Physiology of maerl algae: Comparison of inter- and intraspecies variations.
calcification
coralline algae
environmental conditions
field experiment
photosynthesis
physiology
plasticity
rhodoliths
Journal
Journal of phycology
ISSN: 1529-8817
Titre abrégé: J Phycol
Pays: United States
ID NLM: 9882935
Informations de publication
Date de publication:
06 2021
06 2021
Historique:
revised:
09
10
2020
received:
17
07
2020
accepted:
08
11
2020
pubmed:
15
12
2020
medline:
2
7
2021
entrez:
14
12
2020
Statut:
ppublish
Résumé
Free-living red coralline algae play an important role in the carbon and carbonate cycles of coastal environments. In this study, we examined the physiology of free-living coralline algae-forming maerl beds in the Bay of Brest (Brittany, France), where Lithothamnion corallioides is the dominant maerl (i.e., rhodolith) species. Phymatolithon calcareum and Lithophyllum incrustans are also present (in lower abundances) at a specific site in the bay. We aimed to assess how maerl physiology is affected by seasonality and/or local environmental variations at the inter- and intraspecific levels. Physiological measurements (respiration, photosynthetic, and calcification rates) were performed using incubation chambers in winter and summer to compare (1) the dominant maerl species at three sites and (2) three coexisting maerl species at one site. Comparison of the three coexisting maerl species suggests that L. corallioides is the best adapted to the current environmental conditions in the Bay of Brest, because this species is the most robust to dissolution in the dark in winter and has the highest calcification efficiency in the light. Comparisons of L. corallioides metabolic rates between stations showed that morphological variations within this species are the main factor affecting its photosynthetic and calcification rates. Environmental factors such as freshwater inputs also affect its calcification rates in the dark. In addition to interspecies variation in maerl physiology, there were intraspecific variations associated with direct (water physico-chemistry) or indirect (morphology) local environmental conditions. This study demonstrates the plasticity of maerl physiology in response to environmental changes, which is fundamental for maerl persistence.
Substances chimiques
Carbonates
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
831-848Informations de copyright
© 2021 Phycological Society of America.
Références
Adey, W. H. & McKibbin, D. L. 1970. Studies on the maerl species Phymatolithon calcareum (Pallas) nov. comb. and Lithothamnium corallioides (Crouan) in the Ria de Vigo. Bot. Mar. 13:100-6.
Amado-Filho, G. M., Moura, R. L., Bastos, A. C., Salgado, L. T., Sumida, P. Y., Guth, A. Z., Francini-Filho, R. B. et al. 2012. Rhodolith beds are major CaCO3 bio-factories in the tropical South West Atlantic. PLoS ONE 7:e35171.
Aminot, A. & Kérouel, R. 2007. Dosage automatique des nutriments dans les eaux marines: méthodes en flux continu. Méthodes d’analyse en milieu marin. IFREMER-QUAE GIE, France. 188 pp.
Atkin, O. K., Bruhn, D., Hurry, V. M. & Tjoelker, M. G. 2005. The hot and the cold: unravelling the variable response of plant respiration to temperature. Funct. Plant Biol. 32:87-105.
Basso, D. & Granier, B. 2012. Calcareous algae in changing environments. Geodiversitas 34:5-11.
BIOMAERL Team. 1998. Maerl grounds: habitats of high biodiversity in European waters. In Barthel, K. G., Barth, H., Bohle-Carbonell, M., Fragakis, C., Lipiatou, E., Martin, P., Ollier, G. & Weydert, M. [Eds.] Third European Marine Science and Technology Conference, (Lisbon, Portugal, 23-27 May 1998), vol. 1, Marine Systems. European Commission, Brussels, pp. 170-178.
Birkett, D. A., Maggs, C. A., Dring, M. J., Boaden, P. J. S. & Seed, R. 1998. Infralittoral Reef Biotopes with Kelp Species (volume VII). An overview of dynamic and sensitivity characteristics for conservation management of marine SACs. Scott. Assoc. Mar. Sci. (UK Marine SACs Project) 174 pp.
Blacke, C. & Maggs, C. A. 2003. Comparative growth rates and internal banding periodicity of maerl species (Corallinales, Rhodophyta) from northern Europe. Phycologia 42:606-12.
Borowitza, M. A. & Larkum, A. W. D. 1987. Calcification in algae: Mechanisms and the role of metabolism. Crit. Rev. Plant Sci. 6:1-45.
Bosence, D. W. J. 1976. Ecological studies on two unattached coralline algae from Western Ireland. Palaeontology 19:365-95.
Bosence, D. W. J. 1980. Sedimentary facies, production rates and facies models for recent coralline algal gravels, Co., Galway, Ireland. Geol. J. 15:91-111.
Burdett, H. L., Keddie, V., MacArthur, N., McDowall, L., McLeish, J., Spielvogel, E., Hatton, A. D. & Kamenos, N. A. 2014. Dynamic photo-inhibition exhibited by red coralline algae in the red sea. BMC Plant Biol. 14:139.
Cabioch, J. 1969. Les fonds de maerl de la Baie de Morlaix et leur peuplement vegetal. Cah. Biol. Mar. 9:131-69.
Cavalcanti, G. S., Gregoracci, G. B., dos Santos, E. O., Silveira, C. B., Meirelles, P. M., Longo, L., Gotoh, K. et al. 2014. Physiologic and metagenomic attributes of the rhodoliths forming the largest CaCO3 bed in the South Atlantic Ocean. ISME J. 8:52-62.
Cavalcanti, G. S., Shukla, P., Morris, M., Ribeiro, B., Foley, M., Doane, M. P., Thompson, C. C., Edwards, M. S., Dinsdale, E. A. & Thompson, F. L. 2018. Rhodoliths holobionts in a changing ocean: host-microbes interactions mediate coralline algae resilience under ocean acidification. BMC Genom. 19:701.
Chalker, B. E. 1981. Simulating light-saturation curves for photosynthesis and calcification by reef-building corals. Mar. Biol. 63:135-41.
Chisholm, J. R. M. 2000. Calcification by crustose coralline algae on the northern Great Barrier Reef. Australia. Limnol. Oceanogr. 45:1476-84.
Cyronak, T., Schulz, K. G. & Jokiel, P. L. 2016. The Omega myth: what really drives lower calcification rates in an acidifying ocean. ICES J. Mar. Sci. 73:558-62.
Dickson, A. G. & Millero, F. J. 1987. A comparison of the equilibrium constants for the dissociation of carbonic acid in seawater media. Deep-Sea Res. 34:1733-43.
Dickson, A. G., Sabine, C. L. & Christian, J. R. 2007. Guide to best practices for ocean CO2 measurements PICES special publication 3. North Pacific Marine Science Organization, Sidney, British Columbia, 191 pp.
Edyvean, R. G. J. & Ford, H. 1987. Growth rates of Lithophyllum incrustans (Corallinales, Rhodophyta) from South West Wales. Br. Phycol. J. 22:139-46.
Egilsdottir, H., Olafsson, J. & Martin, S. 2015. Photosynthesis and calcification in the articulated alga Ellisolandia elongate (Corallinales, Rhodophyta) from intertidal rock pools. J. Phycol. 51:59-70.
Esteban, R., Martinez, B., Fernández-Marín, B., Becerril, J. M. & Garcia-Plazaola, J. I. 2009. Carotenoid composition in Rhodophyta: insights into xanthophyll regulation in Corallina elongata. Eur. J. Phycol. 44:221-30.
Fazakerley, H. & Guiry, M. D. 1998. The Distribution of Maerl Beds Around Ireland and Their Potential For Sustainable Extraction: Phycology Section. Report to the Marine Institute Dublin. National University of Ireland, Galway, 34 pp.
Ford, H., Hardy, F. G. & Edyvean, R. G. J. 1983. Population biology of the crustose red alga Lithophyllum incrustans Phil. Three populations on the east coast of Britain. J. Linn. Soc. 23:353-63.
Foster, M. S. 2001. Rhodoliths: Between rocks and soft places. J. Phycol. 37:659-67.
Foster, M. S., Amado-Filho, G., Kamenos, N., Riosmena-Rodriguez, R. & Steller, D. L. 2013. Rhodoliths and rhodolith beds. Smithson. Contrib. Mar. Sci. 39:143-55.
Frantz, J. M. & Bugbee, B. 2005. Acclimation of plant population to shade: Photosynthesis, respiration, and carbon use efficiency. J. Am. Soc. Hortic. Sci. 130:918-27.
Gomez, L. D., Noctor, G., Knight, M. R. & Foyer, C. H. 2004. Regulation of calcium signalling and gene expression by glutathione. J. Exp. Bot. 55:1851-9.
Grall, J. 2002. Biodiversité spécifique et fonctionnelle du maerl: réponses à la variabilité de l'environnement côtier. PhD dissertation, Université de Bretagne Occidentale, 340 pp.
Guillou, M., Grall, J. & Connan, S. 2002. Can low sea urchin densities control macro-epiphytic biomass in a north-east maerl bed ecosystem (Bay of Brest, Brittany, France)? J. Mar. Biol. Assoc. UK 82:867-76.
Heijden, L. H. & Kamenos, N. A. 2015. Reviews and syntheses: Calculating the global contribution of coralline algae to total carbon burial. Biogeosciences 12:6429-41.
Hernández-Kantún, J., Rindi, F., Adey, W. H., Heesch, S., Peña, V., Le Gall, L. & Gabrielson, P. W. 2015. Sequencing type material resolves the identity and distribution of the generitype Lithophyllum incrustans, and related European species L. hibernicum and L. bathyporum (Corallinales, Rhodophyta). J. Phycol. 51:791-807.
Hofmann, L. C. & Heesch, S. 2018. Latitudinal trends in stable isotope signatures and carbon concentrating mechanisms of northeast Atlantic rhodoliths. Biogeosciences 15:6139-49.
Hofmann, L. C., Schoenrock, K. & de Beer, D. 2018. Arctic coralline algae elevate surface pH and carbonate in the dark. Front. Plant Sci. 9:1416.
Hurd, C. L., Harrison, P. J., Bischof, K. & Lobban, C. S. 2014. Seaweed ecology and physiology, 2nd ed. Cambridge University Press, Cambridge, UK, 551 pp.
Kamenos, N. A. & Law, A. 2010. Temperature controls on coralline algal skeletal growth. J. Phycol. 46:331-5.
Kamenos, N. A., Moore, P. G. & Hall-Spencer, J. M. 2004. Nursery-area function of maerl grounds for juvenile queen scallops Aequipecten opercularis and other invertebrates. Mar. Ecol. Prog. Ser. 274:183-9.
Keegan, B. F. 1974. The macrofauna of maerl substrates of the West coast of Ireland. Cah. Biol. Mar. 15:513-30.
Kim, J. H., Lam, S. M. N. & Kim, K. Y. 2013. Photo-acclimation strategies of the temperate coralline alga Corallina officinalis: a perspective on photosynthesis, calcification, photosynthetic pigment contents and growth. Algae 28:355-63.
King, R. J. & Schramm, W. 1982. Calcification in the maerl coralline alga Phymatolithon calcareum: effects of salinity and temperature. Mar. Biol. 70:197-204.
Kirk, J. T. O. 2011. Light and Photosynthesis in Aquatic Ecosystems, 3rd ed. Cambridge University Press, New York, 662 pp.
Le Pape, O., Del Amo, Y., Menesguen, A., Aminot, A., Quéquiner, B. & Tréguer, P. 1996. Resistance of a coastal ecosystem to increasing eutrophic conditions: the Bay of Brest (France), a semi- enclosed zone of Western Europe. Cont. Shelf Res. 16:1885-907.
Lee, E. T. Y. & Bazin, M. J. 1991. Environmental factors influencing photosynthetic efficiency of the micro red alga Porphyridium cruentum (Agardh) Nageli in light-limited cultures. New Phytol. 118:513-9.
Lewis, E. & Wallace, D. W. R. 1998. Program Developed for CO2 System Calculations. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, U.S. Department of Energy, Oak Ridge, Tennessee. https://doi.org/10.3334/CDIAC/otg.CO2SYS_DOS_CDIAC105
Martin, S., Castets, M. D. & Clavier, J. 2006. Primary production, respiration and calcification of the temperate free-living coralline alga Lithothamnion corallioides. Aquat. Bot. 85:121-8.
Martin, S., Charnoz, A. & Gattuso, J. P. 2013. Photosynthesis, respiration and calcification in the Mediterranean crustose coralline alga Lithophyllum cabiochae (Corallinales, Rhodophyta). Eur. Jour. Phycol. 48:163-72.
Martin, S., Clavier, J., Chauvaud, L. & Thouzeau, G. 2007. Community metabolism in temperate maerl beds I. Carbon and carbonate fluxes. Mar. Ecol. Prog. Ser. 335:19-29.
Martin, S., Clavier, J., Guarini, J. M., Chauvaud, L., Hily, C., Grall, J., Thouzeau, G., Jean, F. & Richard, J. 2005. Comparison of Zostera marina and maerl community metabolism. Aquat. Bot. 83:161-74.
Martin, S. & Hall-Spencer, J. M. 2017. Effects of ocean warming and acidification on rhodolith/maerl beds. In Riosmena-Rodriguez, R., Nelson, W. & Aguirre, J. [Eds.] Rhodolith/Maerl Beds: A Global Perspective. Springfield International Publishing, Cham, Switzerland, pp. 87-102.
McCoy, S. J. & Kamenos, N. A. 2015. Coralline algae (Rhodophyta) in a changing world: integrating ecological, physiological, and geochemical responses to global change. J. Phycol. 51:6-24.
Mehrbach, C., Culberson, C. H., Hawley, J. E. & Pytkowicz, R. N. 1973. Measurement of the apparent dissociation constants of carbonic acid in seawater at atmospheric pressure. Limnol. Oceanogr. 18:897-907.
Mendoza, M. L. & Cabioch, J. 1998. Étude comparée de la réproduction de Phymatolithon calcareum (Pallas) Adey & McKibbin et Lithothamnion corallioides (P & H Crouan) P & H Crouan (Corallinales, Rhodophyta), et reconsidérations sur la définition des genres. Can. J. Bot. 76:1433-45.
Nelson, W. A. 2009. Calcified macroalgae - critical to coastal ecosystems and vulnerable to change: a review. Mar. Freshwater Res. 60:787-801.
Ní Longphuirt, S., Clavier, J., Grall, J., Chauvaud, L., Le Loc'h, F., Le Berre, I., Flye-Sainte-Marie, J., Richard, J. & Leynaert, A. 2007. Primary production and spatial distribution of subtidal microphytobenthos in a temperate coastal system, the Bay of Brest, France. Estuar. Coast. Shelf Sci. 74:367-80.
Noisette, F., Egilsdottir, H., Davoult, D. & Martin, S. 2013. Physiological responses of three temperate coralline algae from contrasting habitats to near-future ocean acidification. J. Exp. Mar. Biol. Ecol. 448:179-87.
Pallardy, S. G. 2008. Physiology of Wood Plants, 3rd ed. Elsevier, Burlington, VT, 412 pp.
Pardo, C., Lopez, L., Peña, V., Hernández-Kantún, J., Le Gall, L., Bárbara, I. & Barreiro, R. 2014. A multilocus species delimitation reveals a striking number of species of coralline algae forming maerl in the OSPAR maritime area. PLoS ONE 9:e104073.
Peña, V., Bárbara, I., Grall, J., Maggs, C. A. & Hall-Spencer, J. M. 2014. The diversity of seaweeds on maerl in the NE Atlantic. Mar. Biodivers. 44:533-51.
Potin, P., Floc'h, J. Y., Augris, C. & Cabioch, J. 1990. Annual growth rate of the calcareous red alga Lithothamnion corallioides (Corallinales, Rhodophyta) in the Bay of Brest, France. Hydrobiologia 204:263-7.
Qui-Minet, Z. N., Coudret, J., Davoult, D., Grall, J., Mendez-Sandin, M., Cariou, T. & Martin, S. 2019. Combined effects of global climate change and nutrient enrichment on the physiology of three temperate maerl species. Ecol. Evol. 9:13787-807.
Qui-Minet, Z. N., Delaunay, C., Grall, J., Six, C., Cariou, T., Bohner, O., Legrand, E., Davoult, D. & Martin, S. 2018. The role of local environmental changes on maerl and its associated non-calcareous epiphytic flora in the Bay of Brest. Estuar. Coast. Shelf Sci. 208:140-52.
Raven, J. A. & Beardall, J. 2003. Carbohydrate metabolism and respiration in algae. In Larkum, A. W. D., Douglas, S. E. & Raven, J. A. [Eds.] Photosynthesis in Algae, Advances in Photosynthesis and Respiration. Springer, Netherlands, Dordrecht, pp. 205-224.
Schoenrock, K. M., Bacquet, M., Pearce, D., Rea, B. R., Schofield, J. E., Lea, J., Mair, D. & Kamenos, N. 2018. Influences of salinity on the physiology and distribution of the Arctic coralline algae, Lithothamnion glaciale (Corallinales, Rhodophyta). J. Phycol. 54:690-702.
Schubert, N. & Garcia-Mendoza, E. 2008. Photo-inhibition in red alga species with different carotenoid profiles. J. Phycol. 44:1437-46.
Schubert, N., Garcia-Mendoza, E. & Pacheco-Ruiz, I. 2006. Carotenoid composition of marine red algae. J. Phycol. 42:1208-16.
Schwartz, Y. B., Kahn, T. G. & Pirrotta, V. 2005. Characteristic low density and shear sensitivity of cross-linked chromatin containing polycomb complexes. Mol. Cell. Biol. 25:432-9.
Smith, A. D. & Key, G. S. 1975. Carbon-dioxide and metabolism in marine environments. Limnol. Oceanogr. 20:493-5.
Solorzano, L. 1969. Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol. Oceanog. 14:799-801.
Steneck, R. S. 1986. The ecology of coralline algal crusts - convergent patterns and adaptative strategies. Annu. Rev. Ecol. Syst. 17:273-303.
Steneck, R. S. & Adey, W. H. 1976. The role of environment in control of morphology in Lithophyllum congestum, a Caribbean algal ridge Builder. Bot. Mar. 19:197-216.
Teichert, S. & Freiwald, A. 2014. Polar coralline algal CaCO3-production rates correspond to intensity and duration of the solar radiation. Biogeosciences 11:833-42.
Ursi, S., Pedersén, M., Plastino, E. & Snoeijs, P. 2003. Intraspecific variation of photosynthesis, respiration and photoprotective carotenoids in Gracilaria birdiae (Gracilariales: Rhodophyta). Mar. Biol. 142:997-1007.
Vazquez-Elizondo, R. M. & Enriquez, S. 2017. Light absorption in coralline algae (Rhodophyta): A morphological and functional approach to understanding species distribution in a coral reef lagoon. Front. Mar. Sci. 4:297.
Williamson, C. J., Brodie, J., Goss, B., Yallop, M., Lee, S. & Perkins, R. 2014. Corallina and Ellisolandia (Corallinales, Rhodophyta) photophysiology over daylight tidal emersion: interactions with irradiance, temperature and carbonate chemistry. Mar. Biol. 161:2051-68.
Williamson, C. J., Perkins, R., Voller, M., Yallop, M. L. & Brodie, J. 2017. The regulation of coralline algal physiology, an in situ study of Corallina officinalis (Corallinales, Rhodophyta). Biogeosciences 14:4485-98.
Wilson, S., Blake, C., Berges, J. A. & Maggs, C. A. 2004. Environmental tolerances of free-living coralline algae (maerl): implications for European marine conservation. Biol. Conserv. 120:283-93.