Skip to main content
Log in

The red macroalga Gracilaria verrucosa in co-culture with the Mediterranean mussels Mytilus galloprovincialis: productivity and nutrient removal performance

  • Published:
Aquaculture International Aims and scope Submit manuscript

Abstract

The feasibility of integrating seaweed cultivation with mussel culture in Bizerte lagoon (north Tunisia) was investigated during 1 year, in order to exploit mussel excretion nutrients as resource input and to reduce the risk of eutrophication. In parallel, to evaluate nutrients’ biofiltering efficiency and uptake rates of the agarophyte Gracilaria verrucosa, growth and nutrient removal from mussel culture water were investigated. In the laboratory, seaweed/mussel co-culture experiments were compared to mussel monoculture systems. The results showed that nitrogen and phosphorus concentrations in monoculture were significantly higher than those in co-culture treatments. Algal growth rate, thallus nutrient contents, and mussel mortality were different between all treatments. The mussel/seaweed biomass ratio of 1:0.28 (treatment 1) was convenient for efficient nutrient uptake and best seaweed growth. Field cultivation trials showed that G. verrucosa grew well in bivalve culturing farm in Bizerte lagoon at a maximum growth rate of 4.45% day−1 attained in spring season. The mean nitrogen content in dry thalli cultured in co-culture with mussel in Bizerte lagoon was 4.19 ± 0.81%. Results indicate that G. verrucosa can efficiently absorb the nutrients from mussel in Bizerte lagoon and can be associated with local mussel farms, mitigating eutrophication, and eventually, increasing economic incomes of farmers.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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 312:77–87

    Article  Google Scholar 

  • Ajjabi Chebil L, Romdhane MS, El Abed A (2005) Etude comparative de l’absorption de l’azote par deux espèces d’algues rouges: Gracilaria verrucosa (Hudson) Papenfuss, 1950 et Gracilaria bursa-pastoris (Gmelin) Silva, 1952. Bull Ins Nat Scien Tech Mer 32:94–102

    Google Scholar 

  • Beji O (2000) Les resources vivantes exploitables du lac de Bizerte: Etat actuel et potentialités. Partie I Bull Inst Scien Tech Mer de Salammbô 27:45–60

    Google Scholar 

  • Ben Said R, Ksouri J (1999) La Rhodophycée Gracilaria Verrucosa du lac de Bizerte (Tunisie): variations mensuelles de la biomasse, du rendement d’extraction et de la qualité de l’agar. Bull Inst Scien Tech Mer de Salammbô 26:127–136

    Google Scholar 

  • Boukef I, El Bour M, El Mejri S, Bejaoui B, Mraouna R, Harzallah A, Boudabous A (2009) Etude de l’influence des facteurs environnementaux sur la distribution de différentes populations bactériennes dans une station mytilicole de la lagune de Bizerte (Nord-Tunisie). Rev Sci Eau 22(1):79–91

    Google Scholar 

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

    Article  Google Scholar 

  • Buschmann AH, Troell M, Kautsky N, Kautsky L (1996) Integrated tank cultivation of salmonids and Gracilaria chilensis (Gracilariales, rhodophyta). Hydrobiologia 326(327):75–82

    Article  Google Scholar 

  • Buschmann AH, Troell M, Kautsky N (2001) Integrated algal farming: a review Cah Biol Mar 42:83–90

    Google Scholar 

  • Chow F, Macciavello J, Santa Cruz S, Fonck O (2001) Utilization of Gracilaria chilensis (Rhodophyta: Gracilariaceae) as biofilter in the depuration of effluents from tank cultures of fish, oyster, and sea urchins. J World Aquac Soc 32(2):214–220

    Article  Google Scholar 

  • Cuomo V, Merrill J, Palomba I, De maio L, Gargiulo M, Cuomo A, Sebastio C (1997) Mariculture with seaweed and mussels for marine environmental restoration and resources production. I J Envir Studies 52:297–310

    Article  Google Scholar 

  • D’Elia CF, DeBoer JA (1978) Nutritional studies of two red algae. II. Kinetics of ammonium and nitrate uptake. J Phycol 14:266–272

    Article  Google Scholar 

  • Dalleli M, Elbour M, Aissa P (2001) Evaluation de la pollution bactérienne de la lagune de Bizerte: résultats préliminaires. J Rech Oceanogr 26:18–28

    Google Scholar 

  • De Castro TR, Guanzo NG (1989) Effect of freezing on photosynthesis of intertidal macroalgae: relative tolerance of Chondrus crispus and Mastocarpus stellatus (Rhodophyta). Israeli J Aquacul - Badmidgeh 45:89–94

    Google Scholar 

  • FAO (2014) The State of World Fisheries and Aquaculture: opportunities and challenges. 16/03/2014

  • Fei XG (2003) Solving the coastal eutrophication problem by large scale seaweed cultivation. Hydrobiologia 512(1):145–151

    Google Scholar 

  • Galimany E, Rose JM, Dixon MS, Wikfors GH (2013) Quantifying feeding behavior of ribbed mussels (Geukensia demissa) in two urban sites (Long Island Sound, USA) with different seston characteristics. Estuar Coasts 36:1265–1273

    Article  CAS  Google Scholar 

  • Grami B, Niquil N, Sakka Hlaili A, Gosselin M, Hamel D, Hadj Mabrouk H (2008) The plankton food web of the Bizerte lagoon (south-western Mediterranean): carbon steady-state modeling using inverse analysis. Est Coast Shel Scien 79:101–121

    Article  Google Scholar 

  • Hanisak MD (1987) Cultivation of Gracilaria and other macroalgae in Florida for energy production. In: Bird KT, Benson PH (eds) Seaweed cultivation for renewable resources. Elsevier, New york, pp 191–218

  • Harrison PJ, Hurd CL (2001) Nutrient physiology of seaweeds: application of concepts to aquaculture. Cah Biol Mar 42(1–2):71–82

    Google Scholar 

  • Hunter DA, Uglow RF (1993) A technique for the measurement of total ammonia, in small volumes of seawater and haemolymph. Ophelia 37:31–40

    Google Scholar 

  • 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(2):173–182

  • Huo Y, Wu H, Chai Z, Xu Sh, Han F, Dong L, He P (2012) Bioremediation efficiency of Gracilaria verrucosa for an integrated multi-trophic aquaculture system with Pseudosciaena crocea in Xiangshan Harbor, China. Aquaculture 326:99–105

  • Jones AB, Dennison WC, Preston NP (2001) Integrated treatment of shrimp effluent by sedimentation, oyster filtration and macroalgal absorption: a laboratory scale study. Aquaculture 193:155–178

    Article  Google Scholar 

  • Kim JK, Kraemer GP, Yarish C (2014) Field scale evaluation of seaweed aquaculture as a nutrient bioextraction strategy in Long Island Sound and the Bronx River Estuary. Aquaculture 433:148–156

    Article  CAS  Google Scholar 

  • Lobban C S, Harrison P J (1997) Seaweed ecology and physiology. Cambridge University Press, Cambridge, pp 366

  • Mao YZ, Hongsheng Y, Zhou Y, Ye N (2009) Potential of the seaweed Gracilaria lemaneiformis for integrated multitrophique aquaculture with scallop Chlamys farreri in North China. J Appl Phycol 21:649–656

    Article  Google Scholar 

  • Marinho-Soriano E, Nunes SO, Carneiro MAA, Pereira DC (2009) Nutrients removal from aquaculture wastewater using the macroalgae Gracilaria birdiae. Biomass Bioenergy 33:327–331

    Article  CAS  Google Scholar 

  • Mensi F, Ksouri J, Hammami W, Romdhane MS (2009) L’algue rouge Gracilaria verrucosa (Hudson) Papenfuss de la lagune de Bizerte (Tunisie septentrionale): essai de culture en mode suspendu et composition biochimique. Bull Inst Nat Scien Tech Mer de Salammbô 36:125–137

    Google Scholar 

  • Mensi F, Ksouri J, Hammami W, Romdhane MS (2014) Etat des connaissances et perspectives de recherches sur la culture de gracilariales (Gracilaria et Gracilariopsis): application à la lagune de Bizerte. Bull Inst Nat Scien Tech Mer de Salammbô 41:25–38

    Google Scholar 

  • Naddafi R, Petterson K, Eklov P (2007) The effect of seasonal variation in selective feeding by zebra mussels (Dreissena polymorpha) on phytoplankton community composition. Freshwater Boil 52:823–842

    Article  Google Scholar 

  • Nagler PL, Glenn EP, Nelson SG, Napolean S (2003) Effects of fertilization treatment and stocking density on the growth and production of the economic seaweed Gracilaria parvispora (Rhodophyta) in cage culture at Molokai, Hawaii. Aquaculture 219:379–391

    Article  Google Scholar 

  • Neori A, Nobre AM (2012) Relationships between trophic levels and economics in aquaculture. Aquacult Eco & Manag 16(1):40–68

    Article  Google Scholar 

  • Neori A, Chopin T, Troell M, Buschmann AH, Kraemer GP, Halling C, Shpigel M, Yarish C (2004) Integrated aquaculture: rationale, evolution and state of the art emphasizing seaweed biofiltration in modern mariculture. Aquaculture 231:361–391

    Article  Google Scholar 

  • Nobre AM, Robertson-Andersson D, Neori A, Sankar K (2010) Ecological economic assessment of aquaculture options: comparison between abalone monoculture and integrated multi-trophic aquaculture of abalone and seaweeds. Aquaculture 306:116–126

    Article  Google Scholar 

  • Pagand P, Blancheton JP, Lemoalle J, Casellas C (2000) The use of high rate algal ponds for treatment of marine effluent from recirculating fish rearing system. Aquac Res 31:729–736

    Article  Google Scholar 

  • Parsons TR, Maita Y, Lalli CM (1984) A manual of chemical and biological methods for seawater analysis. Pergamon Press, Oxford, pp 173

  • Piazzi L, Ceccherelli G (2017) Eutrophication affects the resistance of fucoids to an introduced alga spread Mar Envir Research 129:189–194

    Article  Google Scholar 

  • Ridler N, Wowchuk M, Robinson B, Barrington K, Chopin T, Robinson S, Page F, Reid G, Szemerda M, Sewuster J, Boyne-Travis N (2007) Integrated multitrophic aquaculture (IMTA): a potential strategic choice for farmers. Aquacult Economics & Management 11(1):99–110

    Article  Google Scholar 

  • Sakka Hlaili A, Grami B, Niquil N, Gosselin M, Hamel D, Troussellier M, Hadj Mabrouk H (2008) The planktonic food web web of the Bizerte lagoon (south-western Mediterranean) during summer: spatial distribution under different anthropogenic pressures. Est Coast Shel Scien 78:61–77

    Article  Google Scholar 

  • Sanderson JC, Cromey CJ, Dring MJ, Kelly MS (2008) Distribution of nutrients for seaweed cultivation around salmon cages at farm sites in north–west Scotland. Aquaculture 278:60–68

    Article  CAS  Google Scholar 

  • Seghetta M, Tørring D, Bruhn A, Thomsen M (2014) Bioextraction potential of seaweed in Denmark—an instrument for circular nutrient management. Scien of the Total Envir 563:513–529

    Google Scholar 

  • Shen YC, Xiong BX, Wang H, Ye FL (2007) A case study on optimal culture structure of prawn-fish-shellfish-algae. Acta Hydrobiologica 31(1):30–38 in Chinese with English abstract

    Google Scholar 

  • Shi H, Zheng W, Zhang X, Zhu M, Ding D (2013) Ecological–economic assessment of monoculture and integrated multi-trophic aquaculture in Sanggou Bay of China. Aquaculture 410–411:172–178

    Article  Google Scholar 

  • Strohmeier T, Strand Ø, Alunno-Bruscia M, Duinker A, Cranford PJ (2012) Variability in particle retention efficiency by the mussel Mytilus edulis. J Exp Biol Ecol 412:96–102

    Article  Google Scholar 

  • Thomsen J, Himmerkus N, Holland N, Sartoris FJ, Bleich M, Tresguerres M (2016) Ammonia excretion in mytilid mussels is facilitated by ciliary beating. J Exp Biol 219:2300–2310

    Article  CAS  PubMed  Google Scholar 

  • ``Troell M, Norbeg J (1998) Modelling output and retention of suspended solids in an integrated salmon-mussel culture. Ecol Model 110(1):65–71

    Article  CAS  Google Scholar 

  • Troell M, Halling C, Nilsson A, Buschmann AH, Kautsky N, Kautsky L (1997) Integrated marine cultivation of Gracilaria chilensis (Gracilariales, Rhodophyta) and salmon cages for reduced environmental impact and increased economic output. Aquaculture 156:45–61

    Article  Google Scholar 

  • Troell M, Halling C, Neori A, Chopin T, Bushmann AH, Kautsky N, Yarish C (2003) Integrated mariculture: asking the right questions. Aquaculture 226:69–90

    Article  Google Scholar 

  • Turki S, Dhib A, Belakhal MF, Frossard V, Balti N, Karrat R, Aleya L (2014) Harmful algal blooms (HABs) associated with phycotoxins in shellfish: what can be learned from five years of monitoring in Bizerte lagoon (southern Mediterranean Sea)? Ecol Eng 67:39–47

    Article  Google Scholar 

  • Wu H, HuoY HM, Wei Z, He P (2015) Eutrophication assessment and bioremediation strategy using seaweeds co-cultured with aquatic animals in an enclosed bay in China. Mar Poll Bull 95(1):342–349

    Article  CAS  Google Scholar 

  • Xu YJ, Wei W, Qian LM (2007) Pollution purification and water quality control of shrimp aquaculture in land-based enclosure by Gracilaria lichevoides (Rhodophyta). J Fish Sci China 14:430–435 in Chinese with English abstract

    CAS  Google Scholar 

  • Yang YF, Fei XG, Song JM, Hu HY, Wang GC, Chung IK (2006) Growth of Gracilaria lemaneiformis under different cultivation conditions and its effects on nutrient removal in Chinese coastal waters. Aquaculture 254:248–255

    Article  Google Scholar 

  • Yarish C, Pereira R (2008) Mass production of marine macroalgae. In: Sven Erik Jørgensen SE, Fath BD (eds) Ecological engineering: encyclopedia of ecology, 5 vols. Elsevier, Oxford, pp 2236–2247

    Google Scholar 

  • Zhou Y, Yang HS, Mao YZ, Yuan XT, Zhang T, Liu Y, Zhang FS (2003) Biodeposition by the Zhikong scallop Chlamys farreri in Sanggou bay, Shandong, northern China. Chin J Zool 38:40–44

    Google Scholar 

Download references

Acknowledgements

Special thanks are due to Mr. Hichem Ben Chrifa, Managing Director of STL (Société Tunisienne des Lagunes), and to its entire staff for their assistance in field investigations.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Leila Chebil Ajjabi.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chebil Ajjabi, L., Abaab, M. & Segni, R. The red macroalga Gracilaria verrucosa in co-culture with the Mediterranean mussels Mytilus galloprovincialis: productivity and nutrient removal performance. Aquacult Int 26, 253–266 (2018). https://doi.org/10.1007/s10499-017-0206-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10499-017-0206-2

Keywords

Navigation