Effect of sand-influence on the morphology of Mazzaella laminarioides (Rhodophyta, Gigartinales) on rocky intertidal shores

Yugreisy Polanco; Ricardo D. Otaíza; Florence Tellier; Karla Pérez-Araneda

doi:10.1515/bot-2022-0076

Article

Effect of sand-influence on the morphology of Mazzaella laminarioides (Rhodophyta, Gigartinales) on rocky intertidal shores

Yugreisy Polanco

Yugreisy Polanco has a M.Sc. in marine ecology from the Faculty of Sciences, Universidad Católica de la Santísima Concepción. Her research expertise is within the field of marine ecology focusing on the morphological variability of red macroalgae.
, Ricardo D. Otaíza

Ricardo D. Otaíza has a Ph.D. in sciences and is an associate professor at the Faculty of Sciences, Universidad Católica de la Santísima Concepción. His research expertise focuses on the life history of marine macroalgae and the factors that determine their distribution and abundance in natural environments. His interests also extend to developing methods for seeding commercially important seaweeds in the natural environments.
, Florence Tellier

Florence Tellier is docteur de l’Université Pierre et Marie Curie (UPMC-Paris VI), France and doctor in biological sciences, ecology mention, Chile. She is an associate professor and dean at the Universidad Católica de la Santísima Concepción. Her research expertise focuses on phylogeny and phylogeography, and on population genetics of marine macroalgae.
and Karla Pérez-Araneda

Karla Pérez-Araneda is a marine biologist and a research assistant at the Faculty of Sciences, Universidad Católica de la Santísima Concepción with expertise in molecular biology.

Published/Copyright: May 15, 2023

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From the journal Botanica Marina Volume 66 Issue 3

Abstract

Morphological variability is common among macroalgae. In central Chile, Mazzaella laminarioides extends throughout the intertidal rocky zones, where blades are reported to grow up to 20 cm in length. Nevertheless, in low rocky intertidal zones with sand-influence, blades are noticeably larger than in other shores without sand effect. The aim of this study was to compare the morphology of M. laminarioides blades from two different conditions. Blades collected from four sites with, and four without, sand-influence were evaluated with traditional morphometry. Results showed that blades were longer and wider in sand-influenced sites. Sand abrasion was not directly evaluated, but indirect effects such as the abundance of bare rock and of sand tolerant species were higher in areas with sand-influence. Also, long blades were restricted to sand-influenced sites, supporting the relation between these two variables. Molecular analyses using the COI marker confirmed large-bladed individuals as M. laminarioides. Results indicated that life cycle phase, seasonality and vertical height were not related to large blades. We suggest that restriction of large blades to sand-influenced sites may be related to the healing processes of basal holdfasts after suffering sand abrasion.

Keywords: blade morphology; morphological variability; regeneration; reproductive phase; rocky intertidal; sand-influence

Corresponding author: Yugreisy Polanco, Departamento de Ecología, Facultad de Ciencias, Universidad Católica de la Santísima Concepción, Alonso de Ribera 2850, 4030000 Concepción, Chile; and Programa de Magíster en Ecología Marina, Universidad Católica de la Santísima Concepción, Alonso de Ribera 2850, 4030000 Concepción, Chile, E-mail: ypolanco@magister.ucsc.cl

About the authors

Yugreisy Polanco

Yugreisy Polanco has a M.Sc. in marine ecology from the Faculty of Sciences, Universidad Católica de la Santísima Concepción. Her research expertise is within the field of marine ecology focusing on the morphological variability of red macroalgae.

Ricardo D. Otaíza

Ricardo D. Otaíza has a Ph.D. in sciences and is an associate professor at the Faculty of Sciences, Universidad Católica de la Santísima Concepción. His research expertise focuses on the life history of marine macroalgae and the factors that determine their distribution and abundance in natural environments. His interests also extend to developing methods for seeding commercially important seaweeds in the natural environments.

Florence Tellier

Florence Tellier is docteur de l’Université Pierre et Marie Curie (UPMC-Paris VI), France and doctor in biological sciences, ecology mention, Chile. She is an associate professor and dean at the Universidad Católica de la Santísima Concepción. Her research expertise focuses on phylogeny and phylogeography, and on population genetics of marine macroalgae.

Karla Pérez-Araneda

Karla Pérez-Araneda is a marine biologist and a research assistant at the Faculty of Sciences, Universidad Católica de la Santísima Concepción with expertise in molecular biology.

Acknowledgments

The authors would like to acknowledge D. Castillo, M. Núñez and L. De Gracia for their help with the fieldwork.

Author contributions: YP: conceptualization, sample collection, methodology, data curation and analysis, interpretation of the results and writing the paper. RO: conceptualization, sample collection, methodology, data curation and analysis, funding acquisition, interpretation of the results and writing the paper. FT: methodology, funding acquisition, review, editing and writing the paper. KPA: molecular analysis methodology.
Research funding: This work was funded by the Programa de Magíster en Ecología Marina and the Centro de Investigación en Biodiversidad y Ambientes Sustentables (CIBAS) of the Universidad Católica de la Santísima Concepción.
Conflict of interest statement: The authors declare that they have no conflicts of interest regarding this article.
Compliance with ethical standards: All procedures were done in compliance with national regulations and ethical standards.

References

Anderson, M.J. (2001). A new method for non-parametric multivariate analysis of variance. Aus. Ecol. 26: 32–46, https://doi.org/10.1111/j.1442-9993.2001.tb00081.x.Search in Google Scholar

Anderson, M.J., Gorley, R.N., and Clarke, K.R. (2008a). Permanova + for primer: guide to software and statistical methods. PRIMER-E, Plymouth, UK.Search in Google Scholar

Anderson, R.J., Anderson, D.R., and Anderson, J.S. (2008b). Survival of sand-burial by seaweeds with crustose bases or life-history stages structures the biotic community on an intertidal rocky shore. Bot. Mar. 51: 10–20, https://doi.org/10.1515/bot.2008.006.Search in Google Scholar

Betancourtt, C., Zapata, J., Latorre, N., Anguita, C., Castañeda, F., Meynard, A., Fierro, C., Espinoza, C., Guajardo, E., Núñez, A., et al.. (2018). Variación espacio-temporal en la composición del ensamble de macroalgas del intermareal rocoso de Maitencillo, Valparaíso, costa central de Chile. Rev. Biol. Mar. Oceanogr. 53: 105–117, https://doi.org/10.4067/s0718-19572018000100105.Search in Google Scholar

Bray, T.L., Neefus, C.D., and Mathieson, A.C. (2006). Morphological and molecular variability of Porphyra purpurea (Roth) C. Agardh (Rhodophyta, Bangiales) from the northwest Atlantic. Nova Hedwigia 82: 1–22, https://doi.org/10.1127/0029-5035/2006/0082-0001.Search in Google Scholar

Brodie, J., Guiry, M.D., and Masuda, M. (1993). Life history morphology and crossability of Chondrus ocellatus forma ocellatus and C. ocellatus forma crispoides from the north-western pacific. Eur. J. Phycol. 28: 183–196, https://doi.org/10.1080/09670269300650281.Search in Google Scholar

Buschmann, A.H., Correa, J.A., Westermeier, R., Hernandez-Gonzalez, M.C., and Norambuena, R. (1999). Mariculture of red algae in Chile. World Aquac. 30: 41–46.Search in Google Scholar

Buschmann, A.H., Väsquez, J.A., Osorio, P., Reyes, E., Filún, L., Hernández-González, M.C., and Vega, A. (2004). The effect of water movement, temperature and salinity on abundance and reproductive of patterns of Macrocystis spp. (Phaeophyta) at different latitudes in Chile. Mar. Biol. 145: 849–862, https://doi.org/10.1007/s00227-004-1393-8.Search in Google Scholar

Calderon, M.S. and Boo, S.M. (2016). Phylogeny of Phyllophoraceae (Rhodophyta, Gigartinales) reveals Asterfilopsis gen. nov. From the southern hemisphere. Phycologia 55: 543–554, https://doi.org/10.2216/16-9.1.Search in Google Scholar

Caro, A.U. and Castilla, J.C. (2004). Predator-inducible defences and local intrapopulation variability of the intertidal mussel Semimytilus algosus in central Chile. Mar. Ecol. Prog. Ser. 276: 115–123, https://doi.org/10.3354/meps276115.Search in Google Scholar

Chopin, T., Bird, C.J., Murphy, C.A., Osborne, J.A., Patwary, M.U., and Floc’h, J.Y. (1996). A molecular investigation of polymorphism in the North Atlantic red alga Chondrus crispus (Gigartinales). Phycol. Res. 44: 69–80, https://doi.org/10.1111/j.1440-1835.1996.tb00378.x.Search in Google Scholar

Clarke, K.R. (1993). Non-parametric multivariate analyses of changes in community structure. Aus. J. Ecol. 18: 117–143, https://doi.org/10.1111/j.1442-9993.1993.tb00438.x.Search in Google Scholar

Clarkston, B.E. and Saunders, G.W. (2010). A comparison of two DNA barcode markers for species discrimination in the red algal family Kallymeniaceae (Gigartinales, Florideophyceae), with a description of Euthora timburtonii sp. nov. Botany 88: 119–131, https://doi.org/10.1139/b09-101.Search in Google Scholar

D’Antonio, C.M. and Gibor, A. (1985). A note on some influences of photon flux density on the morphology of germlings of Gelidium robustum (Gelidiales, Rhodophyta) in culture. Bot. Mar. 28: 313–316, https://doi.org/10.1515/botm.1985.28.7.313.Search in Google Scholar

Daly, A. and Mathieson, A.C. (1977). The effects of sand movement on intertidal seaweeds and selected invertebrates at bound rock, new Hampshire, USA. Mar. Biol. 55: 45–55, https://doi.org/10.1007/bf00392570.Search in Google Scholar

Darriba, D., Taboada, G.L., Doallo, R., and Posada, D. (2012). JModelTest 2: more models, new heuristics and parallel computing. Nat. Methods 9: 772, https://doi.org/10.1038/nmeth.2109.Search in Google Scholar PubMed PubMed Central

Dawson, E., Acleto, C., and Foldvik, N. (1964). The seaweeds of Peru. Nova Hedwigia 13: 1–111.Search in Google Scholar

Díaz-Tapia, P., Bárbara, I., and Díez, I. (2013). Multi-scale spatial variability in intertidal benthic assemblages: differences between sand-free and sand-covered rocky habitats. Estuar. Coast. Shelf. Sci. 133: 97–108, https://doi.org/10.1016/j.ecss.2013.08.019.Search in Google Scholar

Fowler-Walker, M.J., Wernberg, T., and Connell, S.D. (2006). Differences in kelp morphology between wave sheltered and exposed localities: morphologically plastic or fixed traits? Mar. Biol. 148: 755–767, https://doi.org/10.1007/s00227-005-0125-z.Search in Google Scholar

Fraser, C.I., Hay, C.H., Spencer, H.G., and Waters, J.M. (2009). Genetic and morphological analyses of the southern bull kelp Durvillaea antarctica (Phaeophyceae: Durvillaeales) in New Zealand reveal cryptic species. J. Phycol. 45: 436–443, https://doi.org/10.1111/j.1529-8817.2009.00658.x.Search in Google Scholar PubMed

Fuentealba, G. (2006). Diferencias morfológicas entre esporofitos y gametofitos de Mazzaella laminarioides (Bory) Fredericq (Rhodophyta: Gigarttinales) en relación con la abrasión por arena, Marine biology thesis. Concepción, Chile, Universidad Católica de la Santísima Concepción.Search in Google Scholar

Gómez, I. and Westermeier, R.C. (1991). Frond regrowth from basal disc in Iridaea laminarioides (Rhodophyta, Gigartinales) at Mehuin, southern Chile. Mar. Ecol. Prog. Ser. 73: 83–91, https://doi.org/10.3354/meps073083.Search in Google Scholar

Gower, J.C. (1966). Some distance properties of latent root and vector methods used in multivariate analysis. Biometrika 53: 325, https://doi.org/10.1093/biomet/53.3-4.325.Search in Google Scholar

Guiry, M.D., and Guiry, G.M. (2022). AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available at: https://www.algaebase.org (Accessed 28 June 2022).Search in Google Scholar

Gutierrez, L. and Fernández, C. (1992). Water motion and morphology in Chondrus crispus (Rhodophyta). J. Phycol. 28: 156–162, https://doi.org/10.1111/j.0022-3646.1992.00156.x.Search in Google Scholar

Hannach, G. and Santelices, B. (1985). Ecological differences between the isomorphic reproductive phases of two species of Iridaea (Rhodophyta, Gigartinales). Mar. Ecol. Prog. Ser. 22: 291–303, https://doi.org/10.3354/meps022291.Search in Google Scholar

Hannach, G. and Waaland, J.R. (1986). Enviroment, distribution and production of Iridaea. Aquat. Bot. 26: 51–78, https://doi.org/10.1016/0304-3770(86)90005-7.Search in Google Scholar

Hoang, D.T., Chernomor, O., von Haeseler, A., Minh, B.Q., and Vinh, L.S. (2018). UFBoot2: improving the ultrafast bootstrap approximation. Mol. Biol. Evol. 35: 518–522, https://doi.org/10.1093/molbev/msx281.Search in Google Scholar PubMed PubMed Central

Hoffmann, A.J. and Santelices, B. (1997). Flora marina de Chile central. Ediciones Universidad Católica de Chile, Santiago, Chile.Search in Google Scholar

Hommersand, M.H., Guiry, M.D., Fredericq, S., and Leister, G.L. (1993). New perspectives in the taxonomy of the Gigartinaceae (Gigartinales, Rhodophyta). Hydrobiologia 260–261: 105–120, https://doi.org/10.1007/bf00049009.Search in Google Scholar

Howe, M. (1914). The marine algae of Perú. Mem. Torrey Bot. Club 15: 99–102.10.5962/bhl.title.97549Search in Google Scholar

Lewis, R.J. and Lanker, M.D. (2004). Branching pattern of gametophytes and tetrasporophytes of Ceramium codicola (Ceramiales, Rhodophyta) is related to phase and reproductive structures. Phycologia 43: 121–125, https://doi.org/10.2216/i0031-8884-43-2-121.1.Search in Google Scholar

Lindstrom, S.C., Hughey, J.R., and Martone, P.T. (2011). New resurrected and redefined species of Mastocarpus (Phyllophoraceae, Rhodophyta) from the northeast pacific. Phycologia 50: 661–683, https://doi.org/10.2216/10-38.1.Search in Google Scholar

Littler, M., Martz, D., and Littler, D. (1983). Effects of recurrent sand deposition on rocky intertidal organisms: importance of substrate heterogeneity in a fluctuating environment. Mar. Ecol. Prog. Ser. 11: 129–139, https://doi.org/10.3354/meps011129.Search in Google Scholar

Meneses, I. (1992). Morphological variation in three species of the genus Ceramium (Ceramiales, Rhodophyta) from Hawaii: differences between reproductive phases and phenotypic plasticity. Bot. Mar. 35: 461–474, https://doi.org/10.1515/botm.1992.35.6.461.Search in Google Scholar

Montecinos, A., Broitman, B.R., Faugeron, S., Haye, P.A., Tellier, F., and Guillemin, M.L. (2012). Species replacement along a linear coastal habitat: phylogeography and speciation in the red alga Mazzaella laminarioides along the south east pacific. BMC Evol. Biol. 12: 97, https://doi.org/10.1186/1471-2148-12-97.Search in Google Scholar PubMed PubMed Central

Otaíza, R. and Fonseca, F. (2011). Effect of dissolved calcium on the formation of secondary attachment structures in different types of branches of Chondracanthus chamissoi (Rhodophyta, Gigartinales). Rev. Biol. Mar. Oceanogr. 46: 263–268, https://doi.org/10.4067/s0718-19572011000200016.Search in Google Scholar

Pacheco-Ruiz, I., Zertuche, J., and Espinoza-Avalos, J. (2005). The role of secondary attachment discs in the survival of Chondracanthus squarrulosus (Gigartinales, Rhodophyta). Phycologia 44: 629–631, https://doi.org/10.2216/0031-8884(2005)44[629:trosad]2.0.co;2.10.2216/0031-8884(2005)44[629:TROSAD]2.0.CO;2Search in Google Scholar

Parada, G.M., Riosmena-Rodriguez, R., Martinez, E.A., and Hernandez-Carmona, G. (2012). Morphological variability of intertidal Eisenia arborea (Laminariales, Ochrophyta) at Punta Eugenia, Baja California Sur. Algae 27: 109–114, https://doi.org/10.4490/algae.2012.27.2.109.Search in Google Scholar

Perrone, C. and Felicini, G.P. (1972). Sur les bourgeons adventifs de Petroglossum nicaeense (Duby) Schotter (Rhodophycees, Gigartinales) en culture. Phycologia 11: 87–95, https://doi.org/10.2216/i0031-8884-11-1-87.1.Search in Google Scholar

Perrone, C. and Felicini, G.P. (1976). Les bourgeons adventifs de Gigartina acicularis (Wulf.) Lamour. (Rhodophyta , Gigartinales) en culture. Phycologia 15: 45–50, https://doi.org/10.2216/i0031-8884-15-1-45.1.Search in Google Scholar

Perrone, C. and Felicini, G.P. (1993). Morphogenetic effects of daylength in Schottera nicaeensis. Hydrobiologia 260–261: 145–150, https://doi.org/10.1007/bf00049013.Search in Google Scholar

Pinochet, J., Domínguez, J., Neira, E., Rojas, C., Acuña, E., Cancino, J.M., and Brante, A. (2018). Tidal height and sand as potential drivers of the ecological interaction of the two intertidal mussels Perumytilus purpuratus and Semimytilus algosus. Mar. Ecol. 39: 1–8, https://doi.org/10.1111/maec.12503.Search in Google Scholar

Rietema, H. (1995). Ecoclinal variation in Rhodomela confervoides along a salinity gradient in the north sea and Baltic sea. Bot. Mar. 38: 475–479, https://doi.org/10.1515/botm.1995.38.1-6.475.Search in Google Scholar

Rodríguez, C.Y. and Otaíza, R.D. (2018). Factors affecting morphological transformation and secondary attachment of apexes of Chondracanthus chamissoi (Rhodophyta, Gigartinales). J. Appl. Phycol. 30: 1157–1166, https://doi.org/10.1007/s10811-017-1305-1.Search in Google Scholar

Rodríguez, C.Y. and Otaíza, R.D. (2020). Morphological variability in a red seaweed: confirmation of co-occurring f. lessonii and f. chauvinii in Chondracanthus chamissoi (Rhodophyta, Gigartinales). J. Phycol. 56: 469–480, https://doi.org/10.1111/jpy.12955.Search in Google Scholar

Ross, P.J., Donaldson, S.L., and Saunders, G.W. (2003). A molecular investigation of Mazzaella (Gigartinales, Rhodophyta) morphologically intermediate between Mazzaella linearis and M. splendens. Bot. Mar. 46: 202–213.10.1515/BOT.2003.020Search in Google Scholar

Santelices, B. (1989). Algas marinas de Chile: distribución ecología, utilización, biodiversidad. Universidad Católica de Chile, Santiago, Chile.Search in Google Scholar

Santelices, B. (1990). Patterns of organizations of intertidal and shallow subtidal vegetation in wave exposed habitats of central Chile. Hydrobiologia 192: 35–57, https://doi.org/10.1007/bf00006226.Search in Google Scholar

Santelices, B. and Martínez, E. (1997). Hierarchical analysis of reproductive potential in Mazzaella laminarioides (Gigrtinaceae, Rhodophyta). Phycologia 36: 195–207, https://doi.org/10.2216/i0031-8884-36-3-195.1.Search in Google Scholar

Santelices, B. and Norambuena, R. (1987). A harvesting strategy for Iridaea laminarioides in central Chile. Hydrobiologia 151–152: 329–333, https://doi.org/10.1007/bf00046148.Search in Google Scholar

Saunders, G.W. (2005). Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos. Trans. R. Soc. B. Sci. 360: 1879–1888, https://doi.org/10.1098/rstb.2005.1719.Search in Google Scholar PubMed PubMed Central

Shaughnessy, F.J. and DeWreede, R. (2001). Size, survival and the potential for reproduction in transplants of Mazzaella splendens and M. linearis (Rhodophyta). Mar. Ecol. Prog. Ser. 222: 109–118, https://doi.org/10.3354/meps222109.Search in Google Scholar

Shaughnessy, F.J., DeWreede, R.E., and Bell, E.C. (1996). Consequences of morphology and tissue strength to blade survivorship of two closely related Rhodophyta species. Mar. Ecol. Prog. Ser. 136: 257–266, https://doi.org/10.3354/meps136257.Search in Google Scholar

Silva, P.C. and DeCew, T.C. (1992). Ahnfeltiopsis, a new genus in the Phyllophoraceae (Gigartinales, Rhodophyceae). Phycologia 31: 576–580, https://doi.org/10.2216/i0031-8884-31-6-576.1.Search in Google Scholar

Smit, A.J. and Bolton, J.J. (1999). Organismic determinants and their effect on growth and regeneration in Gracilaria gracilis. J. Appl. Phycol. 11: 293–299, https://doi.org/10.1023/a:1008102409472.10.1023/A:1008102409472Search in Google Scholar

Trifinopoulos, J., Nguyen, L.T., von Haeseler, A., and Minh, B.Q. (2016). W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis. Nucleic Acids Res. 44: W232–W235, https://doi.org/10.1093/nar/gkw256.Search in Google Scholar PubMed PubMed Central

Vázquez-Delfín, E., Boo, G.H., Rodríguez, D., Boo, S.M., and Robledo, D. (2016). Hypnea musciformis (Cystocloniaceae) from the Yucatan Peninsula: morphological variability in relation to life-cycle phase. Phycologia 55: 230–242, https://doi.org/10.2216/15-118.1.Search in Google Scholar

Vera, C., Lobos, P., and Romo, H. (2008). Gametophyte-sporophyte coalescence in populations of the intertidal carrageenophyte Mazzaella laminarioides (Rhodophyta). J. Appl. Phycol. 20: 883–887, https://doi.org/10.1007/s10811-007-9238-8.Search in Google Scholar

Vieira, V.M.N.C.S., Engelen, A.H., Huanel, O.R., and Guillemin, M.L. (2021). Differential frond growth in the isomorphic haploid–diploid red seaweed Agarophyton chilense by long-term in situ monitoring. J. Phycol. 57: 592–605, https://doi.org/10.1111/jpy.13110.Search in Google Scholar PubMed PubMed Central

Viviani, C.A. (1979). Ecogeografia del litoral chileno. Stud. Neotrop. Fauna Enviroment 14: 65–123, https://doi.org/10.1080/01650527909360548.Search in Google Scholar

Westermeier, R., Rivera, P.J., Chacana, M., and Gómez, I. (1987). Biological bases for management of Iridaea laminarioides Bory in southern Chile. Hydrobiologia 151–152: 313–328, https://doi.org/10.1007/bf00046147.Search in Google Scholar

Zar, J. (2010). Biostatistical analysis. Pearson Prentice Hall, Upper Saddle River, NJ.Search in Google Scholar

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Received: 2022-12-03

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Keywords for this article

blade morphology; morphological variability; regeneration; reproductive phase; rocky intertidal; sand-influence