building to support the Promotion Trials. Activities included schemes for the creation of officially recognized Farmer Trainers, training agricultural extension staff in convening/moderation skills and developing local-level understanding of how better integration of farming enterprises can boost productivity and conserve the natural environment.

At least 30 government staff working at provincial and district levels in five provinces, have benefited from these types of capacity building activities. With FAO support, DLF developed new approaches to staff training to build this capacity, which places a greater emphasis on “Peer-to-Peer” learning techniques and takes advantage of new communication opportunities available through social media. Local government staff in the five provinces say they now have more “confidence” to engage with poor communities and welcome the new approaches to capacity building which focus on their workplace and increase professional exchange with their peers.

**10. Effectiveness of international support**

Based on estimates from monitoring data collected during 2017, farming families participating in Promotion Trials generated additional fish for family consumption and fish seed worth approximately USD 85 200. During 2018, the monetary value of Trial production is confidently expected to increase to at least USD 100 000. This represents a total contribution to the local economy of approximately USD 185 000 over two years.

<figure><img src="image_119.png" /><figcaption>**Figure 9:** Food Aid provided to a village school in Savannakhet by World Food Programme (WFP).</figcaption></figure>

While these figures are approximate, they can be used to illustrate the effectiveness of the FAO/DLF partnership. Over the same two-year period, the FAO local contribution was approximately USD 124 000, which indicates that FAO's investment in developing DLF's institutional capacity has been effective. Within two years, it has produced tangible benefits to the food and nutrition security of poor communities in five provinces worth at least 150 percent of the total investment. These benefits are also likely to further increase, as the FAO intervention was designed to be sustained both in terms of the changes farmers have made to their farming systems and in terms of the developments in government staff capacity.

A comparison with alternative strategies to improve food and nutrition security in the Lao People's Democratic Republic is also useful. For example, many poor rural communities are supported by food donations from the World Food Program (e.g. as support to school lunch programs), and WFP average
expenditure per beneficiary has gradually increased over the last few years to nearly USD 40 in the Asia-Pacific region (World Food Assistance 2017 - Taking Stock and Looking Ahead). If WFP were to provide this type of assistance to 200 families over two years, it would cost approximately USD 88 000. While the FAO contribution is initially greater, the longer-term benefits of strengthening DLF's institutional capacity and establishing more resilient and efficient farming systems among poor communities, makes this investment a more effective strategy.
# RACEWAY-IN-POND AQUACULTURE SYSTEM

Liu Xingguo, Xu Hao, Gu Zhaojun, Wang Xiaodong

## Abstract

A combined ecological engineering facility composed of aquaculture ponds linked to an ecological ditch, an ecological pond, and a subsurface flow constructed wetland was designed and tested as a Raceway-in-Pond Aquaculture System (RPAS). The mean removal rates of ammonia nitrogen (NH<sup>4</sup>-N), total nitrogen (TN), total phosphorus (TP), potassium permanganate index (CODMn), and chlorophyll a (Chl-a) by the ecological depurating facilities were 44.2, 47.6, 63.4, 61.5, and 83.0 percent, respectively. These were significantly lower than in the control pond (*p*<0.05). Compared with traditional pond aquaculture, the RPAS increases the fish production from 0.75 to 0.82 (mean value) kg/m<sup>3</sup>, and reduces the feed coefficient ratio by 8.2 percent. By improving the water quality and providing a good culture environment, the RPAS contributes to improve the culture efficiency.

## 1 Introduction

In China, the freshwater ponds cover 2 668.835 km<sup>2</sup>, and produce 22.11 million tonnes, accounting for almost 74.7 percent of the total freshwater aquaculture products (China Fisheries Year Book, 2019). However, most of China aquaculture ponds were built during the 1960s and 1970s and many problems have arisen since, among which the extensive production, the inefficient use of water resources or the pollution, which seriously impede any further development of pond aquaculture (Xu, Liu, Wu, 2009). In Hangjiahu district, Zhejiang province, the production of 1 kg of freshwater fish is reported to consume 4 to 6.5 m<sup>3</sup> of water, and the annual emissions of permanganate index (CODMn), total nitrogen (TN) and total phosphorus (TP) were 199 kg 101 kg, 5.0 kg per 1 hm<sup>2</sup> aquaculture pond. The cumulative impacts of pond aquaculture have thus become an important issue in China (Zhou and Wen, 2004; Huang *et al.*, 2007).

Ecologically-engineered aquaculture systems are an environmentally friendly and healthy alternative. Indeed, by using ecological engineering to design and construct pond aquaculture systems, it is possible to regulate the water quality and control the pollution. This paper describes the first freshwater recirculating aquaculture pond system designed in China, which consists of three purification units (ecological ditch, ecological pond and composite artificial wetland) and culture ponds. A running test was conducted over a 210 days rearing period, in order (1) to investigate the purification effects of the different ecologically-engineered facilities on the water discharged by aquaculture and (2) to provide a reference for constructing ecologically-engineered pond aquaculture system in support to the freshwater fish farming in China. The primary results are presented in this article.

## 2 Material and methods

### 2.1 The Raceway-in-Ponds Aquaculture Systems (RPAS)

#### 2.1.1 Design equations

The ecologically-engineered pond facilities and recirculating aquaculture system were designed by following the relevant standards and results from related studies. The following equations were used:

Sub-surface Flow Constructed Wetland (SFCW) - Eq. (1):

$$ \text{SFCW volume: } V = Q_{av} t / \varepsilon \quad (1) $$
where Qav is the average flow (m³/d), t is the hydraulic retention time (d), V is wetland volume (m³), and ε is SFCW porosity (dimensionless) (HJ, 2011).

Ecological ditch and ecological pond - Eq. (2):

$$ \text{area: } A = QS_0 t / N_a \qquad (2) $$

where Q is the sewage flow (m³/d), S₀ is influent BOD₅ (g/m³), t is the water dwelling time (d), and Nₐ is area load (g/(m²·d)) (HICEA, 1994).

The RPAS was constructed by using three traditional static ponds (P1, P2 and P3) and 200 m of drainage ditch at Punan aquafarm (31°57'01"N, 120°08'52"E), Songjiang district, Shanghai, China. Considering the results from previous trials, the daily volume of water recycled was set to be 10 percent (Liu and He, 1992). The regulating reservoir was used to construct an ecological pond and the subsurface flow wetland. According to Eq. (1) and characteristics of CODMn in the pond water discharge, t was determined to be 0.4 d, with ε = 0.50 (gravel of average diameter of 50 mm), and Qav = 1500 m³/d, V was 1200 m³. The depth of the SFCW was 0.7 m, and the surface was 1500 m². According to Eq. (2) and the concentrations of BOD₅ (g/m³) in pond water discharge, it was determined that Nₐ was 40 g/(m²·d), Q was 1500 m³/d, t was 1.5 d, and the eco-pond area (a) was 2750 m².

### 2.1.2 System construction

The RPAS covers 2 hectares and consists of three culture ponds (15000 m²) and three purification units that include an ecological ditch (500 m²), an ecological pond (2500 m²) and a 1500 m² sub-surface flow constructed wetland (SFCW). The three culture ponds are connected in series, and drainage channels are located on both sides of the ponds, with the ecological pond (eco-pond) and SFCW at one end. The ecological ditch (eco-ditch) is also connected with the external river so that water replenishment can be performed. The components of the system have different elevation levels. The ponds and eco-ditch have the same elevation, but the eco-pond is higher by 30 cm than eco-ditch and by 35 cm than SFCW. There is a water pump at the end of eco-ditch to fill the ecological pond so that when water is added, it flows by gravity into the SFCW, before entering a re-aeration pond, and the culture pond 1, 2 and 3. The water also can flow into eco-ditch from the bottom of pond 3, thus forming the recirculating system (Figure 1).

<figure><img src="image_120.png" /><figcaption>**Figure 1:** Layout of the RAPS.</figcaption></figure>

### 2.2 Experiment

The experiment was conducted during 210 days, from 15 March 2014 to 14 November 2014. A static pond near the RPAS was selected as a control (Figure 2). The control pond without recirculation corresponded to the stagnant water conditions, representative of traditional aquaculture ponds. In the culture ponds (P1, P2 and P3) and control, fish were stocked in polyculture, associating grass carp (*Ctenopharyngodon idellus*) (45 percent of the total weight), blunt-snout bream (*Megalobrama amblycephala*) (40 percent of the total weight), as well as silver carp (*Hypophthalmichthys molitrix*), bighead carp (*Aristichthys nobilis*) and crucian carp (*Carassius cuvieri*) altogether accounting for 15 percent of the total weight. The initial stocking density was 0.15 kg/m³ in each pond. During the experiment, fish were fed 10000 kg of feed, with the same quantity in each pond. The pump water flow was 120 m³h⁻¹, the daily circulated volume was 2800 m³/day, and the actual daily exchange rate of the pond water was 9.6 percent.
<figure><img src="image_121.png" /></figure>

©Liu Xingguo

<caption>**Figure 2:** Components of the Raceway-in-Pond Aquaculture System: a) ecological ditch, b) ecological pond and SFCW c) overview of the RPAS.</caption>

# 3 Results

## 3.1 Water quality in RPAS

With the exception of COD<sub>Mn</sub> for which concentration gradually reduced overtime in the different RPAS units (p<0.05), the quantity of TN, NH<sub>4</sub><sup>+</sup>-N and TP remained stable throughout the progress of the growing-out (p>0.05). In contrast, COD<sub>Mn</sub>, TN and NH<sub>4</sub><sup>+</sup>-N in the control pond kept on increasing during the same period. The NH<sub>4</sub><sup>+</sup>-N concentration increased from 0.68 mg/l in March to 1.45 mg/l in October, a 2.13 folds increase. At the end of the experiment, the concentrations of COD<sub>Mn</sub>, TN and NH<sub>4</sub><sup>+</sup>-N were all significantly higher in control than in the RPAS (p<0.05, Figure 3)).

<figure><img src="image_122.png" /></figure>
<figure><img src="image_123.png" /><figcaption>Fig. 3: Water quality and purification efficiency.</figcaption></figure>

## 3.2 Fish production

The fish production parameters in the RPAS and control are presented in Table 1. At the end of the experiment, the mean yield in RPAS was 0.82 kg/m³ and the mean feed conversion ratio (FCR) was 1.22. In the control pond, the fish yield was 0.75 kg/m³ and the FCR 1.33. The fish production in the RPAS was thus 8.5 percent higher than in the traditional pond, and the FCR was 8.2 percent lower. Meanwhile, there was also difference in fish yield and FCR between the three culture ponds. The production was obviously higher in P1 than in P2 and P3 (Table 1).

<table><caption>Table 1: Production of the RPAS</caption><thead><tr><th></th><th>Initial weight<br>kg</th><th>Stocking<br>density<br>kg/m³</th><th>Harvest<br>weight<br>kg</th><th>Yield<br>kg/m³</th><th>Feed weight<br>kg</th><th>Feed<br>coefficient</th></tr></thead><tbody><tr><td>Pond 1</td><td>1 500</td><td>0.2</td><td>8 406</td><td>0.84</td><td>10 000</td><td>1.19</td></tr><tr><td>Pond 2</td><td>1 500</td><td>0.2</td><td>8 320</td><td>0.83</td><td>10 000</td><td>1.20</td></tr><tr><td>Pond 3</td><td>1 500</td><td>0.2</td><td>7 874</td><td>0.79</td><td>10 000</td><td>1.27</td></tr><tr><td>Control pond</td><td>1 500</td><td>0.2</td><td>7 515</td><td>0.75</td><td>10 000</td><td>1.33</td></tr></tbody></table>

## 3.3 Water-savings and emission-reduction

In China, traditional aquaculture ponds exchange water 3 to 5 times a year, but only 1 or 2 times a year in RPAS system. Moreover, the discharged water is depurated by the ecological pond. Table 2 compares the water consumption and pollution emission by RPAS and traditional static pond aquaculture systems. RPAS saves 63.6 percent of water, compared to the traditional system, and reduces the emission of TN, TP and COD<sub>Mn</sub> by 87.8 percent, 91.7 percent and 78.1 percent, respectively. (Table 2)

<table><caption>Table 2: Water consumption and pollution comparison of ecological engineering and the traditional pond aquaculture</caption><thead><tr><th rowspan="2">Item</th><th colspan="2">Water losses m³/kg</th><th rowspan="2">TN emissions<br>g/kg fish</th><th rowspan="2">TP<br>emissions<br>g/kg fish</th><th rowspan="2">COD<sub>Mn</sub><br>emissions<br>g/kg fish</th></tr><tr><th>Evaporation</th><th>Water exchanges and<br>drainage</th></tr></thead><tbody><tr><td>Traditional pond<br>aquaculture</td><td>0.18</td><td>5.25</td><td>15.9</td><td>2.64</td><td>49.5</td></tr><tr><td>Ecological engineering<br>pond aquaculture</td><td>0.18</td><td>1.95</td><td>1.95</td><td>0.22</td><td>10.9</td></tr><tr><td>Average reduction ratio<br>percent</td><td></td><td>63.6</td><td>87.8</td><td>91.7</td><td>78.1</td></tr></tbody></table>

Note: Total nitrogen emissions (emissions of per unit of production) = emissions of total nitrogen × water discharge of per unit product. Total phosphorus and COD<sub>Mn</sub> emissions calculated with the total nitrogen emissions.
## 4 Results and discussions

Although the nutrient concentrations in the control pond increased during the growing-out period, they remained stable (TN, TP and $NH_4^+$-N) or even decreased ($COD_{Mn}$) in the RPAS system. The purification units, consisting of the eco-ditch, eco-pond and SFCW thus proved to be effective (Figure 2). These units are a natural treatment system based on a biological symbiosis between macrophytes (*Phragmites* sp., *Acorus* sp., etc.), microorganisms (bacteria, fungi, algae), and their interactions with the soil and water chemistry (Schulz, Gelbrecht and Rennert, 2003). On the other side, the water quality in the culture ponds decreased with the water flow. This is probably the consequence of fact that the first pond (P1) was continuously replenished with clean water (i.e. the final effluent after the purification units) (Zhang *et al.*, 2011). However, monthly variations were also observed, as a result of seasonal oscillations, including physicochemical and biological variations within the purification units, influent fluctuation, and climate changes.

The fish production efficiency highlights the purification effects by the RPAS, which provides better environmental conditions to fish during the rearing period, contributes to an accelerated growth and minimizes the FCR, thus improving the overall culture efficiency (Zhang *et al.*, 2011).

The present study also revealed that RPAS saved 63.6 percent of water, compared to the traditional pond, and reduced the emission of TN, TP and $COD_{Mn}$ by 87.8 percent, 91.7 percent and 78.1 percent, respectively. Constructing ecological engineering facilities might be an effective way to control aquaculture pollution.

However, some researchers believe that ecological engineering facilities such as this constructed wetland are too space-consuming (Sindilariu, Wolter and Reiter, 2008). Therefore, in order to maximize the beneficial effects of the engineering facilities, it will be necessary to assess the most reasonable surface ratio between the purification units and the aquaculture pond.

## 5. Acknowledgments

This study was funded by the “Twelve Five” Project, National Science and Technology Program “Freshwater aquaculture pond ecosystem engineering control technology research (2012BAD25B01)”. We would like to thank the colleagues from the ponds ecological engineering research centre of the Chinese Academy of Fishery Sciences for their help with field sampling, and the editors and reviewers for their helpful suggestions and comments.

## 6. References

* **China Agriculture Press.** 2019. *China Fisheries Year Book 2019*. Beijing, China: 21-49. (in Chinese).

* **Harbin Institute of Civil Engineering and Architecture (HICEA).** 1994. *Design Rules on Wastewater Stabilization Ponds*. China Plan Publishing Company, Beijing, China: 22 p. (in Chinese).

* **HJ.** 2011. HJ 2005-2010. *Technical specification of constructed wetlands for wastewater treatment engineering*. Chinese standard, Ministry of Environmental Protection, Beijing, China. 9 p.

* **Huang, H., Wang, X. Q., Wei, X. H., He, X. Y., Zhang, M. & Yao, W. Z.** 2007. A research on the quantity of discharged pollutant of freshwater breed aquatics in Hangjiahu area. *Environmental Monitoring in China* 23(2): 94-97. (in Chinese with English abstract).

* **Schulz, C., Gelbrecht, J. & Rennert, B.** 2003. Water quality and nutrient budget in closed shrimp (*Penaeus monodon*) culture systems, *Aquacult. Eng.* 27: 159-176.
Sindilariu, P.D., Wolter, C. & Reiter, R. 2008. Constructed wetlands as a treatment method for effluents from intensive trout farms. *Aquaculture* 277: 179-184.

Xu, H., Liu, X.G. & Wu, F. 2009. Freshwater ponds standardize and culture system constructed, *Chinese Fishery* 8: 7-9. (in Chinese with English abstract).

Zhang, S. Y., Li, G., Wu, H. B., Liu, X. G., Yao, Y. H., Tao, L. & Liu, H. 2011. An integrated recirculating aquaculture system (RAS) for land-based fish farming: The effects on water quality and fish production. *Aquacult. Eng.* 45: 93-102.

Zhou, J. F. & Wen, Y. M. 2004. Effects of fish aquaculture on water environment in the Zhujiang river delta, *Acta Scientiarum Natcralium Universitatis Sunyatseni* 43(5): 104-106. (in Chinese with English abstract).
# INCREASING CARP AND SMALL INDIGENOUS SPECIES PRODUCTION IN SEMI-INTENSIVE PONDS THROUGH ENHANCING PERIPHYTON GROWTH

Sunila Rai, Kamala Gharti, Madhav Shrestha, Sabita Jha, Rajan Poudel, Rahul Ranjan, James Diana, Hillary Egna

## Abstract

Carp is the major group of fish grown in South Asia. However, productivity of carp is still low. From 2014 to 2017 on-station and on-farm trials were conducted in Nepal to evaluate production of carp (Silver carp *Hypophthalmichthys molitrix*, Bighead carp *Aristichthys nobilis*, Grass carp *Ctenopharyngodon idella*, Common carp *Cyprinus carpio*, Rohu *Labeo rohita* and Mrigal *Cirrhinus mrigala*) and small indigenous fish species (SIS) such as *Dedhuwa Esomus danricus* and *Pothi Puntius sophore*. Profit in a periphyton enhanced system and performances of various substrates (split bamboo, whole bamboo, banana midrib, plastic bottle) were also tested. Results showed that the yield of carp, FCR and profit were better in periphyton enhanced ponds. An on-station trial using split bamboo as a substrate with 50 percent feeding revealed that the net yield of carp was 55 percent higher in carp-SIS ponds with periphyton enhancement (5.45 ± 0.45 t/ha/yr) compared to without periphyton ponds (3.51 ± 0.42t/ha/yr). Reduced feed input and periphyton enhancement resulted in increased profit in carp-SIS ponds with periphyton enhancement by 109 percent over ponds without periphyton enhancement. No such differences were found in field trials except in FCR. All experimental substrates split bamboo, whole bamboo, banana midrib and plastic bottle were equal in terms of carp and SIS production and profit from carp. However, banana midrib was not durable and decayed faster requiring replacements 3-4 times during the experimentation period. Thus reduced feeding with split bamboo as a periphyton substrate has been found to be effective for small-scale farmers.

## 1. Introduction

Carp polyculture is practiced throughout South Asia, however, yields from these systems are less than optimum (Jha *et al.*, 2018). In Nepal, carp polyculture is the major aquaculture system used, contributing about 87.5 percent of total fish production (Kunwar and Adhikari, 2016). Carp are grown semi-intensively using fertilizers and supplementary feed where the feed cost is up to 70 percent of total operational cost (Yadav and Rai, 2014). For small-scale farmers it is hard to bear the feed cost. Providing an alternative means to reduce the feed cost has thus become essential for economic viability of the system to small-scale farmers. In most pond production systems, only a small proportion of nutrient input (30 percent) is converted into harvestable matter while the rest is lost into sediments, effluent water and atmosphere (Acosta Nassar *et al.*, 1994; Beveridge *et al.*, 1994; Olah *et al.*, 1994). Improving the conversion of nutrients into harvestable matters by enhancing the natural food production may be a suitable solution to the problem of higher cost, as well as loss of nutrient inputs. Enhancing the growth of periphyton in pond production systems has been proved to be a suitable method to increase the natural food production (Azim *et al.*, 2001a; Rai *et al.*, 2008; Jha *et al.*, 2018).

Many fish in wild, as well as in culture, rely on periphyton for its food. Indian major carp (Wahab *et al.*, 1999; Ramesh *et al.*, 1999; Rai *et al.*, 2010), tilapia (Hem and Avit, 1994; Dabbadie, 1996; Shrestha and Knud-Hansen, 1994; Milstein *et al.*, 2009; Jiwyam, 2013), common carp (Rai and Yi, 2012) as well prawn (Udin *et al.*, 2007) prefer periphyton as natural food. Significant research in periphyton based aquaculture was carried out using different substrates such as bamboo poles, PVC pipes, sugarcane bagasse, jute stick, plastic sheet, bamboo side branches, rice straw, coconut coir and coconut shell in Bangladesh, India and Nepal (Azim *et al.*, 2001a; Azim *et al.*, 2001b; Azim *et al.*, 2002; Keshavnath *et al.*, 2001a, Rai *et al.*, 2008; Shirin *et al.*, 2013; Santhiya *et al.*, 2017; Jha *et al.*, 2018). Among these substrates, bamboo and coconut coir was better (Keshavnath *et al.*, 2001; Azim *et al.*, 2002; Van Dam *et al.*, 2002, Santhiya *et al.*, 2017).
Carp-SIS polyculture is not new to Nepal. Farmers have been harvesting varieties of SIS from household ponds for a long time. The technology received more attention starting in 2009, when formal studies began in Terai, Nepal with technical support from Bangladesh. It added nutrition sensitivity to the aquaculture due to micro-nutrient rich nature of SIS (Roos et al., 2006, Rai et al., 2014). In Nepal, three recent consecutive studies have been done to evaluate the production of carp and SIS and the profitability in periphyton enhanced systems. Technology and results of carp polyculture and carp-SIS polyculture in periphyton enhanced systems tested on the research station and in farmers' pond have been summarized in this paper chronologically.

## 2. Effect of substrates on carp production

Periphyton is considered an appropriate natural food for fish (Hepher, 1988). The nutritive value of periphyton is high (ash 15-19 percent, protein 23-26 percent, energy 19-20 kJ/g) (Azim et al., 2002). It is estimated that potential fish production from a periphyton enhanced pond is around 5 t/ha/y (Azim et al., 2001b; Van Dam et al., 2002). However, in practice fish production obtained from the system is less than this figure. A preliminary trial was carried out in farmers' ponds to assess effect of split bamboo substrate on carp polyculture. The trial was done at Sukranagar Village Development Committee in Chitwan District for 240 days from 20 April to 28 December 2014. The experiment included two treatments: T1 (Carp) and T2 (Carp+bamboo substrate) and four replicates. Fingerlings of Silver carp (20 percent), Bighead carp (5 percent), Grass carp (30 percent), Common carp (15 percent), Rohu (20 percent) and Mrigal (10 percent) were stocked at a rate of 20 000 fish/ha whereas two SIS, Dedhuwa and Pothi were stocked at a rate of 50 000 fish/ha in 1:1 ratio. Prior to stocking, split bamboo mats (Figure 1) were attached in substrate ponds to enhance periphyton growth covering 2 percent of pond surface area. Carp were fed with dough of rice bran and mustard oil cake (1:1) at the rate of 3 percent BW/day and Grass carp with grass and banana leaves at 50 percent BW/day. Water quality parameters such as temperature, Secchi disk visibility, DO and pH were monitored biweekly.

<figure><img src="image_124.png" /><figcaption>**Figure 1:** Split bamboo mat used as a substrate in the on-farm trial.</figcaption></figure>

Although a periphyton feeder like Rohu and Common carp, Catla was not included in the experiment but was replaced Bighead carp. Growth rate and net yield of Rohu (0.8 ± 0.0 g/fish/day and 0.9 ± 0.0 t/ha/yr) and Common carp (2.1 ± 0.1 g/fish/day and 0.8 ± 0.1 t/ha/yr) was higher in periphyton enhanced ponds because both species benefitted from periphyton (Rai et al., 2012) and supplementary feed. Despite higher yield of Rohu and Common carp in periphyton enhanced ponds, net yield of carp did not differ between carp ponds with and without periphyton enhancement (Table 1). Full feeding (3 percent BW) was used in the experiment which might have supplied sufficient nutrients for growth of carp and thus carp may not have used periphyton. Therefore, periphyton enhancement at full feeding of 3 percent BW did not reduce the feed input and gross margin remained unaffected (Table 2). Periphyton
enhancement at full feeding was not found effective probably due to sufficient supplementary feed in the system but the periphyton technology could be effective in carp polyculture with reduced feeding.

<table><caption>**Table 1:** Yield and FCR in carp and carp + substrate treatments (mean ± SE)</caption><thead><tr><th rowspan="2">Yield (t/ha/yr)</th><th colspan="2">Treatment</th></tr><tr><th>Carp</th><th>Carp + Substrate</th></tr></thead><tbody><tr><td>GFY of carp only (t/ha/yr)</td><td>5.40 ± 0.06<sup>a</sup></td><td>5.69 ± 0.21<sup>a</sup></td></tr><tr><td>NFY of carp only (t/ha/yr)</td><td>4.04 ± 0.06<sup>a</sup></td><td>4.31 ± 0.13<sup>a</sup></td></tr><tr><td>Feed conversion ratio (FCR)</td><td>3.34 ± 0.07<sup>a</sup></td><td>3.23 ± 0.02<sup>a</sup></td></tr></tbody></table>

Similar superscripts for values in a row indicate no significant difference among the values.

<table><caption>**Table 2:** Gross margin (NRP/100 m²/240 days) analysis in carp and carp + substrate treatments (mean ± SE)</caption><thead><tr><th rowspan="2"></th><th colspan="2">Treatment</th></tr><tr><th>Carp</th><th>Carp + Substrate</th></tr></thead><tbody><tr><td>Feed</td><td>3 008 ± 38<sup>a</sup></td><td>3 045 ± 59<sup>a</sup></td></tr><tr><td>Total variable cost</td><td>4 205 ± 38<sup>b</sup></td><td>4 367 ± 59<sup>a</sup></td></tr><tr><td>Return</td><td>7 771 ± 85<sup>a</sup></td><td>8 181 ± 169<sup>a</sup></td></tr><tr><td>Gross margin</td><td>3 565 ± 109<sup>a</sup></td><td>3 814 ± 120<sup>a</sup></td></tr></tbody></table>

Similar superscripts for values in a row indicate no significant difference among the values.

Note: Exchange rate used was USD 1 = NRP 101.4 during fish harvesting.

### 3. Production of periphyton to enhance yield in polyculture ponds with carp and small indigenous species

Carp polyculture is the major aquaculture system in Nepal. Pond production largely goes to the market. Intentional inclusion of SIS into carp polyculture helps these systems contribute to household consumption and nutrition. The intake of nutrient-rich SIS intended to improve the health and nutrition of women and children because vitamin A, calcium, zinc, and iron are found to be much higher in the eyes, head, organs, and viscera of SIS (Roos et al., 2007). Adding periphyton substrates to these ponds should increase fish production and nutrition. An experiment was conducted at Agriculture and Forestry University (AFU), Chitwan, Nepal to develop a cost effective means to increase fish production. The experimental period was 210 days from 24 August 2014 to 28 March 2015. The experiment included four treatments, T₁ (Carp+100 percent feeding), T₂ (Carp+SIS+100 percent feeding), T₃ (Carp+SIS+50 percent feeding+Bamboo substrate) and T₄ (Carp+SIS+Bamboo substrate) each with three replications. Silver carp (20 percent), Bighead carp (5 percent), Grass carp (20 percent), Common carp (20 percent), Rohu (25 percent) and Mrigal (10 percent) were stocked at a density of 15 000 fish/ha whereas two SIS, Dedhuwa and Pothi were stocked at a ratio of 1:1 and at a density of 50 000 fish/ha. Carp excluding Grass carp were fed daily with freshly made dough of mustard oil cake and rice bran (1:1) at the rate of 2 percent BW whereas Grass carp was fed daily with grass at 50 percent BW. Floats and sinkers were tied to two ends of top and base of split bamboo mats (Figure 2) to suspend them in the water column in each substrate pond. Substrate covered 1 percent surface area of a substrate pond.
<figure><img src="image_125.png" /></figure>

©Hillary Egna

**Figure 2:** Split bamboo mat used as a substrate with floats and sinkers tied to the top ends and bottom ends in the experiment. Vertically suspended split bamboo mat in the experimental pond.

On station trial revealed that carp are benefitted by periphyton enhancement. Yield of carp and combined fish yield were best in ponds with reduced feeding (1 percent BW) and periphyton enhancement (Table 3). SIS production was higher in T₂ with SIS and carp at 100 percent feeding (2 percent BW) than in T₃ or T₄. FCR was best (1.02) in T₃ compared to the other two feeding treatments. Lower FCR in substrate ponds indicated periphyton could decrease feed supply to carp. However, in terms of profit, the reduced feeding treatment (T₃) and no feeding treatment (T₄) performed best (Table 4). Some of these results were probably affected by the grow-out schedule, including three months (mid November to mid February) of winter conditions when growth in all treatments was reduced and feed consumption was also changed. Most likely, full feeding would have been the second most profitable and productive system if the trials were conducted only during warm temperatures. Nevertheless, carp-SIS polyculture with reduced-feeding including periphyton-enhancement seemed most productive and profitable.

<table><caption>**Table 3:** Yields of carp and SIS in different treatments (mean ± SE)</caption><thead><tr><th rowspan="2"></th><th colspan="4">Treatment</th></tr><tr><th>T<sub>1</sub></th><th>T<sub>2</sub></th><th>T<sub>3</sub></th><th>T<sub>4</sub></th></tr></thead><tbody><tr><td>NFY of carp only (t/ha/yr)</td><td>4.36 ± 0.47<sup>ab</sup></td><td>3.51 ± 0.42<sup>b</sup></td><td>5.45 ± 0.45<sup>a</sup></td><td>4.15 ± 0.40<sup>ab</sup></td></tr><tr><td>NFY of SIS only (t/ha/yr)</td><td>-</td><td>0.21 ± 0.07<sup>a</sup></td><td>0.05 ± 0.02<sup>b</sup></td><td>0.05 ± 0.02<sup>b</sup></td></tr><tr><td>Combined NFY (t/ha/yr)</td><td>4.36 ± 0.47<sup>ab</sup></td><td>3.72 ± 0.36<sup>b</sup></td><td>5.52 ± 0.43<sup>a</sup></td><td>4.20 ± 0.41<sup>ab</sup></td></tr><tr><td>Feed conversion ratio (FCR)</td><td>2.44 ± 0.30<sup>a</sup></td><td>2.44 ± 0.21<sup>a</sup></td><td>1.02 ± 0.06<sup>b</sup></td><td>-</td></tr></tbody></table>

Similar superscripts for values in a row indicate no significant difference among the values.

T₁ – Carp+100 percent feeding, T₂ – Carp+SIS+100 percent feeding, T₃ – Carp+SIS+50 percent feeding + bamboo substrate, T₄ – Carp + SIS + bamboo substrate

<table><caption>**Table 4:** Gross margin (NRs/100 m²/210 days) analysis of different treatments (mean ± SE)</caption><thead><tr><th rowspan="2"></th><th colspan="4">Treatment</th></tr><tr><th>T<sub>1</sub></th><th>T<sub>2</sub></th><th>T<sub>3</sub></th><th>T<sub>4</sub></th></tr></thead><tbody><tr><td>Cost</td><td></td><td></td><td></td><td></td></tr><tr><td>Feed</td><td>1 627 ± 166<sup>a</sup></td><td>1 382 ± 7<sup>a</sup></td><td>871 ± 47<sup>b</sup></td><td>-</td></tr><tr><td>Total variable cost</td><td>3 248 ± 166<sup>a</sup></td><td>3 056 ± 10<sup>a</sup></td><td>2 796.8 ± 46.7<sup>b</sup></td><td>1 851 ± 3.2<sup>c</sup></td></tr><tr><td>Return</td><td></td><td></td><td></td><td></td></tr><tr><td>Carp</td><td>6 440 ± 6 80<sup>ab</sup></td><td>5 200 ± 613<sup>b</sup></td><td>8 031 ± 631<sup>a</sup></td><td>6 136 ± 574<sup>ab</sup></td></tr><tr><td>SIS</td><td>-</td><td>509 ± 101<sup>a</sup></td><td>324 ± 45<sup>a</sup></td><td>383 ± 29<sup>ab</sup></td></tr><tr><td>Gross return</td><td>6 440 ± 680<sup>ab</sup></td><td>5 710 ± 525<sup>b</sup></td><td>8 355 ± 613<sup>a</sup></td><td>6 519 ± 563<sup>ab</sup></td></tr><tr><td>Gross margin</td><td>3 193 ± 622<sup>bc</sup></td><td>2 654 ± 520<sup>c</sup></td><td>5 558 ± 588<sup>a</sup></td><td>4 618 ± 566<sup>ab</sup></td></tr></tbody></table>
Similar superscripts for values in a row indicate no significant difference among the values.

T₁ – Carp+100 percent feeding, T₂ – Carp+SIS+100 percent feeding,

T₃ – Carp+SIS+50 percent feeding+periphyton enhancement, T₄- Carp+SIS+periphyton enhancement

Note: Exchange rate used was USD 1 = NRP 99.6 during fish harvesting.

**4. Potential substrates for periphyton enhancement in carp-SIS polyculture**

Substrate is one of the key factors in determining fish production in a periphyton enhanced aquaculture system. The substrate type determines quantity and quality of periphyton. Periphyton biomass was found greater in natural substrates due probably to hydrophilic nature of the materials or leaching of nutrients from the substrates (Van Dam *et al.*, 2002). In addition to growing periphyton, substrate also drives away predators and poachers. In previous experiments, split bamboo mats were used as a periphyton substrate. Although yields were better in split bamboo ponds, farmers faced difficulty in partial harvesting of both carp and SIS. Substrates interfered in the netting of fish, although on the positive side, they may also have provided hiding places for fish to avoid predation by birds. Thus, an experiment was carried out to assess alternative substrates for periphyton enhancement in farmer's ponds in Nawalparasi district. Prior to the experiment, a workshop was organized to learn farmers' choices and perspectives on types of substrate.

Based on farmers' suggestions, four locally available substrates split bamboo, whole bamboo, banana midrib and plastic bottle (Figure 3) were tested for periphyton enhancement in farmers' ponds at Seri and Nandapur in Nawalparasi district for 7 months from 12 April to 10 November 2017. Six carp species as in previous experiments Silver carp (20 percent), Bighead carp (5 percent), Grass carp (20 percent), Common carp (20 percent), Rohu (25 percent) and Mrigal (10 percent) were stocked at 15 000 fish/hectare whereas SIS (Dedhuwa and Pothi) were stocked at unrecorded densities. Eggs and juveniles of SIS were simply allowed to enter the ponds along canal water through water inlet. Considering best results obtained with reduced feeding in previous experiments, the feeding rate was fixed at 1.5 percent BW/day for carp in this experiment while feeding rate of Grass carp was kept same of 50 percent BW/day.

<figure><img src="image_126.png" /><figcaption>**Figure 3:** Banana mid rib (a), whole bamboo (b), plastic bottles (c) used as substrates in the on-farm trial.</figcaption></figure>

The yields of carp and SIS and gross margin in each treatment ponds are given in Tables 5 and 6, respectively. Yields of carp and SIS, and gross margin were the same in all ponds indicating that fish were not benefitting from substrates and periphyton enhancement as in a previous trial in farmers' ponds. In on-farm trials farmers do the pond management, and level of management varies farmer to farmer to affect the results. Among substrates used split bamboo, whole bamboo and plastic bottles were more durable than banana midrib. Banana midrib decayed fast within 2-3 months and was replaced 3-4 times during experimental period. So, care should be taken while using banana midribs because excessive loading might cause oxygen deficiency to fish. Lower DO in the rice straw treatment ponds due to increased biological oxygen demand was also reported by Rai *et al*. (2008). Although banana is
easily available in the farm and has multiple uses, replacement effort is important. The substrate should be checked regularly and decayed midribs should be removed quickly. Feed conversion ratio was less than 1.9 in all periphyton enhanced ponds, indicating periphyton enhancement has potential for reducing supplemental feed input. FCR was better in split bamboo ponds than in control ponds which might be due to utilization of periphyton by carp. Probably split bamboo mat provided greater surface area for periphyton colonization. Most likely differences in the surface area of each substrate type, the exposure to sunlight, and the attraction of algae to the substrate surface made each substrate type a unique environment for the production of periphyton and thus resulted in a difference in fish production.

<table><caption>**Table 5:** Yields of carp and SIS in different treatments (mean ± SE)</caption><thead><tr><th rowspan="2"></th><th colspan="5">Treatments</th></tr><tr><th>T1</th><th>T2</th><th>T3</th><th>T4</th><th>T5</th></tr></thead><tbody><tr><td>NFY of carp only (t/ha/yr)</td><td>3.63 ± 0.49a</td><td>3.87 ± 2.78a</td><td>4.05 ± 0.74a</td><td>4.28 ± 0.97a</td><td>4.34 ± 3.75a</td></tr><tr><td>NFY of SIS only (t/ha/yr)</td><td>0.07 ± 0.47a</td><td>0.07 ± 2.78a</td><td>0.1 ± 0.02a</td><td>0.1 ± 0.97a</td><td>0.08 ± 3.75a</td></tr><tr><td>Combined NFY (t/ha/yr)</td><td>3.59 ± 0.49a</td><td>3.82 ± 0.28a</td><td>4.03 ± 0.74a</td><td>4.27 ± 0.10a</td><td>4.30 ± 0.37a</td></tr><tr><td>Feed conversion ratio (FCR)</td><td>2.0 ± 0.0b</td><td>1.5 ± 0.1a</td><td>1.7 ± 0.2ab</td><td>1.8 ± 0.1ab</td><td>1.9 ± 0.2ab</td></tr></tbody></table>

Similar superscripts for values in a row indicate no significant difference among the values.

T₁ – Without substrate, T₂ – Split bamboo, T₃ – Whole bamboo, T₄ – Banana midrib, T₅ – Plastic bottle

<table><caption>**Table 6:** Gross margin (NRs/100 m² pond/21 days) analysis for different treatments (mean ± SE)</caption><thead><tr><th></th><th>T<sub>1</sub></th><th>T<sub>2</sub></th><th>T<sub>3</sub></th><th>T<sub>4</sub></th><th>T<sub>5</sub></th></tr></thead><tbody><tr><td>Cost</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Feed</td><td>1 368 ± 192<sup>a</sup></td><td>1 066 ± 75<sup>a</sup></td><td>1 306 ± 288<sup>a</sup></td><td>1 452 ± 117<sup>a</sup></td><td>1 489 ± 25<sup>a</sup></td></tr><tr><td>Total variable cost</td><td>2 422 ± 193<sup>a</sup></td><td>2 124 ± 74<sup>a</sup></td><td>2 362 ± 287<sup>a</sup></td><td>2 509 ± 115<sup>a</sup></td><td>2 460 ± 111<sup>a</sup></td></tr><tr><td>Return</td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Carp</td><td>6 258 ± 846<sup>a</sup></td><td>6 678 ± 461<sup>a</sup></td><td>6 993 ± 1 281<sup>a</sup></td><td>7 386 ± 206<sup>a</sup></td><td>7 485 ± 636<sup>a</sup></td></tr><tr><td>SIS</td><td>83 ± 0<sup>a</sup></td><td>75 ± 17<sup>a</sup></td><td>109 ± 26<sup>a</sup></td><td>115 ± 27<sup>a</sup></td><td>87 ± 13<sup>a</sup></td></tr><tr><td>Gross return</td><td>6 342 ± 846<sup>a</sup></td><td>6 753 ± 473<sup>a</sup></td><td>7 102 ± 1 283<sup>a</sup></td><td>7 501 ± 180<sup>a</sup></td><td>7 572 ± 643<sup>a</sup></td></tr><tr><td>Gross margin</td><td>3 920 ± 655<sup>a</sup></td><td>4 630 ± 440<sup>a</sup></td><td>4 741 ± 1 062<sup>a</sup></td><td>4 992 ± 164<sup>a</sup></td><td>5 111 ± 749<sup>a</sup></td></tr></tbody></table>

Similar superscripts for values in a row indicate no significant difference among the values.

Note: Exchange rate used was USD 1 = NRP 103.6 during fish harvesting.

## 5. Conclusion

Carp polyculture is the most popular aquaculture practice in South Asia (Miah *et al.*, 1997), due mainly to the higher production in polyculture compared to monoculture semi-intensive ponds and higher market demands for Indian major carps (Wahab *et al.*, 1995). Periphyton enhanced carp polyculture is mostly practiced by small-scale farmers in Nepal where farmers add substrate in 6-7 species stocked carp ponds to avoid poaching rather than for its food value, because poaching is a common problem. Based on results of three trials it seems that periphyton enhancement system using split bamboo mat with reduced feeding rate at 1-1.5 percent BW/day could be a better option for carp polyculture and carp-SIS polyculture. Quickly decaying substrate may be as good as other natural substrates in terms of periphyton colonization but their decomposition might affect water quality adversely. Although technology is aimed to benefit small-scale farmers its application to commercial farmers should be sought.

## 6. Acknowledgement

We would like to thank women farmers of Sundardeep Women Fish Farmers' Cooperative in Majhui, Chitwan, and farmers of Mishrit Cooperative in Seri and Nanadapur, Nawalparasi for their participation in the on-farm trials. We are thankful to Mr. Sovan Mahato, President of RIDS (Rural Integrated
Development Society), Ms. Usha Chaudhary, Field Supervisor of Twinning support for development of women fish farmers' organizations in Nepal project and Ram Bhajan Mandal, Ph.D. student of Fisheries Program, Agriculture and Forestry University who assisted with all of the field and Lab work. We are grateful to funders AquaFish Innovation Lab, USAID and AgriCord/FFD. Second and third research were a component of the former AquaFish Innovation Lab, which was supported in part by the US Agency for International Development (USAID CA/LWA No. EPP-A-00-06-0012-00), and in part by participating institutions. The opinions expressed herein are those of the authors and do not necessarily reflect the views of USAID.

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# CURRENT PRACTICES OF INTEGRATED MANGROVE-SHRIMP FARMING IN VIET NAM

Phan Thanh Lam

## Abstract

Integrated mangrove-shrimp farming systems combine sylviculture with the production of shrimps (seeds of wild species and of Penaeus monodon), crab and/or fish. It could be a good alternative to prevent mangrove loss and promote forest conservation measures. This study describes the current integrated mangrove-shrimp farming practices, provides an assessment of the gaps between existing farming practices and selected food standard criteria, and gives some insight on the sustainability of farms' operation. A survey of one hundred farms was conducted by RIA2 in 2017. The findings show that many integrated mangrove-shrimp farms implement a low risk and sustainable production, compatible with many organic certification requirements: no feeding, low stocking density, no use of banned chemical or drug, wild-seed source, positive community relations, valid property rights, and biodiversity protection. However, several other criteria are not yet fully met, especially with regard to effluent management, farms registration, management of mortality, labour arrangements, farm hygiene, and record-keeping requirements. To cope with the increasing food safety, quality and sustainability requirements, current farms have to improve in these areas. Moreover, most current shrimp farms are small-scale farms, and their specificities must be considered in the future development of the aquaculture sector. The possible solutions for this inclusion of smaller farms in the value chain could be horizontal coordination and vertical coordination.

Key words: integrated mangrove-shrimp; farming practices; small-scale farms

## 1. Introduction

Shrimp farming takes place in coastal areas by using a great diversity of farming system (Vu and Phan 2008; Nguyen and Dang 2009; Nguyen et al., 2009; Tran et al., 2013). It plays an important role in Vietnamese aquaculture, not only by contributing to significant export earnings but also by creating jobs and increasing the income of local people (Cannon and Johnson, 2013; CBI, 2012; Nguyen et al., 2009; De Silva and Nguyen, 2011; Tran et al., 2013). Small-farms owned and managed by families still dominate in the Mekong River Delta (Phan et al., 2009; Tran et al., 2013) but aquaculture farms, especially small ones are considered highly vulnerable in the value chain (Siar and Sajise, 2009; Tran et al., 2013; Washington and Ababouch, 2011a). Small-farms must be included in the future development of the sector, because they account for more than 200 000 operators (Phan et al., 2011; SFP, 2013; Tran et al., 2013).

In Viet Nam, aquaculture is the main occupation of many small-scale coastal shrimp farmers, who have very few other opportunities to diversify their livelihoods (Le, 2009; Nhuong et al., 2003; Tran et al., 2013). Including them in the future development of the value chain can be achieved through horizontal or vertical coordination (Khiem et al., 2010; Khoi, 2011; De Silva and Nguyen, 2011; Umesh et al., 2009). Hence, policymakers need to find suitable measures to support them in the planning processes (Dey and Ahmed, 2005; De Silva and Nguyen, 2011). An overview of the difference in farming practices among farm categories can provide valuable information to policy makers, thus supporting policies and developing strategies suited to specific farm categories.

On the other hand, market trends for certified seafood products are increasing as customers pay more attention to the quality of products (Corsin et al., 2007; Reilly 2007; Yamprayoon and Sukhumparnich 2010). So far, certification has mainly been the realm of large aquaculture farms operated by seafood processors (Belton et al., 2011; Bush et al., 2010; Trifković, 2013). Some large-farms have achieved certification such as the Aquaculture Stewardship Council (ASC), the Best Aquaculture Practices of the
Global Aquaculture Alliance (GAA-BAP) or the Good Agricultural Practices of the GlobalG.A.P. association of producers and retailers (Fisheries Directorate, 2013; Lam and Truong, 2010; SFP, 2013; Vu et al., 2013).

However, achieving certification may be a challenging task for small-farms, due to their limited capacity (Belton and Little, 2011; Bush and Belton, 2012; Haugen, Bremer and Kaiser, 2013; Khiem et al., 2010; Pham et al., 2011; Trifković, 2013; Umesh et al., 2009). Moreover, the economic cost of certification can be another restriction as the profitability of certified production may not be higher than that of uncertified production because of the more costly investments and difficulties to implement standards (Dey and Ahmed, 2005; Haugen, Bremer and Kaiser, 2013; Khiem et al., 2010; Oosterveer, 2006; Tran et al., 2013).

As a result, it seems that assessment of the sustainability of shrimp farming as only been carried out through certification programmes, but it must encompass all categories of farms to see how they can comply with the standards too and to identify the constraints to success. The sustainable development of an industry is affected by many value chain actors (Grunert et al., 2005; Tran et al., 2013; Vo, Bush and Le, 2009). Growing-out farms are the primary producers of the value chain. Understanding better their operation thus provides the basis for policy-making and development of more appropriate strategies in support to the development of the whole value chain.

This paper describes and assesses the current integrated mangrove-shrimp farming practices. It also provides an analysis of the gaps between current farming practices and selected food standard criteria. Finally, it gives some insight into factors related to sustainability of the farms operation.

## 2. Methodology

**Site selection:** data was collected from shrimp farms in the Mekong River Delta (MKD). The survey sites (at district level) were selected by using a purposive sampling method, after analysing the distribution of shrimp farms by culture area and type of production. The criteria used were 1) the concentration of certain shrimp systems (i.e. type of shrimp system in a given district); 2) the importance of the shrimp culture area (i.e. total shrimp pond surface (ha) per district); and 3) the historical development of shrimp farming systems.

**Shrimp farms selection:** At each selected site, a collaboration with local officers allowed to check the lists of shrimp producers and to classify the farms. After that, a randomized stratified sampling was applied to select a sub-set of farms in each district to be interviewed. The total sample size was 100 mixed mangrove-shrimp farms, of which 30 were surveyed by the "Sustaining Ethical Aquaculture Trade" (SEAT) project in 2011 and 70 by RIA2 in 2017.

**Shrimp farm data collection:** Structured-questionnaires were developed, and the questionnaire was standardized through pilot interviews. The standardized questionnaire was used to collect data from integrated farms. Enumerators were trained on interviewing skills, data recording and methods for minimizing errors during the investigation process. Selected interviewees were owners, managers or technicians who participated or managed farm operations; sometimes interviewees were a group of people working in the same large-scale farms. The interviewees had to know reasonably well the operation of their farm. The information was recorded and checked on the same day. Information gaps were supplemented by telephone. The information collected in the study provided data from the last production cycle.

**Data analysis and interpretation:** Data analysis was performed to answer research questions and databases were exported to relevant statistical software packages such as SPSS 21 (SPSS Inc., Illinois, United States of America) and MS Excel 2007 for statistical analysis. Descriptive analysis was used to estimate the frequency of responses, mean and standard deviation.
# 3. Results

## 3.1. General information

*General development trends:* In the 1970s, extensive shrimp culture based on wild seed started in the mangrove-forest areas, along the coastal zones of the MKD (Nhuong *et al.*, 2002, 2003). The total shrimp farmed area reached 70 000 hectares by the beginning of 1970s (Nhuong *et al.*, 2002). From 1975 to 1990, shrimp culture remained extensive and supplied the domestic market. This is the time when destruction of mangrove-forest for constructing shrimp ponds took place (Nhuong *et al.*, 2003; Phan and Populus, 2007); around 75 000 ha of mangrove forest were lost to exploit fuels and develop agriculture and shrimp culture. A step change occurred around 1987 (Nhuong *et al.*, 2003), when international trade spurred expansion of shrimp aquaculture (Tran *et al.*, 2013). The development of shrimp farming was also driven by the introduction of artificial hatchery production, the gradual improvement in culture technology for grow-out farming, and the broader Government economic reform, the *Doimoi* policy (Nhuong *et al.*, 2002; Nhuong, 2011; Tran *et al.*, 2013). Hatchery development occurred mainly in Central Viet Nam where Nha Trang University introduced the technology to local hatcheries for its spread to the private sector. By the middle of the 1990s, shrimp farming faced serious epidemic diseases in the MKD, and the industry came to a halt. After that, shrimp disease declined as a result of effective improvement in the seed quality and management practices but it still caused significant economic damages to farmers (Nhuong *et al.*, 2003).

Since 2000, the shrimp industry has developed rapidly, following the Decree 09/2000/NQ-CP allowing farmers to convert saltpans and low producing, saline rice fields into shrimp ponds. The shrimp farmed area increased from 171 820 ha in 1999 to 422 060 ha in 2001, reaching 601 850 ha in 2013. According to MOFI (2006), the total conversion of agricultural land to shrimp culture was around 310 000 ha during the period 1999 to 2005, 42 percent of which came from low-yielding rice land conversion. Since 2005, shrimp farming has continued to grow but mainly through improved-extensive and semi-intensive culture systems instead of the traditional extensive system. However, performances are still limited, particularly in terms of farm infrastructure and access to good quality seed. Moreover, large shrimp mortalities still occur and cause losses to shrimp farmers, particularly in the more intensive systems (DoAH, 2012; Nguyen *et al.*, 2009; VIFEP, 2009).

Ca Mau province now has the largest farming area, accounting for 45 percent of the MKD shrimp farming areas, and the main shrimp systems are the mixed mangrove-shrimp, the rice-shrimp rotation system and the improved-extensive system (Table 1). Soc Trang, Bac Lieu and Ben Tre provinces are also important shrimp farming areas, where the main systems are semi-intensive. The other provinces have a less important shrimp farming area, and the main systems are the improved-extensive and the semi-intensive. Ca Mau, Bac Lieu and Soc Trang provinces altogether contributed 68 percent of the total MKD shrimp production in 2013 (Fisheries Directorate, 2014).

<table><caption>**Table 1:** Major indicators of shrimp farm-systems classification</caption><thead><tr><th rowspan="2">Indicator</th><th colspan="5">BTS</th><th>WLS</th></tr><tr><th>Intensive model</th><th>Semi-intensive</th><th>Improved-Extensive</th><th>Mixed mangrove-shrimp</th><th>Rice-shrimp rotation</th><th>Semi-intensive</th></tr></thead><tbody><tr><td>1. Seed sources</td><td>Artificial</td><td>Artificial</td><td>Natural /Artificial</td><td>Natural /Artificial</td><td>Artificial</td><td>Artificial</td></tr><tr><td>- Density</td><td>≥20pcs/m²</td><td>≥10pcs/m²</td><td>≥1pcs/m²</td><td>≥0.5pcs/m²</td><td>≥3pcs/m²</td><td>≥45pcs/m²</td></tr><tr><td>- Bio-security</td><td>PCR test</td><td>PCR test</td><td>No</td><td>No</td><td>PCR test</td><td>PCR test</td></tr><tr><td>2. Feeding regime</td><td>Pellet feed</td><td>Pellet feed</td><td>Natural</td><td>Natural</td><td>Pellet feed</td><td>Pellet feed</td></tr><tr><td>- eFCR</td><td>≥1.3</td><td>≥1.0</td><td>0</td><td>0</td><td>≥1.0</td><td>≥1.0</td></tr><tr><td>3. Shrimp yield</td><td>≥4 tonnes/ha</td><td>≥1tonnes/ha</td><td>≥0.2tonnes/ha</td><td>≥0.2tonnes/ha</td><td>≥0.5tonnes/ha</td><td>≥5tonnes/ha</td></tr></tbody></table>
<table><tr><td>- Survival rate</td><td>≤95 percent</td><td>≤95 percent</td><td>≤50 percent</td><td>≤50 percent</td><td>≤90 percent</td><td>≤95 percent</td></tr><tr><td>4. Water exchange</td><td>Top-up</td><td>Top-up</td><td>Tidal cycle</td><td>Tidal cycle</td><td>Top-up</td><td>Top-up</td></tr><tr><td>- Aeration use</td><td>Yes</td><td>No/Yes</td><td>No</td><td>No</td><td>No</td><td>Yes</td></tr><tr><td>5. Management</td><td>Company<sup>a</sup>/ Salaried manager</td><td>Household/ Salaried manager</td><td>Household</td><td>Household</td><td>Household</td><td>Household/ Salaried manager</td></tr></table>

**Mangrove destruction and integrated mangrove-shrimp farming:** Mangrove forests provide a wide range of ecosystems services, including biodiversity, nutrients cycling and carbon storage, climate change mitigation, coastal protection, nursery ground for fish and shrimps, fuel, tourism and a source of income and food security for local communities (Laure 2017). The largest mangrove area of Viet Nam is located in the southern region of Ca Mau, but its area decreased from 400 000 ha in the 1960s to 73 000 hectares in 1990 under different drivers (Figure 1): the use of herbicides during the Indochina war, the conversion to agriculture (for rice plantations from 1975 to 1979), and to aquaculture (shrimp ponds from 1995 to 2008) as well as the urban development in recent years (Minh *et al.*, 2001, Nguyen *et al.*, 2011; Van *et al.*, 2015; Richards and Friess, 2015). Coastal resources are now threatened by the rapid and unregulated growth of the fishery sector, coastal agriculture, marine transportation and ports, oil and gas exploitation, tourism development, high population density and the daily migration to coastal cities of 1000 people (MFF Viet Nam, 2015). This also puts the provision of ecosystems services provided by mangrove forests at risk and negatively impacts the livelihoods and food security of coastal communities.

<figure><img src="image_127.png" /><figcaption>**Figure 1.** Land cover maps of the Ca Mau for the years 1953, 1975, 1979, 1992, 2004, 2011 (Source: Van *et al.*, 2015).</figcaption></figure>

Blue carbon is the carbon stored and sequestered in coastal ecosystems such as mangrove, sea-grass and tidal marsh. The blue carbon is stored in the living biomass and the non-living biomass like dead wood pool, above and below ground (about 80 percent in the soils). At the global scale, shrimp farming had devastating effects on mangrove forests, by emitting tremendous quantities of blue carbon while also threatening ecosystem goods and services. The conversion of mangrove to shrimp pond farming is not a light hand process. It generates high greenhouse gases (GHG) emissions from land use change (carbon loss from mangrove deforestation and pond excavation), and from GHG activities linked to the farming system. These include use of feed if any, agricultural inputs for pond management, nitrous oxide (N₂O) emissions from fish/shrimp fed farming system and methane (CH₄) emissions for aquaculture developed in freshwater and brackish water.

<footnote><sup>a</sup>Farm is fully owned and operated by Aquaculture Ltd. company or Seafood processor; BTS: black tiger shrimp; WLS: white-legged shrimp. Source: Phan *et al.* (2011)</footnote>
Preventing mangrove loss and adopting conservation measures could help reduce blue carbon emissions. Integrated mangrove-shrimp farming systems combine sylviculture with shrimps (both wild seeds and artificial seeds of *Penaeus monodon*), crab and/or fish farming. It could be an alternative solution to reverse blue carbon emissions into sequestration if forest is well managed. In Viet Nam, these systems are regulated by the provincial governments to maintain a mangrove-to-water surface ratio of at least 60 percent and are characterized by no or low feed, no or low fertilization, passive water exchange and low production (Decision 186/2006/QD-TTg, 178/2001/QĐ-TTg; Jonell and Henricksson, 2014). Three different kinds of integrated mangrove-shrimp pond systems can be distinguished (Bosma *et al.*, 2014): (1) the integrated farming with canals between platforms planted with mangroves (Figure 2a); (2) the associated farming with large areas of water intermixed with large mangrove area (Figure 2b), and (3) the separated farming with a dyke separating ponds from forest (Figure 2c, d).

<figure><img src="image_128.png" /><figcaption>**Figure 2.** Forms of integrated mangrove-shrimp farm (Source: Bosma *et al.*, 2016).</figcaption></figure>

## 3.2. Current shrimp farming practices

### 3.2.1. Shrimp farms characteristics

#### a) Shrimp farms characteristics

*Farm history:* Most farms were established more than 20 years before the study (20.7 ± 6.01 years), and they are owned by independent families (87 percent of total surveyed farms).

*Pond infrastructures:* The farms do not have reservoirs or sediment ponds, as all ponds are used for growing-out shrimp. The water is sourced directly from the river but the exchange is not fully controlled, leading to an increased risk of disease.

The integrated mangrove-shrimp farms are characterized by a low stocking density. No feed is used so that the shrimp rely on natural feed in ponds. The pond size is larger than in the non-integrated shrimp farms (4.37 ± 2.89 ha per farm), but considering that part of the surface is covered with mangrove (51 percent on average), the actual surface available for shrimp is similar to non-integrated systems. Generally, water depth is over 1 m (1.12 ± 0.23 m), and most ponds are earthen as very few have a polyethylene sheet covering. As a result, some ponds have a low structural quality, with unstable dykes and water leakages. Moreover, predators like crabs, snails, or wild fish cannot not be controlled although they may act as a pathogen vectors for from one pond to another.

#### b) Status of labour in farms

The average age of respondents ranged between 40-60 years old (47.6 ± 11.7) with over 20 years of experience (20.4 ± 7.42 years). As a result, their technical husbandry skills to manage the shrimp ponds is relatively good. The farm management is frequently based on family labour (>80 percent of surveyed farms), but all farms also hire part-time workers under verbal agreements for sludge removal and pond
preparation. This shows the significant employment impact on local communities, both in terms of permanent and seasonal jobs.

### 3.2.2. Technical aspects

#### a) Pond preparation and stocking

Only 30 percent of the farms carry out water preparation such as water storage and treatment before stocking, but most of them remove sediment after each crop. Shrimp post-larvae (PL) are purchased from private hatcheries, but most farms do not know the broodstock source. They also do not care about a polymerase chain reaction (PCR) test for post-larvae before buying and stocking (87 percent). Shrimp mortality rates (>95 percent at harvest time) are higher in the integrated mangrove-shrimp farming due to the inconsistent seed quality, which is an important factor affecting production efficiency. Shrimp PLs are stocked directly into the ponds in 80 percent of the surveyed farms, with only 20 percent using nursing ponds first. The stocking density is lower, with intermittent restocking and harvest (20.3 ± 12.4 PL/m²/year, 6-7 restocking/year at a density of 3.58 ± 2.51 PL/m² per stocking).

#### b) Feed and water management

The integrated mangrove-shrimp system does not use external feed for shrimp.

As the farms are often located in coastal areas and estuaries, the water comes mainly from the river-mouth, coastal canals, with a few farms getting their water from primary and secondary canals. The integrated mangrove-shrimp ponds are filled with untreated water and 2-3 days later, stocked with PL.

Eighty-four percent of the surveyed farms use a “partial drainage and water replacement” method, to cope with the fluctuation of the environmental conditions and disease outbreaks risks. The water exchange is based on the tidal regime, so it is usually carried out fortnightly or monthly. Water filling also bring additional wild seeds and natural feeds into the ponds. The farms with large ponds can only carry out partial water exchange, around 20-40 percent of the total volume (26.3 ± 7.11 percent of total water volume).

#### c) Effluent management

Drainage is carried out by gravity. Wastewater is not treated and is released directly into the surrounding rivers and canals that are also used to fill the ponds. As many ponds cannot be fully drained, especially the large ones, wastewater is partially reused at the beginning of a new production cycle. Sludge is removed from the ponds and dropped over the dykes after each harvest. Although the unfed mangrove-shrimp systems produce much lower volumes of sludge, the water exchanges lead to the accumulation of significant quantities that need to be removed annually. However, the storage capacity of the dykes is limited and some sludge has to be released into the rivers.

#### d) Shrimp disease management

Most farms have experienced shrimp mortality during their production cycles. The main cause is shrimp disease (>70 percent of survey farms), followed by extreme weather events and seed quality. At the time of the survey, the most common shrimp diseases were the *White Spot Syndrome Virus (WSSV)*, followed by the *Yellow Head Virus (YHV)* and *Vibrosis*.

A low water quality such as a high Biological Oxygen Demand (BOD) or Chemical Oxygen Demand (COD) is certainly an aggravating factor of shrimp disease occurrence (Anh et al., 2010; Oanh and Phuong, 2012) but the rapid spread of mortalities is mostly the result of the discharge of untreated wastewater and sludge, especially during outbreaks. Hence, the pathogens from infected ponds are likely to spread to other ponds (Anh et al., 2010; Oanh and Phuong, 2012) as Hoa et al., (2011) found that WSSV can be transmitted horizontally through water, via carrier organisms and/or by cannibalism of infected shrimp. The transmission from neighbouring ponds (at current crop or from previous crop) was the main route for WSSV transmission in the semi-intensive shrimp farming system. A clear
separation between the canals used for water supply and drainage would be needed, but this is not yet the case in the MKD (Anh et al., 2010a).

### 3.2.3. Economic aspects

#### a) Harvesting management

The integrated mangrove-shrimp farms harvest shrimp after three months and then carry out monthly stocking and harvesting. The survival rate is low (Table 2) and the system produces less than 250 kg shrimp/ha/year, with an average size of 20-30 pieces per kg. Once harvested, shrimp are sold to the collectors or wholesalers but since the integrated mangrove-shrimp farms are frequently located in remote areas, it is more common that collectors come to the farm.

<table><caption>**Table 2:** Shrimp farming: Harvesting and marketing in two provinces of the MKD</caption><thead><tr><th>Items</th><th>Bạc Lieu (N=35)</th><th>Ca Mau (N=35)</th><th>All (N=70)</th></tr></thead><tbody><tr><td>Number of stocking (times/year)</td><td>5.36 ± 1.27</td><td>5.4 ± 1.17</td><td>5.38 ± 1.21</td></tr><tr><td>Duration between stocking (months)</td><td>2.06 ± 0.81</td><td>1.32 ± 0.53</td><td>1.69 ± 0.78</td></tr><tr><td>Stocking density (PL/ha/year)</td><td>16.8 ± 9.51</td><td>24.0 ± 14.0</td><td>20.3 ± 12.4</td></tr><tr><td>Survival rate at harvest (percent)</td><td>3.93 ± 3.49</td><td>2.24 ± 2.18</td><td>3.09 ± 3.01</td></tr><tr><td>Aquaculture production (kg/ha/year)</td><td>487 ± 269</td><td>616 ± 506</td><td>550 ± 405</td></tr><tr><td>Black tiger shrimp (percent)</td><td>36 percent</td><td>38 percent</td><td>37 percent</td></tr><tr><td>Wild shrimp (percent)</td><td>12 percent</td><td>20 percent</td><td>17 percent</td></tr><tr><td>Crab (percent)</td><td>27 percent</td><td>14 percent</td><td>20 percent</td></tr><tr><td>Fish (percent)</td><td>25 percent</td><td>27 percent</td><td>26 percent</td></tr><tr><td>Share of shrimp sold to collectors / wholesalers (percent)</td><td>69 percent / 31 percent</td><td>83 percent / 17 percent</td><td>76 percent / 24 percent</td></tr></tbody></table>

#### b) Economic efficiency

The integrated production generates a lower shrimp yield and economic performance per hectare than intensive shrimp farming system, but the size of shrimp is bigger and thus they deserve a better market price. Moreover, wild shrimp, wild fish and crabs provide an additional income from the ponds and since the stocking density is low, no artificial feeding is used and less chemical are employed, the integrated system could classify for some premium markets such as the organic production certifiable by organisations like *Naturland*.

Shrimp and crab seed are the highest costs in the system, with USD 852/ha/year, accounting for 41 percent of the total costs. Labour comes next with USD 750/ha/year or 36 percent of total costs, although they are often family labour. Gross return from black tiger shrimp production was USD 2 523/ha/year, accounting for 57 percent of total income (Table 3), and the net return was USD 1 170/ha/year.
<table><caption>**Table 3:** Cost-benefit analysis for the integrated mangrove-shrimp farm model (Source: IPSARD, 2016)</caption><thead><tr><th>Items (per 1ha)</th><th>1 000 VND</th><th>USD</th></tr></thead><tbody><tr><td>Outflows:</td><td>70 685</td><td>3 213</td></tr><tr><td>Costs for fix asset (harvest sluice, boat, others facilities)</td><td>41 000</td><td>1 864</td></tr><tr><td>Costs for mangrove shrimp production</td><td></td><td></td></tr><tr><td>Black tiger shrimp seed</td><td>14 250</td><td>648</td></tr><tr><td>Crab seed</td><td>4 500</td><td>204</td></tr><tr><td>Mangrove plantation</td><td>1 500</td><td>68.2</td></tr><tr><td>Mangrove protection and management</td><td>120</td><td>5.45</td></tr><tr><td>Removing mud</td><td>7 500</td><td>341</td></tr><tr><td>Lime, chemical for treatment</td><td>475</td><td>21.5</td></tr><tr><td>Trap, harvest net</td><td>1 340</td><td>60.9</td></tr><tr><td>Family labour</td><td>16 500</td><td>750</td></tr><tr><td>Inflows:</td><td>96 430</td><td>4 383</td></tr><tr><td>Black tiger shrimp</td><td>55 500</td><td>2 523</td></tr><tr><td>Crab</td><td>12 800</td><td>582</td></tr><tr><td>Fish and others</td><td>5 200</td><td>236</td></tr><tr><td>Wood</td><td>21 860</td><td>994</td></tr><tr><td>Others (carbon, existent value)</td><td>1 070</td><td>48.6</td></tr><tr><td>Net return:</td><td>25 745</td><td>1 170</td></tr></tbody></table>

### 3.2.4. Shrimp farm certification and sustainability issues

#### a) Main certification issues of shrimp farms

As trends in shrimp consumption increase, the requirements for product quality and food safety also become more stringent. A comparison between the integrated mangrove-shrimp farming in the MKD and the practices requested by shrimp systems, such as the Best Aquaculture Practices of the Global Aquaculture Alliance (GAA-BAP), the Good Agricultural Practices of the Global G.A.P. association of producers and retailers, the Aquaculture Stewardship Council (ASC) or Naturland shows that many farms are already compliant with criteria like the non use of external feed, low stocking density (≤15 PL/m²), no banned chemical/drug use, good relationships with community, respect of property rights or biodiversity protection.

However, there are also several criteria that farms cannot meet, especially for effluent management (most farms release their wastewater without any treatment and they don't have sediment basins), shrimp mortality management (lack of proper methods), labour arrangements (verbal contracts), farm hygiene, and recordkeeping requirements.

To meet standard criteria, the current farms need to improve their practices and for this, they need to get support from the local officers on technical aspects (training courses) and management issues such as trade name registration, land ownership certification or property right. Unlike the intensive farms that have greater financial and physical assets, the integrated mangrove-shrimp farms have limited resources, making certification a more difficult target for them. Moreover, several criteria are particularly difficult for the small individual farms. This includes the requirement on labour, farming infrastructure, storage and disposal of supplies, effluent management, microbial sanitation, shrimp disease control, and traceability requirements. In addition, the technical and financial constraints resulting from recordkeeping, adjustment of farms (e.g. remove the on-farm toilet, no animal and livestock on-farms) and certification fee constitute a major difficulty for them.
b) Main constraints to sustainable development

The shrimp farmers surveyed perceive three important factors that are likely to affect the long-term
development of shrimp farming (Table 4).

Seed quality is the first one. At present, shrimp mortality is high during the growing-out, >95 percent, and the main perceived cause is the seed quality. Moreover, due to their biological characteristics, shrimp are sensitive to environmental changes, so that water quality and extreme weather variability are aggravating factors.

Water quality is another key issue. It has fluctuated in recent years and tended to decline. Many farms
pointed out that the use of chemicals has increased over the last five years, and that the bad water quality
may also be resulting from nutrient discharge by other industries.

Over 70 percent of shrimp farms surveyed mentioned they had faced shrimp disease problems, and most of them had to use therapeutic methods during the production cycle. Shrimp health management has become increasingly complex with new diseases in recent years.

**3.3. Recommendations for improving shrimp farming practices**

The integrated mangrove shrimp farming is a relevant model, adapted to natural conditions and farmers'
constraints that produces good quality shrimp, and could be a relevant model for organic certification.
It is regulated by the provincial government to maintain a mangrove-to-water surface ratio of at least
60 percent and is characterized by a large culture area, a low stocking density, a limited-to-no use of
chemical or feeds, a limited-to-no use of fertilization, passive water exchange and low yield (Decisions
186/2006/QĐ-TTg and 178/2001/QĐ-TTg). The current mangrove-to-water surface ratio is 51:49
percent but the development plan calls for mangrove to reach 60 percent in the future, hence, the need
to intensify the farming to maintain the aquaculture production (shrimp, crab, wild shrimp and fish
production. From our study, three important technical factors emerged for this (Table 5):

- The shrimp yield is higher when the PLs are stocked in nursing ponds before their release into the growing-out ponds. Thus, we suggest that farmers should buy good quality seed and apply nursing techniques in order to reduce the shrimp mortality.

- The shrimp yield is higher when the shrimp PLs are stocked at a suitable stocking density, 10-15 PLs/m²/year. With this stocking density, the shrimp grow well in the absence of external feeding and it also complies with the criteria for organic certification.

- The shrimp yield is higher when probiotics are applied into shrimp ponds to improve water quality and create a natural food base for shrimp growth. The declining natural food base observed in recent years requires probiotics addition to be restored (Johnston *et al.*, 2000; Nguyen *et al.*, 2009).
<table><caption>**Table 4:** Major factors impeding the sustainable development of shrimp farming</caption><thead><tr><th>Constraints</th><th>Current farming practices</th><th>Solutions and outcomes</th><th>How does it related to sustainability?</th></tr></thead><tbody><tr><td>Shrimp disease</td><td>- Shrimp disease (&gt;70 percent).<br/>- Main disease: WSSV, YHV.</td><td>- Solutions: Update and improve technical skills; use of good seed; new technology for production.<br/>- Expected outcomes: Successful harvest (less mortality and high yields); lower cost from using less of chemicals and drugs.</td><td>- Why it is important: Indicates a better farm management, effective health management protocols.<br/>- How it relates to sustainability indicator (SIs): Effective environmental and health management, a higher biodiversity promotes sustainability, contributes to the protection of natural capital and to enhance economic performance.</td></tr><tr><td>Water quality</td><td>- Farms do not have sediment ponds.<br/>- Water quality is not monitored regularly.<br/>- Wastewater released without treatment.</td><td>- Solutions: Update and improve technical skills; Upgrading of farm infrastructure; new technology for production<br/>- Expected outcomes: No or low incidence of challenges to the farm from government; less negative effects to public environment; lower disease incidence and lower seed mortalities.</td><td>- Why it is important: It indicates environmentally responsible and friendly farming; also a proxy indicator of better sector governance (i.e. zoning, planning)<br/>- How it relates to SIs: Environmentally friendly farming; good sector management (zoning, planning); fewer social risks (less risk from food safety issues) and environmental risk (from pollution or contamination of the environment); improves yields.</td></tr><tr><td>Seed quality</td><td>- High shrimp mortality in the extensive farms (&gt;95 percent), SD is &lt;15 PL/m².</td><td>- Solutions: Use of good seed; update and improve technical skills.<br/>- Expected outcomes: Less disease incidence; less mortality; and higher yields.</td><td>- Why it is important: Indication of good risk management practices.<br/>- How it relates to SIs: Farmers' widespread use encourages seed producers to adopt seed certification standards. This improves overall productivity and sustainability of farming.</td></tr></tbody></table>

<table><caption>**Table 5:** Average shrimp yield associated with different practices</caption><thead><tr><th>Items</th><th>Shrimp yield (kg/ha/year)</th></tr></thead><tbody><tr><td>Nursing applied?</td><td></td></tr><tr><td>No</td><td>191</td></tr><tr><td>Yes</td><td>216</td></tr><tr><td>Probiotics applied?</td><td></td></tr><tr><td>No</td><td>187</td></tr><tr><td>Yes</td><td>214</td></tr><tr><td>Stocking density (PL/m²/year)</td><td></td></tr><tr><td>&lt;10</td><td>139</td></tr><tr><td>10-15</td><td>212</td></tr><tr><td>&gt;15</td><td>203</td></tr></tbody></table>
# 4. Discussion

## 4.1. Farming practices: challenges to reach food standards

Consumers are increasingly concerned about the environmental and social impacts of food production in developing countries (Belton and Bush, 2014; Brunori et al., 2011; Bush, 2008; Bush and Oosterveer, 2007; Corsin, Funge-Smith and Jesper, 2007; Jespersen et al., 2014; Oosterveer, 2006). They are also interested in the process through which a product travels and its process-oriented quality (Brunori et al., 2011; Corsin, Funge-Smith and Jesper, 2007; Reilly, 2007; Yamprayoon and Sukhumparnich, 2010; Young, Goulding and Stirrat, 2011).

Food certification has been identified as a way of demonstrating the sustainability of aquaculture production (Bush et al., 2010; Bush and Oosterveer, 2007, 2012; Kelling, 2012; Mohan, 2013; Young, Goulding and Stirrat, 2011). Farmed shrimp is a target species for the Vietnamese seafood export, and it has moved towards meeting various food standards to maintain access to its access to markets.

Private governance standards have now become the norm as farmers have to comply with food quality and safety standards to gain or maintain their position in export markets (Bush et al., 2010). The focus of new regulations covers all operations from farm-to-fork and the primary responsibility for marketing safe food lies with producers and processors (Reilly 2007). The general principles of food hygiene also extend to all operations, including the primary production of food (Reilly, 2007; Washington and Ababouch, 2011; Tran et al., 2013), to such extend that some authors now view it as a trade barrier (Reilly, 2007; De Silva and Nguyen, 2011; Tran et al., 2013).

Seafood producing countries should overcome challenges by continuously improving the whole production chain (Bush, Khiem and Chau, 2010; Bush and Belton, 2012; Reilly, 2007). The main constraint for farmers is that they frequently lack access to proper knowledge and awareness on requirements, and they also lack expertise and training on compliance with standards requirements on technical requirements, implementation and monitoring capacity (Jespersen et al., 2014; Kelling, Kruijssen and Li, 2010; Mohan, 2013; Ponte et al., 2014). Washington and Ababouch (2011) suggested that farms should follow the national standards, as it would make it easier for them to then meet the additional criteria requested by the private standards and certification (Nietes-Satapornvanit, 2014). Farm-level certification contributes to sustainable seafood trading, but it is still beset with significant limits such as measuring the impacts of the external environment on the farms (Allsopp, Johnston and Santillo, 2008; Bush et al., 2013; Bush and Belton, 2012; Han and Immink, 2013).

Moreover, although food standards pay more attention to the primary production at the farm level, fraud in the value chain is often not associated with farmers but rather intermediaries such as secondary processors where illegal/poor practices occur such as lack of the knowledge on food hygiene and safety (Fisheries Directorate, 2012; VASEP, 2014; Vu et al., 2013). Moreover, the certification schemes should be integrated with other governance mechanisms and public rulings, including local standards that are already in place, making use of the existing local expertise (Bush et al., 2013).

## 4.2. Farm upgrading - the key barriers to upgrading

Shrimp has become a major product in the international seafood trade, and there is an increasing pressure from markets such as the European Union, the United States of America and Japan on food safety and sustainability of farmed seafood. This prompted a value chain upgrading to reduce environmental, social and economic risks (Jespersen et al., 2014; Khiem et al., 2010; Pham et al., 2011; Ponte et al., 2014).

Ponte et al., (2014) presented upgrading strategies for the seafood farm-level in Asia. These included the improvement of the process, the improvement of the product, the improvement of the volume and the improvement of the variety. At farm level, the barriers include the lack of explicit economic incentives (e.g. improved market access or increased price), the limited access to capital to invest in improved management practices, and the lack of appropriate skills for smallholders. Another one relates
to the economic risks associated with market volatility and quality regulation (Bush and Belton, 2012; Ponte et al., 2014).

To implement upgrading strategies, the shrimp sector needs finance to invest, but shrimp farmers are currently facing financial constraints (lack of operational finance) and constraints on access to credit (limited access to credit, or lack of access to credit for production inputs). The costs associated with upgrading include the certification fees (USD 4 500-6 000), the annual fees (USD 1 000-2 000) (Haugen, Bremer and Kaiser, 2013; Nguyen, 2012), the cost for consultants providing technical support (USD 10 000-15 000), the cost for farm re-structuring and for water/effluent quality monitoring (Fisheries Directorate, 2014).

However, even though the producers bear high costs of investment, the farms certified by GAA-BAP achieved better production (Lam and Truong, 2010), while an 11 percent price premium (Lam and Truong, 2010). Nonetheless, these costs are high and tend to exclude the weakest farms, especially the small-producers, from the export supply chain (Belton, 2010; Belton et al., 2011; Dey and Ahmed, 2005; Haugen, Bremer and Kaiser, 2013; Khiem et al., 2010; Oosterveer, 2006; Pham et al., 2011; Subasinghe, Soto and Jia, 2009).

**5. Conclusions**

Shrimp has dominated Viet Nam's seafood exports over the last decade (Fisheries Directorate, 2013; Tuan et al., 2013) and the industry has shown a strong growth in export value, with annual growth rates of over 12 percent since 2001. The substitution of black tiger by white legged shrimp in some major producing countries has resulted in Viet Nam becoming the biggest producer of black tiger shrimp. Large areas are used for the farming of the species, usually at a lower level of intensity that provides Viet Nam with opportunities to differentiate its shrimp export.

With current emerging trends, it is likely that shrimp commodities will continue to head towards the sustainable production practices promoted by third party standards on food safety animal welfare, environmental integrity and social responsibility (MARD, 2014; De Silva and Nguyen, 2011; Tuan et al., 2013). The integrated mangrove-shrimp farming system, with its low stocking density, no feeding and lower use of chemicals is a less risky and more sustainable model, which has a strong potential for the organic certification market (Naturland, 2012; Nguyen et al., 2009; Vu et al., 2013).

Moreover, most of these farms are small-scale, so that the promotion of this model would allow smallholders to be included in the future development of the aquaculture sector. However, for this to happen, the smaller-scale farms will have to be included in the value chain through horizontal coordination and vertical coordination (Khiem et al., 2010; Khoi, 2011; De Silva and Nguyen, 2011; Umesh et al., 2009).

**6. Acknowledgements**

This study was prepared with the financial assistance of SEAT project (European Union/FP7 research project no. 222889) and FAO (LOA.FAVIE 50/2017). The data were collected under the Department of Agriculture and Rural Development of Ca Mau and Bac Lieu provinces in the Mekong River Delta, the Vietnamese Directorate of Fisheries. Special gratitude goes to the integrated mangrove-shrimp farms in the MKD for providing the data and relevant reports.

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# BRINE SHRIMP *ARTEMIA* PRODUCTION IN COASTAL SALT PONDS IN ASIA

Liying Sui, Nguyen Van Hoa, Montakan Tamtin, Patrick Sorgeloos, Gilbert Van Stappen

## Abstract

The brine shrimp *Artemia* is a highly required, convenient and cost-effective live food in marine larviculture. *Artemia* cysts, originating from a limited number of inland salt lakes, are a commodity traded worldwide. Over the past decades, *Artemia* pond production in solar saltworks has emerged as an alternative to cope with possible cyst shortages and high market prices, and as a tool to fulfill local cyst demands associated to local aquaculture developments. This article provides an overview on *Artemia* pond production in a number of countries in the South, with emphasis on the production techniques.

## 1. Introduction

Aquaculture is thought to supplement the over-exploited fisheries in fulfilling the need of the growing human population for high quality animal protein. One of the problems faced by the hatchery stage of fish and crustaceans is the quantitative and qualitative supply of brine shrimp *Artemia*. *Artemia* are naturally spread worldwide in hypersaline lakes and in coastal saltponds where seawater is concentrated by evaporation until crystallization. Its freshly hatched nauplii are an essential live food for farmed marine crustacean and fish larvae, due to their availability and convenience as dry cysts that can be kept in a viable state on the shelf. *Artemia* cysts are the trade coin in the marine aquaculture business and are naturally harvested in a limited number of salt lakes. In a scenario of climate change and increasing harvesting pressure on these natural salt lakes, it is difficult to manage the dynamics of the *Artemia* population cycles and hence to predict cyst harvests over the mid- and long-term. New locations such as solar saltworks, suitable for *Artemia* biomass and cyst production, have been more or less successfully exploited in a number of countries in the south over the last decades. Although the bulk of *Artemia* cyst product still originates from the Great Salt Lake and other inland salt lakes (e.g. in China, Kazakhstan, the Russian Federation), the production of cysts in solar saltworks may make up for a considerable share of local markets.

*Artemia* naturally occur in medium to high salinity evaporation salt ponds (salinity ranging from 60 to 200 g/l), in solar saltworks, and are mainly found in ponds at intermediate salinity levels since the organism has no defence mechanisms against predators (which are generally dwindling or absent above 80-100 g/l). The presence of *Artemia* in sufficient numbers allows to improve the salt production quantitatively and qualitatively as it is not only needed for controlling algal blooms, but their corpses also eventually provide essential nutrients for the development of the red halophilic *Halobacterium* that help promote evaporation in the crystallization ponds. Reduced levels of dissolved organic matter and viscosity, as well as red coloration of saturated brine, thereby improve salt production qualitatively and quantitatively (Tackaert and Sorgeloos, 1993). Therefore, *Artemia* culture turns out as a profitable economic activity integrated with the salt production, provided salt producers are willing to adopt the technology and researchers support such endeavor with research and sustained dissemination activities.

*Artemia* pond production can be seen as a form of extractive aquaculture, in which low-cost products are turned into high-quality products, such as cysts and protein-rich biomass, for local use in marine shrimp and fish farm. In the development of *Artemia* pond production, issues such as the ability of the (often introduced) *Artemia* strain(s) to adapt to local climatological and biological conditions, and the socio-economic imperatives of the local aquaculture environment need to be considered. We thus hope that the information presented will help the emergence of new initiatives in areas in the South where often fisheries resources are over-exploited, and where initiatives to diversify aquaculture are currently underway.
## 2. Intensive management of *Artemia* cyst production in Viet Nam

Since the first initiatives in early 1980s, interest in the seasonal culture of *Artemia* in the Mekong Delta has steadily expanded and mainly aimed at cyst production. The Mekong delta is characterized by a tropical monsoon climate with an annual average air temperature of 26.1°C. In April-May, air temperatures frequently exceed 35°C. The dry season generally lasts from November/December to April/May. The pond system is described as static as there is no continuous flow of water from one pond to another. Brine shrimp are generally inoculated in January, at high densities (> 20 nauplii/l) in ponds with an appropriate salinity of 80-90 g/l. Within nearly 20 years after the first inoculation, the originally inoculated SFB-type *A. franciscana* has evolved into the so-called Vinh Chau (VC) strain with characteristics different from the original mother strain, especially increased temperature tolerance (Kappas *et al.*, 2004). Over the past few years the culture area had more or less stabilized to 200-400 ha. Cysts of the VC strain are considered of excellent quality for their small size, high hatching and nutritional qualities, especially the levels of highly unsaturated fatty acids (Nguyen Thi Ngoc Anh *et al.*, 2009, 2010). They are therefore sold at prices which may be twice the price of the Great Salt Lake type cysts or more.

<figure><img src="image_129.png" /></figure>

©Liying Su

<caption>**Figure 1:** Intensive *Artemia* cyst production in Vinh Chau-Bac Lieu, Mekong Delta, Viet Nam.</caption>

Ponds are intensively managed, targeting increasing yields and enhancing operational efficiency. Ponds are oriented, with the longest axis parallel to dominant winds for a better oxygen diffusion into the water column. As salt ponds are shallow, excavating (part of) the pond bottom and/or heightening the dikes to increase the water depth is often done to enlarge the production volume and to reduce temperature stress for *Artemia*. Predators and food competitors are kept out and/or removed from the *Artemia* ponds as much as possible by using a variety of tools. A fertilized pond with a lower salinity (which surface is about 30 percent of the total surface used for *Artemia* culture) is generally used to produce phytoplankton-rich green water that serves as feed for *Artemia*. Green water is pumped from this common fertilization pond(s) into the culture ponds, if needed after mixing it with brine to maintain sufficiently high salinity levels (Vu Do Quynh anh Nguyen, 1987; Baert *et al.*, 1997). Green water is often supplemented with chicken manure and cheap agricultural by-products (such as micronized rice bran and soy pellets) which may be consumed directly by the brine shrimp population or act as a substrate for the proliferation of bacteria (so called biofloc technology), which in their turn are consumed by *Artemia*. Frequent raking of the pond bottom is provided to avoid the excessive growth of macroalgae and re-suspends particles that have settled down and makes them accessible again for filtration uptake by *Artemia*. Two to three weeks after inoculation, *Artemia* starts reproducing, generally first ovoviviparously and later oviparously. High production of cysts usually occurs in February and March as water temperature stays below 35°C. Towards the end of the dry season the productivity decreases as a result of the high temperature, food limitation and senescence of the population, which may collapse prematurely in extreme cases. To boost production, ponds are sometimes re-inoculated towards the second half of the dry season for a new production run (“crop” or “cycle”) but higher water levels are needed in order to avoid excessive water temperatures.
As outlined in detail by Nguyen and Sorgeloos (2015) this combined salt-cum-*Artemia* production in Viet Nam has become a very lucrative business with major socio-economic ramifications in the coastal areas of Vinh Chau – Bac Lieu in the Mekong Delta: over 500 families of salt farmers have improved their income by more than USD 5 000 per household and per dry season with the production and sales of brine shrimp (mostly cysts but also now adult brine shrimp biomass harvested towards the end of the dry season, through the first months of the rainy season). Although cyst harvests amount to about 50 tonnes in a dry season of 3 to 4 months, these meet less than 10 percent of the present demand for *Artemia* cysts by the Vietnamese aquaculture industry. Local availability of top-quality *Artemia* cysts has allowed Viet Nam to become the first in the world to develop commercial mud crab hatcheries (as umbrella *Artemia* can be used to replace rotifers at the start of feeding). As the profitability of seasonal solar salt production is under much pressure in many countries around the world integrated salt with brine shrimp production should be further explored: it can make this artisanal sector, often involving many thousands of households, again profitable (with brine shrimp *Artemia* as extra by-product and thanks to its filterfeeding activity producing a higher NaCl quality) and furthermore contribute to the expansion of local fish and shellfish farming activities as the *Artemia* ponds can be used in the rainy season for the ongrowing of mud skipper, mud crab, etc.

**3. Intensive Artemia biomass production in Thailand**

*Artemia* culture was introduced into Thailand in 1978 to produce cysts. Since then the status of Artemia culture has changed as a function of aquaculture demand, causing a shift of Artemia production from cysts to biomass. Nowadays the production in Thailand is entirely based on the use of the so-called “ami” as feed. Ami is the waste product of the industrial production of monosodium glutamate (MSG), a flavour enhancer commonly used in the food industry. Most MSG is produced by bacterial fermentation, in a process similar to the production of vinegar or yogurt: during fermentation, Corynebacterium bacteria, cultured with carbohydrates excrete amino acids into a culture broth from which MSG is isolated. The waste product is a dark coloured viscous liquid, which is further fermented prior to application in the pond. This fermented product is applied in the ponds at various rates (up to about 100 l/ha/day, but generally lower), depending on the state of the product, the primary production in the pond, the overall pond turbidity, and the Artemia densities in the pond.

<figure><img src="image_130.png" /><figcaption>**Figure 2:** Intensive *Artemia* biomass production and purification system in Thailand.</figcaption></figure>

*Artemia* may be harvested manually with harvesting nets, by light attraction, or semi-automatically. Yields are in the range of 1 500-3 000 kg wet weight/ha/month. If transported alive, the biomass are acclimated at 40-50 g/l before packing. The current annual production of *Artemia* biomass is estimated to be 500-600 tonnes with a value of USD 615 000-737 000. Of this amount, 75 percent is used for the domestic market, either live, chilled or frozen, in hatcheries of shrimp and high-value fish (such as seabass and grouper), for shrimp broodstock (as a substitute for blood worm *Glycera sp.* and sandworm *Arenicola sp.*) and for ornamental fish (replacing e.g. cladocerans or the sludge worm *Tubifex tubifex*). A quarter of the total production is exported as frozen *Artemia* biomass. Live *Artemia* is sold (generally in a 5 kg box) at the price of USD 1.0-1.5/kg; frozen *Artemia* has a price of about USD 2/kg.
The *Artemia* production procedure in Thailand thus appears relatively simple. It is therefore an attractive alternative for more elaborate production methods requiring the need to maintain an algae-rich fertilizer pond, to add supplemental feeds for the *Artemia* population etc, such as practiced in Viet Nam. In the absence of scientific study of the biochemical and biological processes ongoing in the “ami” production tanks and of the nutrient dynamics in the *Artemia* ponds, extension of the technique chiefly relies on the ‘trial and error’ principle. Moreover, presently decreasing market demand is a major bottleneck for further expansion of the production even in Thailand, rather than production capacity and technology.

**4. Extensive Artemia cyst and biomass production in China**

China is the world's biggest salt producer, with the Bohai Bay coastal area in north-eastern China being one of the country's main production areas with about 250 000 ha of salt evaporation ponds, mainly operated by large salt production companies. The production area has been decreasing over recent years as salt ponds have been turned into urban and industrial areas. China is also a leading country for aquaculture, with an annual aquaculture production of 47 million tonnes -excluding aquatic plants- (data of 2017, FAO, 2019). The fast development of aquaculture leads to an increasing demand for *Artemia* cysts: from 600 tonnes commercial dry product in 2000 to about 1 500 tonnes in 2012, corresponding to roughly 50 percent of the entire world production. The cysts are mainly used in the hatcheries of penaeid shrimp, giant river prawn and mitten crab, as well as in larviculture of several marine fish species. Though several hundreds of tonnes of cysts are harvested in various inland salt lakes in China and in Bohai Bay coastal saltworks, they are largely insufficient to meet the country's demands. Although statistical data are not centralized, it is estimated that an average 1 300 tonnes of cysts are imported annually from the Russian Federation, Kazakhstan and the United States of America; meanwhile about 400 tonnes of cysts are exported to Thailand, the Republic of Korea and other countries.

In the late 1980s and early 1990s, the harvesting of cysts and biomass of the local parthenogenetic strains has become a considerable industry, employing several hundreds of people. Closer biological management of the salt ponds was proposed through the scientifically-supported introduction of *A. franciscana* (Tackaert and Sorgeloos, 1991). By 1997, Bohai Bay *Artemia* production approximated 600 tonnes for cysts and 20 000 tonnes biomass. Allochtonous *A. franciscana* was prominently present in the area from the end of the twentieth century onwards (Zheng *et al.*, 2004; Van Stappen *et al.*, 2007). By the end of the century, due to the fast development of Chinese aquaculture and the shortage of *Artemia* cyst resources worldwide, extensive *Artemia* pond production received a lot of attention in the Bohai Bay area. Large areas of salt land (about 33 000 ha) were used to construct ponds for *Artemia* production. The size of these ponds varied from several hundred m² to 100 ha, with cyst yields reaching 3-60 kg wet weight per ha. In contrast to monsoon Southeast Asia, *Artemia* biomass and cysts are mostly produced in an extensive way: no organic manure or agriculture by-products are added to the ponds as supplemental feeds. The *Artemia* production in the Bohai Bay generally starts in June (about one month after the first spring emergence of *Artemia* nauplii) when the water temperature has increased to about 20°C. It ends towards the end of November when the water temperature drops to less than 10°C. The harvest is usually interrupted by heavy rains, often occurring from July until mid August. Generally the autumn harvest (September to end of November) accounts for 2/3 of the total harvest.
<figure><img src="image_131.png" /></figure>

**Figure 3:** Harvesting of *Artemia* cysts and Biomass from Bohai Bay saltponds, Wudi, Shandong Province, China.

<figure><img src="image_132.png" /></figure>

**Figure 4:** *Artemia* inoculation at Bohai Bay saltworks, Wudi, Shandong Province, China.

Since 2010, interest in *Artemia* pond production has risen again, aiming to produce high quality Bohai Bay *Artemia* cysts. This lead to the involvement of a number of saltwork managers in semi-intensive pond culture, including supplementation with chicken manure to stimulate algal blooms in the ponds. *Artemia* cysts from the Bohai Bay salt ponds on the other hand are known for higher hatchability and better nutritional value and are thus sold in China at a price 150 percent higher than inland cysts, reaching USD 75-80 per kg in 2016. Recently, so-called *Artemia* nauplii hatcheries have been established in the vicinity of fish and shellfish hatcheries, supplying shrimp and fish farmers with freshly hatched *Artemia* nauplii, as the specialized *Artemia* hatching enterprises are more professional and more efficient in cyst hatching procedures than the hatcheries, especially the smaller ones. Also *Artemia* biomass is used, mostly as fresh feed for shrimp farms. Only a small percentage of biomass is frozen, to be used during winter and early spring, when biomass is not available in the field. The price for fresh biomass was USD 0.5 per kg wet weight in 2016.

In spite of occasional upsurges of initiatives, the Bohai Bay production has been stagnating or even declining in recent years due to the reduction in the overall size of the salt production area and to overharvesting. Yields have also decreased as a consequence of extensive discharge of effluents from desalination and bromine extraction plants into lower salinity evaporation ponds (usually at 50-60 g/l), which provide the intake water for *Artemia* production ponds. The bromine extraction effluents (often acidified to pH 2-3 and deprived of live plankton organisms) have a profoundly negative impact on the salt pond ecosystem. Although the buffering capacity of the soil allows recovery to weak alkalinity (pH 7-8) after three to four steps of the evaporation procedure, there has been a marked decline in harvested quantities and hatching quality of Bohai Bay *Artemia* cysts (Sui *et al.*, 2013). The average annual production in the area presently only accounts for less than 30 percent of the production in the 1990s.
Unstable and unpredictable *Artemia* pond production thus remains a problem in China. Suitable techniques adapted to the local environment, such as fertilization regimes, still need to be developed.

**5. Conclusion**

The above case studies highlight integrated *Artemia* biomass and salt production. Such endeavors have proved successful in leveling-up welfare of rural communities (especially in the Viet Nam case), but have also been the basis for industrial activities as in the China case, the world's leading salt producer and second world source of *Artemia* cysts (both inland and coastal). This problem is indeed a challenge when promoting this sort of extractive aquaculture in countries needing *Artemia* cysts and biomass to boost their local aquaculture production, for example in many countries in Africa but also in countries with a well established aquaculture sector such as Latin America, where programmes for sector diversification are underway. Such diversification programmes need to overcome the many difficulties associated with the production of poorly studied species in captivity, in particular the larviculture stage and its nutritional needs. Therefore, a challenge but also an opportunity ahead is to understand what "proper management" means in terms of ecological characteristics of ponds, and what the dynamics of the *Artemia* population over production cycles will be, allowing to predict future yields, especially in a context of climate change. These aspects of *Artemia* production have hardly been studied so far. This is linked to monitoring the genotype composition of the *Artemia* population over time associated to key phenotypic traits, together with monitoring the critical stressors or selective forces acting on the gene pool over the production cycle.

Bottlenecks associated to introductions may reduce the species' genetic diversity and the ability to respond to changing local environmental circumstances. These case studies have in common that *Artemia* pond production has been initiated or accompanied with inoculation of non-indigenous *Artemia* species, *A. franciscana* being the species of choice, with cysts often from San Francisco Bay in the United States of America. The impact of *Artemia* translocation needs to be evaluated and minimized in order to comply with international agreements to protect biodiversity and in any case the need to conserve local *Artemia* biodiversity should be of paramount importance when designing future inoculation activities, as *Artemia* resources stand as a natural patrimony for the sustainable expansion of aquaculture. On the positive side such introductions can also be seen as a model system and opportunity to study adaptation, selection and interspecies competition processes.

**6. References**

Anh, N.T.N., Hoa, N.V., Van Stappen, G. & Sorgeloos, P. 2009. Effect of different supplemental feeds on proximate composition and *Artemia* biomass production in salt ponds. *Aquaculture* 286: 217-225.

Anh, N.T.N., Hoa, N.V, Van Stappen, G. & Sorgeloos, P. 2010. Effect of partial harvesting strategies on *Artemia* biomass production in Vietamese salt works. *Aquaculture Research* 41: 289-298.

Baert, P., Nguyen Thi Ngoc Anh, Vu Do Quynh, Nguyen Van Hoa & Sorgeloos, P. 1997. Increasing cyst yields in *Artemia* culture ponds in Viet Nam: the multi-cycle system. *Aquaculture Research* 28: 809-814.

Kappas, I., Abatzopoulos, T.J., Van Hoa, N., Sorgeloos, P. & Beardmore, J.A. 2004. Genetic and reproductive differentiation of *Artemia franciscana* in a new environment. *Marine Biology* 146(1): 103-107.

Nguyen, V.H. & Sorgeloos P. 2015. Integrated salt and brine shrimp *Artemia* production in artisanal salt works in the Mekong delta in Viet Nam: a socio-economic success story as model for other regions in the world. In S. Lauret, ed. *Proceedings of the International Conference on Solar Salt Works & The Economic Value of Biodiversity*, p. 137-144. European Union Salt, Brussels, 245 pp.
Sui, L.Y., Deng, Y.G., Wang, J., Sorgeloos, P. & Van Stappen, G. 2014. Impact of brine acidification on hatchability, survival and reproductive performance of *Artemia* parthenogenetica and *Artemia franciscana* in saltponds, Bohai Bay, China. *Chinese Journal of Oceanology & Limnology* 32(1): 81-87.

Tackaert, W. & Sorgeloos, P. 1991a. Biological management to improve *Artemia* and salt production at Tang Gu saltworks in the People's Republic of China. In L. Cheng, ed. Proceedings of the International Symposium "Biotechnology of solar saltfields", p. 78-83. Tang Gu, PR China, September 17-21, 1990, Tanggu, Tianjin, PR China.

Tackaert, W. & Sorgeloos, P. 1991b. Salt, *Artemia* and shrimp. Integrated production in the People's Republic of China: the Tang Gu Saltworks. *World Aquaculture* 22: 11-17.

Tackaert, W. & Sorgeloos, P. 1993. The use of brine shrimp *Artemia* in biological management of solar saltworks. In H. Kakihana, H.R. Hardy Jr., T. Hoshi & K. Tokyokura, eds. *Proceedings of the 7th International Symposium on Salt*, 617-622. Vol. 1. Elsevier Science Publishers B.V., Amsterdam.

Van Stappen, G., Yu Haiying, Wang Xiaomei, Hoffman, S., Cooreman, K., Bossier, P. & Sorgeloos, P. 2007. Occurrence of allochthonous *Artemia* species in the Bohai Bay area, PR China, as confirmed by RFLP analysis and laboratory culture tests. *Fundamental and Applied Limnology* 170: 21-28.

Vu Do Quynh & Nguyen N.L. 1987. Inoculation of *Artemia* in experimental ponds in central Viet Nam: an ecological approach and a comparison of three geographical strains. In P. Sorgeloos, D.A. Bengtson, W. Decleir & E. Jaspers, eds. *Artemia Research and its Applications*, 253-269. Vol.3, Proceedings of the Second International Symposium on the brine shrimp *Artemia*, (Eds). Universa press, Wetteren, Belgium.

Zheng, B., Sun, S., Ma, L. 2004. The occurrence of an exotic bisexual *Artemia* species, *Artemia franciscana*, in two coastal salterns of Shandong Province, China. *Journal of the Ocean University of China* 3: 171-174.
# THE RAPID DEVELOPMENT OF THE INTEGRATED RICE-FISH, RICE-MITTEN CRAB AND RICE-CRAYFISH FARMING IN CHINA

Yongxu Cheng, Jiayao Li

## 1. Introduction

### 1.1 The integrated farming of rice and aquatic animals is the upgrade of rice-fish co-culture

The integrated farming of rice and aquatic animals developed on the basis of the traditional rice-fish co-culture systems in China. China has a long history of farming fish in rice paddies. There are records of this practice, more than 2000 years ago, in Hanzhong, Shanxi province and Chengdu, Sichuan province. But rice-fish co-culture only began to develop rapidly from the early 1980s, with the attention and support of governments and agencies at all levels. Since then, the integrated farming of rice and aquatic animals has entered a period of rapid development. From 1983 to 2000, the total area of integrated rice and aquatic animals farming has increased each year, from 4 413 ha to 1.53 million ha. In the meantime, the production of aquatic animals increased from 36 300 tonnes to 746 000 tonnes, with a yield raising from 5.5 kg/667 m² to 32.5 kg/667 m².<fnref n="31" />

From the end of last century to 2010 and the rise of interest in efficient agriculture, integrated farming of rice and aquaculture has been vigorously promoted due to its high comparative efficiency and important contribution to the increase of farmers' income. But at the same time, the rapid development of fish farming in rice fields has caused concerns about the sustainability of rice production, which area decreased from 1.53 million ha to 1.32 million ha. However, during this period, the decline in the cultivated area was compensated by the increase in rice yield to 1.24 million tonnes, as a result of improvements in farming technology. The fish yield also increased, from 32.5 kg/667m² to 61.9 kg/667 m². In some newly developed areas, the red carp yield even reached 75-100 kg/ 667m².

Traditional rice-fish co-culture is dominated by conventional fish species, mainly common carp, which does not have a high contribution to farmers’ income. But the development of new integrated rice and aquatic animal farming technologies could change this. Indeed, in recent years, crabs, crayfish, loach, rice field eel, softshell turtle have replaced the traditional species, because of their high economic value and adaptation to farming. “Rice-field aquaculture technology” was the main driving technology entering the households between 2008 and 2010. The new development concept and technologies created a new balanced relationship between rice and aquaculture, bringing about a new round of development. 2010 became a key turning point. The total area of integrated farming of rice and aquatic animal stopped declining and recovered. By 2016, it had already reached 1.52 million ha, with an aquaculture production increasing from 1.24 million tonnes to 1.63 million tonnes, and a yield rising from 61.9 kg/667m² to 76.8 kg/667m². In 2017, the total integrated area reached 1.87 million ha. Rice-fish, rice-mitten crab and rice-crayfish are now the most rapidly developing models.

### 1.2 The maturation of integrated farming of rice and aquaculture animal model is the result of the joint efforts of all parties

The integrated farming of rice and aquaculture has undergone a fast development during the last three decades, as a result from continued innovations, the introduction of new and high-valued species, the government policies support, market drivers, improvement in cooking methods, and increasing concerns on food safety (Wang *et al.* 2017):

* The academe has continuously explored and improved the theoretical framework of rice and aquaculture symbiosis, providing the theoretical background for its development.

<footnote n="31">³¹ 667 m² corresponds to one traditional Chinese unit of surface, the mu</footnote>
* The departments in charge of fishery promotion at all levels have summed up their scientific knowledge and practical experience to make great contributions to its promotion.

* The need for social development has provided impetus for its development as:

1. It has improved the farmers' income and greatly stimulated their enthusiasm for rice planting.

2. It has also greatly met the need for developing a more environmentally friendly and modern agriculture and the people's demand for high-quality aquatic products.

## 2. Distribution and current trends

### 2.1 Differences between the traditional rice-fish co-culture and the integrated rice and aquatic animals farming

The integrated farming of rice and aquatic animals relates to the traditional rice-fish co-culture by four characteristics:

* First, its rice yield is not lower than with the traditional rice-fish co-culture or rice monoculture.

* Second, the farmed aquatic animals species are not only the common carps, but also some higher value species, such as crab, crayfish, softshell turtle etc.

* Third, it puts more consideration on the food safety of aquatic animal.

* Finally, it requires feeding aquatic animals with balanced formulated diet, unlike the traditional rice-fish co-culture, in which no feed is used.

### 2.2 Distribution of traditional rice-fish co-culture in China

The traditional rice-fish co-culture is still widely distributed in China, and more than 25 provinces and municipalities in China have also developed the integrated farming of rice and aquatic animals. In 2016, 10 provinces, including Sichuan, Hubei, Hunan, Guizhou, Yunnan, Jiangsu, Zhejiang, Anhui, Jiangxi and Liaoning, had the largest area of rice-fish co-culture, accounting for 86.7 percent of the total area in China. Sichuan, Zhejiang, Hubei, Jiangsu, Anhui, Hunan, Jiangxi, Liaoning, Yunnan and Guizhou Provinces, have the highest production, accounting for more than 96.4 percent of the total output. Among them, Sichuan province has the largest rice-fish co-culture area, higher than 0.27 million ha and accounting for 18 percent of the country output: 350 000 tonnes, worth RMB 6.5 billion<fnref n="32" />, as well as RMB 18.5 billion of comprehensive benefits.

### 2.3 The change from “rice-fish co-culture” to “integrated farming of rice and aquatic animals”

The practices in rice fields depend on the historical development in the region, with two models currently coexisting: the traditional rice-fish co-culture and the new integrated farming of rice and aquatic animals. At present, both are balanced, following the transformation of the traditional fish farming model in rice field into the standardized integrated farming of rice and aquatic animals. As a result, the total area and yield of integrated rice and aquatic animals farming gradually increased. In addition, the integrated farming of rice and aquatic animals model has gradually extended to provinces where rice-fish farming was not traditional.

Among the ten main provinces practicing the traditional rice-fish co-culture, changes have been significant, with 100 percent of the total area converted to the new integrated farming of rice and aquatic animals model in Hubei province, 94.6 percent in Liaoning province and 87.6 percent in Anhui province (these provinces are classified as “sufficient transformation regions”). In Hunan and Yunnan provinces, the conversion is 74.8 percent and 59.2 percent respectively. These two provinces are ranked as “semi-sufficient transformation regions”, whereas Sichuan, Guizhou, Jiangxi, Jiangsu and Zhejiang provinces are “active transformation regions”. Gradual adoption of the integrated farming of rice and

<footnote n="32">³² RMB 1=USD 0.15.</footnote>
aquatic animals has also occurred in Jilin, Heilongjiang, Ningxia, Fujian, Guangxi, Tianjin, Henan and other provinces (regions and cities).

## 2.4 Typical models of integrated farming of rice and aquatic animals

### 2.4.1 Rice-fish

Rice-fish co-culture model has a long history and is widely distributed across China. Fish species are generally carps, black carp (Mylopharyngodon piceus), grass carp (Ctenopharyngodon idellus), silver carp (Hypophthalmichthys molitrix), bighead carp (Aristichthys nobilis) and common carp (Cyprinus carpio), especially the Oujiang color strain. This "field engineering transformation of rice fields" allows full use of the ecological environment and promotes mutually beneficial synergies between rice and fish. By producing an additional harvest in the same field, it permits full use of the water surface. Fish can also eat weeds, plankton and aquatic insects in rice fields, which reduces the feeding cost and the need to spread polluting pesticides. Fish also provide an organic fertilizer needed to grow rice. This model is suitable for large paddy fields with a good water quality. Stocking of fish seedlings should be as early as possible to prolong the growth period of fish without affecting the growth of rice seedlings. The fish growing-out extends to about 10 months by raising the ridges of the field to store water after rice harvest. During winter, fish can also be stored in the rice field.

### 2.4.2 Rice-crab

In rice-crab co-culture, the same principle of symbiosis between the crop and aquatic animal is applied. Crabs remove weeds and control pests in the field, and their excrements fertilize the water and promote the growth of rice. Moreover, rice provides an abundant natural bait and good habitat conditions for the river crabs, resulting in a mutually beneficial ecological cycle. The typical model of rice-crab co-culture is the "panshan model", under which, rice seedlings are alternately planted along a broad and narrow line. A suitable stubble control is used to prolong the growth period of crabs, and high quality crab feed is distributed to improve their quality. The rice-crab co-culture is mainly observed in Heilongjiang, Jilin, Liaoning, Ningxia, Zhejiang, Chongming county of Shanghai, Jiangsu, Hebei, Hubei and Yunnan. It is also widely used in Ningxia and Jilin provinces.

### 2.4.3 Rice-crayfish

The integrated farming of rice and crayfish is mainly distributed in southern provinces of China, such as Hubei, Jiangsu, Anhui, Hunan, Zhejiang, Yunnan, Sichuan. There are two models:

1. the rice-crayfish co-culture, in which crayfish farming is carried out with rice farming; and

2. the rotational rice-crayfish farming, in which both crayfish broodstock or seedlings are released after rice harvest, and crayfish are cultured during the idle period of rice planting.

In the rotational rice-crayfish, rice planting and crayfish farming do not overlap in time and space and the harm of rice field operation to crayfish is avoided. Due to its simple operation and high income, this model has developed rapidly in recent years and it has become the most popular integrated farming of rice and aquatic animals model in China, even becoming one of the main sources of farmed crayfish.

## 3. Integrated farming of rice and aquaculture

### 3.1 Generic technologies

One of the main reasons for the rapid development of integrated rice and aquatic animals farming is the reduction in the use of chemical fertilizers and pesticides through biological control while ensuring a double production of rice and aquatic animal. In Zhejiang for example, the use of pesticide in rice-shrimp decreased by 35 percent, and by 59 percent in rice-loach. In Ningxia, it decreased by 50 percent in rice-crab farming.
**3.1.1 Fertilization**

The conventional rice production relies mainly on chemical fertilizers, which can cause ecological and environmental problems when overused. With integrated farming, fertilization process has changed and new practices include:

1. Optimal fertilization based on soil testing. By determining the actual fertility of the soil and the nutrient needs for crops, the optimal fertilization ratio and fertilizer application amount are calculated using standard formula.

2. Segmented fertilization. Fertilization is provided at different stages: a basal fertilization followed several supplementary fertilizations. The principle is to consider basal fertilization as the main supply, and to supplement it by small amounts of supplementary fertilization. Organic fertilizer is mainly used in both basal and supplementary fertilizations.

**3.1.2 Pests and weeds control**

The control of pests and weeds in conventional rice farming mainly depends on chemical drugs, which causes problems related to pesticide residues and environmental pollution. With the integrated farming of rice and aquatic animals, the principle to prioritize the "ecological prevention and control, reducing the use of pesticides" applies.

1. Use of new pest control equipment. New insect trap lamps and insect nets have been invented and applied. The new insect net effectively blocks pests and protects rice. The new lamp uses different light sources and suitable spectral range to trap and kill pests.

2. Biological control. The competition between farmed and unwanted species is promoted in a way that allows controlling pests and weeds, by sharing the knowledge acquired through research on the biological characteristics of pests, weeds and aquaculture animals, and on the prevention and control of their performances.

**3.2 Technical performance**

In recent years, fourteen different integrated models grouped in five categories (rice-crab, rice-crayfish, rice-turtle, rice-fish, rice-loach) have been described. Over twenty key technologies have also been developed, allowing the traditional "rice-fish co-culture" to transform into rice, fish, crayfish and crab co-culture, rotation, intercropping etc. Some examples of innovations are described below:

**3.2.1 Innovations in rice-fish farming**

The "Rice-Fish Symbiosis" theory was put forward in 1981. In the integrated rice-fish ecosystem, fish can directly or indirectly control weeds and pests, utilize zoobenthos, plankton and detritus. On the other hand, residual feeds and feces from fish can also provide nutrients for rice. This system makes full use of the interaction between rice and fish, promotes multiple-level cyclic utilization of nutrients, and channels more energy flow into rice and fish (Ni and Wang, 1988).

While the integrated rice-fish farming was developing rapidly, a series of technical innovations were achieved. The most important one was digging ditch and puddle in rice fields, to provide refuge for fish during rice harvest time or the dry season. This innovation is also used for other integrated rice-field aquaculture animals such as crabs or crayfish. The width and depth of ditches are 1.5-4.0 m and 1.0-1.5 m, respectively, and the area of the refuge normally amounts to eight to ten percent of the rice field area (Zhang et al., 2017). The relationship between the importance of the refuge and the fish or aquatic animal yield was studied, and the results suggest that the design of the refuge is important for both rice and fish yields (Hu et al., 2016). Other infrastructure improvements are also important, in particular a dyke for water storage and fish farming during winter, or fencing for preventing predators (Gui et al., 2018).
### 3.2.2 Research progress on rice-crab farming

Following the wide adoption of the integrated rice-fish farming, Chinese government and non-government agencies started promoting the rice-crab (crab seed) co-culture with the same success (Li et al., 2007). This model has expanded in the north of China, in particular in the Liaoning and Jilin provinces where the most famous “Panshan model” is practiced. Research studies on this integrated rice-crab farming model highlighted several benefits:

1. Rice-crab farming improves soil fertility and soil texture (Wang et al., 2011a, Wang et al., 2013).

2. The impact of crabs on zoobenthos becomes increasingly significant with the growth of crabs, and a crab density of 10 ind.m-2 is recommended suggested to maintain the zoobenthos diversity (Li et al., 2013).

3. Rice-crab farming helps to reduce the competition for nutrients and light by weeds, reducing the reliance on chemical herbicide, and thereby increasing the rice yield (Xu et al., 2014).

4. Rice plants provide shelter for crabs, and keep the water temperature close to optimum levels, reducing the ratio of precocity of crabs (Wang et al., 2011a; 2011b). Precocious crabs have a low value because of their poor growth rate, poor survival and short life span (Li et al., 2011).

5. The study on cost-benefit suggests that further development of key technologies, increased governmental support, or higher production scale are important factors for improving cost-benefits of rice-crab farming in the future (Li et al., 2014).

### 3.2.3 Rotational rice-crayfish farming model

As a simple operation, rotational rice-crayfish farming has developed rapidly and become the most popular way of farming crayfish in China. Rice fields require a good water quality, and soils that retain water. The paddy size varies from one to a few hectares, with a ditch accounting for 3-6 percent of total paddy area. Levees and fencing must strong to ensure that water is withheld, and to prevent escape of crayfish (Gui et al., 2018). A combined group of submerged macrophytes including *Elodea canadensis*, *Vallisneria natans*, *Ceratophyllum demersum* and other species should be transplanted into the rice field to maintain the water quality and provide refuge for molting crayfish during the growth cycle. The coverage rate of submerged macrophytes is often over 50 percent of paddy area (Gui et al., 2018).

Two stocking strategies are used. In the most common one, crayfish broodstock (> 35 g/ind.) is stocked at 300-450 kg/ha, with a female to male sex ratio of 3:1. In the second strategy, young crayfish dislodged from females are stocked at a density ranging from 150 000 to 2 250 000 ind/ha (Gui et al., 2018).

In order to eradicate unwanted aquatic animals, quicklime is used 10-15 days prior to stocking (300-750 kg/ha). Following that, inorganic and/or organic manure is used to enhance the growth of feed organisms, and lights are also used to attract and trap insects that fall into the water, providing an additional food source. After the rice harvest, the straws are also used to cultivate feed organisms. In winter, fertilizers are used to enhance the growth of feed organisms for crayfish. Living forages are also used when available.

Due to its large scale and rapid development, a lot of studies have been done on the production and ecological effects of rice-crayfish farming. In addition to its advantages, studies also revealed the “dual character” of rice-crayfish farming:

1. In most case, rice yield of rice-crayfish model is increased by 4.6-14 percent compared with conventional rice monoculture. However, due to the higher price of crayfish, the rice management for rice was sometimes poor occasionally leading to a reduction of the rice yield.

2. Rice-crayfish farming improves the soil fertility, but aggravates the soil gleization.

3. The water use efficiency and conservation is not stable. In some cases water is conserved, but in some cases the water consumption is also increased.

4. The rice-crayfish farming decreases the use of chemical fertilizers and application of pesticides. The eutrophication risk results from the increased water nutrient concentration.
5. Crayfish in rice field can control the amounts of pests, but disease prevention and biodiversity conservation in rice-crayfish field still need further improvement (Cao *et al.*, 2017).

### 4. Economic performance

The ministry of agriculture established an integrated rice and aquatic animals farming demonstration area, allowing measuring some economic indicators. The rice yield was stable, at more than 500 kg per 667 m², and the efficiency of rice field increased by nearly 100 percent. In a national survey, the average benefit of integrated farming of rice and aquatic animals per 667 m² increased by more than 90 percent compared to that of rice monoculture. The average increase was RMB 524.76³³ in output value, up to > RMB 1000 yuan under the new integrated farming of rice and aquatic animals model. For example, the increase with the rice-crayfish model was RMB 1 456.28 (+258 percent), RMB 13 744.94 (+2290 percent) with the rice-turtle model, or RMB 2 484.33 (+351 percent) for the rice-crab model.

Among all models, the integrated rice-crayfish farming model developed the fastest. In 2017, the total area of crayfish farming in China reached 800 000 ha, generating a social and economic output value of about RMB 268.5 billion, with a direct output value of the farming industry at about RMB 48.5 billion. The area of integrated rice-crayfish farming alone was about 570 000 ha in 2017, accounting for 70.83 percent of the total farming area of crayfish. In 2017, the rice-crayfish farming accounted for 47.54 percent of the total area of integrated farming of rice and aquatic animals in China. This model plays an important role in promoting the efficiency of rice field and increasing farmers' income.

### 5. Constraints

There are still constraints in the development of these models, despite the rapid development in recent years:

1. The integrated farming of rice and aquatic animals model needs further enrichment and innovation. The current models cannot meet the various needs and specific conditions, especially the insufficient exploration of the benefits from supporting co-culture, intercropping and rotation. To popularize integrated farming of rice and aquatic animal, additional new models need to be developed.

2. Field engineering for large-scale mechanization: the trend of modern agricultural mechanization is becoming more and more obvious. The integrated farming of rice and aquatic animals often causes problems for the mechanization of harvest operations. As of now, if the stubble is not well connected, and the aquatic products in the rice field have not reached the market size, the mechanized rice harvest cannot be conducted.

3. It is urgent to formulate standards for developing integrated farming of rice and aquatic animals model. As the comparative benefit of aquaculture is usually higher than that of rice, the ditch and puddle are, sometimes, too large, deviating from the development objective of promoting rice production through aquaculture. Therefore, it is urgent to establish technical standards for clarifying technical indicators on stabilizing rice yield, ecological and environmental protection, standardizing the practices in integrated farming of rice and aquatic animal, and ensuring the sustainable and healthy development of this model.

4. Brand building needs to be further strengthened for rice produced under integrated farming of rice and aquatic animals model. At present, China has not yet established a famous brand of rice from these models of farming. The rice brand should be promoted all over the country through the joint effort of the alliance, between the provincial and municipal departments, and the enterprises.

5. Fishing methods and fishing tools need to be further improved. The rice fields differ significantly from the ponds, and the tools developed for harvesting ponds are often not

<footnote n="33">³³ RMB 1 = USD 0.15.</footnote>
applicable. As a result, it often takes a long time for aquatic products to be caught and sold, and if they get injured or damaged during the fishing process, it will affect their value and the profit. Thus, new fishing tools and fishing methods need to be developed.

## 6. Future prospects

In China, 30 million hectares of rice fields currently produce nearly 200 million tonnes of rice, generating an apparent rice yield of about 440 kilograms per 667 m². In 2017, the total area of integrated farming of rice and aquatic animals in China was 1.468 million ha, accounting for only 4.5 percent of the total rice field area of China. The rice yield at the integrated farming demonstration unit established by the ministry of agriculture is higher than 500 kg per 667 m², which highlights great room for development as it shows that it is possible to increase significantly the economic income with the production of aquatic animals without affecting the rice yield.

In the meantime, the development of integrated farming of rice and aquatic animals model has been given a lot of attention and was strongly supported by governments at all levels by providing a good policy environment during the 13th five-year plan period. Due to its considerable economic and ecological benefit, it has also received a wide recognition from all segments, with more and more enterprises and farmers trying it to produce rice and aquaculture animals, by integrated farming in their rice fields. In support to these dynamics, several investment may have to be considered.

### 6.1 Strengthening innovation of models and technologies

* In order to support the development goals of "stabilizing rice production and efficiency, promoting rice by aquaculture, ensuring quality and safety, and promoting ecological and environmental protection", continuous investment in new technological models will be needed to cope with the different ecological and geographical conditions, and farm specifications.

* Innovative key technologies for integrated farming are needed in many areas, including rice planting, aquaculture, pests prevention and control, stubbles joint, water and fertilizer management, field engineering, aquatic animals harvesting and processing, quality control etc.

### 6.2 Accelerating the demonstration and promotion of models and technologies

* Create a batch of large-scale and cost-effective demonstration units, with emphasis on scale, standardization, branding and industrialization.

* Organize the compilation of unified training materials and strengthen the training of key technical people.

### 6.3 Establish standards as soon as possible

* Organize the research to develop relevant standards for integrated rice and aquatic animals farming, and to accelerate the development of sub-standards for specific models of rice-crab, rice-crayfish, rice-turtle, rice-loach, rice-fish, etc.

* Document the technical performance of various integrated farming of rice and aquatic animals models in stabilizing rice production, increasing efficiency and product quality, protecting the environment, etc.

* Define technical performance requirements and technical evaluation methods, and gradually form a standard system for demonstration and promotion.

### 6.4 Strengthen the theoretical background

* Breeding of rice varieties suitable for integrated farming of rice and aquatic animal that are disease resistance and have appropriate growth cycle and taste.

* Study the role of biodiversity in building a suitable environment for the growth of aquatic animals, and to improve the use of natural feed in rice field.
* Study the ecological and economic effects of integrated farming of rice and aquatic animals system, by focusing on improving the efficient use of nitrogen, phosphorus and other nutrients.

## 6.5 Strengthen brand-building strategies

* Explore the ecological value of integrated farming of rice and aquatic animals model and build brands highlighting the ecological and healthy rice and aquatic products.

* Promote the production of rice field products in accordance with the requirements of pollution-free, green and organic food in various regions, and focus on ecological and health brands.

* Government departments should make use of their own advantages to increase guidance and publicity, so that the green ecological characteristics of rice field crops and aquatic products are well known.

## 6.6 Support new agricultural business entities and improve modern agricultural management system

* Support new types of agricultural business entities such as large professional households, family farms, leading enterprises and professional cooperatives.

* Strengthen the industrialization and actively promote the integrated farming of rice and aquatic animal.

* Establish an integrated value chain through unified varieties, management, service, distribution and brand to further enhance the industrialization.

## 7. References

Wang, Q., Li, Z., Gui, J., Liu, J., Ye, S., Yuan, J. & De Silva, S.S. 2017. Paradigm changes in freshwater aquaculture practices in China: Moving towards achieving environmental integrity and sustainability. *Ambio* 47(4): 1-17.

Ni, D.S. & Wang, J. 1998. *Theory and practice of fish culture in rice fields*. Agricultural Press, Beijing, China.

Hu, L.L, Zhang, J., Ren, W.Z., Guo, L., Cheng, Y.X., Li, J.Y., Li K.X., Zhu Z.W., Zhang J.E., Luo S.M., Cheng L., Tang J.J. & Chen X. 2016. Can the co-cultivation of rice and fish help sustain rice production? *Scientific Reports* 6 : 28728.

Gui, J., Tang, Q., Li, Z., Liu, J. & De Silva S.S. 2018. *Aquaculture in China: Success Stories and Modern Trends*. John Wiley & Sons, Oxford, UK.

Li, X.D, Dong, S.L., Lei, Y.Z. & Li, Y.H. 2007. The effect of stocking density of Chinese mitten crab *Eriocheir sinensis* on rice and crab seed yields in rice-crab culture systems. *Aquaculture* 273 (4): 487-493.

Wang, A., Wang, W., Ma, X.Z., Wang, Q., Yu, Y.Q. & Chen, W.X. 2011a. Study on the changes of water environmental factors in rice-crab culture system. *Hubei Agricultural Sciences* 50 (17): 3514-3519.

Wang, Q., Wang, W., Ma, X.Z., Chen, Z.Z. & Yu, Y.Q. 2011b. The Effects of Integrated Rice-crab Production on Soil Physical and Chemical Properties. *Hubei Agricultural Sciences* 50 (19): 3948-3952.

Wang, Y.J., An, H., Yan, Y., Liu, M.D. & Luo, G.X. 2013. A Study on Soil Humus Compositions and their Characteristics in Different Modes of Rice-Crab Combinations. *Chinese Journal of Soil Science* 44 (2): 343-347.
Li, Y., Wang, W., Ma, X.Z. & Zhang, Y.J. 2013. Effect of rice-crab culture system on zoobenthos diversity in paddy field. *Chinese journal of Eco-Agriculture* 21 (7): 838-843.

Li, X., Li, Z., Liu, J. & De Silva, S. 2011. Advances in precocity research of the Chinese mittencrab *Eriocheir sinensis*. *Aquacult. Int.* 19: 251-267.

Xu, M., Ma, X.Z. & Wang, W. 2014. Effects of different cultivation patterns on rice yield and crab in rice-crab culture system. *Scientia Agricultura Sinica* 47 (9): 1828-1835.

Li, J.Y., Chang, D., Li, B.N., Wu, X.G., Zhu, Z.W. & Cheng, Y.X. 2014. Benefit-cost analysis of different rice-based production systems. *Journal of Fisheries of China* 38 (9): 1431-1438.

Cao, C.G., Jiang, Y., Wang, J.P., Yuan, P.L, Chen, S.W. 2017. “Dual character” of rice-crayfish culture and strategies for its sustainable development. *Chinese Journal of Eco-Agriculture* 25 (9): 1245-1253.
# IMPROVING LIVELIHOODS OF INDIGENOUS AND LOCAL COMMUNITIES THROUGH INTEGRATION OF FISH IN TERRACED RICE FIELDS IN YUNNAN, PEOPLE'S REPUBLIC OF CHINA

Yanni Xiao

## 1. Introduction

Yunnan province is situated in the southwestern border of China. Complex geographical conditions in Yunnan have led to the formation of water resources in many rivers and lakes. Many major rivers originate in the province, there are more than 40 large natural lakes, dams and ponds with a surface area of 32 400 hectares. The unique climatic and geographical conditions in Yunnan have created rich and varied environments and, relatedly, a rich biodiversity. It has been particularly important for the development of the aquatic biodiversity and abundant fishery resources in Yunnan. As of 2013, 629 species of fish have been recorded in Yunnan province, of which 594 were indigenous fish, ranking first among all provinces in the country.

Honghe County is located in the southern part of Yunnan province. It is a key target county in the country's poverty alleviation and development strategy, which is characterized as “border area, ethnic minority, mountain area and poverty-prone”. The land area of the entire county is 2 028.5 square kilometers, with 96 percent covered by mountainous area. The total area of the terraced fields is about 20 000 hectares. The aggregate population of Honghe County is 340 600. Minority nationalities account for 96.2 percent of the total population which includes Hani, Yi, Dai, Yao and other ethnic groups. As of the end of 2016, there were 15 413 families (66 771 people) recorded as “under-poverty”.

The Honghe Hani terraced fields have a history of more than 1 300 years. They are also the birthplace of China's distinctive high quality red rice. Over 9 300 hectares of paddy fields are retaining water and producing rice as the staple food for the indigenous people and community. At the thirty-seventh World Heritage conference on 22 June 2013, the Honghe Hani terraces were listed as a World Heritage Site for culture, and also as a Globally Important Agricultural Heritage Site (GIAHS). This site is the forty-fifth World Heritage Site in China.

<figure><img src="image_133.png" /></figure>

©Yanni Xiao

<caption>**Figure 1:** Typical landscapes in the Honghe County, Yunnan province.</caption>

However, the Hani terraced fields are facing many problems limiting sustainable development. First, the overall development level of the economy is limited, the infrastructure of the rice paddies is poor, and the economic return of rice production is low due to low productivity and poor market price.
Second, there is hardly any use of mechanized equipment in terraced rice-field, and rather farmers still depend on physical labour for agriculture activities like tilling, ploughing, planting and harvesting. Third, the willingness of many locals to continue to rice farming is diminishing, and young people are emigrating away from the land, preferring to work in cities instead of staying in the country. Fourth, the phenomenon of abandoned terrace rice-paddy has emerged, and caused collapse of paddy dikes. Fifth, to reduce the agricultural labour required, instead of planting rice, some farmers replant sugarcane or vegetables in the terraced fields, and the spraying of pesticides/herbicides on these crops causes pollution also of the terraced rice fields. Sixth, local farmers are poorly educated and lack the knowledge for technical innovation. There is a need for capacity building so that they understand and use modern science and technology.

There is a proverb in Honghe County, “No matter the height of the mountain, there is a water spring at the top” that means water keeps running in the Honghe Hani terraces all over the year, no matter the height (山有多高, 水有多高). The natural resources are available, especially water, but they have not been fully utilized.

In 2016, to combat the challenges of livelihood improvement and poverty reduction in the Honghe County, the Yunnan Zhonghai Fishery Company (YZFC) began work on technology innovations in terraced rice paddies, and was technically supported by the Freshwater Fisheries Research Center (FFRC) of the Chinese Academy of Fishery Sciences (CAFS). The first postdoctoral research station in Yunnan province was set up in Honghe County to study locally-appropriate solutions. The researchers extensively studied the production, protection and sustainable development of Hani terraced fields and determined that the terraced field area is suitable for integrated rice-fish farming. There are more than 6 700 ha terraced rice paddies that could be benefit from this integrated practices in Honghe County. Moreover, it was found that the water quality in the rice fields conforms to the national standard for raising “pollution-free fish”. It was concluded that it is feasible to promote the integrated rice-fish system in Hani terrace fields.

As a complementary and symbiotic agricultural ecological circulation system, the “integrated rice-fish system” efficiently combines rice cultivation and aquaculture. It has the advantages of increasing rice yields while saving land and labour, and thus provides economic, ecological and social benefits for Hani people and their terraced fields. The integrated system will build a strong foundation for the sustainable development of Hani terraced fields in the future; it will provide a mature technology model for improving yields from paddy fields in Yunnan province in general and therefore be an effective way to reduce poverty.

The principle of rice-fish farming in Honghe County basically includes three parts: Economic Benefit, Ecological Benefit, and Social Benefit. By the end of 2020, with the goal of building 6 670 ha high yield demonstration fields in the whole county, the total economic output value can reach RMB 1.2 billion<fnref n="34" /> annually. Each household can improve their income of RMB 40 000 each year. The economic benefits of rice-fish co-cultivation can encourage local farmers to reuse abandoned paddy fields, or reduce planting area of sugarcane and corn, therefore, reducing the input of fertilizer and pesticide. On the other hand, before rice-fish farming, farmers need to reinforce ridges and dredge ditches. It improves the ability of drought resistance and flood drainage. Through increasing output value and terrace facilities construction, rural labor force was retained and accumulated practical experience for promoting the protection of Hani terrace and the development of ecological agriculture.

According to the experiment and demonstration analysis from Yunnan Zhonghai Fishery Company, the breeding loaches in the paddy field were obtained by the purchase price of RMB 24 per kilogram. Terraced fields of 0 to 700 meters above sea level can breed loaches for three seasons each year, with the annual output amount of 22 500 kg per hectare (1 500 kg per mu) and the output value of more than RMB 30 000. Terraced fields above 700 meters above sea-level can breed loaches for two seasons each year, with the output value of RMB 10 000 per mu. In accordance with the goal of building 6 670 ha high yield demonstration fields in the whole county, especially in terrace fields area, the total economic

<footnote n="34">³⁴ RMB 1 = USD 0.15.</footnote>
output value can reach RMB 1.2 billion annually. Each household can improve the income of RMB 40 000 each year. In this way, more than 22 860 families in the county can improve their incomes and get rich, more than 12 860 households, 51 200 people can cast off poverty. (The minimum income to be "not poverty is RMB 4 000/person/year). The traditional cultivation mode of Hani terrace fields in the past is only planted one crop of rice in summer and full of water in winter, otherwise, Terraces were suffering the risk of collapsing. In this season, we call it "winter fallow fields" (冬闲田). Terraces become natural ponds for fish farming, which provides enough natural food for fish growth. With the current stocking density of 300 kg per ha fish fry, the expected total output reaches 1 500 kg of carps per ha.

At present, YZFC focuses on making full use of the unique water resources during implementation of the "integrated rice-fish system" in Honghe County. Rice fields provide a suitable living environment and rich natural food organisms for loach resulting in good fish growth. Therefore, farmers neither need to do the extra feeding work, nor aeration. Loaches and other fish activities not only loosen the soil for rice roots and thus promote rice growth, but also provide organic manure which acts as fertilizer for the rice. According to the analysis, the rice grain yield can be increased by more than 5 percent per unit area. In order to increase the yield of rice and fish, it is necessary to maintain the paddy dikes and deepen the peripheral ditches regularly. The ability to resist drought and drainage in terraced fields has also been effectively improved.

YZFC has established the production chain from species selection, breeding, grow-out production, processing, to product marketing. The extension and management model was a combination of Government-support, capacity development of farmers and their organization into cooperatives, and development of private enterprise. The overall goal is poverty alleviation in terrace rice culture region of Yunnan province. The results showed that the "integrated rice-fish system" has great significance for the protection and development of Hani terraced fields.

The seed supply is the most important input in the innovative agro-aquaculture system. In order to provide good quality and a sufficient amount of loach fingerlings to the demonstration and extension of the rice-fish farming project, FFRC and YZFC have jointly invested USD 9.23 million to build a hatchery in Meng Long village, Honghe County. The first phase of the hatchery occupies an area of 30 ha and a 1 100 m² indoor hatching workshop. The hatchery has a capacity to produce 3 billion loach fingerlings (body length: 5-7 cm), with an output value of USD 185 million. It can meet the stocking demand of 6 700 ha terraced rice-field for high yield demonstration in the county. The hatchery contributed to promote integrated rice-fish demonstration to the county's terrace rice-paddy, and potentially to benefit for more than 1 million poor households. Furthermore, it fills the gap of fish seed supply in Yunnan Province, by providing a guarantee for the scaling up for "rice and fish integration".

Since 2016, FFRC has successfully provided two new aquaculture varieties to the hatchery in Honghe county and Hekou County for trial demonstration in rice-paddy. These are a farmed type of common carp called "Furui Carp No. 2" (福瑞鲤2号) and a farmed type of tilapia called "吉富罗" (JIFU - Genetically Improved Farmed Tilapia). Currently, the hatchery has 60 000 pairs of loach breeders, 30 000 pairs of 吉富罗 (JIFU) tilapia brooders and 14 000 pairs of Furui carp No. 2 "福瑞鲤2号" breeders. The fine breeder lines guaranteed the quality fish seed supply for the project implementation of rice-fish integration for Hani terraced rice-paddy innovation and poverty reduction.

In addition, YZFC has also carried out the following measures for the implementation of the "integrated rice-fish system" in the Hani Terrace rice-paddy.

## 2. Training

"Give a man a fish, you feed him a day; teach a man to fish, you feed him the whole life" is an eminent old saying in China, that means it is better to teach farmers some aquaculture skills than give them fish directly. YZFC has conducted technical training program on aquaculture for farmers in Honghe County
since 2016. Up to the end of 2017, there are more than 20 000 people were trained on aquaculture, they are from 13 townships, 120 village committees and 360 natural villages in Honghe County. The training courses were taught by specialists and experts from FFRC and YZFC. Before the training, specialists and experts did deep investigation on the local situation and resources in each village, by walking from town to town, village to village. The aquaculture models and techniques were taught based on local specific conditions, and on-site technical guidance were conducted accordingly. After the training, many local people became professional workers with rice-fish integration management skills, harvest and marketing knowledge. Some became “local experts” and provided technical service to neighbor farmers, capable in helping other poor families in fighting poverty in Honghe County.

<figure><img src="image_134.png" /><figcaption>**Figure 2:** Training courses on aquaculture for farmers in Honghe County.</figcaption></figure>

**3. Cooperative creation**

The cooperative of rice-fish integration is organized by local community farmers engaged in terrace rice-paddy spontaneously, aiming to share technical experience, unite farmers for inputs purchasing and contracts with leading enterprises in seed supply, farming standards, product marketing, etc. The Honghe county government actively encourage the poor households to join professional cooperatives, explains the advantage and working mechanism, and liaisons governmental poverty alleviation funds to find any financial loan support. By joining professional cooperatives, farmers can easily solve problems of fish seed supply, technical services, financial support and products marketing. To incentive the standardized farming operation and quality products, the Honghe county government provided bonus of USD 300 to each poor household who has joined the program. Public banks and rural credit cooperatives offered interest-free loan (maximum USD 7 700) for each family when they are endorsed by professional cooperatives. At present, there are 196 professional cooperatives on standardized rice-fish farming in Honghe County.

**4. Land transfer and consolidation**

In cases of farmers who own land but lack operational laborers and ability in farming management, they are encouraged the transfer of their rice paddy to farmers who are capable in production scaling up. The households receive rent through the transfer of land and paid labor work in participating through the production cycle. So that the poor householder will convert from “aid receiver” into “self-aided” for a sustainable poverty alleviation manner.

**6 Guaranteed price**

Yunnan Zhonghai Fishery Company guarantees provision of aquaculture seedlings at a price below 30 percent of the market price of Yunnan seedlings. 2017 to 2018, the loach seedling price and the carp seedling price which provided for standardized farming-breeding professional cooperatives and
communities were RMB<fnref n="35" /> 0.1 per tail and RMB 25 per kilogram. When carp and loach grow up to the market-required specifications, Zhonghai Fishery company buys them back at a predetermined price (loaches are RMB 24 per kilogram and the carps are RMB 35 per kilogram in 2017 to 2018). This cooperation model has effectively solved the problems of farmers' lack of breeding technology and marketing connection.

From 2016 to 2017, YZFC provided a total of 160 million fish fingerlings to Hani terrace rice-fields, with an area of 1 500 ha, and associated more than 2 000 households covering 13 towns, 112 village committees, 336 natural villages, which helped 10 000 people to get out of poverty and become rich. In 2018, the overall implementation area of rice-fish co-cultivation is 1 667 hectares (Fish: 1 000 ha, Loach: 667 ha). At the beginning of 2018, Zhonghai Fishery Company had started the experiments on the development of integrated rice-bullfrog system on the edge of the terrace fields and paddy fields which rarely uses in rice production.

On June 15, 2017, FAO officially opened the YZFC Hani Terrace “Integrated Rice-Fish System Research and Training Center” which is the first of its kind with such an award by FAO in China.

<figure><img src="image_135.png" /></figure>

©Yanni Xiao

<caption>**Fig. 3:** Official opening of the YZFC Hani Terrace “Integrated Rice-Fish System Research and Training Center”.</caption>

On October 9, 2018, Mr. Tang Qisheng, academician of the Chinese Academy of Engineering, Mr. Zhang Xianliang, the director of Fisheries Bureau, Ministry of Agriculture and Rural affairs of China, and 36 experts from the Chinese Academy of Engineering, the Chinese Academy of Aquatic Sciences held a technical seminar on rice and fish comprehensive cultivation in Hani terraced fields in Honghe County. On the same day, Academician Workstation of Tang Qisheng was officially established in Honghe County.

<footnote n="35">³⁵ RMB 1 = USD 0.15.</footnote>
<figure><img src="image_136.png" /><figcaption>**Figure 4:** Technical seminar on rice and fish comprehensive cultivation in Hani terraced fields.</figcaption></figure>

In March 2017, several senior government officers of Yunnan province visited the hatchery of YZFC and sites of “integrated rice-fish system” in Hani terrace rice-fields, as well as the local participating households, they highly prized the contribution of FFRC and YZFC. They stated that “integrated rice-fish system” is an innovative approach in agro-aquaculture system. This model is not only the development of agroecology and circular economy, but also benefit to improve the livelihood of the indigenous people through double income sources (i.e. revenue is received from both the rice and the fish). The government departments have pledged to support the further development of leading agricultural companies, such as YZFC, to expand in meeting more and more demand of poverty reduction in the province. In addition, the government will support the branding establishment for ecological agriculture in Yunnan province.

<figure><img src="image_137.png" /><figcaption>**Figure 5:** In March 2017, several senior government officers of Yunnan province visited the hatchery of YZFC and sites of “integrated rice-fish system” in Hani terrace rice-fields.</figcaption></figure>

FFRC and Zhonghai's "integrated rice-fish system" has just started. In 2019, several problems remain to be tackled. At macro level:

1. The basic research on rice and fishery comprehensive cultivation is still weak. The rice-fish integrated breeding models and techniques suitable for different regions and altitudes still need to be further studied, screened and matured. We will keep exploring more models which are suitable for different regions.

2. The strength and effectiveness of technical training still needs to be improved. We need to explore appropriate teaching methods so that local people can understand and learn as soon as they see them.
3. Lack of special funds to support ecological recycling agriculture projects in national agricultural comprehensive development zones in Yunnan province. We will actively apply for policy support and financial support from the government with our own resources. At the same time, we appeal to all people and enterprises who are concerned about Hani terraces to invest in Honghe.

At the company level, YZFC will continue to promote the work of rice-fish farming in Hani terraced fields, and actively establish the brand of products such as Well-known Trademark, organic products etc. On the other hand, we will operate modern technology and networks to build online sales platforms. Let more people know about Hani terrace fields and purchase products in efficient ways to help local people.

## 7 Acknowledgements

Specially thanks to FAO, FFRC, Chinese Academy of Aquatic Sciences, Fisheries Bureau of the Agricultural Department of Yunnan Province, the government of Honghe County.
LIST OF THE AUTHORS OF THE CONTRIBUTED PAPERS

(Alphabetical order)

**Cesar William Albuquerque De Sousa**
Empresa Brasileira de Pesquisa Agropecuária
(Embrapa) Pesca e Aquicultura
Palmas-TO
Brazil

**Diana Edithe Andria Mananjara**
FOFIFA/DRZVP
Antananarivo
Madagascar

**Rija Andriamarolaza**
APDRA
Antananarivo
Madagascar

**Joël Aubin**
INRA
Agrocampus Ouest
Rennes
France

**Harrison Charo-Karisa**
WorldFish
Egypt

**Yongxu Cheng**
Shanghai Ocean University
Pudong
China

**Valerio Crespi**
Food and Agriculture Organization of the
United Nations
Rome
Italy

**Lionel Dabbadie**
Cirad/FAO
Rome
Italy

**James Diana**
University of Michigan
Ann Arbor
United States of America

**Peter Edwards**
Emeritus Professor
Aquaculture and Aquatic Resources
Management
Asian Institute of Technology
Klong Luang, Pathumthani
Thailand

**Hillary Egna**
Oregon State University
Corvallis
United States of America

**Wenresti Gallardo**
Associate Professor
Department of Marine Science and Fisheries
College of Agricultural and Marine Sciences
Sultan Qaboos University
Oman

**Kamala Gharti**
Agriculture and Forestry University
Rampur, Chitwan
Nepal

**Matthias Halwart**
Aquaculture Branch Head
Fisheries and Aquaculture Dept.
Rome
Italy

**Xu Hao**
Fishery Machinery and Instrument Research
Institute
Chinese Academy of Fishery Sciences
China

**Jérôme Hussenot**
IKT*HUS Consulting
Noirmoutier en l'Ile
France

**Nick Innes-Taylor**
FAO consultant and Advisor
Department of Livestock and Fisheries
The Lao People's Democratic Republic
**Sabita Jha**

Agriculture and Forestry University
Rampur, Chitwan
Nepal

**Sidiki Keita**

Directeur Général de l'Agence Nationale de l'Aquaculture
Ministère des Pêches, de l'Aquaculture et de l'Économie Maritime
Conakry
République de Guinée

**Jiayao Li**

Shanghai Ocean University
Pudong
China

**Phan Thanh Lam**

Research Institute for Aquaculture
Minh
Viet Nam

**Philippe Martel**

APDRA
Antananarivo
Madagascar

**Olivier Mikolasek**

Cirad
Montpellier
France

**Jean-Michel Mortillaro**

CIRAD-FOFIFA
Antananarivo
Madagascar

**Fr Godfrey Nzamujo o.p**

Songhai Centre Porto-Novo
Benin

**Ahmed Nasr Allah**

WorldFish
Egypt

**Manoel Xavier Pedroza Filho**

Empresa Brasileira de Pesquisa Agropecuária
(Embrapa) Pesca e Aquicultura
Palmas
Brazil

**Rajan Poudel**

Agriculture and Forestry University
Rampur, Chitwan
Nepal

**Sunila Rai**

Agriculture and Forestry University
Rampur, Chitwan
Nepal

**Modestine Raliniaina**

FOFIFA/DRZVP
Antananarivo
Madagascar

**Domoina Rakotomanana**

FOFIFA/DRZVP
Antananarivo
Madagascar

**Rahul Ranjan**

Agriculture and Forestry University
Rampur, Chitwan
Nepal

**Madhav Shrestha**

Agriculture and Forestry University
Rampur, Chitwan
Nepal

**Chanthaboun Sirimanotham**

Deputy Director-General
Department of Livestock and Fisheries
The Lao People's Democratic Republic

**Krishna R. Salin**

Aquaculture and Aquatic Resources
Management
Asian Institute of Technology
Thailand

**Patrick Sorgeloos**

Laboratory of Aquaculture and Artemia
Reference Center
Ghent University
Belgium

**Liying Sui**

Asian Regional Artemia Reference Center
College of Marine and Environmental Sciences
Tianjin University of Science and Technology
China

**Montakan Tamtin**

Phetch Buri Coastal Aquaculture Research and
Development Center
Thailand
**Nguyen Van Hoa**

College of Aquaculture and Fisheries
Cantho University
Viet Nam

**Gilbert Van Stappen**

Laboratory of Aquaculture and Artemia
Reference Center
Ghent University
Belgium

**Yanni Xiao**

Yunnan Zhonghai Fishery Company (YZFC)
Yunnan province
China

**Wang Xiaodong**

Fishery Machinery and Instrument Research
Institute
Chinese Academy of Fishery Sciences
China

**Liu Xingguo**

Fishery Machinery and Instrument Research
Institute
Chinese Academy of Fishery Sciences
China

**Derun Yuan**

Network of Aquaculture Centres in
Asia-Pacific
Bangkok
Thailand

**Gu Zhaojun**

Fishery Machinery and Instrument Research
Institute
Chinese Academy of Fishery Sciences
China
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<figure><img src="image_139.png" /></figure>
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A workshop, aimed at collecting and documenting the diversity of integrated agriculture aquaculture practices (IAA), was organized on 25 August 2018 in Montpellier, France, during the International conference AQUA 2018 of the World and European Aquaculture Societies.

The objectives were to clarify how an IAA implemented within an agroecological approach could help alleviating poverty and hunger, and to identify the knowledge gaps to be filled to ensure the sustainability of IAA. Twenty five speakers presented background information and case studies in front of a full room.

ISBN 978-92-5-132010-5 ISSN 2070-6987

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9

789251

320099

CA7209EN/1/12.19