Advertisement

Carbon and nitrogen accumulation and interspecific competition in two algae species, Pyropia haitanensis and Ulva lactuca, under ocean acidification conditions

  • Binbin Chen
  • Lidong Lin
  • Zengling Ma
  • Tiantian Zhang
  • Weizhou Chen
  • Dinghui ZouEmail author
Article

Abstract

If the atmospheric CO2 continues to increase as predicted, Pyropia haitanensis would experience the coupled effects of ocean acidification (OA) and interference from the epiphyte alga Ulva lactuca. In the current study, we evaluated the carbon (C) and nitrogen (N) accumulation in P. haitanensis and U. lactuca under OA conditions, as well as the interspecific competition between these two algae. We found that, under mono-culture conditions, OA significantly enhanced the growth of both P. haitanensis and U. lactuca and markedly increased the soluble carbohydrate (SC) content and C/N ratios in P. haitanensis, but reduced its soluble proteins (SP) content. In U. lactuca, OA reduced its SP content, but increased C/N ratios, while its SC content was not significantly affected. Under biculture conditions, the rapid growth of U. lactuca and its comparatively more efficient use of nutrients resulted in insufficient available N sources for P. haitanensis. Biculture with U. lactuca increased SC but declined SP content. This also resulted in some membrane injuries that were indicated by increased malondialdehyde (MDA) content and depressed growth in P. haitanensis. Biculture with U. lactuca was disadvantageous for carbon and nitrogen accumulation in P. haitanensis. The results demonstrated that under conditions of OA, the negative effects caused by the epiphyte U. lactuca were more pronounced. If the CO2 levels rise as predicted, Ulva algae would severely interfere with maricultivation of P. haitanensis.

Keywords

Pyropia haitanensis Ulva lactuca Carbon and nitrogen accumulation Ocean acidification Interspecific competition Climate change 

Notes

Funding information

This work was supported by the National Natural Science Foundation of China (Nos. 41706147 and 41876124), the National Natural Science Foundation of Guangdong Province (2018B030311029), and the Fundamental Research Funds for the Central Universities of China (217BQ082).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical statement

This article does not contain any studies with animals performed by any of the authors.

References

  1. Anderson RJ, Monteiro PMS, Graham JL (1996) The effect of localised eutrophication on competition between Ulva lactuca (Ulvaceae, Chlorophyta) and a commercial resource of Gracilaria verrucosa (Gracilaria Cease, Rhodophyta). Hydrobiologia 326(327):291–296CrossRefGoogle Scholar
  2. Andria JR, Vergara JJ, Perez-Llorens JL (1999) Biochemical responses and photosynthetic performance of Gracilaria sp. (Rhodophyta) from Cádiz, Spain, cultured under different inorganic carbon and nitrogen levels. Eur J Phycol 34:497–504CrossRefGoogle Scholar
  3. Bowler C, Van Montagu M, Inze D (1992) Superoxide dismutase and stress tolerance. Annu Rev Plant Physiol Plant Mol Biol 43:83–116CrossRefGoogle Scholar
  4. Cai WJ, Hu X, Huang WJ, Murrell MC, Lehrter JC, Lohrenz SE, Chou WC, Zhai W, Hollibaugh JT, Wang Y (2011) Acidification of subsurface coastal waters enhanced by eutrophication. Nat Geosci 4:766–770CrossRefGoogle Scholar
  5. Chen F, Johns MR (1991) Effect of C/N ratio and aeration on the fatty acid composition of heterotrophic Chlorella sorokiniana. J Appl Phycol 3:203–209CrossRefGoogle Scholar
  6. Chen B, Zou D (2015) Altered seawater salinity levels affected growth and photosynthesis of Ulva fasciata (Ulvales, Chlorophyta) germlings. Acta Oceanol Sin 34(8):108–113CrossRefGoogle Scholar
  7. Chen B, Ma J, Cai Y, Sun B, Gao S, Hu X, Yang J (2013) Morphological and molecular analysis of attached Ulva L. green algae from Porphyra rafts from Rudong coasts in Jiangsu Province. Mar Environ Sci 32:394–397 (In Chinese with English abstract)Google Scholar
  8. Chen B, Zou D, Jiang H (2015) Elevated CO2 exacerbates competition for growth and photosynthesis between Gracilaria lemaneiformis and Ulva lactuca. Aquaculture 443:49–55CrossRefGoogle Scholar
  9. Chen B, Zou D, Ma J (2016) Interactive effects of elevated CO2 and nitrogen- phosphorus supply on the physiological properties of Pyropia haitanensis (Bangiales, Rhodophyta). J Appl Phycol 28(2):1235–1243CrossRefGoogle Scholar
  10. Chen B, Zou D, Yang Y (2017a) Increased iron availability resulting from increased CO2 enhances carbon and nitrogen metabolism in the economical marine red macroalga Pyropia haitanensis (Rhodophyta). Chemosphere 173:444–451CrossRefGoogle Scholar
  11. Chen B, Zou D, Zhu M (2017b) Growth and photosynthetic responses of Ulva lactuca L. (Ulvales, Chlorophyta) germlings to different pH levels. Mar Biol Res 13(3):351–357CrossRefGoogle Scholar
  12. Cornwall CE, Hepburn CD, Pritchard D, Currie KI, McGraw CM, Hunter KA, Hurd CL (2012) Carbon-use strategies in macroalgae: differential responses to lowered pH and implications for ocean acidification. J Phycol 48:137–144CrossRefGoogle Scholar
  13. Drechsler Z, Beer S (1991) Utilization of inorganic carbon by Ulva lactuca. Plant Physiol 97:1439–1444CrossRefGoogle Scholar
  14. Fabricius KE, Kluibenschedl A, Harrington L, Noonan S, De'ath G (2015) In situ changes of tropical crustose coralline algae along carbon dioxide gradients. Sci Rep 5:9537CrossRefGoogle Scholar
  15. Fei X (2004) Solving the coastal eutrophication problem by large scale seaweed cultivation. Hydrobiologia 512(1–3):145–151CrossRefGoogle Scholar
  16. Fong P, Zedler JB, Donohoe RM (1993a) Nitrogen versus phosphorous limitation of algal biomass in shallow coastal lagoons. Limnol Oceanogr 38:906–923CrossRefGoogle Scholar
  17. Fong P, Donohoe RM, Zedler JB (1993b) Competition with macroalgae and benthic cyanobacterial limits phytoplankton abundance in experimental microcosms. Mar Ecol Prog Ser 100:97–102CrossRefGoogle Scholar
  18. Friedlander M (1992) Gracilaria conferta and its epiphytes: the effect of culture conditions on growth. Bot Mar 35:423–428CrossRefGoogle Scholar
  19. Friedlander M, Gonen Y, Kashman Y, Beer S (1996) Gracilaria conferta and its epiphytes: 3. Allelopathic inhibition of the red seaweed by Ulva cf. lactuca. J Appl Phycol 8:21–25CrossRefGoogle Scholar
  20. Gordillo FJ, Figueroa FL, Niell FX (2003) Photon- and carbon-use efficiency in Ulva rigida at different CO2 and N levels. Planta 218:315–322CrossRefGoogle Scholar
  21. Gran G (1952) Determination of the equivalence point in potentiometric titrations of seawater with hydrochloric acid. Oceanol Acta 5:209–218Google Scholar
  22. Gruber N, Hauri C, Lachkar Z, Loher D, Frölicher TL, Plattner GK (2012) Rapid progression of ocean acidification in the California current system. Science 337:220–223CrossRefGoogle Scholar
  23. Harvey BP, Gwynn-Jone D, Moore PJ (2013) Meta-analysis reveals complex marine biological responses to the interactive effects of ocean acidification and warming. Ecol Evol 3(4):1016–1030CrossRefGoogle Scholar
  24. Health RL, Packer L (1968) Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198CrossRefGoogle Scholar
  25. Hepburn CD, Pritchard DW, Cornwall CE, Mcleod RJ, Beardall J, Raven JA, Hurd CL (2011) Diversity of carbon use strategies in a kelp forest community: implications for a high CO2 ocean. Glob Chang Biol 17:2488–2497CrossRefGoogle Scholar
  26. Hofmann GE, Barry JP, Edmunds PJ, Gates RD, Hutchins DA, Klinger T, Sewell MA (2010) The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism-to-ecosystem perspective. Annu Rev Ecol Evol Syst 41:127–147CrossRefGoogle Scholar
  27. IPCC (Intergovernmental Panel on Climate Change) (2007) Climate change 2007 synthesis report. Cambridge University Press, New YorkCrossRefGoogle Scholar
  28. Kang JW, Chung IK (2017) The effects of eutrophication and acidification on the ecophysiology of Ulva pertusa Kjellman. J Appl Phycol 29:2675–2683CrossRefGoogle Scholar
  29. Kerrison P, Suggett DJ, Hepburn LJ, Steinke M (2012) Effect of elevated pCO2 on the production of dimethylsulphoniopropionate (DMSP) and dimethylsulphide (DMS) in two species of Ulva (Chlorophyceae). Biogeochemistry 110:5–16CrossRefGoogle Scholar
  30. Khatun S, Ali MB, Hahn E-J, Paek KY (2008) Copper toxicity in Withania somnifera: growth and antioxidant enzymes responses of in vitro growing plants. Environ Exp Bot 64:279–285CrossRefGoogle Scholar
  31. Kleypas J, Langdon C (2000) Overview of CO2-induced changes in seawater chemistry. Proceedings 9th International Coral Reef Symposium, Bali, Indonesia 2, pp 23–27Google Scholar
  32. Kochert G (1978a) Carbohydrate determination by phenol sulphuric acid method. In: Hellebust JA, Craigie JS (eds) Handbook of Phycological methods: physiological and biochemical methods. Cambridge University Press, Cambridge, pp 95–97Google Scholar
  33. Kochert G (1978b) Protein determination by dye binding. In: Hellebust JA, Craigie JS (eds) Handbook of phycological methods: physiological and biochemical methods. Cambridge University Press, Cambridge, pp 91–93Google Scholar
  34. Lewis E, Wallace DWR (1998) Program developed for CO2 system calculations. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, US Department of Energy, Oak RidgeCrossRefGoogle Scholar
  35. Li L, Dong K, Tang X (2008) Response of interspecific competition between Ulva pertusa and Grateloupia filicina to UV-B irradiation enhancement. Environ Sci 29:2766–2772 (In Chinese with English abstract)Google Scholar
  36. Luo MB, Liu F, Xu ZL (2012) Growth and nutrient uptake capacity of two co-occurring species, Ulva prolifera and Ulva linza. Aquat Bot 100:18–24CrossRefGoogle Scholar
  37. Magnusson G, Larsson C, Axelsson L (1996) Effects of high CO2 treatment on nitrate and ammonium uptake by Ulva lactuca grown in different nutrient regimes. Sci Mar 60:179–189Google Scholar
  38. Mercado JM, Javier F, Gordillo L, Niell X, Figueroa FL (1999) Effects of different levels of CO2 on photosynthesis and cell components of the red alga Porphyra leucosticte. J Appl Phycol 11:455–461CrossRefGoogle Scholar
  39. Naldi M, Wheeler PA (2002) 15N Measurement of ammonium and nitrate uptake by Ulva fenestrata (Chlorophyta) and Gracilaria pacifica (Rhodophyta): comparison of net nutrient disappearance, release of ammonium and nitrate, and 15N accumulation in algal tissue. J Phycol 38:135–144CrossRefGoogle Scholar
  40. Olabarria C, Arenas F, Viejo RM, Gestoso I, Vaz-Pinto F, Incera M, Rubal M, Cacabelos E, Veiga P, Sobrino C (2013) Response of macroalgal assemblages from rockpools to climate change: effects of persistent increase in temperature and CO2. Oikos 122:1065–1079CrossRefGoogle Scholar
  41. Orr JC, Fabry VJ, Aumont O, Bopp L, Doney SC, Feely RA, Gnanadesikan A, Gruber N, Ishida A, Joos F, Key RM, Lindsay K, Maier-Reimer E, Matear R, Monfray P, Mouchet A, Najjar RG, Plattner GK, Rodgers KB, Sabine CL, Sarmiento JL, Schlitzer R, Slater RD, Totterdell IJ, Weirig MF, Yamanaka Y, Yool A (2005) Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681–686CrossRefGoogle Scholar
  42. Pang SJ, Zhang ZH, Zhao HJ, Sun JZ (2007) Cultivation of the brown alga Hizikia fusiformis (Harvey) Okamura: stress resistance of artificially raised young seedlings revealed by chlorophyll fluorescence measurement. J Appl Phycol 19:557–565CrossRefGoogle Scholar
  43. Rivers JS, Peckol P (1995) Interactive effects of nitrogen and dissolved inorganic carbon on photosynthesis, growth, and ammonium uptake of the macroalgae Cladophora vagabunda and Gracilaria tikvahiae. Mar Biol 121:747–753CrossRefGoogle Scholar
  44. Sarker MY, Bartsch I, Olischläger M, Gutow L, Wiencke C (2013) Combined effects of CO2, temperature, irradiance and time on the physiological performance of Chondrus crispus (Rhodophyta). Bot Mar 56:63–74CrossRefGoogle Scholar
  45. Sun Y, Bao X, Sun Q, Rao D, Xiao C, Xun J (2012) The prevention and elimination of hostile organisms occurred in the raft type cultivation of Gelidium amansii lamx. J Zhejiang Ocean U (Nat Sci) 31:79–84 In Chinese with English abstract)Google Scholar
  46. Verschoor AM, Van Dijk MA, Huisman J, Van Donk E (2013) Elevated CO2 concentrations affect the elemental stoichiometry and species composition of an experimental phytoplankton community. Freshw Biol 58:597–611CrossRefGoogle Scholar
  47. Xu J, Gao K (2013) Co-effects of CO2 and solar UVR on the growth and photosynthetic performance of the economic red macroalga Porphyra haitanensis. Acta Oceanol Sin 35:184–190 (In Chinese with English abstract)Google Scholar
  48. Xu J, Gao K (2015) Photosynthetic performance of the red alga Pyropia haitanensis during emersion, with special reference to effects of solar UV radiation, dehydration and elevated CO2 concentration. Photochem Photobiol 91:1376–1381CrossRefGoogle Scholar
  49. Xu Z, Zou D, Zhang X, Liu S, Gao K (2008) Effects of increased atmospheric CO2 and N supply on growth, biochemical compositions and uptake of nutrients in Gracilaria lemaneiformis (Rhodophyta). Acta Ecol Sin 28:3752–3759 (In Chinese with English abstract)CrossRefGoogle Scholar
  50. Xu D, Wang D, Li B, Fan X, Zhang X, Ye N, Wang Y, Mou S, Zhuang Z (2015) Effects of CO2 and seawater acidification on the early stages of Saccharina japonica development. Environ Sci Technol 49:3548–3556CrossRefGoogle Scholar
  51. Zou D (2005) Effects of elevated atmospheric CO2 on growth, photosynthesis and nitrogen metabolism in the economic brown seaweed, Hizikia fusiforme (Sargassaceae, Phaeophyta). Aquaculture 250:726–735CrossRefGoogle Scholar
  52. Zou D, Chen X (2002) Effects of elevated CO2 concentration on growth and some physiological and biochemical traits in Enteromorpha clathrata (Chlorophyta). Mar Sci Bull 21:38–45. (In Chinese with English abstract)Google Scholar
  53. Zou D, Gao K (2002) Effects of desiccation and CO2 concentrations on emersed photosynthesis in Porphyra haitanensis (Bangiales, Rhodophyta), a species farmed in China. Eur J Phycol 37:587–592CrossRefGoogle Scholar
  54. Zou D, Gao K (2004) Exogenous carbon acquisition of photosynthesis in Porphyra haitanensis (Bangiales, Rhodophyta) under emersed state. Prog Nat Sci 14(02):138–144CrossRefGoogle Scholar
  55. Zou D, Gao K (2010) Physiological responses of seaweeds to elevated atmospheric CO2 concentrations. In: Seckbach P, Einav R, Israel A (eds) Seaweeds and their role in globally changing environments. Springer, Dordrecht, pp 115–126CrossRefGoogle Scholar
  56. Zou D, Gao K, Ruan Z (2001) Effects of elevated CO2 concentration on photosynthesis and nutrients uptake of Ulva lactuca. J Ocean Univ Qingdao 31:877–882 (In Chinese)Google Scholar
  57. Zou D, Gao K, Luo H (2011) Short- and long-term effects of elevated CO2 on photosynthesis and respiration in the marine macroalga Hizikia fusiformis (Sargassaceae, Phaeophyta) grown at low and high N supplies. J Phycol 47:87–97CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Binbin Chen
    • 1
    • 2
  • Lidong Lin
    • 3
  • Zengling Ma
    • 1
  • Tiantian Zhang
    • 1
  • Weizhou Chen
    • 4
  • Dinghui Zou
    • 2
    Email author
  1. 1.College of Life and Environmental ScienceWenzhou UniversityWenzhouChina
  2. 2.School of Environment and EnergySouth China University of TechnologyGuangzhouChina
  3. 3.Dongtou Fisheries Science and Technology Research InstituteWenzhouChina
  4. 4.Department of BiologyShantou UniversityShantouChina

Personalised recommendations