Abstract
An 8-week feeding trial was conducted to evaluate the effect of dietary macro-algae in diet of juvenile Pacific white shrimp, Litopenaeus vannamei. The five macro-algae ingredients, including Saccharina japonica, Porphyra dioica, Gracilariopsis lemaneiformis, Ulva lactuca, and Undaria pinnatifida, were used for test diets, named SJD, PDD, GLD, ULD, and UPD, respectively. A reference diet (RD) and five test diets (30% test ingredients and 70% RD) were formulated. Each diet was randomly assigned to triplicate groups of 40 shrimp (initial body weight, 2.00 ± 0.01 g) and the shrimp were hand fed four times a day to apparent satiation. During the last 2 weeks, the fecal samples were collected by siphoning. The results showed that among five test diets, shrimp fed the SJD had the highest weight gain and the lowest feed coefficient, shrimp fed the SJD and GLD shared the same survival ratio and were significantly higher than shrimp fed the PDD and UPD (p < 0.05). For the composition of whole body, shrimp fed the SJD had the highest protein and lipid content compared with the shrimp fed other test diets. Apparent dry matter digestibility from high to low was: P. dioica, S. japonica, G. lemaneiformis, U. lactuca, and U. pinnatifida. Apparent protein digestibility of five macro-algae was highest in U. pinnatifida and lowest in G. lemaneiformis. Additionally, the highest apparent digestibility of gross energy was found in P. dioica. Apparent digestibility of total phosphorous in five ingredients was generally low and highest in S. japonica which was significantly higher than other ingredients (p < 0.05). These results indicated that S. japonica is more suitable for feed ingredient than other four kinds of macro-algae.
Similar content being viewed by others
Explore related subjects
Discover the latest articles, news and stories from top researchers in related subjects.Avoid common mistakes on your manuscript.
Introduction
The yield of Pacific white shrimp, Litopenaeus vannamei, is highest among all the cultured shrimp species in the world. Rapid growth and high survival rate make it a good choice for intensive aquaculture (Williams et al. 1996; Ponce-Palafox et al. 1997). Especially in recent years, the unprecedented development of shrimp farming has demonstrated its increasing vital role in fishery economy.
To promote sustainable aquaculture development, the search for fish meal substitutes and alternative dietary protein sources has been an international research priority that could be of considerable economic advantage (Lee 2002). Many studies have been conducted to replace fish meal with plant-derived protein sources such as soybean meal, corn gluten meal, cottonseed meal, and so on (Kikuchi 1999; Albrektsen et al. 2006; Fordeskjaervik et al. 2006; Amaya et al. 2007; Hernandez et al. 2007; Lim and Lee 2009). These studies concluded that minimizing the use of fish meal in aquaculture diets is essential for the sustainability of the aquaculture industry (Naylor et al. 2009).
Marine algae, an important marine biological resource, contain an abundance of nutrition and a variety of bioactive compounds, not only rich in carbohydrates, proteins, lipids, vitamins, and fibers (Pulz and Gross 2004; Silva and Barbosa 2009), but also contain all essential amino acids in various concentrations (Galland-Irmouli et al. 1999; Macartain et al. 2007) and all essential minerals (Cabrita et al. 2016). A small amount of algae supplementation in aquafeeds has been shown to improve immune systems (Turner et al. 2002, Schleder et al. 2017), increase lipid metabolism (Nakagawa 1997; Güroy et al. 2011), virus and bacyerial resistance (Boonsri et al. 2017), improve gut function (Michiels et al. 2012), and enhance stress resistance (Nath et al. 2012; Sheikhzadeh et al. 2012). Algae resource is extremely rich in China; there are more than 1000 different types of macro-algae and over 100 kinds are considered to have economic value. Therefore, used as a new feed ingredient, macro-algae have great potential. At present, several species of marine algae have already been used for partial replacement as complementary protein source in the diet of L. vannamei, such as Hypnea cervicornis J. Agardh and Cryptonemia crenulata (J. Agardh) J. Agardh (Silva and Barbosa 2009), Ulva clathrata (Roth) C. Agardh (Cruz-Suárez et al. 2009a, b), Gracilaria parvispora I.A. Abbott, and Ulva lactuca Linnaeus (Rodríguez-González et al. 2014). Cruz-Suárez et al. 2009a, b, 2010) and Peña-Rodríguez et al. (2011) had found that inclusion of U. clathrata in the diet of L. vannamei improves growth, food conversion ratio, and pigmentation and modifies fatty acid and sterol content in muscle. Schleder et al. (2017) concluded that Undaria pinnatifida enhances shrimp immunity and specifically inhibit Vibrio spp., while Sargassum filipendula increases shrimp resistance to thermal variation. Pallaoro et al. (2016) demonstrated that substitution of up to 50% of Ulva lactuca in commercial feed for L. vannamei does not interfere with the growth performance of shrimp.
In addition to quantify the gross composition of feed ingredients, knowledge of their digestibility is needed in order to assess the nutritional value (Shields and Lupatsch 2012). Apparent digestibility coefficients (ADC) reflect the percentage of a feed ingredient sample that is absorbed by an animal’s intestinal tract (Lin et al. 2005). In the past decades, although many studies have been carried out on the application of macro-algae as a potential ingredient in the diets of L. vannamei (Briggs and Funge-Smith 1996; Gamboadelgado et al. 2007; Ju et al. 2009, 2012; Basri et al. 2015), basic research data on the apparent digestibility of macro-algae ingredients for L. vannamei is still insufficient. The accurate determinations of chemical composition of macro-algal ingredients and the precise assessment of digestibility and absorption of nutrients are the basis for developing macro-algae as feed ingredients and feed additives. Therefore, detailed research on the apparent digestibility of macro-algae for L. vannamei is particularly important.
The objective of the present study was to evaluate the potential of five macro-algae as feed ingredients in formulated diets for juvenile Pacific white shrimp, L. vannamei.
Materials and methods
Five test ingredients
The five test ingredients were Saccharina japonica, Porphyra dioica, Gracilariopsis lemaneiformis, Ulva lactuca, and Undaria pinnatifida, all of which were bought from specialized stores.
Diet preparation
The reference and test diets were formulated according to Table 1. Five test diets were prepared using the method of “nested algorithm” (Cho and Kaushik 1990) by incorporation of 30% test ingredients into the reference diet (RD). Yttrium oxide (Y2O3) was used as an external indicator and was incorporated into the RD as well as test diets. Nutrient and amino acids composition of feed ingredients are shown in Tables 2 and 3. Nutrient and amino acids composition of the RD and test diets are presented in Tables 4 and 5. All dry ingredients were finely ground and sieved with a 60-mm mesh, then weighed precisely and mixed thoroughly with the oils and distilled water. The 1.2-mm diameter pellets were cold-extruded using a pelletizer (Institute of Chemical Engineering, South China University of Technology, Guangdong, China) and heated in an electric oven at 90 °C for 60 min, then air-dried to approximately 10% moisture, sealed, and stored at − 20 °C until fed.
Feeding trial
This experiment was carried out in an indoor flow-through system of the Guangdong Evergreen Group (Zhanjiang, China), and juvenile shrimp were obtained from a commercial hatchery. Prior to the experiment, the shrimp were stocked in a 1000-L fiberglass tank for 2 weeks to acclimate to the internal culture environment and fed with a commercial diet (44% crude protein, 8% crude lipid, Guangdong Evergreen Group, China). At the beginning of the experiment, 20 shrimp were randomly sampled and stored frozen (− 20 °C) until analysis of the initial proximate composition. A total of 720 uniform-sized shrimp (the mean weight, 2 g) in good health and condition were selected and distributed randomly into 18 500-L cylindrical fiberglass tanks, at a density of 40 shrimp per tank. Each diet was randomly assigned to triplicate tanks. All shrimp were hand fed four times daily at 7:00, 12:00, 17:00, and 21:00 for 8 weeks. The shrimp were initially fed at 8% of biomass, and the feeding rate was adjusted weekly in a range of 6–10% based on biomass by using an estimated growth rate established in the laboratory. The uneaten feed, feces, and molts were removed by siphoning immediately from tanks every day.
During the experimental period, filtered seawater (salinity, 29–30 g L−1) was constantly supplied to each tank at a flow rate of 1.0 L min−1. Water temperature, pH, dissolved oxygen, and ammonia nitrogen ranged from 27 to 30 °C, 8.0–8.4, 5–6, and 0.02–0.05 mg L−1, respectively. Natural light-dark cycle was used during the trial (5 August to 30 September).
Sample collection
During the last 2 weeks of experiment, fresh fecal samples with integrated envelope were siphoned and collected from each tank into separate bottles 1 h after feeding, then partially dried, overnight, in a convection oven at 90 °C. Dried samples were stored at − 20 °C until analyzed. At the end of the whole feeding trial, shrimp in each tank were weighed and sampled 24 h after the last feeding. Six shrimp were selected randomly from each tank for the analysis of the proximate composition of the whole body.
Chemical analysis
Moisture, crude protein, crude lipid, and ash content in the diets were determined following the methods described by AOAC (1995). Moisture was determined by oven-drying at 105 °C for 24 h. Crude protein content (N × 6.25) was determined by the Kjeldahl method after acid digestion using an Auto Kjeldahl System (1030-Auto-analyzer, Tecator, Sweden). Crude lipid content was determined by the ether-extraction method using a Soxtec System HT (Soxtec System HT6, Tecator, Sweden). And ash content was determined using a muffle furnace at 550 °C for 24 h. Gross energy was determined using an adiabatic bomb calorimeter (HR-15A Adiabatic Bomb Calorimeter, Changsha, China).
Amino acid composition of ingredients and feces were determined using an automatic amino acid analyzer (Hitachi, Model 835-50, Hitachi, Japan) with the column (Hitachi custom ion exchange resin no.2619). Samples were hydrolyzed in 6 N HCl at 110 °C for 22 h, then were separated by the ion exchange column and reaction with ninhydrin solution, and the amino acid concentrations were obtained by spectrophotometry. Yttrium oxide content of diets and feces were determined by ICP atomic emission spectrophotometry [ICP; model: IRIS Advantage (HR), Thermo Jarrel Ash Corporation, U.S.A] at the Centralized Analytical Laboratory at Sun Yat-sen University, China.
Calculations and statistical analysis
Percent weight gain (WG), feed coefficient (FC), and survival ratio (SR) were calculated as follows:
where the W 2 is final weight (g) of shrimp and W 1 is initial weight (g).
Apparent digestibility coefficients (ADC) for dry matter, protein, amino acid, energy and phosphorus of each diet were calculated using the following equations:
where the concentrations of nutrients (N) and Y2O3 (Y) are in % dry matter.
The results are presented as means±standard deviation. All data were statistically analyzed by SPSS 20.0 (SPSS, USA). The data were first tested for homogeneity. If the data had similar variances, then one-way analysis of variance (ANOVA) was used to made statistical comparisons. When there were significant differences (p < 0.05) among groups, multiple comparisons among means were made with LSD and Duncan’s new multiple-range test (Duncan 1955).
Results
Growth performance
Growth performance of juvenile L. vannamei fed with the reference and test diets are shown in Table 6. Shrimp fed the reference diet had the highest WG and lowest FC compared with five test diets. Among the five macro-algae diets, shrimp fed the SJD and GLD shared the same SR (97.5%) and were significantly higher than shrimp fed the PDD and UPD (p < 0.05), the lowest SR (86.67%) was observed in shrimp fed the PDD. For the WG, shrimp fed the SJD (178.35%) was significantly higher than other test diets (p < 0.05), and the lowest WG (128.87%) was found in shrimp fed the PDD. FC of five test diets ranged from 1.73 to 2.68, and lowest in shrimp fed the SJD, followed by UPD, ULD, GLD, and PDD.
Body composition
Body composition of juvenile L. vannamei fed with the reference and test diets is shown in Table 7. The protein and lipid contents of shrimp fed the reference diet were significantly higher than the five test diets (p < 0.05). The moisture and ash content of shrimp fed the reference diet were significantly lower than the five test diets (p < 0.05). Among the five macro-algae diets, shrimp fed the SJD had the highest protein and lipid content. The lowest protein content was observed in shrimp fed the PDD and the lowest lipid content was found in shrimp fed the ULD. Comparing the shrimp fed five test diets, shrimp fed the PDD had the highest ash content while shrimp fed the GLD had the lowest ash content, the moisture content of shrimp ranged from 78.70% (ULD) to 80.58% (UPD).
Apparent digestibility of five test ingredients
Apparent digestibility coefficients (ADC) for dry matter, crude protein, energy, and phosphorus of feed ingredients for L. vannamei are given in Table 8. Apparent dry matter digestibility (ADMD) of five test ingredients ranged from 35.3 to 60.4%; P. dioica had the highest ADMD and U. pinnatifida had the lowest ADMD. Apparent protein digestibility (APD) of ingredients ranged from 44.9 to 60.5%, and the highest and lowest APD were observed for U. pinnatifida and U. lactuca, respectively. Apparent energy digestibility ranged from 31.3% (S. japonica) to 68.2% (P. dioica). The total phosphorus apparent digestibility of five test ingredients is highest in S. japonica (29.5%) and lowest in P. dioica (9.1%).
Amino acid profiles of five feed ingredients
Amino acid analyses of five feed ingredients are presented in Table 3. For nine essential amino acids, the highest concentration was observed in P. dioica and lowest in S. japonica. In addition, high concentrations of valine and leucine were found in P. dioica and U. lactuca. The five macro-algae ingredients all have low concentrations of methionine and histidine. For eight non-essential amino acids, aspartic and glutamic acids constitute together a large part of the amino acid fraction of the five ingredients.
Apparent digestibility of amino acids
Apparent digestibility coefficients (ADC) of amino acids of feed ingredients for L. vannamei are given in Table 9. The ADC of total amino acids, S. japonica and P. dioica were significantly higher than the other three macro-algae (p < 0.05). The highest ADC of amino acids was found in S. japonica (73.5%) and the lowest ADC of amino acids was observed in U. lactuca (50.0%). For the ADC of individual amino acids, there were significant differences (p < 0.05) among the five macro-algae. The highest ADC of essential amino acids was found in U. pinnatifida and S. japonica had the lowest ADC of lysine and methionine, two limiting amino acids. Additionally, the ADCs were very different among various amino acids within the same ingredient.
Discussion
Saccharina japonica is more suitable as a feed ingredient than the other four macro-algae. Additionally, some follow-up experiments need to be done to explore further the optimal addition of macro-algae in feeds, and formulate a reasonable feed formula to develop new cost-efficient compound feed used for shrimp.
The present results on growth performance indicated that shrimp fed the reference diet had the highest WG and were significantly higher than shrimp fed the five macro-algae diets. The better performance of shrimp fed the reference diet was partly due to the higher protein content. It is well known that the growth performance and survival of the shrimp reflects the quality of the dietary ingredients, particularly the protein source (Sudaryono et al. 1995). In contrast, increasing macro-algae meal in the test diets could increase the fiber content, lower the feed digestibility, and thus affect the growth performance of the shrimp. Briggs and Funge-Smith (1996) also observed a significant reduction in growth of P. monodon fed diets containing 30% red seaweed Gracilaria spp. Negative effects could be attributed to the high ash content, low dietary protein content, or the high levels of soluble fiber present in the test diets caused by high algae inclusion levels. Among the five test diets, shrimp fed the SJD had the highest WG and the lowest FC, which indicated that the nutrients in S. japonica can be better utilized by L. vannamei than those of the other four macro-algae.
Whole-body proximate composition of shrimp was significantly affected by the macro-algae inclusion. In the present study, the inclusion of macro-algae in the diet resulted in lower protein content and higher ash content in shrimp compared to the control group, which caused low feed digestibility and poor growth performance.
So far, research on the apparent digestibility of algae ingredient for aquatic animals are limited. Xu et al. (2011) added 33% dried Gracilaria lemaneiformis (DGL) as an ingredient instead of 10% fish meal and 24% starch in diets for teleost fish Siganus canaliculatus, and the results showed that although the growth performance and feed utilization efficiency of fish fed the DGL-diet were inferior to fish fed the control diet, there were no significant differences in the ADC of dry matter, protein between DGL-diet and control diet. This suggested that G. lemaneiformis can partly replace fish meal and starch in diets for the teleost fish, S. canaliculatus. In the present study, the ADCs of nutrients for five test macro-algae were generally low and this may be related to the high fiber contents in the macro-algae.
ADMD provides a measure of the total quantity of an ingredient that is digested and absorbed. Because all components of an ingredient are not digested equally, apparent dry matter digestibility coefficients can provide a better estimate of the quantity of indigestible material presented in feed ingredients than digestibility coefficients for individual nutrients, which, in some cases, are minimally affected by indigestible material in the diet (Brunson et al. 2015). In the present study, shrimp fed the PDD had the highest ADMD, and shrimp fed the UPD had the lowest ADMD. The relatively higher ADMD of P. dioica could be explained by the more digestible starch compounds in the ingredient which could be better utilized by the animals. By contrast, the relatively lower ADMD of U. pinnatifida maybe attributed to high content of polysaccharides and ash which are difficultly digested by L. vannamei as shown in other studies (Sullivan and Reigh 1995; Stone et al. 2000; Lee 2002; Zhou et al. 2004). Appler (2010) found that the carbohydrate content of algae is usually over 40%, of which contains most non-peptic or non-nutritional carbohydrate with complicated structure that may result in poor palatability. Therefore, apparent dry matter digestibility of algae for animals is generally low.
Generally, the protein quality of dietary ingredients is a leading factor affecting aquaculture performance and APD is the effective evaluation index of availability of protein in feedstuff utilized by aquatic animals. In the present study, the highest APD was observed in shrimp fed the UPD and the lowest APD was observed in shrimp fed the ULD. The higher APD of UPD may be due to its well-balanced amino acid profile (Andrews and Page 1974), while the lower APD of ULD was probably due to poor protein quality in U. lactuca. In addition, lower protein digestibility of in high-lipid ingredients might be related to the formation of protein- and oxidized-fat complexes during drying (Ufodike and Matty 1983; Anderson et al. 1995).
Energy digestibility (ED) of ingredients tends to be inversely related to their fiber content (Hilton and Hodson 1983; Kirchgessner et al. 1986). In this study, The ED of shrimp fed the PDD was significantly higher than other test groups, indicating that the energy of P. dioica was better utilized by L. vannamei than the other four macro-algae.
Phosphorus is not only an important constituent of nucleic acids and cell membranes, but also an essential mineral nutrient for growth (Baeverfjord et al. 1998), skeletal development (Åsgård and Shearer 2015), and reproduction of aquatic animals (Hardy and Shearer 2011). However, as a critical pollutant in the aquatic environment, excessive excretion of phosphorus into water can stimulate the growth of algae and phytoplankton, thus reducing dissolved oxygen and causing water pollution (Miller et al. 1974; Sugiura et al. 1999). In the present study, shrimp fed the SJD had the highest ADC of phosphorus and shrimp fed the PDD had the lowest. This result indicated that phosphorus in S. japonica can be better used by L. vannamei than the other four macro-algae ingredients, and S. japonica as feed ingredient could more effectively protect the aquaculture water from pollution.
In general, macro-algae are considered as high nutritional value food, but most of them contain a low proportion of essential amino acids, especially lysine, a limiting factor in feedstuff (Brown et al. 1997). According to Fox et al. (1995), diets deficient in lysine, methionine, and arginine limited the growth of juvenile L. vannamei. In this study, shrimp fed the SJD diet had the best growth performance despite the lowest contents of these three amino acids in S. japonica and SJD. By contrast, P. dioica and PDD had the highest contents of these three limiting amino acids, but the shrimp had the worst growth performance. This result was in disagreement with the findings of Fox et al. (1995) and this could be partially a consequence of the higher fiber content in P. dioica and PDD.
The apparent amino acid digestibility of feed ingredient depends on not only its content, but also on the physical and chemical properties of the ingredient itself, the structural properties of amino acid itself, and other factors (Terrazas-Fierro et al. 2010; Oujifard et al. 2012). In the present study, shrimp fed the SJD had the highest ADC of total amino acid, whereas shrimp fed the ULD had the lowest. However, the ADCs were significantly different among various amino acids within the same ingredient. Therefore, the availability of amino acid cannot be estimated directly from the ADC of crude protein, as also reported by Masumoto et al. (1996), Lupatsch et al. (1997), Wilson et al. (1981), and Silva et al. (2000). By contrast, other studies have observed that the amino acid availability tended to reflect protein digestibility—an ingredient with high protein digestibility usually has high amino acid digestibility (Mu et al. 2000; Zhou et al. 2004; Yang et al. 2009).
Above all, as a new compound feed ingredient used for aquatic animals, macro-algae have enormous value. The high level of carbohydrates in macro-algae can reduce the amount of supplemental starch in formulated diets and minimize competition with human food sources. Furthermore, application of macro-algae in formulated diets can promote the coordinated development of aquaculture. However, due to the presence of a large amount of anti-nutritional factors (such as non-starch polysaccharides) in algae that may affect the palatability of diets, the digestibility of feeds and growth performance for aquatic animals will decrease when the addition of algae in feeds is too high. Therefore, appropriate additives that are highly palatable and digestible to animals are recommended to be added in formulated diets.
References
Albrektsen S, Mundheim H, Aksnes A (2006) Growth, feed efficiency, digestibility and nutrient distribution in Atlantic cod (Gadus morhua) fed two different fish meal qualities at three dietary levels of vegetable protein sources. Aquaculture 261:626–640
Amaya EA, Davis DA, Rouse DB (2007) Replacement of fish meal in practical diets for the Pacific white shrimp (Litopenaeus vannamei) reared under pond conditions. Aquaculture 262:393–401
Anderson JS, Lall SP, Anderson DM, Mcniven MA (1995) Availability of amino acids from various fish meals fed to Atlantic salmon (Salmo solar). Aquaculture 138:291–301
Andrews JW, Page JW (1974) Growth factors in the fish meal component of catfish diets. J Nutr 104:1091–1096
AOAC (1995) Official methods of analysis of the Association of Analytical Chemists Arlington. J Assoc Off Anal Chem Method 954:02
Appler HN (2010) Evaluation of Hydrodictyon reticulatum as protein source in feeds for Oreochromis (Tilapia) niloticus and Tilapia zillii. J Fish Biol 27:327–334
Åsgård T, Shearer KD (2015) Dietary phosphorus requirement of juvenile Atlantic salmon, Salmo salar L. Aquac Nutr 3:17–23
Baeverfjord G, Asgard T, Shearer KD (1998) Development and detection of phosphorus deficiency in Atlantic salmon, Salmo salar L. parr and post-smolts. Aquac Nutr 4:1–11
Basri NA, Shaleh SRM, Matanjun P, Noor NM, Shapawi R (2015) The potential of microalgae meal as an ingredient in the diets of early juvenile Pacific white shrimp, Litopenaeus vannamei. J Appl Phycol 27:857–863
Boonsri N, Rudtanatip T, Withyachumnarnkul B, Wongprasert K (2017) Protein extract from red seaweed Gracilaria fisheri prevents acute hepatopancreatic necrosis disease (AHPND) infection in shrimp. J Appl Phycol 29:1597–1608
Briggs MRP, Funge-Smith SJ (1996) The potential use of Gracilaria sp. meal in diets for juvenile Penaeus monodon Fabricius. Aquac Res 27:345–354
Brown MR, Jeffrey SW, Volkman JK, Dunstan GA (1997) Nutritional properties of microalgae for mariculture. Aquaculture 151:315–331
Brunson JF, Romaire RP, Reigh RC (2015) Apparent digestibility of selected ingredients in diets for white shrimp Penaeus setiferus L. Aquac Nutr 3:9–16
Cabrita ARJ, Maia MRG, Oliveira HM, Sousa-Pinto I, Almeida AA, Pinto E, Fonseca AJM (2016) Tracing seaweeds as mineral sources for farm-animals. J Appl Phycol 28:3135–3150
Cho CY, Kaushik SJ (1990) Nutritional energetics in fish: energy and protein utilization in rainbow trout (Salmo gairdneri). World Rev Nutr Diet 61:132–172
Cruz-Suárez LE, Tapia-Salazar M, Villarreal-Cavazos D, Beltran-Rocha J, Nieto-López MG, Lemme A, Ricque-Marie D (2009a) Apparent dry matter, energy, protein and amino acid digestibility of four soybean ingredients in white shrimp Litopenaeus vannamei juveniles. Aquaculture 292:87–94
Cruz-Suárez LE, Tapia-Salazar M, Nieto-López MG, Guajardo-Barbosa C, Ricque-Marie D (2009b) Comparison of Ulva clathrata and the kelps Macrocystis pyrifera and Ascophyllum nodosum as ingredients in shrimp feeds. Aquac Nutr 15:421–430
Cruz-Suárez LE, León A, Peña-Rodríguez A, Rodríguez-Peña G, Moll B, Ricque-Marie D (2010) Shrimp/Ulva co-culture: a sustainable alternative to diminish the need for artificial feed and improve shrimp quality. Aquaculture 301:64–68
Duncan DB (1955) Multiple range and multiple f tests. Biometrics 11:1–42
Fordeskjaervik O, Refstie S, Aslaksen MA, Skrede A (2006) Digestibility of diets containing different soybean meals in Atlantic cod (Gadus morhua); comparison of collection methods and mapping of digestibility in different sections of the gastrointestinal tract. Aquaculture 261:241–258
Fox JM, Lawrence AL, Li-Chan E (1995) Dietary requirement for lysine by juvenile Penaeus vannamei using intact and free amino acid sources. Aquaculture 131:279–290
Galland-Irmouli AV, Fleurence J, Lamghari R, Luçon M, Rouxel C, Barbaroux O (1999) Nutritional value of proteins from edible seaweed Palmaria palmata (Dulse). J Nutr Biochem 10:353–359
Gamboadelgado J, Peñarodríguez A, Ricquemarie D, Cruzsuárez LE (2007) Assessment of nutrient allocation and metabolic turnover rate in pacific white shrimp Litopenaeus vannamei co-fed live macroalgae Ulva clathrata and inert feed: dual stable isotope analysis. J Shellfish Res 30:969–978
Güroy D, Güroy B, Merrifield DL, Ergün S, Tekinay AA, Yiğit M (2011) Effect of dietary Ulva and Spirulina on weight loss and body composition of rainbow trout, Oncorhynchus mykiss (Walbaum), during a starvation period. J Anim Physiol Anim Nutr 95:320–327
Hardy RW, Shearer KD (2011) Effect of dietary calcium phosphate and zinc supplementation on whole. Can J Fish Aquat Sci 42:181–184
Hernandez MD, Martinez FJ, Jover M, Garcia GB (2007) Effects of partial replacement of fish meal by soybean meal in sharpsnout seabream (Diplodus puntazzo) diet. Aquaculture 263:159–167
Hilton JW, Hodson PV (1983) Effect of increased dietary carbohydrate on selenium metabolism and toxicity in rainbow trout (Salmo gairdneri). J Nutr 113:1241–1248
Ju ZY, Forster IP, Dominy WG (2009) Effects of supplementing two species of marine algae or their fractions to a formulated diet on growth, survival and composition of shrimp (Litopenaeus vannamei). Aquaculture 292:237–243
Ju ZY, Deng DF, Dominy W (2012) A defatted microalgae (Haematococcus pluvialis) meal as a protein ingredient to partially replace fish meal in diets of Pacific white shrimp (Litopenaeus vannamei, Boone, 1931). Aquaculture 354-355:50–55
Kikuchi K (1999) Partial replacement of fish meal with corn gluten meal in diets for Japanese flounder Paralichthys olivaceus. J World Aquacult Soc 30:357–363
Kirchgessner M, Kürzinger H, Schwarz FJ (1986) Digestibility of crude nutrients in different feeds and estimation of their energy content for carp (Cyprinus carpio, L). Aquaculture 58:185–194
Lee SM (2002) Apparent digestibility coefficients of various feed ingredients for juvenile and grower rockfish (Sebastes schlegeli). Aquaculture 207:79–95
Lim SJ, Lee KJ (2009) Partial replacement of fish meal by cottonseed meal and soybean meal with iron and phytase supplementation for parrot fish Oplegnathus fasciatus. Aquaculture 290:283–289
Lin HZ, Guo Z, Yang Y, Zheng W, Li ZJ (2005) Effect of dietary probiotics on apparent digestibility coefficients of nutrients of white shrimp Litopenaeus vannamei Boone. Aquac Res 35:1441–1447
Lupatsch I, Kissil GW, Sklan D, Pfeffer E (1997) Apparent digestibility coefficients of feed ingredients and their predictability in compound diets for gilthead seabream, Sparus aurata, L. Aquac Nutr 3:81–89
MacArtain P, Gill CI, Brooks M, Campbell R, Rowland IR (2007) Nutritional value of edible seaweeds. Nutr Rev 65:535–543
Masumoto T, Ruchimat T, Ito Y, Hosokawa H, Shimeno S (1996) Amino acid availability values for several protein sources for yellowtail (Seriola quinqueradiata). Aquaculture 146:109–119
Michiels J, Skrivanova E, Missotten J, Ovyn A, Mrazek J, Smet SD (2012) Intact brown seaweed (Ascophyllum nodosum) in diets of weaned piglets: effects on performance, gut bacteria and morphology and plasma oxidative status. J Anim Physiol Anim Nutr 96:1101–1111
Miller WE, Maloney TE, Greene JC (1974) Algal productivity in 49 lake waters as determined by algal assays. Water Res 8:667–679
Mu YY, Lam TJ, Guo JY, Shim KM (2000) Protein digestibility and amino acid availability of several protein sources for juvenile Chinese hairy crab Eriocheir sinensis H. Milne-Edwards (Decapoda, Grapsidae). Aquac Res 31:757–765
Nakagawa H (1997) Effect of dietary algae on improvement of lipid metabolism in fish. Biomed Pharmacother 51:345–348
Nath PR, Khozin-Goldberg I, Cohen Z, Boussiba S, Zilberg D (2012) Dietary supplementation with the microalgae Parietochloris incisa, increases survival and stress resistance in guppy (Poecilia reticulata) fry. Aquac Nutr 18:167–180
Naylor RL, Hardy RW, Bureaus DP, Chiu A, Elliott M, Farrell AP (2009) Feeding aquaculture in an era of finite resources. Proc Nat Acad Sci U S A 106:15103–15110
Oujifard A, Seyfabadi J, Kenari AA, Rezaei M (2012) Growth and apparent digestibility of nutrients, fatty acids and amino acids in Pacific white shrimp, Litopenaeus vannamei, fed diets with rice protein concentrate as total and partial replacement of fish meal. Aquaculture 342–343:56–61
Pallaoro MF, do Nascimento Vieira F, Hayashi L (2016) Ulva lactuca (Chlorophyta Ulvales) as co-feed for Pacific white shrimp. J Appl Phycol 28:3659–3665
Peña-Rodríguez A, Mawhinney TP, Ricque-Marie D, Cruz-Suárez LE (2011) Chemical composition of cultivated seaweed Ulva clathrata (Roth) C. Agardh. Food Chem 129:491–498
Ponce-Palafox J, Martinez-Palacios CA, Ross LG (1997) The effects of salinity and temperature on the growth and survival rates of juvenile white shrimp, Penaeus vannamei, Boone, 1931. Aquaculture 157:107–115
Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–658
Rodríguez-González H, Orduña-Rojas J, Villalobos-Medina JP, García Ulloa M, Polanco-Torres A, López-Álvarez ES, Montoya-Mejía M, Hernández-Llamas A (2014) Partial inclusión of Ulva lactuca and Gracilaria parvispora meal in balanced diets for white leg shrimp (Litopenaeus vannamei). J Appl Phycol 26:2453–2459
Schleder DD, da Rosa JR, Guimarães AM, Ramlov F, Maraschin M, Seiffert WQ, do Nascimento Vieira F, Hayashi L, Andreatta ER (2017) Brown seaweeds as feed additive for white-leg shrimp: effects on thermal stress resistance, midgut microbiology, and immunology. J Appl Phycol 29:2471–2477
Sheikhzadeh N, Tayefinasrabadi H, Oushani AK, Enferadi MH (2012) Effects of Haematococcus pluvialis supplementation on antioxidant system and metabolism in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 38:413–419
Shields RJ, Lupatsch I (2012) Algae for aquaculture and animal feeds. Technikfolgenabschätzung – Theorie und Praxis 21: 23–37
Silva RL, Barbosa JM (2009) Seaweed meal as a protein source for the white shrimp Litopenaeus vannamei. J Appl Phycol 21:193–197
Silva SSD, Gunasekera RM, Gooley G (2000) Digestibility and amino acid availability of three protein-rich ingredient-incorporated diets by murray cod Maccullochella peelii peelii (Mitchell) and the Australian shortfin eel Anguilla australis Richardson. Aquac Res 31:195–205
Stone DA, Allan GL, Parkinson S, Rowland SJ (2000) Replacement of fish meal in diets for Australian silver perch, Bidyanus bidyanus: III Digestibility and growth using meat meal products. Aquaculture 186:311–326
Sudaryono A, Hoxey MJ, Kailis SG, Evans LH (1995) Investigation of alternative protein sources in practical diets for juvenile shrimp, Penaeus monodon. Aquaculture 134:313–323
Sugiura SH, Raboy V, Young KA, Dong FM, Hardy RW (1999) Availability of phosphorus and trace elements in low-phytate varieties of barley and corn for rainbow trout (Oncorhynchus mykiss). Aquaculture 170:285–296
Sullivan JA, Reigh RC (1995) Apparent digestibility of selected feedstuffs in diets for hybrid striped bass (Morone saxatilis, ♀ x Morone chrysops, ♂). Aquaculture 138:313–322
Terrazas-Fierro M, Civera-Cerecedo R, Ibarra-Martínez L, Goytortúa-Bores E, Herrera-Andrade M, Reyes-Becerra A (2010) Apparent digestibility of dry matter, protein, and essential amino acid in marine feedstuffs for juvenile whiteleg shrimp Litopenaeus vannamei. Aquaculture 308:166–173
Turner JL, Dritz SS, Higgins JJ, Minton JE (2002) Effects of Ascophyllum nodosum extract on growth performance and immune function of young pigs challenged with Salmonella typhimurium. J Anim Sci 80:1947–1953
Ufodike EBC, Matty AJ (1983) Growth responses and nutrient digestibility in mirror carp (Cyprinus carpio) fed different levels of cassava and rice. Aquaculture 31:41–50
Williams AS, Davis DA, Arnold CR (1996) Density-dependent growth and survival of Penaeus setiferus and Penaeus vannamei in a semi-closed recirculating system. J World Aquacult Soc 27:107–112
Wilson RP, Robinson EH, Poe WE (1981) Apparent and true availability of amino acids from common feed ingredients for channel catfish. J Nutr 111:923–929
Xu S, Zhang L, Wu Q, Liu X, Wang S, You C (2011) Evaluation of dried seaweed Gracilaria lemaneiformis, as an ingredient in diets for teleost fish Siganus canaliculatus. Aquacult Int 19:1007–1018
Yang Q, Zhou X, Zhou Q, Tan B, Chi S, Dong X (2009) Apparent digestibility of selected feed ingredients for white shrimp Litopenaeus vannamei, Boone. Aquac Res 41:78–86
Zhou QC, Tan BP, Mai KS, Liu YJ (2004) Apparent digestibility of selected feed ingredients for juvenile cobia Rachycentron canadum. Aquaculture 241:441–451
Funding
The authors thank the funding of China Agriculture Research System-47 (CRAS-47), the Project of the fundamental Research Funds for the Central Universities (161gpy36), the Special Project of Marine Fishery Science and Technology of Guangdong Province (A201601C11), and the Central Institutes of Public Welfare Projects (2014A08YQ02).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Yang, F., Xie, S., Niu, J. et al. Effect of dietary macro-algae in diet of juvenile Pacific white shrimp Litopenaeus vannamei . J Appl Phycol 30, 1335–1344 (2018). https://doi.org/10.1007/s10811-017-1323-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-017-1323-z