Advertisement

Journal of Applied Phycology

, Volume 31, Issue 1, pp 561–573 | Cite as

Culture of Chondracanthus teedei and Gracilariopsis longissima in a traditional salina from southern Spain

  • Ricardo BermejoEmail author
  • Manuel Macías
  • Claudia L. Cara
  • Josefina Sánchez-García
  • Ignacio Hernández
Article

Abstract

The cultivation of two red macroalgal species, Chondracanthus teedei (Martens ex Roth) and Gracilariopsis longissima (S.G. Gmelin) Steentoft M, L.M. Irvine & W.F. Farnham, was assessed in a traditional salina, a system of earthen ponds used for marine salt extraction taking advantages of solar evaporation and tidal cycle. Vegetative thalli of both species were cultivated in rafts holding polypropylene ropes, from January to June 2015, when lock-gates were opened during the period of no salt production. The effects of three factors in the net growth rate were analysed: seedling density, water motion and seasonality. Water motion and seasonality showed a significant effect in the growth of both species. Seedling density only showed a significant effect in the growth of Gp. longissima, where the growth rates improved at high seedling densities. Values of tissue N were generally lower than critical quotas, suggesting that maximum growth was limited by the concentrations of dissolved nutrients. In addition, the high salinity and temperatures in late spring seemed to condition the values of net growth rate. The study suggested that macroalgal cultivation of these two valuable species could be a promising complementary activity in the integrated management of the salina during winter and early spring, when salinity is lower than 40 PSU, if nutrients in the water are increased with the semi-intensive fish cultivation and the hydrodynamic conditions along the rafts are enhanced.

Keywords

Rhodophyta Earthen ponds Net growth rate Macroalgal cultivation Nitrogen Yield 

Notes

Acknowledgements

Ricardo Bermejo was supported by a postdoctoral fellowship from the University of Cádiz (Contrato Puente, Plan Propio de Investigación 2014). This version of the manuscript was greatly improved by suggestions provided by two referees. We thank R. Love and S. Molina for field assistance.

Funding information

This study was funded by Project RNM 1235 of the Consejería de Economía y Conocimiento of the Junta de Andalucía (Spain).

References

  1. Abreu MH, Pereira R, Yarish C, Buschmann AH, Sousa-pinto I (2011) IMTA with Gracilaria vermiculophylla: productivity and nutrient removal performance of the seaweed in a land-based pilot scale system. Aquaculture 312:77–87CrossRefGoogle Scholar
  2. Alonso-Villalobos C, Ménanteau L (2004) Métodos y técnicas de explotación salinera. In: Fernando-Olmedo NR (ed) Salinas de Andalucía. Consejeria de Medio Ambiente (Junta de Andalucía), Sevilla, pp 47–51Google Scholar
  3. Alonso-Villalobos C, Gracia Prieto FJ, Ménanteau L (2003) Las salinas de la Bahía de Cádiz durante la antigüedad: Visión geoarqueológica de un problema histórico. SPAL Rev Prehist Arqueol 12:317–332Google Scholar
  4. Alonso-Villalobos C, Ménanteau L, Rubio-García JC, Severo-Aguiló P (2004) Una visión histórica de las salinas andaluzas. In: Fernando-Olmedo NR (ed) Salinas de Andalucía. Consejería de Medio Ambiente (Junta de Andalucía), Sevilla, pp 25–46Google Scholar
  5. Anderson M, Gorley R, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. Primer-E Ltd, Plymouth, p 204Google Scholar
  6. Avila M, Piel MI, Caceres JH, Alveal K (2011) Cultivation of the red alga Chondracanthus chamissoi: sexual reproduction and seedling production in culture under controlled conditions. J Appl Phycol 23:529–536CrossRefGoogle Scholar
  7. Britton RH, Johnson AR (1987) An ecological account of a Mediterranean salina: the Salin de Giraud, Camargue (S. France). Biol Conserv 42:185–230CrossRefGoogle Scholar
  8. Bulboa CR, Macchiavello JE, Oliveira EC, Fonck E (2005) First attempt to cultivate the carrageenan producing seaweed Chondracanthus chamissoi (C. Agardh) Kutzing (Rhodophyta; Gigartinales) in Northern Chile. Aquac Res 36:1069–1074.Google Scholar
  9. Bulboa C, Véliz K, Sáez F, Sepúlveda C, Vega L, Macchiavello J (2013) A new method for cultivation of the carragenophyte and edible red seaweed Chondracanthus chamissoi based on secondary attachment disc: development in outdoor tanks. Aquaculture 410-411:86–94Google Scholar
  10. Burfeind DD, Udy JW (2009) The effects of light and nutrients on Caulerpa taxifolia and growth. Aquat Bot 90:105–109CrossRefGoogle Scholar
  11. Carrington E, Grace SP, Chopin T (2001) Life history phases and the biomechanical properties of the red alga Chondrus crispus (Rhodophyta). J Phycol 37:699–704CrossRefGoogle Scholar
  12. Choi HG, Kim YS, Kim JH, Lee SJ, Park EJ, Ryu J, Nam KW (2006) Effects of temperature and salinity on the growth of Gracilaria verrucosa and G. chorda, with the potential for mariculture in Korea. J Appl Phycol 18:269–277CrossRefGoogle Scholar
  13. Chopin T, Buschmann AH, Halling C, Troell M, Kautsky N, Neori A, Kraemer GP, Zertuche-González JA, Yarish C, Neefus C (2001) Integrating seaweeds into marine aquaculture systems: a key toward sustainability. J Phycol 37:975–986CrossRefGoogle Scholar
  14. Creed JC, Norton TA, Kain JM (1997) Intraspecific competition in Fucus serratus germlings: the interaction of light, nutrients and density. J Exp Mar Biol Ecol 212:211–223CrossRefGoogle Scholar
  15. Duarte CM, Dennison WC, Orth RJW, Carruthers TJB (2008) The charisma of coastal ecosystems: addressing the imbalance. Estuar Coasts 31:233–238CrossRefGoogle Scholar
  16. Engkvist R, Malm T, Nilsson J (2004) Interaction between isopod grazing and wave action: a structuring force in macroalgal communities in the southern Baltic Sea. Aquat Ecol 38:403–413CrossRefGoogle Scholar
  17. Faucci A, Boero F (2000) Structure of an epiphytic hydroid community on Cystoseira at two sites of different wave exposure. Sci Mar 64:255–264CrossRefGoogle Scholar
  18. Friedlander M, Kashman Y, Weinberger F, Dawes CJ (2001) Gracilaria and its epiphytes: 4. The response of two Gracilaria species to Ulva lactuca in a bacteria-limited environment. J Appl Phycol 13:501–507CrossRefGoogle Scholar
  19. Ganesan M, Thiruppathi S, Jha B (2006) Mariculture of Hypnea musciformis (Wulfen) Lamouroux in south east coast of India. Aquaculture 256:201–211CrossRefGoogle Scholar
  20. Gerard VA, Mann KH (1979) Growth and production of Laminaria longicruris (Phaeophyta) populations exposed to different intensities of water movement. J Phycol 15:33–41CrossRefGoogle Scholar
  21. Guiry MD (1984) Structure, life history and hybridization of atlantic Gigartina teedii (Rhodophyta) in culture. Br Phycol J 19:37–55CrossRefGoogle Scholar
  22. Guiry MD, Guiry GM (2017) AlgaeBase. World-wide electronic publication. National University of Ireland, Galway http://www.algaebase.org Google Scholar
  23. Hanisak MD (1983) The nitrogen relationship of marine macroalgae. In: Carpenter EJ, Capone DG (eds) Nitrogen in the marine environment. Academic Press, New York, pp 669–730Google Scholar
  24. He Q, Zhang YJ, Chai Z, Wu H, Wen S, He P (2014) Gracilariopsis longissima as biofilter for an Integrated Multi-Trophic aquaculture (IMTA) system with Sciaenops ocellatus: Bioremediation efficiency and production in a recirculating system. Indian J Geo-Marine Sci 43:528–537Google Scholar
  25. Hernandez I, Peralta G, Perez-Llorens JL, Vergara JJ, Niell FX (1997) Biomass and growth dynamics of Ulva species in Palmones River estuary. J Phycol 33:764–772CrossRefGoogle Scholar
  26. Hernandez I, Fernandez-Engo MA, Perez-Llorens JL, Vergara JJ (2005) Integrated outdoor culture of two estuarine macroalgae as biofilters for dissolved nutrients from Sparus aurata waste waters. J Appl Phycol 17:557–567CrossRefGoogle Scholar
  27. Hernández I, Pérez-Pastor A, Vergara JJ, Martínez-Aragón JF, Fernández-Engo MÁ, Pérez-Lloréns JL (2006) Studies on the biofiltration capacity of Gracilariopsis longissima: from microscale to macroscale. Aquaculture 252:43–53CrossRefGoogle Scholar
  28. Hernández I, Cara CL, Sánchez-García J, Macías M, Robyn L, Bermejo R (2016) Cultivos de macroalgas en el litoral gaditano: estado actual y perspectivas para su desarrollo. Algas 52:5–10Google Scholar
  29. Hortas F, Muñoz-Pascual G, Pérez-Hurtado A (2004) Avifauna de las salinas atlánticas. In: Fernando-Olmedo NR (ed) Salinas de Andalucía. Consejeria de Medio Ambiente (Junta de Andalucía), Sevilla, pp 223–231Google Scholar
  30. Huo YZ, Xu SN, Wang YY, Zhang JH, Zhang YJ, Wu WN, Chen YQ, He PM (2011) Bioremediation efficiencies of Gracilaria verrucosa cultivated in an enclosed sea area of Hangzhou Bay, China. J Appl Phycol 23:173–182CrossRefGoogle Scholar
  31. Hurd CL (2000) Water motion, marine macroalgal physiology, and production. J Phycol 36:453–472CrossRefGoogle Scholar
  32. Hurtado AQ, Agbayani RF, Sanares R, De Castro-Mallare MTR (2001) The seasonality and economic feasibility of cultivating Kappaphycus alvarezii in Panagatan Cays, Caluya, Antique, Philippines. Aquaculture 199:295–310CrossRefGoogle Scholar
  33. Israel A, Martínez-Goss M, Friedlander M (1999) Effect of salinity and pH on growth and agar yield of Gracilaria tenuistipitata var. liui in laboratory and outdoor cultivation. J Appl Phycol 11:543–549CrossRefGoogle Scholar
  34. Kain JM, Destombe C (1995) A review of the life-history, reproduction and phenology of Gracilaria. J Appl Phycol 7:269–281CrossRefGoogle Scholar
  35. Kloareg B, Quatrano RS (1988) Structure of the cell walls of marine algae and ecophysiological functions of the matrix polysaccharides. Oceanogr Mar Biol Annu Rev 26:259–315Google Scholar
  36. Kumar M, Kumari P, Gupta V, Reddy CRK, Jha B (2010) Biochemical responses of red alga Gracilaria corticata (Gracilariales, Rhodophyta) to salinity induced oxidative stress. J Exp Mar Biol Ecol 391:27–34CrossRefGoogle Scholar
  37. Leigh EGJ, Paine RT, Quinn JF, Suchanek TH (1987) Wave energy and intertidal productivity. Proc Natl Acad Sci U S A 84:1314–1318CrossRefGoogle Scholar
  38. Lourenço SL, Barbarino E, Nascimento A, Freitas JNP, Diniz GS (2006) Tissue nitrogen and phosphorus in seaweeds in a tropical eutrophic environment: what a long-term study tells us. J Appl Phycol 18:389–398CrossRefGoogle Scholar
  39. Martínez-Aragón JF, Hernández I, Pérez-Lloréns JL, Vázquez R, Vergara JJ (2002) Biofiltering efficiency in removal of dissolved nutrients by three species of estuarine macroalgae cultivated with sea bass (Dicentrarchus labrax) waste waters 1. Phosphate. J Appl Phycol 14:365–374CrossRefGoogle Scholar
  40. Masero JA, Pérez-Hurtado A (2001) Importance of the supratidal habitats for maintaining overwintering shorebird populations: how redshanks use tidal mudflats and adjacent saltworks in southern Europe. Condor 103:21–30CrossRefGoogle Scholar
  41. Molina-Montenegro MA, Muñoz AA, Badano EI, Morales BW, Fuentes KM, Cavieres LA (2005) Positive associations between macroalgal species in a rocky intertidal zone and their effects on the physiological performance of Ulva lactuca. Mar Ecol Prog Ser 292:173–180CrossRefGoogle Scholar
  42. Neori A, Chopin T, Troell M, Buschmann AH, Kraemer GP, Hallin C, Shpigel M, Yarsh C (2004) Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture 231:361–391CrossRefGoogle Scholar
  43. Padhi S, Swain PK, Behura SK, Baidya S, Behera SK, Panigrahy MR (2011) Cultivation of Gracilaria verrucosa (Huds) Papenfuss in Chilika Lake for livelihood generation in coastal areas of Orissa State. J Appl Phycol 23:151–155CrossRefGoogle Scholar
  44. Parages ML, Figueroa FL, Conde-Álvarez RM, Jiménez C (2014) Phosphorylation of MAPK-like proteins in three intertidal macroalgae under stress conditions. Aquat Biol 22:213–226CrossRefGoogle Scholar
  45. Pereira L (2012) A review of the nutrient composition of selected edible seaweeds. In: Pomin VH (ed) Seaweed: ecology, nutrient composition and medicinal uses. Nova Science Publishers, Inc., New York, pp 15–47Google Scholar
  46. Pereira L, Mesquita JF (2004) Population studies and carrageenan properties of Chondracanthus teedei var. lusitanicus (Gigartinaceae, Rhodophyta). J Appl Phycol 16:369–383CrossRefGoogle Scholar
  47. Pérez-Lloréns JL, Brun FG, Andría J, Vergara JJ (2004) Seasonal and tidal variability of environmental carbon related physico-chemical variables and inorganic C acquisition in Gracilariopsis longissima and Enteromorpha intestinalis from Los Toruños salt marsh (Cádiz Bay, Spain). J Exp Mar Biol Ecol 304:183–201CrossRefGoogle Scholar
  48. Pérez-Lloréns JL, Hernández I, Vergara JJ, Brun FG, León Á (2016) ¿Las algas se comen? Un periplo por la biología, la historia, las curiosidades y la gastronomía. Servicio de Publicaciones de la Universidad de Cádiz, Cádiz, pp 336Google Scholar
  49. Peteiro C, Freire Ó (2011) Effect of water motion on the cultivation of the commercial seaweed Undaria pinnatifida in a coastal bay of Galicia, Northwest Spain. Aquaculture 314:269–276CrossRefGoogle Scholar
  50. Peteiro C, Freire Ó (2013) Biomass yield and morphological features of the seaweed Saccharina latissima cultivated at two different sites in a coastal bay in the Atlantic coast of Spain. J Appl Phycol 25:205–213CrossRefGoogle Scholar
  51. R Development Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna http://www.R-project.org/ Google Scholar
  52. Rothman MD, Anderson RJ, Boothroyd CJT, Kemp FA, Bolton JJ (2009) The gracilarioids in South Africa: long-term monitoring of a declining resource. J Appl Phycol 21:47–53CrossRefGoogle Scholar
  53. Ryder E, Nelson SG, McKeon C, Glenn EP, Fitzsimmons K, Napolean S (2004) Effect of water motion on the cultivation of the economic seaweed Gracilaria parvispora (Rhodophyta) on Molokai, Hawaii. Aquaculture 238:207–219CrossRefGoogle Scholar
  54. Sadoul N, Walmsley J, Charpentier B (1998) Salinas and nature conservation. In: Crivelli AJ, Jalbert J (eds) Conservation of Mediterranean wetlands n°9. Station Biologique de la Tour du Valat, Arles, p 99Google Scholar
  55. Sato Y, Yamaguchi M, Hirano T, Fukunishi N, Abe T, Kawano S (2017) Effect of water velocity on Undaria pinnatifida and Saccharina japonica growth in a novel tank system designed for macroalgae cultivation. J Appl Phycol 29:1429–1436CrossRefGoogle Scholar
  56. Shukla R, Kumar M, Chakraborty S, Gupta R, Kumar S, Sahoo D, Kuhad RC (2016) Process development for the production of bioethanol from waste algal biomass of Gracilaria verrucosa. Bioresour Technol 220:584–589CrossRefGoogle Scholar
  57. Stabili L, Acquaviva MI, Biandolino F, Cavallo RA, de Pascali SA, Fanizzi FP, Narracci M, Petrocelli A, Cecere E (2012) The lipidic extract of the seaweed Gracilariopsis longissima (Rhodophyta, Gracilariales): a potential resource for biotechnological purposes? Nat Biotechnol 29:443–450Google Scholar
  58. Steentoft M, Irvine LM, Farnham WF (1995) Two terete species of Gracilaria and Gracilariopsis (Gracilariales, Rhodophyta) in Britain. Phycologia 34:113–127CrossRefGoogle Scholar
  59. Stevens CL, Hurd CL (1997) Boundary-layers around bladed aquatic macrophytes. Hydrobiologia 346:119–128CrossRefGoogle Scholar
  60. Torrejón J (1994) El área portuaria de la Bahía de Cádiz. Tres mil años de puerto. In: CEHOPU (ed) Puertos Españoles En La Historia. Ministerio de Obras Públicas, Transportes y Medio Ambiente, Madrid, pp 117–145Google Scholar
  61. Torrejón J (1997) Las salinas de la bahía de Cádiz. In: Malpica-Cuello A, González-Alcantud JA (eds) Congreso Internacional de La Comisión de Historia de La Sal. Centro de Investigaciones Etnológicas Angel Ganivet (Junta de Andalucía), Granada, pp 169–194Google Scholar
  62. Vásquez JA, Alonso-Vega JM (2001) Chondracanthus chamissoi (Rhodophyta, Gigartinales) in northern Chile: ecological aspects for management of wild populations. J Appl Phycol 13:267–277CrossRefGoogle Scholar
  63. Villazán B, Salo T, Brun FG, Vergara JJ, Pedersen MF (2015) High ammonium availability amplifies the adverse effect of low salinity on eelgrass Zostera marina. Mar Ecol Prog Ser 536:149–162CrossRefGoogle Scholar
  64. Wakibia JG, Anderson RJ, Keats DW (2001) Growth rates and agar properties of three gracilarioids in suspended open-water cultivation in St . Helena Bay , South Africa. J Appl Phycol 13:195–207CrossRefGoogle Scholar
  65. Wheeler PA, Björnsäter BR (1992) Seasonal fluctuations in tissue nitrogen, phosphorus, and N:P for five macroalgal species common to the Pacific northwest coast. J Phycol 28:1–6CrossRefGoogle Scholar
  66. Yang MY, Macaya EC, Kim MS (2015) Molecular evidence for verifying the distribution of Chondracanthus chamissoi and C. teedei (Gigartinaceae, Rhodophyta). Bot Mar 58:103–113Google Scholar
  67. Zhou W, Sui Z, Wang J, Chang L (2013) An orthogonal design for optimization of growth conditions for all life history stages of Gracilariopsis lemaneiformis (Rhodophyta). Aquaculture 392–395:98–105CrossRefGoogle Scholar
  68. Zinoun M, Cosson J, Deslandes E (1993) Influence of culture conditions on growth and physicochemical properties of carrageenans in Gigartina teedii (Rhodophyceae—Gigartinales). Bot Mar 36:131–136CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Biology, Division of EcologyUniversity of CadizPuerto RealSpain
  2. 2.Earth and Ocean Sciences Department, Ryan Institute and School of Natural SciencesNational University of Ireland, Galway, Co.GalwayIreland
  3. 3.Department of Botany, Ryan Institute and School of Natural SciencesNational University of Ireland, Galway, Co.GalwayIreland
  4. 4.Department of Chemical Engineering and Food Technology, Faculty of SciencesUniversity of CadizPuerto RealSpain
  5. 5.University Institute of Marine Research (INMAR), Campus de Excelencia Internacional del Mar (CEIMAR)University of CadizPuerto RealSpain

Personalised recommendations