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Effect of Bivalves on Water Quality, Microbial Load and Growth Performance of P. vannamei and M. cephalus in Halophyte-based Integrated Multi-trophic Aquaculture Reared under Pond Conditions
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First Online 03-07-2023|
Background: IMTA is an integrated and eco-friendly farming approach, where organisms from different trophic levels can be cultured in the same system to take advantage of the synergistic interaction between species.
Methods: The experiment was conducted in earthen ponds for four months to investigate the effect of bivalves (M. casta) in halophyte-based IMTA on water quality, growth performance and microbial load. Shrimp and fish were fed with commercial feed containing 35% and 30% crude protein, respectively.
Result: The total ammonia nitrogen, nitrate-nitrogen and nitrite were comparatively low in treatments, T1 (0.13±0.012, 0.013±0.003 and 0.45±0.01, respectively) and T2 (0.15±0.005, 0.017±0.003 and 0.50±0.01, respectively). Similarly, the better average body weight, specific growth rate and feed conversion ratio were found in treatments, T1 (Shrimp: 33.87±0.88 g, 6.20±0.01% 1.10±0.02 respectively, Fish: 94.18±0.08 g, 1.59±0.001% and 1.60±0.006 respectively) and T2 (Shrimp: 32.37±0.60 g, 6.16±0.02% and 1.15±0.02 respectively fish: 92.91±0.2 g, 1.59±0.009 and 1.63±0.08 respectively). Therefore it can be concluded that the use of bivalves helps to create better water quality for the growth and survival of P. vannamei and M. cephalus in halophyte-based integrated multi-trophic aquaculture.
IMTA is an integrated and eco-friendly farming approach that allows organisms from different trophic levels to be cultivated in the same system to exploit the advantage of the synergistic interaction between species (Chopin et al., 2013). IMTA differs from the conventional polyculture method in which fish species from the same trophic level are cultured together (Barrington, 2009). In IMTA models, nutrients unutilized by one trophic level are diverted to lower trophic levels, where they are recaptured and used by the organisms for their growth and development (Custodio et al., 2017). Thus, IMTA reduces waste, ensures environmental sustainability through biomitigation (Barrington, 2009), increases productivity through product diversification and improves the overall resilience of the aquaculture sector (Troell et al., 2014). IMTA involves the incorporation of fed aquaculture species (e.g., fish/shrimp), inorganic extractive species (e.g., seaweeds/algae) and organic extractive species (e.g., suspension/deposit-feeders) at optimal ratio (Troell et al., 2009). Proper selection and proportions of different species based on their economic value and ecosystem function are important to achieve a balance in the biological and chemical processes in IMTA (Barrington, 2009).
The integration of extractive species in IMTA involves the use of bivalves, the filter-feeding organism to remove the organic nutrients while seaweeds remove the inorganic waste nutrients to mitigate the negative environmental impact of fed aquaculture (Gallardi, 2014). Organic extractive species such as bivalves reduce the nutrient load in the culture system mainly particulate waste (fish/shrimp feed waste and feces) through suspension filter feeding (Jones and Iwama, 1991; Troell et al., 2003). This in turn reduces the TSS or turbidity levels in post-harvest farm effluent, eventually reducing the eutrophication of the ecosystem (Sasikumar and Viji, 2015). So when the extractive species are incorporated into the fed aquaculture (e.g. fish/shrimp), they convert the waste into productive resources. In addition, they act as a carbon sink due to shell formation and are economically viable as they do not require pelleted feed (Sanz-Lazaro et al., 2018). Alongside these ecological benefits, there is a growing market for cultured bivalves, which are considered high-value items that generate significant profits. The health benefits of bivalves are attributed mainly to their moderately high omega-3 fatty acids and lower fat content (Holmyard, 2008). Aquatic invertebrates, mostly marine bivalves, accounted for 16.2 million tonnes of the 24.3 million tonnes of non-fed species produced in 2020. Bivalve mollusc exports totaled USD 4.3 billion in 2020, accounting for about 2.8 percent of all aquatic product exports worldwide (FAO, 2022).
Bivalves affect the water column through filtering, grazing, altering nutrient cycles, direct excretion and microbially-assisted remineralization of their organic deposits in sediments (Petersen et al., 2010). Phytoplankton numbers and blooms can be affected by massive bivalve assemblages. They can reduce phytoplankton concentration and decrease turbidity (Cranford et al., 2003). The distribution of nitrogen is significantly altered by bivalves, particularly when they add nitrogen in the form of ammonium (NH4+), remove phosphorus through deposition and recycle silicate by transporting it from the water column into the sediment. The ammonium excreted by bivalves is easily utilized for primary production, thereby increasing the nitrogen turnover in the water column. Furthermore, some bivalves, like mussels, can accumulate certain metals, such as copper in their pseudofeces (Cranford et al., 2003).
Due to their environmental adaptability and marketability, it is necessary to consider native mussel species to design IMTA systems (Sasikumar and Viji, 2015). Meretrix casta was therefore used as an extractive species in this experiment due to its widespread availability in the experimental area.
MATERIALS AND METHODS
Experimental design and species used
Nine rectangular earthen ponds (200 m-2 each) were used for this study with two treatments, namely T1 (A. officinalis as an inorganic extractive and M. casta as organic extractive species) and T2 (B. gymnorhiza as an inorganic extractive and M. casta as organic extractive species and the control (without organic and inorganic extractive species). Each treatment has three replicates (n=3) randomly distributed between treatments. The fed species in this experiment were Mugil cephalus and Penaeus vannamei. The species combination and stocking density are shown in Table 1.
Pond preparation, stocking and post-stocking management
The experimental ponds were sundried, ploughed and prepared according to the method described by Biswas et al., (2019). Post-larvae -12 of P. vannamei were obtained from the commercial hatchery in the coastal region of Kakinada andhra Pradesh. The grey mullet, M. cephalus fingerlings collected from the wild were used for the study. A. officinalis and B.gymnorhiza saplings were obtained from the Coringa Mangrove Nursery of the Forest Department in Kakinada and hra Pradesh. M. casta was obtained from a nearby water-logged mangrove areas. A. officinalis and B. gymnorhiza were installed (Fig 1) in the pond using floating PVC frames, while M. casta was spread over the pond bottom. P. vannamei and M. cephalus were fed commercial diets containing 35% and 30% crude protein, respectively.
Physico-chemical parameters of water
A mercury thermometer was used to measure the water temperature. pH meter (Eutech PC 450, Thermo Scientific, Singapore) was used for measuring water pH. The Winkler’s method was used to determine dissolved oxygen (DO), total ammonical nitrogen (TAN.), nitrite-nitrogen (NO2-N), nitrate-nitrogen (NO3-N), total phosphorous, total alkalinity, hardness, total suspended solids, biological Oxygen Demand (BOD), chemical oxygen Demand (COD), were measured at 15-day intervals using standard methods (APHA, 2005).
Estimation of microbial population in pond water
The total vibrio count (TVC) and total heterotrophic bacteria (THB) were observed fortnightly by following the method of Kumar et al., (2014).
The growth performance of the shrimp and fish is calculated by usingthe following formulas:
RESULTS AND DISCUSSION
The physic-chemical characteristics of all the experimental pond water are shown in Table 2. All water quality criteria for the culture of brackishwater fish and shrimp were within the ideal range throughout the experiment; (Biswas et al., 2012; Biswas et al., 2017). There was no difference (p>0.05) in the mean values of pH, temperature, alkalinity, salinity, or hardness between the treatments. Other measures including DO, TAN, NO2 and NO3 showed a statistically significant difference (p<0.05) between treatments. In contrast to the polyculture system, a significantly (p<0.05) lower DO level was observed in the IMTA-based treatments (T1 and T2). Compared to the polyculture system, the IMTA-based system showed significantly (p<0.05) lower values for the nutritional parameters TAN, NO2, NO3 and phosphate-phosphorus. DO is essential for aquaculture production (Rahman et al., 2020; Mahmudi et al., 2022). All treatment ponds recorded a DO level greater than 5 mg L-1 (MoEF, 2005; Boyd, 1992). Shrimp, fish and microbes all consume the DO produced by photosynthesis during the day (Boyd, 1992). In all treatments, the DO concentration was higher than 8 mg L-1 during the day, with a decrease in oxygen levels at night. The mangrove treatments had a low oxygen concentration; This could be because treatments with mangrove-based vegetation resulted in higher respiratory rates. Oxygen depletion at night was not a serious problem due to the presence of aerators (Moroyoqui-Rojo et al., 2012). Total ammonia levels (TAN) increased concomitantly with the higher stocking density of Nile tilapia, which negatively impacted growth, immunity, dissolved oxygen levels and digestive enzyme function (Dawood et al., 2019). The bacterial breakdown of organic materials such as feed waste, feces and other organic waste is the main source of ammonia in any aquatic system. Nitrite is a by-product of nitrification and its concentration is inversely correlated with that of ammonia (Bhatnagar and Devi, 2013). Therefore, the IMTA system is successful in reducing the inorganic nitrogenous compounds (NO2-N, NO3-N and TAN) and phosphate-phosphorus (PO4-P) concentration when M. casta, A. officinalis and B. gymnorhiza were used as extractive species (Moroyoqui-Rojo et al., 2012; Oliveira et al., 2021). BOD and COD were found to differ significantly between treatments (p<0.05); the T1 treatment had the lowest values, followed by the T2 treatment and control ponds had the highest values, which may be related to an increase in the concentration of decaying materials (Nandan and Azis, 1990). The presence of filter feeders such as clams, which reduce TSS (p<0.05), may account for the lower values in the halophyte-based system (Cloern, 1982). In an integrated cage aquaculture system, Kaspar et al., (1985) found that bivalves can reduce phytoplankton bloom intensity and turbidity and oysters can decrease eutrophication (Viji et al., 2014). Studies by Cloern (1982) and Officer et al., (1982) in the San Francisco Bay area further demonstrated that the abundance of bivalve suspension feeders directly decreased the amount of suspended solids available for remineralization by pelagic consumers and bacterioplankton.
Monitoring of microbial population in pond water
In this work, it was discovered that the presence of bivalves is crucial in reducing both THB and TVC in culture water. The total vibrio count and total heterotrophic bacteria are shown in Table 3, Fig 2 and 3. Significantly (p<0.05) lower TVC and THB were found in T1 and T2 than in control. The presence of bivalves such as M. casta in T1 and T2 treatments helps to reduce THB and TVC. Bivalves have effective filtration abilities that can remove excess nitrogenous waste from feed and feces, reducing the nutrients available for bacterial growth. Unlike nitrate, a higher concentration of ammonia or organic nitrogen provides a better environment for microbial growth (Zhuang et al., 2020). Many species of the genus Vibrio are known to transmit various diseases to farmed shrimp and finfish (Alavandi et al., 2004; Austin and Zhang, 2006). The co-culture of P. vannamei and C. gigas appeared to improve the physiological circumstances that reduced the prevalence of Vibrio in the intestine, which was vulnerable to environmental factors (Xing et al., 2013). Bivalves raised in a co-culture system had gut bacterial populations that were more diverse than the ones raised in a monoculture system (Omont et al., 2020). The eastern oyster (C. virginica) may have the ability to control microbial populations in the tidal creek of South Carolina’s North Inlet (Wetz et al., 2002). One of the main causes of the disappearance of micro-sized protists is believed to have been the grazing activity of C. gigas, which efficiently retains particle size >5 µm (Dupuy et al., 2000). As a result, the decline in Vibrio populations in the presence of bivalves can be used as a sign that aquatic species are in good health (Xing et al., 2013).
The growth parameters of P. vannamei and M. cephalus are presented in Table 4. There were significant (p<0.05) changes in final body weight, SGR (%), FCR, PER and total production in P. vannamei and M. cephalus. The higher final weight, SGR, PER and total production in the T1 and T2 group of fed species due to better water quality in IMTA resulted in better growth performances of shrimp and fish (Rejeki et al., 2016). On the other hand, when seabass was exposed to high concentrations of ammonia, Lemarie et al., (2004) observed weight loss and growth retardation. In the present study, the FCR was lower in the halophyte-based IMTA system than in the control due to better feed utilization of fed species in the IMTA systems, Biswas et al., (2020) reported that in IMTA there was 22% reduction in FCR compared to the polyculture system. In the present study, FCR was reduced by 14% in T1 and 7% in T2 treatment compared to control. The survival rate of P. vannamei is significantly higher in the halophyte-based IMTA than in the control, this could be attributed to the better water quality created by the extractive species in IMTA, the same result was reported by Biswas et al., 2019 and Naskar et al., 2022. While in the case of M. cephalus, no significant difference was observed among the treatments.
CONFLICT OF INTEREST
- A.P.H.A. (2005). Standard Methods for the Examination of Water and Wastewater, 21st ed. American Public Health Association (A.P.H.A.), Washington D.C.
- Alavandi, S.V., Vijayan, K.K., Santiago, T.C., Poornima, M. et al. (2004). Evaluation of Pseudomonas sp. PM 11 and Vibrio fluvialis PM 17 on immune indices of tiger shrimp Penaeus monodon. Fish Shellfish Immunol. 17(2): 115-120.
- Austin, B. and Zhang, X.H. (2006). Vibrio harveyi: A significant pathogen of marine vertebrates and invertebrates. Lett. Appl. Microbiol. 43(2): 119-124.
- Barrington, K., Chopin, T. and Robinson, S. (2009). Integrated multi- trophic aquaculture (I.M.T.A.) in marine temperate waters. Integrated mariculture: A global review. FAO Fisheries and Aquaculture Technical Paper. 529: 7-46.
- Bhatnagar, A. and Devi, P. (2013). Water quality guidelines for the management of pond fish culture. International Journal of Environmental Sciences. 3(6): 1980-2009.
- Biswas, G., Ananda Raja, R., De, D., Sundaray, J.K., Ghoshal, T.K. et al. (2012). Evaluation of productions and economic returns from two brackishwater polyculture systems in tide-fed ponds. J. Appl. Ichthyol. 28(1): 116-122.
- Biswas, G., Kumar, P., Ghoshal, T.K., Kailasam, M. et al. (2020). Integrated multitrophic aquaculture (I.M.T.A.) outperforms conventional polyculture with respect to environmental remediation, productivity and economic return in brackishwater ponds. Aquaculture. 516: 734626. https://doi.org/10.1016/ j.aquaculture.2019.734626.
- Biswas, G., Kumar, P., Kailasam, M., Ghoshal, T.K. et al. (2019). Application of integrated multi trophic aquaculture (I.M.T.A.) concept in Brackishwater ecosystem: The first exploratory trial in the Sundarban, India. Journal of Coastal Research. 86: 49-55.
- Biswas, G., Sundaray, J.K., Bhattacharyya, S.B., Shyne Anand, P.S. et al. (2017). Influence of feeding, periphyton and compost application on the performances of striped grey mullet (Mugil cephalus L.) fingerlings in fertilized brackishwater ponds. Aquaculture. 481: 64-71.
- Boyd, C.E. (1992). Shrimp Pond Bottom Soil and Sediment Management. In Proceedings of the Special Session on Shrimp Farming. Baton Rouge: World Aquaculture Society Baton Rouge, LA, U.S.A., 166-181.
- Chopin, T., MacDonald, B., Robinson, S., Cross, S. et al. (2013). The canadian integrated multi-trophic aquaculture network (C.I.M.T.A.N.)-A network for a new ERA of ecosystem responsible aquaculture. Fisheries. 38: 297-308.
- Cloern, J.E. (1982). Does the benthos control phytoplankton biomass in south San Francisco Bay Marine ecology progress series. Oldendorf. 9: 191-202.
- Cranford, P., Dowd, M., Grant, J. et al. (2003). Ecosystem level effects of marine bivalve aquaculture. A Scientific Review of The Potential Environmental Effects of Aquaculture in Aquatic Ecosystems. 1: 51-95.
- Custodio, M., Villasante, S., Cremades, J. et al. (2017). Unravelling the potential of halophytes for marine integrated multi- trophic aquaculture (I.M.T.A.) a perspective on performance, opportunities and challenges. Aquaculture Environment Interactions. 9: 445-460.
- Dawood, M.A., Shukry, M., Zayed, M.M. et al. (2019). Digestive enzymes, immunity and oxidative status of Nile tilapia (Oreochromis niloticus) reared in intensive conditions. Slovenian Veterinary Research. 56: 99-108.
- De Oliveira Gomes, L.E., Sanders, C.J., Nobrega, G.N. et al. (2021). Ecosystem carbon losses following a climate-induced mangrove mortality in Brazil. Journal of Environmental Management. 297: 113381. DOI: 10.1016/j.jenvman.2021.113381.
- Dupuy, C., Pastoureaud, A., Ryckaert, M. et al. (2000). Impact of the oyster Crassostrea gigas on a microbial community in Atlantic coastal ponds near La Rochelle. Aquatic Microbial Ecology. 22: 227-242.
- FAO, (2022). The State of World Fisheries and Aquaculture 2022. Sustainability in Action, Rome, Italy.
- Gallardi, D. (2014). Effects of bivalve aquaculture on the environment and their possible mitigation: A review. Fisheries and Aquaculture Journal. 5(3). Research Article Open Access http://dx.doi.org/10.4172/2150-3508.1000105.
- Holmyard, J. (2008). Potential for offshore mussel culture. Shellfish News. 25: 19-22.
- Jones and Iwama. (1991). Polyculture of the pacific oyster, crassostrea gigas (Thunberg), with chinook salmon, oncorhynchus tshawytscha. Aquaculture. 92: 313-322.
- Kaspar, H.F., Gillespie, P.A., Boyer, I.C. et al. (1985). Effects of mussel aquaculture on the nitrogen cycle and benthic communities in Kenepuru sound, marlborough sounds, New Zealand. Marine Biology. 85: 127-136.
- Kumar, S., Anand, P.S.S., De, D., Sundaray, J.K. et al. (2014). Effects of carbohydrate supplementation on water quality, microbial dynamics and growth performance of giant tiger prawn (Penaeus monodon). Aquac. Int. 22: 901-912.
- Lemarie, G., Dosdat, A., Covès, D. et al. (2004). Effect of chronic ammonia exposure on growth of European seabass (Dicentrarchus labrax) juveniles. Aquaculture. 229 (1-4): 479-491.
- Mahmudi, M., Musa, M., Bunga, A. et al. (2022). A water quality evaluation of integrated mangrove aquaculture system for water treatment in super-intensive white leg shrimp pond. Journal of Ecological Engineering. 23: 287-296.
- MoEF. (2005). Coastal Aquaculture Authority Act, 2005. http://www. caa.gov.in/about_caa.html.
- Moroyoqui-Rojo, L., Flores-Verdugo, F.J., Hernández-Carmona, G. et al. (2012). Nutrient removal using two species of mangrove (Rhizophora mangle and Laguncularia racemosa) in experimental shrimp (Litopenaeus vannamei) culture ponds. Ciencias Marinas. 38: 333-346.
- Nandan, S.B. and Azis, P.A. (1990). Studies on BOD sub (5) and Dissolved Oxygen in the Kadinamkulam Kayal, Southern Kerala. Mahasagar. 23: 95-101.
- Naskar, S., Biswas, G., Kumar, P., De, D., Sawant, P.B. et al. (2022). Effects of estuarine oyster, Crassostrea cuttackensis as the extractive species at varied densities on productivity and culture environment in brackishwater integrated multi-trophic aquaculture (BIMTA) system. Aquaculture. 554: 738128. DOI: 10.1016/j.aquaculture.2022.738128.
- Officer, C.B., Smayda, T.J. and Mann, R. (1982). Benthic filter feeding: A natural eutrophication control. Mar. Ecol. Prog. Ser. 9: 203-210.
- Omont, A., Elizondo-Gonz´alez, R., Quiroz-Guzm´an, E. et al. (2020). Digestive microbiota of shrimp Penaeus vannamei and oyster Crassostrea gigas co-cultured in integrated multi- trophic aquaculture system. Aquaculture. 521: 059-735.
- Petersen, C., Costa-Pierce, B.A., Dumbauld, B.R., Friedman, C. et al. (2010). Ecosystem Concepts for Sustainable Bivalve Mariculture. The National Academies Press.
- Rahman, A., Dabrowski, J. and McCulloch, J. (2020). Dissolved oxygen prediction in prawn ponds from a group of one step predictors. Information Processing in Agriculture. 7: 307-317.
- Rejeki, S., Ariyati, R.W. and Widowati, L.L. (2016). Application of integrated multi tropic aquaculture concept in an abraded brackish water pond. Jurnalteknologi. 78: 4-2.
- Sanz-Lazaro, C., Fernandez-Gonzalez, V., Arechavala-Lopez, P. et al. (2018). Depth matters for bivalve culture in integrated multitrophic aquaculture (I.M.T.A.) and other polyculture strategies under non-eutrophic conditions. Aquaculture International. 26: 1161-1170.
- Sasikumar, G. and Viji, C.S. (2015). Integrated Multi-Trophic Aquaculture Systems (I.M.T.A.).
- Troell, M., Halling, C., Neori, A. et al. (2003). Integrated mariculture: Asking the right questions. Aquaculture. 226: 69-90.
- Troell, M., Joyce, A., Chopin, T. et al. (2009). Ecological engineering in aquaculture-potential for integrated multi-trophic aquaculture (IMTA) in marine offshore systems. Aquaculture. 297: 1-9.
- Troell, M., Naylor, R.L., Metian, M. et al. (2014). Does Aquaculture Add Resilience to the Global Food System?. Proceedings of the National Academy of Sciences. 111: 13257-13263.
- Viji, C.S., Chadha, N.K., Kripa, V. et al. (2014). Can oysters control eutrophication in an integrated fish-oyster aquaculture system?. Journal of the Marine Biological Association of India. 56(2): 67-73.
- Wetz, M.S., Lewitus, A.J., Koepfler, E.T. et al. (2002). Impact of the eastern oyster Crassostrea virginica on microbial community structure in a salt marsh estuary. Aquatic Microbial Ecology. 28: 87-97.
- Xing, M., Hou, Z., Yuan, J. et al. (2013). Taxonomic and functional metagenomic profiling of gastrointestinal tract microbiome of the farmed adult turbot (Scophthalmus maximus). FEMS Microbiology Ecology. 86: 432-443.
- Zhuang, W., Yu, X., Hu, R. et al. (2020). Diversity, function and assembly of mangrove root-associated microbial communities at a continuous fine-scale. Biofilms and Microbiomes. 6: 1-10.
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