High predictability of direct competition between marine diatoms under different temperatures and nutrient states

The distribution of marine phytoplankton will shift alongside changes in marine environments, leading to altered species frequencies and community composition. An understanding of the response of mixed populations to abiotic changes is required to adequately predict how environmental change may affect the future composition of phytoplankton communities. This study investigated the growth and competitive ability of two marine diatoms, Phaeodactylum tricornutum and Thalassiosira pseudonana , along a temperature gradient (9–35°C) spanning the thermal niches of both species under both high‐nitrogen nutrient‐replete and low‐nitrogen nutrient‐limited conditions. Across this temperature gradient, the competitive outcome under both nutrient conditions at any assay temperature, and the critical temperature at which competitive advantage shifted from one species to the other, was well predicted by the temperature dependencies of the growth rates of the two species measured in monocultures. The temperature at which the competitive advantage switched from P. tricornutum to T. pseudonana increased from 18.8°C under replete conditions to 25.3°C under nutrient‐limited conditions. Thus, P. tricornutum was a better competitor over a wider temperature range in a low N environment. Being able to determine the competitive outcomes from physiological responses of single species to environmental changes has the potential to significantly improve the predictive power of phytoplankton spatial distribution and community composition models

Phytoplankton mortality in a changing thermal seascape.

Predicting spatiotemporal distributions of phytoplankton biomass and community composition heavily relies on experimental studies that document how environmental conditions influence population growth rates. In unicellular phytoplankton the net population growth rate is the difference between the cell division rate and the death rate. Along with predation and disease, phytoplankton mortality arises from abiotic stress. Although the effect of temperature on the net population growth rate is well understood, studies examining thermally induced death rates in phytoplankton are scarce. We investigated how cell division and death rates of the diatom Phaeodactylum tricornutum varied within its thermal tolerance limits (thermal niche), and at temperatures just above its upper thermal tolerance limit. We show that death rates were largely independent of temperature when P. tricornutum was grown within its thermal niche, but increased significantly at temperatures that approached or exceeded its upper thermal tolerance limit. Furthermore, the sensitivity of mortality increased with the duration of exposure to heat stress and was affected by the pre-acclimation temperature. Heat waves can be expected to significantly affect phytoplankton mortality episodically. The increasing frequency of heat waves accompanying global warming can be expected to drive changes in phytoplankton community structure due to interspecific variability of thermal niches with potential implications for food web dynamics and biogeochemical cycles

Projected expansion of Trichodesmium’s geographical distribution and increase of growth potential in response to climate change

Estimates of marine N₂ fixation range from 52 to 73 Tg N yr‾¹, of which we calculate up to 84% is from Trichodesmium based on previous measurements of nifH gene abundance and our new model of Trichodesmium growth. Here we assess the likely effects of four major climate change‐related abiotic factors on the spatiotemporal distribution and growth potential of Trichodesmium for the last glacial maximum (LGM), the present (2006‐2015) and the end of this century (2100) by mapping our model of Trichodesmium growth onto inferred global surface ocean fields of pCO₂, temperature, light and Fe. We conclude that growth rate was severely limited by low pCO₂ at the LGM, that current pCO₂ levels do not significantly limit Trichodesmium growth and thus, the potential for enhanced growth from future increases of CO₂ is small. We also found that the area of the ocean where sea surface temperatures (SST) are within Trichodesmium’s thermal niche increased by 32% from the LGM to present, but further increases in SST due to continued global warming will reduce this area by 9%. However, the range reduction at the equator is likely to be offset by enhanced growth associated with expansion of regions with optimal or near optimal Fe and light availability. Between now and 2100, the ocean area of optimal SST and irradiance is projected to increase by 7%, and the ocean area of optimal SST, irradiance and iron is projected to increase by 173%. Given the major contribution of this keystone species to annual N₂ fixation and thus pelagic ecology, biogeochemistry and CO₂ sequestration, the projected increase in the geographical range for optimal growth could provide a negative feedback to increasing atmospheric CO₂ concentrations

An integrated response of Trichodesmium erythraeum IMS101 growth and photo-physiology to Iron, CO₂, and light intensity

We have assessed how varying CO 2 (180, 380, and 720 μatm) and growth light intensity (40 and 400 μmol photons m -2 s -1 ) affected Trichodesmium erythraeum IMS101 growth and photophysiology over free iron (Fe') concentrations between 20 and 9,600 pM. We found significant iron dependencies of growth rate and the initial slope and maximal relative PSII electron transport rates (rP m ). Under iron-limiting concentrations, high-light increased growth rates and rPm; possibly indicating a lower allocation of resources to iron-containing photosynthetic proteins. Higher CO 2 increased growth rates across all iron concentrations, enabled growth to occur at lower Fe' concentrations, increased rPm and lowered the iron half saturation constants for growth (K m ). We attribute these CO 2 responses to the operation of the CCM and the ATP spent/saved for CO 2 uptake and transport at low and high CO 2 , respectively. It seems reasonable to conclude that T. erythraeum IMS101 can exhibit a high degree of phenotypic plasticity in response to CO 2 , light intensity and iron-limitation. These results are important given predictions of increased dissolved CO 2 and water column stratification (i.e., higher light exposures) over the coming decades

Inorganic carbon and pH dependency of Trichodesmium's photosynthetic rates.

We established the relationship between photosynthetic carbon fixation rates and pH, CO2 and HCO3- concentrations in the diazotroph Trichodesmium erythraeum IMS101. Inorganic 14C-assimilation was measured in TRIS-buffered ASW medium where the absolute and relative concentrations of CO2, pH and HCO3- were manipulated. First, we varied the total dissolved inorganic carbon concentration (TIC) (< 0 to ~ 5 mM) at constant pH, so ratios of CO2 and HCO3- remained relatively constant. Second, we varied pH (~ 8.54 to 7.52) at constant TIC, so CO2 increased whilst HCO3- declined. We found that 14C-assimilation could be described by the same function of CO2 for both approaches but showed different dependencies on HCO3- when pH was varied at constant TIC than when TIC was varied at constant pH. A numerical model of Trichodesmium's CCM showed carboxylation rates are modulated by HCO3- and pH. The decrease in Ci assimilation at low CO2, when TIC was varied, is due to HCO3- uptake limitation of the carboxylation rate. Conversely, when pH was varied, Ci assimilation declined due to a high-pH mediated increase in HCO3- and CO2 leakage rates, potentially coupled to other processes (uncharacterised within the CCM model) that restrict Ci assimilation rates under high-pH conditions

Iron and phosphorus co-limit nitrogen fixation in the eastern tropical North Atlantic

The role of iron in enhancing phytoplankton productivity in high nutrient, low chlorophyll oceanic regions was demonstrated first through iron-addition bioassay experiments1 and subsequently confirmed by large-scale iron fertilization experiments2. Iron supply has been hypothesized to limit nitrogen fixation and hence oceanic primary productivity on geological timescales3, providing an alternative to phosphorus as the ultimate limiting nutrient4. Oceanographic observations have been interpreted both to confirm and refute this hypothesis5, 6, but direct experimental evidence is lacking7. We conducted experiments to test this hypothesis during the Meteor 55 cruise to the tropical North Atlantic. This region is rich in diazotrophs8 and strongly impacted by Saharan dust input9. Here we show that community primary productivity was nitrogen-limited, and that nitrogen fixation was co-limited by iron and phosphorus. Saharan dust addition stimulated nitrogen fixation, presumably by supplying both iron and phosphorus10, 11. Our results support the hypothesis that aeolian mineral dust deposition promotes nitrogen fixation in the eastern tropical North Atlantic

Predicting the Electron Requirement for Carbon Fixation in Seas and Oceans

Marine phytoplankton account for about 50% of all global net primary productivity (NPP). Active fluorometry, mainly Fast Repetition Rate fluorometry (FRRf), has been advocated as means of providing high resolution estimates of NPP. However, not measuring CO2-fixation directly, FRRf instead provides photosynthetic quantum efficiency estimates from which electron transfer rates (ETR) and ultimately CO2-fixation rates can be derived. Consequently, conversions of ETRs to CO2-fixation requires knowledge of the electron requirement for carbon fixation (Φe,C, ETR/CO2 uptake rate) and its dependence on environmental gradients. Such knowledge is critical for large scale implementation of active fluorescence to better characterise CO2-uptake. Here we examine the variability of experimentally determined Φe,C values in relation to key environmental variables with the aim of developing new working algorithms for the calculation of Φe,C from environmental variables. Coincident FRRf and 14C-uptake and environmental data from 14 studies covering 12 marine regions were analysed via a meta-analytical, non-parametric, multivariate approach. Combining all studies, Φe,C varied between 1.15 and 54.2 mol e- (mol C)-1 with a mean of 10.9±6.91 mol e- mol C)-1. Although variability of Φe,C was related to environmental gradients at global scales, region-specific analyses provided far improved predictive capability. However, use of regional Φe,C algorithms requires objective means of defining regions of interest, which remains challenging. Considering individual studies and specific small-scale regions, temperature, nutrient and light availability were correlated with Φe,C albeit to varying degrees and depending on the study/region and the composition of the extant phytoplankton community. At the level of large biogeographic regions and distinct water masses, Φe,C was related to nutrient availability, chlorophyll, as well as temperature and/or salinity in most regions, while light availability was also important in Baltic Sea and shelf waters. The novel Φe,C algorithms provide a major step forward for widespread fluorometry-based NPP estimates and highlight the need for further studying the natural variability of Φe,C to verify and develop algorithms with improved accuracy. © 2013 Lawrenz et al

CO2 modulation of the rates of photosynthesis and light-dependent O2 consumption in Trichodesmium

As atmospheric CO₂ concentrations increase, so too does the dissolved CO₂ and HCO₃‾ concentrations in the world’s oceans. There are still many uncertainties regarding the biological response of key groups of organisms to these changing conditions, which is crucial for predicting future species distributions, primary productivity rates, and biogeochemical cycling. In this study, we established the relationship between gross photosynthetic O₂ evolution and light-dependent O₂ consumption in Trichodesmium erythraeum IMS101 acclimated to three targeted pCO₂ concentrations (180 µmol mol‾¹=low-CO₂, 380 µmol mol‾¹=mid-CO₂, and 720 µmol mol‾¹=high-CO₂). We found that biomass- (carbon) specific, light-saturated maximum net O₂ evolution rates (PnC,max) and acclimated growth rates increased from low- to mid-CO₂, but did not differ significantly between mid- and high-CO₂. Dark respiration rates were five times higher than required to maintain cellular metabolism, suggesting that respiration provides a substantial proportion of the ATP and reductant for N₂ fixation. Oxygen uptake increased linearly with gross O₂ evolution across light intensities ranging from darkness to 1100 µmol photons m¯² s¯¹. The slope of this relationship decreased with increasing CO₂, which we attribute to the increased energetic cost of operating the carbon-concentrating mechanism at lower CO₂ concentrations. Our results indicate that net photosynthesis and growth of T. erythraeum IMS101 would have been severely CO₂ limited at the last glacial maximum, but that the direct effect of future increases of CO₂ may only cause marginal increases in growth

A Key Marine Diazotroph in a Changing Ocean: The Interacting Effects of Temperature, CO2 and Light on the Growth of Trichodesmium erythraeum IMS101

Trichodesmium is a globally important marine diazotroph that accounts for approximately 60-80% of marine biological N2 fixation and as such plays a key role in marine N and C cycles. We undertook a comprehensive assessment of how the growth rate of Trichodesmium erythraeum IMS101 was directly affected by the combined interactions of temperature, pCO2 and light intensity. Our key findings were: low pCO2 affected the lower temperature tolerance limit (Tmin) but had no effect on the optimum temperature (Topt) at which growth was maximal or the maximum temperature tolerance limit (Tmax); low pCO2 had a greater effect on the thermal niche width than low-light; the effect of pCO2 on growth rate was more pronounced at suboptimal temperatures than at supraoptimal temperatures; temperature and light had a stronger effect on the photosynthetic efficiency (Fv/Fm) than did CO2; and at Topt, the maximum growth rate increased with increasing CO2, but the initial slope of the growth-irradiance curve was not affected by CO2. In the context of environmental change, our results suggest that the (i) nutrient replete growth rate of Trichodesmium IMS101 would have been severely limited by low pCO2 at the last glacial maximum (LGM), (ii) future increases in pCO2 will increase growth rates in areas where temperature ranges between Tmin to Topt, but will have negligible effect at temperatures between Topt and Tmax, (iii) areal increase of warm surface waters (> 18°C) has allowed the geographic range to increase significantly from the LGM to present and that the range will continue to expand to higher latitudes with continued warming, but (iv) continued global warming may exclude Trichodesmium spp. from some tropical regions by 2100 where temperature exceeds Topt

Assessing the uncertainties of model estimates of primary productivity in the tropical Pacific Ocean

Author Posting. © Elsevier B.V., 2009. This is the author's version of the work. It is posted here by permission of Elsevier B.V. for personal use, not for redistribution. The definitive version was published in Journal of Marine Systems 76 (2009): 113-133, doi:10.1016/j.jmarsys.2008.05.010.Depth-integrated primary productivity (PP) estimates obtained from satellite ocean color based models (SatPPMs) and those generated from biogeochemical ocean general circulation models (BOGCMs) represent a key resource for biogeochemical and ecological studies at global as well as regional scales. Calibration and validation of these PP models are not straightforward, however, and comparative studies show large differences between model estimates. The goal of this paper is to compare PP estimates obtained from 30 different models (21 SatPPMs and 9 BOGCMs) to a tropical Pacific PP database consisting of ~1000 14C measurements spanning more than a decade (1983- 1996). Primary findings include: skill varied significantly between models, but performance was not a function of model complexity or type (i.e. SatPPM vs. BOGCM); nearly all models underestimated the observed variance of PP, specifically yielding too few low PP (< 0.2 gC m-2d-2) values; more than half of the total root-mean-squared model-data differences associated with the satellite-based PP models might be accounted for by uncertainties in the input variables and/or the PP data; and the tropical Pacific database captures a broad scale shift from low biomass-normalized productivity in the 1980s to higher biomass-normalized productivity in the 1990s, which was not successfully captured by any of the models. This latter result suggests that interdecadal and global changes will be a significant challenge for both SatPPMs and BOGCMs. Finally, average root-mean-squared differences between in situ PP data on the equator at 140°W and PP estimates from the satellite-based productivity models were 58% lower than analogous values computed in a previous PP model comparison six years ago. The success of these types of comparison exercises is illustrated by the continual modification and improvement of the participating models and the resulting increase in model skill.This research was supported by a grant from the National Aeronautics and Space Agency Ocean Biology and Biogeochemistry program (NNG06GA03G), as well as by numerous other grants to the various participating investigator