Abstract
Salinization in tropical estuarine environments is expected as a result of climate change. The physiological performance of mangrove-associated key macroalgae can negatively be affected by increased salinity in such habitats. Thus, we analyzed photobiological and biochemical responses of the closely related red algae Bostrychia calliptera and Bostrychia montagnei incubated under a range of salinities (5, 11, 18, 37, 47, and 57 SA). Effective and maximum quantum yield, relative electron transport rate vs. photon fluence rate curves, photosynthetic parameters, and complementary energy dissipation pathways indicated that both species had lower photosynthetic performance under increased salinity, which was more strongly pronounced in B. calliptera. Both species increased their organic osmolyte contents with rising salinity stress. Dulcitol was the main organic osmolyte synthesized by B. calliptera, whereas B. montagnei synthesized dulcitol and sorbitol. Our results demonstrate that increased salinity in estuaries due to climate change will be detrimental to photosynthesis of both macroalgae, with B. calliptera more affected than B. montagnei. As B. montagnei synthesizes both dulcitol and sorbitol, it is more tolerant to salinity stress compared to B. calliptera. Our data document for the first time a new organic osmolyte distribution pattern in Bostrychia species, namely the occurrence of dulcitol only.
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References
Alvares, C. A., J. L. Stape, P. C. Sentelhas, J. L. De Moraes Gonçalves & G. Sparovek, 2013. Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22: 711–728.
Bindoff, N. L., W. W. L. Cheung, J. G. Kairo, J. Arístegui, V. A. Guinder, R. Hallberg, N. Hilmi, N. Jiao, M. S. Karim, L. Levin, S. O’Donoghue, S. R. Purca Cuicapusa, B. Rinkevich, T. Suga, A. Tagliabue, & P. Williamson, 2019. Changing Oean, Marine Ecosystems, and Dependent Communities In Pörtner, H.-O., D. C. Roberts, V. Masson-Delmotte, P. Zhai, M. Tignor, E. Poloczanska, K. Mintenbeck, A. Alegría, M. Nicolai, A. Okem, J. Petzold, B. Rama, & N. M. Weyer (eds), IPCC Special Report: The Ocean and Cryosphere in a Changing Climate. In press: 447–587, https://www.ipcc.ch/srocc/download-report/.
Borburema, H. D. S., R. P. Lima & G. E. C. Miranda, 2020. Effects of ocean warming, eutrophication and salinity variations on the growth of habitat-forming macroalgae in estuarine environments. Acta Botanica Brasilica 34: 662–672.
Borburema, H. D. S., Ê. N. A. Barbosa & G. E. C. Miranda, 2021. Decontamination protocol of the macroalga Bostrychia binderi Harvey (Rhodophyta) for unialgal cultures and laboratory studies. Hoehnea 48: e582020.
Borburema, H. D. S., N. S. Yokoya, L. P. Soares, J. M. C. Souza, F. Nauer, M. T. Fujii, C. B. Pasqualetii, G. E. C. Miranda & E. Marinho-Soriano, 2022a. Mangrove macroalgae increase their growth under ocean acidification: a study with Bostrychia ( Rhodophyta ) haplotypes from different biogeographic provinces. Journal of Experimental Marine Biology and Ecology 552: 151740.
Borburema, H. D. S., N. S. Yokoya, J. M. C. Souza, F. Nauer, M. S. Barbosa-silva & E. Marinho-Soriano, 2022b. Ocean warming and increased salinity threaten Bostrychia (Rhodophyta) species from genetically divergent populations. Marine Environmental Research 178: 105662.
Borlongan, I. A. G., M. R. J. Luhan, P. I. P. Padilla & A. Q. Hurtado, 2016. Photosynthetic responses of ‘Neosiphonia sp. epiphyte-infected’ and healthy Kappaphycus alvarezii (Rhodophyta) to irradiance, salinity and pH variations. Journal of Applied Phycology 28: 2891–2902.
Carneiro, M. A., do A., J. F. de J. Resende, S. R. Oliveira, F. de O. Fernandes, H. D. dos S. Borburema, M. S. Barbosa-Silva, A. B. G. Ferreira, & E. Marinho-Soriano, 2020. Performance of the agarophyte Gracilariopsis tenuifrons in a multi-trophic aquaculture system with Litopenaeus vannamei using water recirculation. Journal of Applied Phycology 33: 481–490.
Celis-Plá, P. S. M., J. M. Hall-Spencer, P. A. Horta, M. Milazzo, N. Korbee, C. E. Cornwall & F. L. Figueroa, 2015. Macroalgal responses to ocean acidification depend on nutrient and light levels. Frontiers in Marine Science 2: 26.
Choi, T.-S., E.-J. Kang, J.-H. Kim & K.-Y. Kim, 2010. Effect of salinity on growth and nutrient uptake of Ulva pertusa (Chlorophyta) from an eelgrass bed. Algae 25: 17–26.
Collins, M., R. Knutti, J. Arblaster, J.-L. Dufresne, T. Fichefet, P. Friedlingstein, X. Gao, W. J. Gutowski, T. Johns, G. Krinner, M. Shongwe, C. Tebaldi, A. J. Weaver, & M. Wehner, 2013. Long-term Climate Change: Projections, Commitments and Irreversibility In Stocker, T. F., D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, & P. M. Midgley (eds), Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press, Cambridge, United Kingdom and New York, NY, USA: 1029–1136.
Cunha, S. R. & C. S. Costa, 2002a. Gradientes de salinidade e freqüência de alagamento como determinantes da distribuição e biomassa de macroalgas associadas a troncos de manguezais na baía de babitonga, SC. Notas Técnicas Facimar 6: 93–102.
Cunha, S. R. & N. R. Duarte, 2002b. Taxas fotossintéticas e respiratórias de macroalgas do gênero Bostrychia. Notas Técnicas Facimar 6: 103–110.
Diehl, N., D. Michalik, G. C. Zuccarello & U. Karsten, 2019. Stress metabolite pattern in the eulittoral red alga Pyropia plicata (Bangiales) in New Zealand—mycosporine-like amino acids and heterosides. Journal of Experimental Marine Biology and Ecology 510: 23–30.
Duarte, R. C. S., G. Barros, S. V. Milesi & T. L. P. Dias, 2020. Influence of macroalgal morphology on the functional structure of molluscan community from hypersaline estuary. Hydrobiologia 847: 1107–1119.
Figueroa, F. L., P. S. M. Celis-Plá, B. Martínez, N. Korbee, A. Trilla & F. Arenas, 2019. Yield losses and electron transport rate as indicators of thermal stress in Fucus serratus (Ochrophyta). Algal Research 41: 101560.
Fontes, K. A. A., S. M. B. Pereira & C. S. Zickel, 2007. Macroalgas do “Bostrychietum” aderido em pneumatóforos de duas áreas de manguezal do Estado de Pernambuco, Brasil. Iheringia—Serie Botanica 62: 31–38.
Gambichler, V., G. C. Zuccarello & U. Karsten, 2021a. Physiological responses to salt stress by native and introduced red algae in New Zealand. Algae 36: 137–146.
Gambichler, V., G. C. Zuccarello & U. Karsten, 2021b. Seasonal changes in stress metabolites of native and introduced red algae in New Zealand. Journal of Applied Phycology 33: 1157–1170.
García, A. F., M. Bueno & F. P. P. Leite, 2016. The Bostrychietum community of pneumatophores in Araçá Bay: An analysis of the diversity of macrofauna. Journal of the Marine Biological Association of the United Kingdom 96: 1617–1624.
Genty, B., J. M. Briantais & N. R. Baker, 1989. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica Et Biophysica Acta 990: 87–92.
Giri, C., E. Ochieng, L. L. Tieszen, Z. Zhu, A. Singh, T. Loveland, J. Masek & N. Duke, 2011. Status and distribution of mangrove forests of the world using earth observation satellite data. Global Ecology and Biogeography 20: 154–159.
Gonçalves, C. T. P., 2020. Florações de macroalgas e seus efeitos sobre a pesca e macrofauna em uma região neotropical. PhD Thesis. Universidade Federal do Rio Grande do Norte.
Graiff, A., I. Bartsch, K. Glaser & U. Karsten, 2021. Seasonal photophysiological performance of adult Western Baltic Fucus vesiculosus (Phaeophyceae) under ocean warming and acidification. Frontiers in Marine Science 8: 666493.
INPE, 2022. Instituto Nacional de Pesquisas Espaciais. Divisão de Satélites e Sistemas Ambientais. http://satelite.cptec.inpe.br/radiacao/.
IPCC, 2014. Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva, Switzerland.
IPCC, 2019. Summary for policymakers In Pörtner, H.-O., D. C. Roberts, V. Masson-Delmotte, P. Zhai, M. Tignor, E. Poloczanska, K. Mintenbeck, A. Alegría, M. Nicolai, A. Okem, J. Petzold, B. Rama, & N. M. Weyer (eds), IPCC Special Report on the Ocean and Cryosphere in a Changing Climate. In press: 1–34, http://www.gtp89.dial.pipex.com/AR4.htm.
Karsten, U., 2012. Seaweed acclimation to salinity and desiccation stress. In Wiencke, C. & K. Bischof (eds), Seaweed Biology: Novel Insights into Ecophysiology, Ecology and Utilization. Springer, Berlin: 87–107.
Karsten, U. & G. O. Kirst, 1989a. The effect of salinity on growth, photosynthesis and respiration in the estuarine red alga Bostrychia radicans. Helgolander Meresunters 43: 61–66.
Karsten, U. & G. O. Kirst, 1989b. Incomplete turgor pressure regulation in the “terrestial” red alga, Bostrychia scorpioides (Huds.) Mont. Plant Science 61: 29–36.
Karsten, U., D. N. Thomas, G. Weykam, C. Daniel & G. O. Kirst, 1991. A simple and rapid method for exctraction and separation of low molecular weight carbohydrates from macroalgae using high-performance liquid chromatography. Plant Physiology and Biochemistry 29: 373–378.
Karsten, U., J. A. West & G. Zuccarello, 1992. Polyol content of Bostrychia and Stictosiphonia (Rhodomelaceae, Rhodophyta) from field and culture. Botanica Marina 35: 11–20.
Karsten, U., J. A. West & E. K. Ganesan, 1993. Comparative physiological ecology of Bostrychia moritziana (Ceramiales, Rhodophyta) from freshwater and marine habitats. Phycologia 32: 401–409.
Karsten, U., S. Koch, J. A. West & G. O. Kirst, 1994a. The intertidal red alga Bostrychia simpliciuscula Harvey ex J. Agardh from a mangrove swamp in Singapore: acclimation to light and salinity. Aquatic Botany 48: 313–323.
Karsten, U., J. A. West, G. C. Zuccarello & G. O. Kirst, 1994b. Physiological ecotypes in the marine alga Bostrychia radicans (Ceramiales, Rhodophyta) from the east coast of the U.S.A. Journal of Phycology 30: 174–182.
Karsten, U., C. Bock & J. A. West, 1995. Low molecular weight carbohydrate patterns in geographically different isolates of the eulittoral red alga Bostrychia tenuissima from Australia. Botanica Acta 108: 321–326.
Karsten, U., S. Koch, G. O. Kirst & J. A. West, 1996a. Physiological responses of the eulittoral macroalga Stictosiphonia hookeri (Rhodomelaceae, Rhodophyta) from Argentina and Chile: salinity, light and temperature acclimation. European Journal of Phycology 31: 361–368.
Karsten, U., A. S. Mostaerti, R. J. King, M. Kamiya & Y. Hara, 1996b. Osmoprotectors in some species of Japanese mangrove macroalgae. Phycological Research 44: 109–112.
Karsten, U., T. Sawall, J. West & C. Wiencke, 2000. Ultraviolet sunscreen compounds in epiphytic red algae from mangroves. Hydrobiologia 1: 159–171.
Kieckbusch, D. K., M. S. Koch, J. E. Serafy & W. T. Anderson, 2004. Trophic linkages among primary producers and consumers in fringing mangroves of subtropical lagoons. Bulletin of Marine Science 74: 271–285.
Kirst, G. O., 1981. Photosynthesis and respiration of Griffithsia monilis (Rhodophyceae): effect of light, salinity, and oxygen. Planta 151: 281–288.
Kirst, G. O., 1990. Salinity tolerance of eukaryotic marine algae. Annual Review of Plant Physiology and Plant Molecular Biology 41: 21–53.
Klughammer, C. & U. Schreiber, 2008. Complementary PS II quantum yields calculated from simple fluorescence parameters measured by PAM fluorometry and the Saturation Pulse method. PAM Application Notes 1: 27–35.
Kremer, B. P., 1976. 14C-Assimilate pattern and kinetics of photosynthetic 14CO2-assimilation of the marine red alga Bostrychia scorpioides. Planta 129: 63–67.
Lalegerie, F., S. Lajili, G. Bedoux, L. Taupin, V. Stiger-Pouvreau & S. Connan, 2019. Photo-protective compounds in red macroalgae from Brittany: considerable diversity in mycosporine-like amino acids (MAAs). Marine Environmental Research 147: 37–48.
Lesser, M. P., 2006. Oxidative stress in marine environments: biochemistry and physiological ecology. Annual Review of Physiology 68: 253–278.
Lide, D. R., 1992. CRC Handbook of Chemistry and Physics. The Chemical Rubber Company, Cleveland: 2385.
Lima, C. S. S., M. L. A. S. Badú & A. L. M. Pessanha, 2020. Response of estuarine fish assemblages to an atypical climatic event in northeastern Brazil. Regional Studies in Marine Science 35: 101121.
Lüning, K., 1990. Seaweeds: Their Environment, Biogeography and Ecophysiology. Wiley, New York.
Machado, G. E. M. & C. A. G. Nassar, 2007. Assembléia de Macroalgas de dois manguezais do núcleo Picinguaba—Parque Estadual da Serra do Mar, São Paulo, Brasil. Rodriguésia 58: 835–846.
Mann, F. D. & T. D. Steinke, 1988. Photosynthetic and respiratory responses of the mangrove-associated red algae, Bostrychia radicans and Caloglossa leprieurii. South African Journal of Botany 54: 203–207.
Marengo, J. A., R. R. Torres & L. M. Alves, 2017. Drought in Northeast Brazil-past, present, and future. Theoretical and Applied Climatology 129: 1189–1200.
Melville, F. & A. Pulkownik, 2006. Investigation of mangrove macroalgae as bioindicators of estuarine contamination. Marine Pollution Bulletin 52: 1260–1269.
Melville, F. & A. Pulkownik, 2007. Investigation of mangrove macroalgae as biomonitors of estuarine metal contamination. Science of the Total Environment 387: 301–309.
Mendonça, I. R. W. & P. C. da Lana, 2021. Richness and biomass distribution of the mangrove macroalgal association in a subtropical estuary. Ocean and Coastal Research 69: e21032.
Mercado, J. M. & F. X. Niell, 2000. Carbon dioxide uptake by Bostrychia scorpioides (Rhodophyceae) under emersed conditions. European Journal of Phycology 35: 45–51.
Nauer, F., H. D. S. Borburema, N. S. Yokoya & M. T. Fujii, 2021. Effects of ocean acidification on growth, pigment contents and antioxidant potential of the subtropical Atlantic red alga Hypnea pseudomusciformis Nauer, Cassano & M.C. Oliveira (Gigartinales) in laboratory. Brazilian Journal of Botany 44: 69–77.
Nauer, F., M. C. Oliveira, E. M. Plastino, N. S. Yokoya & M. T. Fujii, 2022. Coping with heatwaves: how a key species of seaweed responds to heat stress along its latitudinal gradient. Marine Environmental Research 177: 105620.
Pedroche, F. F., J. A. West, G. C. Zuccarello & U. Karsten, 1995. Marine red Algae of the mangroves in pacific Mexico and Guatemala. Botanica Marina 38: 111–119.
Peña, E. J., R. Zingmark & C. Nietch, 1999. Comparative photosynthesis of two species of intertidal epiphytic macroalgae on mangrove roots during submersion and emersion. Journal of Phycology 35: 1206–1214.
Pereira, D. T., C. Simioni, E. P. Filipin, F. Bouvie, F. Ramlov, M. Maraschin, Z. L. Bouzon & É. C. Schmidt, 2017. Effects of salinity on the physiology of the red macroalga, Acanthophora spicifera (Rhodophyta, Ceramiales). Acta Botanica Brasilica 31: 555–565.
Post, E., 1936. Systematische und pflanzengeographische Notizen zur Bostrychia-Caloglossa Assoziation. Revue Algologie 9: 1–84.
Reed, R. H., 1983. The osmotic responses of Polysiphonia lanosa (L.) Tandy from marine and estuarine sites: evidence for incomplete recovery of turgor. Journal of Experimental Marine Biology and Ecology 68: 169–193.
Rios-Marin, F., E. J. Peña-Salamanca & R. Benítez-Benítez, 2021. Efecto del pH en las tasas de bioacumulación de metales pesados en la macroalga Bostrychia calliptera (Rhodomelaceae, Ceramiales). Acta Biológica Colombiana 26: 226–234.
Rybczyk, J. M., J. W. Day Jr., A. Yánez-Arancibia & J. H. Cowan, 2012. Global climate change and estuarine systems. In Day, J. W., Jr., B. C. Crump, W. M. Kemp & A. Yáñez-Arancibia (eds), Estuarine Ecology. Wiley-Blackwell, Singapore: 497–519.
Sales, N. D. S., A. S. B. V. Baeta, L. G. de Lima & A. L. M. Pessanha, 2018. Do the shallow water habitats of a hypersaline tropical estuary act as nursery grounds for fishes? Marine Ecology 39: e12473.
Sánchez de Pedro, R., F. X. Niell & R. Carmona, 2014. Understanding the intertidal zonation of two macroalgae from ex situ photoacclimation responses. European Journal of Phycology 49: 538–549.
Sánchez de Pedro, R., U. Karsten, F. X. Niell & R. Carmona, 2016. Intraspecific phenotypic variation in two estuarine rhodophytes across their intertidal zonation. Marine Biology 163: 221.
Sánchez de Pedro, R., F. X. Niell & R. Carmona, 2022. Close but distant: emersion promotes ecophysiological differentiation between two rhodophytes within an estuarine intertidal zone. Journal of Experimental Marine Biology and Ecology 547: 151664.
Sassi, R., M. B. B. Kutner & G. F. Moura, 1988. Studies on the decomposition of drift seaweed from the northeast Brazilian coastal reefs. Hydrobiologia 157: 187–192.
Scherner, F., R. Ventura, J. B. Barufi & P. A. Horta, 2013. Salinity critical threshold values for photosynthesis of two cosmopolitan seaweed species: providing baselines for potential shifts on seaweed assemblages. Marine Environmental Research 91: 14–25.
Scherner, F., C. M. Pereira, G. Duarte, P. A. Horta, C. B. E. Castro, J. B. Barufi & S. M. B. Pereira, 2016. Effects of ocean acidification and temperature increases on the photosynthesis of tropical reef calcified macroalgae. PLoS ONE 11: 1–14. https://doi.org/10.1371/journal.pone.0154844.
Schreiber, U., W. Bilger, & C. Neubauer. 1995. Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of In vivo photosynthesis. In: Schulze, E.-D., & M. M. Caldwell (Eds.). Ecophysiology of Photosynthesis. Springer-Verlag: Berlin Heidelberg. 49–70.
Starr, R. & J. Zeikus, 1993. UTEX-the culture collection of algae at the University of Texas at Austin. Journal of Phycology 23(Suppl 2): 1–106.
Suggett, D. J., O. Prášil & M. A. Borowitzka, 2011. Chlorophyll a Fluorescence in Aquatic Sciences. Springer, Dordrecht.
Talarico, L., 1996. Phycobiliproteins and phycobilisomes in red algae: adaptive responses to light. Scientia Marina 60: 205–222.
Vieira, E. A., H. R. Filgueiras, M. Bueno, F. P. P. Leite & G. M. Dias, 2018. Co-occurring morphologically distinct algae support a diverse associated fauna in the intertidal zone of Araçá Bay, Brazil. Biota Neotropica 18: 1–8.
Walsby, A. E., 1997. Numerical integration of phytoplankton photosynthesis through time and depth in a water column. New Phytologist 136: 189–209.
West, J. A., G. C. Zuccarello, F. F. Pedroche & U. Karsten, 1992. Marine red algae of the mangroves in Pacific Mexico and their polyol content. Botanica Marina 35: 567–572.
Xavier, J. H. A., C. A. M. M. Cordeiros, G. D. Tenório, A. F. Diniz, E. P. N. P. Júnior, R. S. Rosa & I. L. Rosa, 2012. Fish assemblage of the Mamanguape Environmental Protection Area, NE Brazil: abundance, composition and microhabitat availability along the mangrove-reef gradient. Neotropical Ichthyology 10: 109–122.
Yokoya, N. S., H. Kakita, H. Obika & T. Kitamura, 1999a. Effects of environmental factors and plant growth regulators on growth of the red alga Gracilaria vermiculophylla from Shikoku Island. Japan. Hydrobiologia 398(399): 339–347.
Yokoya, N. S., E. M. Plastino, M. R. A. Braga, M. T. Fujii, M. Cordeiro-Marino, V. R. Eston & J. Harari, 1999b. Temporal and spatial variations in the structure of macroalgal communities associated with mangrove trees of Ilha do Cardoso, São Paulo state, Brazil. Revista Brasileira De Botânica 22: 195–204.
Acknowledgements
We are grateful to Niklas Plag (University of Rostock, Applied Ecology and Phycology) for the technical support during dulcitol and sorbitol analyses by HPLC. H.D.S. Borburema is grateful to the Coordination for the Improvement of Higher Education Personnel (CAPES-Brazil) by funding his stay at University of Rostock (Germany) for research activities (Finance code: 88887.586537/2020-00). We thank the anonymous reviewers and our editor Dr. Sally Entrekin for their constructive comments that greatly improved the manuscript.
Funding
This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001 and 88887.586537/2020-00, Ph.D. fellowships for H.D.S. Borburema. This study was also supported within the framework of the Research Training Group Baltic TRANSCOAST funded by the DFG (Deutsche Forschungsgemeinschaft) under grant number GRK 2000/1. This is Baltic TRANSCOAST publication no. GRK2000/00XY).
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Borburema, H.D.S., Graiff, A., Karsten, U. et al. Photobiological and biochemical responses of mangrove-associated red macroalgae Bostrychia calliptera and Bostrychia montagnei to short-term salinity stress related to climate change. Hydrobiologia 850, 4515–4530 (2023). https://doi.org/10.1007/s10750-022-05006-4
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DOI: https://doi.org/10.1007/s10750-022-05006-4