The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level

Trait-based approaches to community structure are increasingly used in terrestrial ecology. We show that such an approach, augmented by a mechanistic analysis of trade-offs among functional traits, can be successfully used to explain community composition of marine phytoplankton along environmental gradients. Our analysis of literature on major functional traits in phytoplankton, such as parameters of nutrient-dependent growth and uptake, reveals physiological trade-offs in species abilities to acquire and utilize resources. These trade-offs, arising from fundamental relations such as cellular scaling laws and enzyme kinetics, define contrasting ecological strategies of nutrient acquisition. Major groups of marine eukaryotic phytoplankton have adopted distinct strategies with associated traits. These diverse strategies of nutrient utilization can explain the distribution patterns of major functional groups and size classes along nutrient availability gradients.     

Molecular mechanism of glucose-6-phosphate utilization in the dinoflagellate Karenia mikimotoi

Phosphorus (P) is an essential nutrient for marine phytoplankton as for other living organisms, and the preferred form, dissolved inorganic phosphate (DIP), is often quickly depleted in the sunlit layer of the ocean. Phytoplankton have developed mechanisms to utilize organic forms of P (DOP). Hydrolysis of DOP to release DIP by alkaline phosphatase is believed to be the most common mechanism of DOP utilization. Little effort has been made, however, to understand other potential molecular mechanisms of utilizing different types of DOP. This study investigated the bioavailability of glucose-6-phosphate (G6P) and its underlying molecular mechanism in the dinoflagellate Karenia mikimotoi. Suppression Subtraction Hybridization (SSH) was used to identify genes up- and down-regulated during G6P utilization compared to DIP condition. The results showed that G6P supported the growth and yield of K. mikimotoi as efficiently as DIP. Neither DIP release nor AP activity was detected in the cultures grown in G6P medium, however, suggesting direct uptake of G6P. SSH analysis and RT-qPCR results showed evidence of metabolic modifications, particularly that mitochondrial ATP synthase f1 gamma subunit and thioredoxin reductase were up-regulated while diphosphatase and pyrophosphatase were down-regulated in the G6P cultures. All the results indicate that K. mikimotoi has developed a mechanism other than alkaline phosphatase to utilize G6P.     

Nutrient limitation of phytoplankton and periphyton growth in upland lakes

SUMMARY 1. Thirty small upland lakes in Cumbria, Wales, Scotland and Northern Ireland were visited three times between April and August 2000. On each occasion water chemistry was measured and phytoplankton bioassays were performed in the laboratory to assess growth‐rate and yield limitation by phosphorus and nitrogen. In addition, yield limitation of periphyton growth was investigated twice, in situ, using nutrient‐diffusing substrata. 2. Over the whole season the percentage frequency of P, N and co‐limitation was 24, 13 and 63%, respectively, for phytoplankton rate limitation and 20, 22 and 58%, respectively, for phytoplankton yield limitation. 3. A clear response of periphyton yield to nutrient additions was found in 75% of all cases and of these, co‐limitation was most common (54%). Average percentage frequency for P and N limitation was 26 and 20%, respectively. 4. Phytoplankton and periphyton showed seasonal changes in nutrient limitation within sites. In particular, co‐limitation became progressively more common as the season progressed. 5. The response of phytoplankton growth rate to ammonium and nitrate addition was identical, but ammonium was a slightly better source of nitrogen than nitrate for phytoplankton yield on 7% and for periphyton yield on 10% of the occasions. However, the magnitude of the effect was small. 6. The concentration of dissolved inorganic nitrogen (DIN) and the molar ratio of DIN to total dissolved phosphorus (TDP), appeared to be the main environmental factors controlling the extent of nitrogen or phosphorus limitation at a given site. Nitrogen limitation was more likely than phosphorus limitation where the DIN was <6.5 mmol m^?3 and the ratio of DIN : TDP was <53. Co‐limitation was the most likely outcome at a DIN concentration <13 mmol m^?3 and at a DIN : TDP molar ratio <250. Above these values phosphorus limitation was most likely. 7. The relatively high frequency of nitrogen limitation and co‐limitation at higher N : P ratios than previously reported, may result from the inability of nitrogen‐fixing cyanobacteria to thrive in these upland lakes where pH and the concentration of phosphorus tended to be low and where flushing rates tended to be high.     

Mixotrophy of a photosynthetic flagellate viewed from an optimal foraging perspective

Mixotrophy, a combination of phototrophic and phagotrophic nutrition, has been found in several classes of phytoplankton (Booras et al. 1988, Jones 2000) and appears to be a successful evolutionary strategy. Heterotrophic nutrition of phytoplankton has been suggested to be an important source of mineral nutrients (Nygaard and Tobiesen 1993). Potentially limiting mineral nutrients, particularly phosphorus (P), are often several orders of magnitude more concentrated in the biomass of food organisms of mixotrophs (e.g. in bacteria) than in the dissolved phase (Vadstein 2000). We used radioactive tracer experiments to show that the simultaneous uptake of P from dissolved inorganic and particular P sources by the marine phytoflagellate Chrysochromulina polylepis followed basic predictions of optimal foraging theory (Stephens and Krebs 1986). Chrysochromulina takes up its P rather unselectively from both bacterial P and dissolved P sources at low dissolved P concentrations, while it becomes more selective at higher dissolved inorganic P (DIP) concentrations. The onset of mixotrophic processes was dependent on DIP concentrations. These findings support the view of mixotrophy as a strategy of nutrient uptake in nutrient poor (oligotrophic) pelagic environments (Nygaard and Tobiesen 1993) and show that ideas of optimal foraging can be applied to unicellular organisms.     

Nutrient limitation of phytoplankton production in Alaskan Arctic foothill lakes

We used 54 enrichment bioassays to assess nutrient limitation (N, P) of ¹⁴C uptake by natural phytoplankton assemblages in 39 lakes and ponds in the Arctic Foothills region of Alaska. Our purpose was to categorize phytoplankton nutrient status in this under-represented region of North America and to improve our ability to predict the response of primary production to anticipated anthropogenically mediated increases in nutrient loading. Experiments were performed across several watersheds and included assays on terminal lakes and lakes occupying various positions in chains (lakes in series within a watershed and connected by streams). In total, 89% (48 of 54) of the bioassays showed significant stimulation of ¹⁴C primary production by some form of nutrient addition relative to unamended controls. A significant response was observed following enrichment with N and P, N alone and P alone in 83, 35 and 22% of the bioassays, respectively. In experiments where N and P proved stimulatory, the influence of N alone was significantly greater than the influence of P alone. Overall, the data point to a greater importance for N than P in regulating phytoplankton production in this region. The degree of response to N and P enrichment declined as the summer progressed and showed no relationship to irradiance or water temperature, suggesting secondary limitation by some micronutrient such as iron as the summer advanced. Phytoplankton nutrient status was often consistent across lakes within a watershed, suggesting that watershed characteristics influence nutrient availability. Lakes in this region will clearly show increased phytoplankton production in response to anthropogenic activities and anticipated changes in climate that will increase nutrient loading.     

Background nutrient concentration determines phytoplankton bloom response to marine heatwaves

Ocean temperature extreme events such as marine heatwaves are expected to intensify in coming decades due to anthropogenic global warming. Reported ecological and economic impacts of marine heatwaves include coral bleaching, local extinction of mangrove and kelp forests and elevated mortalities of invertebrates, fishes, seabirds and marine mammals. In contrast, little is known about the impacts of marine heatwaves on microbes that regulate biogeochemical processes in the ocean. Here we analyse the daily output of a near‐global ocean physical–biogeochemical model simulation to characterize the impacts of marine heatwaves on phytoplankton blooms in 23 tropical and temperate oceanographic regions from 1992 to 2014. The results reveal regionally coherent anomalies of shallower surface mixing layers and lower surface nitrate concentrations during marine heatwaves. These anomalies exert counteracting effects on phytoplankton growth through light and nutrient limitation. Consequently, the responses of phytoplankton blooms are mixed, but can be related to the background nutrient conditions of the study regions. The blooms are weaker during marine heatwaves in nutrient‐poor waters, whereas in nutrient‐rich waters, the heatwave blooms are stronger. The corresponding analyses of sea‐surface temperature, chlorophyll a and nitrate based on satellite observations and in situ climatology support this relationship between phytoplankton bloom anomalies and background nitrate concentration. Given that nutrient‐poor waters are projected to expand globally in the 21st century, this study suggests increased occurrence of weaker blooms during marine heatwaves in coming decades, with implications for higher trophic levels and biogeochemical cycling of key elements.     

A comparison of phosphorus immobilization in sediments of freshwater and coastal marine systems

The extent to which sediments of aquatic systems immobilize or release phosphorus can affect dramatically the P content of overlying waters. Data from 48 different aquatic systems suggests that there may be a major difference between fresh- and salt-water systems in this immobilization. Under oxic conditions (water overlying sediments had dissolved oxygen > 0.5 mg/L) P is strongly immobilized in sediments of most fresh-water systems. In sediments of most salt-water systems P is released from sediments and behaves, essentially, as a conservative tracer of benthic decomposition. This difference in P cycling is large enough to have an influence on the often cited difference in phytoplankton nutrient limitation between fresh- and salt-water systems.     

The role of dissolved organic matter bioavailability in promoting phytoplankton blooms in Florida Bay

The clear, shallow, oligotrophic waters of Florida Bay are characterized by low phytoplankton biomass, yet periodic cyanobacteria and diatom blooms do occur. We hypothesized that allochthonous dissolved organic matter (DOM) was providing a subsidy to the system in the form of bound nutrients. Water from four bay sites was incubated under natural light and dark conditions with enrichments of either DOM ( > 1 kD, 2×DOM) or inorganic nutrients (N+P). Samples were analyzed for bacterial numbers, bacterial production, phytoplankton biomass, phytoplankton community structure, and production, nutrients, and alkaline phosphatase (AP) activity. The influence of 2×DOM enrichment on phytoplankton biomass developed slowly during the incubations and was relatively small compared to nutrient additions. Inorganic nutrient additions resulted in an ephemeral bloom characterized initially as cyanobacterial and brown algae but which changed to dinoflagellate and/or brown algae by day six. The DIN:TP ratio decreased 10-fold in the N+P treatments as the system progressed towards N limitation. This ratio did not change significantly for 2×DOM treatments. In addition, these experiments indicated that both autotrophic and heterotrophic microbial populations in Florida Bay may fluctuate in their limitation by organic and inorganic nutrient availability. Both N+P and 2×DOM enrichments revealed significant and positive response in bioavailability of dissolved organic carbon (BDOC). Potential BDOC ranged from 1.1 to 35.5%, with the most labile forms occurring in Whipray Basin. BDOC at all sites was stimulated by the 2×DOM addition. Except for Duck Key, BDOC at all sites was also stimulated by the addition of N+P. BDOC was lower in the dry season than in the wet season (5.56% vs. 16.86%). This may be explained by the distinct chemical characteristics of the DOM produced at different times of year. Thus, both the heterotrophic and autotrophic microbial communities in Florida Bay are modulated by bioavailability of DOM. This has ramifications for the fate of DOM from the Everglades inputs, implicating DOM bioavailability as a contributing factor in regulating the onset, persistence, and composition of phytoplankton blooms.     

Uptake and transport of phosphorus by Agrostis capillaris seedlings from rapidly hydrolysed organic sources extracted from32 P-labelled bacterial cultures

Cultures of the soil bacterium Serratia liquifaciens grimesii were grown with³² P labelled phosphate, to produce a uniformly³² P labelled source of microbial P. Extracts of the bacteria were prepared by sonication, dialysis and filtration to provide a clear sterile solution which was characterised in terms of dissolved organic and condensed P (DOP and DCP) and molecular weight range. The extract was used as a source of P to Agrostis capillaris L. seedlings in nutrient solution from which orthophosphate was omitted. In a time course experiment, root surface phosphatase activity increased as soon as extract was added to the root medium, DOP was rapidly hydrolysed and orthophosphate concentration increased rapidly. These processes were complete within about 8 h, after which phosphatase activity fell to its original level, and the plants absorbed molybdate reactive P from the nutrient solution so that it reached its original concentration over 48 h. DCP concentrations did not change significantly throughout the experiment. This work clearly demonstrated that DOP but not DCP, as a component of a bacterial extract produced by a relatively straightforward method, was quickly hydrolysed and the P made available for plant uptake.     

Nutrient and iron limitation to <Emphasis Type="Italic">Ulva</Emphasis> blooms in a eutrophic coastal lagoon (Sacca di Goro,Italy)

Growth patterns and bloom formation of the green seaweed Ulva rigida were analysed in the eutrophic Sacca di Goro lagoon (Po River Delta, Italy). Variations of standing biomasses and elemental composition of Ulva were analysed through an annual cycle with respect to nitrogen, phosphorus and iron. Growth rates, nutrient and iron uptake and nitrate storage by macroalgal thalli were also assessed with field experiments during the formation of a spring bloom. The control of Ulva growth and the bloom formation depended on multiple factors, especially on nitrogen availability and iron deficiency. In the nitrate rich waters of the Sacca di Goro lagoon, nitrate accumulation in Ulva thalli was inversely related with Fe uptake, indicating an influence of Fe limitation on N acquisition. Since length and magnitude of nitrate luxury uptake are inversely related to the size of the intracellular nitrate pools, in nitrate rich waters the fast growing Ulva may face risk of N-limitation not only when exposed to low N concentrations or at high biomass levels, but also when exposed to pulsed dissolved nitrate concentrations at low iron availability. The potential Fe limitation could be affected by processes controlled by geochemical reactions and by macroalgal growth and decomposition. Both Fe oxidation during the active macroalgal growth and the formation of insoluble FeS and FeS₂ during bloom collapse can result in a drastic decrease of soluble iron. Thus, a potential limitation of Fe to macroalgae can occur, determining positive feedbacks and potentially controlling the extent of bloom development and persistence.     

Nutrient addition effects on chlorophyll a,phytoplankton biomass,and heterocyte formation in Lake Erie’s central basin during 2014–2017: Insights into diazotrophic blooms in high nitrogen water

1. Phosphorus (P) usually is the primary limiting nutrient of phytoplankton biomass, but attention towards nitrogen (N) and trace nutrients, such as iron (Fe), has surfaced. Additionally, N-fixing cyanobacterial blooms have been documented to occur in N-rich, P-poor waters, which is counterintuitive from the paradigm that low N and high P promotes blooms. For example, Lake Erie's central basin has Dolichospermum blooms when nitrate concentrations are high, which raises questions about which nutrient(s) are selecting for Dolichospermum over other phytoplankton and why an N-fixer is present in high N waters?
2. We conducted a 4-year (2014–2017) study in Lake Erie's central basin to determine which nutrient (P, N, or trace nutrients such as Fe, molybdenum [Mo], and boron [B]) constrained chlorophyll concentration, phytoplankton biovolume, and nitrate assimilation using nutrient enrichment bioassays. The enriched lake water was incubated in 1-L bottles in a growth chamber programmed at light and temperatures of in situ conditions for 4–7 days. We also quantified heterocytes when N-fixing cyanobacteria were present.
3. Compared to the non-enriched control, the P-enriched (+P) treatment had significantly higher chlorophyll and phytoplankton biovolume in c. 75% of experiments. Combination enrichments of P with ammonium-N, nitrate-N, Fe, Mo, and B were compared to the +P treatment to determine secondary limitations. +P and ammonium-N and +P nitrate-N resulted in higher chlorophyll in 50% of experiments but higher phytoplankton biovolume in only 25% of experiments. These results show that P was the primary limiting nutrient, but there were times when N was secondarily limiting.
4. Chlorophyll concentration indicated N secondary limitation in half of the experiments, but biovolume indicated only N secondary limitation in 25% of the experiments. To make robust conclusions from nutrient enrichment bioassays, both chlorophyll and phytoplankton biovolume should be measured.
5. The secondary effects of Fe, Mo, and B on chlorophyll were low (<26% of experiments), and no secondary effects were observed on phytoplankton biovolume and nitrate assimilation. However, +P and Fe resulted in more chlorophyll than +P in experiments conducted during Dolichospermum blooms, and +P and B significantly increased the number of heterocytes in Dolichospermum. These results indicate that low Fe availability might select for Dolichospermum, and low B constrains heterocyte formation in the central basin of Lake Erie. Furthermore, these results could apply to other lakes with high N and low P where diazotrophic cyanobacterial blooms occur.

     

Diatom elemental and morphological changes in response to iron limitation: a brief review with potential paleoceanographic applications

Diatoms are a major group of phytoplankton that account for approximately 40% of the ocean carbon fixation and the vast majority of biogenic silica production through the construction of their cell walls (termed frustules). These frustules accumulate and are partially preserved in the ocean sediments. Diatom growth and nutrient utilization in high‐nitrate, low‐chlorophyll regions of the world’s oceans are mostly regulated by iron availability. Diatoms acclimate to iron limitation by decreasing cell size. The associated increase in surface area‐to‐volume ratio and decrease in diffusive boundary layer thickness may improve nutrient uptake kinetics. In parallel, cellular silicon (Si) contents are elevated in iron‐limited diatoms relative to nitrogen (N) and carbon (C). Variations in degree of silicification and nutritional requirements of iron‐limited diatoms have been hypothesized to account for higher cellular Si and/or lower cellular N and C, respectively. However, in some diatoms, frustule silicification does not significantly change when cells are iron‐limited. Instead, changes in the Si‐containing valve surface area relative to volume within these diatoms is hypothesized to be responsible for the variations in the cellular Si : N and Si : C ratios. In particular, some examined iron‐limited pennate diatoms have reduced widths relative to their lengths (i.e. lower length‐normalized widths, LNW) compared to iron‐replete cells. In the pennate diatom Fragilariopsis kerguelensis, the mean LNWs of valves preserved in sediments throughout the Southern Ocean (a well‐characterized iron‐limited region) is positively correlated with satellite‐derived, climatological net primary productivity in the overlying waters. Because of the specific morphological changes in pennate diatom frustules in response to iron availability, the valve morphometerics (e.g. LNWs) can potentially be used as a diagnostic tool for iron‐limited diatom growth and relative changes in the Si : N (and Si : C) ratios in extant diatom assemblages as well as those preserved in the sediments.     

The role of phosphorus on planktonic production of the Gironde plume waters in the Bay of Biscay

More and more studies emphasize the status of phosphorus (P)as the principal limiting nutrient of phytoplankton growth,especially in coastal waters under the influence of freshwaterdischarges. The purpose of the present paper is to investigatethe role of P on planktonic production in the waters influencedby the Gironde discharges; the Gironde being one of the twolargest rivers on the French Atlantic coast. The survey is basedon several cruises made in 1998 and 1999. Two different patternswere observed for waters with salinity below and above 34.5.For waters with salinity < 34.5, P was found to be the firstlimiting nutrient of winter and spring phytoplankton blooms,based on undetectable phosphate (< 20 nM), high NO₃ : PO₄ratios, typically > 100 : 1, short phosphate turnover time(1 to 2 h), high alkaline phosphatase activities (mean of 176nM h^-1 in late May 1999) and ultimately great increases of chlorophylla (Chl a) and primary production in phosphate-enriched samplesrelative to controls. This limitation could be partly explainedby the Gironde nutrient supplies, which were phosphate deficientcompared with the mineral nitrogen(N_min : PO₄ was > 40 withina salinity range 16–33). In summer, corresponding to theperiod of low influence of Gironde supplies (low runoff anda spreading effect of the plume), phytoplankton growth wouldbe controlled by both P and nitrogen (N), according to low nitrateand the major effect of combined P+N (NH₄) enrichment on Chla and primary production compared with the addition of N orP singly. In early October, after the first autumn gales, themixed layer was enriched with a sufficient supply of nutrientsto support exponential phytoplankton growth for 4 days in enclosures.The pattern was different for waters at the limit of the Girondeplume and Atlantic oceanic waters (within salinity range 34.5–35.4).P would not be the single limiting nutrient of winter bloomsand spring phytoplankton growth since low phosphate, and alsolow nitrate and silicate, availability were recorded and phosphateaddition alone had no effect on phytoplankton biomass and productionin bioassays. The early P limitation of winter blooms had consequencesfor the phytoplankton community structure in the Gironde plumewaters (salinity < 34.5). Whereas major cells of these bloomswere greater than 20 µm in size, phytoplankton growthin spring and autumn was dominated by 3–20 µm (e.g.53% of Chl a in late April 1999) and < 3 µm cells (e.g.29% of Chl a). The decreasing size of phytoplankton cells isemphasized by the severe competition between bacteria and algaefor phosphate, since bacteria dominated phosphate uptake inspring (e.g. 87% in late April, 77% in late May). Bacteria tendedto have greater affinity for phosphate and seemed also to beP limited at certain times in spring, according to results fromphosphate enrichment bioassays in late May 1999. The alternativemethod for phytoplankton to obtain P would be the use of thedissolved organic phosphorus pool by alkaline phosphatase activity.According to the movement of ³³P after initial labelling ofmicrobial populations and a subsequent cold chase, the majortransfer of P occurred from the bacterial to the dissolved fraction.We hypothesize that algae obtain part of its dissolved organicphosphorus from bacteria-originated organic phosphorus compounds.     

Nutrient limitation of phytoplankton in solar salt ponds in Shark Bay,Western Australia

The aim of this research was to examine nutrient limitation of phytoplankton in solar salt ponds of varying salinity at Useless Inlet in Western Australia. These ponds use solar energy to evaporate seawater for the purpose of commercial salt production. A combination of techniques involving water column nutrient ratios, comparisons of nutrient concentrations to concentration of magnesium ions and bioassays were used in the investigation. Comparisons of changes in dissolved inorganic nitrogen to phosphorus ratios and concentrations of dissolved inorganic nutrients against changes in concentrations of the conservative cation Mg²⁺ indicated that phytoplankton biomass was potentially nitrogen limited along the entire pond salinity gradient. Nutrient addition bioassays indicated that in low salinity ponds, phytoplankton was nitrogen limited but in high salinity ponds, phosphorus limited. This may be due to isolation of phytoplankton in bioassay bottles from in situ conditions as well as to changes in phytoplankton species composition between ponds, and the variable availability of inorganic and organic nutrient sources. The differences in limiting nutrient between methods indicate that phytoplankton cells may be proximally limited by nutrients that are not theoretically limiting at the pond scale. Dissolved organic nutrients constituted a large proportion of total nutrients, with concentrations increasing through the pond sequence of increasing salinity. From the change in nutrient concentrations in bioassay bottles, sufficient dissolved organic nitrogen may be available for phytoplankton uptake in low salinity ponds, potentially alleviating the dissolved inorganic nitrogen limitation of phytoplankton biomass. Guest Editors: J. John & B. Timms Salt Lake Research: Biodiversity and Conservation—Selected Papers from the 9th Conference of the International Society for Salt Lake Research     

沿岸海域富营养化与赤潮发生的关系

综述了赤潮的发生与沿岸海域富营养化的关系。近几十年来,人类活动使得天然水体的富营养化进程大大加速。营养负荷的增加与高生物量水华的增多相联系。控制营养输入后,浮游植物生物量或有害藻类水华事件也相应减少。营养的组成与浮游植物的种类组成及水华的形成有密切联系。有机营养对有害藻类水华的促进作用受到关注。营养输入时机影响浮游植物种间竞争的结果,因而对浮游植物的群落演替具有深远影响。由于浮游植物存在生理差异,因而对营养加富的反应因种而异。营养在调控某些有毒藻类的毒素产量方面也发挥着重要作用。此外,营养输入与藻类水华之间存在复杂的间接联系。当然,营养状况并非浮游植物群落演替的唯一决定因素。研究结果提示,控制营养输入、减缓水域富营养化是减少有害藻类水华发生的有效途径,而深入研究典型有害藻类的营养生理对策则为防治并最终消除有害藻类水华提供了理论基础。