21
Soft‐shelled Turtles

Qingjun Shao and John S. Lucas

21.1 Introduction

The Chinese soft‐shelled turtle, Pelodiscus sinensis, is a high‐valued species for farming in the Asia region (Figure 21.1). Traditionally, the soft‐shelled turtle is considered to have medicinal properties due to its high nutritional value. As well as its food value, it was cultured in common carp ponds in order to control fish stocking density. This is according to the first record in aquaculture history by aquaculturist Mr. Fan Li in ‘Fish Farming Experiences’, more than 2400 years ago (Ling, 1977).

Image described by caption and surrounding text.

Figure 21.1 The Chinese soft‐shelled turtle, Pelodiscus sinensis.

Source: V. Menkov 2009. Reproduced under the terms of the Creative Commons Attributions license, CC‐BY‐SA 3.0.

21.2 Biology

The Chinese soft‐shelled turtle, Pelodiscus sinensis (also known as Trionyx sinensis), has the colloquial names, Zhong‐hua‐bie, Jia‐yu (shelled fish, with ‘shell’ bone) and Wang‐ba in Chinese. In Mainland China, there are two genera and six species of soft‐shelled turtles (Family Trionychidae). The two genera are: Pelodiscus and Palea. The widespread distribution of Pelodiscus sinensis in China even includes Qinghai, Xinjiang and Tibet in north‐western parts of China. Furthermore, farming this species has spread to all provinces and autonomous regions in China. Beyond mainland China, this species is distributed in Taiwan, Japan, Korea and Vietnam1. It has been introduced to Malaysia, Singapore, Thailand, Philippines, Timor, Batan Islands, Guam, Hawaiian Islands and mainland USA.

Another soft‐shelled turtle, Palea steindachneri, is listed in Appendix III of the CITES Convention and as an Endangered Species in the IUCN Red List (2007). Farming has considerably impacted the wild populations but farming of Palea steindachneri continues in China.

21.2.1 Morphology and Physiology

Soft‐shelled turtles do not have the usual hard, fused plates that make up the carapace (shell) of most turtles. The central part of their carapace has solid bone beneath it like other turtles, but its surface is leathery and especially flexible along the sides, which are known as ‘skirts’. These are clearly evident in Figure 21.1.

Chinese soft‐shelled turtles are amphibious, and they usually live in salinities of not more than 3–5‰. They prefer the secluded regions of a wide range of aquatic environments, rivers, lakes, reservoirs, ponds, pools and mountain streams, where they inhabit the shore substrates and bushes. They are belligerent, aggressive and predatory, but sensitive to the movement of objects and other kinds of animals in their vicinity. Their lungs are used for respiration both on land and in the water, as they rise to breathe. They also use a pharyngeal organ with villi‐like gills to get oxygen from the ambient water, especially when immersed during their hibernation.

As reptiles, their body temperature varies and is similar to their immediate environment. Thus, they are sensitive to variations in water temperature. Their metabolic rate declines sharply when the water temperature drops below 20°C. They stop feeding at temperatures below 15°C and hibernate under pond mud or in wet soil above the pond water level when the temperature is below 10°C. When the water temperature is above 35°C in summer, the turtles retreat under the shade of trees. The suitable temperature range for the turtle’s growth is about 20–35°C and the water temperature for optimum growth is 28–32°C, especially in indoor culture.

During hibernation, there is little respiration and a very low metabolic rate. The lungs respiratory function is replaced by the pharyngeal villi for getting oxygen in water or in wet sands. After hibernating for 5–6 months over winter, the body weight is reduced by 10–15%, and some physically vulnerable turtles may die during a long period of hibernation; that is, especially when hibernating in anoxic conditions under mud with high organic matter content.

Soft‐shelled turtles usually emerge from the water and bask for 2– 3 h/day on sunny days in summer to kill surface pathogens, e.g., fungi and bacteria. This helps to promote shell growth, and body calcium and phosphorus metabolism. It also increases their body temperature and metabolic rate if the water temperature is not high enough for good growth. So, it is very necessary to have 5–10% land beside an earthen pond for basking or to build a similar amount of accessible basking roof above water level.

21.2.2 Diet

Soft‐shelled turtles are voracious feeders and omnivorous, but high‐protein animal food is favoured. In the wild, juvenile soft‐shelled turtles search for large zooplankters, aquatic insects and other invertebrates, such as aquatic worms (Limnodrilus hoffeisteri), and invertebrate larvae as their food. As juveniles grow, they begin to prey on shrimp, tadpoles and small fish. When animal food is short, they will feed on aquatic and terrestrial plants, and scavenge on animal carcasses. In farming conditions, they are fed on high‐quality artificial feeds, internal organs of poultry, small fish, shrimp, snails and clams, depending on the farming method. Plant feeds such as various seeds, melons, vegetables, and leaves of aquatic and terrestrial plants may be used as supplementary feeds when necessary.

Although soft‐shelled turtles can survive for a long period without any feed, their growth is inhibited, and body weight reduced under such conditions. Excessive culture density or food shortage will cause cannibalism. This especially occurs when various sizes of soft‐shelled turtles are cultured together: the small individuals may be eaten by the large ones. Also, the small turtles often cannot get enough feed for normal growth under these competitive conditions.

21.2.3 Growth

The growth of soft‐shelled turtles is relatively slow in the wild. The hibernation period lasts about half a year in the Yangtze River Basin regions, and the growth period is not more than 6 mo each year because the water temperature is unfavourable, being less than 25°C. In the wild, it usually takes 4–5 years for turtles to reach marketable size in Yangtze River Basin regions. However, under artificial farming conditions where water temperature is kept about 30°C, with good water quality and artificial feeds, the turtles grow rapidly and may reach a commercial size of about 400 g in 8–12 mo.

Like many other cultured animals, the growth rates of soft‐shelled turtle within the same batch of juveniles under the same conditions vary from individual to individual. This can lead to cannibalism and they need to be sorted and cultured in size classes during artificial culture conditions.

21.2.4 Reproduction

Reproduction follows a typical reptilian pattern. The male fertilizes the female through copulation. Eggs are fertilized in the female’s reproductive system, developing internally for 10–20 days and then being laid to hatch later. Soft‐shelled turtles reach sexual maturity in the wild:

  • at about six years of age in the north of the Yellow River (ca. 37°N);
  • at about four years in the middle and lower Yangtze River region (ca. 32°N);
  • at three years in the south of China;
  • at just two years of age in Hainan (ca. 19°N) and Taiwan (ca. 23°N).

These differences result from the temperature regime during the turtles’ growth and development. A further effect of temperature regimes between northern and southern China is variation in the duration of the oviposition period. It is from:

  • June to August in the most northern regions of China;
  • May to August in central and eastern China;
  • April to September in southern regions of China; and
  • March to October in the Hainan and Taiwan islands.

Temperature also plays a role in mating: in the middle and lower Yangtze River regions, the sexually mature turtles mate when water temperature increases to about 20°C in April or May.

With day‐length and temperature increasing, females gradually begin laying eggs as spring turns into summer. The female turtles lay eggs two or three weeks after mating. Eggs are usually laid at night when the surroundings are quiet. Laying sites are usually concealed places and eggs are buried in moist soft soil above the water level. In order to prevent direct sunlight, reduce evaporation, avoid groundwater flooding and maintain enough air in the nest, turtles make their individual burrows in shady places. They put sand back over the burrow with their hind limbs and smooth the surface flat with their plastron (under surface of carapace) to erase traces of the burrow and prevent pests from invading it. The hatchlings emerge from the burrow and move immediately down into the nearby water.

About 20 days later, the turtles mate again after previous egg laying. Adults can mate several times during breeding seasons each year or there can be multiple egg batches after one mating. Sperm can survive in the female’s fallopian tubes for five or more months. While soft‐shelled turtles lay eggs several times a year, the number of eggs per batch, the timing of laying, the number of egg batches and the egg weight are directly related to the female’s body size, age, nutritional status, geographic location and genetics, etc. Approximate numbers of eggs per batch range from several to more than 20, and 3–5 batches of eggs may be produced in a year by a female turtle.

21.3 Aquaculture Development

As well as extensive and polyculture, intensive farming of soft‐shelled turtles in China can be traced back to the late 1970s. Furthermore, the development of intensive farming may be divided into three phases:

  1. The first phase of modern development was from the mid‐1970s to the early 1990s. In this phase, the farming of soft‐shelled turtles depended mainly on wild‐caught turtles. Soft‐shelled turtles were farmed at low density in polyculture ponds and production was very limited.
  2. The second phase was from the early to mid‐1990s. It was a period of rapid development (Figure 21.2). With the improvement of people's living standards and higher incomes, the demand for soft‐shelled turtles increased rapidly in Chinese coastal regions and bigger cities. At the same time, aquaculture technology developed into intensive monoculture indoors in an environment with water temperature controlled around 28°C to 32°C. Stocking density significantly improved with about 40–80 turtles/m2 from hatchlings up to body weight 50 g and about 15–30 turtles/m2 for body weights greater than 150 g. The price of the soft‐shelled turtles increased to 580 CNY/kg (ca.‐ USD 85). Hatchlings were 30–35 CNY each and the price of broodstock reached more than 1000 CNY/kg in Zhejiang Province, which was one of the major regions for soft‐shelled turtles. Driven by high profits, various regions entered the turtle culture industry, promoting the rapid development of soft‐shelled turtle farming.
  3. The third phase is from the mid‐1990s to the present. It is a continuing phase of rapid development (Figure 21.2). Due, however, to uneven quality and taste of meat, overproduction and steadying of market demand, prices declined (Figure 21.3). Farming methods changed from the second phase of high‐density indoor or outdoor monoculture or both, to lower stocking densities together with an increasing level of fish and turtle polyculture. With further improvement of farming techniques such as disease prevention, strains and hybrid selection, the production and demand for soft‐shelled turtles in mainland China were almost balanced. Farming techniques tended to mature, and it was almost the most profitable aquaculture practice in China, so that soft‐shelled turtle farming in indoor dark tanks and outdoor earthen ponds was continuously developed, and more and more companies and businesspeople invested in the turtle farming.
Area graph illustrating the annual production of soft-shelled turtles, Pelodiscus sinensis, in China over the period 1994–2014, displaying an ascending curve with shaded region.

Figure 21.2 Annual production of soft‐shelled turtles, Pelodiscus sinensis, in China over the period 1994–2014.

Source: Data from FAO 2015. Source: Reproduced with permission from John Lucas.

Area graph of value per kg of soft-shelled turtles, Pelodiscus sinensis, in China over the period 1994–2014, displaying a curve with shaded region.

Figure 21.3 Value per kg of soft‐shelled turtles, Pelodiscus sinensis, in China over the period 1994–2014.

Source: Data from FAO 2015. Source: Reproduced with permission from John Lucas.

Production techniques are well‐developed and compare favourably with those developed for many other aquacultured species in mainland China.

21.3.1 Commercial Farming

Traditionally, soft‐shelled turtles supplied in markets were fished from local ponds, reservoir, rivers and lakes. The regional popularity of the turtle stimulated interest in pond culture in the early 1950s and 1960s. In the early 1980s, soft‐shelled turtles in ponds were popular in the Yangtze Basin areas and the Pearl Basin areas including the provinces of Zhejiang, Hunan, Hubei, Jiangxi, Jiangsu, Anhui, Guangdong and Guangxi. Large‐scale indoor culture of soft‐shelled turtles on an intensive scale started in the 1990s as described in section 21.3. Expansion was mainly stimulated by high profits with:

  • significantly reduced culture time;
  • lower prices of hatchlings; and
  • development of feed and culture technology.

Local markets remained the outlet for all productions since the incomes of the people in these two basins were higher than other regions in Mainland China. Total production in mainland China since 1995 is shown in Figure 21.2.

In recent years, the province of greatest soft‐shelled turtle production in China has been the Zhejiang Province, which is located in the south of Shanghai and near Lake Taihu. The Great Canal of Beijing extending to Hangzhou and the Qiangtang River crosses the province. Based on estimation from Zhejiang Bureau of Ocean and Fisheries, the total amount of soft‐shelled turtle production in Zhejiang Province in 2008 was 110 000–120 000 t (about 52% of the total soft‐shelled turtle production in Mainland China). In terms of marketing, there were about 41 000 t from Jiaxin City, 27 500 t from Hangzhou City, 22 000 t from Huzhou City and 5200 t from Jinhua City. The total value was about 5 billion CNY. The total culture pond area is about 7300 ha (730 million m2), and the total area of indoor tank culture with temperature control is about 7.5 million m2.

21.4 Culture Facilities

The culture methods for soft‐shelled turtles consist mainly of outdoor earthen ponds, indoor concrete tanks, and a combination of both through the phases of development. The quality of turtles cultured indoors in concrete tanks is lower than those from earthen pond culture, and pharmaceuticals are used more frequently to prevent diseases in indoor culture. However, the period of rearing to marketable size is shorter and the costs per kg of turtle produced are lower for indoor culture. Thus, indoor culture is attractive as a more economic industry. Currently, indoor cultured turtles account for more than half of the total production.

21.4.1 Indoor Culture

The construction of indoor concrete tanks must meet the environmental requirements of soft‐shelled turtles. They must have good insulation properties and be equipped with appropriate heating, aeration, drainage and other facilities. The tanks are 15–45 m2 of bottom area and 60–120 cm height. The upper tank walls curve inwards 8–10 cm to prevent the turtles from escaping. Net bags are suspended above the bottom of the tanks in order to add hiding places and so reduce the level of biting at high stocking densities. Net bags being used in indoor tanks are shown in Figure 21.4. Culture in the dark also assists in reducing the level of biting.

Image described by caption and surrounding text.

Figure 21.4 Netting bags that are used to provide cover in indoor tanks for soft‐shelled turtles.

Source: Reproduced with permission from Qingjun Shao.

Progressively more farms are using temperature‐controlled indoor tanks to rear the soft‐shelled hatchlings up to 50–150 g then transfer them to earthen ponds for subsequent grow out. In this way juveniles are initially cultivated in controlled conditions to improve growth and survival rates. This is a two‐stage method of culture.

21.4.2 Pond Culture

Pond culture of soft‐shelled turtles includes monoculture, and polyculture with fish, shrimp and aquatic plants. The quality of the soft‐shelled turtles cultured in this way is quite similar to that of wild turtles and is much better than those cultured indoor in dark tanks. Furthermore, this culture method also improves the usage of water, with less water exchange and less energy required to supply water to the culture system. The farmer’s income will increase when prices for pond‐reared turtles are higher.

Typical pond preparation is required before stocking the turtles in earthen ponds. This includes preparation such as:

  • clearing surplus silt
  • checking the water inlet and outlet
  • building escape‐proof walls
  • disinfecting the pond with quicklime

Water must be kept 1.0–2.0 m in depth, with 10–25 cm bottom sludge, and the slope of the pond walls must be 45° or less. It is necessary to keep the dry land or platform about 5–10% of pond water area for the turtles to bask during the daytime. The height of escape‐proof walls must be 40–50‐cm. Particular attention is needed for the water outlet and inlet to prevent turtles escaping.

The stocking density depends on turtle size or body weight, pond depth, and how much yield the producer hopes to gain. Suggested stocking densities of turtles are shown in Table 21.1.

Table 21.1 Recommended stocking densities of Chinese soft‐shelled turtles in earthen ponds.

Body weigh (g)Stocking density in
earthen ponds (no./m2)		Suitable earthen
pond sizes (m2)
4 –506–1250–100
51–1503–6500–1500
>1501–2500–5000
Broodstock0.5–11000–15 000

Turtles are stocked in grow‐out ponds when water temperature reaches about 25°C, from March to May, and the optimal body weight of turtles is 150–250 g. Before stocking, turtles are disinfected with 3% salt water or 20 mg/L potassium permanganate for 5–10 min. Various kinds of ponds are built with an escape‐prevention structure or enclosure in order to confine the turtles (Figure 21.5).

Image described by caption.

Figure 21.5 The edge of a pond with walls to prevent turtles from escaping and with feeding sites for placing food along the slope above the water level, out of reach of fish.

Source: Reproduced with permission from Qingjun Shao.

In order to have good pond water quality, the soft‐shelled turtles are polycultured with other aquatic animals such as filter‐feeding fish and bottom feeders; and aquatic plants such as water hyacinth (Eichhornia crassipes) and water lettuce (Pistia stratiotes). In general, in order to avoid fish taking the turtles’ feed, feeding sites are established near the pond water level. Feeding sites are shown in Figure 21.5. In order to control small feral fish, some carnivorous species of fish, such as mandarin fish, may be stocked at the same time. The stocking densities of the fish are based on what natural food sources are available in the ponds and the suggested numbers are listed in Table 21.2.

Table 21.2 Recommended stocking densities of various fish species polycultured in earthen ponds with Chinese soft‐shelled turtles, Pelodiscus sinensis.

Fish speciesBody weight
(g)		Stocking density
(number/ha)
Silver carp100–200500–200
Bighead100–200150–450
Crucian carp20–100300–750
Common carp20–100300–600
Grass carp150–300100–500
Mandarin fish5–10100–300

In the process of culture, it is necessary to pay considerable attention to management of water quality and disease prevention. There is no need to set up aerating machines in ponds because the various species in polyculture are feeding in their niches at a reasonable nutritional level without major inputs of feed. Water quality is maintained within the requirements of pH 7–8, total alkalinity 0.5–3.5 mmol/L, transparency 25–35 cm, and water colour of yellow‐green or tea green. Quicklime or biological agents are used to regulate the water quality every 15–20 days if the water is too fertile. Diseases are common in ponds and there may be regular use of quicklime or a mixture of copper sulphate and ferrous sulphate, at a ratio of 5:2 and concentration of 0.7 g/m3. Medicated feeds may be used, such as those used for fish, if the turtles are in poor health.

There needs to be quietness when the turtles are basking on sunny days or they abruptly return to the water and this behaviour, with the advantage of removing fouling and pathogens from the body surface, is reduced.

21.5 Culture Stages

21.5.1 Breeding

The cultivation of broodstock turtles is carried out in specialized outdoor ponds. The pond is disinfected by the application of quicklime or bleaching powder (chlorine) before stocking. The optimum stocking density is 0.5–1.0 turtle/m2. Broodstock are stocked before the autumn season so that they can have enough time to adapt to their new environment and get enough nutrients for reproduction next summer. They are given specific artificial feed or natural feed, such as fresh trash fish, prawn, snails, earthworms and vegetables in the ponds. Daily management requires strict feeding times and locations, stable feed quality and suitable quantity, and a quiet environment. Meanwhile, the water depth and transparency of broodstock ponds are maintained at 150–180 cm and 35–40 cm, respectively. Specific attention is paid to the management of water quality and to disease prevention or control.

All male and female soft‐shelled turtles selected as broodstock must be healthy, without any injury and more than 3–4 years old. They must be physically robust, and more than 1 kg and 2 kg body weight for males and females, respectively. The appropriate female to male ratio is 3–5: 1. More than 85% of eggs will hatch successfully if fertilization of eggs is normal. A high ratio of females to males reduces the egg fertilization rate, while a low ratio of females increases fighting amongst the males, which effects the subsequent survival and recovery of females after laying.

About 3–5% of the broodstock pond area is established at the north or west side of the pond for turtle laying at night during the breeding season, which goes from May to late August. The laying site consists of about 30–40 cm of fine moist sand under a shed with a cover to protect the eggs from sunlight and rain. The laying site environment must be stable in water content, sand temperature and air movement, etc. In order to prevent water flooding the laying site it is set about 40–60 cm higher than the pond water level. It is connected by a slope so that turtles can crawl from the pond to the laying site (Figure 21.6) and return to the pond after laying their eggs. Some specific structures are needed near the laying site in order to prevent rodents, snakes and other wildlife from eating the turtle eggs.

Image described by caption.

Figure 21.6 A laying site for soft‐shelled turtles. It consists of a raised area of soil along the edge of the pond. There is a covering roof and ramps for the turtles to crawl up to the laying site.

Source: Reproduced with permission from Qingjun Shao.

Twelve to 14 hr after the female has laid, the eggs are collected and the fertilized eggs selected for hatching. The animal pole of a fertilized egg must be uppermost; otherwise the egg will not hatch.

21.5.2 Hatchery

There is natural and artificial incubation. Natural hatching outdoors in pond culture is only 10–40% successful because of unfavourable weather and predators, while hatching success under artificial conditions is normally >90%. During artificial incubation, the interior temperature is kept between 28–34°C, the relative humidity at 75–85% and the moisture content of the sand bed at 8–12%. Ventilation facilities are needed to supply sufficient oxygen to the eggs. Close attention is paid to orient the pale or white animal pole of fertilised eggs uppermost. Two kinds of sands may be chosen for incubation: river sand and soil sand. Clean river sand with grain size 0.5–1.0 mm is best for egg incubation.

The incubation procedure is to first cover the bottom of the hatching box with 5–6 cm of sand, and then the fertilised eggs are put into the sand with animal pole uppermost (Figure 21.7). Finally, the eggs are covered with 3–5 cm depth of sand (Figure 21.8). Several layers of eggs may be kept in a wood container.

Image described by caption.

Figure 21.7 Orderly rows of fertilised turtle eggs on a base of sand in a hatchery box.

Source: Reproduced with permission from Qingjun Shao.

Orderly rows of fertilised turtle eggs on a base of sand in a hatchery box.

Figure 21.8 Covering eggs with more sand.

Source: Reproduced with permission from Qingjun Shao.

The egg boxes are stacked and stored in a hatchery room (Figure 21.9) Incubation time depends on accumulated temperature, i.e., degree–hours. For example, if the average temperature during 24 July to 30 July is 28°C, the accumulated degree hours is 28 × 144 = 4032 degree–hours. Incubation takes about 36 000 degree–hours. The best temperature for incubation is 30–32°C, and it takes about 45 days to complete the incubation period, i.e., reach the approximate degree–hours. If sand temperature is a little higher than 32°C during the incubation period, the proportion of male turtle hatchlings will be more than females.

2 Rows of stacked hatchery boxes with turtle eggs and sand in a hatchery room with a half-naked man standing in the background.

Figure 21.9 Stacking egg boxes before use in a hatchery room.

Source: Reproduced with permission from Qingjun Shao.

21.5.3 Nursery

The newly‐emerged hatchling turtles absorb and utilize their remaining yolk, so they do not need any feed during the first two or three days. After that, they are fed on artificial feed or traditional feeds such as zooplanktonic copepods and aquatic worms (Limnodrilus hoffeiste) or liver, fish, shrimp and snails may be used. It takes 3 months for the body weight of hatchling turtles to increase from 4 to 50 g in the nursery pond. It is the most critical phase because of easy attacks by predators such as carnivorous fish, birds, frogs and snakes, and fighting each other. A little negligence of management will result in diseases and high mortality rates.

The turtles are fed twice a day, initially at 2% of body weight and gradually increasing to about 3%–5% when using artificial feeds. In practice, the amounts of feed are based on many factors, such as feed palatability, nutrient content, water quality, weather conditions, and turtle health. As they grow, there is size variation within batches. Turtles must be sorted and separated into similar‐sized groups in order to prevent them from fighting and harming smaller ones. Because of the high‐density and ready morbidity, it is very important to prevent disease outbreaks, especially from hatchling to juvenile stages.

21.5.4 Grow‐out

Soft‐shelled turtles are generally reared indoors up to 150 g body weight. When outdoor temperature reaches 25°C in mid May to early June, turtles are transferred from indoors to outdoors. In order to reduce the stress of water temperature change, the temperature difference between indoor and outdoor is kept to less than 3°C. By the end of October, turtles reach marketable size (>400 g). The optimum stocking density in earthen ponds is 2–4 turtles/m2. Turtles are fed twice a day, according to 2%–3% of body weight, at 07:00 and 17:00 hr. In the process, it is desirable to keep quiet and not disturb the turtles from feeding and basking in the sun during the daytime. Basking areas are set near the feed platform or a feed platform may also be used for basking in order to reduce the amount of activity. As in cultivating broodstock turtles, pharmaceuticals are used for disinfection in water and medicated feeds are administered according to the government regulations when turtles are infected.

21.6 Water Quality

21.6.1 Management

Water management in earthen ponds is as important for soft‐shelled turtles culture as it is for fish culture in earthen ponds. It is necessary to keep water transparency to about 25–35 cm in order to avoid turtles biting each other and to avoid fungi and parasite diseases. If the water contains too much plankton, however, there is need to stock with filter‐feeding fish, such as silver carp and bighead. Alternatively, 5–25% of the pond surface area may be stocked with water hyacinth or water cabbage or other water plants to absorb nutrients from the water pond (Wang et al., 2007). Meanwhile, quicklime at 20–30 g/m3 may be used every two weeks or some of the pond water exchanged with new water. After harvesting, the pond bottom mud is removed, and the pond bottom left to dry in the sun for 20–30 days so that bottom organic matter can be broken down and be disinfected. Fertilisers such as pig or poultry manure are used when filling a pond to promote plankton growth or these are used if the water has poor plankton content during the turtle farming period. Water transparency of the turtle pond decreases as the plankton grows. It is undesirable to have trees near earthen ponds, especially on the east and south sides, in order to maximise the sunlight on the ponds and thus promote plankton and warm water,

21.6.2 Water Parameters

DO, nitrogenous compounds, pH, hardness and other parameters of waters strongly influence the soft‐shelled turtle’s feeding and growth. Generally, DO is maintained at not less than 5–6 mg/L. Although soft‐shelled turtles mainly use their lungs to breathe, they have requirements of DO in the water for using pharyngeal villa respiration, especially during hibernation. High DO can also effectively prevent the anaerobic decomposition of organic matter in the water, reducing the levels of NH4+/NH3, NO2−, H2S, CH4 and other toxic compounds (Chapter 4). Intensive farming, with high‐density stocking and artificial feeding, results in considerable organic waste and low DO. So, the process of renewal of DO is blocked and toxic substances, such as those above, which cannot be converted into non‐toxic substances, result in ‘low‐dissolved oxygen syndrome’, thereby affecting the healthy growth of soft‐shelled turtle. Therefore, it is essential to maintain the DO of the culture water in the progress of soft‐shelled turtle breeding.

It is desirable to rear soft‐shelled turtles in neutral or slightly alkaline water, pH from 7.5–8.0, because alkaline water may inhibit the growth of bacteria. The culture water is treated with lime or bleaching powder (chlorine) every 15 days at a dose of about 2–3g/m3 in order to regulate the pH and kill pathogenic microorganisms and parasites.

Ammonia nitrogen (NH3‐N) is the main toxic substance in the water that causes turtles to be poisoned if excessively accumulated. Therefore, the content of ammonia nitrogen in water is tested regularly to keep it less than 0.02 mg/L. Other water parameters such as hardness and NO2− must also be regulated by water controlling methods.

21.7 Nutrition, Feeding and Feed Formulation

Feed costs are the largest component in the production of Chinese soft‐shelled turtles, accounting for 35–45% of the total cost. Efficient and economic feeds, together with effective feeding practices are essential. Nutrition is the most advanced field of soft‐shelled turtle culture and their general nutrient requirements have been established in recent years (Table 21.3). As for other animals in aquaculture, proteins, lipids, carbohydrates, vitamins, minerals, calcium and phosphorus, are necessary to meet the requirements for good growth and health of soft‐shelled turtles.

Table 21.3 Nutritional requirements of Chinese soft‐shelled turtles, Pelodiscus sinensis.

NutrientRequirementSource
Protein33%3, 42%*
43%−50%		Wang et al., 2014) (Zhou et al., 2013
Sun et al., 1997; Qian & Zhu, 2002
Lipid7%–8%Qian & Zhu, 2001; 2002
Carbohydrate18%–25%Sun et al., 1997

* Young juveniles.

21.7.1 Nutritional Requirements

Protein is the most expensive component in balanced fish feeds and often the most important factor affecting growth rate of cultured species, and thus there are studies about the optimal protein requirements of soft‐shelled turtles. Some researchers consider that the optimal protein levels for this species are at or exceed 43g/kg feed (e.g., He et al., 2002). This was found for post‐hatch juveniles of a Japanese strain of turtles, for which optimum protein was 42g/kg feed. However, the optimum protein level in feed was ca. 33g/kg feed for small juveniles (ca. 4.8g) (Wang et al., 2014). The specific growth rate (SGR) of these latter juveniles increased with protein content up to this level and did not increase at higher levels. Protein efficiency ratio (PER) increased with feed protein content up to 33g/kg and then declined at levels above this.

Basically, the protein requirements of Chinese soft‐shelled turtle reflect their requirements of essential and non‐essential amino acids. These amino acid requirements have been estimated through studying the amino acid content of muscle and ‘skirt’ (leathery edging of the carapace) tissue (He et al., 2002).

There is no systematic report on requirements for lipids such as EPA and DHA for soft‐shelled turtles.

Feed supplements have been tested and found to influence the growth and health of soft‐shelled turtles:

  • Vitamin C. There is a dietary requirement for ascorbic acid (vitamin C) (Vc) to obtain maximum growth of soft‐shelled turtles when cultured indoors in dark conditions, although soft‐shelled turtle can synthesize a small amount (Shao et al., 2004). Ascorbic acid is provided in feeds in the form of phosphorylated L‐ascorbic acid at 184–192 mg/kg feed.
  • Vitamin C. A level of 370–380 mg/kg feed gave optimal carapace collagen and strength (Wang & Huang, 2015).
  • Vitamin E. A level of 250–500 mg/kg feed significantly improved non‐specific immune response, i.e., blood cell phagocytosis and serum bactericidal activity (Zhou et al., 2005).
  • Iron. A level of ca. 280 mg/kg iron in feed, as ferric citrate, significantly improved growth rate, food conversion ratio (FCR) and protein efficiency ratio (PER) in juvenile turtles (Chu et al., 2007).

21.7.2 Feed Formulation and Manufacture

There were three stages in the development of feeds for soft‐shelled turtles:

  • The first was from the 1970s to the early 1990s. There was extensive culture and the main features of the feeding regime were directly feeding many ingredients including high levels of waste products, resulting in poor food conversion ratios (FCR).
  • The second stage from the early 1990s to the mid‐1990s was the formulated feed stage. It was characterized by using compound feeds, such as commercial eel feed, and gradually optimizing ingredients for soft‐shelled turtles.
  • The third stage of the industry is a relatively low‐protein, high‐quality stage, which is characterised by feed with reduced crude protein content and feed costs correspondingly lowered.

Feeds used in intensive pond culture of soft‐shelled turtles are formulated to provide almost all required nutrients in the proper proportions. Typical commercial feed formulations are shown in Table 21.4. The feed protein is mainly provided by expensive imported white fishmeal. The crude protein content of white fishmeal is about 65%, while that of brown fishmeal (from oily fish) is about 55%. If a proportion of white fishmeal could be replaced by a plant source of protein or microbe protein, the feed costs could be decreased to the advantage of the industry. The commonly‐used ingredients in commercial compound feeds are mainly white fishmeal, brown fishmeal, soybean meal, fermented bean meal, wheat gluten, corn protein meal, yeast, animal liver meal, α‐starch, wheat flour, corn or soybean oil, Ca(H2PO4)2, vitamins, and minerals.

Table 21.4 Typical commercial feed formulation for Chinese soft‐shelled turtles, Pelodiscus sinensis.

% ingredient
IngredientsHatchling
up to 50 g
body wt		Turtles
50 to 150 g
body wt		Turtles
>150 g
body wt
White fishmeal605248
Brown fishmeal–36
α‐starch222220
Wheat flour––2
Soybean meal–23
Fermented bean meal235
Animal liver meal532
Corn protein meal–23
Wheat gluten331
Yeast meal133
Ca(H2PO4)21.51.51.5
Mineral premix222
Vitamin premix222
Zeolite powder1.51.51.5
Total100100100

All the solid ingredients need to be ground into fine particles smaller than 200 μm, and then mixed well. Then every 100 kg of compound powdered feed needs the addition of about 2–4 kg plant oil or some fish oil to supply sufficient fatty acid requirements and energy. About 20% water is added and a machine is used to make semi‐moist feed pellets. The feed must be sufficiently viscous so that it is not easily spread by the turtle crawling around during its long period of feeding, which is about 30 minutes to 2 hours according to its body size. Fine particles are required so that the feed can be digested and absorbed easily by the turtles.

21.7.3 Feeding

During the nursery stage, the turtles are fed 3–5 times per day. This begins in the early morning (6 am) and ends at night (10 pm), especially in indoor culture. At body weight more than 150 g it is sufficient to feed the turtles twice a day, i.e., in the morning (7 am) and in the afternoon (5 pm), as is practiced in feeding some fish. Feeding must be under water during the nursery stage to encourage the juvenile turtles to feed and grow well. At body weight more than 100 g, the feed is placed on a slope above water level where the turtles emerge to feed. This reduces feed waste and, in ponds, avoids the possibility of wild fish taking the expensive turtle feeds.

The food intake per day of the turtles during the suitable culture season is about 2–3% of body weight with artificial particle feeds or 5–10% of body weight with fresh feeds. However, in ponds, the feeding rate needs to be adjusted according to weather condition, water temperature, water quality, turtle health, and other factors. In farming practice, this means that the feed needs to be enough for a feeding period of about 2 hours for nursery turtles and at least an hour for turtles with body weight of more than 150 g. Otherwise, there is insufficient feed. Alternatively, it is necessary to avoid overfeeding with feed loss and wastage, and potential loss of water quality.

Cleaning and using quicklime are very necessary to disinfect the feeding site after the turtles have finished feeding in order to reduce or prevent disease breakouts

21.8 Infectious Diseases2

Soft‐shelled turtles grow slowly and are seldom moribund in their natural environment. However, with the development of intensive culture and modified environmental conditions in culture, there has been a significant increase in diseases of soft‐shelled turtles. According to incomplete statistics, the overall disease incidence in farmed soft‐shelled turtles is 20–40%. The mortality rate may be 20–50% in some poorly‐managed farms. There are some common diseases, such as parotitis, white plastron (ventral portion of carapace) disease, haemorrhage, perforation disease, enlarged and red neck disease, skin ulcer disease, and fungus disease (dermatomycosis). One disease often results in many symptoms, and one symptom results from several diseases, so that it may be very difficult to diagnose and treat turtle diseases.

Controlling water quality is the most important way to avoid disease outbreaks.

21.8.1 Viruses

21.8.1.1 Parotitis (‘Mumps’)

Symptoms

Parotitis is evident in sick turtles that are generally drowsy and with a floppy neck so that the turtle’s head cannot draw back into its shell. Their parotid (salivary) glands, mouth, oesophagus, and intestines are abnormal. The liver is grey to brown colour and fragile. Infected turtles in the same pond will sometimes present two kinds of disease symptoms:

  • Parotid glands congested with blood and reddish; eroded, with secretions; mouth, oesophagus and intestines inflamed; plastron, limbs and tail are swollen with blood.
  • Parotid glands whitish and eroded, with secretions; oesophagus, stomach and intestine congested with necrotic tissue; plastron white without any blood colour.

There have been a number of studies on the prevention and control of parotitis, including Chen (1994) and Xu (2002).

21.8.2 Bacterial Diseases

21.8.2.1 White Plastron Disease (Haemorrhagic Intestinal Necrosis)

Pathogens: Aeromonas hydrophila, Edwardsiella tarda, Proteus vulgaris

Symptoms: The bodies of sick turtles are pale, showing a state of extreme anaemia and oedematous. The liver is grey and brown with little or no blood; the gallbladder is swollen; the kidneys and spleen are dark. The body musculature is pale and bloodless. Juvenile turtles (100–200 g) are susceptible, particularly from May to July when the water temperature is 25–30°C (Chen, 1994).

21.8.2.2 Putrid Skin Disease

Pathogens: Aeromonas hydrophila, Aeromonas sobria, Pseudomonas Species and other Bacteria

Symptoms: Surface erosion and ulceration are the main symptoms of this disease. Lesions can also occur on limbs, neck, carapace, skirts and tail. Initially, part of the skin is inflamed. Then there is necrosis followed by ulceration of the affected area, which gradually increases until muscles and bone are exposed. In severe cases, the neck bones are exposed, limbs rot away and claws fall off. This disease frequently occurs in high‐density indoor culture.

21.8.2.3 Furunculosis Disease

Pathogen: Aeromonas hydrophila punctata

Symptoms: In the early stage, small white bulges appear on the surface of the turtle’s skin. They gradually become more prominent, expanding and forming boils. In severe cases these become festering holes in the carapace concurrent with the skin disease. This disease infects both juvenile and adult turtles, and is most common from May to July, when the temperature is at 20–30°C.

21.8.2.4 Perforation Disease

Pathogens: Aeromonas hydrophila, Proteus vulgaris, Klebsiella pneumoniae, Alcaligenes Species

Symptoms: In the early stage, white sores of 2 to 10 mm diameter appear on the soft‐shelled turtle's dorsal shell, plastron and skirt. The sores develop scabs and bleed. The scabs soon fall off, with the original sore site left as a small hole with inflamed edge. There is bleeding from the interior of the hole in severe cases. This disease can infect all stages of soft‐shelled turtles but occurs especially in juvenile turtles and especially during indoor culture.

21.8.3 Fungal Diseases

21.8.3.1 White Speckle Disease

Pathogen: Mucor Species

Symptoms and damage: White spots appear on the carapace of soft‐shelled turtles in the early stages and are not easily detected. Then the white spots gradually increase and extend to other parts of the body, forming a white‐spotted necrotic epidermis, which peels. This disease is common from April to June and mainly affects juvenile turtles in the nursery phase (Chen, 1994).

21.8.4 Protozoan Parasites

There are several kinds of endoparasitic protozoa, such as Trypanosoma species, and species of Myxosporidia and Coccidia; while Vorticella is an ectoparasite.

21.8.4.1 Vorticella Disease

Pathogen: Vorticella Species

Symptoms and damage: This stalked ciliate infests the surface of turtles at very high densities. The limbs, carapace, plastron, skirts and neck of the sick turtles have white lesions. When the water is deep green, the vacuoles of the ciliate are densely green and the whole surfaces of the soft‐shelled turtles are green. The disease does not lead to the death of soft‐shelled turtles, but their feeding and growth rate decrease.

21.8.5 Metazoan Parasites

Leeches

Leeches are common ectoparasites of soft‐shelled turtles. They infest the turtles’ body surface, skirts and limbs, causing irritation, loss of appetite and body weight. This leads to malnutrition and, if serious, can cause death.

21.9 Harvesting and Processing

After soft‐shelled turtles reach the desired market size, they are harvested, transported to the processing plant and processed. These practices are relatively standardised across the industry.

21.9.1 Harvesting

Soft‐shelled turtles may be harvested year around, according to consumer demand. However, they tend not to be harvested during the rapid growth period from July to September. There are many methods for harvesting:

  • Hand capture or rake capture are effective when small numbers are requested. Collectors wearing protective pants, going downstream and using their feet in the sediment. When treading on a turtle, they capture the turtle using their hands.
  • Rake capture. Rakes made of wood cause less damage to the soft‐shelled turtles than metal ones. The rake handle length is about 1.5 m; the space between teeth is 10–20 cm. Rake teeth are inserted deep into mud. The soft‐shelled turtles are detected by contact with the rake’s teeth and then captured by hand. This method is used to capture adult turtles, broodstock turtles and turtles after hibernation.
  • Purse seine capture. The meshes of the purse seines are slightly larger than the meshes of fish nets. The seine net is set and taken in smoothly and rapidly because turtles will go into the sediment if there is some sound.

Drained‐pond capture. If large numbers or a whole pond of turtles are to be captured, the pond is drained and dried, and the turtles collected from around the pool during the day and by using lights at night

21.9.2 Processing and Cooking

There are hundreds of processing and cooking methods in Chinese cuisine.

The soft‐shelled turtle is killed by cutting the neck or opening the ventral shell. The turtle is cleaned by removing the viscera, and it is then ready for processing and cooking. The main processing and uses of soft‐shelled turtle include:

  • cooking to produce a great variety of dishes;
  • health food medicines;
  • health food medicines through processing with traditional Chinese medicines; and
  • mixing with other traditional Chinese medicines as a kind of medicine for treating some specific human diseases.

21.9.2.1 Cooked as Dishes

There are many ways of cooking soft‐shelled turtles, including boiling, frying, steaming, soaking (e.g., in rice wine) or making into soup, for a great variety of dishes. These may involve the whole or parts of the turtle cooked with other edible animal tissues, vegetables or edible plant seeds. Cooked soft‐shelled turtles may be vacuum packed for sale.

21.9.2.2 Medicines

Healthy Food Medicines

The soft‐shelled turtle is cooked with traditional Chinese medicines, plant seeds or tissues as medicinal food for sick or weak persons. It is a food to support body health and food for health recovery.

Soaking in Alcohol with Traditional Chinese Medicines

Slaughtered and cleaned soft‐shelled turtles or their organs are soaked in rice wine with traditional Chinese medicines for daily drinking to support the human body’s health.

An Ingredient of Medicines

Whole or parts of the soft‐shelled turtle are used as an ingredient of traditional Chinese medicines by powdering and specified processing. In addition, the turtle’s shell is traditionally used as a medicine for children and old people as a calcium supplement.

21.9.3 Marketing

Usually, soft‐shelled turtles are harvested and sold alive after they weigh 400 g. The main marketing methods are:

  • the turtles are sold alive by the farmer at the pond side or farm gate to middle‐men or restaurants. The middle‐men whole‐sale the turtles to local market dealers, who finally sell to the consumers.
  • the farmer takes the turtles to the local market which sells vegetable, meat and aquatic products, and there sells directly to the consumers (Figure 21.10).
  • a soft‐shelled turtle production company sells them through the company’s specialised shops in cities, with a marked brand and quality guarantee or specified years of culture, for a high price. Small quantities of soft‐shelled turtle are processed and packed, then sold in local markets or supermarkets, or exported to Japan, South Korea and other Southeast Asian countries. The turtles with brand names are sold at 3–5 times and even 10 times the price of turtles without brand names, even in China. These brand‐name turtles are of high quality with a culture period of 3–5 yr in earthen ponds or polycultured with fishes or aquatic plants. The turtle’s price at a city supermarket or at a brand‐name shop may be 300–400 CNY/kg or even higher, if it is polycultured with fish for 4–5 yr.
Image described by caption.

Figure 21.10 Soft‐shelled turtles, Pelodiscus sinensis, and toads for sale in a market, Xiamen City, Fujian Province, China.

Source: Reproduced with permission from Qi Lin.

Despite these high prices, the farm gate price of indoor cultured soft‐shelled turtles was only about 30–32 CNY/kg in Hangzhou in July 2009, since consumers considered that the quality of these soft‐shelled turtles was much poorer than those cultured in earthen ponds. The price of soft‐shelled turtles depends on many factors that affect turtle quality: period of culture, culture environment (e.g., pond or dark indoors), geographic origin, body weight, sex (males are more valuable), condition of health, and status of brand name.

In retail markets, dealers may help customers by slaughtering and cleaning the soft‐shelled turtle after weighing if the customer requests this.

21.9.4 Consumption

Most Chinese, Japanese, Korean and Southeast Asian people like to eat soft‐shelled turtles. They are often chosen as one of the dishes for special occasions such as traditional holidays, festivals, banquets, family gatherings, friends getting together, birthday parties, business meetings and weddings. This is because soft‐shelled turtles are tasty and considered to have high nutritional value for health. During the meal every participant will usually take one or two pieces of turtle meat with their chopsticks and they will also have some turtle soup. An example of a special dish of cooked Chinese soft‐shelled turtle is shown in Figure 21.11.

Image described by caption and surrounding text.

Figure 21.11 A Chinese dish of soft‐shelled turtle soup.

Source: E. Andrade 2006. Reproduced under the Creative Commons Attribution NoDerivatives license, CC‐BY‐ND 2.0.

21.10 The Future of Soft‐Shelled Turtle Farming

Based on Chinese traditional food culture, many people would like to consume soft‐shelled turtle if the quality is good and safe. There will be increasing consumption with increasing economic development in most parts of China. More soft‐shelled turtles will be produced through fish‐turtle polyculture or ecological culture methods in earthen ponds and in greenhouses with sunlight, since there are fewer disease breakouts with these methods compared to indoor dark culture. There are needs to improve survival rate during the nursery phase, reduce the period of the nursery phase and improve turtle meat quality. This is likely to be solved by two‐stage farming methods with an indoor temperature‐controlled nursery phase and then culture in outdoor ponds or in sunlit greenhouses. There are geographic strains of P. sinensis (e.g., Zhou et al., 2013) and there may be substantial genetic variation in a population (Que et al., 2007). New strains and hybrid strains will be bred extensively for production on a larger scale. Chemical treatments that are more effective and leave fewer residues must be developed for disease control during culture. Finally, it is most important to train the farmers in basic culture knowledge such as how to:

  • control water quality;
  • choose appropriate methods for disease prevention and control;
  • set up turtle farmers’ associations; and
  • improve the management of farming risks and other aspects of soft‐shelled turtle production.

21.11 Summary

  • Chinese soft‐shelled turtles, Pelodiscus sinensis, do not have the usual hard and fused shell plates of most turtles. They are cooked with the shell to produce many culinary dishes and used in a variety of medicines
  • Soft‐shelled turtles are voracious feeders and omnivorous. They are amphibious with lungs for aerial respiration and a pharyngeal organ with villi‐like gills for aquatic respiration. As reptiles, their body temperature, and hence metabolic rate and behaviour, vary with their immediate environment to the extent that behaviour ceases below 10°C. This results in slow growth and a longer period to sexual maturity in farms at high latitudes.
  • Reproduction follows a typical reptilian pattern. The male fertilises the female through copulation. Eggs are fertilised internally and then laid to hatch later. Eggs for culture are collected and placed in hatching boxes in sand. Incubation time then depends on degree–hours, i.e., 28° × 144 hr = 4032 degree–hours.
  • Farming methods consist mainly of indoor concrete tanks, outdoor earthen ponds or a combination of both where juveniles are reared indoors and transferred. The quality of turtles cultured indoors is lower than those from earthen ponds and antibiotics are used more frequently. However, indoor culture has the economic attractions of a shorter period to marketable size and lower costs. Pond culture is often polyculture with deliberate stocking of fish and aquatic plant species to improve the quality of turtles. These turtles are comparable in quality to wild turtles and thus valuable.
  • Farmed soft‐shelled turtles require high protein feeds and feeds are the largest cost in producing the turtles. The feeds account for 35–45% of the total cost. Considering this, there has been substantial research on turtle nutrition and their general requirements have been established in recent years.
  • Soft‐shelled turtles are seldom moribund in their natural environment. However, there is often significant disease in culture. Skin diseases are common and controlling water quality is particularly important for avoiding disease outbreaks.
  • There will be increasing demand for soft‐shelled turtles, dependent on quality. Consequently, it is important to set up farmers’ associations and training.

References

  1. Chen, P. F. (1994). Prevention trial of complication diseases of soft‐shelled turtles, ‘White Spot’, ‘piercing’, ‘mumps’. Freshwater Fisheries (Chinese), 24: 38–39.
  2. Chu, J‐H., Chen, S‐M. and Huang, C‐H. (2007). Effect of dietary iron concentrations on growth, hematological parameters, and lipid peroxidation of soft‐shelled turtles, Pelodiscus sinensis. Aquaculture, 269(1–4),532–537.
  3. He, R. G., Mao, X. Y., Wang, Y. L. et al. (2002). Study on the optimal levels of energy, crude protein and essential amino acid model of diets for growing turtle. Journal of Fisheries of China (Chinese), 24, 46–51.
  4. Ling, S. W. (1977). Aquaculture in Southeast Asia: A Historical Review. University of Washington Press, Seattle.
  5. Qian, G. Y. and Zhu, Q. H. (2001). The impact of different growth conditions on nutrients content of the Chinese soft‐shelled turtles. Journal of Nutrition (Chinese), 23, 181–183.
  6. Qian, G. Y. and Zhu, Q. H. (2002). The impact of feed types on nutrients content of soft‐shelled turtles. Journal of Fisheries (Chinese), 26, 133–138.
  7. Que, Y., Zhu, B., Rosenthal, H. et al. (2007). Isolation and characterization of microsatellites in Chinese soft‐shelled turtle, Pelodiscus sinensis. Molecular Ecology Resources, 7(6), 1265 – 1267.
  8. Shao, Q. J., Zhang, L. H., Liu, J. X. et al. (2004). Effect of dietary Vc supplementation on growth and tisssue Vc content in juvenile soft‐shelled turtle Trionyx sinensis. Acta Hydrobiologica Sinica, 28(3), 269–274.
  9. Sun, H. T., Xuan, Z. Q., Wang, Z. Z. et al. (1997). The requirement of fat‐sugar mixtured salts and amino acid of soft‐shelled turtles. Chinese Fisheries Society Aquatic Animal Nutrition and Feed Research Papers, 1, 241–249.
  10. Wang, C‐C. and Huang, C‐H. (2015). Effects of dietary vitamin C on growth, lipid oxidation, and carapace strength of soft‐shelled turtle, Pelodiscus sinensis. Aquaculture, 445, 1– 4.
  11. Wang, J., Qi, Z. and Yang, Z. (2014). Evaluation of the protein requirement of juvenile Chinese soft‐shelled turtle (Pelodiscus sinensis, Wiegmann) fed with practical diets. Aquaculture, 433, 252–255.
  12. Wang, M., Ma, J. J. and Shao, Q. J. (2007). The earth pond culture of soft‐shelled turtle Trionyx sinensis. Reservior Fisheries (Chinese), 27, 24–26.
  13. Xu, J. H. (2002). Effective control of turtles parotitis. China Fisheries, (9): 50–52.
  14. Zhou, F., Ding, X., Feng, H. et al. (2013). The dietary protein requirement of a new Japanese strain of juvenile Chinese soft shell turtle, Pelodiscus sinensis. Aquaculture, 74, 412–413.
  15. Zhou, X., Niu, C. and Sun, R. (2005). The effects of vitamin E on non‐specific immune response of the juvenile soft‐shelled turtle Pelodiscus sinensi. Fisheries Science, 71(3), 612–617.

Notes