Phytoplankton size structure is key for the ecology and biogeochemistry of pelagic ecosystems, but the relationship between cell size and maximum growth rate (μmax) is not yet well understood. We ...used cultures of 22 species of marine phytoplankton from five phyla, ranging from 0.1 to 106 μm3 in cell volume (Vcell), to determine experimentally the size dependence of growth, metabolic rate, elemental stoichiometry and nutrient uptake. We show that both μmax and carbon‐specific photosynthesis peak at intermediate cell sizes. Maximum nitrogen uptake rate (VmaxN) scales isometrically with Vcell, whereas nitrogen minimum quota scales as Vcell0.84. Large cells thus possess high ability to take up nitrogen, relative to their requirements, and large storage capacity, but their growth is limited by the conversion of nutrients into biomass. Small species show similar volume‐specific VmaxN compared to their larger counterparts, but have higher nitrogen requirements. We suggest that the unimodal size scaling of phytoplankton growth arises from taxon‐independent, size‐related constraints in nutrient uptake, requirement and assimilation.
The universal temperature dependence of metabolic rates has been used to predict how ocean biology will respond to ocean warming. Determining the temperature sensitivity of phytoplankton metabolism ...and growth is of special importance because this group of organisms is responsible for nearly half of global primary production, sustains most marine food webs, and contributes to regulate the exchange of CO2 between the ocean and the atmosphere. Phytoplankton growth rates increase with temperature under optimal growth conditions in the laboratory, but it is unclear whether the same degree of temperature dependence exists in nature, where resources are often limiting. Here we use concurrent measurements of phytoplankton biomass and carbon fixation rates in polar, temperate and tropical regions to determine the role of temperature and resource supply in controlling the large-scale variability of in situ metabolic rates. We identify a biogeographic pattern in phytoplankton metabolic rates, which increase from the oligotrophic subtropical gyres to temperate regions and then coastal waters. Variability in phytoplankton growth is driven by changes in resource supply and appears to be independent of seawater temperature. The lack of temperature sensitivity of realized phytoplankton growth is consistent with the limited applicability of Arrhenius enzymatic kinetics when substrate concentrations are low. Our results suggest that, due to widespread resource limitation in the ocean, the direct effect of sea surface warming upon phytoplankton growth and productivity may be smaller than anticipated.
The Red Sea depicts a north–south gradient of positively correlated temperature and nutrient concentration. Despite its overall oligotrophic characteristics, primary production rates in the Red Sea ...vary considerably. In this study, based on five cruises and a 2‐year time series (2016–2018) sampling in the Central Red Sea, we determined phytoplankton photosynthetic rates (PP) by using 13C as a tracer and derived phytoplankton net growth rates (μ) and chlorophyll a (Chl a)‐normalized photosynthesis (PB). Our results indicate a ninefold variation (14–125 mgC m−2 h−1) in depth‐integrated primary production and reveal a marked seasonality in PP, PB, and μ. Depth‐integrated PP remained <30 mg C m−2 h−1 during spring and summer, and peaked in autumn–winter, particularly in the southernmost stations (~17°N). In surface waters, phytoplankton grew at a slow rate (0.2 ± 0.02 d−1), with the population doubling every 3.5 days, on average. However, during the autumn–winter period, when Chl a concentrations peaked in the central and southern regions, μ increased to values between 0.60 and 0.84 d−1, while PB reached its maximum rate (7.8 mgC mg Chl a−1 h−1). We used path analysis to resolve direct vs. indirect components between correlations. Our results show that nutrient availability modulates the photosynthetic performance and growth of phytoplankton communities and that PB and μ fluctuations are not directly associated with temperature changes. Our study suggests that similarly to other oligotrophic warm seas, phosphorus concentration exerts a key role in defining photosynthetic rates and the biomass levels of phytoplankton communities in the region.
The distribution of bioactive trace metals has the potential to enhance or limit primary productivity and carbon export in some regions of the world ocean. To study these connections, the ...concentrations of Cd, Co, Cu, Fe, Mo, Ni, and V were determined for 110 surface water samples collected during the Malaspina 2010 Circumnavigation Expedition (MCE). Total dissolved Cd, Co, Cu, Fe, Mo, Ni, and V concentrations averaged 19.0 ± 5.4 pM, 21.4 ± 12 pM, 0.91 ± 0.4 nM, 0.66 ± 0.3 nM, 88.8 ± 12 nM, 1.72 ± 0.4 nM, and 23.4 ± 4.4 nM, respectively, with the lowest values detected in the Central Pacific and increased values at the extremes of all transects near coastal zones. Trace metal concentrations measured in surface waters of the Atlantic Ocean during the MCE were compared to previously published data for the same region. The comparison revealed little temporal changes in the distribution of Cd, Co, Cu, Fe, and Ni over the last 30 years. We utilized a multivariable linear regression model to describe potential relationships between primary productivity and the hydrological, biological, trace nutrient and macronutrient data collected during the MCE. Our statistical analysis shows that primary productivity in the Indian Ocean is best described by chlorophyll a, NO3, Ni, temperature, SiO4, and Cd. In the Atlantic Ocean, primary productivity is correlated with chlorophyll a, NO3, PO4, mixed layer depth, Co, Fe, Cd, Cu, V, and Mo. The variables salinity, temperature, SiO4, NO3, PO4, Fe, Cd, and V were found to best predict primary productivity in the Pacific Ocean. These results suggest that some of the lesser studied trace elements (e.g., Ni, V, Mo, and Cd) may play a more important role in regulating oceanic primary productivity than previously thought and point to the need for future experiments to verify their potential biological functions.
Key Points
The distribution of trace metals in waters of the global ocean was determined
No multiyear variation in the distribution of trace metals in the Atlantic Ocean was observed
Some metals correlate with primary productivity, suggesting potential metal limitation
We determined the rates of photosynthesis and respiration in batch cultures of 22 marine phytoplankton species from five phyla covering a range of 7 orders of magnitude in cell size. Rates were ...determined during the exponential growth phase and also during the stationary phase, when cell growth was limited by nitrogen availability. We observed, in all growth phases, a curvature in the size scaling of carbon fixation, such that the relationship between carbon-specific photosynthesis and cell size was unimodal, with the highest rates being measured in intermediate-size species. The log–log relationship between individual metabolic rates and cell size showed an overall lineal pattern with a slope equal or near 1, irrespective of whether volume or carbon is used as a metric for cell size. Thus, our results demonstrate that when small species (<50μm3 cell diameter) are considered together with intermediate- and large-sized species phytoplankton metabolism does not follow Kleiber's 3/4-power rule. Considering all species together, respiration losses represented on average 9% and 22% of total carbon fixation during the exponential growth and stationary phases, respectively. Carbon-specific respiration was largely independent of cell size and growth phase, but tended to take higher values in the dinoflagellates. During the stationary growth phase, and contrary to other groups, most diatoms were able to maintain carbon fixation rates similar to those measured during exponential growth. Our results highlight the ability of intermediate-to-large size species to sustain high metabolic rates in spite of their cell size, which helps to explain why they dominate phytoplankton blooms in the ocean.
•Size-scaling of phytoplankton metabolism cannot be predicted by Kleiber’s rule.•Both large and small phytoplankton species sustain similar metabolic rates.•Intermediate-size phytoplankton species can attain faster biomass-specific metabolic rates.•There are significant taxon-related differences in metabolic rates.
Transparent exopolymer particles (TEP) are an abundant class of suspended organic particles, mainly formed by polysaccharides, which play important roles in biogeochemical and ecological processes in ...the ocean. In this study we investigated horizontal and vertical TEP distributions (within the euphotic layer, including the upper surface) and their short-term variability along with a suite of environmental and biological variables in four distinct regions of the Southern Ocean. TEP concentrations in the surface (4 m) averaged 102.3 ± 40.4 μg XG eq. L−1 and typically decreased with depth. Chlorophyll a (Chl a) concentration was a better predictor of TEP variability across the horizontal (R2 = 0.66, p < 0.001) and vertical (R2 = 0.74, p < 0.001) scales than prokaryotic heterotrophic abundance and production. Incubation experiments further confirmed the main role of phytoplankton as TEP producers. The highest surface TEP concentrations were found north of the South Orkney Islands (144.4 ± 21.7 μg XG eq. L−1), where the phytoplankton was dominated by cryptophytes and haptophytes; however, the highest TEP:Chl a ratios were found south of these islands (153.4 ± 29.8 μg XG eq (μg Chl a)−1, compared to a mean of 79.3 ± 54.9 μg XG eq (μg Chl a)−1 in the whole cruise, in association with haptophyte dominance, proximity of sea ice and high exposure to solar radiation. TEP were generally enriched in the upper surface (10 cm) respect to 4 m, despite a lack of biomass enrichment, suggesting either upward transport by positive buoyancy or bubble scavenging, or higher production at the upper surface by light stress or aggregation. TEP concentrations did not present any significant cyclic diel pattern. Altogether, our results suggest that photobiological stress, sea ice melt and turbulence add to phytoplankton productivity in driving TEP distribution across the Antarctic Peninsula area and Atlantic sector of the Southern Ocean.
Display omitted
•Transparent exopolymer particles (TEP) were measured in the Southern Ocean during summer.•Phytoplankton were the main drivers of both horizontal and vertical TEP distribution.•Light stress and sea ice melt and retreat further tuned TEP distribution.•TEP enrichment generally occurred near the upper surface (0.1 vs 4 m).•Upper-surface enrichment was likely enhanced by wind-provoked turbulence and bubbles.
Resolving the environmental drivers shaping planktonic communities is
fundamental for understanding their variability, in the present and the
future, across the ocean. More specifically, addressing ...the
temperature-dependence response of planktonic communities is essential as
temperature plays a key role in regulating metabolic rates and thus potentially
defining the ecosystem functioning. Here we quantified plankton metabolic
rates along the Red Sea, a uniquely oligotrophic and warm environment, and
analysed the drivers that regulate gross primary production (GPP), community
respiration (CR), and net community production (NCP). The study was conducted
on six oceanographic surveys following a north–south transect along the
Saudi Arabian coast. Our findings revealed that GPP and CR rates increased
with increasing temperature (R2=0.41 and 0.19, respectively;
p<0.001 in both cases), with a higher activation energy (Ea) for
GPP (1.20±0.17 eV) than for CR (0.73±0.17 eV). The higher Ea
for GPP than for CR resulted in a positive relationship between NCP and
temperature. This unusual relationship is likely driven by the relatively
higher nutrient availability found towards the warmer region (i.e. southern Red Sea), which favours GPP rates above the threshold that
separates autotrophic from heterotrophic communities (1.7 mmol O2 m−3 d−1) in this region. Due to the arid nature, the basin
lacks riverine and terrestrial inputs of organic carbon to subsidise a
higher metabolic response of heterotrophic communities, thus constraining CR
rates. Our study suggests that GPP increases steeply with increasing
temperature in the warm ocean when relatively high nutrient inputs are
present.
Due to the increasing constraints on using the radioactive isotope
C to measure primary productivity (
C-PP), we determined the surface carbon fixation rates in the Mediterranean Sea, using the ...alternative stable isotope
C method (
C-PP). Rates obtained (
C-POCp) were compared with simultaneous
C-POCp measurements in samples of different volumes (72 mL and 1.2 L). We also tested the variation of the percentage of dissolved primary production (PER), to the total productivity using organic and inorganic filters (
C method).
C-POCp rates ranged from 0.4, in the Ionian basin, to 1.5 mgC m
h
in the Ligurian region. These results agreed with those found with the
C-PP in 1.2-L samples (two sample
-test,
= 1.035,
= 22,
= 0.31). However, we found that
C-POCp rates derived from 72-mL incubations were 46% lower than those measured with
C-PP. The discrepancy between large and small volume incubations was likely due to differences in the number of large phytoplankton cells within the community. PER values measured with silver membrane filters yielded similar results than those obtained using polycarbonate filters. Our findings showed that when the sample size is carefully chosen, the
C-PP provide comparable results to
C-PP even in waters of low productivity in the Mediterranean Sea.
Short-term experiments indicate that seawater acidification can cause a decrease in the rate of calcification by coccolithophores, but the relationship between carbonate chemistry and coccolithophore ...calcification rate in natural assemblages is still unclear. During the Malaspina 2010 circumnavigation, we measured primary production, calcification, coccolithophore abundance, particulate inorganic carbon (PIC) concentration, and the parameters of the carbonate system, along basin-scale transects in the tropical Atlantic, Indian and Pacific oceans. Euphotic layer-integrated calcification and mean cell-specific calcification in the euphotic layer ranged between 2–10 mgC m−2 d−1 and 5–20 pgC cell−1 d−1, respectively. We found a significant relationship between primary production and calcification, such that the calcification to primary production (CP/PP) ratio was relatively invariant among ocean basins, with an overall mean value of 0.05 ± 0.04. Extrapolating this value to the entire ocean would result in a global pelagic calcification rate of 2.4 PtC yr−1. The mean PIC concentration in surface waters was 1.8 ± 1.6 mgC m−3 and its turnover time averaged 20 d. We combined our data of calcification, primary production, and carbonate chemistry from Malaspina 2010 with those obtained during two previous cruises in the northern Arabian Sea. Both the CP/PP ratio and cell-specific calcification were largely constant across a wide range of calcite saturation state (1.5–6.5),
HCO
3
−
/
H
+
(0.08–0.24; mol: μmol), and pH (7.6–8.1), which indicates that calcification by natural coccolithophore assemblages was independent of carbonate chemistry. Our results suggest that coccolithophore calcification, at least in tropical regions, may not be decreasing in the currently acidifying ocean.
Measurements of isotopic composition of marine primary producers are a valuable tool to follow and trace the source and cycling of organic matter in the marine systems, as well to describe the ...physiological status of aquatic photosynthetic organisms. Although stable isotope data abounds in the literature, relatively limited information regarding the isotopic signatures of marine primary producers is available for the Red Sea. Here we present data on carbon concentration (and nitrogen when possible) of phytoplankton, macroalgae, seagrasses, mangroves and salt-marsh plants, and examine how their isotopic signatures differed among plant types across a north-south gradient in the Red Sea. We also tested the potential use of deuterium, δD, to distinguish among primary producers whose carbon isotopic values may overlap. Our findings showed a clear differentiation of carbon and nitrogen content between the different groups of primary producers, as well as between species. Seagrasses and mangroves had on average larger carbon (30 and 49 % of C, respectively) and nitrogen content (1.8 % N) than other groups. In terms of stable carbon isotopes, seagrasses and macroalgae tended to be heavier (-7.3 ‰ and -13.3 ‰, respectively) than halophytes, mangroves, and phytoplankton, which showed statistically similar and lighter δ13C values (between -24 ‰ and -26 ‰). There was a tendency for the nitrogen isotopic composition of seagrass and macroalgae to become lighter from the southern to the northern Red Sea, in parallel to a decline in nitrogen concentration in the tissues, indicative of a higher dependence of nitrogen fixation as a source of nitrogen toward the more oligotrophic northern Red Sea. Our results showed an overlap in the δ13C and δ15N values between macroalgae and seagrasses; however, their δD values were significantly different (seagrasses -56.6 ± 2.8 ‰ and macroalgae -95.7 ± 3.4 ‰). This remarkable difference offers a promising alternative for ecological studies where a similar range of isotopic values could mask different potential sources.
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