nitrite-dependent methane-oxidizing bacteria

ABSTRACT The importance of anaerobic oxidation of methane (AOM) as a methane sink in freshwater systems is largely unexplored, particularly in peat ecosystems. Nitrite-dependent anaerobic methane oxidation (n-damo) was recently discovered and reported to be catalyzed by the bacterium “Candidatus Methylomirabilis oxyfera,” which is affiliated with the NC10 phylum. So far, several “Ca. Methylomirabilis oxyfera” enrichment cultures have been obtained using a limited number of freshwater sediments or wastewater treatment sludge as the inoculum. In this study, using stable isotope measurements and porewater profiles, we investigated the potential of n-damo in a minerotrophic peatland in the south of the Netherlands that is infiltrated by nitrate-rich ground water. Methane and nitrate profiles suggested that all methane produced was oxidized before reaching the oxic layer, and NC10 bacteria could be active in the transition zone where countergradients of methane and nitrate occur. Quantitative PCR showed high NC10 bacterial cell numbers at this methane-nitrate transition zone. This soil section was used to enrich the prevalent NC10 bacteria in a continuous culture supplied with methane and nitrite at an in situ pH of 6.2. An enrichment of nitrite-reducing methanotrophic NC10 bacteria was successfully obtained. Phylogenetic analysis of retrieved 16S rRNA and pmoA genes showed that the enriched bacteria were very similar to the ones found in situ and constituted a new branch of NC10 bacteria with an identity of less than 96 and 90% to the 16S rRNA and pmoA genes of “Ca. Methylomirabilis oxyfera,” respectively. The results of this study expand our knowledge of the diversity and distribution of NC10 bacteria in the environment and highlight their potential contribution to nitrogen and methane cycles.

Interactive effects of low pH and high ammonium levels responsible for the decline of Cirsium dissectum (L.) Hill

The decline of Cirsium dissectum in dessicatingwetlands is attributed to acidification and eutrophication. Experimentalevidence was obtained for the first time on ammonium toxicity under low pH. Inahydroculture experiment, interactive effects of nitrogen forms (250μmol NH4+ or 250μmolNO3−) and pH (4, 5 or 6) were studied with regardtothe vitality of C. dissectum seedlings. The results showthat 250 μmol l−1 ammonium as sole nitrogensource only had negative effects on C. dissectum incombination with a low pH. Ammonium uptake at a rhizosphere pH of 4, resultedinlower nitrogen contents of both roots and shoots, lower internal pH of rootsandshoots and increased contents of basic amino-acids, resulting indecreased survival rate and biomass development. At higher pH, or when nitratewas the nitrogen source, these processes do not take place. This phenomenonstresses the importance of periodic influence of base rich groundwater duringthe winter in wet species-rich heathlands and grasslands, necessary torestore the acid neutralising capacity of the soil. Anthropogenic lowering ofthe groundwater table will lead to acidification enabling ammonium to becometoxic to herbaceous plant species such as C. dissectum.

Microbial Transformations of Nitrogen, Sulfur, and Iron Dictate Vegetation Composition in Wetlands: A Review

The majority of studies on rhizospheric interactions focus on pathogens, mycorrhizal symbiosis, or carbon transformations. Although the biogeochemical transformations of N, S, and Fe have profound effects on vegetation, these effects have received far less attention. This review, meant for microbiologists, biogeochemists, and plant scientists includes a call for interdisciplinary research by providing a number of challenging topics for future ecosystem research. Firstly, all three elements are plant nutrients, and microbial activity significantly changes their availability. Secondly, microbial oxidation with oxygen supplied by radial oxygen loss from roots in wetlands causes acidification, while reduction using alternative electron acceptors leads to generation of alkalinity, affecting pH in the rhizosphere, and hence plant composition. Thirdly, reduced species of all three elements may become phytotoxic. In addition, Fe cycling is tightly linked to that of S and P. As water level fluctuations are very common in wetlands, rapid changes in the availability of oxygen and alternative terminal electron acceptors will result in strong changes in the prevalent microbial redox reactions, with significant effects on plant growth. Depending on geological and hydrological settings, these interacting microbial transformations change the conditions and resource availability for plants, which are both strong drivers of vegetation development and composition by changing relative competitive strengths. Conversely, microbial composition is strongly driven by vegetation composition. Therefore, the combination of microbiological and plant ecological knowledge is essential to understand the biogeochemical and biological key factors driving heterogeneity and total (i.e., microorganisms and vegetation) community composition at different spatial and temporal scales.

Fast and Inexpensive Detection of Total and Extractable Element Concentrations in Aquatic Sediments Using Near-Infrared Reflectance Spectroscopy (NIRS)

Adequate biogeochemical characterization and monitoring of aquatic ecosystems, both for scientific purposes and for water management, pose high demands on spatial and temporal replication of chemical analyses. Near-infrared reflectance spectroscopy (NIRS) may offer a rapid, low-cost and reproducible alternative to standard analytical sample processing (digestion or extraction) and measuring techniques used for the chemical characterization of aquatic sediments. We analyzed a total of 191 sediment samples for total and NaCl-extractable concentrations of Al, Ca, Fe, K, Mg, Mn, N, Na, P, S, Si, and Zn as well as oxalate- extractable concentrations of Al, Fe, Mn and P. Based on the NIR spectral data and the reference values, calibration models for the prediction of element concentrations in unknown samples were developed and tested with an external validation procedure. Except Mn, all prediction models of total element concentrations were found to be acceptable to excellent (ratio of performance deviation: RPD 1.8–3.1). For extractable element fractions, viable model precision could be achieved for NaCl-extractable Ca, K, Mg, NH4 +-N, S and Si (RPD 1.7–2.2) and oxalate-extractable Al, Fe and P (RPD 1.9–2.3). For those elements that showed maximum total values below 3 g kg−1 prediction models were found to become increasingly critical (RPD <2.0). Low concentrations also limited the performance of NIRS calibrations for extracted elements, with critical concentration thresholds <0.1 g kg−1 and 3.3 g kg−1 for NaCl and oxalate extractions, respectively. Thus, reliable NIRS measurements of trace metals are restricted to sediments with high metal content. Nevertheless, we demonstrated the suitability of NIRS measurements to determine a large array of chemical properties of aquatic sediments. The results indicate great potential of this fast technique as an analytical tool to better understand the large spatial and temporal variation of sediment characteristics in an economically viable way.

Understanding the realised niche of an amphibious softwater plant, Eleocharis multicaulis

The West European amphibious plant Eleocharis multicaulis, characteristic of softwater lakes, is rare and endangered in many regions. The present study aimed to evaluate several presumed niche features suggested in syntaxonomic studies, to reveal other important niche variables affecting the cover of this species and to quantify these responses. A dataset of 724 environmental and vegetation variables was built from a survey of 59 plots in The Netherlands and Belgium. Discriminant analysis, Pearson goodness-of-fit calculations, weighted averages and presence profiles were used. We found that Eleocharis multicaulis performs best in base-poor environments with an or- ganic top layer and an established vegetation. The species is apparently N limited and profits from N input as long as NO3 - is dominant over NH4 + . A high atmospheric N deposition is detrimental, because the resulting strong acidification leads to dominance of NH4 + over NO3 - . Intense acidification in agricultural areas has probably been an important extinction factor in the recent past. We hypothesise that current variability of soil Si, a very good predictor for the species performance, might reflect these acidifi- cation processes. This hypothesis is supported by the fact that Si is correlated with trophic status, which is likely higher in agricultural regions. Nowadays, Eleocharis multicaulis suffers from agricultural P, K and alkalinity inputs as well as reduced oxy- gen supply (e. g. by reduced water-level dynamics), all leading to a lower redox state. These factors could bring about competitive suppression by other species, a high NH4 + /NO3 - ratio and P mobilisation.

Selecting predictors for discriminant analysis of species performance: an example from an amphibious softwater plant.

Selecting an appropriate variable subset in linear multivariate methods is an important methodological issue for ecologists. Interest often exists in obtaining general predictive capacity or in finding causal inferences from predictor variables. Because of a lack of solid knowledge on a studied phenomenon, scientists explore predictor variables in order to find the most meaningful (i.e. discriminating) ones. As an example, we modelled the response of the amphibious softwater plant Eleocharis multicaulis using canonical discriminant function analysis. We asked how variables can be selected through comparison of several methods: univariate Pearson chi-square screening, principal components analysis (PCA) and step-wise analysis, as well as combinations of some methods. We expected PCA to perform best. The selected methods were evaluated through fit and stability of the resulting discriminant functions and through correlations between these functions and the predictor variables. The chi-square subset, at P < 0.05, followed by a step-wise sub-selection, gave the best results. In contrast to expectations, PCA performed poorly, as so did step-wise analysis. The different chi-square subset methods all yielded ecologically meaningful variables, while probable noise variables were also selected by PCA and step-wise analysis. We advise against the simple use of PCA or step-wise discriminant analysis to obtain an ecologically meaningful variable subset; the former because it does not take into account the response variable, the latter because noise variables are likely to be selected. We suggest that univariate screening techniques are a worthwhile alternative for variable selection in ecology.

Coexistence and niche differentiation at large spatial scale in a West-European softwater plant community

AbstractThere is growing evidence that species are able to coexist in communities through niche separation, and that consistent community structuring can take place at the biogeographical scale, as the same biotic interactions can determine species’ fate at large scales. In this study, we document niche differentiation at a larger scale within a specific plant community of softwater lakes in Western Europe. Five species were selected for their relative frequency and wide geographical distribution within the dataset that we collected. Their niches were modelled both from presence–absence data and from ordinal abundance data, using mixed regression techniques (generalized linear mixed models and proportional odds mixed models, respectively). The modelled realized niches differed among the species on the West-European scale, although strict separation was not shown and geographical coverage is not complete. Plant strategy characterization of the species supported the assumption that functional traits underpin the niche differentiation among the species through fitness trade-offs. Mechanistic experimental research at a range of spatial scales is needed to test the importance of different community structuring mechanisms at the biogeographical scale, such as biotic interactions and environmental filtering.n

Selecting predictors for discriminant analysis of species performance: an example from an amphibious softwater plant: Selecting predictors for discriminant analysis

Selecting an appropriate variable subset in linear multivariate methods is an important methodological issue for ecologists. Interest often exists in obtaining general predictive capacity or in finding causal inferences from predictor variables. Because of a lack of solid knowledge on a studied phenomenon, scientists explore predictor variables in order to find the most meaningful (i.e. discriminating) ones. As an example, we modelled the response of the amphibious softwater plant Eleocharis multicaulis using canonical discriminant function analysis. We asked how variables can be selected through comparison of several methods: univariate Pearson chi-square screening, principal components analysis (PCA) and step-wise analysis, as well as combinations of some methods. We expected PCA to perform best. The selected methods were evaluated through fit and stability of the resulting discriminant functions and through correlations between these functions and the predictor variables. The chi-square subset, at P < 0.05, followed by a step-wise sub-selection, gave the best results. In contrast to expectations, PCA performed poorly, as so did step-wise analysis. The different chi-square subset methods all yielded ecologically meaningful variables, while probable noise variables were also selected by PCA and step-wise analysis. We advise against the simple use of PCA or step-wise discriminant analysis to obtain an ecologically meaningful variable subset; the former because it does not take into account the response variable, the latter because noise variables are likely to be selected. We suggest that univariate screening techniques are a worthwhile alternative for variable selection in ecology.