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Photosynthetic carbon fixation by tropical coral reef phytoplankton assemblages: a UVR perspective
Photosynthetic carbon fixation by tropical coral reef phytoplankton assemblages: a UVR perspective
ALGAE. 2013. Sep, 28(3): 281-288
Copyright ©2013, The Korean Society of Phycology
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
  • Received : May 05, 2013
  • Accepted : August 08, 2013
  • Published : September 15, 2013
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About the Authors
Gang Li
Key Laboratory of Marine Bio-resources and Ecology, South China Sea Institute of Oceanology, CAS, Guangzhou, Guangdong 510301, China
Zhiwei Che
Sanya Marine Environment Monitoring Station, SOA, Sanya, Hainan 572000, China
Kunshan Gao
State Key Laboratory of Marine Environmental Science, Xiamen University, Xiamen, Fujian 361005, China
ksgao@xmu.edu.cn
Abstract
Photosynthetic carbon fixation regulates air-sea CO 2 fluxes in the waters of coral reefs. However, little has been documented on the effects of solar UV radiation (UVR, 280-400 nm) upon photosynthetic behaviors of phytoplankton dwelling in these ecosystems. In order to evaluate the aforesaid, surface dwelling tropical coral reef phytoplankton assemblages collected from the South China Sea were exposed to solar radiation (i.e., photosynthetically active radiation [PAR] + UV radiation A [UVA] + UV radiation B [UVB], 280-700 nm; PAR + UVA, 320-700 nm; and PAR, 400-700 nm) under static or simulated-mixing conditions. Under the static condition, UVA and UVB significantly reduced the carbon fixation with the maximum of 22.4 and 15.3%, respectively; while lower UVR-related photosynthetic inhibition was observed in case of phytoplankton samples being subjected to mixing. At a moderate level of mixing (i.e., circulation time 80 min), the UVA and UVB caused inhibition were lowered by 52.1 and 79.6%, respectively. Based on this it could be stated that vertical mixing induced by winds and/or tides in the natural environments could reduce the inhibitory effect of solar UVR on phytoplankton productivity in the coral reefs water.
Keywords
INTRODUCTION
Global warming, ocean acidification and increased UVB irradiance (280-315 nm) are known to influence marine organisms (Zepp et al. 2011). Corals, being no exception, are also subjected to these adversities (Banaszak and Lesser 2009). Coral reefs around the world have been bleached and endangered, possibly due to climate changes (Cantin et al. 2010, van Woesik and Jordán-Garza 2011, Hughes et al. 2012). Apart from various physico-chemical parameters of the environments, survival of corals also depends on several biological parameters that play vital roles in directly or indirectly affecting these reef builders. For e.g., phytoplankton in these ecosystems would be important for sustenance of coral reefs as the changes in phytoplankton photosynthetic processes in coral reef waters are known to influence stability of these ecosystems (Lesser 2004, Furnas et al. 2005). Growth of corals often makes their habitats to be oligotrophic and increase sunlight penetration (Dunne and Brown 1996, Kuwahara et al. 2010). Phytoplankton in coral reef water would thus be exposed to higher solar radiation.
Solar ultraviolet radiation (UVR, 280-400 nm) harms corals and primary producers in these waters (Banaszak and Lesser 2009). Phytoplankton species (especially those in the upper mixing layer), while utilizing light energy for photosynthesis, are also exposed to UVR that is known to reduce their growth, photosynthesis and calcification, damage DNA or D1 protein and pigments (Helbling et al. 1992, Buma et al. 2003, Bouchard et al. 2005, Roy et al. 2006, Gao et al. 2009, Li et al. 2011). Moderate levels of UV radiation A (UVA, 315-400 nm) also have positive effects, such as photo-repair of UV radiation B (UVB)-damaged DNA (Buma et al. 2003) and stimulate photosynthetic CO 2 -fixation at low photosynthetically active radiation (PAR) (Mengelt and Prézelin 2005, Li et al. 2011) or at PAR absence conditions (Gao et al. 2007, Li and Gao 2013). Mixing that moves phytoplankton up and down the water column causes fluctuation of the levels of solar radiation, enhancing non-photochemical quenching (Milligan et al. 2012) and lowering synthesis of UV-screening compounds (e.g., mycosporine-like amino acids [MAAs]) (Hernando et al. 2006), and also mitigating the negative effects of UVR (Neale et al. 1998). Such impacts of UVR fluctuation due to vertical mixing on phytoplankton photosynthesis have been extensively elaborated (e.g., Neale et al. 1998, Barbieri et al. 2002, Helbling et al. 2003, Milligan et al. 2012).
Coral reefs in the South China Sea are endangered as well, with the coverage decreased by 80% during the past 30 years (Hughes et al. 2012), likely being contributed by climate changes and environment degradations. Following this insight, extensive studies were conducted on these coral reefs (e.g., Li et al. 2008, Dong et al. 2009, Huang et al. 2011, Hughes et al. 2012); however, rather less attention was paid to phytoplankton in these coral reef waters (Zhang et al. 2009, Shen et al. 2010, Li and Gao 2013). As a habitat sharing counterpart to corals, phytoplankton may indirectly affect the survival of corals (discussed earlier); in view of this point, it is essential to evaluate the physiological effects of environments on these organisms. Here, we focus on examining the impacts of solar UVR on photosynthetic carbon fixation of phytoplankton assemblages from a coral reef water of the South China Sea and its relationship with mixing.
MATERIALS AND METHODS
- Sample collection
A coral reef region of Xisha Islands in the South China Sea ( Fig. 1 ), where about 127 species of corals (Li et al. 2008) and more than 150 species of coral reef fishes (Sun
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Site of study i.e., Yongxing Island in the South China Sea Scale bar represents: 50 km.
et al. 2005) were recorded, was chosen as the experimental area. Surface seawater samples (20 cm depth) were collected at a site 300 m off Yongxing Island (16°51′ N, 112°20′ E) (the largest island amongst the Xisha Islands [~1.8 km 2 ]), using a 10 L acid-cleaned (1 N HCl) polycarbonate container from 23 March to 1 April (Julian day 81 to 90) of 2007. Sample collections were carried out four times each day. The water samples collected in the morning (8:30 AM) were used for photosynthetic measurement and treated for chlorophyll a (Chl a ) content and species determinations within 15 min after the collections. The samples collected at 11:30 AM, 14:30 PM, and 17:30 PM were solely used to analyze Chl a and species composition. The water in the sampling area was reported to be oligotrophic with low nitrate (0.8 μmol L -1 ) and phosphate (0.12 μmol L -1 ) concentrations (Li et al. 2012).
- Environmental measurements
Sea surface temperature (SST), salinity (SSS) as well as wind speeds were obtained from Xisha Oceanic Monitoring Station located 100 m off the sampling site. Surface pH value was measured with an Okaton pH meter (Vernon Hills, IL, USA).
Incident solar radiation was continuously monitored using a diving broad-band radiometer (ELDONET; Real Time Computers Inc., Mohrendorf, Germany). This device efficiently measures the terrestrial or underwater solar irradiance of three ranges of UVB (280-315 nm), UVA (315-400 nm), and PAR (400-700 nm) (Häder et al. 1999). It is also equipped with a temperature and depth sensor to obtain the underwater profiles.
- Experimental design
Photosynthetic carbon fixation by phytoplankton assemblages was measured by dispensing pre-filtered seawater (180 μm-pore mesh) into 50 mL quartz or glass tubes, inoculating NaH 14 CO 3 solution (see below) and exposing to static or simulated-mixing conditions as described below with three radiation treatments (triplicate for each): a) PAR + UVA + UVB (PAB, 280-700 nm), uncovered quartz tubes; b) PAR + UVA (PA, 325-700 nm), uncovered glass tubes (50% transmittance at 325 nm); and c) PAR alone (P, 400-700 nm), quartz tubes wrapped with Ultraphan UV Opak Digefra film (50% transmittance at 395 nm) (UV Opak; Digefra, Munich, Germany). The transmission spectra of the tubes or cut-off foils and measurable errors have been reported previously (Li et al. 2011).
A time-series (days 81 to 90) of the impact of UVR exposure on photosynthesis was measured under static condition, through directly incubating phytoplankton samples in the three treatments in a water tank of 1.5 m × 1.0 m × 0.2 m (described below).
Effect of vertical mixing caused fluctuation on UVR exposure was determined by carrying out two sets of experiments: one set (days 89, 90) was comprised of 7 mixing depths, i.e., 0 (static condition), 3.2, 6.7, 10.2, 14, 16, and 21 m (close to bottom of euphotic zone) ( Fig. 2 ). The fluctuated irradiance that the samples received was simulated by continuously manipulating the different covering layers of neutral screens and simultaneously altering the solar radiation levels. For e.g., 3.2 m mixing depth, one layer of screen was covered and removed with a 20 min interval, fluctuating the cell-received irradiance from 100 to 55% and then backwards up to 100%; and for e.g., 21 m mixing depth, 6 layers of screens were covered one by one with a 20 min interval, decreasing the irradiance stepwise from 100, 55, 25, 15, 6, 3 to 1.5% and then removed the screens one by one to backwards up to 100% of surface sunlight. The other set (days 86, 87), a simulated 14 mmixed- depth was designed to determine the effects of UVR at varying mixing frequencies on the photosynthesis, i.e., 4 layers of neutral screens were covered then removed one by one, fluctuating the cell received irradiance stepwise from 100, 55, 25 to 15% of surface sunlight then backwards up to 100%; here, the intervals of changing screens were set at 5, 10, 20, and 30 min for each different incubation, making the circulation time of 40, 80, 160, and 240 min, respectively. We are aware that using stacks of neutral screens to block sunlight does not mimic the differential attenuation of UVR and PAR in water column,
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Typical underwater profiles of solar photosynthetically active radiation (PAR, 400-700 nm), UV radiation A (UVA, 315-400 nm), and UV radiation B (UVB, 280-315 nm) in W m-2, with K (m-1) values indicating the attenuation coefficients obtained on Julian day 82.
but it indeed provides very useful information to accomplish the objective of this study.
- Photosynthetic carbon fixation
Each of the aforesaid 50 mL sample was inoculated with 100 μL of 5 μCi (0.185 MBq) NaH 14 CO 3 solution (ICN Radiochemicals, Irvine, CA, USA). All the three sets of the aforesaid tubes containing phytoplankton samples were incubated for 6 h (9:30-15:30) under solar radiation in a tank continuously flushed with surface seawater at 25- 30℃ in order to mimic the natural environmental conditions. These samples were then filtered onto a Whatman GF/F glass fiber filter (25 mm in diameter) which was placed into a 20 mL scintillation vial; followed by this, they were exposed to HCl fumes overnight and dried to expel the non-fixed 14 C. A fixed volume (3 mL) of scintillation cocktail (UltimaGold; Perkin Elmer, Waltham, MA, USA) was added to each vial and the incorporated 14 C was measured with a liquid scintillation counter (LS 6500; Beckman Coulter, Fullerton, CA, USA). The carbon fixation rate of phytoplankton assemblages was calculated according to Holm-Hansen and Helbling (1995).
- Chlaand species analyses
Chl a concentration was determined by filtering 1.8-2.5 L of surface seawater onto a GF/F filter (25 mm), followed by extraction with 5 mL absolute methanol at room temperature (28-32℃) for 3 h in the dark (Helbling et al. 2003); optical density of the extractions was then measured with a scanning spectrophotometer (UV 2102-PC; CANY, Shanghai, China). Chl a content was calculated based on the equation of Porra (2002). For distinguishing the proportion of small cell-fractions (<5 μm), a sub-sample was pre-filtered through a 5 μm-pore Nitex mesh (Surrey, BC, Canada) and Chl a content was measured as described above.
For taxonomic analyses, the seawater samples (50 mL each) were fixed with buffered formalin (final concentration of 0.4%) and allowed to settle for 24 h in a cylinder of Utermöhl Chamber (Hydro-Bios, Kiel, Germany). Phytoplankton species were identified and enumerated with the aid of an inverted microscope (IX51; Olympus, Tokyo, Japan).
- Data analyses
Inhibition of photosynthetic carbon fixation or productivity due to UVR exposure was calculated based on the following formulae (Helbling et al. 1992):
  • Inh-UVA (%) = (PP- PPA)/PPAB× 100%
  • Inh-UVB (%) = (PPA- PPAB)/PPAB× 100%,
where Inh-UVA and Inh-UVB are the inhibition caused by UVA or UVB; P P , P PA , and P PAB are the photosynthetic production or carbon fixation rate under PAR-alone, PAR + UVA, and PAR + UVA + UVB, respectively.
Paired t-test was used to determine the significant differences among PAB, PA, and P treatments; one way ANOVA was used to establish the significant differences of UVR effects between under varying light and static conditions (control). The correlation analyses between the variables were established using a Kendall’s τ test with 95% confidence limit.
RESULTS
Typical profiles of sunlight ( Fig. 2 ) obtained on Julian day 82 showed the changes of solar irradiance with increasing water depth, wherein the lower limit of euphotic zone reached 22 m (K, 0.2 m -1 ); whereas 1% of surface
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(A) Total phytoplankton biomass, chlorophyll a (Chl a, μg L-1) and percentage (%) of Chl a in pico- and nanophytoplankton fraction (<5 μm). (B) Carbon fixation capacity (μg C L-1 h-1) and (C) photosynthetic rate (μg C [μg Chl a]-1 h-1) of phytoplankton assemblages exposed to photosynthetically active radiation (PAR) + UV radiation A (UVA) + UV radiation B (UVB) (PAB, 280-700 nm), PAR + UVA (PA, 325-700 nm), and PAR (P, 400-700 nm). (D) UVA or UVB caused inhibition (%). Vertical bars represent standard deviations (n = 3).
UVA and UVB penetrated to 12 m (K, 0.40 m -1 ) and 8.4 m (K, 0.55 m -1 ), respectively.
Total ozone column concentration over Yongxing Island varied from 251 to 255 Dobson Units from Julian day 80 to 92 ( http://jwocky.gsfc.nasa.gov/ ). Daily PAR doses of 4.9-9.3 MJ m -2 , UVA of 0.83-1.46 MJ m -2 and UVB of 33.6-61.7 KJ m -2 were recorded. SST and SSS ranges of 25.3-29.7℃ and 33.8-34.2 were recorded, and the ranges of pH and day-averaged wind speed were 8.18-8.36 and 1.95-5.77 m s -1 , respectively.
Total Chl a concentration varied from 0.25 to 0.99 μg L -1 , wherein smaller cells (<5 μm) accounted for 65 to 96% of total Chl a ( Fig. 3 A). During the study period, smaller
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Photosynthetic rate (μg C [μg Chl a]-1 h-1) of phytoplankton assemblages (A) at various mixing depths or (B) at a fixed depth with different mixing frequencies under photosynthetically active radiation (PAR) + UV radiation A (UVA) + UV radiation B (UVB) (PAB, 280-700 nm), PAR+UVA (PA, 325-700 nm), and PAR-alone (P, 400-700 nm). The inhibition (%) due to UVA or UVB exposure at various mixing depths (C) and at a fixed depth with varying mixing frequencies (D). Vertical bars represent standard deviations (n = 3 or 6).
cells accounted for maximal proportion of Chl a content on day 88, while larger ones accounted for this maximum on day 89 ( Fig. 3 A). Microscopic analysis revealed that filamentous cyanobacteria were the most abundant species, although some unicellular diatoms e.g., Achanthes abbreviate and Coscinodiscus spp. were occasionally spotted.
Photosynthetic ability of phytoplankton assemblages recorded under maximal solar radiation ranged from 1.0 to 4.89 μg C L -1 h -1 , on days 82 and 88, respectively ( Fig. 3 B); whereas photosynthetic rate varied from 4.06 to 7.74 μg C (μg Chl a ) -1 h -1 ( Fig. 3 C). In particular, higher levels of Chl a content and photosynthetic productivity (carbon fixation) were documented in the last few days ( Fig. 3 A-C). The presence of solar UVA and UVB significantly (p < 0.05) reduced the photosynthetic productivity except on days 82 and 90 of UVB ( Fig. 3 B & C). The percentage decline in carbon fixation rate ranged from 5.3 to 22.4% in case of UVA, while it ranged from 2.1 to 15.3% in case of UVB ( Fig. 3 D). Additionally, based on the fact that Chl a biomass and photosynthetic rate positively correlated to SST ( Table 1 ), it could be stated that higher temperature favored the growth of phytoplankton. A positive correlation was also observed between UVB inhibition and UVB/PAR ratio ( Table 1 ).
Exposing phytoplankton assemblages to changing irradiance (i.e., alter sunlight level stepwise from 100 to 1.5%, then back up to 100%) under mixing regimes with mixing depths increasing from 0 to 16 m, caused an increase in photosynthetic rate (PAB treatment), i.e., an increase of 5.07 to 6.87 μg C (μg Chl a ) -1 h -1 was observed. When the mixing depth deepened to 21 m however, the photosynthetic rate decreased to 6.41 μg C (μg Chl a ) -1 h -1 ( Fig. 4 A). Moreover, a drastic decline of UVA caused inhibition on photosynthetic ability was also noted, from 8.07 to -1.80% ( Fig. 4 C). The inhibition caused by UVB displayed a similar decreasing trend as that of UVA ( Fig. 4 C). Finally, as mixing depth increased, the increase in photosynthetic ability under the UVR absence condition (P) indicated that the photoinhibition due to PAR exposure occurred when the mixing was less than 16 m ( Fig. 4 A).
At a fixed-mixing depth of 14 m, when the mixing frequencies decreased (by prolonging the intervals of covering or removing screening filters from 5 to 30 min) and cells assembly received the same doses of sunlight, the photosynthetic rate (PAB) sharply decreased from 6.98 to 5.21 μg C (μg Chl a ) -1 h -1 ( Fig. 4 B). Here, the inhibition caused by UVA exposure remained almost constant (i.e., ~8.38%). The inhibition caused by UVB sharply decreased from 10.6 to 1.3% as the rate of mixing varied from 40 to 80 min per circulation, while this value increased to 22.5% in case of slow mixing ( Fig. 4 D). The inhibition due to UVA or UVB exposure was significantly lowered by 52.1 and 79.6% at moderate-mixing (80 min per circulation) as compared to static condition.
DISCUSSION
Coral reefs are generally distributed in shallow tropical waters (Stone 2006), and are often subjected to tides and / or wind induced vertical mixing. Here, we demonstrated that moderate mixing lowered the UVR caused inhibition on photosynthesis of phytoplankton assemblages in the coral reef waters of the South China Sea; moreover, photoinhibition was not only caused by UVR but also PAR, even when the mixing reached as deep as 16 m in this area.
More resistance of phytoplankton to UV radiation, indicated by lower UVR caused photoinhibition ( Fig. 3 D), was recorded in this coral reef water, as compared to that of the cell assemblies from coastal water for the same time period (Wu et al. 2010). It would be attributed by the long term high solar radiation and light penetration ( Fig. 2 ) since the higher light exposure could make the cells induce more efficient defensive or repair mechanisms involved in the protection and repair processes e.g., synthesizing and accumulating the MAAs and antioxidant enzymes (Hernando et al. 2006). Higher temperature (~28℃) in this water could be another cause for depressing the inhibitory effects of UVR, likely attributed by the enhancing activities of enzymes involved in the processes of damage-repair or photosynthesis (Buma et
r2and p-values of various parameters studied plotted against the environmental parametersThe parameters include chlorophylla(Chla, μg L-1), carbon fixation per volume of seawater (C-Vol, μg C L-1h-1) or per Chla(photosynthetic rate, μg C [μg Chla]-1h-1), and UV radiation B (UVB) or UV radiation A (UVA) caused inhibition (%) under solar radiation, whilst the environmental parameters include wind speed (WS, m s-1), surface seawater temperature (SST, ℃) and salinity (SSS), pH, ozone (D. U.), photosynthetically active radiation (PAR, MJ m-2) and ratios of UVB or UVA to PAR.*Significant differences (p < 0.05).
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r2 and p-values of various parameters studied plotted against the environmental parameters The parameters include chlorophyll a (Chl a, μg L-1), carbon fixation per volume of seawater (C-Vol, μg C L-1 h-1) or per Chl a (photosynthetic rate, μg C [μg Chl a]-1 h-1), and UV radiation B (UVB) or UV radiation A (UVA) caused inhibition (%) under solar radiation, whilst the environmental parameters include wind speed (WS, m s-1), surface seawater temperature (SST, ℃) and salinity (SSS), pH, ozone (D. U.), photosynthetically active radiation (PAR, MJ m-2) and ratios of UVB or UVA to PAR. *Significant differences (p < 0.05).
al. 2003). This fact can also explain the reason why higher photosynthetic productivity was observed at higher temperatures, i.e., the carbon fixation rate was positively correlated to SST ( Table 1 ).
In natural marine environments, it is obvious to understand that mixing would cause a change in optical property in the water column, thereby influencing quantity and quality of solar irradiance therein. Coral reef waters are often well mixed due to the tides and / or winds (Gardner et al. 2011). Changes in UVR levels like those produced by mixing can affect the performance and fitness of aquatic organisms (Hebling et al. 2003, Hernando et al. 2006). Depth and intensity (rate) of mixing had a profound effect on the UVR induced damage to photosynthesis of phytoplankton, as shown here ( Fig. 4 ) or in other studies (Barbieri et al. 2002, Hebling et al. 2003). Guan and Gao (2008) have formerly reported that the intensity and duration of UVR exposure are critical to balance the UVR damage and repair processes. As the mixing depth increased, phytoplankton were exposed more periodically to lower levels of solar radiation; the UVR damages could thus be counteracted by repair processes, resulting in the higher photosynthetic rate and lower UVR induced inhibition ( Fig. 4 A & C). Simultaneously, the increasing photosynthetic ability with mixing depth also indicated that not only solar UVR but PAR photoinhibited the carbon fixation of phytoplankton assembly, even when the mixing deepened to 16 m ( Fig. 4 A). When the intensity of mixing was kept moderate (80 min per circulation) for a certain time interval (6 h) and the frequency of light exposure varied, i.e., high / low, a decrease in UVR inhibition was noted, as compared to the slow-mixed, fast-mixed or static samples ( Fig. 4 D). This indicates that a certain time period is necessary to balance the UVR caused damage and to initiate the repair processes (Neale et al. 1998, Guan and Gao 2008).
Based on the study conducted here ( Fig. 4 ), it could be stated that apart from the intensity or dose of solar irradiation and its dynamics (Cullen and Lesser 1991, Gardner et al. 2011), there are several other environmental parameters such as mixing which play a pivotal role in and account for the extent of UVR induced inhibition on photosynthesis of phytoplankton assemblages from the coral reefs. The mixing that usually prevails the coral reef water would surely help in combating UVR harms on phytoplankton therein; this would in turn help establish a conducive environment for corals and would help them to flourish.
Acknowledgements
The authors would like to thank the comments of the two anonymous reviewers that helped to improve this manuscript. This work was financially supported by the National Natural Science Foundation (Nos. 40930846, 41120164007 and 41206132), National Basic Research Program of China (No. 2009CB421207), Program for Changjiang Scholars and Innovative Research Team (No. IRT0941), China-Japan collaboration project from MOST (No. S2012GR0290), Guangdong Natural Science Foundation (No. S2011040000151) and MEL Visiting Fellowship Program (No. MELRS1006). The authors are grateful to Yaxing He, Zhongming Lu, Jinwen Liu, Yi Wang and Yan Yang for their helpful assistances and to Dr. K. G. Suresh Kumar for polishing the English in this manuscript.
References
Banaszak A. T. , Lesser M. P. 2009 Effects of solar ultraviolet radiation on coral reef organisms. Photochem. Photobiol. Sci. 8 1276 - 1294
Barbieri E. S. , Villafañe V. E. , Helbling E. W. 2002 Experimental assessment of UV effects upon temperate marine phytoplankton when exposed to variable radiation regimes. Limnol. Oceanogr. 47 1648 - 1655
Bouchard J. N. , Campbell D. A. , Roy S. 2005 Effects of UV-B radiation on the D1 protein repair cycle of natural phytoplankton communities from three latitudes (Canada, Brazil, and Argentina). J. Phycol. 41 273 - 286
Buma A. G. J. , Boelen P. , Jeffrey W. H. 2003 UVR-induced DNA damage in aquatic organisms. In Helbling, E. W. & Zagarese, H. E. (Eds.) UV Effects in Aquatic Organisms and Ecosystems. The Royal Society of Chemistry Cambridge 291 - 327
Cantin N. E. , Cohen A. L. , Karnauskas K. B. , Tarrant A. M. , McCorkle D. C. 2010 Ocean warming slows coral growth in the central Red Sea. Science 329 322 - 325
Cullen J. J. , Lesser M. P. 1991 Inhibition of photosynthesis by ultraviolet radiation as a function of dose and dosage rate: results for a marine diatom. Mar. Biol. 111 183 - 190
Dong Z. -J. , Huang H. , Huang L. M. , Li Y. -C. 2009 Diversity of symbiotic algae of the genus Symbiodinium in scleractinian corals of the Xisha Islands in the South China Sea. J. Syst. Evol. 47 321 - 326
Dunne R. P. , Brown B. E. 1996 Penetration of solar UVB radiation in shallow tropical waters and its potential biological effects on coral reefs: results from the central Indian Ocean and Andaman Sea. Mar. Ecol. Prog. Ser. 144 109 - 118
Furnas M. , Mitchell A. , Skuza M. , Brodie J. 2005 In the other 90%: phytoplankton responses to enhanced nutrient availability in the Great Barrier Reef Lagoon. Mar. Pollut. Bull. 51 253 - 265
Gao K. , Ruan Z. , Villafañe V. E. , Gattuso J. -P. , Helbling E. W. 2009 Ocean acidification exacerbates the effect of UV radiation on the calcifying phytoplankter Emiliania huxleyi. Limnol. Oceanogr. 54 1855 - 1862
Gao K. , Wu Y. , Li G. , Wu H. , Villafañe V. E. , Helbling E. W. 2007 Solar UV-radiation drives CO2-fixation in marine phytoplankton: a double-edged sword. Plant Physiol. 144 54 - 59
Gardner J. P. A. , Garton D. W. , Collen J. D. 2011 Near-surface mixing and pronounced deep-water stratification in a compartmentalised, human-disturbed atoll lagoon system. Coral Reefs 30 271 - 282
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. , Lebert M. , Marangoni R. , Colombetti G. 1999 ELDONET: European Light Dosimeter Network hardware and software. J. Photochem. Photobiol. B Biol. 52 51 - 58
Helbling E. W. , Gao K. , Gonçalves 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
Helbling E. W. , Villafañe V. , Ferrario M. , Holm-Hansen O. 1992 Impact of natural ultraviolet radiation on rates of photosynthesis and on specific marine phytoplankton species. Mar. Ecol. Prog. Ser. 80 89 - 100
Hernando M. , Schloss I. , Roy S. , Ferreyra G. 2006 Photoacclimation to long-term ultraviolet radiation exposure of natural sub-Antarctic phytoplankton communities: Fixed surface incubations versus mixed mesocosms. Photochem. Photobiol. 82 923 - 935
Holm-Hansen O. , Helbling E. W. 1995 Técnicas para la medición de la productividad primaria en el fitoplancton. In Alveal, K., Ferrario, M. E., Oliveira, E. C. & Sar, E. (Eds.) Manual de Métodos Ficológicos. Universidad de Concepción Concepción 329 - 350
Huang H. , Dong Z. , Huang L. , Yang J. , Di B. , Li Y. , Zhou G. , Zhang C. 2011 Latitudinal variation in algal symbionts within the scleractinian coral Galaxea fascicularis in the South China Sea. Mar. Biol. Res. 7 208 - 211
Hughes T. P. , Huang H. , Young M. A. L. 2012 The wicked problem of China’s disappearing coral reefs. Conserv. Biol. 27 261 - 269
Kuwahara V. S. , Nakajima R. , Othman B. H. R. , Kushairi M. R. M. , Toda T 2010 Spatial variability of UVR attenuation and bio-optical factors in shallow coral-reef waters of Malaysia. Coral Reefs 29 693 - 704
Lesser M. P. 2004 Experimental biology of coral reef ecosystems. J. Exp. Mar. Biol. Ecol. 300 217 - 252
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. Coasts 36 728 - 736
Li G. , Gao K. , Gao G. 2011 Differential impacts of solar UV radiation on photosynthetic carbon fixation from the coastal to offshore surface waters in the South China Sea. Photochem. Photobiol. 87 329 - 334
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 (6º S-20º N) of early summer phytoplankton species compositions and size-fractioned productivity from Java Sea to South China Sea. Mar. Biol. Res. 8 163 - 171
Li Y. , Huang H. , Dong Z. , Lian J. , Zhou G. 2008 Headway of study on coral reefs ecological restoration. Acta Ecol. Sin. (in Chinese) 28 5048 - 5054
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
Milligan A. J. , Aparicio U. A. , Behrenfeld M. J. 2012 Fluorescence and nonphotochemical quenching responses to simulated vertical mixing in the marine diatom Thalassiosira weissflogii. Mar. Ecol. Prog. Ser. 448 67 - 78
Neale P. J. , Davis R. F. , Cullen J. J. 1998 Interactive effects of ozone depletion and vertical mixing on photosynthesis of Antarctic phytoplankton. Nature 392 585 - 589
Porra R. J. 2002 The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth. Res. 73 149 - 156
Roy S. , Mohovic B. , Gianesella S. M. , Schloss I. , Ferrario M. , Demers S. 2006 Effects of enhanced UV-B on pigment-based phytoplankton biomass and composition of mesocosm-enclosed natural marine communities from three latitudes. Photochem. Photobiol. 82 909 - 922
Shen P. P. , Tan Y. H. , Huang L. M. , Zhang J. L. , Yin J. Q. 2010 Occurrence of brackish water phytoplankton species at a closed coral reef in Nansha Islands, South China Sea. Mar. Pollut. Bull. 60 1718 - 1725
Stone R. P. 2006 Coral habitat in the Aleutian Islands of Alaska: depth distribution, fine-scale species associations, and fisheries interactions. Coral Reefs 25 229 - 238
Sun D. R. , Lin Z. J. , Qiu Y. S. 2005 Survey of coral reef fish resources of the Xisha Islands. Period. Ocean Univ. China (in Chinese) 35 225 - 231
van Woesik R. , Jordán-Garza A. G. 2011 Coral populations in a rapidly changing environment. J. Exp. Mar. Biol. Ecol. 408 11 - 20
Wu Y. , Gao K. , Li G. , Helbling E. W. 2010 Seasonal impacts of solar UV radiation on the photosynthesis of phytoplankton assemblages in the coastal water of the South China Sea. Photochem. Photobiol. 86 586 - 592
Zepp R. G. , Erickson D. J. 3rd , Paul N. D. , Sulzberger B. 2011 Effects of solar UV radiation and climate change on biogeochemical cycling: interactions and feedbacks. Photochem. Photobiol. Sci. 10 261 - 279
Zhang C. -X. , Sun X. -L. , Xie W. -L. , Xie S. -Y. , Zhan D. -L. , Zhang Y. -B. , Zhang J. -B. , Chen C. -L. 2009 Seasonal changes of the phytoplankton in Xuwen coral reef area. Oceanol. Limnol. Sin. (in Chinese) 40 159 - 165