Abstract
The brown macroalgae in the order Fucales include foundation species on rocky habitats of temperate regions. This work focused on Fucus guiryi, a recently described species segregated from F. spiralis in a molecular basis. It inhabits the upper intertidal zone from the eastern North Atlantic to the subtropical Canary Islands, where is considered its southern limit. We examined morphology and anatomy of vegetative and reproductive structures of F. guiryi from the Canary Islands. Several distinctive characteristics in habit existed between F. guiryi and other species of the genus distributed northwards, such as length and width of stipe and branches, number of branches, and morphology and number of receptacles. Anatomical features reported here for the first time exhibited subtle differences with temperate F. vesiculosus, F. spiralis and F. serratus. The morphology and arrangement of medulla, cortex and meristoderm were also distinctive for F. guiryi. Mucilage in cellular interstitial spaces constitutes good evidence that explains the presence of F. guiryi at its warmest distribution limit in the Canary Islands.
References
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Barsanti, L. & Gualtieri, P. (2014) Algae. Anatomy, biochemistry, and biotechnology, second edition. CRC Press, Boca Raton, Florida, 362 pp.
Bellgrove, A., McKenzie, P.F., Cameron, H. & Pocklington, J.B. (2017) Restoring rocky intertidal communities: Lessons from a benthic macroalgal ecosystem engineer. Marine Pollution Bulletin 117: 17–27. https://doi.org/10.1016/j.marpolbul.2017.02.012
Bishop, M.J., Fraser, J. & Gribben, P. (2013) Morphological traits and density of foundation species modulate a facilitation cascade in Australian mangroves. Ecology 94: 1927–1936. https://doi.org/10.1890/12-1847.1
Bond, P., Brown, M., Moated, R., Gledhill, M., Hill, S. & Nimmo, M. (1999) Arrested development in Fucus spiralis (Phaeophyceae) germlings exposed to copper. European Journal of Phycology 34: 513–521. https://doi.org/10.1080/09541449910001718871
Børgesen, F. (1926) Marine algae from the Canary Islands especially from Teneriffe and Gran Canaria II. Phaeophyceae. Det Kgl Danske Videnskabernes Selskab Biologiske Meddelelser 6: 1–112.
Brownlee, C. & Berger, F. (1995) Extracellular matrix and pattern in plant embryos: on the lookout for developmental information. Trends in Genetics 11: 344–348. https://doi.org/10.1016/S0168-9525(00)89104-0
Charrier, G., Delzon, S., Domec, J-C., Zhang, L., Delmas, C.E.L., Merlin, I., Corso, D., King, A., Ojeda, H., Ollat, N., Prieto, J., Scholach, T., Skinner, P., van Leeuwen, C. & Gambetta, G.A. (2018) Leaf mortality and a dynamic hydraulic safety margin prevent significant stem embolism in the world’s top wine regions during drought. Science Advances 4: eaao6969.
Colombo, P., Curcio, M.F., Giaccone, G. (1982) Biologia dello sviluppo di un endemismo mediterraneo del genere Cystoseira (Phaeophyceae, Fucales): Cystoseira sedoides C. Agardh. Naturalista Siciliana 6: 81–93.
Coyer, J.A., Peters, A.F., Hoarau, G., Stam, W.T. & Olsen, J.L. (2002) Hybridization of the marine seaweeds, Fucus serratus and Fucus evanescens (Heterokontophyta: Phaeophyceae) in a 100-year-old zone of secondary contact. Proceedings of the Royal Society B: Biological Sciences 269: 1829–1834. https://doi.org/10.1098/rspb.2002.2093
Evert, R.F. (2006) Esau’s Plant Anatomy, 3rd Edition. John Wiley & Sons Inc. Hoboken, New Jersey, U.S.A., 138 pp.
Fries, L. (1984) Induction of plantlets in axenically cultivated rhizoids of Fucus spiralis. Canadian Journal of Botany 62: 1616–1620. https://doi.org/10.1139/b84-216
Gómez Garreta, A., Barcelo Martí, M.C., Ribera Siguán, M.A. & Rull Lluch, J. (2001) Fucales Dumort. In: Gómez Garreta, A. (Ed.) Flora Phycologica Iberica. Vol. 1, Fucales. Universidad de Murcia Press, Murcia, Spain, pp. 19–25
Goodner, B. & Quatrano, R.S. (1993) Fucus embryogenesis: a model to study the establishment of polarity. The Plant Cell 5: 1471–1481. https://doi.org/10.1105/tpc.5.10.1471
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Hayat, M.A. (1993) Stains and cytochemical methods. Plenum Press, New York, 455 pp.
Hillebrand, H. (2004) On the generality of the latitudinal diversity gradient. The American Naturalist 163: 192–211. https://doi.org/10.1086/381004
Jones, C.G., Lawton, J.H. & Shachak, M. (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78: 1946–1957. https://doi.org/10.1890/0012-9658(1997)078[1946:PANEOO]2.0.CO;2
Jueterbock, A., Tyberghein, L., Verbruggen, H., Coyer, J.A., Olsen, J.L. & Hoarau, G. (2013) Climate change impact on seaweed meadow distribution in the North Atlantic rocky intertidal. Ecology and Evolution 3: 1356–1373. https://doi.org/10.1002/ece3.541
Jueterbock, A., Coyer, J.A., Olsen, J.L. & Hoarau, G. (2018) Decadal stability in genetic variation and structure in the intertidal seaweed Fucus serratus (Heterokontophyta: Fucaceae). BMC Evolutionary Biology 18: 94. https://doi.org/10.1186/s12862-018-1213-2
Kerswell, A.P. (2006) Global biodiversity patterns of benthic marine algae. Ecology, 87: 2479–2488. https://doi.org/10.1890/0012-9658(2006)87[2479:GBPOBM]2.0.CO;2
Knight, M. & Parke, M. (1950) A biological study of Fucus vesiculosus L. and F. serratus L. Journal of the Marine Biological Association of the United Kingdom 26: 439–514. https://doi.org/10.1017/S0025315400055454
Kuo, J. (2007) Electron microscopy methods and protocols, 2nd Edition. Humana Press Inc. Totowa, New Jersey, 608 pp.
Leandro, A., Pereira, L. & Gonçalves, A.M. (2019) Diverse applications of marine macroalgae. Marine Drugs 18: 17–32. https://doi.org/10.3390/md18010017
Linnaeus, C. (1753) Species plantarum, exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. Vol. 2. Holmiae: Impensis Laurentii Salvii, Stockholm, pp. 561–1200.
Lourenço, C.R., Zardi, G.I., McQuaid, C.D., Serrão, E.A., Pearson, G.A., Jacinto, R. & Nicastro, K.R. (2016) Upwelling areas as climate change refugia for the distribution and genetic diversity of a marine macroalga. Journal of Biogeography 43: 1595–1607. https://doi.org/10.1111/jbi.12744
Lüning, K. (1990) Seaweeds: their environment, biogeography, and ecophysiology. John Wiley & Sons Inc, New York, U.S.A., 544 pp.
Mabeau, S. & Kloareg, B. (1987) Isolation and analysis of the cell walls of brown algae: Fucus spiralis, F. ceranoides, F. vesiculosus, F. serratus, Bifurcaria bifurcata and Laminaria digitata. Journal of Experimental Botany 38: 1573–1580. https://doi.org/10.1093/jxb/38.9.1573
Malero-Jiménez, I.J., Salvo, A.E., Báez, J.C., Bañares-España, E., Reul, A. & Flores-Moya, A. (2017) North Atlantic oscillation drives the annual occurrence of an isolated, peripheral population of the brown seaweed Fucus guiryi in the Western Mediterranean Sea. PeerJ 5: e4048. https://dx.doi.org/10.7717/peerj.4048
Martínez, B., Afonso-Carrillo, J., Anadón, R., Araújo, R., Arenas, F., Arrontes, J., Bárbara, I., Borja, A., Díez, I., Duarte, L., Fernández, M., García Tasende, M., Gorostiaga, J.M., Juanes, J.A., Peteiro, C., Puente, A., Rico, J.M., Sangil, C., Sansón, M., Tuya, F. & Viejo, R.M. (2015) Regresión de las algas marinas en la costa Atlántica de la Península Ibérica y en las islas Canarias por efecto del cambio climático. Algas, Boletín Informativo de la Sociedad Española de Ficología 49: 5–12.
Moss, B.L. (1950) Studies in the genus Fucus: II. The anatomical structure and chemical composition of receptacles of Fucus vesiculosus from three contrasting habitats. Annals of Botany 14: 395–410. https://doi.org/10.1093/oxfordjournals.aob.a083254
Niell, F.X., Jimenez, C. & Fernandez, J.A. (1987) The forms of Fucus spiralis L. in the Canary Islands: discriminant and canonical analysis applied to define a new form. Botanica Marina 30: 27–32. https://doi.org/10.1515/botm.1987.30.1.27
Orellana, S., Hernández, M. & Sansón, M. (2019) Diversity of Cystoseira sensu lato (Fucales, Phaeophyceae) in the eastern Atlantic and Mediterranean based on morphological and DNA evidence, including Carpodesmia gen. emend. and Treptacantha gen. emend. European Journal of Phycology 54 (3): 447–465. https://doi.org/10.1080/09670262.2019.1590862
Pérez Ruzafa, I.M. (2001) Fucus L. In: Gómez Garreta, A. (Ed.) Flora Phycologica Iberica. Vol. 1, Fucales. Universidad de Murcia Press, Murcia (Spain), pp. 33–61.
Pozharitskaya, O.N., Shikov, A.N., Obluchinskaya, E.D. & Vuorela, H. (2019) The pharmacokinetics of fucoidan after topical application to rats. Marine Drugs 17 (12): 687–696. https://doi.org/10.3390/md17120687
Quatrano, R.S. (1980) Gamete release, fertilization, and embryogenesis in the Fucales. In: Gantt, E. (Ed.) Handbook of phycological methods: developmental and cytological methods. Cambridge University Press, Cambridge, pp. 60–68.
Raimundo, S.C., Avci, U., Hopper, C., Pattathil, S., Hahn, M.G. & Popper, Z.A. (2016) Immunolocalization of cell wall carbohydrate epitopes in seaweeds: presence of land plant epitopes in Fucus vesiculosus L. (Phaeophyceae). Planta 243 (2): 337–354. https://doi.org/10.1007/s00425-015-2412-3
Reyes, J. & Sansón, M. (1999) Estudio fenológico de dos poblaciones de Fucus spiralis en Tenerife, islas Canarias (Fucales, Phaeophyta). Vieraea 27: 53–65.
Riera, R., Sangil, C. & Sansón, M. (2015) Long-term herbarium data reveal the decline of a temperate-water algae at its southern range. Estuarine, Coastal and Shelf Science 165: 159–165. https://doi.org/10.1016/j.ecss.2015.05.008
Rosa, G.P., Barreto, M.C. & Seca, A.M. (2019) Pharmacological effects of Fucus spiralis extracts and phycochemicals: a comprehensive review. Botanica Marina 62 (2): 167–178. https://doi.org/10.1515/bot-2018-0047
Savonitto, G., Alongi, G. & Falace, A. (2019) Reproductive phenology, zygote embryology and germling development of the threatened Carpodesmia barbatula (= Cystoseira barbatula) (Fucales, Phaeophyta) towards its possible restoration. Webbia 74 (2): 317–323. https://doi.org/10.1080/00837792.2019.1692594
Schiel, D.R. (2004) The structure and replenishment of rocky shore intertidal communities and biogeographic comparisons. Journal of Experimental Marine Biology and Ecology 300 (1): 309–342. https://doi.org/10.1016/j.jembe.2004.01.001
Schiel, D.R. & Foster, M.S. (2015) The biology and ecology of giant kelp forests. University of California Press, Oakland, California, U.S.A., 395 pp.
Scott, G.W., Hull, S.L., Hornby, S.E., Hardy, F.G. & Owens, N.J.P. (2001) Phenotypic variation in Fucus spiralis (Phaeophyceae): morphology, chemical phenotype and their relationship to the environment. European Journal of Phycology 36: 43–50. https://doi.org/10.1080/09670260110001735188
Steedman, H.F. (1950) Alcian blue 8GS: a new stain for mucin. The Quarterly Journal of Microscopical Science 91 (4): 477–479. https://doi.org/10.1242/jcs.s3-91.16.477
Vadas, R.L., Johnson, S. & Norton, T.A. (1992) Recruitment and mortality of early post- settlement stages of benthic algae. British Phycological Journal 27: 331–351. https://doi.org/10.1080/00071619200650291
Viejo, R.M., Martínez, B., Arrontes, J., Astudillo, C. & Hernández, L. (2011) Reproductive patterns in central and marginal populations of a large Brown seaweed: drastic changes at the southern range limit. Ecography 34: 75–84. http://dx.doi.org/10.1111/j.1600-0587.2010.06365.x
Voskoboinikov, G.M., Makarov, M.V. & Ryzhik, I.V. (2006) Changes in the composition of photosynthetic pigments and cellular structure of the brown algae Fucus vesiculosus L. and F. serratus L. from the Barents Sea during a prolonged period of darkness. Russian Journal of Marine Biology 32 (1): 20–27. https://doi.org/10.1134/S1063074006010032
Zardi, G.I., Nicastro, K.R., Canovas, F., Ferreira-Costa, J., Serrão, E.A. & Pearson, G.A. (2011) Adaptive traits are maintained on steep selective gradients despite gene flow and hybridization in the intertidal zone. PLoS ONE 6: e19402. https://doi.org/10.1371/journal.pone.0019402
Amico, V., Giaccone, G., Colombo, P., Colonna, P., Mannino, A. & Randazzo, R. (1985) Un nuovo approcio allo studio della sistemática del genere Cystoseira C. Agardh (Phaeophyta, Fucales). Bollettino delle sedute della Accademia Gioenia di Scienze Naturali in Catania 18: 887–986.
Barsanti, L. & Gualtieri, P. (2014) Algae. Anatomy, biochemistry, and biotechnology, second edition. CRC Press, Boca Raton, Florida, 362 pp.
Bellgrove, A., McKenzie, P.F., Cameron, H. & Pocklington, J.B. (2017) Restoring rocky intertidal communities: Lessons from a benthic macroalgal ecosystem engineer. Marine Pollution Bulletin 117: 17–27. https://doi.org/10.1016/j.marpolbul.2017.02.012
Bishop, M.J., Fraser, J. & Gribben, P. (2013) Morphological traits and density of foundation species modulate a facilitation cascade in Australian mangroves. Ecology 94: 1927–1936. https://doi.org/10.1890/12-1847.1
Bond, P., Brown, M., Moated, R., Gledhill, M., Hill, S. & Nimmo, M. (1999) Arrested development in Fucus spiralis (Phaeophyceae) germlings exposed to copper. European Journal of Phycology 34: 513–521. https://doi.org/10.1080/09541449910001718871
Børgesen, F. (1926) Marine algae from the Canary Islands especially from Teneriffe and Gran Canaria II. Phaeophyceae. Det Kgl Danske Videnskabernes Selskab Biologiske Meddelelser 6: 1–112.
Brownlee, C. & Berger, F. (1995) Extracellular matrix and pattern in plant embryos: on the lookout for developmental information. Trends in Genetics 11: 344–348. https://doi.org/10.1016/S0168-9525(00)89104-0
Charrier, G., Delzon, S., Domec, J-C., Zhang, L., Delmas, C.E.L., Merlin, I., Corso, D., King, A., Ojeda, H., Ollat, N., Prieto, J., Scholach, T., Skinner, P., van Leeuwen, C. & Gambetta, G.A. (2018) Leaf mortality and a dynamic hydraulic safety margin prevent significant stem embolism in the world’s top wine regions during drought. Science Advances 4: eaao6969.
Colombo, P., Curcio, M.F., Giaccone, G. (1982) Biologia dello sviluppo di un endemismo mediterraneo del genere Cystoseira (Phaeophyceae, Fucales): Cystoseira sedoides C. Agardh. Naturalista Siciliana 6: 81–93.
Coyer, J.A., Peters, A.F., Hoarau, G., Stam, W.T. & Olsen, J.L. (2002) Hybridization of the marine seaweeds, Fucus serratus and Fucus evanescens (Heterokontophyta: Phaeophyceae) in a 100-year-old zone of secondary contact. Proceedings of the Royal Society B: Biological Sciences 269: 1829–1834. https://doi.org/10.1098/rspb.2002.2093
Evert, R.F. (2006) Esau’s Plant Anatomy, 3rd Edition. John Wiley & Sons Inc. Hoboken, New Jersey, U.S.A., 138 pp.
Fries, L. (1984) Induction of plantlets in axenically cultivated rhizoids of Fucus spiralis. Canadian Journal of Botany 62: 1616–1620. https://doi.org/10.1139/b84-216
Gómez Garreta, A., Barcelo Martí, M.C., Ribera Siguán, M.A. & Rull Lluch, J. (2001) Fucales Dumort. In: Gómez Garreta, A. (Ed.) Flora Phycologica Iberica. Vol. 1, Fucales. Universidad de Murcia Press, Murcia, Spain, pp. 19–25
Goodner, B. & Quatrano, R.S. (1993) Fucus embryogenesis: a model to study the establishment of polarity. The Plant Cell 5: 1471–1481. https://doi.org/10.1105/tpc.5.10.1471
Guiry, M.D. & Guiry, G.M. (2021) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from: https://www.algaebase.org (Accessed 13 June 2021).
Hayat, M.A. (1993) Stains and cytochemical methods. Plenum Press, New York, 455 pp.
Hillebrand, H. (2004) On the generality of the latitudinal diversity gradient. The American Naturalist 163: 192–211. https://doi.org/10.1086/381004
Jones, C.G., Lawton, J.H. & Shachak, M. (1997) Positive and negative effects of organisms as physical ecosystem engineers. Ecology 78: 1946–1957. https://doi.org/10.1890/0012-9658(1997)078[1946:PANEOO]2.0.CO;2
Jueterbock, A., Tyberghein, L., Verbruggen, H., Coyer, J.A., Olsen, J.L. & Hoarau, G. (2013) Climate change impact on seaweed meadow distribution in the North Atlantic rocky intertidal. Ecology and Evolution 3: 1356–1373. https://doi.org/10.1002/ece3.541
Jueterbock, A., Coyer, J.A., Olsen, J.L. & Hoarau, G. (2018) Decadal stability in genetic variation and structure in the intertidal seaweed Fucus serratus (Heterokontophyta: Fucaceae). BMC Evolutionary Biology 18: 94. https://doi.org/10.1186/s12862-018-1213-2
Kerswell, A.P. (2006) Global biodiversity patterns of benthic marine algae. Ecology, 87: 2479–2488. https://doi.org/10.1890/0012-9658(2006)87[2479:GBPOBM]2.0.CO;2
Knight, M. & Parke, M. (1950) A biological study of Fucus vesiculosus L. and F. serratus L. Journal of the Marine Biological Association of the United Kingdom 26: 439–514. https://doi.org/10.1017/S0025315400055454
Kuo, J. (2007) Electron microscopy methods and protocols, 2nd Edition. Humana Press Inc. Totowa, New Jersey, 608 pp.
Leandro, A., Pereira, L. & Gonçalves, A.M. (2019) Diverse applications of marine macroalgae. Marine Drugs 18: 17–32. https://doi.org/10.3390/md18010017
Linnaeus, C. (1753) Species plantarum, exhibentes plantas rite cognitas, ad genera relatas, cum differentiis specificis, nominibus trivialibus, synonymis selectis, locis natalibus, secundum systema sexuale digestas. Vol. 2. Holmiae: Impensis Laurentii Salvii, Stockholm, pp. 561–1200.
Lourenço, C.R., Zardi, G.I., McQuaid, C.D., Serrão, E.A., Pearson, G.A., Jacinto, R. & Nicastro, K.R. (2016) Upwelling areas as climate change refugia for the distribution and genetic diversity of a marine macroalga. Journal of Biogeography 43: 1595–1607. https://doi.org/10.1111/jbi.12744
Lüning, K. (1990) Seaweeds: their environment, biogeography, and ecophysiology. John Wiley & Sons Inc, New York, U.S.A., 544 pp.
Mabeau, S. & Kloareg, B. (1987) Isolation and analysis of the cell walls of brown algae: Fucus spiralis, F. ceranoides, F. vesiculosus, F. serratus, Bifurcaria bifurcata and Laminaria digitata. Journal of Experimental Botany 38: 1573–1580. https://doi.org/10.1093/jxb/38.9.1573
Malero-Jiménez, I.J., Salvo, A.E., Báez, J.C., Bañares-España, E., Reul, A. & Flores-Moya, A. (2017) North Atlantic oscillation drives the annual occurrence of an isolated, peripheral population of the brown seaweed Fucus guiryi in the Western Mediterranean Sea. PeerJ 5: e4048. https://dx.doi.org/10.7717/peerj.4048
Martínez, B., Afonso-Carrillo, J., Anadón, R., Araújo, R., Arenas, F., Arrontes, J., Bárbara, I., Borja, A., Díez, I., Duarte, L., Fernández, M., García Tasende, M., Gorostiaga, J.M., Juanes, J.A., Peteiro, C., Puente, A., Rico, J.M., Sangil, C., Sansón, M., Tuya, F. & Viejo, R.M. (2015) Regresión de las algas marinas en la costa Atlántica de la Península Ibérica y en las islas Canarias por efecto del cambio climático. Algas, Boletín Informativo de la Sociedad Española de Ficología 49: 5–12.
Moss, B.L. (1950) Studies in the genus Fucus: II. The anatomical structure and chemical composition of receptacles of Fucus vesiculosus from three contrasting habitats. Annals of Botany 14: 395–410. https://doi.org/10.1093/oxfordjournals.aob.a083254
Niell, F.X., Jimenez, C. & Fernandez, J.A. (1987) The forms of Fucus spiralis L. in the Canary Islands: discriminant and canonical analysis applied to define a new form. Botanica Marina 30: 27–32. https://doi.org/10.1515/botm.1987.30.1.27
Orellana, S., Hernández, M. & Sansón, M. (2019) Diversity of Cystoseira sensu lato (Fucales, Phaeophyceae) in the eastern Atlantic and Mediterranean based on morphological and DNA evidence, including Carpodesmia gen. emend. and Treptacantha gen. emend. European Journal of Phycology 54 (3): 447–465. https://doi.org/10.1080/09670262.2019.1590862
Pérez Ruzafa, I.M. (2001) Fucus L. In: Gómez Garreta, A. (Ed.) Flora Phycologica Iberica. Vol. 1, Fucales. Universidad de Murcia Press, Murcia (Spain), pp. 33–61.
Pozharitskaya, O.N., Shikov, A.N., Obluchinskaya, E.D. & Vuorela, H. (2019) The pharmacokinetics of fucoidan after topical application to rats. Marine Drugs 17 (12): 687–696. https://doi.org/10.3390/md17120687
Quatrano, R.S. (1980) Gamete release, fertilization, and embryogenesis in the Fucales. In: Gantt, E. (Ed.) Handbook of phycological methods: developmental and cytological methods. Cambridge University Press, Cambridge, pp. 60–68.
Raimundo, S.C., Avci, U., Hopper, C., Pattathil, S., Hahn, M.G. & Popper, Z.A. (2016) Immunolocalization of cell wall carbohydrate epitopes in seaweeds: presence of land plant epitopes in Fucus vesiculosus L. (Phaeophyceae). Planta 243 (2): 337–354. https://doi.org/10.1007/s00425-015-2412-3
Reyes, J. & Sansón, M. (1999) Estudio fenológico de dos poblaciones de Fucus spiralis en Tenerife, islas Canarias (Fucales, Phaeophyta). Vieraea 27: 53–65.
Riera, R., Sangil, C. & Sansón, M. (2015) Long-term herbarium data reveal the decline of a temperate-water algae at its southern range. Estuarine, Coastal and Shelf Science 165: 159–165. https://doi.org/10.1016/j.ecss.2015.05.008
Rosa, G.P., Barreto, M.C. & Seca, A.M. (2019) Pharmacological effects of Fucus spiralis extracts and phycochemicals: a comprehensive review. Botanica Marina 62 (2): 167–178. https://doi.org/10.1515/bot-2018-0047
Savonitto, G., Alongi, G. & Falace, A. (2019) Reproductive phenology, zygote embryology and germling development of the threatened Carpodesmia barbatula (= Cystoseira barbatula) (Fucales, Phaeophyta) towards its possible restoration. Webbia 74 (2): 317–323. https://doi.org/10.1080/00837792.2019.1692594
Schiel, D.R. (2004) The structure and replenishment of rocky shore intertidal communities and biogeographic comparisons. Journal of Experimental Marine Biology and Ecology 300 (1): 309–342. https://doi.org/10.1016/j.jembe.2004.01.001
Schiel, D.R. & Foster, M.S. (2015) The biology and ecology of giant kelp forests. University of California Press, Oakland, California, U.S.A., 395 pp.
Scott, G.W., Hull, S.L., Hornby, S.E., Hardy, F.G. & Owens, N.J.P. (2001) Phenotypic variation in Fucus spiralis (Phaeophyceae): morphology, chemical phenotype and their relationship to the environment. European Journal of Phycology 36: 43–50. https://doi.org/10.1080/09670260110001735188
Steedman, H.F. (1950) Alcian blue 8GS: a new stain for mucin. The Quarterly Journal of Microscopical Science 91 (4): 477–479. https://doi.org/10.1242/jcs.s3-91.16.477
Vadas, R.L., Johnson, S. & Norton, T.A. (1992) Recruitment and mortality of early post- settlement stages of benthic algae. British Phycological Journal 27: 331–351. https://doi.org/10.1080/00071619200650291
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Voskoboinikov, G.M., Makarov, M.V. & Ryzhik, I.V. (2006) Changes in the composition of photosynthetic pigments and cellular structure of the brown algae Fucus vesiculosus L. and F. serratus L. from the Barents Sea during a prolonged period of darkness. Russian Journal of Marine Biology 32 (1): 20–27. https://doi.org/10.1134/S1063074006010032
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