Patrick J. Neale

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%).

Ultraviolet sunscreens in Gymnodinium sanguineum (Dinophyceae): mycosporine-like amino acids protect against inhibition of photosynthesis

Marine phytoplankton are sensitive to inhibition of photosynthesis by solar ultraviolet (UV) radiation, although sensitivity varies, depending on the growth environment. A mechanism suggested to increase resistance to UV inhibition is the accumulation of UV‐absorbing compounds, such as the mycosporine‐like amino acids (MAAs) found in many marine organisms. However, the effectiveness of these compounds as direct optical screens in microorganisms has remained unclear. The red‐tide dinoflagellate Gymnodinium sanguineum Hirasaka accumulates about 14‐fold more MAAs (per unit of chlorophyll) in high (76 W·m−2) than in low (15 W·m−2) growth irradiance. Biological weighting functions were estimated for UV inhibition of photosynthesis and showed that the high‐light‐grown cultures have lower sensitivity to UV radiation at wavelengths strongly absorbed by the MAAs. The time course of photosynthesis during exposure to UV radiation was measured using pulsed amplitude modulated (PAM) fluorometry and displayed a steady‐state level after 15 min of exposure, indicating active repair of damage to the photosynthetic apparatus. Repair was blocked in the presence of the antibiotic streptomycin, yet high‐light G. sanguineum remained less sensitive to UV radiation than did low‐light cultures. These experiments show that MAAs act as spectrally specific UV sunscreens in phytoplankton.

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.

BENEFICIAL AND DETRIMENTAL EFFECTS OF UV ON AQUATIC ORGANISMS: IMPLICATIONS OF SPECTRAL VARIATION

Solar ultraviolet radiation (UVR) may have beneficial as well as detrimental effects on living systems. For example, UV-B radiation (280-320 nm) is generally dam- aging, while UV-A radiation (320-400 nm) may cause damage or stimulate beneficial photorepair of UV-B damage. The nature of both direct and indirect effects of UVR in nature depends on both the photon flux density and the spectral composition of the radiation incident on aquatic organisms across environmental UVR gradients in space (depth, trans- parency, elevation) and time (diel, seasonal, interannual). Here we use the common and widespread freshwater cladoceran Daphnia pulicaria as a model organism to demonstrate the potential importance of these wavelength-specific effects of UVR to the ecology of aquatic organisms. UVR-exposure experiments are used to manipulate both natural solar and artificial UVR sources to examine the beneficial as well as detrimental effects of different wavelengths of UVR. Changes in the spectral composition of solar radiation are also examined along several natural environmental gradients including diel gradients, depth gradients, and dissolved organic carbon (DOC) gradients. The implications of variation in the spectral composition of UVR for aquatic organisms are discussed. The first biological weighting function (BWF) for a freshwater cladoceran is presented here. It demonstrates that the shortest UV-B wavelengths in sunlight are potentially the most damaging per photon. However, due to the greater photon flux density of longer wavelength UVR in sunlight, the net potential damage to Daphnia in nature is greatest for the longer wavelength UV-B and shorter wavelength UV-A radiation in the 305-322 nm range. Overall the contribution of UV-B to the total mortality response of Daphnia exposed to full-spectrum solar radiation for 7 h on a sunny summer day is 64% while UV-A con- tributes 36%. The BWF for Daphnia is used with the transmission spectrum for Mylar D to demonstrate that Mylar D cuts out only about half of the damaging UVR in sunlight. Following exposure to damaging UV-B, Daphnia exhibits a dramatic increase in survival in the presence of longer wavelength UV-A and visible radiation due to the stimulation of photoenzymatic repair. We present data that demonstrate the importance of both atmospheric ozone and DOC in creating strong environmental gradients in the intensity (irradiance) and spectral composition of solar UVR in nature. The light-absorbing component of DOC, chromophoric dissolved organic matter (CDOM), is particularly important in creating depth refugia from damaging UV-B in freshwater ecosystems. CDOM may also cause intense variations in the ratio of potentially beneficial UV-A to detrimental UV-B radiation to which aquatic organisms are exposed. In addition to changes in atmospheric ozone, future changes in CDOM related to climate change or other environmental disturbances may substantially alter the underwater exposure of a variety of aquatic organisms to different wavelengths of solar UVR.

Photobleaching of dissolved organic material from a tidal marsh-estuarine system of the Chesapeake Bay.

Wetlands and tidal marshes in the Rhode River estuary of the Chesapeake Bay act as important sources of dissolved organic carbon and strongly absorbing dissolved organic matter (DOM) for adjacent estuarine waters. The effects of solar exposure on the photochemical degradation of colored DOM (CDOM) were examined for material derived from different sources (estuarine and freshwater parts of the Rhode River, sub‐watershed stream, marshes) in this estuarine ecosystem. Consistent with changes in fluorescence emission, absorption loss upon exposure to different portions of the solar spectrum (i.e. different long‐pass cut‐off filters) occurred across the entire spectrum but the wavelength of maximum photobleaching decreased as the cut‐off wavelength of the filter decreased. Our results illustrate that solar exposure can cause either an increase or a decrease in the CDOM absorption spectral slope, SCDOM, depending on the spectral quality of irradiation and, thus, on the parameters (e.g. atmospheric composition, concentration of UV‐absorbing water constituents) that affect the spectral characteristics of the light to which CDOM is exposed. We derived a simple spectral model for describing the effects of solar exposure on CDOM optical quality. The model accurately, and consistently, predicted the observed dependence of CDOM photobleaching on the spectral quality of solar exposure.

Partitioning spectral absorption in case 2 waters: discrimination of dissolved and particulate components

A series of three mathematical procedures is derived to discriminate the light absorption by phytoplankton, colored dissolved organic matter, and nonpigmented particulates in waters in which absorption is dominated by factors other than phytoplankton (i.e., case 2 waters). The procedures utilize normalized absorption cross-sectional spectra of the absorption components and matrix inversion to solve for the coefficients that scale the normalized spectra. The procedures differ in the amount of ancillary measurements incorporated to reduce the variability of the estimates. The procedure that incorporates no ancillary information is expected to be unbiased only over long time periods. Application of the procedures to a 15-day time series of continuously monitored data from the Rhode River, Maryland, revealed the presence of large (approximately twofold) changes in absorption at 440 nm over periods of a few hours. Hourly sampling over a 24-h period confirmed that the changes in measured optical coefficients corresponded to changes in water quality. Errors in estimates of absorption components were of a magnitude consistent with those observed in development of the procedures and confirmed the progressive improvement achieved by incorporation of additional information. Over the time period observed, changes in optical properties appeared to be driven by advective processes.

SHORT-TERM AND LONG-TERM EFFECTS OF TEMPERATURE ON PHOTOSYNTHESIS IN THE DIATOM THALASSIOSIRA PSEUDONANA UNDER UVR EXPOSURES1

Temperature is expected to modify the effects of ultraviolet radiation (UVR) on photosynthesis by affecting the rate of repair. We studied the effect of short‐term (1 h) and long‐term (days) acclimation to temperature on UVR photoinhibition in the diatom Thalassiosira pseudonana Hasle et Heimdal. Photosynthesis was measured during 1 h exposures to varying irradiances of PAR and UVR + PAR at 15, 20, and 25°C, the latter corresponding to the upper temperature limit for optimal growth in T. pseudonana. The exposures allowed the estimation of photosynthesis–irradiance (P–E) curves and biological weighting functions (BWFs) for photoinhibition. For the growth conditions used, temperature did not affect photosynthesis under PAR. However, photoinhibition by UVR was highly affected by temperature. For cultures preacclimated to 20°C, the extent of UVR photoinhibition increased with decreasing temperature, from 63% inhibition of PAR‐only photosynthesis at 25°C to 71% at 20°C and 85% at 15°C. These effects were slightly modified after several days of acclimation: UVR photoinhibition increased from 63% to 75% at 25°C and decreased from 85% to 80% at 15°C. Time courses of photochemical efficiency (ΦPSII) under UVR + PAR were also fitted to a model of UVR photoinhibition, allowing the estimation of the rates of damage (k) and repair (r). The r/k values obtained for each temperature treatment verified the responses observed with the BWF (R2 = 0.94). The results demonstrated the relevance of temperature in determining primary productivity under UVR exposures. However, the results suggested that temperature and UVR interact mainly over short (hours) rather than long (days) timescales.

Interaction of UV Radiation and Inorganic Carbon Supply in the Inhibition of Photosynthesis: Spectral and Temporal Responses of Two Marine Picoplankters¶

The effect of ultraviolet radiation (UVR) on inhibition of photosynthesis was studied in two species of marine picoplankton with different carbon concentration mechanisms: Nannochloropsis gaditana Lubián possesses a bicarbonate uptake system and Nannochloris atomus Butcher a CO2 active transport system. Biological weighting functions (BWFs) for inhibition of photosynthesis by UVR and photosynthesis vs irradiance (PI) curves for photosynthetically active radiation (PAR) were estimated for both species grown with an enriched CO2 supply (high dissolved inorganic carbon [DIC]: 1% CO2 in air) and in atmospheric CO2 levels (low DIC: 0.03% CO2). The response to UVR and PAR exposures was different in each species depending on the DIC treatment. Under PAR exposure, rates of maximum photosynthesis were similar between treatments in N. gaditana. However, the cultures growing in high DIC had lower sensitivity to UVR than the low DIC cultures. In contrast, N. atomus had higher rates of photosynthesis under PAR exposure with high DIC, but the BWFs were not significantly different between treatments. The results suggest that one or more processes in N. gaditana associated with HCO3− transport are target(s) for UV photodamage because there was relatively less UV inhibition of the high DIC‐grown cultures in which inorganic carbon fixation is supplied by passive CO2 diffusion. Time courses of photochemical efficiency in PAR, during UV exposure and during subsequent recovery in PAR, were determined using a pulse amplitude modulated fluorometer. The results were consistent with the BWFs. In all time courses, a steady state was obtained after an initial decrease, consistent with a dynamic balance between damage and repair as found for other phytoplankton. However, the relationship of response to exposure showed a steep decline in activity that is consistent with a constant rate of repair. A novel feature of a model developed from a constant repair rate is an explicit threshold for photosynthetic response to UV.

Impacts of Solar UVR on Aquatic Microorganisms

C. R. BOOTH AND J. H. MORROW, Biospherical Instruments, San Dlego, CA, USA THOMAS P. COOHILL, Ultraviolet Consultants, Bowling Green, KY, USA JOHN J. CULLEN, Dalhousie University, Halifax, Nova Scotla, Canada JOHN E. FREDERICK, University of Chicago, IL, USA DONAT-P. HADER, University of Erlangen-Nurnberg, Germany OSMUND HOLM-HANSEN, Scripps Institution of Oceanography, La Jolla, CA, USA WADE H. JEFFREY, University of West Florida, Pensacola, FL, USA DAVID L. MITCHELL, M.D. Anderson Cancer Center, Smithvllle, TX, USA PATRICK J. NEALE, Smithsonian Environmental Research Center, Edgewater, MD, USA IGOR SOBOLEV, Chemical and Polymer Technology, Inc., Orinda, CAI USA JAN VAN DER LEUN, University of Utrecht, The Netherlands ROBERT C. WORREST, CIESIN, Washington, DC, USA

The 1996 North American Interagency Intercomparison of Ultraviolet Monitoring Spectroradiometers

Concern over stratospheric ozone depletion has prompted several government agencies in North America to establish networks of spectroradiometers for monitoring solar ultraviolet irradiance at the surface of the Earth. To assess the ability of spectroradiometers to accurately measure solar ultraviolet irradiance, and to compare the results between instruments of different monitoring networks, the first North American Intercomparison of Ultraviolet Monitoring Spectroradiometers was held September 19–29, 1994 at Table Mountain outside Boulder, Colorado, USA. This Intercomparison was coordinated by the National Institute of Standards and Technology and the National Oceanic and Atmospheric Administration (NOAA). Participating agencies were the Environmental Protection Agency, National Science Foundation, Smithsonian Environmental Research Center, and Atmospheric Environment Service, Canada. Instruments were characterized for wavelength accuracy, bandwidth, stray-light rejection, and spectral irradiance responsivity, the latter with a NIST standard lamp calibrated to operate in the horizontal position. The spectral irradiance responsivity was determined once indoors and twice outdoors, and demonstrated that, while the responsivities changed upon moving the instruments, they were relatively stable when the instruments remained outdoors. Synchronized spectral scans of the solar irradiance were performed over several days. Using the spectral irradiance responsivities determined with the NIST standard lamp, and a simple convolution technique to account for the different bandwidths of the instruments, the measured solar irradiances agreed within 5 %.