Integrated multi-trophic aquaculture of red drum (Sciaenops ocellatus) and sea cucumber (Holothuria scabra): Assessing bioremediation and life-cycle impacts

TL;DR: The methodology defined here can be a powerful tool to predict the magnitude of environmental benefits that can be expected from new and complex production systems and to show potential impact transfer between spatial scales.

Abstract: Environmental sustainability of aquaculture is a complex issue involving effects at local (e.g. benthic deterioration), regional (e.g. eutrophication) and global (e.g. catches for feed production) scales as a consequence of farming operations (e.g. waste emissions) and industrial processes involved in the product value chain. Integrating these effects using a holistic and multi-scale framework is essential to assess the environmental sustainability of innovative production systems such as Integrated Multi-Trophic Aquaculture (IMTA), in which organisms of different trophic levels are co-cultured on the same farm to minimize aquaculture waste. The environmental performances of theoretical production scenarios of red drum (Sciaenops ocellatus) sea cage monoculture and an open-water IMTA co-culturing of red drum and sea cucumber (Holothuria scabra) were assessed with mathematical models at local and global scales. First, the particulate waste bioremediation potential of sea cucumber production was estimated using an individual-based bioenergetic model. Second, environmental impacts of the monoculture and the IMTA systems were estimated and compared using life cycle assessment (LCA), calculated per kg of edible protein and t of product, including uncertainty analysis. Given the current limits to stocking density observed for sea cucumbers, its co-culture in sea cages suspended beneath finfish nets may decrease slightly (by 0.73%) farm net particulate waste load and benthic impact. The monoculture and IMTA showed little difference in impact because of the large difference in production scales of finfish and sea cucumber species. Removing 100% of finfish feces particulate waste requires cultivating sea cucumber at scale similar to that of finfish (1.3 kg of sea cucumber per kg of finfish). Nonetheless, LCA showed trends in IMTA performance: lower eutrophication impact and net primary production use but higher cumulative energy demand and climate change impacts, generating an impact transfer between categories. Intensification of sea cucumber culture could increase local and global environmental benefits, but further research is necessary to design rearing units that can optimize production and/or bioremediation and that can be practically integrated into existing finfish monoculture units. The methodology defined here can be a powerful tool to predict the magnitude of environmental benefits that can be expected from new and complex production systems and to show potential impact transfer between spatial scales. We recommend applying it to other IMTA systems and species associations and including socio-economic criteria to fully assess the sustainability of future seafood production systems.

Summary

1 Introduction

• LCA has been extensively applied to aquaculture systems, with 65 studies and 179 aquaculture systems reviewed in a recent meta-analysis (Bohnes et al., 2018) .
• LCA has been used mostly to identify problematic stages or components of systems and to compare alternatives such as intensive vs. extensive systems, monoculture vs. polyculture and open water vs. closed recirculating systems.
• The present study examined environmental benefits and trade-offs for finfish monoculture of shifting to an open-water IMTA system co-culturing suspended sea cucumber culture beneath finfish cages, by assessing the latter's mitigation potential at local and global scales.

2.2 Inventories

• The LCIs of both systems were developed and their environmental impacts were estimated using SimaPro 8.5 software and its databases (PRé Consultants, Amersfoot, Netherlands).
• The ecoinvent 3.0 database was used for all background data except feed ingredients, which were taken from the French EcoAlim v.1.3 database.
• See the Supplementary Material for detailed LCIs.

2.2.1 Description of the monoculture system and its animal production parameters

• The finfish monoculture system described a scenario of a semi-industrial red-drum farm with floating sea cages located on Mayotte Island, Indian Ocean (see Chary et al., 2019) .
• Culture cycles are 20 months long with progressive harvests from month 13.
• Harvested products range from portion-size to 3000 g per individual.
• No chemotherapeutants (e.g. antibiotics) are used during finfish production.
• Feed consists of commercial pressed pellets produced on La Reunion Island and imported to the farm by sea shipping.

2.2.2 Assumptions and data sources for the monoculture

• Annual production data (i.e. feed inputs and finfish harvest volumes) were taken from farm simulations under routine conditions with the FINS farm-scale model (Chary et al., 2019) .
• FINS is a simple model combining farm production and waste emission modules to simulate farm production, feed requirements and waste discharge for finfish sea-cage systems.
• FINS includes several submodels (e.g. individual growth model, mass balance model), which were parametrized for red drum.
• Data on the ingredient mix were provided by a commercial feed-mill manager in La Reunion (data not shown due to confidentiality).

2.2.3 Sea cucumber system assumptions and data sources

• Sea cucumbers must be processed to obtain a dry cooked commercial product called "bêche-de-mer".
• The protein content in the final product is 51.2% (Average from Ozer et al., 2004) giving an edible protein content in fresh sea cucumbers of 3.8%.
• Processing stages into bêche-de-mer were not included in the LCA system boundaries.

2.2.4 Individual bioenergetic model and population model for the sea cucumber

• On-farm sea cucumber biomass dynamics were calculated by multiplying the number of individuals by the individual weight predicted by DEB.
• The population dynamics model of sea cucumber represents (i) initial seeding (initial condition), (ii) culture-harvesting strategies, (iii) natural mortality and (iv) culture losses (e.g. poaching, predation).
• Since maximum stocking density is reached at the end of the culture cycle, it also corresponds to the system's productivity.

2.2.5 Grow-out emissions from monoculture and IMTA

• In the sea cucumber LCI, net N emissions, net P solid and dissolved emissions and net ThOD were calculated as solid and dissolved emissions from sea cucumber growth minus avoided emissions associated with IFF.
• ThOD coefficients for sea cucumber feces were estimated as 0.764 kg O 2 per kg.

2.2.6 Inputs imported to Mayotte

• On Mayotte, most economic inputs used on the farm are imported from La Reunion or France.
• Therefore, most processes were adapted to include sea transport (1700 km from La Reunion and 9800 km from France) by transoceanic ship from the closest trading ports, and land transport (30 km) by truck from the port to the farm facilities.
• Fuels were assumed to be imported from Singapore (7000 km).

2.3.2 Life cycle impact assessment and uncertainties

• It is important to include uncertainty analysis in comparative LCAs, since deterministic results that do not include significance information can lead to oversimplified conclusions (Mendoza Beltran et al., 2018) , especially in ex-ante analysis.
• Uncertainties due to unrepresentativeness (i.e. degree of reliability, completeness, temporal correlation, geographical correlation, technological correlation and sample size) of foreground processes were estimated with the Numerical Unit Spread Assessment Pedigree following the method of Henriksson et al. (2014) and included in the LCI of the monoculture and the IMTA.
• The authors simulated 1000 Monte Carlo runs to propagate these uncertainties to the LCIA results per impact category, as commonly done in LCA uncertainty analysis (Avadí and Fréon, 2013) .
• A paired t-test was used to determine statistical significance of the systems' difference in environmental impacts.
• The null hypothesis in the t-test was that IMTA and monoculture systems have equal environmental impacts per functional unit.

3.2 LCIA results

• The authors discuss the mitigation potential of the IMTA system in terms of i) the bioremediation efficiency of sea cucumber system co-cultured with finfish and ii) comparison of the impacts of the finfish monoculture and IMTA systems estimated by LCA.
• Perspectives are then discussed for decreasing the IMTA's benthic impact and overall lifecycle impacts.

4.1 Sea cucumber bioremediation potential

• The waste mitigation potential of sea cucumbers may not be sufficient to significantly reduce environmental effects of solid waste deposition on the seabed, and additional analyses are necessary to fully assess local ecological effects of IMTA systems.
• This is also true to account for other emissions (e.g. GHGs) occurring at the farm and other life-cycle stages and that can have impacts at the global scale.
• Therefore, to compare environmental performances of monoculture and IMTA systems fully, the analysis must be supplemented with more holistic impact assessment and related to the main functions of both systems, as performed in the LCA.

4.2 LCIA: comparison of monoculture and IMTA

• Compared to the monoculture, the IMTA system tended to decrease EU and NPPU impacts but increase CC and CED.
• This eco-intensification reduced the overall amount of feed used per unit of biomass produced, which explained the decrease in NPPU.
• Ecological intensification of aquaculture (Aubin et al., 2019) , through IMTA, shifted environmental burdens to energy-related global impact categories such as CC and CED.
• These components were not visible in the contribution analysis because of the large difference in production scales.
• Close integration of farm activities and infrastructure becomes less likely in IMTA farms with more balanced production between primary and secondary species; therefore, environmental impacts will likely increase if sea cucumber production increases.

4.3 Other perspectives to improve environmental performances

• Local and global environmental benefits of the IMTA system were generally low because of the low productivity of sea cucumbers; increasing them will require finding practical methods to intensify sea cucumber production.
• One option is to investigate the choice and design of rearing structures that can increase the culture surface area and thus the bioremediation potential of the system.
• With a threelevel structures, the CS could be 'virtually' divided by three, i.e. 45:1 and WEE could increase to 2.20%.
• Finding practical farming methods for sea cucumbers to be added to a pre-existing monoculture system thus remains a challenge.

Figures

Figure 1. Processes within the boundaries of (a) the monoculture system and (b) the integrated multi-trophic aquaculture system. Environmental impacts are calculated for whole-farm

Figure 3. Mean LCA impacts of the fish monoculture and fish/sea cucumber integrated multitrophic aquaculture (IMTA) systems (scaled to the largest value per category) expressed per kg of edible protein and per t of fresh aquatic product. Error bars represent 1 standard error calculated from 1000 Monte Carlo simulations. CC: Climate change; AC: Acidification

Figure 2. Annual flux of biomass and waste in the sea cucumber system and its bioremediation performances when co-cultured beneath finfish cages in an integrated multitrophic aquaculture system. Figures are given for the simulated growth of an initial population of 5 000 individuals cultured on an area of 1 372 m². DW = dry weight, WW = wet weight

Frequently asked questions

Q1. What are the contributions in "Integrated multi-trophic aquaculture of red drum (sciaenops ocellatus) and sea cucumber (holothuria scabra): assessing bioremediation and life-cycle impacts" ?

In this paper, the authors evaluated the environmental sustainability of aquaculture using a holistic and multi-scale framework, where organisms of different trophic levels are co-cultured on the same farm.