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Does increased salinity influence the competitive outcome of two producer species?

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Abstract

Within the context of global climate changes, it is expected that low-lying coastal freshwater ecosystems will face seawater intrusion with concomitant increase in salinity levels. Increased salinity may provoke disruption of competitive relationships among freshwater species. However, species may be capable of acclimating to salinity, which, in turn, may influence the resilience of ecosystems. Accordingly, this work aimed at assessing the effects of multigenerational exposure to low levels of salinity in the competitive outcome of two species of green microalgae: Raphidocelis subcapitata and Chlorella vulgaris. To attain this, three specific objectives were delineated: (1) compare the toxicity of natural seawater (SW) and NaCl (as a surrogate of SW) to the two microalgae, (2) determine the capacity of the two microalgae species to acclimate to low salinity levels, and (3) assess the influence of exposure to low salinity levels in the competitive outcome of the two microalgae. Results revealed SW to be slightly less toxic than NaCl for the two microalgae. The EC25,72 h for growth rate was 4.63 and 10.3 mS cm−1 for R. subcapitata and 6.94 and 15.4 mS cm−1 for C. vulgaris, respectively for NaCl and SW. Both algae were capable of acclimating to low levels of salinity, but C. vulgaris seemed to acclimate faster than R. subcapitata. When exposed in competition, under control conditions, the growth rates of C. vulgaris were lower than those of R. subcapitata. However, C. vulgaris was capable of acquiring competitive advantage equaling or surpassing the growth rate of R. subcapitata with the addition of NaCl or SW, respectively. The multigenerational exposure to low levels of salinity influenced the competitive outcome of the two algae both under control and salinity exposure. These results suggest that long-term exposure to low salinity stress can cause shifts in structure of algae communities and, therefore, should not be neglected since algae are at the basis of food web constituting important energetic resources to higher trophic levels.

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References

  • Affenzeller MJ, Darehshouri A, Andosch A, Lütz C, Lütz-Meindl U (2009) Salt stress-induced cell death in the unicellular green alga Micrasterias denticulata. J Exp Bot 60:939–954

    Article  CAS  Google Scholar 

  • Alyabyev AJ, Loseva NL, Gordon LK, Andreyeva IN, Rachimova GG, Tribunskih VI, Ponomareva AA, Kemp RB (2007) The effect of changes in salinity on the energy yielding processes of Chlorella vulgaris and Dunaliella maritima cells. Thermochim Acta 458:65–70

    Article  CAS  Google Scholar 

  • Arisz SA, Munnik T (2011) The salt stress-induced LPA response in Chlamydomonas is produced via PLA2 hydrolysis of DGK-generated phosphatidic acid. J Lipid Res 52:2012–2020

    Article  CAS  Google Scholar 

  • Barghbani R, Rezaei K, Javanshir A (2012) Investigating the effects of several parameters on the growth of Chlorella vulgaris using Taguchi’s experimental approach. Int J Biotechnol Wellness Ind 1:128–133

    Google Scholar 

  • Bengtsson J (1986) Life histories and interspecific competition between three Daphnia species in rockpools. J Anim Ecol 641–655

  • Berube KA, Dodge JD, Ford TW (1999) Effects of chronic salt stress on the ultrastructure of Dunaliella bioculata Chlorophyta, Volvocales: mechanisms of response and recovery. Eur J Phycol 342:117–123

    Article  Google Scholar 

  • Bervoets L, Verheyen R, Blust R (1996) Uptake of zinc by the midge larvae Chironomus riparius at different salinities: role of speciation, acclimation, and calcium. Environ Toxicol Chem 15:1423–1428

    Article  CAS  Google Scholar 

  • Blakeslee CJ, Galbraith HS, Robertson LS, St John White B (2013) The effects of salinity exposure on multiple life stages of a common freshwater mussel, Elliptio complanata. Environ Toxicol Chem 32:2849–2854

    Article  CAS  Google Scholar 

  • Bock C, Krienitz L, Proeschold T (2011) Taxonomic reassessment of the genus Chlorella (Trebouxiophyceae) using molecular signatures (barcodes)including description of seven new species. Fottea 11:293–312

    Article  Google Scholar 

  • Bossuyt BT, Janssen CR (2003) Acclimation of Daphnia magna to environmentally realistic copper concentrations. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology 136:253–264

    Google Scholar 

  • Brito AC, Newton A, Tett P, Fernandes TF (2012) How will shallow coastal lagoons respond to climate change? A modeling investigation. Estuarine. Coastal and Shelf Science 112(1):98–104

    Article  CAS  Google Scholar 

  • Carpenter KD, Rounds SA (2013) Plankton communities and summertime declines in algal abundance associated with low dissolved oxygen in the Tualatin River, Oregon (No. 2013–5037). US Geological Survey

  • Chen X, Stillman JH (2012) Multigenerational analysis of temperature and salinity variability affects on metabolic rate, generation time, and acute thermal and salinity tolerance in Daphnia pulex. J Therm Biol 37:185–194

    Article  Google Scholar 

  • Dassanayake NH (2008) Effects of salinity, atrazine, molinate and chlorpyrifos individually and as mixtures to the freshwater alga Pseudokirchneriella subcapitata and cladocerans Daphnia carinata. University of Technology, Faculty of Science, Sydney

    Google Scholar 

  • Dunlop JE, Kefford BJ, McNeil VH, McGregor GB, Choy S, Nugegoda D (2008) A review of guideline development for suspended solids and salinity in tropical rivers of Queensland, Australia. Australas J Ecotoxicol 14:129–142

    Google Scholar 

  • Elmaghrabi AM, Ochatt S, Rogers HJ, Francis D (2013) Enhanced tolerance to salinity following cellular acclimation to increasing NaCl levels in Medicago truncatula. Plant Cell Tiss Organ Cult 114:61–70

    Article  CAS  Google Scholar 

  • Etxeberria E, Pozueta-Romero J, Gonzales P (2012) In and out of the plant storage vacuole. Plant Sci 190:52–61

    Article  CAS  Google Scholar 

  • Feniova IY, Razlutsky VI, Palash AL (2011) Temperature effects of interspecies competition between cladoceran species in experimental conditions. Inland Water Biol 4:65–71

    Article  Google Scholar 

  • Fergola P, Cerasuolo M, Pollio A, Pinto G, DellaGreca M (2007) Allelopathy and competition between Chlorella vulgaris and Pseudokirchneriella subcapitata: experiments and mathematical model. Ecol Model 208:205–214

    Article  Google Scholar 

  • Ferguson, M D (2011) The influence of humic acid and water hardness on the partitioning of silver ions and nanoparticles between fresh water and freshwater algae.WWU Masters Thesis Collection. Paper 182

  • Fischer BB, Pomati F, Eggen RI (2013) The toxicity of chemical pollutants in dynamic natural systems: the challenge of integrating environmental factors and biological complexity. Science of the Total Environment 449:253–259

  • Foit K, Kaske O, Liess M (2011) Competition increases toxicant sensitivity and delays the recovery of two interacting populations. Aquat Toxicol 106–107:25–31

    Google Scholar 

  • Ghazy MMED, Habashy MM, Kossa FI, Mohammady EY (2009) Effects of salinity on survival, growth and reproduction of the water flea, Daphnia magna. Nat Sci 7:28–42

    Google Scholar 

  • Gonçalves AMM, Castro BB, Pardal MA, Gonçalves F (2007) Salinity effects on survival and life history of two freshwater cladocerans (Daphnia magna and Daphnia longispina). In Annales De Limnologie-International Journal of Limnology. EDP Sciences. Vol. 43, pp 13–20

  • Huang CJ, Wei G, Jie YC, Xu JJ, Zhao SY, Wang LC, Anjum SA (2015) Responses of gas exchange, chlorophyll synthesis and ROS-scavenging systems to salinity stress in two ramies (Boehmerianivea L.) cultivars. Photosynthetica 1–9.

  • Hutchinson GE (1961) The paradox of the plankton. Am Nat 95:137–145

    Article  Google Scholar 

  • IPCC, Intergovernmental Panel on Climate Change (2013) Climate change 2013: the physical science basis. Working Group I Contribution to the Intergovernmental Panel on Climate Change Fifth Assessment Report. Cambridge University Press, Cambridge

    Google Scholar 

  • Johnson HL, Stauber JL, Adams MS, Jolley DF (2007) Copper and zinc tolerance of two tropical microalgae after copper acclimation. Environ Toxicol 22:234–244

    Article  CAS  Google Scholar 

  • Katzmann S, Waringer-Löschenkohl A, Waringer JA (2003) Effects of inter-and intraspecific competition on growth and development of Bufo viridis and Bufo bufo tadpoles. Limnologica—Ecology and Management of Inland Waters 33:122–130

    Article  Google Scholar 

  • Kearney BD, Byrne PG, Reina RD (2012) Larval tolerance to salinity in three species of Australian anuran: an indication of saline specialisation in Litoria aurea. PLoS One 7(8):e43427

    Article  CAS  Google Scholar 

  • Kefford BJ, Palmer CG, Pakhomova L, Nugegoda D (2004) Comparing test systems to measure the salinity tolerance of freshwater invertebrates. Water SA 30:499–506

    Article  Google Scholar 

  • Keperesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Scie 40:482–487

    Article  Google Scholar 

  • Khatkar D, Kuhad M (2000) Short-term salinity induced changes in two wheat cultivars at different growth stages. Biol Plant 43:629–632

    Article  CAS  Google Scholar 

  • Kirrolia A, Bishnoia NR, Singhb N (2011) Salinity as a factor affecting the physiological and biochemical traits of Scenedesmus quadricauda. J Algal Biomass Utln 2:28–34

    Google Scholar 

  • Knillmann S, Stampfli NC, Beketov MA, Liess M (2012) Intraspecific competition increases toxicant effects in outdoor pond microcosms. Ecotoxicology 21:1857–1866

    Article  CAS  Google Scholar 

  • Kwok KWH, Grist EPM, Leung KMY (2009) Acclimation effect and fitness cost of copper resistance in the marine copepod Tigriopus japonicus. Ecotoxicol Environ Safe 72:358–364

    Article  CAS  Google Scholar 

  • Lee JS, Ray RI, Little BJ (2007) Comparison of Key West and Persian Gulf seawaters. CORROSION//2007. Houston, TX: NACE International, Paper No. 07518

  • Leitao J, Ribeiro R, Soares AM, Lopes I (2013) Tolerance to copper and to salinity in Daphnia longispina: implications within a climate change scenario. PloS One 8(8):e68702

  • Lemoine Y, Schoefs B (2010) Secondary keto carotenoid astaxanthin biosynthesis in algae: a multifunctional response to stress. Photosynth Res 106:155–177

    Article  CAS  Google Scholar 

  • Liquete C, Piroddi C, Drakou EG, Gurney L, Katsanevakis S (2013) Current status and future prospects for the assessment of marine and coastal ecosystem services: a systematic review. PLoS One 8(7):e67737

    Article  CAS  Google Scholar 

  • Lob DW, Silver P (2012) Effects of elevated salinity from road deicers on Chironomus riparius at environmentally realistic springtime temperatures. Freshwater Science 31:1078–1087

    Article  Google Scholar 

  • Loureiro C, Pereira JL, Pedrosa MA, Gonçalves F, Castro BB (2013) Competitive outcome of Daphnia-Simocephalus experimental microcosms: salinity versus priority effects. PLoS One 8(8):e70572

    Article  CAS  Google Scholar 

  • Lopes JF, Silva CI, Cardoso AC (2008) Validation of a water quality model for the Ria de Aveiro lagoon, Portugal. Environ Modell Softw 23: 479–494

  • Luo W, Pröschold T, Bock C, Krienitz L (2010) Generic concept in chlorella-related coccoid green algae (Chlorophyta, Trebouxiophyceae). Plant Biol 12:545–553

    Article  CAS  Google Scholar 

  • Martinoia E, Massonneau A, Frangne N (2000) Transport processes of solutes across the vacuolar membrane of higher plants. Plant Cell Physiol 41:1175–1186

    Article  CAS  Google Scholar 

  • Matile P (1978) Biochemistry and function of vacuoles. Annu Rev Plant Physiol 29:193–213

    Article  CAS  Google Scholar 

  • McGranahan DA, Balk D, Anderson B (2007) The rising tide: assessing the risks of climate change and human settlements in low elevation coastal zones. Environ Urban 19:17–39

    Article  Google Scholar 

  • Nicolle A, Hansson LA, Brönmark C (2010) Habitat structure and juvenile fish ontogeny shape zooplankton spring dynamics. Hydrobiologia 652(1):119–125

    Article  Google Scholar 

  • OECD (2006) Freshwater alga and cyanobacteria, growth inhibition test, no. 201. Organization for Economic Cooperation and Development, Paris

    Book  Google Scholar 

  • Osundeko O, Dean AP, Davies H, Pittman JK (2014) Acclimation of microalgae to wastewater environments involves increased oxidative stress tolerance activity. Plant Cell Physiol 55:1848–1857

    Article  CAS  Google Scholar 

  • Pratt R, Fong J (1940) Studies on Chlorella vulgaris ii. Further evidence that chlorella cells form a growth-inhibiting substance. Am J Bot 27:431–436

    Article  CAS  Google Scholar 

  • Roebeling PC, Costa L, Magalhães-Filho L, Tekken V (2013) Ecosystem service value losses from coastal erosion in Europe: historical trends and future projections. J Coast Conserv 17(3):389–395

    Article  Google Scholar 

  • Rubio F, Gassman W, Schroeder JI (1995) Sodium-driven potassium uptake by the plant potassium transporter HKT1 and mutations conferring salt tolerance. Science 270:1660–1663

    Article  CAS  Google Scholar 

  • Ryan CA, Walker-Simmons M (1983) Plant vacuoles. Methods Enzymol 96:580–589

    Article  CAS  Google Scholar 

  • Santos-Echeandía J, Caetano M, Brito P, Canario J, Vale C (2012) The relevance of defining trace metal baselines in coastal waters at a regional scale: the case of the Portuguese coast (SW Europe). Mar Environ Res 79:86–99

    Article  Google Scholar 

  • Santos MAPF, Vicensotti J, Monteiro RTR (2007) Sensitivity of four test organisms (Chironomus xanthus, Daphnia magna, Hydra attenuata and Pseudokirchneriella subcapitata) to NaCl: an alternative reference toxicant. J Braz Soc Ecotoxicol 2:229–236

    Article  Google Scholar 

  • Sarma SSS, Mangas-Ramirez E, Nandini S (2003) Effect of ammonia toxicity on the competition among three species of cladocerans (Crustacea: Cladocera). Ecotoxicol Environ Safety 55:227–235

    Article  CAS  Google Scholar 

  • Satyavani G, Chandrasehar G, Krishna VK, Goparaju A, Ayyapann S, Neelakanta RP, Balakrishna MP (2012) Toxicity assessment of expired pesticides to green algae Pseudokirchneriella subcapitata. ISRN Toxicology, Article ID 247072

  • Simmons JA (2012) Toxicity of major cations and anions (Na+, K+, Ca2+, Cl, and SO4 2−) to a macrophyte and an alga. Environmental Toxicology Chemistry 31:1370–1374

    Article  CAS  Google Scholar 

  • Singh SC, Sinha RP, Hader DP (2002) Role of lipids and fatty acids in stress tolerance in cyanobacteria. Actaprotozoologica 41:297–308

    CAS  Google Scholar 

  • Small C, Nicholls RJ (2003) A global analysis of human settlement in coastal zones. J Coast Res 19:584–599

    Google Scholar 

  • Stein JR (1973) Handbook of phycological methods: culture methods and growth measurement. Cambridge University Press, Cambridge, GB

    Google Scholar 

  • Talebi AF, Tabatabaei M, Mohtashami SK, Tohidfar M, Moradi F (2013) Comparative salt stress study on intracellular ion concentration in marine and salt-adapted freshwater strains of microalgae. Not Sci Biol 5:309–315

    CAS  Google Scholar 

  • Tillmanns AR, Burton SK, Pick FR (2011) Daphnia pre-exposed to toxic microcystis exhibit feeding selectivity. Int Rev Hydrobiol 96:20–28

    Article  Google Scholar 

  • Wan WO (2010) Perspectives on the use of algae as biological indicators for monitoring and protecting aquatic environments, with special reference to Malaysian freshwater ecosystems. Tropical Life Sciences Research 21:51–67

    Google Scholar 

  • Watanabe K, Imase M, Sasaki K, Ohmura N, Saiki H, Tanaka H (2006) Composition of the sheath produced by the green alga Chlorella sorokiniana. Lett Appl Microbiol 42:538–543

    Article  CAS  Google Scholar 

  • Wink M (1993) The plant vacuole: a multifunctional compartment. J Exp Bot:231–246

  • Yang XE, Wu X, Hao HL, He ZL (2008) Mechanisms and assessment of water eutrophication. Journal of Zhejiang University Science B 9:197–209

    Article  CAS  Google Scholar 

  • Zuanon JAS, Salaro AL, Veras GC, Tavares MM, Chaves W (2009) Acute and chronic salinity tolerance in adult siamese fighting fish, Betta splendens. Rev Bras Zootec 38:2106–2110

    Article  Google Scholar 

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Acknowledgments

This study was funded by national funds (OE) through FCT/MEC and co-funded by FEDER through COMPETE (POFC), by FSE and POPH and the research project SALTFREE (projects: IF/00475/2013; PTDC/AAC-CLI/111706/2009). C. Venâncio is grant holder from FCT (ref. SFRH/BD/81717/2011). This research was also partially supported by Strategic Funding UID/AMB/50017/2013 through national funds provided by FCT—Foundation for Science and Technology and European Regional Development Fund (ERDF) in the framework of the program PT2020.

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Venâncio, C..., Anselmo, E., Soares, A. et al. Does increased salinity influence the competitive outcome of two producer species?. Environ Sci Pollut Res 24, 5888–5897 (2017). https://doi.org/10.1007/s11356-016-8346-x

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