Towards the Development and Assessment of Integrated Multi-Trophic Aquaculture Systems for Existing Fish Farms in the South China Sea

Abstract

As the frontiers of food production have expanded, the cultivation of marine organisms in coastal zones and the open ocean has developed rapidly. China is responsible for more than 60% of global aquaculture production. The dominant marine aquaculture industry in China is suspended mariculture which uses net cages, longlines or other structures to cultivate aquatic organisms in open ocean water at relatively low cost. A problem associated with suspended systems, however, is that they are essentially open. Any waste generated by farming activity is released directly into the supporting water body. This is of critical concern in the aquaculture of fed species that require substantial inputs of feed to facilitate production. If the sustainable development of suspended mariculture is to be ensured, solutions that limit or mitigate these adverse impacts are vital. 

The implementation of Integrated Multi-Trophic Aquaculture (IMTA), a form of ecological engineering in aquaculture, has been proposed to help alleviate the impacts of suspended mariculture. Prototypical IMTA systems aim to integrate extractive (non-fed) aquaculture species with fed species, so that the extractive species assimilate farm waste and produce harvestable biomass that can generate revenue. The aims of the research presented here were to evaluate the current state of IMTA in China and to develop and assess IMTA systems for use at existing fish monoculture farms in the South China Sea. 

A systematic and quantitative review of relevant literature was conducted to provide a clear and comprehensive account of research that has investigated the adverse impacts of suspended mariculture in China and to review research that is relevant to the use of IMTA systems for mitigating adverse impacts. To achieve this, 218 peer-reviewed papers published in English language journals were examined extensively. Eighteen adverse impacts originating from suspended mariculture were identified and categorised as chemical, ecological, physical and socioeconomic impacts. Eighteen measures for mitigating the impacts of suspended mariculture were identified, of which IMTA was the most frequently recommended. The most frequently studied benefits of IMTA were its capabilities for bioremediation and increasing farm production. Less commonly studied were seven additional benefits that require further investigation. These were the potential for IMTA to improve ecosystem function, increase financial return, improve overall farm sustainability, decrease stock mortality, increase product quality, control pathogens and improve the public’s opinion of aquaculture. The current challenges facing the expansion of commercial IMTA include limited use of new technology by farmers, limited personnel skills, decreasing production of low trophic level species, biogeographic and temporal barriers, and negative intra-system feedbacks. Based on the findings of this review, three field studies were conducted to develop and assess the potential for adding IMTA systems to existing fish farms in Hong Kong, a region in the South China Sea currently dominated by fish monoculture. 

The first field study assessed the technical and economic feasibility of integrating the commercially valuable scallop Mimachlamys nobilis at an existing fish monoculture farm. Scallops were grown for 201 days through mid-summer from June – December in lantern nets hung directly from fish farm platforms at treatment depths of 1 m, 3.5 m and 6 m. Only the 1 m treatment attained the target mean height-at-harvest of 80 mm. Fitted von Bertalanffy growth functions showed significant differences in growth performance between depths. The VBGFs projected that the 3.5 m and 6 m treatments would require an additional 26 and 59 days of culture respectively to reach a height-at-harvest of 80 mm. Mortality of scallops was significantly lower at 1 m (53 ± 12.5%) compared to that at 3.5 m (70 ± 9.0%) and 6 m (83 ± 4.5%). The slower growth and higher mortality at 3.5 m and 6 m were probably caused by periodically low oxygen content in deeper water which decreased to mid-summer lows of 4.96, 3.08 and 1.73 mg.L-1 at 1 m, 3.5 m and 6 m, respectively. Growth, mortality and financial data from the field trial were used in bioeconomic assessments of two typical farm sizes; small (45 m2) and large (315 m2). The initial investment, discounted payback time and 10-year net present value of the projects was US$ 5,485.51, three years and US$ 20,211.33 for the small farm, and US$ 27.659.03, two years and US$ 227,406.49 for the large farm. A sensitivity analysis revealed that the profitability of operations was most sensitive to changes in scallop mortality and sales price. This study confirmed that physically integrating M. nobilis at existing fish farms is technically and economically feasible.

The second field study integrated the filter feeding scallop M. nobilis and the deposit feeding sea cucumber Holothuria leucospilota with the fed finfish Trachinotus blochii. Analyses of nitrogen and carbon stable isotopes were used to evaluate the whether M. nobilis and H. leucospilota were directly assimilating fish farm waste. The IMTA systems were established at an existing fish monoculture farm in Hong Kong. Trachinotus blochii was raised on a rotating diet of pellets, trash fish and bread. The stable isotope ecology of the three consumer systems was evaluated using δ15N, δ13C and Bayesian mixing models. The T. blochii system was assessed as the model system because all dietary components were known. Results confirmed that stable isotope Bayesian mixing models can be used to generate precise estimates of the dietary components of aquaculture organisms raised on multiple dietary sources in open water. In the M. nobilis system it was clear that bread and trash fish made little to no contribution to scallop biomass (< 10%) but the mixing model was unable to differentiate between the contributions of suspended particulates, pellets or fish faeces due to similar isotopic signatures among these sources. Nevertheless, at 1 m depth M. nobilis grew from 44.8 ± 0.38 mm to 80.7 ± 2.51 mm shell height in 201 days which confirmed that the dietary sources available at the farm were suitable for successful cultivation. In the H. leucospilota system, stable isotope analysis revealed that the sea cucumbers were probably not consuming fish farm waste. In addition, H. leucospilota lost biomass from 81.7 ± 5.25 to 55.4 ± 23.5 g wet weight in 131 days which indicated that either the culture environment or dietary sources at the IMTA system were not suitable for cultivation. Therefore, M. nobilis is a promising candidate for IMTA and further research into its bioremediation potential is recommended. Holothuria leucospilota is not recommended for integration with fish in southern China and alternative deposit-feeding species should be explored.

The third field study assessed the production and bioremediation potential of integrating the macroalga Sargassum hemiphyllum at an existing fish farm in Hong Kong. There has been a growing body of literature recommending this perennial macroalga for the bioextraction of surplus nutrients at aquaculture sites in the South China Sea during winter. The current study used modular seaweed frames to cultivate S. hemiphyllum during two production experiments that addressed several challenges facing commercial implementation of S. hemiphyllum in IMTA. In Experiment 1, epiphyte colonisation of thalli significantly distorted estimates of specific growth rate (SGR), which showed an uncorrected SGR of 3.17 ± 1.97%.day-1 but an epiphyte-corrected SGR of 2.19 ± 1.89%.day-1. Periodic air-exposure was tested as a method to reduce epiphyte loads on algal thalli but was unsuccessful because air-exposed thalli deteriorated rapidly. Predator exclusion nets were tested as a method mitigate grazing by naturally abundant algivores. Exclusion nets were successful in mitigating grazing pressure because unprotected thalli were completely consumed by grazers while protected thalli grew well. Experiment 2 was conducted as a late-season, open-ended production trial to identify the end of a potential S. hemiphyllum cultivation season. The experiment was initiated in late February and was terminated at the beginning of April when cumulative thallus dropoff reached 17.19 ± 19.20%.line-1, coinciding with a maximum water temperature of 22.9 °C at the end of winter. Based on the productivity of S. hemiphyllum over the course of the two experiments, it was estimated that S. hemiphyllum could accumulate 3.75 ± 2.21 to 11.86 ± 4.12 kg.N.ha-1 and 63.01 ± 37.14 to 199.44 ± 69.28 kg.C.ha-1. However, algal tissue δ15N and δ13C signatures could not be used to confirm the direct assimilation of fish farm waste due to isotopic noise in the growth environments that were characterised by substantial anthropogenic pressure. Data from a multispecies grouper farm was used to estimate the scale of S. hemiphyllum that would be necessary to extract all surplus N and C released from fish husbandry. It was estimated that 0.33 ± 0.03 to 7.27 ± 0.77 ha of cultivation was required for each ton of fish produced. Estimates were heavily influenced by species-specific feed conversion ratios. Nutrient credits are a potential source of additional revenue in macroalgae mariculture; one ton of S. hemiphyllum dry biomass sequestered 53.78 ± 4.31 N credits and 1.49 ± 0.04 C credits. Therefore, S. hemiphyllum is a promising candidate for use in IMTA in the South China Sea and further research into production systems and financial feasibility is recommended. 

The research presented in this thesis has made a substantial contribution to the development, assessment and implementation of IMTA systems in the South China Sea. The systematic review and three field studies identified opportunities for IMTA systems in southern China and tested extractive species that could aid in the bioremediation of suspended, settling and dissolved waste originating from fish farms. While several challenges still face the successful implementation of IMTA commercially, the development and implementation of engineered systems is a promising measure for reducing the adverse impacts of suspended monoculture while simultaneously increasing overall farm production. The primary aims of this research were achieved; IMTA systems were implemented and assessed at existing fish farms in Hong Kong, and recommendations for expansion and future research were made. The research findings from this thesis can be applied immediately to larger-scale research projects that aim to expand production to commercial scales.

Date of Award	27 Aug 2018
Original language	English
Awarding Institution	City University of Hong Kong
Supervisor	Kwan Sing Paul LAM (Supervisor), Kwan Sing Paul LAM (Supervisor) & Trevor TELFER (External Co-Supervisor)