Skip to main content
Log in

Biomass variation and reproductive phenology of Gracilaria gracilis in a Patagonian natural bed (Chubut, Argentina)

  • Published:
Journal of Applied Phycology Aims and scope Submit manuscript

Abstract

The biomass variation and the reproduction of the natural Gracilaria gracilis bed in Bahía Bustamante (Patagonia, Argentina) were analyzed for 2 years, with the aim of determining the present situation of the population for an updated status overview; establishing the relevant features of the temporal variation in both biomass and reproductive states in relation to environmental factors, epiphytes and associated algae; and assessing carpospore availability for future spore-culture development. Field measurements and sampling were performed monthly between March 2006 and February 2008. In both years, G. gracilis biomass presented marked seasonal variations, with a minimum in winter and a maximum in late spring and in summer. During both years, coexistence of the three life-cycle phases was found, with dominance of tetrasporophytes. Two data sets from individuals originated from sexual reproduction (tetraspores and carpospores) and from asexual reproduction by thallus fragmentation were analyzed separately. In the fragmentation fraction, tetrasporophyte frequencies remained higher than those for gametophytes. However, in the spore-originated fraction, a generation ratio close to 0.5 was observed. Female gametophytes bearing cystocarps were always present, with a maximum in summer and autumn. Biological data were related to environmental factors by means of canonical correspondence analysis (CCA). The first year was characterized by higher biomass values of G. gracilis and Undaria pinnatifida, lower epiphytism, larger Gracilaria thalli and greater proportion of mature tetrasporophytes and gametophytes. The second year was characterized by a high proportion of Gracilaria vegetative thalli and high epiphyte density. The best time to obtain spores from cystocarpic thalli would be in summer and early autumn.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10

Similar content being viewed by others

References

  • Alveal K, Romo H, Werlinger C, Oliveira C (1997) Mass cultivation of the agar-producing Gracilaria chilensis (Rhodophyta) from spores. Aquaculture 148:77–83

    Article  Google Scholar 

  • Boraso AL, Ciancia M, Cerezo A (2006) Seaweed resources of Argentina. In Critchley AT, Ohno M, Largo DB (eds) World Seaweed Resources– An Authoritative Reference System. Electronic version 1.0. Eti Information Services Ltd: www.etiis.org.uk,26

  • Boraso de Zaixo AL (1983) Ecología de Gracilaria verrucosa (Hudson) Papenfus en poblaciones de la provincia de Chubut (Argentina). PhD Thesis, Universidad Nacional de Buenos Aires, 172 pp

  • Boraso de Zaixso AL (1984) Crecimiento de Gracilaria verrucosa en condición suspendida. Mem Soc Latinoam Acuicultura 5:415–418

    Google Scholar 

  • Boraso de Zaixso AL (1987) Gracilaria verrucosa in Golfo Nuevo, Chubut, Argentina. I. Population parameters and environmental factors. Hydrobiologia 151/152:238–244

    Google Scholar 

  • Boraso de Zaixo AL (1989) Ecological considerations for the possibility of culturing Gracilaria verrucosa in Argentina. In Oliveira EC, Kautsky N (eds) Cultivation of seaweeds in Latin America. Universidad de Sao Paulo, pp 51–58

  • Boraso de Zaixso AL (1995a) La población de Gracilaria verrucosa (Hudson) Papenfuss en Bahía Arredondo (Chubut, Argentina). Natur Patagónica Ser Cs Biol 3:85–106

    Google Scholar 

  • Boraso de Zaixso AL (1995b) Utilización de algas marinas. In: Ferrario M & Sar E (eds) Macroalgas de Interés Económico. Universidad Nacional de La Plata. Red de Editoriales Universitarias, pp 15–55

  • Boraso de Zaixso AL, Paternoster I (1985). Demografía, reproducción y propagación en poblaciones de Gracilaria verrucosa (Hudson) Papenfuss de la provincia del Chubut (Rep. Argentina). I. Golfo Nuevo. Contrib CENPAT n° 99, 26

  • Boraso de Zaixso AL, Zaixso HE, Romanello E (1997) Estudios sobre la población de Gracilaria gracilis de Bahía Melo (prov. de Chubut, Argentina). Natur Patagónica Cienc Biol 5:1–27

    Google Scholar 

  • Brito LL, Silva ST (2004) Fases reproductivas de Gracilaria damaecornis J. Agardh (Gracilariaceae: Rhodophyta). Bol Inst Oceanogr Venezuela Univ Oriente 43:33–36

    Google Scholar 

  • Buschmann AH, Gómez P (1993) Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes. Hydrobiologia 260/261:345–351

    Article  Google Scholar 

  • Buschmann AH, Westermeier R, Retamales CA (1995) Cultivation of Gracilaria on the sea-bottom in southern Chile: a review. J Appl Phycol 7:291–301

    Article  Google Scholar 

  • Buschmann AH, Correa JA, Westermeier R, Hernández-González M, Norambuena R (2001) Red algal farming in Chile: a review. Aquaculture 194:203–220

    Article  Google Scholar 

  • Candia AI (1988) Ciclo reproductivo in vitro de dos poblaciones de Gracilaria Greville (Rhodophyta, Gracilariaceae) de Lenga, Bahia San Vicente. Gayana Bot 45:357–364

    Google Scholar 

  • Casas GN, Piriz ML (1996) Surveys of Undaria pinnatifida (Laminariales, Phaeophyta) in Golfo Nuevo, Argentina. Hydrobiologia 326/327:213–215

    Article  Google Scholar 

  • Casas GN, Piriz ML (1998) Cultivo experimental de la agarífera Gracilaria gracilis (Gracilariales, Rhodophyta) en golfo Nuevo, Argentina. Natur Patagónica Cienc Biol 6:51–69

    Google Scholar 

  • Casas GN, Scrosati R, Piriz ML (2004) The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina). Biol Invasions 6:411–416

    Article  Google Scholar 

  • Critchley AT (1993) Gracilaria (Rhodophyta, Gracilariales): An economically important agarophyte. In: Ohno M, Critchley AT (eds) Seaweed Cultivation and Marine Ranching. JICA, Japan, pp 89–112

    Google Scholar 

  • Dawes CP (1995) Suspended cultivation of Gracilaria in the sea. J Appl Phycol 7:303–313

    Article  Google Scholar 

  • Destombe C, Valero M, Vernet P, Couvet D (1989) What controls haploid–diploid ratio in the red alga, Gracilaria verrucosa? J Evol Biol 2:317–338

    Article  Google Scholar 

  • Destombe C, Valero M, Guillemin ML (2010). Delineation of two sibling red algal species: Gracilaria gracilis and Gracilaria dura (Gracilariales, Rhodophyta) using multi DNA markers: resurrection of the species G. dura previously described in the northern Atlantic 200 years ago. J Phycol (in press)

  • Eberlein K, Kattner G (1987) Automatic method for the determination of ortho-phosphate and total dissolved phosphorous in the marine environment. Fresenius Z Anal Chem 326:354–357

    Article  CAS  Google Scholar 

  • Engel C, Aberg P, Gaggiotti OE, Destombe C, Valero M (2001) Population dynamics and stage structure in a haploid-diploid red seaweed, Gracilaria gracilis. J Ecol 89:436–450

    Article  Google Scholar 

  • Grasshoff K, Ehrhardt M, Kremling K (1983) Methods of Seawater Analysis. Verlag Chemie, Weinheim, p 419

    Google Scholar 

  • Guillemin ML, Faugeron S, Destombe C, Viard F, Correa JA, Valero M (2008a) Genetic variation in wild and cultivated populations of the haploid-diploid red alga Gracilaria chilensis: how farming practices favor asexual reproduction and heterozygosity. Evolution 62:1500–1519

    Article  PubMed  Google Scholar 

  • Guillemin ML, Ait Akki S, Givernaud T, Mouradi A, Valero M, Destombe C (2008b) Molecular characterisation and development of rapid molecular methods to delineate species of Gracilariaceae from the Atlantic coast of Morocco. Aquat Bot 89:324–330

    Article  CAS  Google Scholar 

  • Hay ME, Norris JN (1984) Seasonal reproduction and abundance of six sympatric species of Gracilaria Grev. (Gracilariaceae; Rhodophyta) on a Caribbean subtidal sand plain. Hydrobiologia 116/117:63–72

    Article  Google Scholar 

  • Hoyle MD (1978) Reproductive phenology and growth rates in two species or Gracilaria from Hawaii. J Exp Mar Biol Ecol 35:273–283

    Article  Google Scholar 

  • Infante R, Candia A (1988) Cultivo de Gracilaria verrucosa (Hudson) Papenfuss e Iridaea ciliata Kützing (Rhodophyta, Gigartinaceae) en laboratorio: esporulación inducida y colonización de carposporas en diferentes sustratos. Gayana Bot 45:297–304

    Google Scholar 

  • Kain JM, Destombe C (1995) A review of the life history, reproduction and phenology of Gracilaria. J Appl Phycol 7:269–281

    Article  Google Scholar 

  • Kuschel FA, Buschmann AH (1991) Abundance, effects and management of epiphytes in intertidal cultures of Gracilaria (Rhodophyta) in Southern Chile. Aquaculture 92:7–19

    Article  Google Scholar 

  • Lapointe BE (1985) Strategies for pulsed nutrient supply to Gracilaria cultures in the Florida Keys: interactions between concentration and frequency of nutrient pulses. J Exp Mar Biol Ecol 93:211–222

    Article  Google Scholar 

  • Levy I, Beer S, Friedlander M (1990) Growth, photosynthesis and agar in wild-type strains of Gracilaria verrucosa and G. conferta (Gracilariales, Rhodophyta), as a strain selection experiment. Hydrobiologia 204/205:381–387

    Article  Google Scholar 

  • Macchiavello J, De Paula EJ, Oliveira EC (1998) Growth rate responses of five commercial strains of Gracilaria (Rhodophyta, Gracilariales) to temperature and light. J World Aquac Soc 29:259–266

    Article  Google Scholar 

  • Marinho-Soriano E, Laugier T, De Casabianca ML (1998) Reproductive strategy of two Gracilaria species, G. bursa-pastoris and G. gracilis, in a Mediterranean Lagoon (Thau, France). Bot Mar 41:559–564

    Article  Google Scholar 

  • Martin JP, Bastida RO (2008) El alga invasora Undaria pinnatifida (Harvey) Suringar en la Ría Deseado (Patagonia Austral, Argentina): ciclo del esporofito y factores ambientales determinantes de su distribución. Rev Biol Mar Oceanogr 43:335–344

    Article  Google Scholar 

  • Mayer AMS (1981) Studies on Gracilaria sp. in Bahía Arredondo, Chubut Province, Argentina. Proc Int Seaweed Symp 10:705–710

    Google Scholar 

  • Oliveira EC, Plastino EM (1984) The life history of some species of Gracilaria (Rhodophyta) from Brasil. Jpn J Phycol 32:1–6

    Google Scholar 

  • Oliveira E, Alveal K, Anderson RJ (2000) Mariculture of the agar-producing gracilarioid red algae. Rev Fish Sci 8:345–377

    CAS  Google Scholar 

  • Orduña-Rojas J, Robledo D (2002) Studies on the tropical agarophyte Gracilaria cornea J. Agardh (Rhodophyta, Gracilariales) from Yucatán, México. II. Biomass assessment and reproductive phenology. Bot Mar 45:459–464

    Article  Google Scholar 

  • Oza RM, Tewari A, Rajyaguru MR (1989) Growth and phenology of red alga Gracilaria verrucosa (Huds.) Papenf. Indian J Mar Sci 18:82–86

    Google Scholar 

  • Pinheiro-Joventino F (1986) Ecological studies of Gracilaria cervicornis (Turn.) J. Ag. in Ceará State, Brazil. Proc Int Seaweed Symp 12:87

    Google Scholar 

  • Piriz ML, Casas G (2001) Introducción de especies y su impacto en la biodiversidad. El caso Undaria pinnatifida (Phaeophyta, Laminariales). In: Alveal K, Antezana T (eds) Sustentabilidad de la biodiversidad. Un problema actual. Bases científico-técnicas. Teorizaciones y proyecciones. Universidad de Concepción, Chile, pp 679–692

    Google Scholar 

  • Polifrone M, De Masi F, Gargiulo GM (2006) Alternative pathways in the life history of Gracilaria gracilis. Aquaculture 261:1003–1013

    Article  Google Scholar 

  • Prieto I, Westermeier R, Muller D (1991) Variación de fenofases de Gracilaria chilensis Bird, McLachlan y Oliveira (Rhodophyta, Gigartinales), en condiciones de cultivo en laboratorio y terreno. Presencia de fases mezcladas. Rev Chil Hist Nat 64:343–352

    Google Scholar 

  • Rebello J, Ohno M, Critchley AT, Sawamura M (1996) Growth rates and agar quality of Gracilaria gracilis (Stackhouse) Steentoft from Namibia, Southern Africa. Bot Mar 39:273–279

    Article  Google Scholar 

  • Romanello EE, Arnoldi G, García H, Taylor R, Medina M (1993) Evaluación del área y biomasa de la pradera de Gracilaria verrucosa (Hudson) Papenfuss en la bahía Melo, provincia del Chubut, Argentina. Natur Patagónica Cienc Biol 1:111–114

    Google Scholar 

  • Romo H, Alveal K (1979) Estudios poblacionales en la pradera de Gracilaria verrucosa (Hudson) Papenfuss de la Isla de los Reyes. Bahía de Concepción. Ciencia y Tecnología del Mar. CONA 4:15–26

    Google Scholar 

  • Santelices B, Doty MS (1989) A review of Gracilaria farming. Aquaculture 78:95–133

    Article  Google Scholar 

  • Santelices B, Fonck E (1979) Ecología y cultivo de Gracilaria lemanaeformis. In: Santelices B (ed) Actas I Simp Algas marinas chilenas. Subsecretaría de Pesca, Ministerio de Economía, Fomento y Reconstrucción, Santiago, pp 165–200

    Google Scholar 

  • Santelices B, Ugarte R (1987) Production of Chilean Gracilaria: problems and perspectives. Hydrobiologia 151/152:295–299

    Article  Google Scholar 

  • Santelices B, Varela D (1995) Regeneration capacity of Gracilaria fragments. Effect of size, age, position and reproductive state. J Appl Phycol 7:283–290

    Article  Google Scholar 

  • Santelices B, Vásquez J, Ohme U, Fonck E (1984) Managing wild crops of Gracilaria in central Chile. Proc Int Seaweed Symp 12:77–89

    Google Scholar 

  • Simonetti G, Giaccone G, Pignatti S (1970) The seaweed Gracilaria confervoides, an important object of autecologic and cultivation research in the northern Adriatic Sea. Helgol Wiss Meeresunters 20:89–96

    Article  Google Scholar 

  • Skriptsova AV, Yakovleva IM (2002) The influence of variations in irradiance upon morphology in an unattached form of Gracilaria gracilis (Stackhouse) Steentoft during field cultivation, South Primorye, Russia. Aquat Ecol 36:511–518

    Article  Google Scholar 

  • Smit AJ (2004) Medicinal and pharmaceutical uses of seaweed natural products: A review. J Appl Phycol 16:245–262

    Article  CAS  Google Scholar 

  • Smit AJ, Robertson BL, du Preez DR (1997) Influence of ammonium-N pulse concentrations and frequency, tank condition and nitrogen starvation on growth rate and biochemical composition of Gracilaria gracilis. J Appl Phycol 8:473–481

    Article  Google Scholar 

  • ter Braak CJF (1986) Canonical correspondence analysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67:1167–1179

    Article  Google Scholar 

  • ter Braak CJF (1995) Ordination. In: Jongman RHG, ter Braak CJF, van Tongeren OFR (eds) Data analysis in community and landscape ecology. Cambridge University Press, Cambridge, pp 91–173

    Chapter  Google Scholar 

  • ter Braak CJF, Smilauer P (1998) CANOCO reference manual and user’s guide to Canoco for Windows. Software for canonical community ordination (version 4). Microcomputer Power, Ithaca, p 351

    Google Scholar 

  • Thornber CS, Gaines SD (2004) Population demographics in species with biphasic life cycles. Ecology 85:1661–1674

    Article  Google Scholar 

  • Treguer P, LeCorre P (1975) Manuel d'analyse des sels nutritifs dans l'eau de mer. (Utilisation de l’Autoanalyser II), 2ème edn. Univ. Bretagne Occidentale, 110

  • Trono GC, Azanza-Corrales R (1981) The seasonal variation in the biomass and reproductive states of Gracilaria in Manila Bay. Proc Int Seaweed Symp 10:743–748

    Google Scholar 

  • Umamaheswara Rao M (1973) Growth and reproduction in some species of Gracilaria and Gracilariopsis in the Palk Bay. Indian J Fish 20:182–192

    Google Scholar 

  • 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 13:195–207

    Article  CAS  Google Scholar 

  • Wentworth CK (1922) A scale of grade and class terms for clastic sediments. J Geol 30:377–392

    Article  Google Scholar 

  • Whyte JN, Englar JR, Saunders RG, Lindsay JC (1981) Seasonal variations in the biomass, quantity and quality of agar, from the reproductive and vegetative stages of Gracilaria (verrucosa type). Bot Mar 23:493–501

    Article  Google Scholar 

  • Zemke-White WL, Ohno M (1999) World seaweed utilization: an end-of-century summary. J Appl Phycol 11:369–376

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by grants from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET): PIP 5045 and Agencia Nacional Argentina para la Promoción Científica y Tecnológica (ANPCyT): BID 1728/OC-AR-PICT 632. We thank Soriano S.A. for their logistic assistance during our work in the field and Christophe Destombe for his valuable suggestions that contributed to manuscript improvement. LAM is a Fellow Member of CONICET. ALB and PIL are Research Members of CONICET.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Patricia I. Leonardi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Martín, L.A., Boraso de Zaixso, A.L. & Leonardi, P.I. Biomass variation and reproductive phenology of Gracilaria gracilis in a Patagonian natural bed (Chubut, Argentina). J Appl Phycol 23, 643–654 (2011). https://doi.org/10.1007/s10811-010-9555-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-010-9555-1

Keywords

Navigation