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Geometric morphometrics shows a close relationship between the shape features, position on thalli, and CaCO3 content of segments in Halimeda tuna (Bryopsidales, Ulvophyceae)

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Abstract

Calcifying green algae of the genus Halimeda J.V. Lamouroux are typical for the modular thalli composed of serial segments. Their CaCO3 content gradually increases with age due to calcification, the intensity of which is largely linked to photosynthesis. The dynamics of segment phenotypic plasticity at different scales and its relation to CaCO3 content is not well known. We investigated the populations of Halimeda tuna in the upper sublittoral of four regions on the Adriatic Sea coast. Using geometric morphometrics, we explored the patterns of segment shape plasticity, their relationships with the spatial factors and CaCO3 content. The results showed that segment position on thalli was the main determinant of their shape features. This effect was considerably more prominent than the differences among plants, populations, or regions. Likewise, the segment shape proved to be a significant predictor of their CaCO3 content. Segments with inversely conical shapes, typical for the lower parts of branches, contained significantly less CaCO3 than the reniform and oval segments that probably contribute most to the overall carbonate budget of the Mediterranean Halimeda draperies.

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Data availability

Primary data used for the analyses are available online at: http://doi.org/10.5281/zenodo.5504135

Code availability

The R scripts used for the analyses are available online at: http://doi.org/10.5281/zenodo.5504135

References

  • Adams, D. C. & E. Otárola-Castillo, 2013. geomorph: an R package for the collection and analysis of geometric morphometric shape data. Methods in Ecology and Evolution 4: 393–399.

    Article  Google Scholar 

  • Anderson, M. J., 2017. Permutational multivariate analysis of variance (PERMANOVA). In Balakrishnan, N., T. Colton, B. Everitt, W. Piegorsch, F. Ruggeri & J. L. Teugels (eds), Wiley StatsRef: Statistics Reference Online Wile, Oxford: 1–15. https://doi.org/10.1002/9781118445112.stat07841.

    Chapter  Google Scholar 

  • Anderson, M. J. & D. C. I. Walsh, 2013. What null hypothesis are you testing? PERMANOVA, ANOSIM and the Mantel test in the face of heterogenous dispersions. Ecological Monographs 83: 557–574.

    Article  Google Scholar 

  • Ballesteros, E., 1991a. Seasonality of growth and production of a deep-water population of Halimeda tuna (Chlorophyceae, Caulerpales) in the north-western Mediterranean. Botanica Marina 34: 291–301.

    Article  Google Scholar 

  • Ballesteros, E., 1991b. Structure of a deep-water community of Halimeda tuna (Chlorophyceae, Caulerpales) from the North-Western Mediterranean. Collectanea Botanica 20: 5–21.

    Article  Google Scholar 

  • Barry, S. C., T. K. Frazer & C. A. Jacoby, 2013. Production and carbonate dynamics of Halimeda incrassata (Ellis) Lamouroux altered by Thalassia testudinum Banks and Soland ex König. Journal of Experimental Marine Biology and Ecology 444: 73–80.

    Article  CAS  Google Scholar 

  • Bilgin, S. & Ö. O. Ertan, 2002. Selected chemical constituents and their seasonal variations in Flabellia petiolata (Turra) Nizam. and Halimeda tuna (Ellis & Sol.) J.V.Lamour. in the Gulf of Antalya (North-eastern Mediterranean). Turkish Journal of Botany 26: 87–90.

    Google Scholar 

  • Böhm, E. L., 1973. Studies on the mineral content of calcareous algae. Bulletin of Marine Science 23: 177–190.

    Google Scholar 

  • Bonacci, O., D. Bonacci, M. Patekar & M. Pola, 2021. Increasing trends in air and sea surface temperature in the Central Adriatic Sea (Croatia). Journal of Marine Science and Engineering 9: 1–17.

    Article  Google Scholar 

  • Borowitzka, M. A. & A. W. D. Larkum, 1976. Calcification in the green alga Halimeda. II. The exchange of Ca2+ and the occurrence of age gradients in calcification and photosynthesis. Journal of Experimental Botany 27: 864–878.

    Article  CAS  Google Scholar 

  • Borowitzka, M. A. & A. W. D. Larkum, 1987. Calcification in algae: mechanisms and the role of metabolism. Critical Reviews in Plant Sciences 6: 1–45.

    Article  Google Scholar 

  • Canals, M. & E. Ballesteros, 1997. Production of carbonate particles by phytobenthic communities on the Mallorca-Menorca shelf, northwestern Mediterranean Sea. Deep-Sea Research II 44: 611–629.

    Article  CAS  Google Scholar 

  • Cardini, A., K. Seetah & G. Barker, 2015. How many specimens do I need? Sampling error in geometric morphometrics: testing the sensitivity of means and variances in simple randomized selection experiments. Zoomorphology 134: 149–163.

    Article  Google Scholar 

  • Carneiro, P. B. M., J. U. Pereira & H. Matthews-Cascon, 2018. Standing stock variations, growth and CaCO3 production by the calcareous green alga Halimeda opuntia. Journal of the Marine Biological Association of the United Kingdom 98: 401–409.

    Article  CAS  Google Scholar 

  • Davies, P. J., 2011. Halimeda bioherms. In Hopley, D. (ed), Encyclopedia of Modern Coral Reefs Springer, Dordrecht: 539–549.

    Chapter  Google Scholar 

  • Drew, E. A., 1983. Halimeda biomass, growth rates and sediment generation on reefs in the Central Great Barrier Reef Province. Coral Reefs 2: 101–110.

    Article  Google Scholar 

  • Gunz, P. & P. Mitteroecker, 2013. Semilandmarks: a method for quantifying curves and surfaces. Hystrix Italian Journal of Mammalogy 24: 103–109.

    Google Scholar 

  • Habel, K., R. Grasman, R. B. Gramacy, P. Mozharovskyi & D. C. Sterratt, 2019. geometry: mesh generation and surface tessellation. R package version 0.4.5. https://CRAN.R-project.org/package=geometry

  • Hall-Spencer, J. M. & B. P. Harvey, 2019. Ocean acidification impacts on coastal ecosystem services due to habitat degradation. Emerging Topics in Life Sciences 3: 197–206.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammer, Ø., D. A. T. Harper & P. D. Ryan, 2001. PAST: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: 1–9.

    Google Scholar 

  • Hillis, L., 1991. Recent calcified Halimedaceae. In Riding, R. (ed), Calcareous Algae and Stromatolites Springer, Heidelberg: 167–188.

    Chapter  Google Scholar 

  • Hillis-Colinvaux, L., 1980. Ecology and Taxonomy of Halimeda: Primary Producer of Coral Reefs, Academic Press, London:

    Google Scholar 

  • Jensen, P. R., R. A. Gibson, M. M. Littler & D. S. Littler, 1985. Photosynthesis and calcification in four deep-water Halimeda species (Chlorophyceae, Caulerpales). Deep-Sea Research 32: 451–464.

    Article  CAS  Google Scholar 

  • Klingenberg, C. P., M. Barluenga & A. Meyer, 2002. Shape analysis of symmetric structures: quantifying variation among individuals and asymmetry. Evolution 56: 1909–1920.

    Article  PubMed  Google Scholar 

  • Kooistra, W. H. C. F. & H. Verbruggen, 2005. Genetic patterns in the calcified tropical seaweeds Halimeda opuntia, H. distorta, H. hederacea, and H. minima (Bryopsidales, Chlorophyta) provide insights in species boundaries and interoceanic dispersal. Journal of Phycology 41: 177–187.

    Article  CAS  Google Scholar 

  • Llobet, I., J. M. Gili & R. G. Hughes, 1991. Horizontal, vertical and seasonal distributions of epiphytic hydrozoa on the alga Halimeda tuna in the Northwestern Mediterranean Sea. Marine Biology 110: 151–159.

    Article  Google Scholar 

  • McNicholl, C., M. S. Koch & L. C. Hofmann, 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.

    Article  Google Scholar 

  • Mucci, A., 1983. The solubility of calcite and aragonite in seawater at various salinities, temperatures, and one atmosphere total pressure. American Journal of Science 283: 780–799.

    Article  CAS  Google Scholar 

  • Neustupa, J. & Y. Nemcova, 2018. Morphological allometry constrains symmetric shape variation, but not asymmetry, of Halimeda tuna (Bryopsidales, Ulvophyceae) segments. PLoS ONE 13: e0206492.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Neustupa, J. & Y. Nemcova, 2020. Morphometric analysis of surface utricles in Halimeda tuna (Bryopsidales, Ulvophyceae) reveals variation in their size and symmetry within individual segments. Symmetry 12: 1271.

    Article  CAS  Google Scholar 

  • Ortegón-Aznar, I., A. Chuc-Contreras & L. Collado-Vides, 2017. Calcareous green algae standing stock in a tropical sedimentary coast. Journal of Applied Phycology 29: 2685–2693.

    Article  CAS  Google Scholar 

  • Pastor, F., J. A. Valiente & J. L. Palau, 2018. Sea surface temperature in the Mediterranean: trends and spatial patterns (1982–2016). Pure and Applied Geophysics 175: 4017–4029.

    Article  Google Scholar 

  • Peach, K. E., M. S. Koch, P. L. Blackwelder, D. Guerrero-Given & N. Kamasawa, 2017. Primary utricle structure of six Halimeda species and potential relevance for ocean acidification tolerance. Botanica Marina 60: 1–11.

    Article  Google Scholar 

  • Perez, S. I., V. Bernal & P. N. Gonzalez, 2006. Differences between sliding semilandmark methods in geometric morphometrics, with an application to human craniofacial and dental variation. Journal of Anatomy 208: 769–784.

    Article  PubMed  Google Scholar 

  • Perrett, J. J. & D. J. Mundfrom, 2010. Bonferroni procedure. In Salkind, N. J. (ed), Encyclopedia of Research Design Sage Publ, Thousand Oaks, CA: 98–101.

    Google Scholar 

  • Pongparadon, S., G. C. Zuccarello & A. Prathep, 2017. High morpho-anatomical variability in Halimeda macroloba (Bryopsidales, Chlorophyta) in Thai waters. Phycological Research 65: 136–145.

    Article  CAS  Google Scholar 

  • Pongparadon, S., S. Nooek & A. Prathep, 2020. Phenotypic plasticity and morphological adaptation of Halimeda opuntia (Bryopsidales, Chlorophyta) to light intensity. Phycological Research 68: 115–125.

    Article  Google Scholar 

  • Prathep, A., R. Kaewsrikhaw, J. Mayakun & A. Darakrai, 2018. The effects of light intensity and temperature on the calcification rate of Halimeda macroloba. Journal of Applied Phycology 30: 3405–3412.

  • Prát, S. & J. Hamáčková, 1946. The analysis of calcareous marine algae. Studia Botanica Čechoslovaca 7: 112–126.

    Google Scholar 

  • R Core Team, 2020. A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna:

    Google Scholar 

  • Rees, S. A., B. N. Opdyke, P. A. Wilson & T. J. Henstock, 2007. Significance of Halimeda bioherms to the global carbonate budget based on a geological sediment budget for the Northern Great Barrier Reef, Australia. Coral Reefs 26: 177–188.

    Article  Google Scholar 

  • Rindi, F., M. M. Pasella, M. F. E. Lee & H. Verbruggen, 2020. Phylogeography of the mediterranean green seaweed Halimeda tuna (Ulvophyceae, Chlorophyta). Journal of Phycology 56: 1109–1113.

  • Rohlf, F. J., 2015. The tps series of software. Hystrix Italian Journal of Mammalogy 26: 9–12.

    Google Scholar 

  • Schaefer, K., T. Lauc, P. Mitteroecker, P. Gunz & F. L. Bookstein, 2006. Dental arch asymmetry in an isolated Adriatic community. American Journal of Physical Anthropology 129: 132–142.

    Article  PubMed  Google Scholar 

  • Smith, J. E., C. M. Smith, P. S. Vroom, K. L. Beach & S. Miller, 2004. Nutrient and growth dynamics of Halimeda tuna on Conch Reef, Florida Keys: possible influence of internal tides on nutrient status and physiology. Limnology and Oceanography 49: 1923–1936.

    Article  Google Scholar 

  • Stark, L. M., L. Almodovar & R. W. Krauss, 1969. Factors affecting the rate of calcification in Halimeda opuntia (L.) Lamouroux and Halimeda discoidea Decaisne. Journal of Phycology 5: 305–312.

    Article  CAS  PubMed  Google Scholar 

  • van Tussenbroek, B. I. & J. K. van Dijk, 2007. Spatial and temporal variability in biomass and production of psammophytic Halimeda incrassata (Bryopsidales, Chlorophyta) in a Caribbean reef lagoon. Journal of Phycology 43: 69–77.

    Article  CAS  Google Scholar 

  • Verbruggen, H., O. De Clerck & E. Coppejans, 2005. Deviant segments hamper a morphometric approach towards Halimeda taxonomy. Cryptogamie Algologie 26: 259–274.

    Google Scholar 

  • Verbruggen, H., O. De Clerck, A. D. R. N’yeurt, H. Spalding & P. S. Vroom, 2006. Phylogeny and taxonomy of Halimeda incrassata, including descriptions of H. kanaloana and H. heteromorpha spp. nov. (Bryopsidales, Chlorophyta). European Journal of Phycology 41: 337–362.

    Article  CAS  Google Scholar 

  • Vergés, A., P. D. Steinberg, M. E. Hay, A. G. B. Poore, A. H. Campbell, E. Ballesteros, K. L. Heck Jr., D. J. Booth, M. A. Coleman, D. A. Feary, W. Figueira, T. Langlois, E. M. Marzinelli, T. Mizerek, P. J. Mumby, Y. Nakamura, M. Roughan, E. Van Sebille, A. S. Gupta, D. A. Smale, F. Tomas, T. Wernberg & S. K. Wilson, 2014. The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proceedings of the Royal Society B 281: 20140846.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vroom, P. S., C. M. Smith, J. A. Coyer, L. J. Walters, C. L. Hunter, K. S. Beach & J. E. Smith, 2003. Field biology of Halimeda tuna (Bryopsidales, Chlorophyta) across a depth gradient: comparative growth, survivorship, recruitment, and reproduction. Hydrobiologia 501: 149–166.

    Article  Google Scholar 

  • Wizemann, A., F. W. Meyer & H. Westphal, 2014. A new model for the calcification of the green macro-alga Halimeda opuntia (Lamouroux). Coral Reefs 33: 951–964.

    Article  Google Scholar 

  • Yñiguez, A. T., J. W. McManus & L. Collado-Vides, 2010. Capturing the dynamics in benthic structures: environmental effects on morphology in the macroalgal genera Halimeda and Dictyota. Marine Ecology Progress Series 411: 17–32.

    Article  Google Scholar 

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Acknowledgements

The authors wish to thank the Ministry of the Sea, Transport, and Infrastructure of the Republic of Croatia for the field research permit no. 6422/2019/JLJ and Prof. Dr. Zrinka Ljubešić for her kind assistance in arranging the research permission. The study was supported by the institutional grant of Charles University ‘Progres Q43’.

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The study was supported by the institutional grant of Charles University ‘Progres Q43’.

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Correspondence to Jiri Neustupa.

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Neustupa, J., Nemcova, Y. Geometric morphometrics shows a close relationship between the shape features, position on thalli, and CaCO3 content of segments in Halimeda tuna (Bryopsidales, Ulvophyceae). Hydrobiologia 849, 2581–2594 (2022). https://doi.org/10.1007/s10750-022-04876-y

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