IMTA with Gracilaria vermiculophylla: Productivity and nutrient removal performance of the seaweed in a land-based pilot scale system
Introduction
Globally, aquaculture continues to be the fastest growing animal food-producing sector. In 2006 it had already equalled wild fisheries in the world's fish supply. Nonetheless, growth rates for aquaculture production are beginning to slow down (FAO, 2009), partially due to the increasing public concerns about aquaculture practices and fish quality. Worries about genetic modified organisms, sanitary issues but also the perception that aquaculture can harm the environment has lead to a rather negative social image of the aquaculture industry (FAO, 2009). In fact, in water downstream from aquaculture farms, changes in the levels of oxygen, suspended organic matter, inorganic nutrient, heavy metals and even drugs can be measured (Buschmann et al., 2008a, De Casabianca et al., 1997, Mendiguchía et al., 2006 Mente et al., 2006, Sanderson et al., 2008). These may negatively impact the downstream biological communities (e.g. Holmer et al., 2008).
The use of ecological engineering tools, such as Integrated Multitrophic Aquaculture (IMTA), to convert monoculture into an ecological and thus more sustainable aquaculture is crucial (Buschmann et al., 2008a, Chopin et al., 2008, Costa-Pierce, 2010, Naylor et al., 2000). In IMTA, seaweeds assimilate the fish-excreted ammonia, phosphate and CO2, converting them into potentially valuable biomass. With this treatment, effluents can recirculate back to the fish ponds or be discharged without endangering the environment (Chopin et al., 2001, Neori et al., 2004). The advantages of using seaweeds as the biofilter component of the IMTA systems came to light more than 30 years ago (Ryther et al., 1975) but are now becoming widely accepted (Hayashi et al., 2008, Neori et al., 2007, Ridler et al., 2007).
Thus, IMTA arises as a sustainable approach, with positive environmental and socio-economic benefits for the fed aquaculture industry (FAO, 2009, Nobre et al., 2010, Ridler et al., 2007). Its application in land-based intensive fish farms can also be a tool to increase recirculation practices and establish full recirculation aquaculture systems (RAS) with all its known associated benefits (Piedrahita, 2003, Wik et al., 2009). Moreover, regulations and incentives on this matter are slowly coming into effect, for example, in Europe (European Regulation N°710/2009) and USA (http://seagrant.gso.uri.edu/sustainable_seafood/ecolabeling.html).
The economic value of the biomass, besides its biofiltration efficacy, is a consideration in choosing the seaweed species to work with in IMTA systems. The cultivation of seaweeds in IMTA promotes higher productivity levels and with less variability than natural seaweed beds due to higher and more constant nutrients availability (Abreu et al., 2009, Lüning and Pang, 2003). Good examples of significant revenues for the fish aquaculture when adopting the IMTA approach already exist with Gracilaria (Abreu et al., 2009, Buschmann et al., 2001, Neori et al., 2000), Ulva (Bolton et al., 2009) and kelp species (Buschmann et al., 2010, Chopin et al., 2008).
Gracilaria is one of the world's most cultivated and valuable seaweeds (Buschmann et al., 2008b, Oliveira et al., 2000, Yarish and Pereira, 2008). Traditionally, its economic importance comes from the phycocolloid industry, being the main source of agar (Armisen, 1995, Peng et al., 2009). Several studies have successfully used Gracilaria species as biofilters. These were mostly developed in tanks (Buschmann et al., 1994, Buschmann et al., 1996, Chow et al., 2001, Friedlander and Levy, 1995, Hanisak, 1987, Martínez-Aragón et al., 2002, Matos et al., 2006, Neori et al., 1998, Neori et al., 2000), offshore systems (Abreu et al., 2009, Anderson et al., 1999, Buschmann et al., 2008c, Halling et al., 2005, Troell et al., 1997) and to a lesser extent in ponds (Haglund and Pedersen, 1993, Jones et al., 2002, Marinho-Soriano et al., 2002, Marinho-Soriano et al., 2009, Nelson et al., 2001, Shpiggel and Neori, 1996). The majority of the studies achieved good results on productivity and agar content, the main destiny for the biomass. Changes in the amount and quality of this phycocolloid in algae produced with distinct nutrient conditions are also well documented (Martinez and Buschmann, 1996, Troell et al., 1997, Friedlander, 2001).
Gracilaria vermiculophylla thrives in Ria de Aveiro lagoon, Portugal (40°38N, 8°43°W). This taxonomic classification was molecularly confirmed by Saunders (2009); until then, this species was misidentified as G. verrucosa and G. bursa-pastoris (e. g. Matos et al., 2006). It is currently the dominant species at that site (Silva et al., 2004), being present throughout the year (Abreu et al., 2010). G. vermiculophylla may have been exploited at this lagoon since the 70s as a component of the vegetable mixture (“moliço”) which was used as a soil conditioner (Silva, 1985).
G. vermiculophylla withstands a wide range of environmental parameters and is now cosmopolitan in its occurrence (Nyberg and Wallentinus, 2009). Controlled experiments with the species revealed similar growth rates at a broad range of temperature and light conditions with no differences between the different life stages. Laboratory nitrogen uptake studies revealed high N uptake values and a preference for ammonia N sources (Abreu et al., 2010). A small scale IMTA cascade system testing the biofiltration efficiency of several macroalgae species (Matos et al., 2006) provided results indicative of a good performance of G. vermiculophylla (misidentified in that study as G. bursa-pastoris). Moreover, this species produces food grade agar (Villanueva et al., 2009) and can be used as animal protein replacement in fish feed (Matos et al., 2006, Pereira et al., 2010). All these facts make G. vermiculophylla a potential good candidate for the biofilter component of an IMTA system.
A review by Troell et al. (2003), listed some of the main lacks in IMTA research. These include studies at relevant scales for extrapolation or commercial implementation; experimental designs to facilitate statistical analyses and comparisons; systems designed to couple nutrient removal efficiency plus high seaweed productivity and long term studies to evaluate the temporal variability of the systems.
In this study, we hypothesized that the productivity and consequent nutrient removal performance of the seaweed biofilter are affected by its cultivation density and the water flow (e.g. nutrient load) of the system. It was expected that the optimal combination of these factors would change throughout time due to the seasonal variation of environmental parameters. The scale under which this study was conducted was expected to provide information necessary for the implementation of a commercial scale system of this kind.
Section snippets
The cultivation system
The G. vermiculophylla cultivation system was established at a land-based fish commercial intensive aquaculture farm (A. Coelho & Castro, Lda) in northern Portugal. This facility produces annually around 40 t of turbot (Scophthalmus rhombus (Linnaeus, 1758), 5 t of sea bass (Dicentrarchus labrax Linnaeus, 1758) and 500 000 Senegalese sole juveniles (Solea senegalensis Kaup, 1858). Recently, the company has been moving towards a full recirculation aquaculture system (RAS), thus its collaboration
Environmental parameters
The experimental periods differentiated the most in terms of temperature and number of hours with light (see Table 1, Table 2). The variation reflected the season's fluctuation, as expected for the Northern Hemisphere. Mean temperatures oscillated between 10.96 ± 0.19 °C and 20.17 ± 0.03 °C, with no differences for the two water flows. Extreme temperature values were registered in December (7.3 °C) and July (26.5 °C).
The daily mean irradiance reaching the surface of the tanks in sunny days (see
Seaweed performance
G. vermiculophylla was able to grow and remove nutrients throughout the 9 months of the experiment in a pilot scale seaweed biofilter tank system. The best results were achieved at a stocking density of 3 kg (ww) m− 2. At this condition, the seaweed system produced 0.7 ± 0.05 kg (dw) m− 2 month− 1 of G. vermiculophylla. The biomass produced was free of epiphytes and removed 221 ± 12.82 g m− 2 month− 1 of C and 40.54 ± 2.02 g m− 2 month− 1 of N.
This work was done in a system exposed to the changing weather conditions,
Final considerations
The harvest of natural Gracilaria beds is not enough to meet demand (Oliveira et al., 2000, FAO, 2003). Spain is a major Gracilaria importer since it is home to some of the biggest agar manufacturing companies. These get their raw material from neighboring Morocco but mostly from far away Chile (pers. comm.). G. vermiculophylla biomass produces an agar with somewhat higher gel strength than reported for the Morocco material (see Givernaud et al., 1999, Villanueva et al., 2009). At the same
Acknowledgments
The authors acknowledge all the help given by Pedro Roque throughout the field work and truly appreciate the support given by the company A. Coelho & Castro, Lda. The authors are also grateful for the valuable comments made to the manuscript by the anonymous reviewers. Maria H. Abreu was supported by the Portuguese Foundation for Science and Technology (FCT) with a PhD scholarship (ref: SFRH/BD/21363/2005) and the program POPH/FSE. R. Pereira was also supported by a fellowship from FCT through
References (106)
- et al.
Traditional vs. integrated multi-trophic aquaculture of Gracilaria chilensis C. J. Bird, J. McLachlan & E. C. Oliveira: productivity and physiological performance
Aquaculture
(2009) - et al.
Screening of cultivated seaweeds for antibacterial activity against fish pathogenic bacteria
Aquaculture
(2006) - et al.
Gracilaria chilensis outdoor tank cultivation in Chile: use of land-based salmon culture effluents
Aquaculture Engineering
(1994) - et al.
Cultivation of red algae in Chile: a review
Aquaculture
(2001) - et al.
Mariculture waste management
- et al.
Multi-trophic integration for sustainable marine aquaculture
- et al.
Effect of nutrient supply on response of photosynthesis and pigmentation to short-term stress (temperature and UV radiation) in Gracilaria conferta (Rhodophyta)
Marine Pollution Buletin
(2010) Seaweed proteins: biochemical, nutritional aspects and potential uses
Trends in Food Science and Technology
(1999)- et al.
Nutrients removed by Kappaphycus alvarezii (Rhodophyta, Solieriaceae) in integrated cultivation with fishes in re-circulating water
Aquaculture
(2008) - et al.
Bioremediation efficiency in the removal of dissolved inorganic nutrients by the red seaweed, Porphyra yezoensis, cultivated in the open sea
Water Research
(2008)