John J. Cullen

Autotrophic Picoplankton in the Tropical Ocean

In phytoplankton of the eastern tropical Pacific Ocean from 25 to 90 percent of the biomass (measured as chlorophyll a) and 20 to 80 percent of the inorganic carbon fixation were attributable to particles that could pass a screen with a 1-micrometer pore diameter. Evidence is presented that these are indeed autotrophic cells and not cell fragments.

Biological weighting function for the inhibition of phytoplankton photosynthesis by ultraviolet radiation

Severe reduction of stratospheric ozone over Antarctica has focused increasing concern on the biological effects of ultraviolet-B (UVB) radiation (280 to 320 nanometers). Measurements of photosynthesis from an experimental system, in which phytoplankton are exposed to a broad range of irradiance treatments, are fit to an analytical model to provide the spectral biological weighting function that can be used to predict the short-term effects of ozone depletion on aquatic photosynthesis. Results show that UVA (320 to 400 nanometers) significantly inhibits the photosynthesis of a marine diatom and a dinoflagellate, and that the effects of UVB are even more severe. Application of the model suggests that the Antarctic ozone hole might reduce near-surface photosynthesis by 12 to 15 percent, but less so at depth. The experimental system makes possible routine estimation of spectral weightings for natural phytoplankton.

FLUORESCENCE-BASED MAXIMAL QUANTUM YIELD FOR PSII AS A DIAGNOSTIC OF NUTRIENT STRESS

In biological oceanography, it has been widely accepted that the maximum quantum yield of photosynthesis is influenced by nutrient stress. A closely related parameter, the maximum quantum yield for stable charge separation of PSII, (φPSII)m, can be estimated by measuring the increase in fluorescence yield from dark‐adapted minimal fluorescence (Fo) to maximal fluorescence (Fm) associated with the closing of photosynthetic reaction centers with saturating light or with a photosynthetic inhibitor such as 3′‐(3,4‐dichlorophenyl)‐1′,1′‐dimethyl urea (DCMU). The ratio Fv/Fm (= (Fm− Fo)/Fm) is thus used as a diagnostic of nutrient stress. Published results indicate that Fv/Fm is depressed for nutrient‐stressed phytoplankton, both during nutrient starvation (unbalanced growth) and acclimated nutrient limitation (steady‐state or balanced growth). In contrast to published results, fluorescence measurements from our laboratory indicate that Fv/Fm is high and insensitive to nutrient limitation for cultures in steady state under a wide range of relative growth rates and irradiance levels. This discrepancy between results could be attributed to differences in measurement systems or to differences in growth conditions. To resolve the uncertainty about Fv/Fm as a diagnostic of nutrient stress, we grew the neritic diatom Thalassiosira pseudonana (Hustedt) Hasle et Heimdal under nutrient‐replete and nutrient‐stressed conditions, using replicate semicontinuous, batch, and continuous cultures. Fv/Fm was determined using a conventional fluorometer and DCMU and with a pulse amplitude modulated (PAM) fluorometer. Reduction of excitation irradiance in the conventional fluorometer eliminated overestimation of Fo in the DCMU methodology for cultures grown at lower light levels, and for a large range of growth conditions there was a strong correlation between the measurements of Fv/Fm with DCMU and PAM (r2 = 0.77, n = 460). Consistent with the literature, nutrient‐replete cultures showed consistently high Fv/Fm (∼0.65), independent of growth irradiance. Under nutrient‐starved (batch culture and perturbed steady state) conditions, Fv/Fm was significantly correlated to time without the limiting nutrient and to nutrient‐limited growth rate before starvation. In contrast to published results, our continuous culture experiments showed that Fv/Fm was not a good measure of nutrient limitation under balanced growth conditions and remained constant (∼0.65) and independent of nutrient‐limited growth rate under different irradiance levels. Because variable fluorescence can only be used as a diagnostic for nutrient‐starved unbalanced growth conditions, a robust measure of nutrient stressed oceanic waters is still required.

Interactive effects of ozone depletion and vertical mixing on photosynthesis of Antarctic phytoplankton

Photosynthesis of Antarctic phytoplankton is inhibited by ambient ultraviolet (UV) radiation during incubations, and the inhibition is worse in regions beneath the Antarctic ozone ‘hole’. But to evaluate such effects, experimental results on, and existing models of, photosynthesis cannot be extrapolated directly to the conditions of the open waters of the Antarctic because vertical mixing of phytoplankton alters UV exposure and has significant effects on the integrated inhibition through the water column,,. Here we present a model of UV-influenced photosynthesis in the presence of vertical mixing, which we constrain with comprehensive measurements from the Weddell-Scotia Confluence during the austral spring of 1993. Our calculations of photosynthesis integrated through the water column (denoted PT) show that photosynthesis is strongly inhibited by near-surface UV radiation. This inhibition can be either enhanced or decreased by vertical mixing, depending on the depth of the mixed layer. Predicted inhibition is most severe when mixing is rapid, extending to the lower part of the photic zone. Our analysis reveals that an abrupt 50% reduction in stratospheric ozone could, in the worst case, lower PT by as much as 8.5%. However, stronger influences on inhibition can come from realistic changes in vertical mixing (maximum effect on PT of about ±37%), measured differences in the sensitivity of phytoplankton to UV radiation (±46%) and cloudiness (±15%).

Photosynthetic characteristics and estimated growth rates indicate grazing is the proximate control of primary production in the equatorial Pacific

Macronutrients persist in the surface layer of the equatorial Pacific Ocean because the production of phytoplankton is limited; the nature of this limitation has yet to be resolved. Measurements of photosynthesis as a function of irradiance (P-I) provide information on the control of primary productivity, a question of great biogeochemical importance. Accordingly, P-I was measured in the equatorial Pacific along 150°W, during February-March 1988. Diel variability of P-I showed a pattern consistent with nocturnal vertical mixing in the upper 20 m followed by diurnal stratification, causing photoinhibition near the surface at midday. Otherwise, the distribution of photosynthetic parameters with depth and the stability of P-I during simulated in situ incubations over 2 days demonstrated that photoadaptation was nearly complete at the time of sampling: photoadaptation had not been effectively countered by upwelling or vertical mixing. Measurements of P-I and chlorophyll during manipulations of trace elements showed that simple precautions to minimize contamination were sufficient to obtain valid rate measurements and that the specific growth rates of phytoplankton were fairly high in situ, a minimum of 0.6 d−1. Diel variability of beam attenuation also indicated high specific growth rates of phytoplankton and a strong coupling of production with grazing. It appears that grazing is the proximate control on the standing crop of phytoplankton. Nonetheless, the supply of a trace nutrient such as iron might ultimately regulate productivity by influencing species composition and food-web structure.

Inhibition of photosynthesis by ultraviolet radiation as a function of dose and dosage rate : results for a marine diatom

The effects of ultraviolet radiation on phytoplankton are usually described as a function of dose (J m−2, weighted appropriately). Experiments conducted in 1988 and 1989 on a marine diatom,Thalassiosira pseudonana (Clone 3H), demonstrate that during lightlimited photosynthesis in visible radiation, the inhibition of photosynthesis by supplemental ultraviolet radiation (principally UV-B: 280 to 320 nm) is a function of irradiance (W m−2) as well as of dose: for equal doses of UV-B, a relatively short exposure to high UV-B irradiance is more damaging to photosynthesis than a longer exposure to lower irradiance. In fact, photoinhibition by UV-B is well described as a monotonic, nonlinear function of irradiance for time scales of 0.5 to 4 h. A nitrate-limited culture was about nine times more sensitive to UV-B than was a nutrient-replete culture, but the kinetics of photoinhibition were similar. These results have some bearing on efforts to describe the effects of ultraviolet radiation on marine primary productivity. Action spectra of photoinhibition by UV can be constructed, but they should only be used to describe photoinhibition for specified time scales. Vertical profiles of relative photoinhibition must be interpreted cautiously because photoinhibition by UV-B is likely to be a function of incubation time and results must therefore be interpreted in the context of vertical mixing.

Ultraviolet radiation, ozone depletion, and marine photosynthesis.

Concerns about stratospheric ozone depletion have stimulated interest in the effects of UVB radiation (280–320 nm) on marine phytoplankton. Research has shown that phytoplankton photosynthesis can be severely inhibited by surface irradiance and that much of the effect is due to UV radiation. Quantitative generalization of these results requires a biological weighting function (BWF) to quantify UV exposure appropriately. Different methods have been employed to infer the general shape of the BWF for photoinhibition in natural phytoplankton, and recently, detailed BWFs have been determined for phytoplankton cultures and natural samples. Results show that although UVB photons are more damaging than UVA (320–400 nm), the greater fluxes of UVA in the ocean cause more UV inhibition. Models can be used to analyze the sensitivity of water column productivity to UVB and ozone depletion. Assumptions about linearity and time-dependence strongly influence the extrapolation of results. Laboratory measurements suggest that UV inhibition can reach a steady-state consistent with a balance between damage and recovery processes, leading to a non-linear relationship between weighted fluence rate and inhibition. More testing for natural phytoplankton is required, however. The relationship between photoinhibition of photosynthesis and decreases in growth rate is poorly understood, so long-term effects of ozone depletion are hard to predict. However, the wide variety of sensitivities between species suggests that some changes in species composition are likely. Predicted effects of ozone depletion on marine photosynthesis cannot be equated to changes in carbon flux between the atmosphere and ocean. Nonetheless, properly designed studies on the effects of UVB can help identify which physiological and ecological processes are most likely to dominate the responses of marine ecosystems to ozone depletion.

Carbon uptake in a marine diatom during acute exposure to ultraviolet B radiation: relative importance of damage and repair

Experiments on a marine diatom, Thalassiosira pseudonana (Hustedt) clone 3H, demonstrate that under moderate photon flux densities (75 μmol quanta·m−2·s−1) of visible light the inhibition of photosynthesis by supplemental ultraviolet (UV) radiation (UV‐B: 280–320 nm) is well described as a hyperbolic function of UV‐B irradiance for time scales of 0.5–4 h. Results are consistent with predictions of a recently developed model of photosynthesis under the influence of UV and visible irradiance. Although net destruction of chlorophyll occurs during a 4‐h exposure to UV‐B, and the effect is a function of exposure, the principal effect of UV‐B is a decrease in chlorophyll‐specific photosynthetic rate. The dependence of photoinhibition on dosage rate, rather than cumulative dose, and the hyperbolic shape of the relationship are consistent with net photoinhibition being an equilibrium between damage and repair. The ratio of damage to repair is estimated by a mathematical analysis of the inhibition of photosynthesis during exposures to UV‐B. A nitrate‐limited culture was much more sensitive to UV‐B than were the nutrient‐replete cultures, but the kinetics of photoinhibition were similar. The analysis suggests that the nutrient‐limited culture was more sensitive than the nutrient‐replete cultures because repair or turnover of critical proteins associated with photosynthesis is inhibited. An inhibitor of chloroplast protein synthesis was used to suppress repair processes. Photoinhibition by UV‐B was enhanced, and inhibition was a function of cumulative dose, as would be expected if damage were not countered by repair. The fundamental importance of repair processes should be considered in the design of field experiments and models of UV‐B effects in the environment, especially in the context of vertical mixing. Repair processes must also be considered whenever biological weighting functions are developed.

On models of growth and photosynthesis in phytoplankton

Abstract A model of the growth of a marine diatom ( Sakshaug et al. , 1989, Limnology and Oceanography , 34 , 198–205) is examined. One equation describes the relationship between chemical composition and growth rate as a function of irradiance and daylength. It is valid for both nutrient-limited and nutrient-saturated growth. The model equation is rearranged to describe photosynthesis normalized to chlorophyll. The new equation is essentially the same as several other models. Its mechanistic basis is the variation of quantum yield as a function of the number of excess photons absorbed by a photosynthetic unit during the time it takes to process one photon. The mechanistic interpretation of the model could be deceptive because the general equation describes a composite response and does not represent any one growth state. Nonetheless, the reformulated equation is important because it shows that at a given temperature, the adapted rate of photosynthesis normalized to chlorophyll is a function solely of growth irradiance. The equation can be used to describe primary production in the sea as a function of insolation and chlorophyll in the water column. For comparison, the model of Ryther and Yentsch (1957, Limnology and Oceanography , 2 , 281–286) is modified and found to fit obsercations as well or better than other formulations. Some date sets are not at all consistent with general models, however. Discrepancies may be due to taxonomic differences, temperature and vertical structure of phytoplankton biomass. It is also possible that changes in the photoynthesis-irradiance relationship associated with unbalanced growth are extremely important in determining primary production in perturbed environments.

Nutrient Limitation of Marine Photosynthesis

Guided by insightful presentations at the previous Brookhaven Symposium (Bannister and Laws, 1980; Eppley, 1980; Goldman, 1980) we address here three questions that have challenged oceanographers for decades: 1) Can photosynthetic performance be used to diagnose the nutritional status of phytoplankton? 2) Should nutrients be incorporated into models of oceanic photosynthesis as a function of chlorophyll and light? and 3) How might we assess nutrient limitation of the specific growth rates or standing crop of phytoplankton in the ocean? We find that ambiguities thwart attempts to formulate robust generalizations. Accordingly, when it comes to nutrient limitation of marine photosynthesis, a good paradigm is hard to find.