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Effects of ocean warming, eutrophication and salinity variations on the growth of habitat-forming macroalgae in estuarine environments

ABSTRACT

Global change and coastal eutrophication are affecting macroalgae worldwide. We analyzed the effects of increased water temperature (25, 28 and 32 °C) and eutrophication on the growth of Bostrychia binderi and Bostrychia montagnei in a range of salinities (18, 24, 30, 36 and 42 PSU) through three independent multifactorial experiments. Both species had higher growth at 25 °C than at 28 and 32 °C (warming scenario projected by IPCC), suggesting a negative effect of ocean warming. The species showed a broad tolerance to the range of salinities tested, with higher growth at 36 and 42 PSU, as a local adaptation strategy. Oligotrophic seawater significantly affected the growth of both species because the lowest growth was found in this condition, whereas highest growth was found with increased availability of nutrients, which is probably because estuaries are nutrient-rich environments due to continental runoff. High temperatures, low salinities and few nutrients had negative interactive effects on the growth of both species. Our results show that ocean warming can be detrimental to the studied macroalgae, and that both species are tolerant to eutrophication, with B. montagnei being more sensitive than B. binderi. Our results also reinforce the euryhaline characteristic of the genus Bostrychia.

Keywords:
Bostrychia; Bostrychietum; climate change; ecophysiology; estuarine macroalgae; eutrophication; global change; growth; salinity variation; sea level rise

Introduction

The Intergovernmental Panel on Climate Change (IPCC) has demonstrated global increases in anthropogenic emissions of greenhouse gases into the atmosphere, mainly carbon dioxide (CO2), which are inducing global changes such as continental and oceanic warming, ocean acidification and sea level rise (Collins et al. 2013Collins M, Knutti R, Arblaster J, et al. 2013. Long-term Climate Change: Projections, Commitments and Irreversibility. In: Qin D, Plattner GK, Tignor M, et al. (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. Cambrige, Cambridge University Press, 2013. p. 1029-1136.; IPCC 2014IPCC. 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 In: Core Writing Team, Pachauri PK, Meyer A. (eds.) IPCC, Geneva, Switzerland. p. 1-151.; Cornwall & Hurd 2020Cornwall CE, Hurd CL. 2020. Variability in the benefits of ocean acidification to photosynthetic rates of macroalgae without CO2-concentrating mechanisms. Marine and Freshwater Research 71: 275-280. ). The concentration of atmospheric CO2 has been rising steadily and has already been recorded at a level above 400 ppm (Hurd et al. 2020Hurd CL, Beardall J, Comeau S, et al. 2020. Ocean acidification as a multiple driver: How interactions between changing seawater carbonate parameters affect marine life. Marine and Freshwater Research 71: 263-274.). Models from the IPCC (2014)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 In: Core Writing Team, Pachauri PK, Meyer A. (eds.) IPCC, Geneva, Switzerland. p. 1-151. project a continuous increase in temperature on all continents and ocean surfaces until the end of the 21st century (2081-2100). These models are projected future scenarios called Representative Concentration Pathways (RCPs). According to the most optimistic scenario (RCP2.6), mean global warming will be approximately 1 °C, while moderate scenarios (RCP4.5 and RCP6.0) predict a warming around 2 °C and the critical scenario (RCP8.5) predicts approximately 4 °C.

Climate change is causing sea level rise due to thermal expansion of water and the melting of glaciers and ice caps (Collins et al. 2013Collins M, Knutti R, Arblaster J, et al. 2013. Long-term Climate Change: Projections, Commitments and Irreversibility. In: Qin D, Plattner GK, Tignor M, et al. (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. Cambrige, Cambridge University Press, 2013. p. 1029-1136.). Sea level rise will lead to the expansion of coastal flooding areas, resulting in estuary level rise and physical and chemical changes in estuarine waters (e.g. changes in: temperature, pH, luminosity, salt wedge affecting salinity gradients), because the estuarine systems are strongly affected by the surrounding sea (Rybczyk et al. 2012Rybczyk JM, Day Jr JW, Yánez-Arancibia A, Cowan JH. 2012. Global Climate Change and stuarine Systems. In: Day Jr JW, Crump BC, Kemp WM, Yáñez-Arancibia A. (eds.) Estuarine Ecology. Hoboken, New Jersey, Wiley-Blackwell, John Wiley & Sons Inc.. p. 497-519.; Couto et al. 2014Couto T, Martins I, Duarte B, Caçador I, Marques JC. 2014. Modelling the effects of global temperature increase on the growth of salt marsh plants. Applied Ecology and Environmental Research 12: 753-764. ).

Besides warming and sea level rise, another process that has been impacting coastal ecosystems worldwide is anthropogenic eutrophication. Human societies have dramatically increased nitrogen (N) and phosphorus (P) exports into aquatic environments across the globe (Smith et al. 1999Smith VH, Tilman GD, Nekola JC. 1999. Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution 100: 179-196.; Fowler et al. 2013Fowler D, Coyle M, Skiba U, et al. 2013. The global nitrogen cycle in the Twentyfirst century. Philosophical Transactions of the Royal Society B: Biological Sciences 368: 1-13.), causing the eutrophication process (Drljepan et al. 2014Drljepan M, McCarthy FM, Hubeny JB. 2014. Natural and cultural eutrophication of Sluice Pond, Massachusetts, USA, recorded by algal and protozoan microfossils. The Holocene 24: 1731-1742. ; Smith et al. 2014Smith VH, Dodds WK, Havens KE, et al. 2014. Comment: Cultural eutrophication of natural lakes in the United States is real and widespread. Limnology and Oceanography 59: 2217-2225. ). Urbanization and use of coastal zones are increasing nutrient inputs into coastal waters, causing eutrophication in coastal ecosystems (Smith et al. 1999Smith VH, Tilman GD, Nekola JC. 1999. Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution 100: 179-196.; Gao et al. 2017Gao G, Clare AS, Rose C, Caldwell GS. 2017. Eutrophication and warming-driven green tides (Ulva rigida) are predicted to increase under future climate change scenarios. Marine Pollution Bulletin 114: 439-447.). Eutrophication has been a growing threat for many coastal ecosystems as estuaries and salt marshes (Bricker et al. 2008Bricker SB, Longstaff B, Dennison W, et al. 2008. Effects of nutrient enrichment in the nation’s estuaries: A decade of change. Harmful Algae 8: 21-32. ; Deegan et al. 2012Deegan LA, Johnson DS, Warren RS, et al. 2012. Coastal eutrophication as a driver of salt marsh loss. Nature 490: 388-392. ; Paerl et al. 2014Paerl HW, Hall NS, Peierls BL, Rossignol KL. 2014. Evolving Paradigms and Challenges in Estuarine and Coastal Eutrophication Dynamics in a Culturally and Climatically Stressed World. Estuaries and Coasts 37: 243-258. ). Agriculture (mainly from fertilizer use), aquaculture (e.g. shrimp and fish farming), wastewater inputs and runoff from urban and industrial areas are all sources of eutrophication in coastal ecosystems (Marinho-Soriano et al. 2011Marinho-Soriano E, Azevedo CAA, Trigueiro TG, Pereira DC, Carneiro MAA, Camara MR. 2011. Bioremediation of aquaculture wastewater using macroalgae and Artemia. International Biodeterioration & Biodegradation 65: 253-257. ; Paerl et al. 2014Paerl HW, Hall NS, Peierls BL, Rossignol KL. 2014. Evolving Paradigms and Challenges in Estuarine and Coastal Eutrophication Dynamics in a Culturally and Climatically Stressed World. Estuaries and Coasts 37: 243-258. ; Tavares et al. 2014Tavares JL, Calado ALA, Fontes RFC. 2014. Estudos iniciais para uso do índice Trix para análise do nível de eutrofização no estuário do rio Potengi - Natal - RN - Brasil. Revista AIDIS de Ingeniería y Ciencias Ambientales. Investigación, desarrollo y práctica 7: 297-308. ; Gao et al. 2017Gao G, Clare AS, Rose C, Caldwell GS. 2017. Eutrophication and warming-driven green tides (Ulva rigida) are predicted to increase under future climate change scenarios. Marine Pollution Bulletin 114: 439-447.).

Costal eutrophication and global change are impacting macroalgae worldwide (Smale & Wernberg 2013Smale DA, Wernberg T. 2013. Extreme climatic event drives range contraction of a habitat-forming species. Proceedings of the Royal Society B: Biological Sciences 280: 20122829. doi: 10.1098/rspb.2012.2829.
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). Substantial loss of macroalgae biodiversity and considerable changes in macroalgae assemblages have already been recorded in the Southwest Atlantic caused by coastal urbanization (Scherner et al. 2013Scherner F, Horta PA, Oliveira EC, et al. 2013. Coastal urbanization leads to remarkable seaweed species loss and community shifts along the SW Atlantic. Marine Pollution Bulletin 76: 106-115. ). Several ecophysiological studies performed in the field or mesocosm systems (e.g.Figueroa et al. 2014Figueroa FL, Bonomi Barufi J, Malta EJ, et al. 2014. Short-term effects of increasing CO2, nitrate and temperature on three mediterranean macroalgae: Biochemical composition. Aquatic Biology 22: 177-193.; Burdett et al. 2015Burdett HL, Hatton AD, Kamenos NA. 2015. Effects of reduced salinity on the photosynthetic characteristics and intracellular DMSP concentrations of the red coralline alga, Lithothamnion glaciale. Marine Biology 162: 1077-1085. ; Celis-Plá et al. 2015Celis-Plá PSM, Hall-Spencer JM, Horta PA, et al. 2015. Macroalgal responses to ocean acidification depend on nutrient and light levels. Frontiers in Marine Science 2: 26. doi: 10.3389/fmars.2015.00026
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; Kim et al. 2016Kim JH, Kang EJ, Edwards MS, et al. 2016. Species-specific responses of temperate macroalgae with different photosynthetic strategies to ocean acidification: A mesocosm study. Algae 31: 243-256. ; Scherner et al. 2016Scherner F, Pereira CM, Duarte G, et al. 2016. Effects of ocean acidification and temperature increases on the photosynthesis of tropical reef calcified macroalgae. PLOS ONE 11: e0154844. doi: 10.1371/journal.pone.0154844
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; Gouvêa et al. 2017Gouvêa LP, Schubert N, Martins CDL, et al. 2017. Interactive effects of marine heatwaves and eutrophication on the ecophysiology of a widespread and ecologically important macroalga. Limnology and Oceanography 62: 2056-2075.; Sampaio et al. 2017Sampaio E, Rodil IF, Vaz-Pinto F, et al. 2017. Interaction strength between different grazers and macroalgae mediated by ocean acidification over warming gradients. Marine Environmental Research 125: 25-33. ; Kumar et al. 2018Kumar A, AbdElgawad H, Castellano I, et al. 2018. Effects of ocean acidification on the levels of primary and secondary metabolites in the brown macroalga Sargassum vulgare at different time scales. Science of The Total Environment 643: 946-956. ; Rich et al. 2018Rich WA, Schubert N, Schläpfer N, et al. 2018. Physiological and biochemical responses of a coralline alga and a sea urchin to climate change: Implications for herbivory. Marine Environmental Research 142: 100-107. ; Al-Janabi et al. 2019Al-Janabi B, Wahl M, Karsten U, et al. 2019. Sensitivities to global change drivers may correlate positively or negatively in a foundational marine macroalga. Scientific Reports 9: 1-10. ) and in the laboratory (e.g.Sinutok et al. 2012Sinutok S, Hill R, Doblin MA, et al. 2012. Microenvironmental changes support evidence of photosynthesis and calcification inhibition in Halimeda under ocean acidification and warming. Coral Reefs 31: 1201-1213. ; Johnson et al. 2014Johnson MD, Price NN, Smith JE. 2014. Contrasting effects of ocean acidification on tropical fleshy and calcareous algae. PeerJ 2: e411. doi: 10.7717/peerj.411
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; Fernández et al. 2015Fernández PA, Roleda MY, Hurd CL. 2015. Effects of ocean acidification on the photosynthetic performance, carbonic anhydrase activity and growth of the giant kelp Macrocystis pyrifera. Photosynthesis Research 124: 293-304.; Kram et al. 2016Kram SL, Price NN, Donham EM, Johnson MD, Kelly ELA, Hamilton SL, Smith JE. 2016. Variable responses of temperate calcified and fleshy macroalgae to elevated pCO2 and warming. International Council for the Exploration of the Sea Journal of Marine Science 73: 693-703.; Young & Gobler 2016Young CS, Gobler CJ. 2016. Ocean acidification accelerates the growth of two bloom-forming macroalgae. PLOS ONE 11: e0155152. doi: 10.1371/journal.pone.0155152
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; Gao et al. 2017Gao G, Clare AS, Rose C, Caldwell GS. 2017. Eutrophication and warming-driven green tides (Ulva rigida) are predicted to increase under future climate change scenarios. Marine Pollution Bulletin 114: 439-447.; Phelps et al. 2017Phelps CM, Boyce MC, Huggett MJ. 2017. Future climate change scenarios differentially affect three abundant algal species in southwestern Australia. Marine Environmental Research126: 69-80. ; Muñoz et al. 2018Muñoz PT, Sáez CA, Martínez-Callejas MB, et al. 2018. Short-term interactive effects of increased temperatures and acidification on the calcifying macroalgae Lithothamnion crispatum and Sonderophycus capensis. Aquatic Botany 148: 46-52. ; Piñeiro-Corbeira et al. 2018Piñeiro-Corbeira C, Barreiro R, Cremades J, Arenas F. 2018. Seaweed assemblages under a climate change scenario: Functional responses to temperature of eight intertidal seaweeds match recent abundance shifts. Scientific reports 8: 1-9. ; Zweng et al. 2018Zweng RC, Koch MS, Bowes G. 2018. The role of irradiance and C-use strategies in tropical macroalgae photosynthetic response to ocean acidification. Scientific Reports 8: 1-11.; Graba-Landry et al. 2018Graba-Landry A, Hoey AS, Matley JK, et al. 2018. Ocean warming has greater and more consistent negative effects than ocean acidification on the growth and health of subtropical macroalgae. Marine Ecology Progress Series 595: 55-69. ; Britton et al. 2019Britton D, Mundy CN, McGraw CM, et al. 2019. Responses of seaweeds that use CO2 as their sole inorganic carbon source to ocean acidification: Differential effects of fluctuating pH but little benefit of CO2 enrichment. International Council for the Exploration of the Sea Journal of Marine Science 76: 1860-1870. ; McNicholl et al. 2019McNicholl C, Koch MS, Hofmann LC. 2019. Photosynthesis and light-dependent proton pumps increase boundary layer pH in tropical macroalgae: A proposed mechanism to sustain calcification under ocean acidification. Journal of Experimental Marine Biology and Ecology 521: 151208. doi: 10.1016/j.jembe.2019.151208
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; Pajusalu et al. 2019Pajusalu L, Albert G, Fachon E, et al. 2019. Ocean acidification may threaten a unique seaweed community and associated industry in the Baltic Sea. Journal of Applied Phycology 32: 2469-2478.; Cornwall & Hurd 2020Cornwall CE, Hurd CL. 2020. Variability in the benefits of ocean acidification to photosynthetic rates of macroalgae without CO2-concentrating mechanisms. Marine and Freshwater Research 71: 275-280. ) have experimentally analyzed the possible effects of global change and eutrophication on the physiological and biochemical responses of macroalgae from different morpho-functional groups.

Other studies have created species distribution models to predict possible effects of global change on the climate niche of some macroalgae (e.g.Wernberg et al. 2011Wernberg T, Russell BD, Moore PJ, et al. 2011. Impacts of climate change in a global hotspot for temperate marine biodiversity and ocean warming. Journal of Experimental Marine Biology and Ecology-pages 400: 7-16.; Smale & Wernberg 2013Smale DA, Wernberg T. 2013. Extreme climatic event drives range contraction of a habitat-forming species. Proceedings of the Royal Society B: Biological Sciences 280: 20122829. doi: 10.1098/rspb.2012.2829.
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; Martínez et al. 2015Martínez B, Arenas F, Trilla A, et al. 2015. Combining physiological threshold knowledge to species distribution models is key to improving forecasts of the future niche for macroalgae. Global Change Biology 21: 1422-1433. ; Khan et al. 2018Khan AH, Levac E, Guelphen L, et al. 2018. The effect of global climate change on the future distribution of economically important macroalgae (seaweeds) in the northwest Atlantic. Facets 3: 275-286. ; Martínez et al. 2018Martínez B, Radford B, Thomsen MS, et al. 2018. Distribution models predict large contractions of habitat-forming seaweeds in response to ocean warming. Diversity and Distributions 24: 1350-1366. ). However, data reporting possible effects of global change on habitat-forming macroalgae in estuarine environments are still scarce in the scientific literature, which is recognized in the review by Koch et al. (2013Koch M, Bowes G, Ross C, Zhang XH. 2013. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology 19: 103-132. ) (a review of > 100 marine plant species), in which they highlighted the possible ability of Bostrychia scorpioides to assimilate bicarbonate (HCO3 -) under ocean acidification.

The Bostrychia genus (Rhodomelaceae, Rhodophyta) includes macroalgae distributed in tropical and temperate regions, which can be found in marine environments as rocky shores (Machado et al. 2011Machado GEM, Nassar CAG, de Széchy MTM. 2011. Phycological flora from the shallow sublittoral zone of the rocky shores of Serra do Mar State Park, Ubatuba, São Paulo. Acta Botanica Brasilica 25: 71-82. ) and continental aquatic environments, but are predominant in mangrove swamps and salt marshes (King & Puttock 1989King RJ, Puttock CF. 1989. Morphology and taxonomy of Bostrychia and Stictosiphonia (Rhodomelaceae, Rhodophyta). Australian Systematic Botany 21: 1-73.). Bostrychia species are the main constituents of the mangrove community known as Bostrychietum (Yokoya et al. 1999Yokoya NS, Plastino EM, Braga MDRA, et al. 1999a. Temporal and spatial variations in the structure of macroalgal communities associated with mangrove trees of Ilha do Cardoso, São Paulo state, Brazil. Brazilian Journal of Botany 22: 195-204. a; Fontes et al. 2007Fontes KA de A, Pereira SMB, Zickel CS. 2007. Macroalgas do “Bostrychietum” aderido em pneumatóforos de duas áreas de manguezal do Estado de Pernambuco, Brasil. Iheringia, Série Botânica 62: 31-38.; Jesus et al. 2015Jesus TB, Aguiar WM, Aleluia FTF. 2015. Distribuição e biomassa de macroalgas associadas a troncos e raízes de manguezais na baía de todos os santos, BA. Revista Brasileira de Ciências Ambientais (Online) 38: 12-20. ). This term was proposed by Post (1936Post E. 1936. Systematische und pflanzengeographische Notizen zur Bostrychia-Caloglossa Assoziation. Revue Algologie 9: 1-84.) and includes mainly rhodophytes as Bostrychia, Caloglossa and Catenella, as well as cyanobacteria and chlorophytes that associate themselves to pneumatophores of Avicennia, and to rhizophores and stems of Rhizophora and Laguncularia (West 1991West JA. 1991. New records of marine algae from Perú. Botanica Marina 34: 459-464.; West et al. 1993West JA, Zuccarello G, Karsten U, Calumpong HP. 1993. Biology of Bostrychia, Stictosiphonia and Caloglossa (Rhodophyta, Ceramiales). In: Calumpong HP, Menez EG. (eds.) Proceedings of the 2nd RP-USA Phycology Symposium /Workshop, Cebu City; Dumaguete City (Philippines). Philippines, Philippine Council for Aquatic and Marine Research and Development. p. 145-162.; Pedroche et al. 1995Pedroche FF, West JA, Zuccarello GC, Sentíes AG, Karsten U. 1995. Marine red algae of the mangroves in Southern Pacific México and Pacific Guatemala. Botanica Marina 38: 111-119.; Yokoya et al. 1999aYokoya NS, Plastino EM, Braga MDRA, et al. 1999a. Temporal and spatial variations in the structure of macroalgal communities associated with mangrove trees of Ilha do Cardoso, São Paulo state, Brazil. Brazilian Journal of Botany 22: 195-204. ; Fontes et al. 2007Fontes KA de A, Pereira SMB, Zickel CS. 2007. Macroalgas do “Bostrychietum” aderido em pneumatóforos de duas áreas de manguezal do Estado de Pernambuco, Brasil. Iheringia, Série Botânica 62: 31-38.; Jesus et al. 2015Jesus TB, Aguiar WM, Aleluia FTF. 2015. Distribuição e biomassa de macroalgas associadas a troncos e raízes de manguezais na baía de todos os santos, BA. Revista Brasileira de Ciências Ambientais (Online) 38: 12-20. ). These macroalgae, along with microalgae, represent a major source of primary productivity in mangrove ecosystems (Karsten et al. 1994aKarsten U, Koch S, West JA, Kirst GO. 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.), as they produce organic matter and participate in nutrient cycling (McClusky & Elliot 2004McClusky DS, Elliot M. 2004. The Estuarine Ecosystem: Ecology Threats and Management. New York, Oxford University Press Inc.). Furthermore, they act as microhabitats for several organisms, mainly protists and invertebrates (García et al. 2016García AF, Bueno M, Leite FPP. 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.; Borburema 2017Borburema HDS 2017. Mudanças ambientais globais, efeitos da variação de temperatura, salinidade e nutrientes sobre o crescimento de espécies de Bostrychia (Rhodophyta). MSc Thesis, Universidade Federal da Paraíba, Rio Tinto.; Vieira et al. 2018Vieira EA, Filgueiras HR, Bueno M, et al. 2018. Co-occurring morphologically distinct algae support a diverse associated fauna in the intertidal zone of Araçá Bay, Brazil. Biota Neotropica 18. doi: 10.1590/1676-0611-bn-2017-0464
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) and can be indicators of environmental quality (Melville & Pulkownik 2006Melville F, Pulkownik A. 2006. Investigation of mangrove macroalgae as bioindicators of estuarine contamination. Journal of Experimental Marine Biology and Ecology 52: 1260-1269. ; Fontes et al. 2007Fontes KA de A, Pereira SMB, Zickel CS. 2007. Macroalgas do “Bostrychietum” aderido em pneumatóforos de duas áreas de manguezal do Estado de Pernambuco, Brasil. Iheringia, Série Botânica 62: 31-38.; Melville & Pulkownik 2007Melville F, Pulkownik A. 2007. Investigation of mangrove macroalgae as biomonitors of estuarine metal contamination. Science of The Total Environment 387: 301-309. ) and food resource for consumers (Campos et al. 2015Campos DMAR, Silva AF, Sales NS, Oliveira REMCC, Pessanha ALM. 2015. Trophic relationships among fish assemblages on a mudflat within a Brazilian Marine protected area. Brazilian Journal of Oceanography 63: 429-442.).

Ecophysiological studies of Bostrychia species with salinity variations have demonstrated their physiological ability to tolerate salinity ranges, showing in some works an optimum growth at low salinities (Karsten & Kirst 1989aKarsten U, Kirst GO. 1989a. The effect of salinity on growth, photosynthesis and respiration in the estuarine red algaBostrychia radicansMont. Helgoländer Meeresuntersuchungen 43: 61-66.; bKarsten U, Kirst GO. 1989b. Incomplete turgor pressure regulation in the “terrestial” red alga, Bostrychia scorpioides (Huds.) Mont. Plant Science 61: 29-36. ; Karsten et al. 1990Karsten U, King RJ, Kirst GO. 1990. The distribution of D-sorbitol and D-dulcitol in the red algal genera Bostrychia and Stictosiphonia (Rhodomelaceae, Rhodophyta) - a re-evaluation. British Phycological Journal 25: 363-366. ; Karsten et al. 1992Karsten U, West JA, Zuccarello G. 1992. Polyol Content of Bostrychia and Stictosiphonia (Rhodomelaceae, Rhodophyta) from Field and Culture. Botanica Marina 35: 11-20. ; Karsten et al. 1993Karsten U, West JA, Ganesan EK. 1993. Comparative physiological ecology of Bostrychia moritziana (Ceramiales, Rhodophyta) from freshwater and marine habitats. Phycologia 32: 401-409.; Karsten et al. 1994aKarsten U, Koch S, West JA, Kirst GO. 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.; bKarsten U, West JA, Zuccarello G, Kirst GO. 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 et al. 1996Karsten U, Mostaert AS, King RJ, Kamiya M, Hara Y. 1996. Osmoprotectors in some species of Japanese mangrove macroalgae. Phycological Research 44: 109-112.). However, effects of increasing temperature on Bostrychia species have still not been well investigated (e.g.Davis & Dawis 1981Davis MA, Dawes CJ. 1981. Seasonal photosynthetic and respiratory responses of the intertidal red alga, Bostrychia binderi Harvey (Rhodophyta, Ceramiales) from a mangrove swamp and a salt marsh. Phycologia 20: 165-173.; Mann & Steinke 1988Mann FD, Steinke TD. 1988. Photosynthetic and respiratory responses of the mangrove-associated red algae, Bostrychia radicans and Caloglossa leprieurii. South African Journal of Botany 54: 203-207. ) and more current studies have investigated physiological responses of Bostrychia species under different light conditions (Cunha & Duarte 2002Cunha SR, Duarte NR. 2002. Taxas fotossintéticas e respiratórias de macroalgas do gênero Bostrychia. Notas técnicas Facimar 6: 103-110.; Pedro et al. 2014Pedro RS, Niell FX, Carmona R. 2014. Understanding the intertidal zonation of two macroalgae from ex situ photoacclimation responses. European Journal of Phycology 49: 37-41. ; Pedro et al. 2016Pedro RS, Karsten U, Niell FX, Carmona R. 2016. Intraspecific phenotypic variation in two estuarine rhodophytes across their intertidal zonation. Marine Biology 163: 221. doi: 10.1007/s00227-016-2997-5
https://doi.org/10.1007/s00227-016-2997-...
) and their mechanisms of inorganic carbon acquisition (Ruiz-Nieto et al. 2014Ruiz-Nieto M, Fernández JA, Niell FX, Carmona R. 2014. Mechanisms of inorganic carbon acquisition in two estuarine Rhodophyceans: Bostrychia scorpioides (Hudson) ex Kützing Montagne and Catenella caespitosa (Withering) L. M. Irvine. Photosynthesis Research 121: 277-284. ). Ryder et al. (1999Ryder K, West J, Nicholls D. 1999. Effects of initial enrichment of nitrogen and phosphorus on Bostrychia and Caloglossa (Ceramiales, Rhodophyta) growth using digital imaging. Phycological Research 47: 39-51. ) analyzed the growth of Bostrychia moritiziana in various N and P conditions, showing that non-enriched treatments by nitrogen resulted in the lowest growth.

Such studies with Bostrychia species investigated the effects of the abiotic variables independently, and the interactive effects of abiotic variables on Bostrychia species are poorly understood. Muangmai et al. (2015Muangmai N, Preuss M, Zuccarello GC. 2015. Comparative physiological studies on the growth of cryptic species of Bostrychia intricata (Rhodomelaceae, Rhodophyta) in various salinity and temperature conditions. Phycological Research 63: 300-306. ) had a two-factor approach, investigating the growth of cryptic species of Bostrychia intricata in various salinity and temperature conditions, nevertheless, it had a mainly taxonomic purpose. Ecological impacts of global change are generated by multiple synchronous or asynchronous drivers which interact with each other (Al-Janabi et al. 2019Al-Janabi B, Wahl M, Karsten U, et al. 2019. Sensitivities to global change drivers may correlate positively or negatively in a foundational marine macroalga. Scientific Reports 9: 1-10. ) and recent reviews have highlighted the need for global change research to consider how stressors may interact and affect species (Rich et al. 2018Rich WA, Schubert N, Schläpfer N, et al. 2018. Physiological and biochemical responses of a coralline alga and a sea urchin to climate change: Implications for herbivory. Marine Environmental Research 142: 100-107. ). Field evidence is essential to assess the consequences of global change on macroalgae, but finding a solid causal link often requires obtaining additional information under controlled laboratory conditions (Piñeiro-Corbeira et al. 2018Piñeiro-Corbeira C, Barreiro R, Cremades J, Arenas F. 2018. Seaweed assemblages under a climate change scenario: Functional responses to temperature of eight intertidal seaweeds match recent abundance shifts. Scientific reports 8: 1-9. ).

Growth experiments of Bostrychia species in the laboratory under controlled conditions that simulate ocean warming and eutrophication can elucidate the possible effects of these global changes on their growth, because the physiological effects caused by the environmental stressors affect algal growth (Gouvêa et al. 2017Gouvêa LP, Schubert N, Martins CDL, et al. 2017. Interactive effects of marine heatwaves and eutrophication on the ecophysiology of a widespread and ecologically important macroalga. Limnology and Oceanography 62: 2056-2075.). Experiments with estuarine organisms that consider various salinity conditions are relevant because the salinity varies naturally in estuaries. Lourenço et al. (2006Lourenço SO, Barbarino E, Nascimento A, et al. 2006. Tissue nitrogen and phosphorus in seaweeds in a tropical eutrophic environment: What a long-term study tells us. Journal of Applied Phycology 18: 389-398. ) evaluated the tissue N and P in macroalgae from a tropical eutrophic environment and found high percentages of these in Bostrychia radicans. For these authors macroalgae function very well as monitors of environmental changes and experimental data are needed to identify the environmental processes that promote changes in macroalgae.

In this context, we analyzed the growth of Bostrychia binderi and Bostrychia montagnei cultivated in three independent multifactorial experiments under three water temperature conditions: average winter temperature, average summer temperature and a warming scenario (RCP8.5) projected by the IPCC until the end of the 21st century combined with various salinity (five values) and nutrient (four levels) conditions. We hypothesized that (1) the analyzed species would have highest growth in high nutrient availability, low salinities and temperature, (2) the species would have the lowest growth under a warming scenario (RCP8.5), showing that future ocean warming conditions can negatively affect the species. This study is the first to evaluate the growth of Bostrychia species in a context of global change.

Materials and methods

Algal collection, establishment and maintenance of cultures

The adult thalli of B. binderi and B. montagnei were collected from the mangrove swamp within the Barra do Rio Mamanguape Environmental Protection Area of, northeastern Brazil, in August 2016 (last winter month/rainy month) and February 2017 (last summer month/dry month) (CPTEC/INPE 2016CPTEC/INPE. 2016. Centro de Previsão de Tempo e Estudos Climáticos/Instituto Nacional de Pesquisas Espaciais. https://clima1.cptec.inpe.br/estacoes/#. 15 May. 2020.
https://clima1.cptec.inpe.br/estacoes/#...
). Specimens collected in August 2016 were submitted to the first experiment (with average winter temperature), and specimens collected in February 2017 were submitted to the second (with average summer temperature) and third experiment [a warming scenario - RCP8.5 - projected by the IPCC (2014)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 In: Core Writing Team, Pachauri PK, Meyer A. (eds.) IPCC, Geneva, Switzerland. p. 1-151. until the end of the 21st century]. More details about set temperatures are provided below. The collection point (6°46'23.24" S, 34°56'20.55" W) was established near the estuary’s mouth because mainly the downstream estuarine populations will be impacted by future ocean warming conditions and sea level rise.

Voucher specimens were deposited in the Lauro Pires Xavier Herbarium (Universidade Federal da Paraíba, Brazil) with the accession numbers JPB 63215 for B. binderi and JPB 63216 for B. montagnei. The Lauro Pires Xavier Herbarium is registered in the Index Herbariorum with acronym JPB.

During the field collections, most of the estuarine sediment was removed from the thalli with estuary water. In the laboratory, the remaining sediment adhered to the thalli was removed by washing and spraying them with sterilized seawater and the associated macrofauna individuals were removed with tweezers under a stereoscopic microscope. The thalli were immersed in liquid detergent based on 5 % sulfonic acid (w/w) for 60 seconds, afterwards the detergent was completely removed from the thalli by several washings with sterilized seawater. The thalli were then immersed in sodium hypochlorite (0.2 % active chlorine L-1 of deionized water) for two minutes, which was completely removed from the thalli with sterilized seawater. These procedures were performed following Borburema (2017)Borburema HDS 2017. Mudanças ambientais globais, efeitos da variação de temperatura, salinidade e nutrientes sobre o crescimento de espécies de Bostrychia (Rhodophyta). MSc Thesis, Universidade Federal da Paraíba, Rio Tinto. to eliminate contaminating organisms.

The seawater used in all procedures and growth experiments was sterilized through filtering using cellulose membrane filters (Millipore® HAWP 0.45 µm pore), followed by heating in a laboratory drying oven at 90 ºC for two hours (after cooling, it was heated up again).

In the laboratory, macroalgae (+ 1 g L-1) were maintained in aquariums containing sterilized seawater (35 PSU + 1) enriched with von Stosch’s solution (VSES) (8 mL L-1), which was prepared as described by Edwards (1970Edwards P. 1970. Illustrated guide to the seaweeds and seagrass in the vicinity of Porto Aransas, Texas. Contributions to Marine Science, Austin, University of Texas.) and modified by reducing vitamin concentrations by 50 % (Yokoya 2000Yokoya NS. 2000. Apical callus formation and plant regeneration controlled by plant growth regulators on axenic culture of the red alga Gracilariopsis tenuifrons (Gracilariales, Rhodophyta). Phycological Research 48:133-142.). The culture medium was continuously aerated and replaced weekly for nutrient renovation, water temperature was maintained at 24 °C (± 0.5) (Karsten & Kirst 1989Karsten U, Kirst GO. 1989a. The effect of salinity on growth, photosynthesis and respiration in the estuarine red algaBostrychia radicansMont. Helgoländer Meeresuntersuchungen 43: 61-66.a), photonic flux density at 60 - 80 µmol photons m-2 s-1 (Karsten et al. 1994a Karsten U, Koch S, West JA, Kirst GO. 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.adapted) and the photoperiod was 12 h: 12 h (light: dark cycle).

Growth experiments

For the growth experiments, apical segments (3 - 3.5 cm in primary axis length, weighing 230 mg + 10) with lateral branches were cut from female plant thalli using scalpels under a stereoscopic microscope. Female plants were used in the experiments because they did not release reproductive products that would have interfered with growth measurements in cultures. Sporophytes and male phases usually released reproductive products.

The apical segments of B. binderi and B. montagnei were experimentally cultivated in 150 mL transparent glass containers containing 100 mL of culture medium, which was replaced weekly. Apical segments were cultivated in continuous immersion because highest photosynthetic activity was recorded in Bostrychia sp. under submersed conditions (Peña et al. 1999Peña EJ, Zingmark R, Nietch C. 1999. Comparative photosynthesis of two species of intertidal epiphytic macroalgae on mangrove roots during submersion and emersion. Journal of Phycology 35: 1206-1214. ). This was considered due to the tidal regime in estuarine ecosystems. Growth experiments were performed in an environmental control chamber through three independent multifactorial experiments. All experiments were carried out for 28 days (Karsten et al. 2000Karsten U, Sawall T, West J, Wiencke C. 2000. Ultraviolet sunscreen compounds in epiphytic red algae from mangroves. Hydrobiologia 1: 159-171. ; Muangmai et al. 2015Muangmai N, Preuss M, Zuccarello GC. 2015. Comparative physiological studies on the growth of cryptic species of Bostrychia intricata (Rhodomelaceae, Rhodophyta) in various salinity and temperature conditions. Phycological Research 63: 300-306. ). Each experiment had 40 treatments (two species x one temperature x five salinities x four nutrient levels) and each treatment had five replicas. The water temperature of each experiment was 25, 28 and 32 °C (+ 0.5) combined with various salinity and nutrient conditions (described below). Photoperiod and photonic flux density conditions described above (for maintenance of cultures) were applied in the experiments.

Temperatures

A temperature of 25 °C was established according to the average surface temperature of water during the winter, 28 ºC according to the average surface temperature during the summer, and 32 ºC was the maximum average temperature scenario (RCP.8.5) projected by the IPCC for the marine area near the algal collection site (Tyberghein et al. 2012Tyberghein L, Verbruggen H, Pauly K, et al. 2012. Bio-ORACLE: A global environmental dataset for marine species distribution modelling. Global Ecology and Biogeography 21: 272-281. ; Assis et al. 2018Assis J, Tyberghein L, Bosch S, et al. 2018. Bio-ORACLE v2.0: Extending marine data layers for bioclimatic modelling. Global Ecology and Biogeography 27: 277-284. ). Temperatures of 25 and 28 ºC were established with reference to the area where the macroalgae were collected, based on temperature data (NSST - Night Sea Surface Temperature) from a ten-year temporal series (monthly averages, January 2007 - December 2016). Temperature data were obtained by the MODIS (Moderate Resolution Imaging Spectroradiometer) sensor coupled to the AQUA satellite from the NASA. NSST data were used to prevent major errors in relation to solar reflectance and discrepancies in SST (Sea Surface Temperature) values for the region (Telles & Delcourt 2015Telles FS, Delcourt FT. 2015. Variação espaço-temporal da clorofila-a e temperatura superficial do mar na Bacia de Campos (RJ). Anaiz XVII Simpósio Bras Sensoriamento Remoto - SBSR 6014-6021. http://marte2.sid.inpe.br/attachment.cgi/sid.inpe.br/marte2/2015/06.15.16.06.13/doc/p1239.pdf .
http://marte2.sid.inpe.br/attachment.cgi...
).

Salinities

Salinities used in each experiment were 18, 24, 30, 36 and 42 PSU. The salinity values were obtained by freezing seawater (35 PSU) and gradually melting it to produce seawater with different salinities. Afterwards, mixtures of seawater with different salinities produced the desired salinities (Yokoya et al. 1999Yokoya NS, Kakita H, Obika H, Kitamura T. 1999b. Effects of environmental factors and plant growth regulators on growth of the red alga Gracilaria vermiculophylla from Shikoku Island, Japan. Hydrobiologia 398: 339-347.b). This salinity range was established according to Campos et al. (2015Campos DMAR, Silva AF, Sales NS, Oliveira REMCC, Pessanha ALM. 2015. Trophic relationships among fish assemblages on a mudflat within a Brazilian Marine protected area. Brazilian Journal of Oceanography 63: 429-442.), who recorded a salinity range between 10 and 42 PSU in the estuary from the Barra do Rio Mamanguape Environmental Protection Area. Salinity was measured with a handheld refractometer.

Nutrients

Sterilized seawater was enriched to obtain different nutrient levels in the experiments by adding VSES. The nutrient levels established were: non-enriched sterilized seawater (N0), sterilized seawater enriched with VSES/2 - 4 mL L-1 (N1), sterilized seawater enriched with VSES - 8 mL L-1 (N2), and sterilized seawater enriched with 2VSES - 16 mL L-1 (N3). VSES corresponds to 8 mL of von Stosch’s solution diluted in 1 L of sterilized seawater (Edwards 1970Edwards P. 1970. Illustrated guide to the seaweeds and seagrass in the vicinity of Porto Aransas, Texas. Contributions to Marine Science, Austin, University of Texas.). Nitrate concentrations at N1, N2 and N3 were around 1.95, 3.9 and 7.8 g L-1, respectively, whereas phosphate concentrations were around 0.15, 0.3 and 0.6 g L-1, respectively.

The concentrations of nitrate, nitrite, phosphate, ammonia and total phosphorous in sterilized seawater used in the experiments were analyzed (n = 3). The dissolved nitrate and nitrite were quantified following the methods proposed by Grasshoff et al. (1983Grasshoff K, Enhardt M, Kremling K. 1983. Methods of Sea Water Analysis. Weinheim, Verlag Chemie.). For dissolved phosphate, the methods suggested by Strickland & Parsons (1972Strickland JDH, Parsons TR. 1972. A pratical handbook of seawater. Canada, Bulletin of the Fisheries Research Board of Canada.) and Grasshoff et al. (1983)Grasshoff K, Enhardt M, Kremling K. 1983. Methods of Sea Water Analysis. Weinheim, Verlag Chemie. were followed. Ammonia concentration was determined using a phenol spectrophotometry method and total phosphorous was determined by the persulphate digestion method (APHA et al. 2005APHA. 2005. Standard methods for the examination of water and wastewater. 21th. edn. Washington, American Public Health Association Washington.). The nutrient concentrations of non-enriched sterilized seawater (N0) are in Table 1.

Table 1
Nutrient concentration in sterilized seawater no enrichment with VS. The values are averages and standard deviations referent to three replicas.

Considering the total-N concentration (mg m-3) in sterilized seawater, the N0 treatments can be categorized as oligotrophic (Hakanson 1994Hakanson L. 1994. A review of effect-dose-sensitivity models for aquatic ecosystems. Internationale Revue der Gesamten Hydrobiologie und Hydrographie 79: 621-667.; Smith et al. 1999Smith VH, Tilman GD, Nekola JC. 1999. Eutrophication: impacts of excess nutrient inputs on freshwater, marine, and terrestrial ecosystems. Environmental Pollution 100: 179-196.). All treatments were performed with sterilized seawater from only one collection.

Growth rate

Apical segments were weighed weekly on an analytical balance when the culture medium was replaced and were gently blotted dry with paper tissue to remove excess water before weighing. At the end of the experiments relative growth rates (RGRs) of the apical segments were estimated following the formula recommended by Yong et al. (2013Yong YS, Yong WTL, Anton A. 2013. Analysis of formulae for determination of seaweed growth rate. Journal of Applied Phycology 25: 1831-1834. ): RGR = [(Wt/Wi)1/t - 1] x 100, where Wt is the fresh weight after t days, Wi is the initial fresh weight, and t is the cultivation period.

Statistical analyses

The following descriptive statistics referent to RGRs were calculated: average, minimum, maximum, standard deviation and error (SD and SE, respectively). The graphic of the average RGRs from the treatments was plotted. RGRs of B. binderi and B. montagnei were compared by a linear model (LM). The effects of the treatments on the RGRs of B. binderi and B. montagnei were assessed using analysis of variance (multifactorial ANOVA) and post hoc Tukey’s tests. The statistical analyses were performed using the R program (4.0.0 version) and the significance value adopted was 5 % (0.05).

Results

Bostrychia binderi had the highest RGR (1.80 % day-1) in the treatment where the apical segments were cultivated at 25 °C, 30 PSU and highest concentration of nutrients (N3), whereas the lowest RGR (0.03 % day-1) was at 32 ºC, 42 PSU and lowest nutrient availability (N0). In treatments without nutrient enrichment (N0) at 28 ºC and 18 PSU, as well as at 32 ºC and 24 PSU, some replicas had no growth.

Bostrychia montagnei showed the highest RGR (2.19 % day-1) in the treatment which was cultivated at 25 °C, 36 PSU and N2 nutrient level. The lowest RGR (0.03 % day-1) was at 32 ºC, 24 PSU and N0. Some replicas of the treatments at 28 ºC: 24 and 36 PSU; 32 ºC: 18, 24, 36 and 42 PSU had no growth, independent of the nutrient level.

Bostrychia montagnei had a higher average RGR (0.83 % day-1 + 0.02 SE) than B. binderi (0.67 % day-1 + 0.02 SE), differing significantly (Fcal = 22.14, p < 0.01). Both species showed higher average RGRs at 25 ºC (B. binderi 1.06 % day-1 + 0.03 SE; B. montagnei 1.21 % day-1 + 0.04 SE) than at 28 ºC (B. binderi 0.51 % day-1 + 0.02 SE; B. montagnei 0.75 % day-1 + 0.04 SE) and 32 ºC (B. binderi 0.43 % day-1 + 0.01 SE; B. montagnei 0.54 % day-1 + 0.03 SE), and were statistically different among the three temperatures (Tab. 2, Fig. 1A-B).

Table 2
Results of the multifactorial ANOVA tests from the growth experiments of B. binderi and B. montagnei cultivated in treatments with temperature (25, 28 and 32 °C), salinity (18, 24, 30, 36 and 42 PSU) and nutrient (N0, N1, N2 and N3) variation. F is referent to the F calculated and df to the degrees of freedom.

Figure 1
RGRs of B. binderi (A) and B. montagnei (B) cultivated in three independent multifactorial growth experiments with temperature (25, 28 and 32 °C), salinity (18, 24, 30, 36 and 42 PSU) and nutrient (N0, N1, N2 and N3) variations. Columns are averages and bars are standard errors of the five replicas. Different letters indicate statistical difference among nutrient levels at the same salinity and temperature.

The salinity variation significantly affected the average RGR of B. binderi and B. montagnei (Tab. 2). B. binderi at 18 PSU had an average RGR of 0.67 % day-1 + 0.16 SE; at 24 PSU 0.59 % day-1 + 0.18 SE; at 30 PSU 0.64 % day-1 + 0.18 SE; at 36 PSU 0.75 % day-1 + 0.15 SE and at 42 PSU 0.72 % day-1 + 0.17 SE. The average RGR at 24 PSU was statistically different from that observed at 36 and 42 PSU and the RGR at 36 PSU was different from 30 PSU (p < 0.01). B. montagnei at 18 PSU showed an average RGR of 0.70 % day-1 + 0.22 SE, at 24 PSU was 0.65 % day-1 + 0.22 SE, at 30 PSU was 0.77 % day-1 + 0.19 SE, at 36 PSU was 0.90 % day-1 + 0.24 SE and at 42 PSU was 0.96 % day-1 + 0.19 SE. For B. montagnei, the average RGR at 24 PSU was statistically different from 36 and 42 PSU and at 30 PSU was different from 42 PSU (p < 0.01). Regarding salinity, the lowest average RGR was found at 24 PSU for both species.

For both species, the lowest average RGRs were found in N0. The average RGR of B. binderi and B. montagnei at N0 was statistically different from the other nutrient levels (N1, N2 and N3) (p < 0.01). The average RGR of B. binderi at N1 was also different from N3. The maximum enrichment resulted in increased growth of B. binderi in most treatments, except that at 25 °C and 36 PSU, 28 °C and 24 PSU, 30 °C and 42 PSU; and at 32 °C and 18 PSU, in which the species showed lower RGRs at N3 than at N2 and/or N1. At 32 °C and 18 PSU, the highest average RGR was at N1 (VSES/2). RGRs observed in the treatments at 25 °C: 18, 24, 30 and 42 PSU; at 28 °C: 18 and 36 PSU; and at 32 °C: 24 - 42 PSU had similar patterns in relation to the nutrient levels (Fig. 1A).

At 25 °C, B. montagnei had the highest average RGRs at intermediate levels of nutrients (N1 and / or N2), decreasing growth at N3, except at 42 PSU. At 28 °C, the species had highest average RGRs at high nutrient availabilities, with no significant decrease in growth at N3. In this temperature there was a noticeable decrease in growth at 36 PSU and N2. At 32 °C, the highest average RGRs were also found at intermediate levels of nutrients, with a decrease in growth at N3 as well (Fig. 1B).

The interaction among temperature, salinity and nutrient showed significant effects (Tab. 2) on the growth of both species. High temperatures (28 and 32 °C), low salinity and oligotrophic conditions (N0) resulted in the lowest growth of B. binderi and B. montagnei (Fig. 1A-B).

Discussion

Data obtained in this study suggest that the growth of B. binderi and B. montagnei could be negatively affected in future warming scenarios since the lowest average RGRs were observed in the warming scenario (32 °C - RCP8.5). Macroalgal growth decreased with increasing temperature (25° > 28 °C > 32 °C). Thermal stress affects metabolic activities and membrane-associated processes. The increasing temperature causes a decrease in enzymatic activity, affects the antioxidant systems by stimulating the production of reactive oxygen species (ROS) (Larkindale et al. 2005Larkindale J, Mishkind M, Vierling E. 2005. Plant responses to high temperature. In: Jenks MA, Hasegawa PM. (eds.) Plant abiotic stress. Oxford, Blackwell Publishing Ltd. p. 100-144.; Bischof & Rautenberger 2012Bischof K, Rautenberger R. 2012. Seaweed responses to environmental stress: Reactive oxygen and antioxidative strategies. In: Wiencke C, Bischof K. (eds.) Seaweed Biology. Berlin, Heidelberg, Springer-Verlag. p. 109-132) and causes changes in resource allocation (e.g. for biosynthesis of antioxidant proteins and detoxifying enzymes) (Collén et al. 2007Collén J, Guisle-Marsollier I, Léger JJ, Boyen C. 2007. Response of the transcriptome of the intertidal red seaweed Chondrus crispus to controlled and natural stresses. New Phytologist 176: 45-55. ; Gouvêa et al. 2017Gouvêa LP, Schubert N, Martins CDL, et al. 2017. Interactive effects of marine heatwaves and eutrophication on the ecophysiology of a widespread and ecologically important macroalga. Limnology and Oceanography 62: 2056-2075.), all of which reduce algal growth (Gouvêa et al. 2017Gouvêa LP, Schubert N, Martins CDL, et al. 2017. Interactive effects of marine heatwaves and eutrophication on the ecophysiology of a widespread and ecologically important macroalga. Limnology and Oceanography 62: 2056-2075.). This result also indicates that female phases of B. binderi and B. montagnei probably grow better in the rainy season. However, field data are need to better understand seasonal effects on the life phases of these species.

For tropical marine macroalgae, lethal and sublethal temperatures have been recorded between 32 °C and 38 °C (Koch et al. 2013Koch M, Bowes G, Ross C, Zhang XH. 2013. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Global Change Biology 19: 103-132. ) (e.g.Miranda et al. 2012Miranda GEC, Yokoya NS, Fujii MT. 2012. Effects of temperature, salinity and irradiance on carposporeling development of Hidropuntia caudata (Gracilariales, Rhodophyta). Revista Brasileira de Farmacognosia 22: 818-824.; Araújo et al. 2014Araújo PG, Ribeiro ALNL, Yokoya NS, Fujii MT. 2014. Temperature and salinity responses of drifting specimens of Kappaphycus alvarezii (Gigartinales, Rhodophyta) farmed on the Brazilian tropical coast. Journal of Applied Phycology 26: 1979-1988. ; Castro & Yokoya 2019 Castro JZ, Yokoya NS. 2019. Growth and biochemical responses of tropical and subtropical strains of Gracilaria domingensis (Gracilariales, Rhodophyta) to temperature and irradiance variations. Journal of Applied Phycology 31: 607-613. ). The maximum temperature tested in this study (32 °C) was not lethal for either species, although their lowest growth was recorded at this temperature. Davis & Dawes (1981Davis MA, Dawes CJ. 1981. Seasonal photosynthetic and respiratory responses of the intertidal red alga, Bostrychia binderi Harvey (Rhodophyta, Ceramiales) from a mangrove swamp and a salt marsh. Phycologia 20: 165-173.) and Mann & Steinke (1988Mann FD, Steinke TD. 1988. Photosynthetic and respiratory responses of the mangrove-associated red algae, Bostrychia radicans and Caloglossa leprieurii. South African Journal of Botany 54: 203-207. ) evaluated photosynthetic and respiratory responses of B. binderi and B. radicans (respectively) under temperature variation (12 to 42 °C and 12 to 37 °C, respectively) in short-term experiments (2 - 3 days) and found that the species had high photosynthetic activity at high temperatures (30 to 42 °C and 32 to 37 °C, respectively). Although the thermal tolerance recorded by these authors should be considered, it is possible that the high photosynthetic activity they recorded was indicative of physiological stress since under stress conditions macroalgae can have the metabolism stimulated to synthesize metabolites associated with cell protection against detrimental environmental factors (Hargrave et al. 2016Hargrave MS, Foggo A, Pessarrodona A, Smale DA. 2016. The effects of warming on the ecophysiology of two co-existing kelp species with contrasting distributions. Oecologia 183: 531-543. ). McCoy et al. (2020McCoy SJ, Santillán-Sarmiento A, Brown MT, Widdicombe S, Wheeler GL. 2020. Photosynthetic response of turf-forming red macroalgae to high CO2 conditions. Journal of Phycology 56: 85-96. ) suggest that increased photosynthetic rates may be a consequence of the energy expenditures related to strong chemical defenses. Nevertheless, biochemical and ecophysiological studies are needed to elucidate the protective strategies of Bostrychia species at high temperatures and to identify their maximum tolerance level.

Both species used in this study tolerated the range of salinities tested, showing highest average RGRs at 36 and 42 PSU. Other ecophysiological studies have shown the euryhaline characteristic of Bostrychia species. Karsten & Kirst (1989Karsten U, Kirst GO. 1989a. The effect of salinity on growth, photosynthesis and respiration in the estuarine red algaBostrychia radicansMont. Helgoländer Meeresuntersuchungen 43: 61-66.a) evaluated the growth of B. radicans in various salinities (9.9 - 37.4) and Karsten et al. (1994a) Karsten U, Koch S, West JA, Kirst GO. 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.evaluated the growth of B. simpliciuscula at salinities of 5 to 70 PSU, observing that increased salinity was accompanied by a decrease in growth rates. In both works, the highest average growth occurred in low salinities (5 - 10) and the temperatures established in these works were 24 and 25 °C, respectively. The results found by these authors differ from those found herein.

However, Karsten et al. (1994Karsten U, West JA, Zuccarello G, Kirst GO. 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.b) evaluated the growth of nine isolates of B. radicans from the eastern coast of the USA, and found different physiological ecotypes in the species in relation to different salinities (5.3, 15, 30, 50 and 70). Six isolates exhibited optimum growth at 30 PSU. Intraspecific (ecotypic differentiation) and interspecific differentiation is important to explain local adaptations to different habitats (Thomas & Kirst 1991Thomas DN, Kirst GO. 1991. Salt tolerance of Ectocarpus siliculosus (Dillw.) Lungb.: comparison of gametophytes, sporophytes isolates of different geographic origin. Botanica Acta 104: 26-36.; Piñeiro-Corbeira et al. 2018Piñeiro-Corbeira C, Barreiro R, Cremades J, Arenas F. 2018. Seaweed assemblages under a climate change scenario: Functional responses to temperature of eight intertidal seaweeds match recent abundance shifts. Scientific reports 8: 1-9. ). The fact that B. binderi and B. montagnei specimens analyzed in this study were collected near the estuary’s mouth could explain the highest average RGRs in high salinities. Aconthophora spicifera, a species that also belongs to Rhodomelaceae, exhibited high tolerance from 25 to 40 PSU, with little changes in its physiology, which favors the occurrence of this species in diverse environments as the supratidal region (Pereira et al. 2017Pereira DT, Simioni C, Filipin EP, et al. 2017. Effects of salinity on the physiology of the red macroalga, Acanthophora spicifera (Rhodophyta, Ceramiales). Acta Botanica Brasilica 31: 555-565. ).

Osmotic acclimation in Bostrychia species has been well documented in the scientific literature. It occurs by increasing the intracellular concentrations of organic osmolytes, D - Sorbitol and D - Dulcitol polyols to maintain Turgor pressure (Karsten & Kirst 1989bKarsten U, Kirst GO. 1989b. Incomplete turgor pressure regulation in the “terrestial” red alga, Bostrychia scorpioides (Huds.) Mont. Plant Science 61: 29-36. ; Karsten et al. 1990Karsten U, King RJ, Kirst GO. 1990. The distribution of D-sorbitol and D-dulcitol in the red algal genera Bostrychia and Stictosiphonia (Rhodomelaceae, Rhodophyta) - a re-evaluation. British Phycological Journal 25: 363-366. ; Karsten et al. 1992Karsten U, West JA, Zuccarello G. 1992. Polyol Content of Bostrychia and Stictosiphonia (Rhodomelaceae, Rhodophyta) from Field and Culture. Botanica Marina 35: 11-20. ; Karsten et al. 1994aKarsten U, Koch S, West JA, Kirst GO. 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.; bKarsten U, West JA, Zuccarello G, Kirst GO. 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 et al. 1996Karsten U, Mostaert AS, King RJ, Kamiya M, Hara Y. 1996. Osmoprotectors in some species of Japanese mangrove macroalgae. Phycological Research 44: 109-112.; Pedro et al. 2016Pedro RS, Karsten U, Niell FX, Carmona R. 2016. Intraspecific phenotypic variation in two estuarine rhodophytes across their intertidal zonation. Marine Biology 163: 221. doi: 10.1007/s00227-016-2997-5
https://doi.org/10.1007/s00227-016-2997-...
). This physiological property of Bostrychia species explains their success in estuarine environments. In future conditions of sea level rise and possible changes in salinity gradients of estuaries, there is a strong possibility that Bostrychia species will adapt because of such physiological property (Duarte et al. 2018Duarte B, Martins I, Rosa R, et al. 2018. Climate change impacts on seagrass meadows and macroalgal forests: An integrative perspective on acclimation and adaptation potential. Frontiers in Marine Science 5. doi: 10.3389/fmars.2018.00190
https://doi.org/10.3389/fmars.2018.00190...
).

In general, B. binderi and B. montagnei tolerated eutrophic levels and had lowest average RGRs at the oligotrophic level (N0), especially in high temperatures (28 and 32 °C), due to interactive effects. B. moritziana showed a similar growth pattern in relation to nutrient levels. Furthermore, this species presented lowest growth in the culture medium without nitrogen enrichment (only sterilized seawater), while at the other three enrichment levels it showed high and similar growth (Ryder et al. 1999Ryder K, West J, Nicholls D. 1999. Effects of initial enrichment of nitrogen and phosphorus on Bostrychia and Caloglossa (Ceramiales, Rhodophyta) growth using digital imaging. Phycological Research 47: 39-51. ). This characteristic of Bostrychia species can be related to the fact that estuaries receive considerable concentrations of nutrients from continental runoff (Hitchcock & Mitrovic 2015Hitchcock JN, Mitrovic SM. 2015. Highs and lows: The effect of differently sized freshwater inflows on estuarine carbon, nitrogen, phosphorus, bacteria and chlorophyll a dynamics. Estuarine, Coastal and Shelf Science 156: 71-82.).

However, in most treatments, B. montagnei showed lower average RGRs at N3 than at N1 and/or N2. Such data suggest that B. montagnei could be more sensitive to hypereutrophic levels than B. binderi. Studies have shown that increasing nutrients can decrease growth of macroalgae (Martins & Yokoya 2010Martins AP, Yokoya NS. 2010. Intraspecific variations in colour morphs of Hypnea musciformis (Rhodophyta) in relation to nitrogen availability. Hoehnea 37: 601-615. ; Faveri et al. 2015Faveri C, Schmidt ÉC, Simioni C, et al. 2015. Effects of eutrophic seawater and temperature on the physiology and morphology of Hypnea musciformis J. V. Lamouroux (Gigartinales, Rhodophyta). Ecotoxicology 24: 1040-1052.; Portugal et al. 2016Portugal AB, Carvalho L, Carneiro PBM, Rossi S, Soares MO. 2016. Increased anthropogenic pressure decreases species richness in tropical intertidal reefs. Marine Environmental Research 120: 44-54. ). High concentrations of ammonium ions in seawater, for example, can cause inhibition of photosynthetic activity and significant variation in chlorophyll a and carotenoid contents (de Faveri et al. 2015Faveri C, Schmidt ÉC, Simioni C, et al. 2015. Effects of eutrophic seawater and temperature on the physiology and morphology of Hypnea musciformis J. V. Lamouroux (Gigartinales, Rhodophyta). Ecotoxicology 24: 1040-1052.). Marinho-Soriano et al. (2006Marinho-Soriano E, Fonseca PC, Carneiro MAA, Moreira WSC. 2006. Seasonal variation in the chemical composition of two tropical seaweeds. Bioresource Technology 97: 2402-2406.) found an inverse relationship between the carbohydrate content and nutrient concentrations in macroalgae. As mentioned above, D-Sorbitol and D-Dulcitol (low molecular weight carbohydrates) are important for osmotic acclimation in Bostrychia species. Detrimental interactive effects of increasing temperature and nutrients were also recorded for the growth of Laurencia catarinensis (Rhodomelaceae) (Gouvêa et al. 2017Gouvêa LP, Schubert N, Martins CDL, et al. 2017. Interactive effects of marine heatwaves and eutrophication on the ecophysiology of a widespread and ecologically important macroalga. Limnology and Oceanography 62: 2056-2075.).

B. binderi at 28 °C: 24 and 30 PSU and at 32 °C: 18 PSU showed a decrease in growth with increasing nutrients, as well as B. montagnei at 28 °C: 36 PSU and N2. In these treatments we observed the proliferation of cyanobacteria and microalgae (mainly diatoms). Usually on the algal surface there are some cyanobacteria, microalgae and bacteria which on ideal conditions proliferate (Fernandes et al. 2011Fernandes DRP, Yokoya NS, Yoneshigue-Valentim Y. 2011. Protocol for seaweed decontamination to isolate unialgal cultures. Revista Brasileira de Farmacognosia 21: 313-316.). These organisms in macroalgae culture medium grow and proliferate faster than macroalgae, competing for nutrients, light and may release substances into the culture medium that inhibit algal growth (Berland et al. 1972Berland BR, Bonin DJ, Maestini ST. 1972. Are some bacteria toxic for marine algae? Marine biology 12: 189-193.).

In conclusion, our study shows that B. binderi and B. montagnei could be negatively affected by future ocean warming conditions, confirming our second hypothesis. Both species showed a broad tolerance to salinity variations, growing better at 36 and 42 PSU, which could be a local adaptation strategy. Due to the species’ tolerance to different salinities, they will likely adapt to future conditions of sea level rise and changes in salinity gradients in estuaries. Oligotrophic waters can negatively affect the growth of the species, especially in high temperatures. Both species showed highest growth at eutrophic levels, probably because estuarine environments are rich in nutrients. However, B. montagnei was more sensitive to eutrophication than B. binderi. Our first hypothesis was not completely confirmed since the highest growth was recorded at high salinities. Interaction analyses of the variables confirmed this observation because high temperatures, low salinities and few nutrients caused the lowest algal growth.

Acknowledgements

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001. We thank Dra. Maria Cristina Basílio Crispim da Silva and the laboratory technician Sérgio Costa de Mello (Universidade Federal da Paraíba) for helping us analyze the nutrients in seawater used in the growth experiments. We thank Dra. Nair Sumie Yokoya (Instituto de Botânica de São Paulo) for the first scientific review of this article.

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Publication Dates

  • Publication in this collection
    22 Mar 2021
  • Date of issue
    Oct-Dec 2020

History

  • Received
    28 June 2020
  • Accepted
    02 Aug 2020
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