Adaptations of a green tide forming Ulva linza (Ulvophyceae, Chlorophyta) to selected salinity and nutrients conditions mimicking representative environments in the Yellow Sea

REFERENCES

• Beach K.S., Smith C.M., Michael T. & Shin H.-W. 1995. Photosynthesis in reproductive unicells of Ulva fasciata and Enteromorpha flexuosa: implications for ecological success. Marine Ecology Progress Series 125: 229–237.
   Web of Science ®Google Scholar
• Callow M.E., Callow J.A., Pickett-Heaps J.D. & Wetherbee R. 1997. Primary adhesion of Enteromorpha (Chlorophyta, Ulvales) propagules: quantitative settlement studies and video microscopy. Journal of Phycology 33: 938–947.
   Web of Science ®Google Scholar
• Campbell J.E. & Fourqurean J.W. 2009. Interspecific variation in the elemental and stable isotope content of seagrasses in South Florida. Marine Ecology Progress Series 387: 109–123.
   Web of Science ®Google Scholar
• Chang P.-H. & Isobe A. 2003. A numerical study on the Changjiang diluted water in the Yellow and East China Seas. Journal of Geophysical Research 108 (C9): 3299. DOI:10.1029/2002JC001749.
   Web of Science ®Google Scholar
• Chen C.T.A. 2008. Distributions of nutrients in the East China Sea and the South China Sea connection. Journal of Oceanography 64: 737–751.
   Web of Science ®Google Scholar
• Choi T.S., Kang E.J., Kim J.-H & Kim K.Y. 2010. Effect of salinity on growth and nutrient uptake of Ulva pertusa (Chlorophyta) from an eelgrass bed. Algae 25: 17–26.
   Google Scholar
• Cohen R.A. & Fong P. 2004a. Nitrogen uptake and assimilation in Enteromorpha intestinalis (L.) Link (Chlorophyta): using 15N to determine preference during simultaneous pulses of nitrate and ammonium. Journal of Experimental Marine Biology and Ecology 309: 67–77.
   Web of Science ®Google Scholar
• Cohen R.A. & Fong P. 2004b. Physiological responses of a bloom-forming green macroalga to short-term change in salinity, nutrients, and light help explain its ecological success. Estuaries 27: 209–216.
   Google Scholar
• Corey P., Kim J.K., Duston J. & Garbary D.J. 2014. Growth and nutrient uptake by Palmaria palmata integrated with Atlantic halibut in a land-based aquaculture system. Algae 29: 35–45.
   Web of Science ®Google Scholar
• Daoji L. & Daler D. 2004. Ocean pollution from land-based sources: East China Sea, China. Ambio 33: 107–113.
   Web of Science ®Google Scholar
• Dickson D.M.J., Jones W. & Davenport J. 1982. Osmotic adaptation in Ulva lactuca under fluctuating salinity regimes. Planta 155: 409–415.
   PubMed Web of Science ®Google Scholar
• Dunnett C.W. 1980. Pairwise multiple comparisons in the unequal variance case. Journal of the American Statistical Association 37: 796–800.
   Google Scholar
• Eppley R.W., Holmes R.W. & Strickland J.D.H. 1967. Sinking rates of marine phytoplankton measured with fluorometer. Journal of Experimental Marine Biology and Ecology 1: 191–208.
   Google Scholar
• Figueroa F.L., Israel A., Neori A., Martínez B., Malta E., Ang P., Inken S., Marquardt R. & Korbee N. 2009. Effects of nutrient supply on photosynthesis and pigmentation in Ulva lactuca (Chlorophyta): responses to short-term stress. Aquatic Biology 7: 173–183.
   Web of Science ®Google Scholar
• Fu M., Wang Z., Li Y., Li R., Sun P., Wei X., Lin X. & Guo J. 2009. Phytoplankton biomass size structure and its regulation in the Southern Yellow Sea (China): seasonal variability. Continental Shelf Research 29: 2178–2194.
   Web of Science ®Google Scholar
• Gao S., Chen X., Yi Q., Wang G., Pan G., Lin A. & Peng G. 2010. A strategy for the proliferation of Ulva prolifera, main causative species of green tides, with formation of sporangia by fragmentation. PLoS ONE 5 (1): e8571. DOI:10.1371/journal.pone.0008571.
   Web of Science ®Google Scholar
• Geng H., Yan T., Zhou M. & Liu Q. 2015. Comparative study of the germination of Ulva prolifera gametes on various substrates. Estuarine, Coastal and Shelf Science 163: 89–95.
   Web of Science ®Google Scholar
• Herlemann D.P.R., Labrenz M., Jürgens K., Bertilssom S., Waniek J.J. & Andersson A.F. 2011. Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME Journal 5: 1571–1579.
   PubMed Web of Science ®Google Scholar
• Kang E.J., Kim J.-H., Kim K., Choi H.-G. & Kim K.Y. 2014. Re-evaluation of green tide-forming species in the Yellow Sea. Algae 29: 267–277.
   Web of Science ®Google Scholar
• Karmer K. & Fong P. 2001. Nitrogen enrichment ameliorates the negative effects of reduced salinity in the green macroalgae Enteromorpha intestinalis. Marine Ecology Progress Series 218: 87–98.
   Web of Science ®Google Scholar
• Keesing J.K., Liu D., Fearns P. & Garcia R. 2011. Inter- and intra-annual patterns of Ulva prolifera green tides in the Yellow Sea during 2007–2009, their origin and relationship to the expansion of coastal seaweed aquaculture in China. Marine Pollution Bulletin 62: 1169–1182.
   PubMed Web of Science ®Google Scholar
• Kim J.-H., Kang E.J., Park M.G., Lee B.-G. & Kim K.Y. 2011. Effects of temperature and irradiance on photosynthesis and growth of a green-tide-forming species (Ulva linza) in the Yellow Sea. Journal of Applied Phycology 23: 421–432.
   Web of Science ®Google Scholar
• Kim J.-H., Lam S.M.N. & Kim K.Y. 2013a. Photoacclimation strategies of the temperate coralline alga Corallina officinalis: a perspective on photosynthesis, calcification, photosynthetic pigment contents and growth. Algae 28: 355–363.
   Web of Science ®Google Scholar
• Kim K., Kim K.Y., Kim J.-H., Kang E.J., Jeong, H.J. & Lee K. 2013b. Synergistic effects of elevated carbon dioxide and sodium hypochlorite on survival and impairment of three phytoplankton species. Algae 28: 173–183.
   Web of Science ®Google Scholar
• Kim K.Y. & Lee I. K. 1996. The germling growth of Enteromorpha intestinalis (Chlorophyta) in laboratory culture under different combinations of irradiance and salinity and temperature and salinity. Phycologia 35: 327–331.
   Web of Science ®Google Scholar
• Kim T.-W., Lee K., Lee C.-K., Jeong H.-D., Seo Y.-S., Lim W.-A., Kim K.Y. & Jeong H.-J. 2013c. Interannual nutrient dynamics in Korean coastal waters. Harmful Algae 30S: S15–S27.
   Google Scholar
• Leliaert F., Zhang X., Ye N., Malta E., Engelen A.H., Mineur F., Verbruggen H. & De Clerck O. 2009. Identity of the Qingdao algal bloom. Phycological Research 57: 147–151.
   Web of Science ®Google Scholar
• Li H.-M., Zhang C.-S., Han X.-R. & Shi X.-Y. 2015. Changes in concentrations of oxygen, dissolved nitrogen, phosphate, and silicate in the southern Yellow Sea, 1980–2012: sources and seaward gradients. Estuarine, Coastal and Shelf Science 163: 44–55.
   Web of Science ®Google Scholar
• Lin A., Shen S., Wang J. & Yan B. 2008. Reproduction diversity of Enteromorpha prolifera. Journal of Integrative Plant Biology 50: 622–629.
   PubMed Web of Science ®Google Scholar
• Lin A.-P., Wang C., Pan G.-H., Song L.-Y., Gao A., Xie X.-J., Wang Z.-Y., Niu J.-F. & Wang G.-C. 2011. Diluted seawater promoted the green tide of Ulva prolifera (Chlorophyta, Ulvales). Phycological Research 59: 295–304.
   Web of Science ®Google Scholar
• Liu D., Keesing J.K., Xing Q. & Shi P. 2009. World's largest macroalgal bloom caused by expansion of seaweed aquaculture in China. Marine Pollution Bulletin 58: 888–895.
   PubMed Web of Science ®Google Scholar
• Liu D., Keesing J.K., Dong Z., Zhen Y., Di B. & Shi Y. 2010. Recurrence of the world's largest green-tide in 2009 in Yellow Sea, China: Porphyra yezoensis aquaculture rafts confirmed as nursery for macroalgal blooms. Marine Pollution Bulletin 60: 1423–1432.
   PubMed Web of Science ®Google Scholar
• Liu D., Keesing J.K., He P., Wang Z. & Shi Y. 2013. The world's largest macroalgal bloom in the Yellow Sea, China: formation and implications. Estuarine, Coastal and Shelf Science 129: 2–10.
   Web of Science ®Google Scholar
• Liu S.M., Zhang J., Chen S.Z., Chen H.T., Hong H.T., Wei H. & Wu Q.M. 2003. Inventory of nutrient compounds in the Yellow Sea. Continental Shelf Research 23: 1161–1174.
   Web of Science ®Google Scholar
• Lotze H.K., Schramm W., Schories D. & Worm B. 1999. Control of macroalgal blooms at early developmental stages: Pilayella littoralis versus Enteromorpha spp. Oecologia 119: 46–54.
   Web of Science ®Google Scholar
• Lotze H.K., Worm B. & Sommer U. 2000. Propagule banks, herbivory and nutrient supply control population development and dominance patterns in macroalgal blooms. Oikos 89: 46–58.
   Web of Science ®Google Scholar
• Luo M.B., Liu F. & Xu Z.L. 2012. Growth and nutrient uptake capacity of two co-occurring species, Ulva prolifera and Ulva linza. Aquatic Botany 100: 18–24.
   Web of Science ®Google Scholar
• Marshall K., Joint I. & Callow M.E. 2006. Effect of marine bacterial isolates on the growth and morphology of axenic plantlets of the green alga Ulva linza. Microbial Ecology 52: 302–310.
   PubMed Web of Science ®Google Scholar
• Martins I., Oliveira J.M., Flindt M.R. & Marques J.C. 1999. The effect of salinity on the growth rate of the macroalgae Enteromorpha intestinalis (Chlorophyta) in the Mondego estuary (west Portugal). Acta Oecologica 20: 259–265.
   Web of Science ®Google Scholar
• Mineur F., Arenas F., Assis J., Davies A.J., Engelen A.H., Fernandes F., Malta E., Thibaut T., Nguyen T.V., Vaz-Pinto F., Vranken S, Serrão E.A. & De Clerck O. 2015. European seaweeds under pressure: consequences for communities and ecosystem functioning. Journal of Sea Research 98: 91–108.
   Web of Science ®Google Scholar
• Nelson T.A., Haberlin K., Nelson A.V., Ribarich H., Hotchkiss R., Van Alstyne K.L., Buckingham L., Simunds D.J. & Fredrickson, K. 2008. Ecological and physiological controls of species composition in green macroalgal blooms. Ecology 89: 1287–1298.
   PubMed Web of Science ®Google Scholar
• Pang S.J., Liu F., Shan T.F., Xu N., Zhang Z.H., Gao S.Q., Chopin T. & Sun S. 2010. Tracking the algal origin of Ulva bloom in the Yellow Sea by a combination of molecular, morphological and physiological analyses. Marine Environmental Research 69: 207–215.
   PubMed Web of Science ®Google Scholar
• Provasoli L. 1958. Effect of plant hormones on Ulva. Biological Bulletin 114: 375–384.
   Web of Science ®Google Scholar
• Rinehart S., Guidone M., Ziegler A., Schollmeier T. & Thornber C. 2014. Overwintering strategies of bloom-forming Ulva species in Narragansett Bay, Rhode Island, USA. Botanica Marina 57: 337–341.
   Web of Science ®Google Scholar
• Seery C.R., Gunthorpe L. & Ralph P.J. 2006. Herbicide impact on Hormosira banksii gametes measured by fluorescence and germination bioassays. Environmental Pollution 140: 43–51.
   PubMed Web of Science ®Google Scholar
• Serôdio J., da Silva J.M. & Catarino F. 2001. Use of in vivo chlorophyll a fluorescence to quantify short-term variations in the productive biomass of intertidal microphytobenthos. Marine Ecology Progress Series 218: 45–61.
   Web of Science ®Google Scholar
• Shi X., Qi M., Tang H. & Han X. 2015. Spatial and temporal nutrient variations in the Yellow Sea and their effects on Ulva prolifera blooms. Estuarine, Coastal and Shelf Science 163: 36–43.
   Web of Science ®Google Scholar
• Smetacek V. & Zingone A. 2013. Green and golden seaweed tides on the rise. Nature 504: 84–88.
   PubMed Web of Science ®Google Scholar
• Smith V.H., Tilman G.E. & Nekola J.C. 1999. Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution 100: 179–196.
   PubMed Web of Science ®Google Scholar
• Son Y.B., Choi B.-J., Kim Y.H. & Park Y.-G. 2015. Tracing floating green algae blooms in the Yellow Sea and the East China Sea using GOCI satellite data and Lagrangian transport simulations. Remote Sensing of Environment 156: 21–33.
   Web of Science ®Google Scholar
• Song W., Li Y., Fang S., Wang Z., Xiao J., Li R., Fu M., Zhu M. & Zhang X. 2015. Temporal and spatial distributions of green algae micro-propagules in the coastal waters of the Subei Shoal, China. Estuarine, Coastal and Shelf Science 163A: 29–35.
   Google Scholar
• Sousa A.I., Martins I., Lillebø A.I., Flindt M.R. & Pardal M.A. 2007. Influence of salinity, nutrients and light on the germination and growth of Enteromorpha sp. spores. Journal of Experimental Marine Biology and Ecology 341: 142–150.
   Web of Science ®Google Scholar
• Spoerner M., Wichard T., Bachhuber T., Stratmann J. & Oertel W. 2012. Growth and thallus morphogenesis of Ulva mutabilis (Chlorophyta) depends on a combination of two bacterial species excreting regulatory factors. Journal of Phycology 48: 1433–1447.
   PubMed Web of Science ®Google Scholar
• Strokal M., Yang H., Zhang Y., Kroeze C., Li L., Luan S., Wang H., Yang S. & Zhang Y. 2014. Increasing eutrophication in the coastal seas of China from 1970 to 2050. Marine Pollution Bulletin 85: 123–140.
   Web of Science ®Google Scholar
• Taylor R., Fletcher R.L. & Raven J.A. 2001. Preliminary studies on the growth of selected ‘green tide’ algae in laboratory culture: effects of irradiance, temperature, salinity and nutrients on growth rate. Botanica Marina 44: 327–336.
   Web of Science ®Google Scholar
• Tyler A.C., McGlathery K.J. & Anderson E.C. 2001. Macroalgae mediation of dissolved organic nitrogen fluxes in a temperate coastal lagoon. Estuarine, Coastal and Shelf Science 53: 155–168.
   Web of Science ®Google Scholar
• Vesty E.F., Kessler R.W., Wichard T. & Coates C. 2015. Regulation of gametogenesis and zoosporogenesis in Ulva linza (Chlorophyta): comparison with Ulva mutabilis and potential for laboratory culture. Frontiers in Plant Science 6: 15. DOI:10.3389/fpls.2015.00015.
   PubMed Web of Science ®Google Scholar
• Wallentinus I. 1984. Comparisons of nutrient uptake rates for Baltic macroalgae with different thallus morphologies. Marine Biology 80: 215–225.
   Web of Science ®Google Scholar
• Wang B., Wang X. & Zhan R. 2003. Nutrient conditions in the Yellow Sea and the East China Sea. Estuarine, Coastal and Shelf Science 58: 127–136.
   Web of Science ®Google Scholar
• Wang J., Jiang P., Cui Y., Li N., Wang M., Lin H., He P. & Qin S. 2010. Molecular analysis of green-tide-forming macroalgae in the Yellow Sea. Aquatic Botany 93: 25–31.
   Web of Science ®Google Scholar
• Wang Y., Wang Y., Zhu L., Zhou B. & Tang X. 2012. Comparative studies on the ecophysiological differences of two green tide macroalgae under controlled laboratory conditions. PLoS ONE 7 (8): e38245. DOI:10.1371/jounal.pone.0038245.
   Web of Science ®Google Scholar
• Wang Z., Xiao J., Fan S., Li Y., Liu X. & Liu D. 2015. Who made the world's largest green tide in China? – an integrated study on the initiation and early development of the green tide in Yellow Sea. Limnology and Oceanography 60: 1105–1117.
   Web of Science ®Google Scholar
• Wichard T. 2015. Exploring bacteria-induced growth and morphogenesis in the green macroalga order Ulvales (Chlorophyta). Frontiers in Plant Science 6: 86. DOI:10.3389/fpls.2015.00086.
   PubMed Web of Science ®Google Scholar
• Wichard T. & Oertel W. 2010. Gametogenesis and gamete release of Ulva mutabilis and Ulva lactuca (Chlorophyta): regulatory effects and chemical characterization of the “swarming inhibitor.” Journal of Phycology 46: 248–259.
   Web of Science ®Google Scholar
• Xia J., Li Y. & Zou D. 2004. Effects of salinity stress on PSII in Ulva lactuca as probed by chlorophyll fluorescence measurements. Aquatic Botany 80: 129–137.
   Web of Science ®Google Scholar
• Yan W., Zhang S., Sun P. & Seitzinger S.P. 2003. How do nitrogen inputs to the Changjiang basin impact the Changjiang River nitrate: a temporal analysis for 1968–1997. Global Biogeochemical Cycles 17: 1091. DOI:10.1029/2002GB002029.
   Web of Science ®Google Scholar
• Zhang J.H., Huo Y.Z., Zhang Z.L., Yu K.F., He Q., Zhang L.H., Yang L.L., Xu R. & He P.M. 2013. Variations of morphology and photosynthetic performances of Ulva prolifera during the whole green tide blooming process in the Yellow Sea. Marine Environmental Research 92: 35–42.
   Web of Science ®Google Scholar
• Zhang X., Wang H., Mao Y., Liang C., Zhuang Z., Wang Q. & Ye N. 2010. Somatic cells serve as potential propagule bank of Enteromorpha prolifera forming a green tide in the Yellow Sea, China. Journal of Applied Phycology 22: 173–180.
   Web of Science ®Google Scholar
• Zhou M.J., Shen Z.L. & Yu R.C. 2008. Responses of a coastal phytoplankton community to increased nutrient input from the Changjiang (Yangtze) River. Continental Shelf Research 28: 1483–1489.
   Web of Science ®Google Scholar