Jens Borum

Interactions among phytoplankton, periphyton, and macrophytes in temperate freshwaters and estuaries

Abstract The physico-chemical environment and the resource needs of phytoplankton, periphyton and macrophytes are markedly different. In this paper we compare the characteristics of the different phototrophs with respect to water movements and diffusive boundary layers, nutrient demands, carbon and oxygen dynamics, and light climate and light requirements. We discuss how these characteristics affect growth dynamics, biomass limitation and biotic interactions of phototrophs in natural habitats, and, finally, we discuss how plant community dominance can be predicted from ecosystem size, depth and nutrient loading. Phytoplankters live in a stirred environment with thin diffusive boundary layers, low nutrient availability and a highly variable light climate. They grow fast and have high nutrient requirements but their biomass is often nutrient limited. Diffusive boundary layers of benthic microalgae and rooted macrophytes are thicker and reduce the exchange of gases and nutrients. Sessile organisms live in a more predictable light climate but may experience severe self-shading and generally grow more slowly than phytoplankters. The nutrient requirements of rooted macrophytes are lower than those of microalgae because of low growth rates, high internal C:N:P ratios and the existence of nutrient conserving mechanisms, and nutrient limitation is less important because the plants exploit the rich nutrient pools of the sediment. The phototrophs compete for light, nutrients and inorganic carbon, and the balance among phototrophs changes with size, depth and nutrient richness of the ecosystem. Phytoplankters dominate in deep lakes and oceanic waters and may also, together with periphyton, dominate in nutrient-rich shallow waters because of shading effects on macrophytes and benthic microalgae. However, shallow lakes and estuaries with low nutrient availability in the water column are dominated by benthic phototrophs because of their lower nutrient requirements and contact to sediment nutrient pools.

Are seagrass growth and survival constrained by the reducing conditions of the sediment

A literature review of the effects of the reducing conditions of the sediment on seagrass metabolism, growth and survival, and of the morphological and physiological adaptations that seagrasses show to cope with sediment anoxia is presented and major gaps in knowledge are identified. The hypothesis that sediment anoxia controls the survival of seagrasses was tested experimentally by increasing the oxygen demand of the sediment with the addition of sucrose. Experiments were performed in a tropical (Southeast Asia) multispecific seagrass meadow, a Mediterranean Cymodocea nodosa meadow, and a temperate Zostera marina meadow. Sulfide levels in pore water and vertical redox profiles were used to characterise the effects of the sucrose additions on the sediment, while plant responses were quantified through the changes in shoot density and leaf growth. Sulfide levels in pore water increased and sediment redox potential decreased after the addition of sucrose to the sediment of different seagrass meadows. The effect of the addition of sucrose to the sediment of seagrasses was species-specific. Leaf growth was reduced and shoot mortality increased in some of the tropical species (e.g., Thalassia hemprichii), but not in others. Neither mortality nor leaf growth of the Mediterranean species C. nodosa was affected by sucrose additions, and only leaf growth was reduced two months after the addition of sucrose in Z. marina. Our results suggest that increased sediment anoxia might be a factor promoting growth inhibition and mortality in seagrasses, although strong differences have been found among different species and environments.

Development of epiphytic communities on eelgrass (Zostera marina) along a nutrient gradient in a Danish estuary

The effect of nutrient enrichment on epiphyte development was examined by following the seasonal development of epiphyte biomass on eelgrass (Zostera marina L.) at four localities along a nutrient gradient in Roskilde Fjord, Denmark between March and December 1982. In the most nutrient-poor area, epiphyte biomass followed a distinct bimodal seasonal pattern with maxima in spring and early fall. Low nutrient availability and a high rate of eelgrass leaf renewal kept epiphyte biomass at a low level throughout the summer period. Unlike phytoplankton, the epiphytic community was not stimulated by nutrient enrichment during spring, however, from May through August, the biomass of both components increased exponentially with increasing concentrations of total N in the water. Along the nutrient gradient, phytoplankton biomass increased 5- to 10-fold, while epiphyte biomass increased 50- to 100-fold. Thus differences in nutrient conditions among study sites were more clearly reflected by epiphytes than phytoplankton.

Is total primary production in shallow coastal marine waters stimulated by nitrogen loading

The global nitrogen cycle has been extensively modified by human activity to the extent that more N is fixed annually by human-driven than by natural processes (Vitousek 1994). This alteration influences production and species composition of terrestrial ecosystems (Tilman 1987) and contributes to acidification and forest dieback (Schulze 1989). The influence of nitrogen on eutrophication of coastal marine ecosystems is even stronger with profound effects on plant communities and food webs (Nixon et al. 1986). The total primary production of marine plants in coastal areas (as organic carbon or dry matter produced annually per unit of surface area within the ecosystem) is generally assumed to increase with increasing loading of nutrients from land (e.g. Boynton et al. 1982, Nixon et al. 1986, Paerl 1993). The effects of widespread eutrophication, such as oxygen deficiency and mass mortality of benthic invertebrates and fish, have alarmed the public and are considered to emerge from the enhanced oxygen consumption required to mineralize the increasing amounts of organic matter produced within the ecosystem. Much of our current analysis and understanding of energy flow and carbon and oxygen dynamics in the coastal marine environment presuppose that anthropogenic loading and total primary production are directly positively related. In the following we will argue, however, that the total primary production of shallow coastal areas, i.e. the combined production of microand macroscopic plants living in the water and at the bottom, does not change systematically by nutrient enrichment. Our analysis is based on a comparison of published rates of total primary production and nitrogen loading from land using the same approach as Boynton et al. (1982) and Nixon et al. (1986) to analyse the dependence of phytoplankton production on nitrogen loading. The data originate from different temperate coastal ecosystems with very different morphometry and hydraulics. The quality of the data (in terms of suitability of methods and number of measurements) also varies considerably among the systems but does not systematically influence the patterns reported. We have tried to ensure a fair representation of systems which are most likely to respond to enhanced nitrogen loading by including relatively deep (mean depth down to 40 m) and clearly phytoplankton dominated ecosystems and by omitting data we suspect overestimate benthic primary production. Thereby, we obtain a balanced analysis of our hypothesis.

Depth Colonization of Eelgrass (Zostera marina) and Macroalgae as Determined by Water Transparency in Danish Coastal Waters

We present a comparative analysis of lower depth limits for growth of eelgrass, large brown algae and other macroalgae measured by SCUBA-diving along 162 transects in 27 Danish fjords and coastal waters, coupled to 1,400 data series of water chemistry (especially nitrogen) and Secchi depth transparency collected between March and October. Danish coastal waters are heavily eutrophied and characterized by high particle concentrations, turbid water and lack of macrophyte growth in deep water. Median values are 3.6 m for Secchi depth and median lower-depth limits are 4.0 m for eelgrass, 5.3 m for brown algae and 5.0 m for other macroalgae. Depth limits for growth of eelgrass and macroalgae increase linearly with transparency in the coastal waters. The relationships are highly significant (p<10−6) and transparency accounts for about 60% of the variability of depth limits. Eelgrass extends approximately to half the maximum depth of macroalgae, presumably because of greater respiratory costs to maintain the below-ground rhizomes and roots of eelgrass, which often constitutes half the plant weight. As a reflection of the importance of total nitrogen (TN) in controlling phytoplankton biomass and thus Secchi depth in coastal marine waters, we found that TN could explain 48–73% of the variation in depth limits of eelgrass and macroalgae, according to a multiplicative model (Y=aXb). As with Secchi depth, the relationship to eelgrass showed a lower slope, reflecting the higher respiratory costs of eelgrass. The models show great sensitivity and a profound quantitative response with proportional effects on Secchi depth and depth limits when total-N concentrations are reduced.

CHANGES IN INTRACELLULAR NITROGEN POOLS AND FEEDBACK CONTROLS ON NITROGEN UPTAKE IN CHAETOMORPHA LINUM (CHLOROPHYTA)1

Changes in the size of intracellular nitrogen pools and the potential feedback by these pools on maximum N uptake (NH4+ and NO3−) rates were determined for Chaetomorpha linum (Müller) Kützing grown sequentially under nutrient‐saturating and nutrient‐limiting conditions. The size of individual pools in N‐sufficient algae could be ranked as residual organic N (RON) comprised mainly of amino acids and amino compounds > protein N > NO3− > NH4+ > chlorophyll N. When the external N supply was removed, growth rates remained high and individual N pools were depleted at exponential rates that reflected both dilution of existing pools by the addition of new biomass from growth and movement between the pools. Calculated fluxes between the tissue N pools showed that the protein pool increased throughout the N depletion period and thus did not serve a storage function. RON was the largest storage reserve; nitrate was the second largest, but more temporary, storage pool that was depleted within 10 days. Upon N resupply, the RON pool increased 3 × faster than either the inorganic or protein pools, suggesting that protein synthesis was the rate‐limiting step in N assimilation and caused a buildup of intermediate storage compounds. Maximum uptake rates for both NH4+ and NO3− varied inversely with macroalgal N status and appeared to be controlled by changes in small intracellular N pools. Uptake of NO3− showed an initial lag phase, but the initial uptake of NH4+ was enhanced and was present only when the intracellular NH4+ pool was depleted in the absence of an external N supply. A strong negative correlation between the RON pool size and maximum assimilation uptake rates for both NH4+ and NO3− suggested a feedback control on assimilation uptake by the buildup and depletion of organic compounds. Enhanced uptake and the accumulation of N as simple organic compounds or nitrate both provide a temporary mechanism to buffer against the asynchrony of N supply and demand in C. linum.

Phytoplankton, nutrients, and transparency in Danish coastal waters

We present a comparative analysis of 1400 data series of water chemistry (particularly nitrogen and phosphorus concentrations), phytoplankton biomass as chlorophylla (chla) concentrations, concentrations of suspended matter and Secchi depth transparency collected from the mid-1980s to the mid-1990s from 162 stations in 27 Danish fjords and coastal waters. The results demonstrate that Danish coastal waters were heavily eutrophied and had high particle concentrations and turbid waters. Median values were 5.1 μg chla 1−1, 10.0 mg DW 1−1 of suspended particles, and Secchi depth of 3.6 m. Chlorophyll concentration was strongly linked to the total-nitrogen concentration. The strength of this relationship increased from spring to summer as the concentration of total nitrogen declined. During summer, total nitrogen concentrations accounted for about 60% of the variability in chlorophyll concentrations among the different coastal systems. The relationship between chlorophyll and total phosphorus was more consistant over the year and correlations were much weaker than encountered for total nitrogen. Secchi depth could be predicted with good precision from measurements of chlorophyll and suspended matter. In a multiple stepwise regression model with In-transformed values the two variables accounted for most of the variability in water transparency for the different seasons and the period March–October as a whole (c. 80%). We were able to demonstrate a significant relationship between total nitrogen and Secchi depth, with important implications for management purposes.

Epiphyte shading and its effect on photosynthesis and diel metabolism of Lobelia dortmanna L. during the spring bloom in a danish lake

Abstract A dense epiphyte community develops on Lobelia dortmanna L. during spring in the mesotrophic waters of Lake Almind, Denmark. This community has attenuated the incident light at 0.5 m depth by 67.4–81.7% within two years. The attenuation is spectrally selective, the proportion of red light transmitted increasing with epiphyte density. Epiphyte attenuation reduces the photosynthesis of Lobelia by increasing the light-compensation point and the saturation light intensity at the surface. These effects are predictable from epiphyte attenuations measured in suspensions scraped from the leaves of Lobelia and on the basis of photosynthesis—light relationships. Epiphyte attenuation and reduction of Lobelia photosynthesis are proportional in low light intensities (i.e., low surface light and/or high epiphyte attenuation) and independent in saturation light. The estimated light-compensation point for diel metabolism of Lobelia during spring was 3.33–3.66 E m−2 day−1 at 0.5 m depth, close to the natural level in the lake. This suggests that Lobelia grows only slowly during spring and resumes growth subsequently during summer and autumn, when epiphyte density decreases due to N and P limitation. The depth limit of Lobelia was found to be 1.0 m. Without epiphyte attenuation, the daily light-compensation point during spring would occur at 3.5 m. This supports the view that epiphyte attenuation may be important as concerns the seasonal growth and depth penetration of host macrophytes.

Oxygen Movement in Seagrasses

Seagrasses are, like all vascular plants, obligate aerobes, which require a continuous supply of oxygen to sustain aerobic metabolism of both aboveand below-ground tissues. Compared to their leaves, seagrass roots and rhizomesmay experience oxygen deprivation for shorter periods, but these below-ground tissues exhibit physiological adaptations which allow them to rely temporarily on anaerobic fermentative metabolism (Pregnall et al., 1984; Smith et al., 1988). Aerobic respiration is energetically about 10 times more efficient than fermentative processes, which tend to accumulate ethanol, acetate, and other potentially toxic metabolites representing a threat to tissue survival (Smith et al., 1988; Crawford and Braendle, 1996). The meristematic tissues, located in the transitionbetweenwater columnand sediment, are especially vulnerable to low oxygen supply and exposure to anaerobic metabolites due to their high metabolic activity and the continuous oxygen supply required for mitotic growth. In addition to the importance of oxygen inside seagrass tissues, maintenance of oxic conditions around roots may provide efficient protection against invasion of reduced toxic compounds and metal ions from the surrounding sediment (Armstrong et al., 1992; Crawford and Braendle, 1996; see also Marba et al., Chapter 6). Accordingly, there are several benefits to plant performance in maintaining a rich oxygen supply to all tissues including roots and rhizomes.

The Response of Experimental Rocky Shore Communities to Nutrient Additions

The aim of this study was to determine whether the experimental nutrient enrichment of littoral rocky shore communities would be followed by a predicted accumulation of fast-growing opportunistic algae and a subsequent loss of perennial benthic vegetation. Inorganic nitrogen (N) and potassium (P) was added to eight concrete mesocosms inhabited by established littoral communities dominated by fucoids. The response to nutrient enrichment was followed for almost 2 1/2 years. Fast-growing opportunistic algae (periphyton and ephemeral green algae) grew significantly faster in response to nutrient enrichment, but the growth of red filamentous algae and large perennial brown algae was unaffected. However, these changes were not followed by comparable changes in the biomass and composition of the macroalgae. The biomass of opportunistic algae was stimulated only marginally by the nutrient enrichment, and perennial brown algae (fucoids) remained dominant in the mesocosm regardless of nutrient treatment level. Established rocky shore communities thus seem able to resist the effects of heavy nutrient loading. We found that the combined effects of the heavy competition for space and light imposed by canopy-forming algae, preferential grazing on opportunistic algae by herbivores, and physical disturbance, succeeded by a marked export of detached opportunistic algae, prevented the fast-growing algae from becoming dominant. However, recruitment studies showed that the opportunistic algae would become dominant when free space was available under conditions of high nutrient loading and low grazing pressure. These results show that established communities of perennial algae and associated fauna in rocky shore environments can prevent or delay the accumulation of bloom-forming opportunistic algae and that the replacement of long-lived macroalgae by opportunistic species at high nutrient loading may be a slow process. Nutrient enrichment may not, in itself, be enough to stimulate structural changes in rocky shore communities.