Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-22T18:50:54.209Z Has data issue: false hasContentIssue false

Standing stock variations, growth and CaCO3 production by the calcareous green alga Halimeda opuntia

Published online by Cambridge University Press:  30 August 2016

Pedro Bastos De Macedo Carneiro*
Affiliation:
Instituto de Ciências do Mar, Universidade Federal do Ceará, Av. Abolição, 3207, Meireles. CEP 60.165-081. Fortaleza, Ceará, Brazil
Jamile Ulisses Pereira
Affiliation:
Instituto de Ciências do Mar, Universidade Federal do Ceará, Av. Abolição, 3207, Meireles. CEP 60.165-081. Fortaleza, Ceará, Brazil
Helena Matthews-Cascon
Affiliation:
Centro de Ciências, Universidade Federal do Ceará, Campus do Pici. CEP 60440-554. Fortaleza, Ceará, Brazil
*
Correspondence should be addressed to:P.B.M. Carneiro, Instituto de Ciências do Mar, Universidade Federal do Ceará, Av. Abolição, 3207, Meireles. CEP 60.165-081. Fortaleza, Ceará, Brazil email: [email protected]

Abstract

The present paper investigates standing stock variations of Halimeda opuntia on a sandstone reef of the South-west Atlantic Ocean, in order to better understand the role of this seaweed as a CaCO3 producer. The study was conducted over two 3-month periods, using photo quadrats to analyse the coverage area, and destructive sampling to quantify area-specific biomass and CaCO3 percentage. The alga occupied 2.4% of the substrate (4464 m2), growing as clumps with an average biomass of 1.59 kg m−2, resulting in a standing stock of 7097.8 kg of alga. This standing stock varied with environmental conditions, particularly wind speed. Assuming an exponential model for these variations, H. opuntia produced at least 13,050.14 kg (54.37 g m−2 day−1) of carbonate sediments. There was a positive correlation between changes in standing stock and coverage, but not with area-specific biomass. This suggests that net algal growth results in the occupation of new spaces, with minimal increases in height or segment density. Therefore monitoring coverage should complement traditional individual-based methods for estimating Halimeda growth and production. Combined, these approaches should result in more accurate models of the role of this alga on marine carbonate budgets.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alexandersson, E.T. and Milliman, J.D. (1981) Intragranular Mg-Calcite cement in Halimeda plates from the Brazilian Continental Shelf. Journal of Sedimentary Research 51, 13091314.Google Scholar
Amado-Filho, G.M., Moura, R.L., Bastos, A.C., Salgado, L.T., Sumida, P.Y., Guth, A.Z., Francini-Filho, R.B., Pereira-Filho, G.H., Abrantes, D.P., Brasileiro, P.S., Bahia, R.G., Leal, R.N., Kaufman, L., Kleypas, J.A., Farina, M. and Thompson, F.L. (2012) Rhodolith beds are major CaCO3 bio-factories in the tropical South West Atlantic. PLoS ONE 7, e35171.CrossRefGoogle ScholarPubMed
Araújo, H.A.B. and Machado, A.D.J. (2008) Benthic Foraminifera associated with the South Bahia Coral Reefs, Brazil. Journal of Foraminiferal Research 38, 2338.CrossRefGoogle Scholar
Bach, S.D. (1979) Standing crop, growth and production of calcareous Siphonales (Chlorophyta) in a South Florida Lagoon. Bulletin of Marine Science 29, 191201.Google Scholar
Bandeira-Pedrosa, M.E., Pereira, S.M.B. and Oliveira, E.C. (2004) Taxonomy and distribution of the green algal genus Halimeda (Bryopsidales, Chlorophyta) in Brazil. Revista Brasileira de Botânica 27, 363377.Google Scholar
Barr, N.G., Kloeppel, A., Rees, T.A.V., Scherer, C., Taylor, R.B. and Wenzel, A. (2008) Wave surge increases rates of growth and nutrient uptake in the green seaweed Ulva pertusa maintained at low bulk flow velocities. Aquatic Biology 3, 179186.CrossRefGoogle Scholar
Barros, K.V.S. and Rocha-Barreira, C.A. (2014) Influence of environmental factors on a Halodule wrightii Ascherson meadow in northeastern Brazil. Brazilian Journal of Aquatic Sciences and Technology 18, 3141.CrossRefGoogle Scholar
Bastos, A.C., Quaresma, V.S., Marangoni, M.B., D'Aagostini, D.P., Bourguignon, S.N., Cetto, P.H., Silva, A.E., Amado-Filho, G.M., Moura, R.L. and Collins, M. (2015) Shelf morphology as an indicator of sedimentary regimes: a synthesis from a mixed siliciclastic–carbonate shelf on the eastern Brazilian margin. Journal of South American Earth Sciences 63, 125136.CrossRefGoogle Scholar
Branner, J.C. (1904) The stone reefs of Brazil, their geological and geographical relations, with a chapter on the coral reefs. Bulletin of the Museum of Comparative Zoology 44, 1285.Google Scholar
Carneiro, P.B.M. and Morais, J.O. (2016) Carbonate sediment production in the equatorial continental shelf of South America: Quantifying Halimeda incrassata (Chlorophyta) contributions. Journal of South American Earth Sciences 72, 16.CrossRefGoogle Scholar
Castro, C.B., Segal, B., Negrão, F. and Calderon, E.N. (2012) Four-year monthly sediment deposition on turbid southwestern Atlantic coral reefs, with a comparison of benthic assemblages. Brazilian Journal of Oceanography 60, 4963.CrossRefGoogle Scholar
Christensen, V. and Pauly, D. (1998) Changes in models of aquatic ecosystems approaching carrying capacity. Ecological Applications 8, S104S109.CrossRefGoogle Scholar
Clifton, K.E. and Clifton, L.M. (1999) The phenology of sexual reproduction by green algae (Bryopsidales) on Caribbean coral reefs. Journal of Phycology 35, 2434.CrossRefGoogle Scholar
DeBoer, J.A., Guigli, H.J., Israel, T.L. and D'Elia, C.F. (1978) Nutritional studies of two red algae. 1. Growth rate as a function of nitrogen source and concentration. Journal of Phycology 14, 261266.CrossRefGoogle Scholar
Dias, F.J.S., Castro, B.M. and Lacerda, L.D. (2013) Continental shelf water masses off the Jaguaribe River (4S), northeastern Brazil. Continental Shelf Research 66, 123135.CrossRefGoogle Scholar
Drew, E.A. (1983) Halimeda biomass, growth rates and sediment generation on reefs in the central great barrier reef province. Coral Reefs 2, 101110.CrossRefGoogle Scholar
Drew, E.A. and Abel, K.M. (1985) Biology, sedimentology and geography of the vast inter-reefal Halimeda meadows within the Great Barrier Reef Province. In Harmelin-Vivien, M. and Salvat, B. (eds) Proceedings of the Fifth International Coral Reef Congress, Ecole Pratique des Hautes Etudes, Tahiti, 27 May-01 June 1985, Volume 5. Tahiti: Antenne Museum-Ephe, pp. 1520.Google Scholar
Edgar, G.J. (1993) Measurement of the carrying capacity of benthic habitats using a metabolic-rate based index. Oecologia 95, 115121.CrossRefGoogle ScholarPubMed
Enos, P. and Perkins, R.D. (1977) Quaternary sedimentation in south Florida. Boulder, CO: Geological Society of America.Google Scholar
Freile, D. and Hillis, L. (1997) Carbonate productivity by Halimeda incrassata in a land proximal lagoon, Pico Feo, San Blas, Panama. In Lessios, H.A. and MacIntyre, I.G. (eds) Proceedings Eighth International Coral Reef Symposium, University of Panama, Panama, 24–29 June 1996, Volume 1. Panama City: Smithsonian Tropical Research Institute, pp. 767771.Google Scholar
Freile, D., Milliman, J.D. and Hillis, L. (1995) Leeward bank margin Halimeda meadows and draperies and their sedimentary importance on the western Great Bahama Bank slope. Coral Reefs 14, 2733.CrossRefGoogle Scholar
Garrigue, C. (1991) Biomass and production of two Halimeda species in the southwest New Caledonian lagoon. Oceanologica Acta 14, 581588.Google Scholar
Gherardi, D.F.M. (2004) Community structure and carbonate production of a temperate rhodolith bank from Arvoredo Island, southern Brazil. Brazilian Journal of Oceanography 52, 207224.CrossRefGoogle Scholar
Gomes, M.P., Vital, H., Eichlere, P.P.B. and Sen-Gupta, B.K. (2015) The investigation of a mixed carbonate-siliciclastic shelf, NE Brazil: side-scan sonar imagery, underwater photography, and surface-sediment data. Italian Journal of Geosciences 134, 922.CrossRefGoogle Scholar
Hadley, S., Wild-Allen, K., Johnson, C. and Macleod, C. (2015) Modeling macroalgae growth and nutrient dynamics for integrated multi-trophic aquaculture. Journal of Applied Phycology 27, 901916.CrossRefGoogle Scholar
Hastings (1996) Population biology: concepts and models. New York, NY: Springer-Verlag.Google Scholar
Hillis-Colinvaux, L. (1980) Ecology and taxonomy of Halimeda: primary producer of coral reefs. In Blaxter, J.H.S., Russel, F.S. and Younge, M. (eds) Advances in marine biology. London: Academic Press.Google Scholar
Hine, A.C., Hallock, P., Harris, M.W., Mullins, H.T., Belknap, D.F. and Jaap, W.C. (1988) Halimeda bioherms along an open seaway: Miskito Channel, Nicaraguan Rise, SW Caribbean Sea. Coral Reefs 6, 173178.CrossRefGoogle Scholar
Hudson, J.H. (1985) Growth rate and carbonate production in Halimeda opuntia: Marquesas Keys, Florida. In Toomey, D. and Nitecki, M. (eds) Paleoalgology: contemporary research and applications. Berlin: Springer-Verlag, pp. 257263.CrossRefGoogle Scholar
Johns, H.D. and Moore, C.H. (1988) Reef to basin sediment transport using Halimeda as a sediment tracer, Grand Cayman Island, West Indies. Coral Reefs 6, 187193.CrossRefGoogle Scholar
Kooistra, W.H.C.F., Coppejans, E.G.G. and Payri, C. (2002) Molecular systematics, historical ecology, and phylogeography of Halimeda (Bryopsidales). Molecular Phylogenetics and Evolution 24, 121138.CrossRefGoogle ScholarPubMed
Leão, Z.M.A.N., Dutra, L.X.C. and Spanó, S. (2006) The characteristics of bottom sediments. In Dutra, G.F., Alen, G.R., Werner, T. and McKenna, S.A. (eds) A rapid marine biodiversity assessment of the Abrolhos Bank, Bahia, Brazil. RAP Bulletin of Biological Assessment 38. Washington, DC: Conservation International, pp. 7581.Google Scholar
Littler, D.S. and Littler, M.M. (2000) Caribbean reef plants: an identification guide to the reef plants of the Caribbean, Bahamas, Florida and Gulf of Mexico. Washington, DC: Offshore Graphics.Google Scholar
Littler, M.M. and Littler, D.S. (1985) Ecological field methods: macroalgae. New York, NY: Cambridge University Press.Google Scholar
Littler, M.M., Littler, D.S. and Lapointe, B.E. (1988) A comparison of nutrient- and light-limited photosynthesis in psammophytic versus epilithic forms of Halimeda (Caulerpales, Halimedaceae) from the Bahamas. Coral Reefs 6, 219225.CrossRefGoogle Scholar
Martins, I., Oliveira, J.M., Flindt, M.R. and Marques, J.C. (1999) The effect of salinity on the growth rate of the macroalgae Enteromorpha intestinalis (Chlorophyta) in the Mondego estuary (west Portugal). Acta Oecologica 20, 259265.CrossRefGoogle Scholar
Mayakun, J., Bunruk, P. and Ko, R. (2014) Growth rate and calcium carbonate accumulation of Halimeda macroloba Decaisne (Chlorophyta: Halimedaceae) in Thai waters. Songklanakarin Journal of Science and Technology 36, 419423.Google Scholar
Milliman, J.D. (1977) Role of calcareous algae in Atlantic continental margin sedimentation. In Flugel, E. (ed.) Fossil algae: recent results and developments. New York, NY: Springer, pp. 232247.CrossRefGoogle Scholar
Monte-Luna, P., Brook, B.W., Zetina-Rejón, M.J. and Cruz-Escalona, V.H. (2004) The carrying capacity of ecosystems. Global Ecology and Biogeography 13, 485495.CrossRefGoogle Scholar
Multer, H.G. (1988) Growth rate, ultrastructure and sediment contribution of Halimeda incrassata and Halimeda monile, Nonsuch and Falmouth Bays, Antigua, W.I. Coral Reefs 6, 179186.CrossRefGoogle Scholar
Multer, H.G. and Clavijo, I. (2004) Halimeda investigations: progress and problems. Miami, FL: NOAA/RSMAS.Google Scholar
Payri, C.E. (1988) Halimeda contribution to organic and inorganic production in a Tahitian reef system. Coral Reefs 6, 251262.CrossRefGoogle Scholar
Pedersen, M.F. and Borum, J. (1997) Nutrient control of estuarine macroalgae: growth strategy and the balance between nitrogen requirements and uptake. Marine Ecology Progress Series 161, 155163.CrossRefGoogle Scholar
Pereira, N.S., Manso, V.A.V., Macedo, R.J.A., Dias, J.M.A. and Silva, A.M.C. (2013) Detrital carbonate sedimentation of the Rocas Atoll, South Atlantic. Anais da Academia Brasileira de Ciências 85, 5772.CrossRefGoogle Scholar
Rees, S.A., Opdyke, B.N., Wilson, P.A. and Henstock, T.J. (2006) 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, 177188.CrossRefGoogle Scholar
Rodrigues, R.P., Knoppers, B.A., Souza, W.F.L. and Santos, E.S. (2009) Suspended matter and nutrient gradients of a small-scale river plume in Sepetiba Bay, SE-Brazil. Brazilian Archives of Biology and Technology 52, 503512.CrossRefGoogle Scholar
Segal, B. and Castro, C.B. (2011) Coral community structure and sedimentation at different distances from the coast of the Abrolhos Bank, Brazil. Brazilian Journal of Oceanography 59, 119129.CrossRefGoogle Scholar
Seitzinger, S.P., Mayorga, E., Bouwman, A.F., Kroeze, C., Beusen, A.H.W., Billen, G., Van Drecht, G., Dumont, E., Fekete, B.M., Garnier, J. and Harrison, J.A. (2010) Global river nutrient export: a scenario analysis of past and future trends. Global Biogeochemical Cycles 24, GB0A08.CrossRefGoogle Scholar
Silva, A.S., Leão, Z.M.A.N., Kikuchi, R.K.P., Costa, A.B. and Souza, J.R.B. (2013) Sedimentation in the coastal reefs of Abrolhos over the last decades. Continental Shelf Research 70, 159167.CrossRefGoogle Scholar
Testa, V. and Bosence, D.W.J. (1998) Carbonate-siliciclastic sedimentation on a high-energy, ocean-facing, tropical ramp, NE Brazil. In Wright, V.P. and Burchette, T.P. (eds) Carbonate ramps. London: The Geological Society, pp. 5571.Google Scholar
Testa, V. and Bosence, D.W.J. (1999) Physical and biological controls on the formation of carbonate and siliciclastic bedforms on the north-east Brazilian shelf. Sedimentology 46, 279301.CrossRefGoogle Scholar
Van Tussenbroek, B.I. and Van Dijk, J.K. (2007) Spatial and temporal variability in biomass and production of psammophytic Halimeda incrassata (Bryopsidales, Chlorophyta) in a Caribbean reef lagoon. Journal of Phycology 43, 6977.CrossRefGoogle Scholar
Verbruggen, H. and Kooistra, W.H.C.F. (2004) Morphological characterization of lineages within the calcified tropical seaweed genus Halimeda (Bryopsidales, Chlorophyta). European Journal of Phycology 39, 213228.CrossRefGoogle Scholar
Vital, H., Gomes, M.P., Tabosa, W.F., Frazão, E.P., Santos, C.L.A. and Plácido, J.S. Jr (2010) Characterization of the Brazilian continental shelf adjacent to Rio Grande do Norte state, NE Brazil. Brazilian Journal of Oceanography 58, 4354.CrossRefGoogle Scholar
Vital, H., Stattegger, K., Amaro, V.E., Schwarzer, K., Frazão, E.P., Tabosa, W.F. and Silveira, I.M. (2008) A modern high-energy siliciclastic-carbonate platform. In Hampson, G., Steel, R., Burgess, P. and Dalrymple, (eds) Recent advances in models of siliciclastic shallow-marine stratigraphy. Tulsa, OK: SEPM Society for Sedimentary Geology, pp. 177190.CrossRefGoogle Scholar
Vroom, P., Smith, C., Coyer, J., Walters, L., Hunter, C., Beach, K. and Smith, J. (2003) Field biology of Halimeda tuna (Bryopsidales, Chlorophyta) across a depth gradient: comparative growth, survivorship, recruitment and reproduction. Hydrobiologia 501, 149166.CrossRefGoogle Scholar
Walters, L.J., Coyer, J.A., Hunter, C.L., Beach, K.S. and Vroom, P.S. (2002) Assexual propagation in the coral reef macroalga Halimeda (Chlorophyta, Bryopsidales): production, dispersal and attachment of small fragments. Journal of Experimental Marine Biology and Ecology 278, 4765.CrossRefGoogle Scholar
Walters, L.J. and Smith, C.M. (1994) Rapid rhizoid production in Halimeda discoidea decaisne (Chlorophyta, Caulerpales) fragments: a mechanism for survival after separation from adult thalli. Journal of Experimental Marine Biology and Ecology 175, 105120.CrossRefGoogle Scholar
Weiner, J., Kinsman, S. and Williams, S. (1998) Modeling the growth of individuals in plant populations: local density variation in a stand population of Xanthium strumarium (Asteraceae). American Journal of Botany 85, 16381645.CrossRefGoogle Scholar
Yñiguez, A.T., McManus, J.W. and Deangelis, D.L. (2008) Allowing macroalgae growth forms to emerge: use of an agent-based model to understand the growth and spread of macroalgae in Florida coral reefs, with emphasis on Halimeda tuna . Ecological Modelling 216, 6074.CrossRefGoogle Scholar
Yong, Y.S., Yong, W.T.L. and Anton, A. (2013) Analysis of formulae for determination of seaweed growth rate. Journal of Applied Phycology 25, 18311834.CrossRefGoogle Scholar