Toxicity of reduced nitrogen in eelgrass (Zostera marina) is highly dependent on shoot density and pH

In sheltered, eutrophicated estuaries, reduced nitrogen (NHx), and pH levels in the water layer can be greatly enhanced. In laboratory experiments, we studied the interactive effects of NHx, pH, and shoot density on the physiology and survival of eelgrass (Zostera marina). We tested long-term tolerance to NHx at pH 8 in a 5-week experiment. Short-term tolerance was tested for two shoot densities at both pH 8 and 9 in a 5-day experiment. At pH 8, eelgrass accumulated nitrogen as free amino acids when exposed to high loads of NHx, but showed no signs of necrosis. Low shoot density treatments became necrotic within days when exposed to NHx at pH 9. Increased NH3 intrusion and carbon limitation seemed to be the cause of this, as intracellular NHx could no longer be assimilated. Remarkably, experiments with high shoot densities at pH 9 showed hardly any necrosis, as the plants seemed to be able to alleviate the toxic effects of high NHx loads through joint NHx uptake. Our results suggest that NHx toxicity can be important in worldwide observed seagrass mass mortalities. We argue that the mitigating effect of high seagrass biomass on NHx toxicity is a positive feedback mechanism, potentially leading to alternative stable states in field conditions.     

Eelgrass, Zostera marina, growth along depth gradients: upper boundaries of the variation as a powerful predictive tool

1200 measurements of eelgrass ( Zostera marina ) biomass, shoot density and cover along 19 depth gradients in Øresund, located between Denmark and Sweden, were analysed to characterise growth of eelgrass in relation to depth. The large data set allowed analyses of boundaries of distribution as well as of average trends. Natural variability is large in shallow water where populations are disturbed by wave action and other physical parameters. Models based on average values, therefore, did not adequately describe growth regulation by resources, and only explained a minor part (up to 30%) of the overall variation in data. In contrast, boundary functions, which describe the upper bounds of distributions, focus on the variation produced by the ultimately growth-regulating resource, and therefore provide models with high predictive power. An exponential model explained up to 90% of the variation in upper bounds of eelgrass shoot density as a function of depth and indicated that shoot density was ultimately regulated by light availability. The boundary functions demonstrated that eelgrass shoot density, biomass and cover followed markedly different patterns as functions of depth and were affected differently by the factors governing their distribution. In addition, boundary functions revealed informative spatial structures in data and illustrated whether a given general trend was caused by changes in maximum values, minimum values or both. For example, upper and lower boundaries of biomass-shoot density relations changed markedly with depth, demonstrating depth-related changes in intraspecific succession and competition patterns. Boundary functions are therefore suggested as a promising tool for analysing ultimate regulating factors of distribution and growth of organisms when large data sets are available.     

A simulation model of production,seasonal changes in biomass and distribution of eelgrass (Zostera marina) in Lake Grevelingen

Summary A simulation model has been described, based on data from Lake Grevelingen, The Netherlands, as a predictive tool for lake management. The model has been developed as part of a large-scale aquatic modelling effort in Lake Grevelingen, carried out in close cooperation with the Delft Hydraulics Laboratory and the Delta Department, Environmental Research Division of the Ministry of Transport and Public Works. Available data on growth rates per unit eelgrass biomass, obtained with the leaf-marking technique, and on above- en below ground biomass and shoot density changes per unit area have been used. A space limitation depending on density of the above ground biomass and a growth limitation due to shortage in below ground biomass have been introduced. The seasonal changes in eelgrass production, both above and below ground, have been simulated as functions of the external forcing variables light, water temperature, wind generated water movements and of the internal control variables due to aging of the plant material. The vertical distribution of eelgrass can be partly explained from the modelling results on space, light and below ground biomass limitations. From the shore down to about 1 m waterdepth the above ground eelgrass biomass suffers from space limitation. Between 1 and 2 m production and biomass reach maximum values. Between 2 and 3 m waterdepth the above ground eelgrass growth is limited by the availability of below ground biomass. Between 3 and 5 m waterdepth both below ground biomass and light are the growth-limiting factors. Below 5 m waterdepth light is not sufficient to sustain net growth of eelgrass from rhizomes. Together with additional data — not used in the model — on seed production and growth of eelgrass shoots from seeds the vertical and horizontal distribution of the dominant macrophyte in the lake can be explained.     

Plant-herbivore interactions mediated by plant toxicity

We explore the impact of plant toxicity on the dynamics of a plant-herbivore interaction, such as that of a mammalian browser and its plant forage species, by studying a mathematical model that includes a toxin-determined functional response. In this functional response, the traditional Holling Type 2 response is modified to include the negative effect of toxin on herbivore growth, which can overwhelm the positive effect of biomass ingestion at sufficiently high plant toxicant concentrations. Two types of consumption decisions of the herbivore are considered. One of these (Case 1) incorporates the adaptation of the herbivore to control its rate of consumption of plant items when that is likely to lead to levels of toxicity that more than offset the marginal gain to the herbivore of consuming more plant biomass, while the other (Case 2) simply assumes that, although the herbivore’s rate of ingestion of plant biomass is negatively affected by increasing ingestion of toxicant relative to the load it can safely deal with, the herbivore is not able to prevent detrimental or even lethal levels of toxicant intake. A primary result of this work is that these differences in behavior lead to dramatically different outcomes, summarized in bifurcation diagrams. In Case 2, a wide variety of dynamics may occur due to the interplay of Holling Type 2 dynamics and the effect of the plant toxicant. These dynamics include the occurrence of bistability, in which both a periodic solution and the herbivore-extinction equilibrium are attractors, as well the possibility of a homoclinic bifurcation. Whether the herbivore goes to extinction in the bistable case depends on initial conditions of herbivore and plant biomasses. For relatively low herbivore resource acquisition rates, the toxicant effect increases the likelihood of ‘paradox of enrichment’ type limit cycle oscillations, but at higher resource acquisition rates, the toxicant may decrease the likelihood of these cycles.     

Variable responses of native eelgrass Zostera marina to a non-indigenous bivalve Musculista senhousia

The transport and establishment of non-indigenous species in coastal marine environments are increasing worldwide, yet few studies have experimentally addressed the interactions between potentially dominant non-native species and native organisms. We studied the effects of the introduced mussel Musculista senhousia on leaf and rhizome growth and shoot density of eelgrass Zostera marina in San Diego Bay, California. We added M. senhousia over a natural range in biomass (0–1200 g dry mass/m²) to eelgrass in transplanted and established beds. The effects of the non-indigenous mussel varied from facilitation to interference depending on time, the abundance of M. senhousia, and the response variable considered. Consistent results were that mussel additions linearly inhibited eelgrass rhizome elongation rates. With 800 g dry mass/m² of M. senhousia, eelgrass rhizomes grew 40% less than controls in two eelgrass transplantations and in one established eelgrass bed. These results indicate that M. senhousia, could both impair the success of transplantations of eelgrass, which spread vegetatively by rhizomes, and the spread of established Z. marina beds to areas inhabited by M. senhousia. Although effects on leaf growth were not always significant, in August in both eelgrass transplantations and established meadows leaf growth was fertilized by mussels, and showed a saturation-type relationship to sediment ammonium concentrations. Ammonium concentrations and sediment organic content were linear functions of mussel biomass. We found only small, non-consistent effects of M. senhousia on shoot density of eelgrass over 6-month periods. In established eelgrass beds, but not in transplanted eelgrass patches (≈0.8 m in diameter), added mussels suffered large declines. Hence, eelgrass is likely to be affected by M. senhousia primarily where Z. marina beds are patchy and sparse. Our study has management and conservation implications for eelgrass because many beds are already seriously degraded and limited in southern California where the mussel is very abundant. Received: 31 May 1997 / Accepted: 4 September 1997     

Photoinhibition and the assembly of light‐limited phytoplankton communities

Photoinhibition is characterised by a decreasing rate of photosynthesis with increasing light. It occurs in many photosynthetic organisms and is especially apparent in phytoplankton species sensitive to high light. Yet, the population and community level consequences of photoinhibition are not well understood. Here, we present a resource competition model that includes photoinhibition. The model shows that, in strong light, photoinhibition leads to an increase of the specific growth rate with increasing population density due to self‐shading. This so‐called Allee effect can be either weak or strong. In monoculture, a strong Allee effect results in two alternative stable states. A low population density does not provide sufficient shade to protect itself against photoinhibition, such that the population goes extinct. Conversely, above a threshold population density the population may create sufficiently turbid conditions to suppress photoinhibition, so that the population can establish itself. When several species compete for light, a species which cannot establish itself due to photoinhibition can be facilitated by other species less sensitive to photoinhibition. If such facilitators are absent, photoinhibition may cause alternative stable states in community composition. Since each alternative stable state is dominated by a single species, photoinhibition does not favour species coexistence. The model predictions are consistent with published competition experiments, and illustrate the complex effects of photoinhibition on community assembly.     

Limited recovery following a massive seagrass decline in subarctic eastern Canada

Over the last few decades, there has been an increasing recognition for seagrasses' contribution to the functioning of nearshore ecosystems and climate change mitigation. Nevertheless, seagrass ecosystems have been deteriorating globally at an accelerating rate during recent decades. In 2017, research into the condition of eelgrass (Zostera marina) along the eastern coast of James Bay, Canada, was initiated in response to reports of eelgrass decline by the Cree First Nations of Eeyou Istchee. As part of this research, we compiled and analyzed two decades of eelgrass cover data and three decades of eelgrass monitoring data (biomass and density) to detect changes and assess possible environmental drivers. We detected a major decline in eelgrass condition between 1995 and 1999, which encompassed the entire east coast of James Bay. Surveys conducted in 2019 and 2020 indicated limited changes post-decline, for example, low eelgrass cover (<25%), low aboveground biomass, smaller shoots than before 1995, and marginally low densities persisted at most sites. Overall, the synthesized datasets show a 40% loss of eelgrass meadows with >50% cover in eastern James Bay since 1995, representing the largest scale eelgrass decline documented in eastern Canada since the massive die-off event that occurred in the 1930s along the North Atlantic coast. Using biomass data collected since 1982, but geographically limited to the sector of the coast near the regulated La Grande River, generalized additive modeling revealed eelgrass meadows are affected by local sea surface temperature, early ice breakup, and higher summer freshwater discharge. Our results caution against assuming subarctic seagrass ecosystems have avoided recent global declines or will benefit from ongoing climate warming.     

The toxicity to Clarias lazera of copper and zinc applied jointly

1. The acute toxicity to juvenile Clarias lazera of a mixture of copper and zinc over a 96 hr exposure period was determined. Fish were exposed to the summation of half the 96 hr TLm value of each toxicant. 2. Percentage survival was much reduced indicating that the metals potentiate each others lethal action. 3. Comparison between metal residues in fish exposed to copper and zinc or to their mixture showed that the uptake of one metal was decreased by the presence of the other. 4. Toxic effects of the mixture on the physiological parameters studied were mainly attributable to copper, indicating that the presence of zinc did not influence the mode of action of copper.     

Restoring Eelgrass (Zostera marina L.) Habitats Using a Simple and Effective Transplanting Technique

Eelgrass beds in coastal waters of China have declined substantially over the past 30 years. In this study, a simple new transplanting technique was developed for eelgrass (Zostera marina L.) restoration. To assist in anchoring single shoots, several rhizomes of rooted shoots were bound to a small elongate stone (50–150 g) with biodegradable thread (cotton or hemp), and then the bound packet was buried at an angle in the sediments at a depth of 2–4 cm. This stone anchoring method was used to transplant eelgrass in early November 2009 and late May 2010 in Huiquan Bay, Qingdao. The method led to high success. Three month survivorship of the transplanted shoots at the two transplant sites was >95%. From April 20 to November 19, 2012, the following characteristics of the 2009 and 2010 transplanted eelgrass beds were monitored: morphological changes, shoot density, shoot height, leaf biomass, and sediment particle size. Results showed that the sexual reproduction period of the planted eelgrass was from April to August, and vegetative reproduction reached its peak in autumn. Maximum shoot height and biomass were observed in June and July. After becoming established, the transplanted eelgrass beds were statistically equal to natural eelgrass beds nearby in terms of shoot height, biomass, and seasonal variations. This indicates that the transplant technique is effective for eelgrass restoration in coastal waters.     

EPIPHYTE-GRAZER INTERACTIONS ON ZOSTERA MARINA (ANTHOPHYTA: MONOCOTYLEDONES): EFFECTS OF DENSITY ON COMMUNITY FUNCTION1

Interactions between algal epiphytes and their grazers can have a significant impact on the structure and function of eelgrass (Zostera marina L.) meadows. In Puget Sound, the herbivorous gastropod Lacuna variegata Carpenter and its congeners appear to remove large quantities of the epiphytic community from eelgrass blades. When snails at typical field densities were used in microcosms, Lacuna significantly reduced epiphytic biomass and areal productivity. Biomass-specific productivity of the epiphytic community showed an increasing trend with increasing snail density. Epiphytic productivity increased nonlinearly with increasing epiphytic biomass. The commonly used logistic population growth formula adequately described this relationship. Grazing rate also increased nonlinearly with increasing epiphytic biomass. The Hailing equation adequately described the relationship between grazing rate and epiphytic biomass. The proportion of the epiphytic biomass found on the oldest blade of an eelgrass shoot was related linearly to epiphytic biomass, suggesting that a constant fraction of the epiphytic community is lost regardless of epiphytic density. Lacuna clearly removed large quantities of epiphytic material from eelgrass blades, significantly altering community function. Modified Lotka-Volterra equations, incorporating the logistic growth form and Hailing grazing equation, should prove useful in modeling the epiphyte–grazer interaction.     

Potential for Sudden Shifts in Transient Systems: Distinguishing Between Local and Landscape-Scale Processes

Thorough understanding of the potential for threshold dynamics and catastrophic shifts to occur in natural systems is of great importance for ecosystem conservation and restoration. However, verifying the presence of alternative stable states, one of the theoretical explanations for sudden shifts in natural systems, has proven to be a major challenge. We examine processes on local and landscape scales in salt-marsh pioneer zones, to assess the presence of alternative stable states in this system. To that end, we investigated the presence of typical characteristics of alternative stable states: bimodality and threshold dynamics. We also studied whether vegetation patches remained stable over long time periods. Analysis of false-color aerial photographs revealed clear bimodality in plant biomass distribution. By transplanting Spartina anglica plants of three different biomass classes on three geographically different marshes, we showed that a biomass threshold limits the establishment of Spartina patches, potentially explaining their patchy distribution. The presence of bimodality and biomass thresholds points to the presence of alternative stable states and the potential for sudden shifts, at small, within-patch scales and on short time scales. However, overlay analysis of aerial photographs from a salt marsh in The Netherlands, covering a time span of 22 years, revealed that there was little long-term stability of patches, as vegetation cover in this area is slowly increasing. Our results suggest that the concept of alternative stable states is applicable to the salt-marsh pioneer vegetation on small spatio-temporal scales. However, the concept does not apply to long-term dynamics of decades or centuries of heterogeneous salt-marsh pioneer zones, as landscape-scale processes may determine the large-scale dynamics of salt marshes. Hence, our results provide the interesting perspective that threshold dynamics may occur in systems with, on the long term, only a single stable state. Author Contributions: Bregje van Wesenbeeck executed the major part of this research and wrote this paper. Johan van de Koppel was involved in every part of this study and restructured major parts of this paper. Peter Herman helped with statistical analyses. Mark Bertness adjusted the design of this study and provided new views. Daphne van der Wal performed GIS analyses. Jan Bakker supervised and facilitated field work. Tjeerd Bouma supervised design of study and paper and substantially contributed to the writing of this paper. All authors commented on several drafts of this paper.     

Acute and chronic effects of Cr(VI) on Hypsiboas pulchellus embryos and tadpoles

In the last few years there has been great concern about declines in the abundance of several species of amphibians around the world. Among amphibians, anurans have a biphasic life cycle, with aquatic tadpoles and generally terrestrial adults, and they have an extremely permeable skin, making them excellent indicators of the health of the environment. A number of different causes have been suggested for the global decline of anurans, the pollution of their habitat by chemical stressors being considered one of the major factors. Among chemical stressors, heavy metals are known for their high toxicity at very low concentrations. This study assessed short- (96 h, 'acute') and long-term (1272 h, 'chronic') exposure to Cr(VI) at lethal (3 to 90 mg 1(-1)) and sublethal concentrations (0.001 to 12 mg 1(-1)) on Hypsiboaspulchellus (previously called Hyla pulchella; see Faivovich et al. 2005) tadpoles (Fam. Hylidae) from central eastern Argentina. Fertilized eggs collected from a clean pond near La Plata (Buenos Aires Province) were used for acute and chronic toxicity testing. Assays were done under controlled laboratory conditions. Results of chronic exposure were used to assess the effect of factors such as toxicant concentration and age of organisms at the beginning of exposure on the response variables (growth, development and survival until metamorphosis). Results indicated a higher sensitivity to Cr(VI) of individuals first exposed as tadpoles than those first exposed as embryos during acute and chronic exposure. Exposure to the highest sublethal concentrations (6 to 12 mg 1(-1)) of the toxicant showed early inhibitory effects on growth of all treated organisms compensated at longer exposure periods with an increase in the growth rate compared to the control groups.     

Mathematical modeling of colony formation in algal blooms: phenotypic plasticity in cyanobacteria

In this paper, we analyzed a mathematical model of algal-grazer dynamics, including the effect of colony formation, which is an example of phenotypic plasticity. The model consists of three variables, which correspond to the biomasses of unicellular algae, colonial algae, and herbivorous zooplankton. Among these organisms, colonial algae are the main components of algal blooms. This aquatic system has two stable attractors, which can be identified as a zooplankton-dominated (ZD) state and an algal-dominated (AD) state, respectively. Assuming that the handling time of zooplankton on colonial algae increases with the colonial algae biomass, we discovered that bistability can occur within the model system. The applicability of alternative stable states in algae-grazer dynamics as a framework for explaining the algal blooms in real lake ecosystems, thus, seems to depend on whether the assumption mentioned above is met in natural circumstances.     

Effects of toxicants on populations: A qualitative approach II. first order kinetics

System level effects exhibited by a population subjected to a chronic or an acute dose of toxicant are the emphasis of this study. A three dimensional model of a toxicant and a population, with state variables (the population biomass, the concentration of toxicant in an organism, and the concentration of toxicant in the environment) coupled by a linear dose-response function, is analyzed analytically. One of the main results presents sufficient conditions, in terms of a system level parameter, for the persistence, and for the extinction, of a population exposed to a chronic dose of toxicant. When depuration and degradation are negligible processes, the effects of toxicant accumulation associated with an acute exposure of a population are analyzed in some detail. Both persistence and extinction are shown to be viable behavior modes of a population in this biochemical setting.     

Wetland macrophyte diversity, trophic status and phytoplankton： a case study of the cascading effects of an invasive herbivore

Shallow water bodies can exist in alternative stable states, a clear water state with high coverage of macrophytes or a turbid state with high phytoplankton biomass. The alternative equilibria hypothesis has been proposed to explain the occurrence of the alternative stable states (Scheffer et al., 1993)[1], which assumes that: 1),     

Competition in the presence of a lethal external inhibitor

The study considers two organisms competing for a nutrient in an open system in the presence of an inhibitor (or toxicant). The inhibitor is input at a constant rate and is lethal to one competitor while being taken up by the other without harm. This is in contrast to previous studies, where the inhibitor decreases the reproductive rate of one of the organisms. The mathematical result of the lethal effect, modeled by a mass action term, is that the system cannot be reduced to a monotone dynamical system of one order lower as is common with chemostat-like problems. The model is described by four non-linear, ordinary differential equations and we seek to describe the asymptotic behavior as a function of the parameters of the system. Several global exclusion results are presented with mathematical proofs. However, in the case of coexistence, oscillatory behavior is possible and the study proceeds with numerical examples. The model is relevant to bioremediation problems in nature and to laboratory bio-reactors.     

Mechanism of Antifungal Action of 2,4,5,6-Tetrachloroisophthalonitrile

Studies of the toxicity of 2,4,5,6-tetrachloroisophthalonitrile (TCIN) to cells of Saccharomyces pastorianus and Neurospora crassa showed that 2 to 4 μg/ml of the toxicant were required to inhibit growth. Several thiol compounds reversed toxicity to growth. Glucose oxidation was severely impaired in treated cells of both test organisms. The toxicant at 2 or 4 μg/ml markedly reduced soluble thiol content of these cells. Bound thiol content was less affected in S. pastorianus cells than soluble thiol content. Uptake of toxicant by yeast cells was accompanied by formation of derivatives, some of which resembled those formed by reaction of glutathione with TCIN in vitro. Coenzyme A, glutathione, and 2-mercaptoethanol readily formed derivatives with TCIN in vitro. The nature of these derivatives was studied using 2-mercaptoethanol products as model substituents. Four derivatives were formed with 2-mercaptoethanol each with similar functional groups but showing dissimilar degrees of mobility during silica gel chromatography. Evidence indicated that these are derivatives of TCIN in which 1 to 4 of the halogens has been substituted by 2-mercaptoethanol. The mechanism of fungicidal action of TCIN is attributed to thiol inactivation.     

Growth dynamics of Zostera in Sevastopol Bay (Crimea,Black Sea)

Density, biomass and primary productivity of eelgrass (Zostera marina L.) and density and biomass of Zostera noltii Hornem. were studied at three locations in Sevastopol Bay, Crimean Peninsula, Ukraine, in April 2002, late September 2002, and late January 2003 at 3 m and 5 m depths. All three growth parameters varied by station, depth, and month. The aboveground biomass (AGB) was greater in September than in April or January at 3 m. It was greater at 5 m than at 3 m in April at one station. For Z. noltii, results were more variable as to month. For belowground biomass (BGB), month and station relationships were not clear cut. It was generally true that total biomass was greatest in September. Significant differences in density, AGB and total biomass were observed for station and month in eelgrass, while in BGB, these differences were significant for depth and for month. Primary production in eelgrass was greatest at both depths in April as compared to September or January. Reproductive shoots were found only during April. Overall, seedlings were found in all collection periods and depths, but were most abundant at the three stations in April.     

Light dependence of Zostera marina annual growth dynamics in estuaries subject to different degrees of eutrophication

We examined the coupling between eelgrass growth dynamics and surface irradiance over an annual cycle in four shallow estuaries of the Waquoit Bay system (MA, USA) that have similar physical characteristics, but are subject to different land-derived nitrogen loading rates and eutrophication. Contrary to our hypothesis, the results show that most measures of eelgrass demographics were positively correlated with surface irradiance in all four estuaries. Of the 45 regression models adjusted between irradiance and demographic variables (density, plastochrone intervals, and above- or belowground biomass, growth, and production, on both a per shoot and areal basis), only nine were non-significant, and only six of those corresponded to the eutrophic estuaries. There was a lack of correlation between shoot density and irradiance in the eutrophic estuaries, in contrast to the strong coupling in estuaries with the lowest nitrogen loads. Severe light limitation and other deleterious impacts imposed by macroalgal canopies on newly recruiting shoots in the eutrophic estuaries likely contributed to the lack of correlation between shoot density and irradiance at the water's surface. Because the range in eutrophication included the range of conditions at which eelgrass can survive, the relatively consistent temporal coupling between surface irradiance and most eelgrass demographic variables found here may also be a feature of other shallow temperate systems undergoing eutrophication, and indicates a measure of plant recruitment (density) to be one of the first parameters to become uncoupled from light reaching the water's surface.     

How do toxicants affect epidemiological dynamics?

Populations are formed of their constituent interacting individuals, each with their own respective within‐host biological processes. Infection not only spreads within the host organism but also spreads between individuals. Here we propose and study a multilevel model which links the within‐host statuses of immunity and parasite density to population epidemiology under sublethal and lethal toxicant exposure. We analyse this nested model in order to better understand how toxicants impact the spread of disease within populations. We demonstrate that outbreak of infection within a population is completely determined by the level of toxicant exposure, and that it is maximised by intermediate toxicant dosage. We classify the population epidemiology into five phases of increasing toxicant exposure and calculate the conditions under which disease will spread, showing that there exists a threshold toxicant level under which epidemics will not occur. In general, higher toxicant load results in either extinction of the population or outbreak of infection. The within‐host statuses of the individual host also determine the outcome of the epidemic at the population level. We discuss applications of our model in the context of environmental epidemiology, predicting that increased exposure to toxicants could result in greater risk of epidemics within ecological systems. We predict that reducing sublethal toxicant exposure below our predicted safe threshold could contribute to controlling population level disease and infection.