Waterfowl grazing in autumn enhances spring seedling recruitment of intertidal Zostera noltii

Feeding pits dug by waterfowl in Zostera noltii meadows are thought to promote seedling recruitment by accumulating seeds and enhancing germination. We tested the latter hypothesis by creating a series of “treatment pits” (resembling natural feeding pits) in the center and at the edge of two meadows near the Island of Sylt (Germany). Seedling density was monitored from the autumn seed set until the following spring. Seedling density (mean, SE) in treatment pits was significantly higher (4.4, 5.3) than in manipulated (2.4, 1.9) and unmanipulated controls (1.4, 0.4), as well as significantly higher in center (2.8, 0.5) relative to edge (2.5, 1.1) locations. Results confirm a facilitating effect of waterfowl grazing on seedling recruitment in spring due to seed accumulation in feeding pits in autumn. The mechanism could provide a valuable tool for the conservation of intertidal Z. noltii meadows in the Wadden Sea.     

Aerial and underwater carbon metabolism of a Zostera noltii seagrass bed in the Banc d’Arguin, Mauritania

Community respiration and primary production were measured in a dense intertidal Zostera noltii bed on the Banc d’Arguin, Mauritania (West Africa) under aerial and submerged conditions. Metabolism was studied in situ in dark and transparent benthic chambers. CO₂ fluxes in the air were measured over a series of short-term incubations (3 min) using an infrared gas analyzer. Dissolved inorganic carbon fluxes were calculated from concentration changes during one-hour underwater incubations. Air and underwater irradiance levels were measured every minute throughout the experiments. Carbon respiration was lower in the air (2.2 mmol m⁻² h⁻¹) than underwater (5.0 mmol m⁻² h⁻¹); similarly, a production-irradiance model fitted to the data indicated that gross maximal photosynthetic rate was markedly lower during emergence (6.0 mmol C m⁻² h⁻¹) than under water (42.7 mmol C m⁻² h⁻¹). The δ¹³C values observed in shoots indicated a decrease in atmospheric CO₂ contribution, compared to dissolved inorganic carbon, in Z. noltii metabolism along a depth gradient within a single location. As the seagrass bed remains under a thin layer of water at low tide at the studied site, the large difference in primary production can be mainly attributed to photosynthesis inhibition by high pH and oxygen concentration, as well as to the negative feedback of self-shading by seagrass leaves during emersion. The observed differences in respiration can be explained by the oxygen deficit at night during low tide near the sediment surface, a deficit that is consistent with the abundance of anoxia-tolerant species.     

Increase in seagrass distribution at Bourgneuf Bay (France) detected by spatial remote sensing

The changes in spatial distribution of intertidal Zostera noltii seagrass beds were studied with multispectral visible-infrared remote sensing in Bourgneuf Bay (France) over a 14-year period, between 1991 and 2005. Six SPOT satellite images acquired at low tide were calibrated using in situ spectroradiometric data and processed with the Normalized Difference Vegetation Index (NDVI). A steady and linear increase in meadow areas was observed between 1991 and 2005 with total surfaces colonized by Z. noltii increasing from 208 to 586 ha, respectively. A greater increase in the densest part of the meadow (NDVI > 0.4) was also observed: it represented only 15% of total meadow surfaces in 1991 vs. 35% in 2005. The seagrass expansion took place mainly towards the lower part of the intertidal zone, while in the upper intertidal zone the meadow appeared strictly limited by the +4 m (Lowest Astronomical Tide) bathymetric level. The influence of Z. noltii above-ground biomass variations on spectral reflectance was analyzed experimentally by spectrometry. Z. noltii displays a characteristic steep slope from 700 to 900 nm, increasing with increasing biomass. A quantitative relationship obtained experimentally between NDVI and the dry weight of leaves was used to produce a biomass distribution map. The distribution of Bourgneuf Bay intertidal seagrass beds is certainly constrained by the water turbidity and we suggest that tidal flat accretion could be a significant variable explaining the observed expansion downwards. With very limited spatial interactions, oyster aquaculture cannot be considered as a threat, while a recent increase in recreational hand fishing of Manila clams within the beds could become problematic.     

Food web analysis of an eelgrass (Zostera marina L.) meadow and neighbouring sites in Mitsukuchi Bay (Seto Inland Sea,Japan) using carbon and nitrogen stable isotope ratios

The contribution of benthic microalgal production has been compared both within and outside a coastal eelgrass (Zostera marina L.) meadow. Carbon and nitrogen stable isotope ratios of suspended particulate organic matter (POM), epiphytic and epilithic organic matter (EOM), leaves of Z. marina (inside the meadow only) and two secondary consumer species (small crustaceans and fish) were measured inside and outside a meadow in Mitsukuchi Bay, Northwest Seto Inland Sea, Japan. Inside the meadow, primary producers (epiphyton) and consumers showed higher δ¹³C signatures than outside. Primary and secondary consumers inside the meadow were mainly dependent on epiphyton on the leaves of Z. marina, while consumer species outside the meadow were basically dependent on epilithon.     

Differential anaerobic decomposition of seagrass (Zostera noltii) and macroalgal (Monostroma obscurum) biomass from Arcachon Bay (France)

Arcachon Bay is characterized by extensive meadows of the seagrass Zostera noltii. Moreover, as a consequence of eutrophication, massive proliferations of the macroalga (Monostroma obscurum) have occurred since the beginning of 1990s.This paper describes the anaerobic decomposition of biomass of both species under experimental conditions by two methods. Firstly, the dynamics of decomposition were studied in situ using litter bags. The remaining biomass and the elemental composition of the decomposing macrophytes were monitored. Secondly, degradation was studied in experimental containers under anoxic conditions in which the release of inorganic nutrients and the development of fermentative and sulfate-reducing bacterial populations were followed.The decomposition rate of total biomass was faster for macroalgae than for the vascular plants, thus corroborating previous observations. However, both in situ and laboratory experiments showed that the anaerobic decomposition of the seagrass Z. noltii resulted in rapid release of inorganic N and P, and increasing C/N and C/P ratios of the residual biomass. As a result, the recycling of inorganic nitrogen and phosphorus compounds was slightly more efficient for Z. noltii than for M. obscurum. Recycling of inorganic nutrients appears to be of a great importance to the whole ecosystem, because of the extensive spreading of Z. noltii in the bay.     

Evaluation of Zostera detritus as a potential new source of zosteric acid

Detritus of the seagrasses Zostera noltii and Z. marina collected on the beaches of Arcachon Lagoon (France) over a 3-year period was screened as a new source of zosteric acid (ZA). This natural sulphated phenolic acid is a high value-added product capable of preventing settlement of marine organisms and protecting crops from fungal diseases. The seasonal variation of the ZA content was quantified in methanolic and aqueous crude extracts using high-performance liquid chromatography. The concentration found ranged from 65 to 456 μg g⁻¹ dry wt for Z. noltii and 51–692 μg g⁻¹ dry wt for Z. marina, respectively. This is the first report of ZA in Zostera noltii. Detrital leaves of Zostera have never before been screened for their bioactive substances. These results show that this low cost, very abundant and renewable, but heretofore unused, marine resource has potential as a source of a rare and naturally occurring bioactive product.     

Temperature tolerance and survival of intertidal populations of the seagrass <Emphasis Type="Italic">Zostera noltii</Emphasis> (Hornemann) in Southern Europe (Ria Formosa,Portugal)

The dwarf seagrass Zostera noltii is an important primary producer in Atlantic coastal ecosystems from Mauritania to southern Norway and the Mediterranean Sea. Sessile intertidal organisms existing at the interface between marine and terrestrial environments may be particularly vulnerable to environmental change. In this study, we asked how near to thermal tolerance limits natural populations of Z. noltii are in the Ria Formosa coastal lagoon system in southern Portugal. We recorded the maximum temperatures in the Ria Formosa during the 2007 summer, and conducted experiments to determine the sub-lethal temperature of Z. noltii shoots sampled at two sites located at different tidal heights. Mortality rates and photosynthetic performance were recorded within a range of heat shock temperatures between 35 and 41°C. Survival was recorded ≤37°C, while higher temperatures led to a sudden drop in photosynthetic capacity followed by mortality (shoot loss) that occurred more rapidly with increasing temperatures. At 39°C and above, the rate of shoot mortality in both sites was close to 100%, occurring between 5 and 13 days after the heat shock. Survival was ca. 95 and 90% at 35 and 37°C, respectively. From these results for Z. noltii populations in the Ria Formosa we estimated sub-lethal temperature to be approximately 38°C for Z. noltii, close to the maximum of 36°C recorded in the summer 2007. Considering predicted trajectories in the coming decades, these results raise concern as to the future viability of intertidal Z. noltii populations near the southernmost edge of their distribution. Handling editor: S. M. Thomaz     

Circular pools in the seagrass beds of the Banc d’Arguin,Mauritania, and their possible origin

The tidal flats of the Banc d’Arguin, Mauritania, are covered by vast beds of Zostera noltii. At low tide these seagrass beds appear to be interspersed with partly vegetated, circular pools of 5–25 m diameter. Between February and May 2001 we described these pools and studied their possible origin. Several hypotheses regarding the origin have been developed. The first group of hypotheses assumes that the pools result from erosion activity. Since human disturbance of seagrass beds at the Banc d’Arguin is virtually non-existent, causes should be found in natural bed disturbances and/or tide or wave action. Therefore, small gaps, simulating holes dug by the crab Callinectes marginatus, were made to see if they would further erode by tidal currents or waves. The experiments showed no erosion. Neither we found support for other hypotheses assuming erosion to be the cause of circular pools. The alternative group of hypotheses stated that sedimentation on the flats would be responsible. We conclude that accretion of creek remnants is the most likely process behind the development of the pools; this conclusion is based on both mapping of the pattern of pools, the sediment profile in and around the pools and the distribution of seagrass biomass. Also the disturbance experiments showed bed accretion rather than bed erosion and support this hypothesis.     

Leaf dynamics and standing stocks of intertidal Zostera noltii Hornem. and Cymodocea nodosa (Ucria) Ascherson on the Banc d'Arguin (Mauritania)

Leaf dynamics and standing stocks of intertidal seagrasses were studied in the Baie d'Aouatif (Parc National du Banc d'Arguin, Mauritania) in April and September 1988. Standing stocks of Zostera noltii Hornem. suggest a unimodal seasonal curve similar to what is found for populations at higher latitudes. Also, leaf growth rates (0.03 cm² cm^–2 day^–1 on average) were similar to those found at higher latitudes in these months. Variation in leaf loss over tidal depth, time and different locations in the Baie d'Aouatif was larger and more often significant than variation in leaf growth. In general, Z. noltii beds in the Baie d'Aouatif had comparable leaf growth rates and standing stocks. In both months losses were almost always higher than or equal to growth.Variation in leaf loss over time was much higher in the plots that were situated high in the intertidal than in lower plots. This is explained by differences in susceptibility to sloughing, which is presumably higher in periods with low tide around noon for shallow depths.In an experiment using artificial shading nets, in situ leaf growth was affected negatively from 94% shading onwards. This shading was observed to reduce the light intensity reaching the seagrass bed to a level below the reported range of light compensation points for Z. noltii. Cymodocea nodosa (Ucria) Ascherson on average had higher leaf area and relative growth rates than Z. noltii and much lower loss rates, resulting in a positive net increase in September. Standing stocks were also higher than for Z. noltii. A mixed seagrass bed containing the above two species and Halodule wrightii Ascherson had the highest observed total biomass: 335 g m^–2 ash-free dry weight.     

Relative effects of nutrient enrichment and grazing on epiphyte-macrophyte (Zostera marina L.) dynamics

The independent and interactive effects of nutrient concentration and epiphyte grazers on epiphyte biomass and macrophyte growth and production were examined in Zostera marina L. (eelgrass) microcosms. Experiments were conducted during early summer, late summer, fall, and spring in a greenhouse on the York River estuary of Chesapeake Bay. Nutrient treatments consisted of ambient or enriched (3× ambient) concentrations of inorganic nitrogen (ammonium nitrate) and phosphate. Grazer treatments consisted of the presence or absence of field densities of isopods, amphipods, and gastropods. epiphyte biomass increased with both grazer removal and nutrient enrichment during summer and spring experiments. The effect of grazers was stronger than that of nutrients. There was little epiphyte response to treatment during the fall, a result possibly of high ambient nutrient concentrations and low grazing pressure. Under low grazer densities of early summer, macrophyte production (g m^–2 d^–1) was reduced by grazer removal and nutrient enrichment independently. Under high grazer densities of late summer, macrophyte production was reduced by enrichment only with grazers absent. During spring and fall there were no macrophyte responses to treatment. The relative influence of epiphytes on macrophyte production may have been related to seasonally changing water temperature and macrophyte requirements for light and inorganic carbon.     

Effects of Epiphytic Load on the Photosynthetic Performance of a Seagrass, <Emphasis Type="Italic">Zostera marina</Emphasis>, Monitored In Vivo by Chlorophyll Fluorescence Imaging

We investigated the effects of epiphytes on photosynthetic activity in a seagrass, Zostera marina. Parameters in our chlorophyll (Chl) fluorescence imaging technique, including Fo, Fm, and Fv/Fm, were monitored from leaf surfaces before and after those epiphytes were removed. Because of the uneven distribution of light intensities, Fm values at the margin of an image were underestimated while those in the central region were overestimated. Chl fluorescence emissions from all leaves except the youngest one were altered by the presence of epiphytes, which predominantly inhabited the surfaces of older leaves. Only a few were found lower on the plant where leaves were very close to each other. Regions where the epiphytes had been loosely bound before their gentle removal showed full restoration of photosynthetic performance to control levels afterward. However, only minor recovery of photosynthesis was found in areas that had been riddled with tightly bound epiphytes and were permanently damaged. In years 2002 and 2003, leaf productivity peaked in May and plummeted in November. More epiphytic diatoms were distributed when the seagrass biomass was larger, with pinnate diatoms dominating.     

Experimental analysis of the response and recovery of Zostera marina (L.) and Halodule wrightii (Ascher.) to repeated light-limitation stress

Seagrasses are considered important indicators of decline in water quality resulting in increased light attenuation that negatively influences their growth and survival. Chronic light-limitation interspersed with unpredictable acute attenuation events have had poorly understood effects on seagrass recovery dynamics. Zostera marina (eelgrass) and Halodule wrightii (shoalgrass) were subject to a matrix of light-deprivation events followed by recovery periods to mimic repeated acute shading events. Plant survival, morphology, biomass, chlorophyll content, and Fv/Fm were assessed over time to determine recovery. At the end of the experiment, all plants were harvested and species-specific treatment effects were determined. Significant differences due to treatments were noted in all parameters measured. In general, responses were similar for both life-stages and between species, suggesting similar physiological tolerance to repeated acute light-attenuation events. Only plants in treatments where light-deprivation was followed by a recovery interval of at least the same duration showed signs of long-term survival. Chlorophyll fluorescence (Fv/Fm) was an important metric for assessing recovery, but it failed to detect the onset of mortality in many plants. Other metrics of plant condition need to be assessed and coupled with chlorophyll fluorescence data to assess seagrass “health”. This is of particular importance in field studies, where the history of the plants is largely unknown.     

Seagrass complexity hierarchies: Influence on fish groups around the coast of Jersey (English Channel)

Recent research has identified a need for seagrass habitat management plans to be based on landscape-level approaches as they offer a more appropriate scale for large mobile fauna than smaller scales. Also, conservation decisions are more likely to be a choice between different seagrass beds rather than parts of individual beds. The present study examined the spatial utilisation of subtidal seagrass beds by fish around the coast of Jersey, English Channel (49°N 02°W) with the aim of identifying influential scales of complexity. A hierarchical-scale of landscape configuration and habitat characteristics was measured for eight seagrass beds using aerial photographic analysis (e.g. core area, contiguity and other landscape metrics), digital echo-sounder data (e.g. depth, canopy height) and diver surveys (e.g. epiphyte load). The contributions of these variables as predictors of functional fish groups were explored using multiple linear regression models. Results indicated that more fragmented seagrass beds supported lower numbers of fish species than more homogenous seagrass landscapes (squared semi-partial correlation coefficient, sr² = − 0.3). Densities of juveniles of larger fish species showed a negative relationship with increased fragmentation of the seagrass (sr² = − 0.34). At smaller scales of structural complexity the densities of cryptic fish were related positively to canopy height (sr² = 0.46). At night, fewer patterns could be explained by the independent variables in the model, which was attributed to the greater movement of fish between the seagrass and adjacent habitats to forage, and a breakdown in the association with seagrass habitat as a refuge from predation.     

Seasonal dynamics of the numbers of larvae of common fouling organisms in Balaklava Bay (Black Sea)

The seasonal dynamics of the numbers of larvae of common fouling organisms—the barnacle Balanus improvisus and the bivalves Mytilaster lineatus and Mytilus galloprovincialis in Balaklava Bay (Black Sea)—were investigated during 2000 and 2001 within the framework of an ecological research project. Under the conditions of an increased anthropogenic load, seasonal fluctuations of the numbers and the distribution of larvae depend on rhythms of the breeding cycles of fouling invertebrates and on the hydrodynamic features of the region (water setup). The differences in the optimum temperatures, hatching intensity, and time of occurrence of larvae in the plankton, as well as the irregular distribution of larvae, allow the three major fouling organisms to reduce interspecific competition for food and the substrate.Original Russian Text Copyright © 2004 by Biologiya Morya, Shalaeva, Lisitskaya.     

Spectral response of the seagrass Zostera noltii with different sediment backgrounds

The efficiency of vegetation indices (VIs) to estimate the above-ground biomass of the seagrass species Zostera noltii Hornem. from remote sensing was tested experimentally on different substrata, since terrestrial vegetation studies have shown that VIs can be adversely influenced by the spectral properties of soils and background surfaces. Leaves placed on medium sand, fine sand and autoclaved fine sand were incrementally removed, and the spectral reflectance was measured in the 400–900 nm wavelength range. Several VIs were evaluated: ratios using visible and near infrared wavelengths, narrow-band indices, indices based on derivative analysis and continuum removal. Background spectral reflectance was clearly visible in the leaf reflectance spectra, showing marked brightness and spectral contrast variations for the same amount of vegetation. Paradoxically, indices used to minimize soil effects, such as the Soil-Adjusted Vegetation Index (SAVI) and the Modified second Soil-Adjusted Vegetation Index (MSAVI₂) showed a high sensitivity to background effects. Similar results were found for the widely used Normalized Difference Vegetation Index (NDVI) and for Pigment Specific Simple Ratios (PSSRs). In fact, background effects were most reduced for VIs integrating a blue band correction, namely the modified specific ratio (mSR₍₇₀₅₎), the modified Normalized Difference (mND₍₇₀₅₎), and two modified NDVIs proposed in this study. However, these indices showed a faster saturation for high seagrass biomass. The background effects were also substantially reduced using Modified Gaussian Model indices at 620 and 675 nm. The blue band corrected VIs should now be tested for air-borne or satellite remote sensing applications, but some require sensors with a hyperspectral resolution. Nevertheless, this type of index can be applied to analyse broad band multispectral satellite images with a blue band.     

Evaluation of a mechanical seed planter for transplanting Zostera marina (eelgrass) seeds

Few seagrass transplant projects worldwide have relied on seeds, and those projects using Zostera marina (eelgrass) seeds have generally found low rates of seedling establishment (<10%). We compared seedling establishment achieved by a mechanical seed planter with seeds broadcast on the sediment surface by hand. The planter injected seeds into the sediment by pumping the seeds, suspended in a gelatin-based matrix, to a benthic sled with eight planting nozzles. As a control for the gel, seeds were also injected into the sediment without gel using a hand-held pipette. Seeds were planted at a density of 300 m⁻² into six replicate plots at each of three sites in the Chesapeake Bay region in September 2005, with seedling establishment measured in April 2006. Burying seeds, either with or without gel, had an overall positive effect on seedling establishment, but the effectiveness and the best method varied among sites. Mean seedling establishment for machine-planted seeds was significantly greater than for broadcast seeds at the Piankatank River site (4% vs. 1%), but not at the York (1.2% vs. 1.4%) or Spider Crab Bay (10.1% vs. 7.4%) sites. The effect of the gel was inconsistent among sites, with the highest seedling establishment (18.8%), resulting from seeds injected by pipette without gel at the Spider Crab site. Seed burial shows promise for increasing seedling establishment relative to seed broadcasting in the Chesapeake region, but further investigation of seed–sediment interactions at specific restoration sites is necessary. Low seedling establishment rates remain a bottleneck for seed-based eelgrass restoration.     

Effect of shading of Zostera marina (eelgrass) on sulfur cycling in sediments with contrasting organic matter and sulfide pools

Eelgrass Zostera marina was collected in spring and autumn from a light-saturated environment with low-organic sediments and a light-limited environment with organic-rich sediments in Denmark. The eelgrass and sediment responses to reduced light conditions were studied in 2-week shading experiments. Z. marina responded to reduced light conditions by decreasing growth rates and a loss of above-ground biomass. The spring plants were most sensitive to light reductions and the relative leaf elongation rates were reduced with up to 58% and the shoot densities with 33-36%. There was no difference in light response in relation to sediment organic matter contents. The sulfate reduction rates were reduced in the shaded low-organic sediments with up to 67%, whereas there was no effect of shading on rates in the organic-rich sediments. The lack of effect of shading in the organic-rich sediments was attributed to a limited coupling between Z. marina production and sediment bacterial carbon cycling. In contrast to the sulfate reduction rates, the pools of reduced sulfur were increased with up to 89% in the shaded, low-organic sediments, suggesting that the reoxidation of sulfides was reduced. Shading had no effect on the pools of sulfides in the organic-rich sediments due to much larger pools of sulfides. The enhanced sensitivity of spring plants to shading was probably due to a low above- to below-ground ratio compared to the autumn plants, which limited the plant-mediated oxidation of the sediments and thus the reoxidation of sulfides. The shaded plants were possibly more exposed to anoxic and sulfidic conditions affecting their growth and survival.     

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.     

Ammonium uptake kinetics in root and leaf cells of Zostera marina L.

Ammonium uptake rates and the mechanism for ammonium transport into the cells have been analysed in Zostera marina L. In the cells of this species, a proton pump is present in the plasmalemma, which maintains the membrane potential. However, this seagrass shows a high-affinity transport mechanism both for nitrate and phosphate which is dependent on sodium and is unique among angiosperms. We have then analysed if the transport of another N form, ammonium, is also dependent of sodium. First, we have studied ammonium transport at the cellular level by measurements of membrane potentials, both in epidermal root cells and mesophyll cells. And second, we have monitored uptake rates in whole leaves and roots by depletion experiments. The results showed that ammonium is taken up by a high-affinity transport system both in root and leaf cells, although two different of kinetics could be discerned in mesophyll cells (with affinity constants of 2.2 ± 1.1 μM NH₄⁺, in the range 0.01-10 μM NH₄⁺, and 23.2 ± 7.1 μM NH₄⁺, at concentrations between 10 and 500 μM NH₄⁺). However, only one kinetic could be observed in epidermal root cells, which showed a K_m = 11.2 ± 1.0 μM NH₄⁺, considering the whole ammonium concentration range assayed (0.01-500 μM NH₄⁺). The higher affinity of leaf cells for ammonium was consistent with the higher uptake rates observed in leaves, with respect to roots, in depletion experiments at 10 μM NH₄⁺ initial concentration. However, when an initial concentration of 100 μM was assayed, the difference between uptake rates was reduced, but still being higher in leaves. Variations in proton or sodium-electrochemical gradient did not affect ammonium uptake, suggesting that the transport of this nutrient is not driven by these ions and that the ammonium transport mechanism could be different to the transport of nitrate and phosphate in this species.