Conference PaperPDF Available

The Integration of Multi-Trophic Concept: A Solution for Modern Aquaculture Sustainable Development

Authors:
  • "Dunarea de Jos" University of Galati
  • Dunarea de Jos University of Galati Romania

Abstract

The IMTA concept represents the future solution for a sustainable and feasible development of aquaculture, as it is applicable for all types of aquaculture production systems. The capacity of modern IMTA technique to valorize the fish wastes into secondary crop production that can improve fish farms profitability makes it an attractive solution for possible investors in aquaculture industrial sector. Also, the social aspect of implementing IMTA is important as it helps to the construction of certain ethics convictions directed to environmental protection. The IMTA can also be a solution for sturgeons’ fish farms during the first years of activity, by limiting the negative balance, till caviar production will start.
Proceedings of
the 34th International Business Information Management Association Conference
(IBIMA)
13-14 November 2019
Madrid, Spain
ISBN: 978-0-9998551-3-3
Vision 2025: Education Excellence and Management of Innovations
through Sustainable Economic Competitive Advantage
Editor
Khalid S. Soliman
International Business Information Management Association (IBIMA)
Copyright 2019
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The Integration of Multi-Trophic Concept: A Solution for Modern Aquaculture Sustainable Development
Alina MOGODAN, Stefan-Mihai PETREA, Ira SIMIONOV, Ciprian Petrisor PLENOVICI, Dragos
CRISTEA, Mioara COSTACHE and Gheorghe Adrian ZUGRAVU
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The Integration of Multi-Trophic Concept:
A Solution for Modern Aquaculture
Sustainable Development
Alina MOGODAN
“Dunărea de Jos” University of Galaţi
alina.antache@ugal.ro
Stefan-Mihai PETREA
*
“Dunărea de Jos” University of Galaţi
stefan.petrea@ugal.ro
Ira SIMIONOV
*
“Dunărea de Jos” University of Galaţi
ira.simionov@gmail.com
Ciprian Petrisor PLENOVICI
“Dunărea de Jos” University of Galaţi
ciprianplenovici@yahoo.com
Dragos CRISTEA
“Dunărea de Jos” University of Galaţi, Romania
dragoscristea@yahoo.com
Mioara COSTACHE
Fish Culture Research and Development Station Nucet, Romania
scp_nucet@yahoo.com
Gheorghe Adrian ZUGRAVU
“Dunărea de Jos” University of Galaţi
zugravuadrian@yahoo.com
Abstract
The IMTA concept represents the future solution for a sustainable and feasible development of
aquaculture, as it is applicable for all types of aquaculture production systems. The capacity of
modern IMTA technique to valorize the fish wastes into secondary crop production that can improve
fish farms profitability makes it an attractive solution for possible investors in aquaculture industrial
sector. Also, the social aspect of implementing IMTA is important as it helps to the construction of
certain ethics convictions directed to environmental protection. The IMTA can also be a solution for
sturgeons’ fish farms during the first years of activity, by limiting the negative balance, till caviar
production will start.
Keywords:
integrated multi-trophic aquaculture, aquaponic
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Introduction
Integrated multi-trophic aquaculture (IMTA) is both conceptually a simple idea and also highly
appealing to regulators: the waste products from one food production process (in this case, fin-fish
production) is acquired and assimilated by other organisms and converted into valuable products.
This process both eliminates waste and increases the productivity of the food production system
(Troell et al. 2003, Neori et al. 2004, Chopin et al. 2006). The paradox is that IMTA is not a new
concept. Asian countries, which provide more than two thirds of the world’s aquaculture production,
have been practicing IMTA (often described as a type of “polyculture”) for centuries, through trial
and error and experimentation (Chopin, 2010).
The Aquaculture Glossary of the Food and Agriculture Organization of the United Nations (FAO,
2008) described ‘integrated aquaculture’ as: aquaculture system sharing resources, water, feeds,
management, etc., with other activities; commonly agricultural, agro industrial, infrastructural (waste
waters, power stations, etc). Soto (2009) defined integrated aquaculture as the culture of aquatic
species within, or together with, the undertaking of other productive activities. Recently integrated
multi trophic aquaculture (IMTA) as a very popular term for a special kind of integrated aquaculture
has emerged, where multi trophic refers to the explicit incorporation of species from different trophic
positions or nutritional levels in the same system (Chopin and Robinson, 2004). It is clear that
‘integrated aquaculture’ has both narrowly defined and broadly defined meanings.
Material and Methods
Integrated aquaculture thereby has the promise to contribute to the sustainability of aquaculture by
reducing the ecological footprint, increasing economic diversification and increasing social
acceptability of culturing systems. IMTA can be thought of in terms of eco-intensification, where the
productivity per unit input is increased (Hughes and Black,2016).
Also, IMTA refers to farming of different aquaculture species together in a way that the system
comprises fed aquaculture, organic extractive and inorganic extractive species in the same production
module to reduce organic and inorganic wastes (Neori et al., 2004). In an IMTA system, the organic
matter comprising uneaten feed and faeces from fed aquaculture (for example, fish or shrimp) is
consumed by the deposit feeders (for example, sea cucumber). In addition, the inorganic nutrients,
mainly nitrogen and phosphorus are absorbed by seaweed (Sumbing et al,.2016).
The opportunity of IMTA is to reposition the value and roles that seaweeds can have in integrated
food production systems and in ecosystem health. One often forgotten function of seaweeds is that
they are excellent nutrient scrubbers (Chopin et al. 2001). Consequently, seaweeds can be used as the
inorganic extractive component of IMTA, recapturing the dissolved nutrients released from the fed
component. They can also be used for recapturing the dissolved nutrient effluents of water treatment
facilities in coastal communities. Moreover, having organisms able to accumulate phosphorus is
becoming increasingly attractive when considering that, in the not too distant future, the next “P
peak” will not be that of petroleum but that of phosphorus. Nutrient bio mitigation is not the only
ecosystem service provided by seaweeds.
Integrated multi-trophic aquaculture is a practice in which the by-products (wastes) from one species
are recycled to become inputs (fertilizers, food and energy) for another through the cultivation, in the
right proportions, of fed aquaculture species (e.g. finfish/shrimp) with organic extractive species (e.g.
suspension and deposit feeders) and inorganic extractive aquaculture species (e.g. seaweeds) (Troell
et al. 2009; Barrington et al. 2009).
In some cases, involving a mix of species, modeling may be a viable tool for determining the balance
among species if it considers the nitrogen produced by shrimp and nitrogen removed by macroalgae
interacting with heterotrophic and nitrifying bacteria. (Sánchez-Romero et al. 2016). Although
phosphorus is most commonly considered the major limiting nutrient in freshwater environments,
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natural pond productivity is usually limited by nitrogen in tropical environments (Knud-Hansen et al.
1991). In sediments with high clay content or those that contain acid-sulphate soils, available
phosphorus can also easily limit algal productivity, since it is rapidly fixed by various cations and
bound up in sediments (Knud-Hansen 1998; Zajdband et al. 2011).
This conversion of waste into secondary raw materials has been considered to address key
environmental impact concerns related to open-water aquaculture systems, although it should be
noted that both bivalve and seaweed cultivation have their own environmental impacts, particularly
upon the benthos (for a review of underlying science and trade-offs in IMTA, see Hughes and Black,
2016) (Alexander et al. 2016).
Role of IMTA
The win/win that IMTA represents has been cited a number of times as a solution to some of the
problems that are facing the European fin-fish aquaculture industry, such as ecological damage,
economic stability, and dependence on commercial feed (Klinger & Naylor 2012, Chopin et al. 2013,
Granada et al. 2015, Hughes and Black, 2016).
Because the aquaculture production in Europe is stagnating, with growth over the last decade only
around 1% per annum, IMTA is considered as a ‘solution’ for European aquaculture, it is perhaps
better to quantify the trade-offs involved in its adoption (Hughes and Black, 2016).
Increased Productivity
Using a mass balance approach, the production of 1 tone of salmon releases approximately 50 kg of
nitrogen into the environment (Wang et al., 2012), which could support the growth of 10 t of seaweed
or 5 t of mussels over the course of the production cycle of the salmon (Holdt and Edwards, 2014).
If instead of framing productivity in terms of per unit feed, we frame it in terms of per unit of fish
meal or fish oil from wild fish stocks (biotic depletion), then the recycling of nitrogen lost to the
environment back into marine proteins and lipids, and the subsequent reincorporation into fish feed,
offers opportunities to increase the productivity in a way that may be meaningful to the farmer
(Hughes and Black, 2016).
From the 10 tone of seaweed produced for every tone of fish, it would be possible to produce 164 kg
of protein and 9 kg of marine lipids (based on the production of Alaria esculenta; Mæhre et al. 2014),
and in theory, these components could be recycled back into fish feed. This has the potential to
significantly reduce the environmental impact of the industry by further reducing reliance on marine
proteins and lipids from wild-harvest fisheries (Hughes and Black, 2016).
Reduced Environmental Impact
In the eco-efficiency win/win, the second win is reduced environmental impact. There are 2 waste
product streams of interest: dissolved nutrients and particulate organic matter (fish faeces and uneaten
pellets). The dissolved waste stream consists mainly of ammonia (Sanderson et al. 2008).
Any direct ecological benefit with direct trophic transfer of nutrient needs to take place within this
limited zone around the fish farm. Furthermore, the bioremediation potential within this zone has
been shown to be limited for both mussels and for seaweed (Broch et al. 2013, Cranford et al. 2013).
Increased Space Requirement
Bostock et al. (2010) estimates of space required for salmon production, 1 ha of salmon production
would require between 17 and 23 ha of seaweed to sequester 10% of the nitrogen output. However, in
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their study, Holdtand Edwards (2014) argue that mussel cultivation is approximately 220% more
efficient than seaweed cultivation per unit area (Holdtand Edwards 2014).
One important consideration for space and IMTA is the development of benthic IMTA, because this
IMTA would probably sit within the footprint of the existing farm, and as such, the space
requirements would be small (Robinson et al., 2011). Initial modelling studies show that benthic
IMTA could well be an appropriate technology to improve productivity and to reduce benthic
enrichment (Cubillo et al., 2016).
Increased Social Licence
Currently, in Denmark exist a legislation to reduce the environmental emission of fish farms, which is
prompting IMTA development (Holdtand Edwards 2014). Public acceptance of aquaculture is a
function of the perceived value in terms of economic benefit weighed against the negative
perceptions, such as environmental degradation (Whitmarsh and Palmieri 2009). A pathway from
better environmental performance to increased social license to increased availability of aquaculture
licenses can already be seen in Norway, where the Norwegian government has created 45 ‘green
aquaculture’ licenses in 2013 (Nikitina 2015).
Increased Complexity
There will also be an increase in the complexity of the biosecurity of the site when dealing with
organisms with different production cycles. Disease is a major constraint on the industry, costing the
industry as a whole approximately $US6 billion annually (Brummett et al. 2014), so any new
production system must not increase the risk of disease.
For example, juvenile cod exposed to infected faecal material suffered 60 to 80% mortality. This
result indicated that in the co-culture of mussels and fin-fish, mussels may act as a reservoir of
infections for V. angillarium (Pietrak et al. 2010). However, in the case of infectious salmon anemia
virus (ISAV), blue mussels were shown not to accumulate the virus and may deactivate the virus
(Skår& Mortensen 2007, Molloy et. al. 2011).
Increased Profitability
IMTA can increase the profitability for the individual operator when the market conditions are right
and can provide a measure of resilience during periods of unfavorable conditions (Whitmarsh et al.
2006, Ridler et al. 2007).
A study from Sanggou Bay - China, based on real data and not models, showed that there was a
significant increase in profitability in an IMTA operation based on scallop and seaweed production,
compared to monocultures of those species alone (Shi et al., 2013). A public perceptions survey
showed that 38% of New York seafood consumers would be prepared to pay 10% extra for IMTA
produced mussels if they carried appropriate labelling (Shuve et al., 2009).
Results and Discussions
Trade-Off Associated with IMTA In Europe Versus Asia
In Asia impact associated with aquaculture and the water column as opposed to the benthic impacts
(Hu et al. 2010, Keesing et al. 2011), and the link between IMTA (seaweed and mussels) and reduced
environmental impacts is much clearer for the water-column impacts than for benthic impacts. the
increased space requirement is less of an issue to an industry more biased toward extensive
production, and the increase in complexity of an IMTA operation is more manageable with a less-
mechanized and more labor-intensive industry that is characteristic of Asian aquaculture. From this
initial characterization, it would appear that the trade-offs for IMTA are more positive for Asia
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compared to Europe. The adoption of IMTA vary according to national and international market
conditions or regulations (Hughes and Black, 2016).
It is important to note that these trade-offs and their weight is entirely scale- and context-dependent
(McShane et al. 2011) and will vary according to national and international market conditions or
regulations.
The overarching philosophy is to promote efficient utilization of farm space for multiple productions
in such a way that limited land can be used for different purposes by which waste from one unit can
be used to serve as input for other units (Kipkemboi et al., 2006; Ofori et al., 2005; OshuwareOben et
al., 2015). Within the IAAS (integrated agriculture aquaculture system), production technology
includes the species considered for culture, the culture facilities and husbandry employed for the
various stages of production (hatchery for fry production, nursery to produce fingerlings for stocking,
and grow-out for the final product, usually for human consumption).
In ponds, water turnover is normally small, and water losses are caused mainly by evaporation and
seepage (Avnimelech et al. 2008). Organic residues such as decaying algae settle to the pond bottom,
a place with limited oxygen supply due to water stratification. Water stratification in tropical ponds is
disturbed during the night due to cooling of surface waters, or during the day due to strong winds or
rain (Diana et al. 1997).
The oxygenation of the pond bottom allows the decomposition of organic matter by aerobic bacteria,
prevents the release of reduced compounds into pond water that are toxic to fish, and provides a good
habitat for benthic organisms (Boyd and Bowman 1997; Zajdband et al. 2011).
In this context, IMTA can be used as a valuable tool towards building a sustainable aquaculture
industry. IMTA systems can be environmentally responsible, diverse, profitable and a source of
employment in coastal regions. IMTA has been practiced for centuries in Asia, but has yet to become
established in Europe. To date, effectiveness of multi-trophic culture has been demonstrated mainly
in pond culture or in high culture-density situations, where changes in concentration of key variables
such as dissolved oxygen, particulate organic matter, or dissolved nutrients can be readily measured
(Cubillo et al., 2014).
The placement of IMTA shellfish adjacent to fish cages means that some of the natural seston that
would otherwise pass through a site without adding to the organic load from the farm, because of its
small size and low settling velocity, now has the potential for redirection to the benthos as
indigestible organic material that can settle in the form of feces.
Increases in the net organic load at fish cages may result in increases in organic deposition.
Consequently, an understanding of conditions where IMTA shellfish may cause increases in net
organic loading at fish farms is warranted.
Efficiencies in IMTA systems are, in part, a function of proportions, or ratios, of extractive species
production to production at the FTL (Atlantic salmon in the Bay of Fundy, New Brunswick, Canada).
These aspects influence the proportionof the overall FTL load that is consumed by organic extractive
species (or absorbed by inorganic extractive species in the case of seaweeds). Previous work by Reid
et al. (2013) compared a number of diets and resulting fecal organic contents and absorption
efficiencies (fraction of organic material digested) for mussels fed natural and salmon culture diets.
If the amount of salmon organics digested by extractive species is greater than the organic fecal load
from seston, a reduction in net IMTA organic load occurs.
The difference in organic load between a mussel–salmon IMTA site and a salmon farm is the same as
the difference between the salmon farm organics absorbed and the seston organics egested (Reid et
al., 2013).
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Treatment of aquaculture wastes implies the development of sustainable approaches to coastal
aquaculture, as the implementation of Integrated Multi-trophic Aquaculture (IMTA) systems, and
microbial nitrification and denitrification in sediments (Chavez-Crooker &Obreque-Contreras 2010;
Marinho-Soriano et al. 2011).
Integrated multi-trophic aquaculture strategies combine a number of complementary organisms at a
farm site to optimize nutrient utilization and reduce solid waste that goes to sediments (Granada et
al., 2015).
The implementation of water recirculating systems facilitates the technological applications of these
biological filters in land-based aquacultures, as the volume of the waste streams becomes more
manageable and various treatment options can be considered, such as recirculation loop mainly found
in outdoor, IMTA, special reactors under anoxic conditions and others (Chavez-Crooker &Obreque-
Contreras 2010; Rijn 2013; Granada et al., 2015).
The use of filter-feeding organisms as nutrient (inorganic and organic) extractors has proven to be a
valid alternative for nutrient bioremediation. The most frequently tested organisms are molluscs,
which filter organic particles, and phytoplankton, and macroalgae, which have the capability of
inorganic nutrient uptake (Marinho-Soriano et al. 2011). Integrated multitrophic aquaculture has been
proposed to achieve environmental sustainability through biomitigation of aquaculture wastes that, as
compared to other accompanying methods, has advantages that may include economic stability by
product diversification and risk reduction, and social acceptability through better management
practices (Troell et al. 2009; Barrington et al. 2009; Granada et al., 2015).
The red algae Gracilaria spp. and the green algae Ulva spp. have been found to be efficient biofilters.
Gracilaria spp. have been examined for their usefulness by laboratory (using tank) (Zhou et al. 2006;
Marinho-Soriano et al. 2011;), outdoor (pond) (Abreu et al. 2009) and field (Zhou et al. 2006a; Yang
et al. 2006; Abreu et al. 2009; Granada et al., 2015) cultivation experiments.
The development of IMTA models provides a quantitative tool to develop and manage the practices
involved through mapping energetic pathways between different trophic groups and the environment.
Thus, these models are helpful in designing IMTA practices to maximize resource utilization and
minimize environmental impacts (Ren et al. 2012; Granada et al., 2015).
Advantages and Disadvantages of IMTA
The use of IMTA could answer public environmental concerns, by providing environmental services
to recycle nutrients and by isolating cultured species and their diseases, for example, from the natural
environment when applied in closed systems. It is perceived to be a sustainable type of aquaculture,
in part because IMTA can make use of alternative feeds rather than those made entirely from fish.
Further, there would be economic advantages from the multiple products that can be sold in new
market areas, including niche markets, and IMTA would open many opportunities for research,
innovation, partnerships, and education (Thomas, 2011).
Conclusions
Environmental Aspects
Nutrient extractive aquaculture is a viable ecological engineering option for managing the
externalities generated by aquaculture operations. Effective government legislation/regulations and
incentives to facilitate the development of IMTA practices and the commercialization of IMTA
products will be necessary. True recognition of the environmental/economic/societal services of
extractive crops would create strong incentives to develop sustainable marine agronomy practices,
such as IMTA, in which seaweeds and invertebrates should also be considered as candidates for a
variety of regulatory measures that internalize these benefits. For example, nutrient and carbon
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trading credits could be used to promote nutrient removal, CO
2
sequestration, oxygen provision and
coastal eutrophication reduction (Chopin, 2010).
Some author relate that integrated multi-trophic aquaculture (IMTA) involves cultivating fed species
with extractive species that utilize the inorganic and organic wastes from aquaculture for their
growth. According to Barrington (2009), IMTA is the practice which combines the appropriate
proportions, the cultivation of fed aquaculture species (e.g. finfish/shrimp) with organic extractive
aquaculture species (e.g. shellfish/herbivorous fish) and inorganic extractive aquaculture species (e.g.
seaweed) to create balanced systems for environmental sustainability (biomitigation) economic
stability (product diversification and risk reduction) and social acceptability (better management
practices) (Sasikumar and Viji, 2016).
Economic Aspects
The market price is an important factor defining the economic potential of an aquaculture enterprise.
Thus, it is important that co culture species do not affect productivity of the principal cultured
species.
To illustrate price shocks, monoculture salmon farming and IMTA were subjected of an immediate
12 % decrease in price and carried, over a 10-year run. Results indicate that mussel and seaweed
farming is less price sensitive, but this may be underestimated in the model which assumes that
mussel and seaweed are grown near a salmon farm with some of the additional costs covered by the
salmon farm and the sensitivity of salmon profitability to falling prices. Nonetheless, the IMTA farm
produces a positive profit margin whereby the monoculture salmon farm does not. This provides
further support for the viability of IMTA (Ridler et al., 2007).
Social Aspects
The social perception of potential of IMTA was studied by Barrington et al (2010) and the most
participants felt that IMTA had the potential to reduce the environmental impacts of salmon farming,
benefit community economies, and improve industry competitiveness and sustainability. Overall, 90
% of general public responders and 89 % of industry responders believed that IMTA would be a
successful venture. Even with a lack of familiarity with IMTA principles, community participants
have confidence in new methods of farming. Many respondents did believe that IMTA would
improve the public’s opinion of the industry. The groups believed that present practices have had a
moderate to great impact on communities (82 % for public, 79 % for industry), whereas IMTA is
expected to have less impact (60 % for community, 70 % for industry) (Ridler et al., 2007).
Acknowledgements
Project H2020-MSCA-RISE-2014 No. 645691: Researches on the potential conversion of
conventional fish farms into organic by establishing a model and good practice guide.
The authors MOGODAN Alina, CRISTEA Victor, PETREA Stefan-Mihai and SIMIONOV Ira-
Adeline are grateful for the technical support offered by MoRAS through the Grant POSCCE ID
1815, cod SMIS 48745 (www.moras.ugal.ro).
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The development of a benthic component, comprised of deposit feeders that will have access to the vertical flux of particles from fish pens, is an important stage in the development of IMTA systems (Cranford et al. 2013). Deposit-feeding sea cucumbers have shown promise in recycling the larger particulate waste fraction through their feeding activities when co-cultured with other species (Ren et al. 2012), playing a bioremediation role while increasing farm profit (Yuan et al. 2013). Previous studies have addressed the performance of benthic organisms in co-culture with bivalves (Zhou et al. 2006), shrimp (Pitt et al. 2004), and salmon (Ahlgren 1998), but few have attempted to model these effects (see Ferreira et al. 2012; Ren et al. 2012). This study aims to simulate growth and environmental effects of deposit-feeding organisms, using sea cucumbers as a model, in order to assess the performance of candidate species both in monoculture and in IMTA with finfish cage culture. 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Sea cucumbers were tested as co-culture candidates for IMTA systems and differences between IMTA and finfish monoculture were simulated. In well-designed integrated systems, food availability under finfish farms enables survival and growth of depositfeeders at the local-scale; in parallel, the organic load of sediments, and therefore the environmental footprint, is reduced. The effects of IMTA on culture profitability and environmental externalities, as well as the coupling between suspended and bottom culture systems, are discussed. The models developed and tested herein provide a research tool to improve our understanding of the dynamics of IMTA systems and to assist in forecasting productivity and profitability of IMTA farms. References Ahlgren, M., 1998. Composition and assimilation of salmon net pen fouling debris by red sea cucumber Parastichopus californicus: implications for polyculture. J. World Aquacult. Soc. 29: 133–139. Chopin, T., Buschmann A.H., Halling C., Troell M., Kautsky N., Neori A., Kraemer G.P., Zertuche-González J.A., Yarish C., Neefus, C. 2001 Integrating seaweeds into marine aquaculture systems: a key towards sustainability. J. Phycol. 37: 975–986. Cranford P.J., Reid G.K., Robinson S.M.C. 2013. Open water integrated multi-trophic aquaculture: constraints on the effectiveness of mussels as an organic extractive component. Aquacult. Env. Interac. 4: 163–173. Ferreira, J.G., Saurel C., Ferreira J.M. 2012. Cultivation of gilthead bream in monoculture and integrated multi-trophic aquaculture. Analysis of production and environmental effects by means of the FARM model. Aquaculture 358–359: 23–34. Ferreira J.G., Hawkins A.J.S., Bricker S.B. 2007. Management of productivity, environmental effects and profitability of shellfish aquaculture – the Farm Aquaculture Resource Management (FARM) model. Aquaculture 264: 160–174. Pitt, R., Duy N.D.Q., Duy T.V., Long H.T.C. 2004. Sandfish (Holothuria scabra) with shrimp (Penaeus monodon) co-culture tank trials. Beche-de-mer Inf. Bull. 20, 12–22. Ren, J.S, Stenton-Dozey J., Plew D.R, Fang J., Gall M. 2012. An ecosystem model for optimising production in integrated multitrophic aquaculture systems. Ecol. Modelling 246: 34–46. Robinson, S.M.C., Martin J.D., Cooper J.A., Lander T.R., Reid G.K., Powell F., Griffin R. 2011. The role of three dimensional habitats in the establishment of Integrated Multi-Trophic Aquaculture (IMTA) systems. Bull. Aquacult. Assoc. Can. 109– 2: 23– 29. Soto, D. 2009. Integrated Mariculture: A Global Review. FAO Fisheries and Aquaculture Technical Paper 529, Rome, 183 pp. Troell, M., Joyce A., Chopin T., Neori A., Buschmann A.H., Fang J.G. 2009. Ecological engineering in aquaculture—potential for integrated multi-trophic aquaculture (IMTA) in marine offshore systems. Aquaculture 297:1−9. Yuan X., Yang H., Meng L., Wang L, Li Y. 2013. Impacts of temperature on the scavenging efficiency by the deposit-feeding holothurian Apostichopus japonicus on a simulated organic pollutant in the bivalve–macroalage polyculture from the perspective of nutrient budgets. Aquaculture 406–407: 97–104. Zhou, Y., Yang H.S., Liu S.L., Yuan X.T., Mao Y.Z., Liu Y., Xu X.L., Zhang F.S. 2006. Feeding and growth on bivalves biodeposits by the deposit feeder Apostichopus japonicus cocultured in lantern nets from longlines. Aquaculture 256: 467–476.
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