Effects of solar UV radiation on photosynthetic performance of the diatom Skeletonema costatum grown under nitrate limited condition
Effects of solar UV radiation on photosynthetic performance of the diatom Skeletonema costatum grown under nitrate limited condition
ALGAE. 2014. Mar, 29(1): 27-34
Copyright © 2014, The Korean Society of Phycology
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
  • Received : September 17, 2013
  • Accepted : February 24, 2014
  • Published : March 15, 2014
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About the Authors
Gang, Li
Key Laboratory of Tropical Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, CAS, Guangzhou, Guangdong 510301, China
Kunshan, Gao
State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, Fujian 361005, China

Availability of nutrients is known to influence marine primary production; and it is of general interest to see how nutrient limitation mediates phytoplankton responses to solar ultraviolet radiation (UVR, 280-400 nm). The red tide diatom Skeletonema costatum was cultured under nitrate (N)-limited and N-replete conditions and exposed to different solar irradiation treatments with or without UV-A (315-400 nm) and UV-B (280-315 nm) radiation. Its photochemical quantum yield decreased by 13.6% in N-limited cells as compared to that in N-replete ones under photosynthetically active radiation (PAR)-alone treatment, and the presence of UV-A or UV-B decreased the yield further by 2.8 and 3.1%, respectively. The non-photochemical quenching (NPQ), when the cells were exposed to stressful light condition, was higher in N-limited than in N-replete grown cells by 180% under PAR alone, by 204% under PAR + UV-A and by 76% under PAR + UV-A + UV-B treatments. Our results indicate that the N limitation exacerbates the UVR effects on the S. costatum photosynthetic performance and stimulate its NPQ.
Solar ultraviolet radiation (UVR, 280-400 nm) is a crucial environmental factor to influence marine primary productivity and consequently the marine ecosystems ( Häder 2011 ). UVR can decrease phytoplankton growth and photosynthesis as well as nutrients uptake ( Sobrino et al. 2004 , Gao et al. 2007 , Korbee et al. 2010 ), harm DNA or protein molecules ( Roy 2000 , Wei et al. 2004 ) and even lead to cell death ( Agustí and Llabrés 2007 ), and therefore, can alter community structures ( Marcoval et al. 2008 , Beardall et al. 2009 ). On the other hand, longer UV-A wavebands (320-400 nm) are known to function in photorepairing the UV-B induced damages to DNA ( Buma et al. 2003 ), trigger chlorophyll fluorescence ( Halldal 1967 ) and energize the photosynthesis of coastal phytoplankton assemblages ( Helbling et al. 2003 , Mengelt and Prézelin 2005 , Gao et al. 2007 , Li and Gao 2013 ).
Availability of nutrients is known to affect the photosynthetic responses of algae to UVR ( Beardall et al. 2001 , 2009 ). Nutrient limitation reduced the sensitivity of the diatom Chaetoceros brevis to photo-induced viability loss ( van de Poll et al. 2005 ). A greater UV-A induced reduction on the dimethysulfide production of the diatom Thalassiosira oceanica was observed under nitrate-limited condition ( Harada et al. 2009 ), as well as the reduced contents of saturated fatty acids in the diatoms Phaeodactylum tricornutum and Chaetoceros muelleri ( Liang et al. 2006 ). The increased UVR sensitivity of the dinoflagellates Gymnodinium sanguineum and Gymnodinium cf. instriatum was also found under nitrate-limited conditions ( Litchman et al. 2002 ), as well as the increased tolerance of the dinoflagellates Heterocapsa sp. to UVR stress under nitrate replete conditions ( Korbee et al. 2010 ). However, the knowledge on the combined effects of UVR and nitrate limitation has been scarcely documented, especially on the photophysiology of diatoms.
The diatom Skeletonema costatum is distributed abundantly and cosmopolitanly in the word’s oceans ( Kooistra et al. 2008 ) and is well known as a typical species of harmful algal blooms ( Wang et al. 2008 ). Long-term UV-B exposure increased its contents of carotenoids and UV-absorbing compounds ( Wu et al. 2009 ); short-term UV-B exposure decreased its protein expression ( Wei et al. 2004 ), but increased its competitive ability as compared to the dinoflagellate Alexandrium tamarense and thus broke their competition balance in growth ( Zhang et al. 2007 ). Nevertheless, this diatom showed a rapid acclimation to solar UVR, even after having been maintained indoor for decades under low UVR-free light condition ( Guan and Gao 2008 ). Since S. costatum is found in waters of varied nitrate concentrations of e.g., from 0 to 12.3 μmol L -1 in the South China Sea ( Ning et al. 2004 ), and little is known about the combined effects of UVR and nitrate limitation on its photochemical performance. Therefore, the aim of this study was to examine the effects of solar UVR on the photosynthetic performance of the diatom S. costatum while growing under nitrate-limited and replete conditions.
- Organism and culture
The diatom Skeletonema costatum (Greville) Cleve (strain 2042) was obtained from the algal species conversation center of Xiamen University and was grown in sterilized artificial seawater at 20℃ and 350 μmol photons m -2 s ‑1 (~75 W m -2 ) photosynthetically active radiation (PAR) irradiance (12 : 12 LD cycle). Two levels of nitrate were set: 830 μmol L ‑1 nitrate of the standard f/2 medium (N-replete, HN) and 0.83 μmol L -1 (N-limited, LN) of nitrate, the same f/2 medium with the nitrate reduced to be equivalent to the surface level of the South China Sea ( Li et al. 2012 ). The cells at mid-exponential phase ( Fig. 1 ) were diluted to 30,000-40,000 cells mL -1 with fresh medium (LN or HN) in the evening before the outdoor experiments started next morning.
PPT Slide
Lager Image
Cell concentrations of Skeletonema costatum grown in N-replete (HN) or N-starved (LN) conditions during the cultured period. The arrow indicates that the culture was taken and diluted to 3-4 × 104 cell mL-1 in the evening before the outdoor experiments next morning. Vertical bars represent the standard deviations (n = 3).
- Irradiance treatments and measurements
In the early morning (7:00 am) of August 4 and 8 of 2010, both the diluted cultures (LN or HN) were dispensed into 500 mL UV-transparent quartz tubes that were incubated in a flow-through water tank to control temperature (20 ± 0.5℃) and exposed to 3 irradiation treatments (triplicate tubes for each nutrient level): a) uncovered quartz tubes, the cells received full sunlight (PAR + UV-A +UV-B [PAB], irradiances above 280 nm); b) quartz tubes wrapped in Folex 320 (Montagefolie, No. 10155099; Folex, Dreieich, Germany), the cells received PAR + UV-A (PA, irradiances above 320 nm); and c) quartz tubes covered with Ultraphan film 395 (UV Opak; Digefra, Munich, Germany), the cells received PAR alone (P, irradiances above 395 nm). The transmission spectra of the tubes and filters are available elsewhere ( Sobrino et al. 2004 ). A radiometer (Eldonet XP; Real Time Computers Inc., Möhrendorf, Germany) was used to monitor the incident solar radiation; it measures every second of UV-B (280-315 nm), UV-A (315-400 nm), and PAR irradiance (400-700 nm) and records the minute-averaged values ( Häder et al. 1999 ). This device has been regularly calibrated with a certified calibration lamp (DH 2000; Oceanic Optics Inc., Dunedin, FL, USA). The PAR irradiance was converted from W m -2 to photon flux (μmol photons m -2 s -1 ) by multiplying by 4.60 according to Neale et al. (2001) .
- Photophysiological parameter measurements
During the incubations (7:00 am to 18:00 pm), 5 mL samples were taken every hour from each tube to determine the photosynthetic performance of S. costatum with a pulse amplitude modulated fluorometer (Xe-PAM; Walz, Effeltrich, Germany). Effective photochemical quantum yield (Y) was determined by measuring the instant maximal fluorescence ( F m ' ) and steady state fluorescence ( F t ) of light-adapted cells, and calculated according to Genty et al. (1990) as: Y = ( F m ' - F t ) / F m ' . The non-photochemical quenching (NPQ) was determined (van Kooten and Snel 1990 ) as NPQ = ( F m - F m ' ) / F m ' , where F m was the maximal fluorescence of dark-acclimated (overnight) cells obtained prior to the outdoor exposure. The saturating pulse was set at 4,800 μmol photons m -2 s -1 for 600 ms and the actinic light at 350 μmol photons m -2 s -1 (~75 W m -2 ) for the effective quantum yield measurement. We are aware the effects of solar UVR could be exaggerated by shifting the cells cultured indoor to the outdoor conditions, but it indeed happens in natural conditions such as after typhoon event ( Li et al. 2009 ) or after heavy cloud covers ( Gao et al. 2007 ) and so provides very useful information to accomplish this study’s objective.
- Data analyses
UV-A or UV-B induced inhibition of Y was calculated as:
  • UV-BInh= (YPA- YPAB) / YP× 100%;
  • UV-AInh= (YP- YPA) / YP× 100%
, where UV-B Inh and UV-A Inh indicate UV-B and UV-A induced inhibition; Y PAB , Y PA , and Y P indicate Y values of the cells under PAB, PA, and P treatments, respectively.
To determine the significant differences (p < 0.05) among three light treatments and between two nutrient treatments, paired-t test was used for the whole day’s comparisons and one way-ANOVA was used for the each time-point comparisons. Non-linear curve fit was used to obtain the relationships between Y (or NPQ) and PAR irradiance, whereas Kendall’s τ test was used to establish the correlations of Y and UV inhibition between the HN and LN treatments.
During a diurnal cycle of solar radiation ( Fig. 2A ), the effective quantum yield (Y) decreased with increasing solar radiation regardless of the radiation treatments with or without UVR, to a minimum value at noon, and then increased with decreasing solar radiation ( Fig. 2B ). The cells grown under nitrate (N)-limited condition had a relatively lower Y value than those under N-repletion e.g., 0.44 in the early morning, that decreased to a minimum of 0.29 at noon and almost completely recovered in the late afternoon ( Fig. 2B ). The diurnal changes of NPQ displayed an opposite pattern to Y ( Fig. 2C ), with the higher values in the presence of UVR than that in PAR alone (p < 0.01). In view of the NPQ ratios of HN to LN grown cells, higher NPQ were found in the LN-grown cells ( Fig. 1C ), indicating a higher heat dissipation. UVR significantly increased the NPQ (p < 0.05), by approximately 57% in LN and 30% in HN-grown cells at noon ( Fig. 2C ).
PPT Slide
Lager Image
(A) Representive incident solar photosynthetically active radiation (PAR, 400-700 nm), UV-A (315-400 nm), and UV-B (280-320 nm) irradiances in W m-2. (B) Diurnal variations in effective quantum yield (Y). (C) Non-photochemical quenching (NPQ) of Skeletonema costatum cells grown under nitrate (N)-limited condition (LN) and exposed to PAR + UV-A + UV-B (PAB, 280-700 nm), PAR + UV-A (PA, 320-700 nm), and PAR (P, 400-700 nm), and their ratios to that of the cells grown under N-replete condition (HN). Vertical bars represent the standard deviations (n = 3).
When PAR intensity increased over 1,500 μmol photons m -2 s -1 (326 W m -2 ), the Y values decreased by approximately 60% as compared to the initials in LN grown cells ( Fig. 3A & B ) with the presence of UV-A reducing the yield by 2.2-21% and addition of UV-B further decreasing it by 6.0-24%, the total inhibition caused by UVR being 12 to 30%. The NPQ value reached 0.89 in LN-grown cells as the PAR was over 1,500 μmol photons m -2 s -1 (326 W m -2 ), being elevated by 46 and 31% respectively by solar UV-A and UV-B. The N limitation enhanced the NPQ by 180% under PAR alone, by 204% under PA and by 76% under PAB, compared to that in N repletion ( Fig. 3C & D ). Moreover, a clear threshold of NPQ of LN-grown cells ( Fig. 3C & D ) occurred when the PAR irradiance was ~230 μmol photons m -2 s -1 (50 W m -2 ) ‒ one fourth of that in HN-grown cells, providing evidence that the lower light energy is needed to spike the NPQ under N-limited conditions.
PPT Slide
Lager Image
Effective quantum yield (Y) (A & B) and non-photochemical quenching (NPQ) (C & D) of Skeletonema costatum cells grown under N-limited (A & C) or N-replete (B & D) conditions and exposed to photosynthetically active radiation (PAR) + UV-A + UV-B (PAB, 280-700 nm), PAR + UVA (PA, 320-700 nm), and PAR (P, 400-700 nm) of overall two days experiments, as a function of PAR. Vertical and horizontal bars represent the standard deviations (n = 3).
Fig. 4 showed the relationships of the Y values, UV-A and UV-B caused inhibition between LN- and HN-grown cells. The LN-grown cells showed about 13% lower Y values than that of HN-grown cells ( Fig. 4A ), and 24.4 and 21.4% higher inhibition caused by UV-A and UV-B, respectively ( Fig. 4B & C ), indicating the N limitation exacerbated the UVR effects on the diatom photosynthetic performance.
PPT Slide
Lager Image
Effective quantum yield (A), UV-A induced (B), and UV-B induced (C) inhibition on Skeletonema costatum cells grown under N-limited condition (LN) versus that of the cells grown under N-replete condition (HN). The bold lines show significant relationships, with r2 of 0.93 for YP, 0.26 for UV-A and 0.47 for UV-B inhibition (p < 0.01), respectively. Vertical and horizontal bars represent the standard deviations (n = 3). rA = 0.92912, p < 0.0001; rB = 0.5074, p = 0.00219; rC = 0.68274, p < 0.0001.
Grown under nitrate limited condition, the diatom S. costatum exhibited lower effective quantum yields (Y) and higher NPQ, as well as higher sensitivity to UVR in contrast to that under N-replete condition. The PAR intensity that initiated the NPQ of N-limited grown cells was one fourth of that of N-replete grown ones. Light history would affect the photophysiological performances of phytoplankton when being shifted from the indoor- to outdoor-conditions, such as the S. costatum strain maintained in the laboratory for decades showed differential responses to UV compared to the strain isolated from coastal water ( Guan and Gao 2008 ), and the Thalassiosira pseudonana showed differential photoinactivations of photosystem II after acclimating to different light levels ( Li and Campbell 2013 ). In natural environments, the light acclimation from very low to very high levels with or without UVR also happens, such as that after typhoon event ( Li et al. 2009 ) or after heavy cloud covers for days or during a diel cycle ( Gao et al. 2007 ), which would cause the exaggerated photoinhibition of S. costatum by solar PAR or UVR ( Figs 2 & 3 ) although this diatom species could rapidly acclimate to the field light conditions ( Guan and Gao 2008 ).
While S. costatum showed similar diurnal patterns of both the yield and NPQ under sunlight to other phytoplankton species or communities (e.g., van de Poll et al. 2005 , Marcoval et al. 2008 ), nitrate limitation decreased its yield and increased its NPQ either in the presence or absence of solar UVR ( Figs 3 & 4 ). Higher availability of nitrogen usually leads to less inhibition by stressful light ( Litchman et al. 2002 , Korbee et al. 2010 , Loebl et al. 2010 ), since the repair of photodamage can be better achieved with more N-requiring enzymes and / or protein cofactors ( Roy 2000 , Beardall et al. 2001 ). Other enzymes such as peroxidase and catalase, that also need N, and can detoxify UVR-induced reactive oxygen species ( Lesser 1996 ) and might also be responsible for the smaller UVR effects under N replete conditions.
The threshold of light intensity that triggers the NPQ in LN-grown cells was one-fourth of that of HN-grown cells ( Fig. 3C & D ). The NPQ, an important strategy for phytoplankton to rapidly (seconds to minutes) regulate photochemistry, is one of the first lines of defense that diatoms use to attenuate the photoinhibitory oxidative damage caused by light stress ( Lavaud et al. 2007 , Korbee et al. 2010 ). The LN-grown cells had significantly (p < 0.01) higher NPQ and lower light to trigger NPQ, comparable to the HN-grown ones ( Fig. 3C & D ); they could have redissipated the excessive energy more effectively under stressful light condition, thus protecting the cells from photoinhibition and maintaining their photosynthetic activity. The field measurements of NPQ by Kashino et al. (2002) and Fujiki et al. (2003) also indicated that the NPQ process is of importance to maintain the photosynthetic activity of phytoplankton. On the other hand, the substances, that need N for their synthesis, e.g., UV-screening compounds like mycosporine-like amino acids were recorded to increase with increasing nitrogen levels ( Litchman et al. 2002 , Korbee et al. 2010 , Barufi et al. 2011 ) and might also attribute to the higher UVR sensitivity in LN- than in HN-grown cells.
The diatom grown under N-limited condition exhibited higher sensitivity to UVR than that grown under N-replete condition, based on the changes in the photochemical quantum yield and NPQ, which indicates that the N limitation exacerbates the effects of UVR on its photosynthetic performance and stimulate its NPQ. Presently, the increased global temperature has directly and indirectly altered the natural conditions of aquatic bodies, e.g., increasing the stratification of surface ocean and making it more oligotrophic ( Boyd et al. 2010 ). Taking into account the worldwide oligotrophic oceans wherein the growth of phytoplankton is limited and the limitation could be exacerbated by the decreased nutrient levels within the upper mixed layer; the negative effects caused by solar UVR would be exacerbated, making phytoplankton cells more sensitive to ambient UVR stress.
We would like to thank the comments of the two anonymous reviewers that helped to improve this manuscript. This study was supported by the National Natural Science Foundation (40930846, 41120164007, 41206132), Program for Changjiang Scholars and Innovative Research Team (IRT_13R51), China-Japan collaboration project from MOST (S2012GR0290), Special Research Fund for the National Non-profit Institutes (2008M15) and MEL Visiting Fellowship Program (MELRS1006). The authors are grateful to Ying Zheng, Guang Gao, Guangyan Ni, Kai Xu, Guiyan Yang and Peng Jin for their experimental assistance.
Agustí S. , Llabrés M. 2007 Solar radiation-induced mortality of marine pico-phytoplankton in the oligotrophic ocean Photochem. Photobiol. 83 793 - 801
Barufi J. B. , Korbee N. , Oliveira M. C. , Figueroa F. L. 2011 Effects of N supply on the accumulation of photosynthetic pigments and photoprotectors in Gracilaria tenuistipitata (Rhodophyta) cultured under UV radiation J. Appl. Phycol. 23 457 - 466
Beardall J. , Sobrino C. , Stojkovic S. 2009 Interactions between the impacts of ultraviolet radiation, elevated CO2, and nutrient limitation on marine primary producers Photochem. Photobiol. Sci. 8 1257 - 1265
Beardall J. , Young E. , Roberts S. 2001 Approaches for determining phytoplankton nutrient limitation Aquat. Sci. 63 44 - 69
Boyd P. W. , Strzepek R. , Fu F. , Hutchins D. A. 2010 Environmental control of open-ocean phytoplankton groups: now and in the future Limnol. Oceanogr. 55 1353 - 1376
Buma A. G. J. , Boelen P. , Jeffrey W. H. , Helbling E. W. , Zagarese H. 2003 UV Effects in Aquatic Organisms and Ecosystems The Royal Society of Chemistry Cambridge UVR-induced DNA damage in aquatic organisms 291 - 327
Fujiki T. , Toda T. , Kikuchi T. , Taguchi S. 2003 Photoprotective response of xanthophyll pigments during phytoplankton blooms in Sagami Bay, Japan J. Plankton Res 25 317 - 322
Gao K. , Li G. , Helbling E. W. , Villafañe V. E. 2007 Variability of UVR effects on photosynthesis of summer phytoplankton assemblages from a tropical coastal area of the South China Sea Photochem. Photobiol. 83 802 - 809
Gao K. , Wu Y. , Li G. , Wu H. , Villafañe V. E. , Helbling E. W. 2007 Solar UV radiation drives CO2fixation in marine phytoplankton: a double-edged sword Plant Physiol. 144 54 - 59
Genty B. , Briantais J. , Baker N. R. 1990 Relative quantum efficiencies of the two photosystems of leaves in photorespiratory and non-photorespiratory conditions Plant Physiol. Biochem 28 1 - 10
Guan W. , Gao K. 2008 Light histories influence the impacts of solar ultraviolet radiation on photosynthesis and growth in a marine diatom, Skeletonema costatum J. Photochem. Photobiol. B Biol. 91 151 - 156
Häder D. -P. 2011 Does enhanced solar UV-B radiation affect marine primary producers in their natural habitats? Photochem. Photobiol. 87 263 - 266
Häder D. -P. , Lebert M. , Marangoni R. , Colombetti G. 1999 ELDONET- European Light Dosimeter Network hardware and software J. Photochem. Photobiol. B Biol. 52 51 - 58
Halldal P. 1967 Ultraviolet action spectra in algology: a review Photochem. Photobiol. 6 445 - 460
Harada H. , Vila-Costa M. , Cebrian J. , Kiene R. P. 2009 Effects of UV radiation and nitrate limitation on the production of biogenic sulfur compounds by marine phytoplankton Aquat. Bot. 90 37 - 42
Helbling E. W. , Gao K. , Goncalves R. J. , Wu H. , Villafañe V. E. 2003 Utilization of solar UV radiation by coastal phytoplankton assemblages off SE China when exposed to fast mixing Mar. Ecol. Prog. Ser. 259 59 - 66
Kashino Y. , Kudoh S. , Hayashi Y. , Suzuki Y. , Odate T. , Hirawake T. , Satoh K. , Fukuchi M. 2002 Strategies of phytoplankton to perform effective photosynthesis in the North Water Deep-Sea Res 49 5049 - 5061
Kooistra W. H. C. F. , Sarno D. , Balzano S. , Gu H. , Andersen R. A. , Zingone A. 2008 Global diversity and biogeography of Skeletonema species (Bacillariophyta) Protist 159 177 - 193
Korbee N. , Mata M. T. , Figueroa F. L. 2010 Photoprotection mechanisms against ultraviolet radiation in Heterocapsa sp. (Dinophyceae) are influenced by nitrogen availability: mycosporine-like amino acids vs. xanthophyll cycle Limnol. Oceanogr 55 899 - 908
Lavaud J. , Strzepek R. F. , Kroth P. G. 2007 Photoprotection capacity differs among diatoms: possible consequences on the spatial distribution of diatoms related to fluctuations in the underwater light climate Limnol. Oceanogr. 52 1188 - 1194
Lesser M. P. 1996 Elevated temperatures and ultraviolet radiation cause oxidative stress and inhibit photosynthesis in symbiotic dinoflagellates Limnol. Oceanogr. 41 271 - 283
Li G. , Campbell D. A. 2013 Rising CO2interacts with growth light and growth rate to alter photosystem II photoinactivation of the coastal diatom Thalassiosira pseudonana PLoS One 8 e55562 -
Li G. , Gao K. 2013 Cell size-dependent effects of solar UV radiation on primary production in coastal waters of the South China Sea Estuar. Coast 36 728 - 736
Li G. , Huang L. , Liu H. , Ke Z. , Lin Q. , Ni G. , Yin J. , Li K. , Song X. , Shen P. , Tan Y. 2012 Latitudinal variability (6ºS-20ºN) of early-summer phytoplankton species compositions and size-fractioned productivity from the Java Sea to South China Sea Mar. Biol. Res. 8 163 - 171
Li G. , Wu Y. , Gao K. 2009 Effects of typhoon Kaemi on coastal phytoplankton assemblages in the South China Sea, with special reference to the effects of solar UV radiation. J. Geophys. Res. 114 G04029 -
Liang Y. , Beardall J. , Heraud P. 2006 Effects of nitrogen source and UV radiation on the growth, chlorophyll fluorescence and fatty acid composition of Phaeodactylum tricornutum and Chaetoceros muelleri (Bacillariophyceae) J. Photochem. Photobiol. B Biol. 82 161 - 172
Litchman E. , Neale P. J. , Banaszak A. T. 2002 Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: photoprotection and repair Limnol. Oceanogr. 47 86 - 94
Loebl M. , Cockshutt A. M. , Campbell D. A. , Finkel Z. V. 2010 Physiological basis for high resistance to photoinhibition under nitrogen depletion in Emiliania huxleyi Limnol. Oceanogr. 55 2150 - 2160
Marcoval M. A. , Villafañe V. E. , Helbling E. W. 2008 Combined effects of solar ultraviolet radiation and nutrients addition on growth, biomass and taxonomic composition of coastal marine phytoplankton communities of Patagonia J. Photochem. Photobiol. B Biol. 91 157 - 166
Mengelt C. , Prézelin B. B. 2005 UVA enhancement of carbon fixation and resilience to UV inhibition in the genus Pseudo-nitzschia may provide a competitive advantage in high UV surface waters Mar. Ecol. Prog. Ser. 301 81 - 93
Neale P. J. , Bossard P. , Huot Y. , Sommaruga R. 2001 Incident and in situ irradiance in Lakes Cadagno and Lucerne: a comparison of methods and models Aquat. Sci. 63 250 - 264
Ning X. , Chai F. , Xue H. , Cai Y. , Liu C. , Shi J. 2004 Physical- biological oceanographic coupling influencing phytoplankton and primary production in the South China Sea J. Geophys. Res. 109 C10005 -
Roy S. , de Mora S. J. , Demers S. , Vemet M. 2000 The Effects of UV Radiation in the Marine Environment Cambridge University Press Cambridge Strategies for the minimisation of UV-induced damage 177 - 205
Sobrino C. , Montero O. , Lubian L. M. 2004 UV-B radiation increases cell permeability and damages nitrogen incorporation mechanisms in Nannochloropsis gaditana Aquat. Sci. 66 421 - 429
van de Poll W. H. , van Leeuwe M. A. , Roggeveld J. , Buma A. G. J. 2005 Nutrient limitation and high irradiance acclimation reduce PAR and UV-induced viability loss in the Antarctic diatom Chaetoceros brevis (Bacillariophyceae) J. Phycol. 41 840 - 850
van Kooten O. , Snel J. F. H. 1990 The use of chlorophyll fluorescence nomenclature in plant stress physiology Photosynth. Res. 25 147 - 150
Wang S. , Tang D. , He F. , Fukuyo Y. , Azanza R. V. 2008 Occurrences of harmful algal blooms (HABs) associated with ocean environments in the South China Sea Hydrobiologia 596 79 - 93
Wei S. F. , Hwang S. -P. L. , Chang J. 2004 Influence of ultraviolet radiation on the expression of proliferating cell nuclear antigen and DNA polymerase α in Skeletonema costatum (Bacillariophyceae) J. Phycol. 40 655 - 663
Wu H. , Gao K. , Wu H. 2009 Responses of a marine red tide alga Skeletonema costatum (Bacillariophyceae) to long-term UV radiation exposures J. Photochem. Photobiol. B Biol. 94 82 - 86
Zhang P. , Tang X. , Dong S. , Cai H. , Xiao H. , Feng L. 2007 UV-B radiation plays different roles in the competition between Alexandrium tamarense and Skeletonema costatum Oceanol. Limnol. Sin. 38 187 - 192