Application of Wet Waste from Shrimp (Litopenaeus vannamei) with or Without Sea Mud to Feeding Sea Cucumber (Stichopus monotuberculatus)

CHEN Yanfeng, HU Chaoqun, and RENChunhua



Application of Wet Waste from Shrimp () with or Without Sea Mud to Feeding Sea Cucumber ()

CHEN Yanfeng1), 2), HU Chaoqun1), *, and RENChunhua1)

1),,,,510301,2),,528231,..

In the present study, the applicability of the wet waste collected from shrimp () to the culture of sea cucumber () was determined. The effects of dietary wet shrimp waste on the survival, specific growth rate (SGR), fecal production rate (FPR), ammonia- and nitrite-nitrogen productions of sea cucumber were studied. The total organic matter (TOM) level in the feces of sea cucumber was compared with that in corresponding feeds. Diet C (50% wet shrimp waste and 50% sea mud mash) made sea cucumber grow faster than other diets. Sea cucumber fed with either diet D (25% wet shrimp waste and 75% sea mud mash) or sole sea mud exhibited negative growth. The average lowest total FPR of sea cucumber occurred in diet A (wet shrimp waste), and there was no significant difference in total FPR between diet C and diet E (sea mud mash) (>0.05). The average ammonia-nitrogen production of sea cucumber in different diet treatments decreased gradually with the decrease of crude protein content in different diets. The average highest nitrite-nitrogen production occurred in diet E treatment, and there was no significant difference in nitrite-nitrogen production among diet A, diet B (75% wet shrimp waste and 25% sea mud mash) and diet C treatments (>0.05). In each diet treatment, the total organic matter (TOM) level in feces decreased to different extent compared with that in corresponding feeds.

sea cucumber;; shrimp;; wet waste; sea mud

1 Introduction

The tropical sea cucumber,,is a commercially valuablespecies which is mainly distributed in South China Sea,Malaysia, Grand Baie, Australia and Samoa (Fan, 2012; Massin, 2002; Rowe and Richmond, 2004; Byrne, 2010). At present, the research onis still art the initial stage, though the larval development and juvenile growth of this specieshave been reported (Hu, 2010; Fan, 2012). There have been few reports onexcept for some studies on phylogeny, molecular markers and genetic barcoding of this species (Byrne., 2010; Yuan., 2012; Uthicke., 2010). There is no doubt that the development of sea cucumber aquaculture industry needs knowledge of dietary requirements. However, nowadays there remains a paucity of information regarding the nutritional requirements ofand the artificial diets which may induce fast growth of thisspecies.

The white shrimp () is a globally important aquacultured species (Frias-Espericueta., 2001; McGraw, 2002; Saoud, 2003; Cheng., 2006). In recent years, although the production ofhas increased rapidly in many countries (Andriantahina, 2012), owing to reckless discharge of effluent containing high concentrations of nitrogen and phosphorus and waste slurry containing uneaten feed and feces into the sea without any effective treatment, shrimp aquaculture industry has led to serious coastal ecosystem pollution and seawater eutrophication. Adverse environmental impacts related to shrimp farming have been reported (Sansanayuth, 1996; Páez-Osuna, 1998; Páez-Osuna, 2001; Burford and Williams, 2001; Anh, 2010). Thus, reasonable treatment and reuse of effluent and waste slurry from shrimp aquaculture industry can be important countermeasures of reducing environmental impacts (Chin and Ong, 1994).

Many studies indicated that the uneaten feed and feces of marine animals were important food sources of sea cucumber (Hauksson, 1979; Tiensongrusmee and Pontjoprawiro, 1988; Ramofafia, 1997). From previous studies, one way of reducing the pollutive impacts of aquaculture industry was the polyculture because a deposit feeder such as sea cucumber below a farm was optimal for reprocessing and removing waste (Ahlgren, 1998; Kang, 2003; Zhou, 2006; Slater and Carton, 2007; Paltzat., 2008). Additionally, some other studies reported that farming wastes from shellfish aquaculture industry could be reused by sea cucumber (Yuan, 2006; Slater, 2009; Maxwell, 2009; Zamora and Jeffs, 2011). However, the polyculture of sea cucumber with shrimp seems immature and defective till now, which has caused some negative results such as slower growth of both species and worse water quality in polyculture compared with monoculture (Purcell, 2006). Moreover, Bell(2007) observed that limited growth and mass mortality of sea cucumber occurred when it was reared with shrimp, exhibiting polyculture was not viable. Therefore, collected shrimp waste is worthy of being estimated whether it can be a useful food source of sea cucumber. However, up to now, there has been no information regarding the applicability of collected wet shrimp waste to sea cucumber aquaculture industry. In contrast, as high quality food, sea mud has been widely used in sea cucumber aquaculture industry (Liu, 2009, 2010; Xia, 2012a, 2012b). Nevertheless, so far no studies have estimated the effect of a diet containing wet shrimp waste and sea mud on the growth of sea cucumber.

The aims of this study are to determine whether wet shrimp waste can be used for the culture of sea cucumber after it is collected, to assess the capability of the mixture containing wet shrimp waste with or without sea mud of inducing the growth of sea cucumber compared with the common industry feed of, and to search a new approach to reuse the waste produced by shrimp aquaculture industry.

2 Materials and Methods

2.1 Experimental Diets

Fresh wet waste containing feces and residual feed (wet shrimp waste in short) of shrimp () were collected with 0.074mm sieve from the sewage outfall of ninety indoor shrimp pools of different shrimp farms (Zhanjiang City, Guangdong, China). During the period of shrimp culture, shrimp was fed with only commercial feeds (Crude protein: 45.4%; Crude lipid: 9.3%; Ash: 10.6%. Guangdong Evergreen Feed Industry Co., Ltd.), and no fishery drugs were put into shrimp pools from which wet waste slurries were collected. After these wastes were mixed well, the seawater in the waste was squeezed out until its moisture content was 33%. Then 67% sea mud was mixed with 33% natural seawater, forming sea mud mashwith a 33% moisture content.

Powderedalga(Yantai XinHai Technology Co., Ltd., Shandong, China) was mixed with distilled water, forming a slurry (Slater, 2009).

The final diets used in this experiment were diet A, wet shrimp waste; diet B, 75% wet shrimp waste and 25% sea mud mash; diet C, 50% wet shrimp waste and 50% sea mud mash; diet D, 25% wet shrimp waste and 75% sea mud mash; diet E, sea mud mash; and diet F,(Table 1). Six kinds of diets were stored in sealed plastic bags at −13℃ separately.

Table 1 Nutrient content in feeds and feces

Notes: Diet F,(% dry weight): 7.34%±0.02% crude protein; 0.66%±0.01% crude lipid; 37.3%±0.04% ash; Data with different letters in the same column are significantly different (0.05).

2.2 Experiment Design and Rearing Conditions

Healthywas obtained through artificial propagation carried out in Zhanjiang Haimao Fisheries Biological Technology Co., Ltd. Guangdong, China. Sea cucumber was taken from ponds and then acclimatized in tanks (3×2×1m3). Sea cucumber was left without feeds for 48 h so that its gut content was evacuated entirely before use. One hundred and twenty sea cucumber individuals (2.02g±0.08g in wet body weight) were randomly selected and placed in 24 plastic containers (70L container, 60L water body), 5 each. The con-tainers were divided into 6 groups, 4 repeats each. Seawater was continuously aerated, and the mean water quality parameters were: temperature 26℃±2℃, salinity 30±2, and dissolved oxygen >5.0mgL−1. About 50% of seawater was changed every day with fresh natural seawater.

Six groups of sea cucumber were fed with six experimental diets, respectively, at about 18:30, once a day. The amount of wet mashed feeds supplied for each treatment per day was equivalent to 30% of the wet body weight of sea cucumber (Zamora and Jeffs, 2011), and uneaten feeds each container were observed every day. We found that this feeding quantity was adequate to sea cucumber in each container. Feces were collected by siphoning twice a day at about 6:00 and 18:00, desalted gently with distilled water and stored at −13℃ until analysis. The feces produced by sea cucumber in each container were pooled together, while the feces produced day and night were collected separately. Container was washed every 5d. This experiment lasted 60d. At the end of experiment, sea cucumber was starved for 48h and weighed in order to determine specific growth rate.

2.3 Chemical Analysis of Feed and Feces

The experimental diets were sampled during preparation and stored at −13℃. These diets and feces were freeze-dried for 24h with their nutrient contents (crude protein, crude lipid and carbohydrate) analyzed according to AOAC (1990).

The total organic matter (TOM) content of feed and feces was determined with a variation of the combustion method described by Byers(1978). After the samples were oven baked at 60℃ for 48h, they were weighed and placed in a furnace at 500℃ for 6h to ensure that organic matter was burnt completely, and then they were re-weighed. Percentage of TOM was calculated by sample weight lost after combustion.

2.4 Survival, Growth and Fecal Production

All deaths were recorded during experiment. Specific growth rate (SGR) and fecal production rate (FPR) were calculated with the method of Zamora and Jeffs (2012):

, and

,

where1and2are initial and final wet body weight of sea cucumbers in each container,is the duration of the experiment (60d),is the number of sea cucumbers in each container, andis the dry weight of feces.

2.5 Ammonia- and Nitrite-Nitrogen Productions

At the middle of experiment, ammonia- and nitrite-ni- trogen concentrations were determined for a whole day. Different diets were placed for all sea cucumbers each container after exchanging water. The concentrations of ammonia- and nitrite-nitrogens each container were analyzed at that time and they were analyzed again 24h later. Ammonia-nitrogen was determined using the salicylate- hypochlorite method (Bower and Holm-Hansen, 1980) while nitrite-nitrogen was determined using the method of Shinn (1941). One container without sea cucumber was used as control. Ammonia- and nitrite-nitrogen productions were calculated using the following equations which were revised by Xia(2012a):

,

2.6 Variation of TOM Content in Feces

The variation of TOM content in feces and that in corresponding feeds were analyzed with the method described by Zamora and Jeffs (2011).

2.7 Statistical Analysis

Statistics was performed using software SPSS 10.0 for Windows with the difference of TOM content between feeds and feces in a diet being tested by independent- samplestest. Inter-treatment differences of SGR, FPR and ammonia- and nitrite-nitrogen productions were tested with one-way ANOVA. Duncan’s multiple range test was used to test the difference among treatments. Differences were considered to be significant if<0.05.

3 Results

3.1 Survival, Growth and Fecal Production

In this study, the average highest SGR of sea cucumber occurred in diet C (0.5102) while the average lowest SGR occurred in diet E (−1.2033). The SGR in diet C (0.5102) was significantly higher than that in diet F (0.3729) while the SGR in diet A (0.1871) was significantly lower than that in diet F (0.3729). The difference in SGR was significant between diets except for that between diet A and B, diet B and F, and diet D and E. Diet C made sea cucumber grow faster than others while diet D and E attenuated the growth of sea cucumber (Fig.1). During experiment, no mortality occurred. However, the slight deformation in epidermis was found in a few individuals.

Fig.1 Specific growth rate (SGR) of sea cucumber. Different letters indicate significant difference among diets, and bars represent standard error.

The difference in night FPR was significant among diets, and the average highest night FPR occurred in diet C (0.031) while the average lowest night FPR occurred in diet A (0.0026). The difference in day FPR was also significant among diets except foe those among diet C, D and E, and the average highest day FPR occurred in diet E (0.0112) while the average lowest day FPR occurred in diet A (0.0008). Besides, the difference in FPR of all diets between day and night was significant (Fig.2).

Fig.2 Night and dayfecal production rate (FPR) of sea cucumber. Different small letters indicate significant difference in night FPR among diets, different capital letters indicate significant difference in day FPR among diets; * indicates significant difference between night and day FPR of a diet; bars represent standard error.

The difference in total FPR was significant among diets except for that between diet C and E. The average highest total FPR occurred in diet C (0.0389) while the average lowest total FPR occurred in diet A (0.0034) (Fig.3).

3.2 Ammonia- and Nitrite-Nitrogen Productions

The difference in ammonia-nitrogen production was significant among diets except for those among diet C, D and E. The average highest ammonia-nitrogen production occurred in diet A (3.0388) while the average lowest ammonia-nitrogen production occurred in diet E (0.6325). The average ammonia-nitrogen production of sea cucumber decreased gradually when the protein content of diets decreased (Fig.4).

The difference in nitrite-nitrogen production was significant among diets except for those among diet A, B and C. The average highest nitrite-nitrogen production occurred in diet E (1.9525) while the average lowest nitrite-nitrogen production occurred in diet C (0.6463) (Fig.5).

Fig.5 Nitrite-nitrogen production of sea cucumber. Different letters indicate significant difference among diets; bars represent standard error.

3.3 Variations of TOM Content in Feces

In this study, the TOM content in feces decreased gradually when the TOM content in feeds decreased. The TOM content in the feces of sea cucumber fed with different diets decreased to different extent in comparison with that in corresponding feeds. With the decrease of TOM content in feeds, the difference of the TOM content between feces and corresponding feeds increased at first and then decreased gradually (Table 1).

4 Discussion

4.1 Mixture of Wet Shrimp Waste and Sea Mud Mash Induced the Growth of Sea Cucumber

Zhu(2005) reported that the optimum dietary protein and lipid requirements of juvenile sea cucumber were about 18%–24% and 5%, respectively. Interestingly, in this study, although all the lipid levels of different diets were lower than 5%, and the protein level of diet A (23.19%) was within this range while that of diet C (12.05%) was lower than this range, sea cucumber grew slower when it was fed with the former than when it was fed with the latter. In general, in aquaculture industry, a binary compound diet is thought to provide a better balance of nutrients for aquatic animals than a single component diet (Coutteau, 1996; Southgate, 2003). Many studies have confirmed that sea cucumber fed with compound diets often exhibit higher survival and growth rates compared with those fed with single component diets (James, 1994; Ramofafia, 1995; Battaglene, 1999; Asha and Muthiah, 2006). Sea mud could provide certain nutrients or digestion regulators to sea cucumber, which included beneficial algae, decaying organic matter and mineral components which were vital to the metabolism of sea cucumber (Liu, 2009; Gong, 2012), avoiding the lack of nutritions in wet shrimp waste. Besides, some components (., beneficial bacteria, predigestion by shrimps, vitamins,) in wet shrimp waste also benefit for the growth of sea cucumber (Yuan, 2006; Slater, 2009). Maybe the fastest growth of sea cucumber in diet C was due to the combination of these factors.

4.2 Comparison of the Effects of Wet Shrimp Waste,and Sea Mud on the Growth of Sea Cucumber

The results of this study showed that sea cucumber grew slower when it was fed with pure wet shrimp waste than when it was fed with. This finding was not in agreement with that of Slater(2009) who found that pure fresh mussel waste which was superior towas an effective artificial diet for juvenile sea cucumber (). This indicated that pure fresh shrimp waste was inferior tothe common industry feed ofwhen it was used to rearing juvenile sea cucumber

In general, the growth of animals was affected by different diets through the interaction of ingestion rate, food conversion ratio and digestion and assimilation efficiency (Yuan, 2006). Ziemann(1992) reported that wet waste slurry from shrimp farms contained elevated concentrations of dissolved nutrients, bacteria and other suspended organic and inorganic solids. After such a mixture entered seawater in container, they scattered immediately because of the aerator, making it impossible to collect uneaten feeds.Therefore, in this study, the ingestion rate, food conversion ratio and assimilation efficiency of sea cucumber could not be determined, making it difficult to make a comparison of these parameters of sea cucumber between wet shrimp waste andtreatments. However, at least one thing was for sure, bad water quality could limit the growth of aquatic animals. A restriction in weight gain of sea cucumber resulted from the increase of ammonia concentration was observed when it was reared with shrimp (Purcell, 2006). Thus, the highest ammonia production in wet shrimp waste treatment appeared to be the only variable to explain the slow growth of sea cucumber in this diet treatment (Fig.4). In contrast, as high quality food,has been widely used in sea cucumber aquaculture industry (Slater, 2009; Liu, 2010; Xia, 2012a, 2012b). Moreover, up to now, the growth restriction of sea cucumber due to bad water quality resulted fromhas not been documented. Although the nutritional level of(protein 7.34%, lipid 0.66%) was lower than that of dietary nutritional requirement of juvenile sea cucumber, it was possible that sea cucumber might compensate such a gap by increasing the amount of food intake (Xia, 2012b).

In this study, a diet of sole sea mud led to the negative growth of sea cucumber. Maybe the nutritional level (protein 0.87%, lipid 0.32%) in sea mud used in this experiment was so low that it was far from for the daily nutritional requirement of sea cucumber. Although sea cucumber might ingest much sea mud as was reflected by relatively high fecal production rate, the nutrient was not enough for the growth of sea cucumber.

4.3 Potentiality of Reducing Organic Pollution from Shrimp Waste by Sea Cucumber

It was reported that sea cucumber could utilize organic matter from waste produced by shellfish and convert it into body tissues (Slater and Carton, 2009; Zamora and Jeffs, 2011, 2012). At the end of this experiment, although the total body weight of sea cucumber in some diet treatments increased and those in others decreased, no death was observed, which suggesting that part of nutrient in feeds was used to maintain the growth of sea cucumber. Thus, the nutrient content in excrement might be lower than that in feed. This was a probable explanation for the decrease of the TOM level in the feces of sea cucumber compared with that in corresponding feeds. This study confirmed that sea cucumber could still reduce the organic content of shrimp waste after it was collected, which was in accordance with the result of Purcell(2006) who found that the organic matter content of sediments of polycultured shrimp and sea cucumber was lower than that in monocultured shrimp. Similar result was also reported by Zhou(2006) who found that the organic matter content in the waste of scallop decreased when it was reared with sea cucumber () inlantern net. This indicated that sea cucumber has the potential of reducing organic pollution of shrimp waste.

4.4 Applicability of Wet Shrimp Waste to Sea Cucumber Culture

On the one hand, excessive ammonia and nitrite in aquaculture water body canbe fatally harmful to aquatic animals. In this study, the high survival rate of sea cucumber in wet shrimp waste treatment indicated that the amount of ammonium and nitrite excretion did not damage them. This suggested that ammonia- and nitrite-ni- trogen productions in this diet treatment were within a safe range. Besides, after sea cucumber was fed with pure wet shrimp waste, its final total body weight increased compared with its initial total body weight. On the other hand, sea cucumber in diet C treatment grew faster than those in wet shrimp waste andtreatments. The ammonia- and nitrite-nitrogen excretion summations of sea cucumber in diet C treatment were lower than those in wet shrimp waste treatment. Thus, when wet shrimp waste became a component of sea cucumber feeds, these feeds had less potential of being harmful to sea cucumber than pure wet shrimp waste. The above results indicated wet shrimp waste could be used for the culture of sea cucumber.

5 Conclusions

This study confirmed that collected wet shrimp waste could be used in sea cucumber aquaculture industry. Although pure wet shrimp waste led to slower growth of sea cucumber than common industry feed of, the mixture containing 50% wet shrimp waste and 50% sea mud was superior to. Moreover, the use of wet shrimp waste by sea cucumber can reduce the pollution of waste from shrimp aquaculture industry.

Acknowledgements

This research was supported by the Key Projects in the National Science & Technology Pillar Program during the 12th Five-year Plan Period (2011BAD13B02, 2012BAD 18B03), the Science & Technology Promoting Projects for Oceanic & Fishery in Guangdong Province (A2011 00D01, A201101D02), and Cooperation Program of Guangdong Province & Chinese Academy of Sciences (2012B091100272).

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(Edited by Qiu Yantao)

DOI 10.1007/s11802-015-2348-z

ISSN 1672-5182, 2015 14 (1): 114-120

© Ocean University of China, Science Press and Spring-Verlag Berlin Heidelberg 2015

(March 28, 2013; revised May 1, 2013; accepted July 10, 2014)

* Corresponding author. Tel: 0086-20-89023216 E-mail: hucq@scsio.ac.cn