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干大型植物作为海胆养殖替代饲料的评价

时间:2021-08-21 来源:未知 编辑:梦想论文 阅读:
Abstract
The aim of this work was to assess the potential use of different dried macroalgae as food in the rearing of Paracentrotus lividus. Growth, consumption and food conversions were compared in adult sea urchins fed with fresh or dried thalli of four macroalgae species. Six experimental diets were tested: (a) fresh Palmaria palmata; (b) freshSaccharina latissima; (c) dry P. palmata; (d) dry S. latissima; (e) dry Laminaria digitata and (f) dry Grateloupia turuturu. Linear growth rates were similar for all treatments. Specific growth rate was higher in sea urchins fed with fresh P. palmata, but no difference was found between animals fed with fresh S. latissima and those fed with dried diets. Regarding daily food consumption (DFC), sea urchins consumed the same amount of dried macroalgae as fresh but exhibited a higher food conversion efficiency (FCE) when fed with fresh P. palmata. However, this FCE was only significantly higher when compared to sea urchins fed with dry L. digitata. Dried G. turuturu is not a suitable diet due to its rapid degradation after rehydration. The results suggest that P. lividus adults can be reared on dried macroalgae thalli without detriment to their somatic growth, especially over short periods. The low cost of feeding sea urchins with this diet could help small shellfish farmers to diversify their production into echinoculture.
 
 
1 INTRODUCTION
Sea urchin roe is highly regarded as a premium food: 100,000 metric tons of sea urchins are annually fished worldwide with a value of over 0.5 billion euros (FAO, 2016). As a result of its high demand and market value (Kelly, 2004), zootechnics of several species of sea urchins have been successfully developed worldwide (Chow, Macchiavello, Cruz, Fonck, & Olivares, 2001; Cook & Kelly, 2009; Liu et al., 2007). Its industry is still in its infancy, producing about 6,000 tons per year in China, Japan, Russia and Ireland (FAO, 2016). In Europe, Paracentrotus lividus (Lamarck, 1816) is the most commonly consumed sea urchin (Kelly, 2004) with a long fishing tradition (Le Gall, 1987). France is the largest consumer of sea urchins in Europe with around 1,000 tons per year (Andrew et al., 2002) and the major importer of sea urchins with around 200 tons in 2015 (FAO, 2016). In fact, since the collapse of the French P. lividus fisheries, demand has been satisfied by increased Irish and Spanish imports (Fernandez & Pergent, 1998). However, P. lividus aquaculture remains a small industry in Europe probably because farming methods are not economically sustainable for shellfish producers. The rearing of this species has two main limiting factors: low growth rate and difficulty in supplying quality and diversified seafood. Paracentrotus lividus is described as a macroalgivore (Lawrence, 2013) which prefers different species of macrophytes depending on its habitat, from Ireland to southern Morocco and throughout the Mediterranean Sea (Bayed, Quiniou, Benrha, & Guillou, 2005; Byrne, 1990; Sánchez?España, Martínez?Pita, & García, 2004). Consequently, production of this species necessitates regular harvesting of fresh macroalgae and their conservation in facilities, which have a relatively high cost, as with other grazers (e.g. abalone; Huchette & Clavier,2004). Moreover, fresh macrophytes that could be used in echinoculture are not always available to farmers due to its seasonality (Fleurence, 1999; Lüning, 1993; Schiener, Black, Stanley, & Green, 2015) and conservation difficulties in summer due to rapid degradation. Although P. lividus can adapt to artificial diets (Fernandez & Pergent, 1998), this alternative is still being developed and usually involves unaffordable high production costs.
 
In order to promote shellfish aquaculture diversification in the northwest French coast with echinoculture, finding alternative sources of food is needed. Dried macroalgae are usually used as attractants in artificial diets (Dworjanyn, Pirozzi, & Liu, 2007; Naidoo, Maneveldt, Ruck, & Bolton, 2006), considering the dietary preference of the reared species for fresh algae (Vadas, 1977; Vadas, Beal, Dowling, & Fegley, 2000). With the aim of reducing costs (economically viable for small enterprises), we carried out sea urchin feeding with dried macroalgae thalli. The objective was to compare growth parameters in P. lividus when this species is fed with the following local fresh or dry macroalgae species: Palmaria palmata,Saccharina latissima, Laminaria digitata and Grateloupia turuturu.
 
2 MATERIALS AND METHODS
2.1 Sea urchins
 
The sea urchins were reared in the Benth'Ostrea Prod aquaculture farm (Bouin, Vendée, France). They were obtained following fertilization carried out in April 2015 from a broodstock harvested in April 2013 in Port Manec'h (47°48′04.0″N 3°44′44.5″W, Brittany, France). Spawning of four females and three males (33.86 ± 13.99 g/whole animal) was chemically induced by injection of KCl solution. Fertilization was carried out in an egg/sperm ratio of 1:4. The larval culture methods were adapted from Kelly, Hunter, Scholfield, and McKenzie (2000). From the experiment's outset, sea urchins were fed ad libitum on the red alga P. palmata and reared in the dark in a closed land?based system with a daily seawater exchange rate of 100% (5 µm filtered seawater at 20°C). The individuals selected were 11 ± 0.25 mm (mean ± SD) in diameter (excluding spines) and one and a half years old at the beginning of the experiment. Individuals were starved for 2 weeks prior the experiment to standardize their nutritional condition.
 
2.2 Macrophyte diets
 
Sea urchins were fed with four species of macroalgae in two different conditions (fresh and dry). Six different feeding treatments were studied: (a) fresh P. palmata (diet FP; also considered as a control diet due to the preference of P. lividus for this species); (b) fresh S. latissima (diet FS); (c) dry P. palmata (diet DP); (d) dry S. latissima (diet DS); (e) dry L. digitata(diet DL) and (f) dry G. turuturu (diet DG). These species are some of the dominant macrophytes in the intertidal zone of the study area. Macroalgae were collected in a sustainable manner by a professional picker every two weeks at low tide from the intertidal zone in Le Croisic (47°16′57.5″N 2°31′25.1″W, Pays de la Loire, France). To control macroalgae harvesting, the ‘Region Pays de la Loire’ allocates only 20 licenses per year.
 
Collected algae were rinsed with filtered seawater, cleaned of epibionts and debris and stored in the dark at 8–10°C in filtered, oxygenated seawater at 37 × 103 mg/L of salinity until their use. Drying was carried out in a greenhouse over 24–48 hr at a temperature range of 25–30°C.
 
2.3 Experimental design
 
The experiment was conducted in the dark, in a recirculating aquaculture system (Figure 1) composed of two identical 150 L tanks equipped with a biofilter, over a period of 8 weeks (between October and December 2016). Seawater was aerated and maintained at 20°C, pH 8 and 37 × 103 mg/L of salinity. A 50% water exchange was carried out weekly.


 
image
Figure 1
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Experimental design. Dotted lines represent control sieves devoid of sea urchins. Red arrows indicate the direction of the sieves rotation. DG, dry Grateloupia turuturu; DL, dryLaminaria digitata; DP, dry Palmaria palmata; DS, dry Saccharina latissima; FP, fresh Palmaria palmata; FS, fresh Saccharina latissima
In order to test the six feeding treatments in triplicate, sea urchins were placed in 18 PVC sieves of 30 cm depth, 20 cm diameter and 2 mm nylon?mesh pore. Twenty sea urchins were randomly distributed in each sieve. Three sieves were then assigned to each feeding treatment. For each diet type, a control sieve, devoid of sea urchins was placed in the tanks to correct for any variation of the macroalgal biomass due to degradation. All sieves were randomly distributed in the tanks and their position rotated every day to avoid possible biases due to their location in the water mass. Total biomass per litre in the tanks was 0.65–0.69 g/L.
 
Feeding, removal of remaining macroalgae and biometrics of sea urchins (i.e. diameter and wet weight; WW) were performed weekly. The sea urchins were fed ad libitum with the same amounts of macroalgae (WW). Fresh macroalgae were drained of excess water, wet weighed and supplied to the corresponding batches. Dried macroalgae were first rehydrated in seawater for 1 hr, drained, wet weighed and distributed. A sample of the same WW as the feeding ration was collected for each treatment and immediately frozen at −20°C, as well as the remaining macroalgae in all treatments and in the control. Macroalgal biomass (given, remaining and control) were all estimated by their dry weight (DW) after freeze?drying in order to avoid biases associated to macroalgal water content variation.
 
2.4 Ingestion and absorption rates
 
Daily food consumption rates (DFC) and food conversion efficiencies (FCE) were calculated according to the formulas modified from Cook and Kelly (2007), Jacquin et al. (2006) and McCarron, Burnell, and Mouzakitis (2009):
 
urn:x-wiley:1355557X:media:are14045:are14045-math-0001
where Fg was the DW (g) of a given macroalgae, Fr was the DW (g) of the remaining macroalgae and Fd was the DW of the macroalgae lost by degradation. W was the WW (g) of the sea urchin and t was the time in days.
urn:x-wiley:1355557X:media:are14045:are14045-math-0002
where Wt was the whole sea urchin WW (g) at time t and Wi was the initial whole sea urchin WW (g).
 
 
During the experiment, a high degradation of G. turuturu was observed, so its DFC and FCE could not be evaluated.
 
2.5 Biometric parameters
 
Sea urchin diameter of each batch was determined every week by image analysis using Imagej software (Schindelin et al., 2012). The widest axis of the sea urchins test (no spines) was measured. Animal batch WW was carried out following 5 min of drying on absorbent paper.
 
Linear growth rate (LGR) and specific growth rate (SGR) were calculated according to the formulas (Cook & Kelly, 2007; Demetropoulos & Langdon, 2004; García?Bueno et al., 2016):
 
urn:x-wiley:1355557X:media:are14045:are14045-math-0003
where LGR was the sea urchin growth in test diameter, Lt the test diameter (mm) at time t, Li the initial test diameter (mm) and t the time in days.
 
where Wt was the whole sea urchin WW (g) at time t, Wi the initial whole sea urchin WW (g) and t the time in days.
 
 
2.6 Biochemical analyses
 
To characterize diet composition, samples of each fresh and rehydrated macroalgae were frozen at −20°C, freeze?dried, pooled by treatment and ground to a fine powder under liquid nitrogen. Aqueous crude extracts (CE) were obtained by homogenization of 1 g of powder in 20 ml of a phosphate buffer solution (20 mmol/L; pH 7) and centrifugation (25,000 g, 20 min, 4°C). Total water?soluble proteins in CE were analysed following the bicinchoninic acid (BCA) assay (Smith et al., 1985) and quantified as bovine serum albumin (BSA). Total water?soluble carbohydrates in CE were analysed according to the method of Dubois, Gilles, Hamilton, Rebers, and Smith (1956).
 
For total lipid analysis, 1 g of powder was rehydrated in 4 ml of ultrapure water. Lipids were then extracted with a mixture of dichloromethane/methanol (1:1 v/v) in a proportion sample/solvent of 1:5 (v/v) and measured gravimetrically as described by Bligh and Dyer (1959).
 
2.7 Statistics
 
Statistical analyses were performed using the SigmaPlot® 9.0 software. Biometrics and growth parameters were compared using one?way ANOVA analysis. When normality or equal variance tests failed, a Kruskal–Wallis one?way analysis of variance on ranks was performed. A posteriori multiple comparison Tukey tests were conducted between diets when significant differences (p < 0.05) were found.
 
For each diet, linear regressions were established between sea urchins weight and diameter. Slope and intercept comparisons were carried out between diets.
 
3 RESULTS
3.1 Sea urchin growth
 
No mortality was observed in any of the diet treatments. Individual diameters and total biomass were similar at day 0 in all batches (Figures 2 and 3). The same pattern was observed for both parameters. Significant differences among treatments were observed only after 5 weeks. Only the FP diet showed a significantly higher (p < 0.001) response compared to the other diets. There was no significant difference between the response of animals fed with FS diet and those fed with dry diets. However, final biomasses of sea urchins fed with dry diets showed a tendency to be lower than those of animals fed with FS diet (Figure 3).
 
Figure 2
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Mean diameter of sea urchin Paracentrotus lividus fed with six different fresh or dry macroalgae diets. DL: dry Laminaria digitata (green, empty circle); DG: dry Grateloupia turuturu (blue, cross); DP: dry Palmaria palmata (black, diamond); DS: dry Saccharina latissima (yellow, square); FP: fresh Palmaria palmata (grey, full circle); FS: fresh Saccharina latissima (orange, triangle). Error bars represent CIs (95%). Symbols indicate significant differences: ***p < 0.001
Figure 3
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Mean biomass of sea urchin Paracentrotus lividus batches fed with six different fresh or dry macroalgae diets. DG: dry Grateloupia turuturu; DL: dry Laminaria digitata; DP: dryPalmaria palmata; DS: dry Saccharina latissima; FP: fresh Palmaria palmata; FS: freshSaccharina latissima. Error bars represent CIs (95%). Symbols indicate significant differences: ***p < 0.001
Somatic growth observed in all treatments showed a highly significant relationship (p < 0.001) between biomass and diameter (Figure 4; Table 1). Comparison of slopes showed significantly (p < 0.05) higher growth in sea urchins fed with fresh versus dry diets throughout the experiment.
 
Figure 4
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Sea urchin Paracentrotus lividus biomass/diameter relationship depending on the type of experimental diet. DG: dry Grateloupia turuturu; DL: dry Laminaria digitata; DP: dry Palmaria palmata; DS: dry Saccharina latissima; FP: fresh Palmaria palmata; FS: fresh Saccharina latissima
Table 1. Equations describing relationships between weight and diameter of sea urchinsParacentrotus lividus fed different experimental diets
  Equation R 2 F P
FP diet y = 0.21x − 1.78 0.9911 671 <0.001
FS diet y = 0.23x − 2.01 0.9874 472 <0.001
DP diet y = 0.19x − 1.50 0.9873 470 <0.001
DS diet y  = 0.19x − 1.47 0.9962 1615 <0.001
DL diet y  = 0.19x − 1.51 0.9918 729 <0.001
DG diet y  = 0.17x − 1.29 0.9892 550 <0.001
Note
 
Abbreviations: DG, dry Grateloupia turuturu; DL, dry Laminaria digitata; DP, dry Palmaria palmata; DS, dry Saccharina latissima; FP, fresh Palmaria palmata; FS, fresh Saccharina latissima.
 
Mean LGR was similar in all the studied treatments (Figure 5a). Significant differences were observed in mean SGR (p < 0.05): FP diet showed a significantly higher value than DS, DL and DG diets, while FS diet showed differences only in comparison to DG diet (Figure 5b).


 
image
Figure 5
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Mean of linear growth rate (a), specific growth rate (b), daily food consumption (c) and food conversion efficiency (d) of sea urchin Paracentrotus lividus fed with different diets throughout the experiment. DG: dry G. turuturu; DL: dry Laminaria digitata; DP: dryPalmaria palmata; DS: dry Saccharina latissima; FP: fresh Palmaria palmata; FS: freshSaccharina latissima. Error bars represent CIs (95%). Symbols indicate significant differences: *p < 0.05
3.2 DFC and FCE
 
Daily food consumption showed a high variability throughout the experiment within and among treatments (Figure 6). Although not statistically supported, values tended to be higher in the first 3 weeks.
 
Figure 6
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Daily food consumption of sea urchin Paracentrotus lividus fed with six different experimental diets throughout the experiment. DL: dry Laminaria digitata; DP: dry Palmaria palmata; DS: dry Saccharina latissima; FP: fresh Palmaria palmata; FS: fresh Saccharina latissima. Error bars represent CIs (95%)
No significant difference was found between sea urchins mean DFC in all treatments (Figure5c). For mean FCE, a significant difference was observed only between FP and DL diets (Figure 5d; p < 0.05).
 
3.3 Biochemical composition of diets
 
The same pattern was observed for water?soluble protein and carbohydrate contents: very low contents in dry diets and values for FS diet higher compared to FP (Table 2). Regarding dried diets, DP and DG had double protein content compared to DS and DL. Carbohydrate content was twice as high in DG and three times less in DL compared to DP and DS diets.


 
Table 2. Biochemical composition (% DW) of the six experimental diets for sea urchins
 
Note
 
Abbreviations: DG, dry Grateloupia turuturu; DL, dry Laminaria digitata; DP, dry Palmaria palmata; DS, dry Saccharina latissima; DW, dry weight; FP, fresh Palmaria palmata; FS, fresh Saccharina latissima.
 
Fresh P. palmata and DP diets presented similar lipid contents and were half that of FS, DL and DG diets.
 
4 DISCUSSION
This study is the first to test dried macroalgae thalli in sea urchin nutrition. Few studies on the use of dried macroalgae to feed abalones (Naidoo et al., 2006) or to constitute formulated diets for fishes (Valente et al., 2006) and sea urchins (Dworjanyn et al., 2007; Jong?Westman, March, & Carefoot, 1995) have been performed.
 
Higher values observed for consumption in the first 3 weeks may be attributed to the 2 weeks starvation period prior to the experiment, indicating the ability to consume more food when it became available (Bandolon, 2014; Cook & Kelly, 2007). Along the duration of the experiment, consumption was, on average, similar in all treatments despite clear differences in the protein and carbohydrate contents between fresh and dried thalli due to rehydration of the latter. This is contradictory with previous works which showed that consumption was negatively correlated to the protein content (Cook & Kelly, 2007; Fernandez & Boudouresque, 2000; Frantzis & Grémare, 1992). As the lipid content was similar for all the diets, we hypothesize that this is also a factor regulating consumption. Moreover, despite the loss of water?soluble compounds in dried diets, higher growth was observed for all the experimental diets compared to previous studies, namely mean LGR from 5 to 12 µm/day and mean SGR from 0.1% to 0.2% per day in Cook and Kelly (2007), mean LGR from 53 to 71 µm/day in Fernandez and Pergent (1998), maximum SGR = 1.3% per day in Frantzis and Grémare (1992) and mean SGR = 0.38% per day in McCarron et al. (2009). In Cook and Kelly (2007), the difference could be explained by their use of older and larger animals, according to allometry relationships. In the other studies, using animals of comparable size to ours, the use of lower nutritional value diets could be responsible for their lower growth rates. This indicates the great potential of natural diets composed of P. palmata, S. latissima, L. digitata and G. turuturu compared to artificial feed (Fernandez & Pergent, 1998) and other macrophytes (Frantzis & Grémare, 1992; McCarron et al., 2009).
 
Fresh macrophytes, specifically P. palmata, allowed the best growth performance, as illustrated by the biometric and SGR assessment. Their biochemical composition was in accordance with that previously published (García?Bueno, 2015; Harnedy & FitzGerald,2013; Jard et al., 2013; Schiener et al., 2015) and are known to best fit P. lividus nutritional requirements (Lawrence, 2013; Vadas et al., 2000).
 
Sea urchins fed with dried diets presented similar diameters and biomass to those fed with fresh S. latissima. They also showed a mean LGR similar to sea urchins fed with fresh P. palmata. Conversion efficiencies were the same in both dried (except for L. digitata) and fresh diets. These results suggest that all the experimental diets could be used without detriment to somatic growth. They also indicate that their lipid content remained high enough after rehydration to promote growth.
 
Concerning G. turuturu, García?Bueno et al. (2016) highlighted the difficulties, due to a rapid degradation, in using fresh G. turuturu thalli in abalone aquaculture and concluded that it might be more appropriate to use dry or powder form. In the present study, we could not evaluate the use of dried G. turuturu due to high degradation, making its sampling and analysis impossible. However, it would be interesting, given its availability, to valorize this invasive algae (Gavio & Fredericq, 2002) in the aquaculture industry. Its use as an ingredient for artificial feeds has not yet been investigated.
 
5 CONCLUSION
We confirmed the suitability of P. palmata and fresh diets for P. lividus nutrition, but without denying the great growth performances of sea urchins when these diets are replaced with dried macroalgae. These diets could therefore be used by farmers without detriment to production, especially during short periods when, for example, the algal biomass is less abundant.
 
Further investigations could be done on the effect of these diets on the sea urchin gonad enhancement and quality. However, for a fattening phase of the production cycle, the lower cost of feeding with natural dried algae compared to the cost of formulated diets could facilitate diversification of activities into echinoculture for small companies.
 
ACKNOWLEDGMENTS
This research was supported by the TAPAS project ‘Tools for Assessment and Planning of Aquaculture Sustainability’ funded by the EU H2020 Research and Innovation Program under Grant Agreement No 678396. The authors wish to thank Benth'Ostrea Prod for providing the living resources. They are also grateful to J. Dumay and M. Morançais for their assistance during biochemical analysis. Many thanks to Maygrett Maher for correcting the English of this paper. The authors declare that they have no conflict of interest.
 
DATA AVAILABILITY STATEMENT
Data sharing is not applicable to this article as no new data were created or analysed in this study.
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