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Appropriate feeding for early juvenile stages of eunicid polychaete Marphysa sanguinea

Appropriate feeding for early juvenile stages of eunicid polychaete Marphysa sanguinea Survival rate (SR) and growth rate (GR) were tested with various feed sources to identify an appropriate feed to improve the productivity in the early life stage of the rock worm Marphysa sanguinea (Montagu, 1813) (Eunicidae: Polychaeta). In addition, feed supply rates were also examined. Three experiments were performed to identify the appropriate feed for the juvenile stages of M. sanguinea. Experiment 1 was done using seven different feed sources and without feed as well for the first 20 days of M. sanguinea culture. Decapsulated Artemia and extruded pellet for shrimp were showed with high SR and GR in the experiment 1. Experiment 2 was performed with five different feed sources. Two feeds were selected from experiment 1 in addition to eel feed, mixed micro-algae, and benthic diatom. Four different quantities of each feed were supplied to 3000 individuals of early juvenile stage of M. sanguinea. High quantity of decapsulated Artemia and shrimp feed resulted with a relatively good SR and GR. In experiment 3, we provided 20, 50, and 75 mg of decapsulated Artemia and shrimp feed to 3000 individuals of M. sanguinea. Our results demonstrated that after 3 months, decapsulated Artemia showed high survival rate and 75 mg/3000 inds provided the best quantity of feed in the earlier life stage culture of M. sanguinea. Keywords: Polychaete, Feed, Feeding rate, Marphysa sanguinea, Decapsulated Artemia Background M. sanguinea lives in a rock block or between gravels Polychaetes with a relatively short life cycle and a strong mixed in tender deposit of upper and low intertidal region reproductivity not only play a role of secondary con- in the whole coast of South Korea and is well distributed sumers in the ocean but also sometimes purify deposit around the world (Glasby and Hutchings 2010; Hutchings by changing the organic ingredients through feeding et al. 2012). The studies on the breeding of M. sanguinea behavior (Clark 1977; Paik 1989; Heo 2011). Polychaetes were done by Imai (Imai 1975, 1976, 1981). Besides, the are considered as an indicator organism of marine pollu- studies on feeding habit and inhabiting environment of tion (Belan 2003; Giangrande et al. 2005; Samuelson adults (Prevedelli et al. 2007), on the early larval develop- 2001), as the major prey of benthic fish and as bait for ment (Imai 1982; Prevedelli et al. 2007), and on the salin- angling becoming a target species of fishermen’s sideline ity tolerance of juvenile (Garcês and Pereira 2011) were (Gambi et al. 1994; Olive 1994, 1999; Younsi et al. 2010). reported. However, the study on early nursery-stock culti- Among the polychaete species, especially, the rockworm vation for mass production of M. sanguinea was meager. Marphysa sanguinea (Montagu, 1813) (Eunicidae), is a The aquaculture of M. sanguinea required the definite commercially important species for aquaculture. technologies for mass production and by supply of appro- priated feed in each production stage. Unfortunately, no feed is placed on the market and only a pellet type of * Correspondence: chkpknu@hanmail.net shrimp or finfish feed is used in the culture of M. sangui- Interdisciplinary Program of Biomedical Engineering, Pukyong National nea. It is not clear that efficiency of such feed is proper as University, Busan 48513, Republic of Korea Department of Marine Bio-materials and Aquaculture, Pukyong National a food source. It is uncertain how such feed affects growth University, Busan 48513, Republic of Korea and survival of M. sanguinea. Especially, survival of larva- Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 2 of 9 juvenile until the third month is crucial to determine a Table 1 Nutritional contents of feed used in this experiment and their ingredients seed production of M. sanguinea, and it is necessary to establish a reasonable food source and feeding rate to Ingredient Protein Lipid Fiber Moisture Others prevent a high mortality in early life stage. Hence, the Shrimp feed Min 52% Min 14.5% Max 3% Max 10% – purpose of this study was to examine survival rate and Decapsulated Min 46% Min 5% Max 5.8% Max 13% – growth rate by testing various feeds to know appropriate Artemia feed, feeding rate, and supply rate in an early stage of Eel feed Min 54% Min 10% Max 15% – Ca 1.5%, P 2.7% nursery-stock production, the biggest fatal stage of M. sanguinea aquaculture. Mixed –– – – Isochrysis microalgae Pavlova, Tetraselmis Methods Benthic –– – – Navicula, To investigate an appropriate feed for early life stage of M. diatom Nitzschia, sanguinea, three different experiments were performed. etc. Experiment 1: preliminary survey with eight different feeds (20 days) decapsulated Artemia, four different quantities such as To investigate a suitable food source in early life stage of 5 mg/3000 inds, 10 mg/3000 inds, 50 mg/3000 inds, and M. sanguinea, 15 ml of seawater filtered by membrane 100 mg/3000 inds were supplied. For mixed microalgae 4 5 filter (GF/C) was put in 6-hole well plate (SPL Life Sci- and benthic diatom, 1 × 10 cells/3000 inds, 1 × 10 cells/ 6 7 ences Inc.), and 100 individuals of larvae were intro- 3000 inds, 1 × 10 cells/3000 inds, and 1 × 10 cells/3000 duced in each hole. The larvae were produced in inds were supplied. Nutritional contents of used feed are Fisheries Science and Technology Center of Pukyong presented in Table 1. The feeding was done for every National University. One microliter of diluted solution 2 daysafter 7daysfrominstallation ofexperiment. of 0.1 g of mud with 10 ml of filtered seawater was put Filtered seawater was renewed constantly, and remained in each hole as substrate to induce the planktonic larvae food was not removed. The experimental periods were to do metamorphosis. Water temperature was main- 60 days by reflecting the high mortality in early juvenile tained as 20 °C, and water was changed in 10 ml every period. Number of setigers and survival rate of worms 2 days. Without food source (control), Chaetoceros sp. were examined at the end of experiment. A rearing tank 4 4 (1 × 10 cells/ml), benthic diatom sp. (1 × 10 cells/ml), (Fig. 1) was constituted with three reserves of Chlorella powder (1 mg), Tetraselmis suecica (1 × 10 45 cm × 9 cm × 5 cm which allowed three replicates of cells/ml), sea mustard (1 ml), decapsulated Artemia experiments. Mud was used as a substrate with 1-cm (1 mg), and extruded pellet (EP) for shrimp (1 mg) were depth. Experimental installations are shown in Fig. 2. The used as food sources. Among them, decapsulated Arte- conditions of seawater were maintained at 20 ± 2 °C, 32– mia and EP for shrimp were started to supply after 33 psu, pH 8.0, and 6–8 ppm of DO during the experi- 6 days of introduction of larvae when they formed (Kim mental period. 2015). Feeds were supplied in every 2 days after renewal of seawater. The feeding tests were triplicated, and the Experiment 3: more detailed investigation on the source experimental period was 20 days. The survival and and the amount of feed for juvenile cultivation (3 months growth rate were calculated at the end of the experi- of experiment) ment. The living worms were counted, and the length Decapsulated Artemia and shrimp feed could be considered was measured by taking 10 juveniles randomly in each as a good efficient feed through the results of experiment 2; experimental group for calculating the growth rate. The hence, a closer feeding amount ranges were investigated in Dixi image program (Ver 2.89, Dixi optics) was used to the third experiment for 3 months. Three quantities such measure the length of juveniles. as 25 mg/3000 inds, 50 mg/3000 inds, and 75 mg/3000 inds of two feeds were reinstalled. The experimental conditions Experiment 2: investigation on the source and the were similar to experiment 2. amount of feed for early juvenile culture (for 2 months) Five feed sources with four quantities in each (total 20 Statistical analysis conditions) were tested. Decapsulated Artemia and Growth rate (GR) was measured with growth of body shrimp feed showing the positive results in experiment 1 length in experiment 1. were also used in addition to eel feed. For microalgae, GR (growth rate) = [(final body length − initial body mixed microalgae solution sold on the market and benthic length)/initial body length] × 100 diatom species generally used for larva of invertebrate as a For experiments 2 and 3, GR was measured with feed were selected (Table 1). For shrimp feed, eel feed, and number of setigers. Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 3 of 9 Fig. 1 Schematic diagram of rearing tank of M. sanguinea juveniles. Arrows indicate the flow of direction of running seawater Survival rate was calculated as Results Experiment 1: a preliminary survey about appropriate feed source of an early larval/juvenile cultivation for SRðÞ survival rate¼ðfinal population number nursery-stock cultivation =initial population numberÞ 100 The decapsulated Artemia and shrimp feed showed the high growth (Fig. 3) and survival rate (Fig. 4). The growth The validation of each study section was made by two- rate (GR) of shrimp feed group was 451.5 ± 13.29% which way ANOVA test with squared transformed data, and was the highest, and decapsulated Artemia was the significant test was conducted with a p value of 0.05. 411.3 ± 6.94% at the end of 20-day experiment. The other The statistical analysis was performed with the Systat v.9 experimental groups were showed similar or lower growth package. rate than the control group (without feed). Fig. 2 Schematic diagram of experimental setup for experiments 2 and 3. Arrows indicate flow of direction of running seawater Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 4 of 9 Fig. 3 Growth rate (GR) of early larval culture with eight different food sources after 20 days. A, without food source (control); B, Chaetoceros sp. 4 4 (1 × 10 cells/ml); C, benthic diatom sp. (1 × 10 cells/ml), D, Chlorella powder (1 mg); E, Tetraselmis suecica (1 × 10 cells/ml); F, sea mustard (1 ml); G, decapsulated Artemia (1 mg); and H, extruded pellet (EP) for shrimp (1 mg) The survival rate (SR) was the highest in decapsulated Experiment 2: first survey for appropriate feed source of Artemia with 61 ± 3.2%. Shrimp feed was followed with an early juvenile cultivation for nursery-stock cultivation 51 ± 3%. The control group was 35 ± 4.6%. The lowest (2 months of experiment) survival rate was 28 ± 3% of sea mustard which is lower Growth and survival rates of juveniles at the end of the than control (Fig. 4). The results of GR and SR were experiment according to feeding amount with different shown that decapsulated Artemia and shrimp feed were feed types are shown in Table 2 and Figs. 5 and 6. In the good candidate for feed of early juvenile stage. survival rate of different feed sources, decapsulated Fig. 4 Survival rates of early larval culture with eight different food sources after 20 days. A, without food source (control); B, Chaetoceros sp. 4 4 (1 × 10 cells/1 ml); C, benthic diatom sp. (1 × 10 cells/1 ml); D, Chlorella powder (1 mg); E, Tetraselmis suecica (1 × 10 cells/1 ml); F, wakame (1 ml); G, decapsulated Artemia (1 mg); and H, extruded pellet (EP) for shrimp (1 mg) Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 5 of 9 Table 2 Survival rate (SR) and number of setigers of M. sanguinea juvenile by feeds (2 months) Trials Group Amount of feed (per 3000 individuals) SR (%) Number of setigers Shrimp feed A 5 mg 1.00 ± 0.01 23.66 ± 1.25 B 10 mg 0.45 ± 0.30 23.58 ± 2.58 C 50 mg 11.81 ± 1.77 24.26 ± 3.78 D 100 mg 3.65 ± 0.29 31.13 ± 4.95 Eel feed A 5 mg 0.21 ± 0.01 26.10 ± 2.19 B 10 mg 3.37 ± 1.40 20.33 ± 1.41 C 50 mg 11.92 ± 3.28 21.80 ± 1.17 D 100 mg 6.70 ± 1.82 22.46 ± 0.80 Decapsulated Artemia A 5 mg 1.67 ± 0.54 29.66 ± 3.65 B 10 mg 9.45 ± 1.33 23.10 ± 2.59 C 50 mg 33.88 ± 2.54 25.03 ± 0.32 D 100 mg 11.62 ± 2.98 33.43 ± 3.20 Benthic diatom A 1 × 10 cell 0 B1×10 cell 0 C1×10 cell 0 D1×10 cell 0.2 ± 0.1 22.00 ± 3.07 Mixed microalgae A 1 × 10 cell 0 B1×10 cell 0 C1×10 cell 0 D1×10 cell 0.03 18.67 ± 3.06 Artemia showed the highest survival rate, followed by by 50 mg of eel feed 11.92 ± 3.28% and 50 mg of shrimp shrimp feed and eel feed. They showed higher SR than other feed 11.81 ± 1.77%, 100 mg of decapsulated Artemia showed two feed sources such as benthic diatom and mixed micro- 11.62 ± 2.98%. algae. Fifty milligrams of decapsulated Artemia showed the In feeding amount, 50 mg showed the highest survival highest average survival rate with 33.88 ± 2.54%. Followed rate in general. Benthic diatom and mixed microalgae Fig. 5 Total survival rate of M. sanguinea juvenile according to the different feeds for 2 months Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 6 of 9 Fig. 6 Number of setigers of M. sanguinea juvenile according to the different feeds for 2 months did not show survival individuals except in 1 × 10 cells which give statistically enough numbers at 20 experimen- (Fig. 5). Two-way ANOVA test showed the significant ef- tal days. fect (p < 0.05) of feed and quantity of feed for survival rate of juvenile (Table 3). In growth presented with number of Experiment 3: final survey for appropriate feed source of setigers, decapsulated Artemia and shrimp feed were an early juvenile cultivation for nursery-stock cultivation higher than eel feed. Benthic diatom and mixed microal- (3 months of experiment) gae were showed 22.00 ± 3.07 setigers and 18.67 ± 3.06 Decapsulated Artemia groupshowedhigher survivalrate setigers, respectively; however, they could not survive until than shrimp feed group on average (Table 5); 75 mg/3000 20 experimental days (Fig. 6). In decapsulated Artemia inds of decapsulated Artemia section showed 7.91 ± 1.28% section with the highest growth rate, 100 mg/3000 inds of survival rate. Next, decapsulated Artemia 50 mg/3000 section was 33.43 ± 3.2 setigers, and 5 mg/3000 inds inds showed 4.36 ± 0.81%, and shrimp feed 75 mg/3000 section was 29.66 ± 3.65 setigers, but 50 mg/3000 inds inds section showed 3.99 ± 1.19% (Fig. 7). In feeding section with the highest survival rate showed a low growth amount, 75 mg/3000 inds showed the highest survival rate as 25.03 ± 0.32 setigers. In all sections, 100 mg/3000 inds in general. Two-way ANOVA test showed the non- section showed the highest growth and 50 mg/3000 inds significant effect (p > 0.05) of feed, significant effect section showed the highest survival rate (Table 2). Consid- (p < 0.05) of quantity of feed, and significant effect ering survival and growth, decapsulated Artemia 50 mg/ (p < 0.05) of interaction of two factors for survival rate of 3000 inds section showed good result. juvenile (Table 6). Two-way ANOVA test showed the non-significant effect In growth presented with number of setigers, decapsu- (p < 0.05) of feed and quantity of feed for increase of seti- lated Artemia had more setigers than shrimp feed. Dec- ger numbers of juvenile (Table 4). So the effects of feed apsulated Artemia showed the highest growth in 75 mg/ and feed quantity were significant for survival rate, not for 3000 inds with 42.2 ± 8.31 setigers, followed by shrimp juvenile’s growth. Two-way ANOVA test was performed feed 75 mg/3000 inds section with 40.33 ± 5.94 setigers. only with shrimp feed, eel feed, and decapsulated Artemia In low amount of feed, growth was similar to shrimp Table 3 Two-way ANOVA test results of survival rate (SR) Table 4 Two-way ANOVA test results of setiger numbers cultured in different feeds for M. sanguinea juveniles cultured in different feeds for Marphysa sanguinea juveniles Source Sum-of-squares df Mean square F ratio P Source Sum-of-squares df Mean square F ratio P a a Feed 20.191 1 20.191 10.174 0.003 Feed 0.145 1 0.145 0.576 0.456 b b Qte of feed 30.851 1 30.851 18.463 0.000 Qte of feed 0.257 1 0.257 1.020 0.320 Feed × Qte of feed 47.995 1 47.995 41.135 0.000 Feed × Qte of feed 0.275 1 0.275 1.092 0.303 a a Feed: various kinds of feeds Feed: various kinds of feeds b b Qte of feed: various quantities of feeds Qte of feed: various quantities of feeds Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 7 of 9 Table 5 Survival rate (SR) and number of setigers of M. Table 6 Two-way ANOVA test results of survival rate (SR) sanguinea juvenile after 3 months cultured in different feeds for M. sanguinea juveniles Feed Group Amount of feed SR (%) Number of Source Sum-of-squares df Mean square F ratio P (per 3000 inds) setigers a Feed 0.987 1 0.987 4.232 0.056 (mg) (growth) Qte of feed 2.646 1 2.646 20.454 0.000 Shrimp feed A 25 2.08 ± 0.29 35.36 ± 5.17 Feed × Qte of feed 4.026 1 4.026 93.244 0.000 B 50 2.37 ± 0.60 37.10 ± 4.98 Feed: various kinds of feeds C 75 3.94 ± 1.19 40.33 ± 5.94 Qte of feed: various quantities of feeds Decapsulated A 25 2.12 ± 0.25 35.90 ± 7.98 Artemia polychaetes Nereis pelagica and Nereis grubei showed poly- B 50 4.36 ± 0.81 39.56 ± 8.31 phagia, Perinereis cultrifera shows phytophagy feeding sea- C 75 7.91 ± 1.28 42.20 ± 5.23 weed, and Perinereis nuntia showed polyphagia placing too much emphasizing on creophagy. Pereneris nuntia showed feed and decapsulated Artemia. With high amount of more than 80% of feeding efficiency with mixed feed of eel feed, growth was higher in decapsulated Artemia than in feed as powder in the Japanese aquaculture farm (Yoshida shrimp feed (Fig. 8). Two-way ANOVA test showed that 1976). But only few reports are available on the early juven- the non-significant effect (p > 0.05) of feed and significa- ile stage of M. sanguinea (Kim 2015). tive effect (p < 0.05) of quantity of feed and significant In the pilot survey for 20 days, creophagy- and effect (p < 0.05) of interaction of two factors for setiger phytophagy-type feeds were tested. It was very clear that numbers of juvenile (Table 7). decapsulated Artemia and shrimp feed were reasonably good for early life stage of M. sanguinea culture and the Discussion and conclusions other feed were shown similar level to the control group Imai (1975) reported that mucilage secreted after 10– (without food) (Fig. 3). Similar result was reported by 13 days from fertilization, later it was well agreed to the Nielsen et al. (1995), filter-feeding Nereis diversicolor report of Kim and Jang (2008). In this experiment, we made grew on a diet of suspended algal cells, but the max- an attempt of food supply from the seventh day of larval re- imum specific growth rate was lower than the feeding lease, as per the report of Kim (2015), and observed that experiments with shrimp meat. In the case of experi- larvae ate organic matter with jaw plate from the seventh ment 1, growth and survival rate of shrimp feed and day. In the larval stage, like other lecitotrophic larvae, the decapsulated Artemia were higher than other feeding worm cannot feed and only looking for appropriate settling sources. Generally, 50 mg/3000 inds sections showed place (Thorson 1950; Jablonski and Lutz 1983). The other good survival rate in feeding amount of shrimp, eel, and Fig. 7 Total survival rate of M. sanguinea juvenile according to the different feeds for 3 months Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 8 of 9 Fig. 8 Number of setigers of M. sanguinea juvenile according to the feeds for 3 months decapsulated Artemia feeds. Decapsulated Artemia diatom and microalgae sections, and it showed a very showed the highest growth rate. Studies performed by low survival rate below 0.2% of survival rate; thus, they Vedel and Riisgård (1993) showed that N. diversicolor could not play a role of food source for M. sanguinea. fed algal cells (Rhodomonas sp.) obtained specific growth Hence, 50 mg/3000 inds of decapsulated Artemia was rates of 3.1% comparable to 3.9% measured in worms in the best food and feeding amount for the first 2 months glass tubes placed 15 cm above the bottom in the eutro- of nursery-stock cultivation. phicated Odense Fjord. The maximum specific growth Two-way ANOVA test showed significant effect of rate of the facultative N. diversicolor fed algae is lower feed and feed quantity for survival rate. However, there than 9% found for the obligate suspension-feeding blue was no significant difference in growth rate. The good mussel Mytilus edulis grown in nature in net bags (Riis- survival rate was showed in decapsulated Artemia. Eel gård and Poulsen 1981). feed showed slightly higher survival rate than shrimp However, 50 mg/3000 inds section with the highest feed for M. sanguinea larvae. But growth rate was higher survival rate showed lower growth than other feeding in shrimp feed and easier to control in water quality amount sections. Both 5 mg/3000 inds and 10 mg/3000 than in eel feed (Kim 2015). This is similar to the result inds sections were showed very low survival rate by in- of N. diversicolor, where the maximum specific growth sufficient food sources. It seems that there was a rate was higher in shrimp feed (Nielsen et al. 1995). cannibalization in the low feeding amount sections. The Hence, decapsulated Artemia and shrimp feed were other section 100 mg/3000 inds was also found with chosen for experiment 3. The quantity of feed supplied relatively low survival rate due to the degradation of was differentiated more and less 25 mg/3000 inds in the water quality by the accumulation of unused feeds. In base of 50 mg/3000 inds. In the experiment 3, our re- addition, there was already no survival being in adhesive sults showed that enough amount of feed can help sur- vival and growth rates, no matter what kind of feed is Table 7 Two-way ANOVA test results of setiger numbers provided. However, decapsulated Artemia showed high cultured in different feeds for Marphysa sanguinea juveniles survival rate and 75 mg/3000 inds section provided the Source Sum-of-squares df Mean square F ratio P best quantity of feed in the earlier life stage culture of Feed 0.075 1 0.075 1.579 0.227 M. sanguinea. Since there were no much studies on the Qte of feed 0.618 1 0.618 45.722 0.000 larvae of M. sanguinea in Korea and other countries, our results were not extensively compared. However, Feed × Qte of feed 0.607 1 0.607 42.775 0.000 a further comparative studies are necessary to clarify the Feed: various kinds of feeds Qte of feed: various quantities of feeds extent of feeding in the larvae of M. sanguinea. Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 9 of 9 Funding Imai T. The early development and breeding of Marphysa sanguinea (Montagu). This work was supported by a Research Grant of Pukyong National University Benthos Res. 1982;23:36–41. (2015 year). 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Appropriate feeding for early juvenile stages of eunicid polychaete Marphysa sanguinea

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Life Sciences; Fish & Wildlife Biology & Management; Marine & Freshwater Sciences; Zoology; Animal Ecology
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Abstract

Survival rate (SR) and growth rate (GR) were tested with various feed sources to identify an appropriate feed to improve the productivity in the early life stage of the rock worm Marphysa sanguinea (Montagu, 1813) (Eunicidae: Polychaeta). In addition, feed supply rates were also examined. Three experiments were performed to identify the appropriate feed for the juvenile stages of M. sanguinea. Experiment 1 was done using seven different feed sources and without feed as well for the first 20 days of M. sanguinea culture. Decapsulated Artemia and extruded pellet for shrimp were showed with high SR and GR in the experiment 1. Experiment 2 was performed with five different feed sources. Two feeds were selected from experiment 1 in addition to eel feed, mixed micro-algae, and benthic diatom. Four different quantities of each feed were supplied to 3000 individuals of early juvenile stage of M. sanguinea. High quantity of decapsulated Artemia and shrimp feed resulted with a relatively good SR and GR. In experiment 3, we provided 20, 50, and 75 mg of decapsulated Artemia and shrimp feed to 3000 individuals of M. sanguinea. Our results demonstrated that after 3 months, decapsulated Artemia showed high survival rate and 75 mg/3000 inds provided the best quantity of feed in the earlier life stage culture of M. sanguinea. Keywords: Polychaete, Feed, Feeding rate, Marphysa sanguinea, Decapsulated Artemia Background M. sanguinea lives in a rock block or between gravels Polychaetes with a relatively short life cycle and a strong mixed in tender deposit of upper and low intertidal region reproductivity not only play a role of secondary con- in the whole coast of South Korea and is well distributed sumers in the ocean but also sometimes purify deposit around the world (Glasby and Hutchings 2010; Hutchings by changing the organic ingredients through feeding et al. 2012). The studies on the breeding of M. sanguinea behavior (Clark 1977; Paik 1989; Heo 2011). Polychaetes were done by Imai (Imai 1975, 1976, 1981). Besides, the are considered as an indicator organism of marine pollu- studies on feeding habit and inhabiting environment of tion (Belan 2003; Giangrande et al. 2005; Samuelson adults (Prevedelli et al. 2007), on the early larval develop- 2001), as the major prey of benthic fish and as bait for ment (Imai 1982; Prevedelli et al. 2007), and on the salin- angling becoming a target species of fishermen’s sideline ity tolerance of juvenile (Garcês and Pereira 2011) were (Gambi et al. 1994; Olive 1994, 1999; Younsi et al. 2010). reported. However, the study on early nursery-stock culti- Among the polychaete species, especially, the rockworm vation for mass production of M. sanguinea was meager. Marphysa sanguinea (Montagu, 1813) (Eunicidae), is a The aquaculture of M. sanguinea required the definite commercially important species for aquaculture. technologies for mass production and by supply of appro- priated feed in each production stage. Unfortunately, no feed is placed on the market and only a pellet type of * Correspondence: chkpknu@hanmail.net shrimp or finfish feed is used in the culture of M. sangui- Interdisciplinary Program of Biomedical Engineering, Pukyong National nea. It is not clear that efficiency of such feed is proper as University, Busan 48513, Republic of Korea Department of Marine Bio-materials and Aquaculture, Pukyong National a food source. It is uncertain how such feed affects growth University, Busan 48513, Republic of Korea and survival of M. sanguinea. Especially, survival of larva- Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 2 of 9 juvenile until the third month is crucial to determine a Table 1 Nutritional contents of feed used in this experiment and their ingredients seed production of M. sanguinea, and it is necessary to establish a reasonable food source and feeding rate to Ingredient Protein Lipid Fiber Moisture Others prevent a high mortality in early life stage. Hence, the Shrimp feed Min 52% Min 14.5% Max 3% Max 10% – purpose of this study was to examine survival rate and Decapsulated Min 46% Min 5% Max 5.8% Max 13% – growth rate by testing various feeds to know appropriate Artemia feed, feeding rate, and supply rate in an early stage of Eel feed Min 54% Min 10% Max 15% – Ca 1.5%, P 2.7% nursery-stock production, the biggest fatal stage of M. sanguinea aquaculture. Mixed –– – – Isochrysis microalgae Pavlova, Tetraselmis Methods Benthic –– – – Navicula, To investigate an appropriate feed for early life stage of M. diatom Nitzschia, sanguinea, three different experiments were performed. etc. Experiment 1: preliminary survey with eight different feeds (20 days) decapsulated Artemia, four different quantities such as To investigate a suitable food source in early life stage of 5 mg/3000 inds, 10 mg/3000 inds, 50 mg/3000 inds, and M. sanguinea, 15 ml of seawater filtered by membrane 100 mg/3000 inds were supplied. For mixed microalgae 4 5 filter (GF/C) was put in 6-hole well plate (SPL Life Sci- and benthic diatom, 1 × 10 cells/3000 inds, 1 × 10 cells/ 6 7 ences Inc.), and 100 individuals of larvae were intro- 3000 inds, 1 × 10 cells/3000 inds, and 1 × 10 cells/3000 duced in each hole. The larvae were produced in inds were supplied. Nutritional contents of used feed are Fisheries Science and Technology Center of Pukyong presented in Table 1. The feeding was done for every National University. One microliter of diluted solution 2 daysafter 7daysfrominstallation ofexperiment. of 0.1 g of mud with 10 ml of filtered seawater was put Filtered seawater was renewed constantly, and remained in each hole as substrate to induce the planktonic larvae food was not removed. The experimental periods were to do metamorphosis. Water temperature was main- 60 days by reflecting the high mortality in early juvenile tained as 20 °C, and water was changed in 10 ml every period. Number of setigers and survival rate of worms 2 days. Without food source (control), Chaetoceros sp. were examined at the end of experiment. A rearing tank 4 4 (1 × 10 cells/ml), benthic diatom sp. (1 × 10 cells/ml), (Fig. 1) was constituted with three reserves of Chlorella powder (1 mg), Tetraselmis suecica (1 × 10 45 cm × 9 cm × 5 cm which allowed three replicates of cells/ml), sea mustard (1 ml), decapsulated Artemia experiments. Mud was used as a substrate with 1-cm (1 mg), and extruded pellet (EP) for shrimp (1 mg) were depth. Experimental installations are shown in Fig. 2. The used as food sources. Among them, decapsulated Arte- conditions of seawater were maintained at 20 ± 2 °C, 32– mia and EP for shrimp were started to supply after 33 psu, pH 8.0, and 6–8 ppm of DO during the experi- 6 days of introduction of larvae when they formed (Kim mental period. 2015). Feeds were supplied in every 2 days after renewal of seawater. The feeding tests were triplicated, and the Experiment 3: more detailed investigation on the source experimental period was 20 days. The survival and and the amount of feed for juvenile cultivation (3 months growth rate were calculated at the end of the experi- of experiment) ment. The living worms were counted, and the length Decapsulated Artemia and shrimp feed could be considered was measured by taking 10 juveniles randomly in each as a good efficient feed through the results of experiment 2; experimental group for calculating the growth rate. The hence, a closer feeding amount ranges were investigated in Dixi image program (Ver 2.89, Dixi optics) was used to the third experiment for 3 months. Three quantities such measure the length of juveniles. as 25 mg/3000 inds, 50 mg/3000 inds, and 75 mg/3000 inds of two feeds were reinstalled. The experimental conditions Experiment 2: investigation on the source and the were similar to experiment 2. amount of feed for early juvenile culture (for 2 months) Five feed sources with four quantities in each (total 20 Statistical analysis conditions) were tested. Decapsulated Artemia and Growth rate (GR) was measured with growth of body shrimp feed showing the positive results in experiment 1 length in experiment 1. were also used in addition to eel feed. For microalgae, GR (growth rate) = [(final body length − initial body mixed microalgae solution sold on the market and benthic length)/initial body length] × 100 diatom species generally used for larva of invertebrate as a For experiments 2 and 3, GR was measured with feed were selected (Table 1). For shrimp feed, eel feed, and number of setigers. Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 3 of 9 Fig. 1 Schematic diagram of rearing tank of M. sanguinea juveniles. Arrows indicate the flow of direction of running seawater Survival rate was calculated as Results Experiment 1: a preliminary survey about appropriate feed source of an early larval/juvenile cultivation for SRðÞ survival rate¼ðfinal population number nursery-stock cultivation =initial population numberÞ 100 The decapsulated Artemia and shrimp feed showed the high growth (Fig. 3) and survival rate (Fig. 4). The growth The validation of each study section was made by two- rate (GR) of shrimp feed group was 451.5 ± 13.29% which way ANOVA test with squared transformed data, and was the highest, and decapsulated Artemia was the significant test was conducted with a p value of 0.05. 411.3 ± 6.94% at the end of 20-day experiment. The other The statistical analysis was performed with the Systat v.9 experimental groups were showed similar or lower growth package. rate than the control group (without feed). Fig. 2 Schematic diagram of experimental setup for experiments 2 and 3. Arrows indicate flow of direction of running seawater Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 4 of 9 Fig. 3 Growth rate (GR) of early larval culture with eight different food sources after 20 days. A, without food source (control); B, Chaetoceros sp. 4 4 (1 × 10 cells/ml); C, benthic diatom sp. (1 × 10 cells/ml), D, Chlorella powder (1 mg); E, Tetraselmis suecica (1 × 10 cells/ml); F, sea mustard (1 ml); G, decapsulated Artemia (1 mg); and H, extruded pellet (EP) for shrimp (1 mg) The survival rate (SR) was the highest in decapsulated Experiment 2: first survey for appropriate feed source of Artemia with 61 ± 3.2%. Shrimp feed was followed with an early juvenile cultivation for nursery-stock cultivation 51 ± 3%. The control group was 35 ± 4.6%. The lowest (2 months of experiment) survival rate was 28 ± 3% of sea mustard which is lower Growth and survival rates of juveniles at the end of the than control (Fig. 4). The results of GR and SR were experiment according to feeding amount with different shown that decapsulated Artemia and shrimp feed were feed types are shown in Table 2 and Figs. 5 and 6. In the good candidate for feed of early juvenile stage. survival rate of different feed sources, decapsulated Fig. 4 Survival rates of early larval culture with eight different food sources after 20 days. A, without food source (control); B, Chaetoceros sp. 4 4 (1 × 10 cells/1 ml); C, benthic diatom sp. (1 × 10 cells/1 ml); D, Chlorella powder (1 mg); E, Tetraselmis suecica (1 × 10 cells/1 ml); F, wakame (1 ml); G, decapsulated Artemia (1 mg); and H, extruded pellet (EP) for shrimp (1 mg) Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 5 of 9 Table 2 Survival rate (SR) and number of setigers of M. sanguinea juvenile by feeds (2 months) Trials Group Amount of feed (per 3000 individuals) SR (%) Number of setigers Shrimp feed A 5 mg 1.00 ± 0.01 23.66 ± 1.25 B 10 mg 0.45 ± 0.30 23.58 ± 2.58 C 50 mg 11.81 ± 1.77 24.26 ± 3.78 D 100 mg 3.65 ± 0.29 31.13 ± 4.95 Eel feed A 5 mg 0.21 ± 0.01 26.10 ± 2.19 B 10 mg 3.37 ± 1.40 20.33 ± 1.41 C 50 mg 11.92 ± 3.28 21.80 ± 1.17 D 100 mg 6.70 ± 1.82 22.46 ± 0.80 Decapsulated Artemia A 5 mg 1.67 ± 0.54 29.66 ± 3.65 B 10 mg 9.45 ± 1.33 23.10 ± 2.59 C 50 mg 33.88 ± 2.54 25.03 ± 0.32 D 100 mg 11.62 ± 2.98 33.43 ± 3.20 Benthic diatom A 1 × 10 cell 0 B1×10 cell 0 C1×10 cell 0 D1×10 cell 0.2 ± 0.1 22.00 ± 3.07 Mixed microalgae A 1 × 10 cell 0 B1×10 cell 0 C1×10 cell 0 D1×10 cell 0.03 18.67 ± 3.06 Artemia showed the highest survival rate, followed by by 50 mg of eel feed 11.92 ± 3.28% and 50 mg of shrimp shrimp feed and eel feed. They showed higher SR than other feed 11.81 ± 1.77%, 100 mg of decapsulated Artemia showed two feed sources such as benthic diatom and mixed micro- 11.62 ± 2.98%. algae. Fifty milligrams of decapsulated Artemia showed the In feeding amount, 50 mg showed the highest survival highest average survival rate with 33.88 ± 2.54%. Followed rate in general. Benthic diatom and mixed microalgae Fig. 5 Total survival rate of M. sanguinea juvenile according to the different feeds for 2 months Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 6 of 9 Fig. 6 Number of setigers of M. sanguinea juvenile according to the different feeds for 2 months did not show survival individuals except in 1 × 10 cells which give statistically enough numbers at 20 experimen- (Fig. 5). Two-way ANOVA test showed the significant ef- tal days. fect (p < 0.05) of feed and quantity of feed for survival rate of juvenile (Table 3). In growth presented with number of Experiment 3: final survey for appropriate feed source of setigers, decapsulated Artemia and shrimp feed were an early juvenile cultivation for nursery-stock cultivation higher than eel feed. Benthic diatom and mixed microal- (3 months of experiment) gae were showed 22.00 ± 3.07 setigers and 18.67 ± 3.06 Decapsulated Artemia groupshowedhigher survivalrate setigers, respectively; however, they could not survive until than shrimp feed group on average (Table 5); 75 mg/3000 20 experimental days (Fig. 6). In decapsulated Artemia inds of decapsulated Artemia section showed 7.91 ± 1.28% section with the highest growth rate, 100 mg/3000 inds of survival rate. Next, decapsulated Artemia 50 mg/3000 section was 33.43 ± 3.2 setigers, and 5 mg/3000 inds inds showed 4.36 ± 0.81%, and shrimp feed 75 mg/3000 section was 29.66 ± 3.65 setigers, but 50 mg/3000 inds inds section showed 3.99 ± 1.19% (Fig. 7). In feeding section with the highest survival rate showed a low growth amount, 75 mg/3000 inds showed the highest survival rate as 25.03 ± 0.32 setigers. In all sections, 100 mg/3000 inds in general. Two-way ANOVA test showed the non- section showed the highest growth and 50 mg/3000 inds significant effect (p > 0.05) of feed, significant effect section showed the highest survival rate (Table 2). Consid- (p < 0.05) of quantity of feed, and significant effect ering survival and growth, decapsulated Artemia 50 mg/ (p < 0.05) of interaction of two factors for survival rate of 3000 inds section showed good result. juvenile (Table 6). Two-way ANOVA test showed the non-significant effect In growth presented with number of setigers, decapsu- (p < 0.05) of feed and quantity of feed for increase of seti- lated Artemia had more setigers than shrimp feed. Dec- ger numbers of juvenile (Table 4). So the effects of feed apsulated Artemia showed the highest growth in 75 mg/ and feed quantity were significant for survival rate, not for 3000 inds with 42.2 ± 8.31 setigers, followed by shrimp juvenile’s growth. Two-way ANOVA test was performed feed 75 mg/3000 inds section with 40.33 ± 5.94 setigers. only with shrimp feed, eel feed, and decapsulated Artemia In low amount of feed, growth was similar to shrimp Table 3 Two-way ANOVA test results of survival rate (SR) Table 4 Two-way ANOVA test results of setiger numbers cultured in different feeds for M. sanguinea juveniles cultured in different feeds for Marphysa sanguinea juveniles Source Sum-of-squares df Mean square F ratio P Source Sum-of-squares df Mean square F ratio P a a Feed 20.191 1 20.191 10.174 0.003 Feed 0.145 1 0.145 0.576 0.456 b b Qte of feed 30.851 1 30.851 18.463 0.000 Qte of feed 0.257 1 0.257 1.020 0.320 Feed × Qte of feed 47.995 1 47.995 41.135 0.000 Feed × Qte of feed 0.275 1 0.275 1.092 0.303 a a Feed: various kinds of feeds Feed: various kinds of feeds b b Qte of feed: various quantities of feeds Qte of feed: various quantities of feeds Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 7 of 9 Table 5 Survival rate (SR) and number of setigers of M. Table 6 Two-way ANOVA test results of survival rate (SR) sanguinea juvenile after 3 months cultured in different feeds for M. sanguinea juveniles Feed Group Amount of feed SR (%) Number of Source Sum-of-squares df Mean square F ratio P (per 3000 inds) setigers a Feed 0.987 1 0.987 4.232 0.056 (mg) (growth) Qte of feed 2.646 1 2.646 20.454 0.000 Shrimp feed A 25 2.08 ± 0.29 35.36 ± 5.17 Feed × Qte of feed 4.026 1 4.026 93.244 0.000 B 50 2.37 ± 0.60 37.10 ± 4.98 Feed: various kinds of feeds C 75 3.94 ± 1.19 40.33 ± 5.94 Qte of feed: various quantities of feeds Decapsulated A 25 2.12 ± 0.25 35.90 ± 7.98 Artemia polychaetes Nereis pelagica and Nereis grubei showed poly- B 50 4.36 ± 0.81 39.56 ± 8.31 phagia, Perinereis cultrifera shows phytophagy feeding sea- C 75 7.91 ± 1.28 42.20 ± 5.23 weed, and Perinereis nuntia showed polyphagia placing too much emphasizing on creophagy. Pereneris nuntia showed feed and decapsulated Artemia. With high amount of more than 80% of feeding efficiency with mixed feed of eel feed, growth was higher in decapsulated Artemia than in feed as powder in the Japanese aquaculture farm (Yoshida shrimp feed (Fig. 8). Two-way ANOVA test showed that 1976). But only few reports are available on the early juven- the non-significant effect (p > 0.05) of feed and significa- ile stage of M. sanguinea (Kim 2015). tive effect (p < 0.05) of quantity of feed and significant In the pilot survey for 20 days, creophagy- and effect (p < 0.05) of interaction of two factors for setiger phytophagy-type feeds were tested. It was very clear that numbers of juvenile (Table 7). decapsulated Artemia and shrimp feed were reasonably good for early life stage of M. sanguinea culture and the Discussion and conclusions other feed were shown similar level to the control group Imai (1975) reported that mucilage secreted after 10– (without food) (Fig. 3). Similar result was reported by 13 days from fertilization, later it was well agreed to the Nielsen et al. (1995), filter-feeding Nereis diversicolor report of Kim and Jang (2008). In this experiment, we made grew on a diet of suspended algal cells, but the max- an attempt of food supply from the seventh day of larval re- imum specific growth rate was lower than the feeding lease, as per the report of Kim (2015), and observed that experiments with shrimp meat. In the case of experi- larvae ate organic matter with jaw plate from the seventh ment 1, growth and survival rate of shrimp feed and day. In the larval stage, like other lecitotrophic larvae, the decapsulated Artemia were higher than other feeding worm cannot feed and only looking for appropriate settling sources. Generally, 50 mg/3000 inds sections showed place (Thorson 1950; Jablonski and Lutz 1983). The other good survival rate in feeding amount of shrimp, eel, and Fig. 7 Total survival rate of M. sanguinea juvenile according to the different feeds for 3 months Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 8 of 9 Fig. 8 Number of setigers of M. sanguinea juvenile according to the feeds for 3 months decapsulated Artemia feeds. Decapsulated Artemia diatom and microalgae sections, and it showed a very showed the highest growth rate. Studies performed by low survival rate below 0.2% of survival rate; thus, they Vedel and Riisgård (1993) showed that N. diversicolor could not play a role of food source for M. sanguinea. fed algal cells (Rhodomonas sp.) obtained specific growth Hence, 50 mg/3000 inds of decapsulated Artemia was rates of 3.1% comparable to 3.9% measured in worms in the best food and feeding amount for the first 2 months glass tubes placed 15 cm above the bottom in the eutro- of nursery-stock cultivation. phicated Odense Fjord. The maximum specific growth Two-way ANOVA test showed significant effect of rate of the facultative N. diversicolor fed algae is lower feed and feed quantity for survival rate. However, there than 9% found for the obligate suspension-feeding blue was no significant difference in growth rate. The good mussel Mytilus edulis grown in nature in net bags (Riis- survival rate was showed in decapsulated Artemia. Eel gård and Poulsen 1981). feed showed slightly higher survival rate than shrimp However, 50 mg/3000 inds section with the highest feed for M. sanguinea larvae. But growth rate was higher survival rate showed lower growth than other feeding in shrimp feed and easier to control in water quality amount sections. Both 5 mg/3000 inds and 10 mg/3000 than in eel feed (Kim 2015). This is similar to the result inds sections were showed very low survival rate by in- of N. diversicolor, where the maximum specific growth sufficient food sources. It seems that there was a rate was higher in shrimp feed (Nielsen et al. 1995). cannibalization in the low feeding amount sections. The Hence, decapsulated Artemia and shrimp feed were other section 100 mg/3000 inds was also found with chosen for experiment 3. The quantity of feed supplied relatively low survival rate due to the degradation of was differentiated more and less 25 mg/3000 inds in the water quality by the accumulation of unused feeds. In base of 50 mg/3000 inds. In the experiment 3, our re- addition, there was already no survival being in adhesive sults showed that enough amount of feed can help sur- vival and growth rates, no matter what kind of feed is Table 7 Two-way ANOVA test results of setiger numbers provided. However, decapsulated Artemia showed high cultured in different feeds for Marphysa sanguinea juveniles survival rate and 75 mg/3000 inds section provided the Source Sum-of-squares df Mean square F ratio P best quantity of feed in the earlier life stage culture of Feed 0.075 1 0.075 1.579 0.227 M. sanguinea. Since there were no much studies on the Qte of feed 0.618 1 0.618 45.722 0.000 larvae of M. sanguinea in Korea and other countries, our results were not extensively compared. However, Feed × Qte of feed 0.607 1 0.607 42.775 0.000 a further comparative studies are necessary to clarify the Feed: various kinds of feeds Qte of feed: various quantities of feeds extent of feeding in the larvae of M. sanguinea. Kim et al. Fisheries and Aquatic Sciences (2017) 20:19 Page 9 of 9 Funding Imai T. The early development and breeding of Marphysa sanguinea (Montagu). This work was supported by a Research Grant of Pukyong National University Benthos Res. 1982;23:36–41. (2015 year). Jablonski D, Lutz RA. Larval ecology of marine benthic invertebrates; paleobiological implications. Biol Rev. 1983;58:21–89. Kim BK. Feed and feeding rate in early stage on seed production of the Availability of data and materials rockworm polychaete Marphysa sanguinea. M. Eng. Thesis, Pukyong National All datasets generated during and/or analyzed during the current study are University, Busan, Korea. 2015. available from the corresponding author on reasonable request. Kim CH, Jang SW. Effects of rearing conditions on the artificial seed production of a polychaete Marphysa sanguinea. J Aquacul. 2008;21:34–40. Authors’ contributions Nielsen AM, Eriksen NT, Iversen JJL, Riisgård HU. Feeding, growth and respiration KHK, BKK, and CHK manufactured the experimental feed and drafted the in the polychaetes Nereis diversicolor (facultative filter-feeder) and N. virens manuscript. KHK, BKK, SKK, and WWP conducted the feeding trial and (omnivorous)—a comparative study. 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A new species of Marphysa Quatrefages, 1865 (Polychaeta: Eunicida: Eunicidae) from northern Australia and a review of Submit your next manuscript to BioMed Central similar taxa from the Indowest Pacific, including the genus Nauphanta Kinberg 1865. Zootaxa. 2010;2352:29–45. and we will help you at every step: Heo CH. Larval development and effect of substrates on juvenile growth of • We accept pre-submission inquiries polychaete Marphysa sanguinea, M. Fish. Thesis, Pukyong National University, Busan, Korea. 2011. � Our selector tool helps you to find the most relevant journal Hutchings P, Glasby CJ, Wijnhoven S. Note on additional diagnostic characters for � We provide round the clock customer support Marphysa sanguinea (Montagu, 1813) (Annelida: Eunicida: Eunicidae), a recently � Convenient online submission introduced species in the Netherlands. Aquat Invasions. 2012;7:277–82. Imai T. 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