Effects of ultraviolet radiation on marine primary production with reference to satellite remote sensing

Abstract

Incubation experiments have shown that ultraviolet radiation (UVR) has significant influences on marine primary production (MPP). However, existing satellite remote sensing models of MPP only consider the effects of visible light radiation, ignoring the UVR. Additionally, the ocean color satellite data currently used for MPP estimation contain no UV bands. To better understand the mechanism of MPP model development with reference to satellite remote sensing, including UVR’s effects, we first reviewed recent studies of UVR’s effects on phytoplankton and MPP, which highlights the need for improved satellite remote sensing of MPP. Then, based on current MPP models using visible radiation, we discussed the quantitative methods used to implement three key model variables related to UVR: the UVR intensity at the sea surface, the attenuation of UVR in the euphotic layer, and the maximum or optimal photosynthetic rate, considering the effects of UVR. The implementation of these UVR-related variables could be useful in further assessing UVR’s effects on the remote sensing of MPP, and in re-evaluating our existing knowledge of MPP estimation at large spatial scales and long-time scales related to global change.

Keywords

photosynthetically active radiation / ultraviolet radiation / marine primary production / satellite remote sensing / radiative transfer model

References

[1] Ahmad Z, Herman J R, Vasilkov A P, Tzortziou M, Mitchell B G, Kahru M (2003). Seasonal variation of UV radiation in the ocean under clear and cloudy conditions. International Society for Optics and Photonics, In Optical Science and Technology, SPIE’s 48th Annual Meeting, 63–73

[2] Barber R T, Borden L, Johnson Z, Marra J, Knudson C, Trees C C (1997). Ground truthing modeled-kPAR and on-deck primary productivity incubations with in-situ observations. Ocean Optics, XIII. International Society for Optics and Photonics, 834–839

[3] Barbieri E S, Villafañe V E, Helbling E W (2002). Experimental assessment of UV effects on temperate marine phytoplankton when exposed to variable radiation regimes. Limnol Oceanogr, 47(6): 1648–1655

[4] Behrenfeld M J (1990). Primary productivity in the Southeast Ocean: effects of Enhanced Ultraviolet-B radiation. Thesis for the Degree of Master of Science. Oregon State University

[5] Behrenfeld M J, Boss E, Siegel D A, Shea D M (2005). Carbon-based ocean productivity and phytoplankton physiology from space. Global Biogeochem Cycles, 19(1), DOI: 10.1029/2004GB002299

[6] Behrenfeld M J, Falkowski P G (1997a). A consumer’s guide to phytoplankton primary productivity models. Limnol Oceanogr, 42(7): 1479–1491

[7] Behrenfeld M J, Falkowski P G (1997b). Photosynthetic rates derived from satellite-based chlorophyll concentration. Limnol Oceanogr, 42(1): 1–20

[8] Behrenfeld M J, Hardy J T, Gucinski H, Hanneman A, Lee H II, Wones A (1993). Effects of ultraviolet-B radiation on primary production along latitudinal transects in the South Pacific Ocean. Mar Environ Res, 35(4): 349–363

[9] Booth C R, Morrow J H (1997). The penetration of UV into natural waters. Photochem Photobiol, 65(2): 254–257

[10] Brühl C H, Crutzen P J (1989). On the disproportionate role of tropospheric ozone as a filter against solar UV-B radiation. Geophys Res Lett, 16(7): 703–706

[11] Calkins J, Thordardottir T (1980). The ecological significance of solar UV radiation on aquatic organisms. Nature, 283(5747): 563–566

[12] Campbell J, Antoine D, Armstrong R, Arrigo K, Balch W, Barber R, Behrenfeld M, Bidigare R, Bishop J, Carr M E, Esaias W, Falkowski P, Hoepffner N, Iverson R, Kiefer D, Lohrenz S, Marra J, Morel A, Ryan J, Vedernikov V, Waters K, Yentsch C, Yoder J (2002). Comparison of algorithms for estimating ocean primary production from surface chlorophyll, temperature, and irradiance. Global Biogeochemical Cycles, 16(3): 9‒1–9‒15

[13] Carr M E, Friedrichs M A M, Schmeltz M, Noguchi Aita M, Antoine D, Arrigo K R, Asanuma I, Aumont O, Barber R, Behrenfeld M, Bidigare R, Buitenhuis E T, Campbell J, Ciotti A, Dierssen H, Dowell M, Dunne J, Esaias W, Gentili B, Gregg W, Groom S, Hoepffner N, Ishizaka J, Kameda T, Le Quéré C, Lohrenz S, Marra J, Mélin F, Moore K, Morel A, Reddy T E, Ryan J, Scardi M, Smyth T, Turpie K, Tilstone G, Waters K, Yamanaka Y (2006). A comparison of global estimates of marine primary production from ocean color. Deep Sea Res Part II Top Stud Oceanogr, 53(5–7): 741–770

[14] Chen S W, Gao K S (2011). Solar ultraviolet radiation and CO₂-induced ocean acidification interacts to influence the photosynthetic performance of the red tide alga Phaeocystis globosa (Prymnesiophyceae). Hydrobiologia, 675(1): 105–117

[15] Cullen J J, Neale P J, Lesser M P (1992). Biological weighting function for the inhibition of phytoplankton photosynthesis by ultraviolet radiation. Science, 258(5082): 646–650

[16] El-Sayed S Z, Stephens F C, Bidigare R R, Ondrusek M E (1990). Effect of ultraviolet radiation on Antarctic marine phytoplankton. In: Kerry K R, Hempel G eds. Antarctic Ecosystems.1st ed. Berlin-Heidelberg: Springer, 379–385

[17] Eppley R W, Stewart E, Abbott M R, Heyman U (1985). Estimating ocean primary production from satellite chlorophyll. Introduction to regional differences and statistics for the Southern California Bight. J Plankton Res, 7(1): 57–70

[18] Frederick J E, Snell H E, Haywood E K (1989). Solar ultraviolet radiation at the earth's surface. Photochem Photobiol, 50(4): 443–450

[19] Friedrichs M A M, Carr M E, Barber R T, Scardi M, Antoine D, Armstrong R A, Asanuma I, Behrenfeld M J, Buitenhuis E T, Chai F, Christian J R, Ciotti A M, Doney S C, Dowell M, Dunne J, Gentili B, Gregg W, Hoepffner N, Ishizaka J, Kameda T, Lima I, Marra J, Mélin F, Moore J K, Morel A, O’Malley R T, O'Reilly J, Saba V S, Schmeltz M, Smyth T J, Tjiputra J, Waters K, Westberry T K, Winguth A (2009). Assessing the uncertainties of model estimates of primary productivity in the tropical Pacific Ocean. J Mar Syst, 76(1–2): 113–133

[20] Gala W R, Giesy J P (1991). Effects of ultraviolet radiation on the primary production of natural phytoplankton assemblages in Lake Michigan. Ecotoxicol Environ Saf, 22(3): 345–361

[21] Gao K S, Li G, Helbling E W, Villafañe V E (2007a). Variability of the UVR effects on photosynthesis of summer phytoplankton assemblages from a tropical coastal area of the South China Sea. Photochem Photobiol, 83(4): 802–809

[22] Gao K S, Wu Y P, Li G, Wu H Y, Villafañe V E, Helbling E W (2007b). Solar UV Radiation drives CO₂ fixation in marine phytoplankton: a double-edged sword. Plant Physiol, 144(1): 54–59

[23] Gao K S, Xu J T, Gao G, Li Y, Hutchins D A, Huang B Q, Wang L, Zheng Y, Jin P, Cai X N, Häder D P, Li W, Xu K, Liu N N, Riebesell U (2012). Rising CO₂ and increased light exposure synergistically reduce marine primary productivity. Nature Climate Change, 2(7): 519–523

[24] Garcia-Pichel F (1994). A model for internal self-shading in planktonic organisms and its implications for the usefulness of ultraviolet sunscreen. Limnol Oceanogr, 39(7): 1704–1717

[25] Guo S C, Qin Y, Zhao B L, Wu J, Chen H, Chen Y, Qin F (2002). The research of the effects of the atmosphere to the ultraviolet radiation. Universitatis Pekinensis, 38(3): 334–341 (Acta Scientiarum Naturalium)

[26] Häder D P, Sinha R P (2005). Solar ultraviolet radiation-induced DNA damage in aquatic organisms: potential environmental impact. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis, 571(1–2): 221–233

[27] He X Q, Bai Y, Pan D L, Chen C T A, Chen Q, Wang D F, Gong F (2013). Satellite views of seasonal and inter-annual variability of phytoplankton blooms in the eastern China seas over the past 14 yr (1998‒2011). Biogeosciences, 10(7): 4721–4739

[28] Helbling E W, Buma A G, de Boer M K, Villafañe V E (2001). In situ impact of solar ultraviolet radiation on photosynthesis and DNA in temperate marine phytoplankton. Mar Ecol Prog Ser, 211: 43–49

[29] Helbling E W, Carrillo P, Medina-Sánchez J M, Durán C, Herrera G, Villar-Argaiz M, Villafañe V E (2013). Interactive effects of vertical mixing, nutrients and ultraviolet radiation: in situ photosynthetic responses of phytoplankton from high mountain lakes in Southern Europe. Biogeosciences, 10(2): 1037–1050

[30] Helbling E W, Gao K S, 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

[31] Helbling E W, Villafañe E V, Holm-Hansen O (1994). Effects of ultraviolet radiation on Antarctic marine phytoplankton photosynthesis with particular attention to the influence of mixing. Antarct Res Ser, 62: 207–227

[32] Herman J R, Krotkov N, Celarier E, Larko G D, Labow G (1999). Distribution of UV radiation at the Earth’s surface from TOMS-measured UV-backscattered radiances. J Geophys Res, D, Atmospheres, 104(D10): 12059–12076

[33] Hirawake T, Takao S, Horimoto N, Ishimaru T, Yamaguchi Y, Fukuchi M (2011). A phytoplankton absorption-based primary productivity model for remote sensing in the Southern Ocean. Polar Biol, 34(2): 291–302

[34] Hiriart V P (2000). Ultraviolet radiation and primary production by Lake Erie phytoplankton communities. Doctoral thesis of University of Waterloo

[35] Højerslev N, Aas E (1991). A relationship for the penetration of ultraviolet B radiation into the Norwegian Sea. J Geophys Res, 96(C9): 17003–17005

[36] Huot Y, Jeffrey W H, Davis R F, Cullen J J (2000). Damage to DNA in Bacterioplankton: A model of damage by ultraviolet radiation and its repair as influenced by vertical mixing. Photochem Photobiol, 72(1): 62–74

[37] IOCCG (2008). Why ocean colour? The societal benefits of ocean-colour technology. In: Platt T, Hoepffner N, Stuart V, Brown C, eds. Reports of the international ocean-colour coordinating group, No.7, IOCCG, Dartmouth, Canada

[38] Ishizaka J, Siswanto E, Itoh T, Murakami H, Yamaguchi Y, Horimoto N, Ishimaru T, Hashimoto S, Saino T (2007). Verification of vertically generalized production model and estimation of primary production in Sagami Bay, Japan. J Oceanogr, 63(3): 517–524

[39] Jin Z H, Charlock T P, Rutledge K, Stamnes K, Wang Y J (2006). Analytical solution of radiative transfer in the coupled atmosphere-ocean system with a rough surface. Appl Opt, 45(28): 7443–7455

[40] Jin Z H, Stamnes K (1994). Radiative transfer in nonuniformly refracting layered media: atmosphere-ocean system. Appl Opt, 33(3): 431–442

[41] Lee Z P (2009). KPAR: An optical property associated with ambiguous values. Journal of Lake Sciences, 21(2): 159–164

[42] Lee Z P, Carder K L, Marra J, Steward R G, Perry M J (1996). Estimating primary production at depth from remote sensing. Appl Opt, 35(3): 463–474

[43] Lee Z P, Du K P, Arnone R, Liew S C, Penta B (2005). Penetration of solar radiation in the upper ocean: a numerical model for oceanic and coastal waters. J Geophys Res, 110(C9): C09019

[44] Lee Z P, Weidemann A, Kindle J, Arnone R, Carder K L, Davis C (2007). Euphotic zone depth: Its derivation and implication to ocean-color remote sensing. J Geophys Res, 112(C3): C03009

[45] Li G (2006). Studies on the relationships of solar ultraviolet radiation (the UVR) and photosynthetic carbon fixation by phytoplankton assemblages from the South China Sea. Doctoral thesis ofShan Tou University (in Chinese)

[46] Li G, Che Z, Gao K S (2013). Photosynthetic carbon fixation by tropical coral reef phytoplankton assemblages: a the UVR perspective. Algae, 28(3): 281–288

[47] Li G, Gao K (2014). Effects of solar UV radiation on photosynthetic performance of the diatom Skeletonema costatum grown under nitrate limited condition. Algae, 29(1): 27–34

[48] Li G, Gao K S (2013). Cell size-dependent effects of solar UV on primary production in coastal waters of the South China Sea. Estuaries Coasts, 36(4): 728–736

[49] Li G, Gao K S, 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(2): 329–334

[50] Li G, Wu Y P, Gao K S (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(G404029): 1–9

[51] Litchman E, Neale P J, Banaszak A T (2002). Increased sensitivity to ultraviolet radiation in nitrogen-limited dinoflagellates: photoprotection and repair. Limnol Oceanogr, 47(1): 86–94

[52] LokaBharathi P A, Krishnakumari L, Bhattathiri P M A, Chandramohan D (1997). UV radiation and primary production in the Antarctic waters. Scientific report: Thirteenth Indian Expedition to Antarctica, 323–334

[53] Lorenzen C J (1970). Surface chlorophyll as an index of the depth, chlorophyll content and primary productivity of the euphotic layer. Limnol Oceanogr, 15(3): 479–480

[54] Madronich S, McKenzie R L, Björn L O, Caldwell M M (1998). Changes in biologically active ultraviolet radiation reaching the earth's surface. J Photochem Photobiol B, 46(1–3): 5–19

[55] Marra J, Ho C, Trees C C (2003). An alternative algorithm for the calculation of primary productivity from remote sensing data. Lamont Doherty Earth Observatory Technical Report (LDEO-2003-1)

[56] Megard R O (1972). Phytoplankton, photosynthesis, and phosphorus in Lake Minnetonka, Minnesota. Limnol Oceanogr, 17(1): 68–87

[57] Mizubayashi K, Kuwahara V S, Segaran T C, Zaleha K, Effendy A W M, Kushairi M R M, Toda T (2013). Monsoon variability of ultraviolet radiation (the UVR) attenuation and bio-optical factors in the Asian tropical coral-reef waters. Estuar Coast Shelf Sci, 126: 34–43

[58] Neale P J, Cullen J J, Davis R F (1998). Inhibition of marine photosynthesis by ultraviolet radiation: variable sensitivity of phytoplankton in the Weddell-Scotia Confluence during the austral spring. Limnol Oceanogr, 43(3): 433–448

[59] Pang S H, Yu H F, He Y Y, Lv H X (2010). Response of Cyanobacterias to UV radiation. Food Sci Technol (Campinas), 35(9): 41–45 (in Chinese)

[60] Singh J, Dubey A K, Singh R P (2011). Antarctic terrestrial ecosystem and role of pigments in enhanced UV-B radiations. Rev Environ Sci Biotechnol, 10(1): 63–77

[61] Smyth T J (2011). Penetration of UV irradiance into the global ocean. J Geophys Res, 116(C11): C11020

[62] Tanskanen A, Krotkov N A, Herman J R, Arola A (2006). Surface ultraviolet irradiance from OMI. IEEE Trans Geosci Rem Sens, 44(5): 1267–1271

[63] Tedetti M, Sempéré R (2006). Penetration of ultraviolet radiation in the marine environment: a review. Photochem Photobiol, 82(2): 389– 397

[64] Tedetti M, Sempéré R, Vasilkov A, Charrière B, Nérini D, Miller W L, Kawamura K, Raimbault P (2007). High penetration of ultraviolet radiation in the south east Pacific waters. Geophys Res Lett, 34(12): L12610

[65] Vasilkov A, Krotkov N, Herman J, McClain C, Arrigo K, Robinson W (2001). Global mapping of underwater UV irradiances and DNA-weighted exposures sea-viewing using total ozone mapping spectrometer and wide field-of-view sensor data products. J Geophys Res, 106(C11): 27205–27219

[66] Vasilkov A P, Herman J R, Ahmad Z, Kahru M, Mitchell B G (2005). Assessment of the ultraviolet radiation field in ocean waters from space-based measurements and full radiative-transfer calculations. Appl Opt, 44(14): 2863–2869

[67] Villafañe V E, Sundbäck K, Figueroa F L, Helbling E W (2003). Photosynthesis in the aquatic environment as affected by UVR. UV effects in aquatic organisms and ecosystems. The Royal Society of Chemistry, Cambridge: 357–397

[68] Vincent W F, Roy S (1993). Solar ultraviolet-B radiation and aquatic primary production: damage, protection, and recovery. Environ Rev, 1(1): 1–12

[69] Wang P C, Wu B Y, Zhang W X (1999). Comparison of UV simulation and measurements of surface ultraviolet radiation. Chinese Journal of Atmosphere Sciences, 23(3): 359–364 (in Chinese)

[70] Wang Y, Yang Z, Tang X X, Liu Y, Li Y Q (2002). The sensitivity variability of seven species of marine microalgae to the influence of UV-B radiation. Acta Scientiae Circumstantiae, 22(2): 225–230 (in Chinese)

[71] Wu Y P, Gao K S (2011). Photosynthetic response of surface water phytoplankton assemblages to different wavebands of UV radiation in the South China Sea. Acta Oceanol Sin, 33(5): 146–151 (in Chinese)

[72] Wu Y P, Gao K S, Li G, Helbling E W (2010). Seasonal impacts of solar UV radiation on photosynthesis of phytoplankton assemblages in the coastal waters of the South China Sea. Photochem Photobiol, 86(3): 586–592

[73] Yuan X C, Yin K D, Zhou W H, Cao W X, Xu X Q, Zhao D (2007). Effects of ultraviolet radiation B (UV-B) on photosynthesis of natural phytoplankton assemblages in a marine bay in Southern China. Chin Sci Bull, 52(4): 545–552

[74] Zhang P Y, Tang X X, Cai P J, Yu J, Yang Z (2005). Effects of UV-B radiation on protein and nucleic acid synthesis in three species of marine Red-Tide Microalgae. Acta Phytoecol Sin, 29(3): 505–509 (in Chinese)

Acknowledgements

This study was supported by the National Basic Research Program of China (No. 2015CB954002), the Public Science and Technology Research Funds Projects for Ocean Research (No. 201505003), the National Natural Science Foundation of China (Grant Nos. 41322039, 41271378, and 41476155), the National High-Tech Research and Development Program of China (No. 2014AA123301) and the “Global Change and Air-Sea Interaction” project of China (No. GASI-03-03-01-01). We thank three anonymous reviewers for their constructive comments, which significantly strengthened the manuscript.

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