Aquacult Int (2013) 21:699–708 DOI 10.1007/s10499-012-9604-7
Effects of continuous and diel intermittent feeding regimes on food consumption, growth and gonad production of the sea urchin Strongylocentrotus intermedius of different size classes Chong Zhao • Weijie Zhang • Yaqing Chang • Haisen Zhou Jian Song • Shibin Luo
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Received: 7 March 2012 / Accepted: 4 October 2012 / Published online: 10 January 2013 Ó Springer Science+Business Media Dordrecht 2013
Abstract We investigated effects of a continuous and three diel feeding regimes on food consumption, growth and gonad production of cultured Strongylocentrotus intermedius of three size classes. There was no significant difference of food consumption, body weight and gonad production between nocturnal and diurnal feeding regimes of S. intermedius of all size classes, greatly challenging the old paradigm on the diel feeding preference of cultured S. intermedius. The continuous and three diel intermittent feeding regimes did not significantly affect body weight of sea urchins of all size classes. However, sea urchins in the large and small size classes which were fed continuously had significantly higher gonad wet weight and gonad index than those fed intermittently. Gonad of sea urchins in the medium size class did not change with feeding regime. The present study increases our understanding of the feeding behavior of cultured S. intermedius, with a potential of direct application in aquaculture. Keywords Nocturnal
Body size Diurnal Feeding regime Strongylocentrotus intermedius
Introduction Like many animals, sea urchins have diel rhythms, indicating sensitivity to light. Some species are nocturnal (e.g., Thornton 1956; Lawrence and Hughes-Games 1972; Nelson and Vance 1979; Carpenter 1984; James 2000; Vaı¨tilingon et al. 2003; Tuya et al. 2004) because of diurnal predators. Paracentrotus lividus is nocturnal in the Mediterranean Sea and diurnal in Irish waters because of different predators that have opposite diel rhythms (Ebling et al. 1966; Dance 1987; Barnes and Crook 2001). These studies suggest the diel feeding behaviors of sea urchins in field are different between species and habitats. In C. Zhao College of Marine Life Science, Ocean University of China, Qingdao 266003, China C. Zhao W. Zhang Y. Chang (&) H. Zhou J. Song S. Luo Key Laboratory of Mariculture & Stock Enhancement in North China’s Sea, Ministry of Agriculture, Dalian Ocean University, Dalian 116023, China e-mail:
[email protected]
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laboratory studies, Yoshida (1966) reported that sea urchins respond to both an increase and a decrease in light intensity. Fuji (1967) convincingly demonstrated that feeding of Strongylocentrotus intermedius is affected by light conditions in laboratory. In his study, more feeding occurred during nighttime than daytime and individuals fed more at low light intensity than at high light intensity. However, whether the diel feeding preference has an application potential in sea urchin aquaculture remains largely unclear. The effects of feeding frequency on the growth performance and commercial production have been widely reported for a variety of marine organisms (e.g., Buurma and Diana 1994; Cho et al. 2003; Silva et al. 2007; Wang et al. 2007; Yamamoto et al. 2007; Lin et al. 2009). However, only a few studies have investigated this question in sea urchins. In the sea urchin Lytechinus variegates, Lawrence et al. (2003) reported that a decrease in frequency of feeding results in a greater proportion of the nutrients being used for maintenance and less for production. They found the total amount of food consumed was greater in those fed every day, although consumption rate was greater in urchins fed intermittently. Minor and Scheibling (1997) reported that sea urchins Strongylocentrotus droebachiensis fed daily got significant greater gonad index than those fed once a week. McCarron et al. (2009) also reported greater gonad production in P. lividus fed continuously than in those fed intermittently. However, neither study found an effective feeding regime that indicated compensatory growth. The effect of an intermittent feeding regime with food provided during the day or night is not known. Because roe of S. intermedius has excellent qualities and nutritional value, it has great commercial value (Chang et al. 2004). The annual yield of the roe of S. intermedius harvested from the north coast of China amounted to 200 tons per year (Ding et al. 2007). Increased commercial demand has resulted in a great interest in its aquaculture. The major aquaculture methods for S. intermedius in China include to culture them off shore at shallow depths in suspended cages feeding them kelp Laminaria japonica and to release them into managed areas of sea floor (Chang et al. 2004). Maintaining a precise feeding regime is essential to sea urchin aquaculture, but the effects of different feeding regimes on S. intermedius have not been investigated. This lack of relevant information obviously hampers the development of the industry. Based on Fuji (1967)’s findings, we hypothesized that diurnal and nocturnal feeding regimes affect food consumption, growth and gonad production in S. intermedius. The following six studies were conducted to test: (1) whether food consumption of S. intermedius significantly differs between diurnal and nocturnal feeding regimes; (2) whether continuous and intermittent feeding regimes significantly affect food consumption of S. intermedius and whether the daily food consumption of S. intermedius is size class dependent; (3) whether diurnal and nocturnal intermittent feeding significantly affect growth of S. intermedius in comparison with continuous feeding; (4) whether diel intermittent feeding regimes significantly affect gonad production of S. intermedius compared to continuous feeding regimes; (5) whether gonad wet weight and gonad index of S. intermedius significantly differ between diurnal and nocturnal feeding regimes; (6) whether a diel intermittent feeding regime is appropriate for aquaculture of S. intermedius.
Materials and methods Sea urchins Sea urchins were produced by multiple mating and then cultivated at a density of 5 9 103 g/m3 under natural photoperiod in the Key Laboratory of Mariculture & Stock
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Enhancement in North China’s Sea, Ministry of Agriculture, Dalian Ocean University, China. After 16 months of laboratory cultivation, five hundred and forty individuals were taken from this cohort. We measured the test diameter of the sea urchins with digital calipers and separated sea urchins into three different size classes (Mean ± SE): Size class 1 (S1), 30.13 ± 0.08 mm Size class 2 (S2), 23.44 ± 0.07 mm Size class 3 (S3), 14.84 ± 0.06 mm. We placed 540 individuals into 36 cages (15 individuals per cage). The cage size is 30 cm (length) * 20 cm (width) * 40 cm (height). There were 3 cages (each containing 15 individuals) for each of the 4 feeding regimes and the 3 size classes. They were randomly distributed among several tanks. Although an independent water supply was not used, independent cages and relatively low density made no interaction between the sea urchins. This made true replicates. There were no significant differences in both test diameter and body weight between groups in each size class (p [ 0.05). All individuals were cultured indoor under natural photoperiod at the Key Laboratory of Mariculture & Stock Enhancement in North China’s Sea, Ministry of Agriculture, Dalian Ocean University in China during the experimental period of 12 weeks on the condition of sea water temperature (9–12 °C), salinity (30–31 %) and pH (7.9–8.1). Feeding regimes Four feeding regimes were used: feeding during the day (diurnal) or during the night (nocturnal), continuously and intermittently. In the continuous feeding regime, sea urchins were fed an excess of kelp (L. japonica). We changed the food of sea urchins in the continuous feeding regime group daily, although no fasting was carried out. In the nocturnal feeding regime, the kelp was placed into the cages at twilight and taken out at daybreak. In the diurnal feeding regime, the kelp was placed into the cages at daybreak and taken out at twilight. In the daily intermittent regime, the sea urchins were fed every other day. We carried out feeding and changing food in a way to minimize disturbance and damage to the sea urchins. Food consumption A known weight of kelp was provided at each feeding regime. The uneaten kelp was removed at the end of the feeding period and reweighed to calculate the amount of kelp consumed. Growth Sea urchins were weighed weekly with an electronic balance. Gonad wet weight and gonad index At the end of the study, 15 sea urchins (5 from each cage) of each size in each group were randomly collected and the gonads removed and weighed. The gonad index (GI) was calculated as follows: GI (%) = Wg/Ww*100, Wg = gonad wet weight, Ww = wet body weight.
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Statistical analysis All variables were calculated using Excel for Windows XP. The original data showed normal distributions and homogeneity of variance. One-way repeated measure ANOVA was performed with the SPSS 16.0 statistical software to detect the difference in food consumption and growth for sea urchins among feeding regimes in different size classes. Daily food consumption, gonad wet weight and gonad index were detected by one-way ANOVA. Duncan’s multiple comparisons were then performed. A probability level of p \ 0.05 was considered statistically significant.
Results
Wet weight of the kelp (g)
Daily food consumption of sea urchins in the three size classes fluctuated irregularly during the experimental period (Figs. 1, 2, 3). Feeding regimes significantly affected food consumption of sea urchins in the large and small size classes. However, no significant difference was found in medium size class sea urchins among feeding regimes. Statistical analysis of average daily food consumption showed a similar conclusion (Fig. 4). In the large size class, sea urchins fed continuously consumed significantly more food than those fed only during the day or every other day, but not significantly more than those fed during the night. Small sea urchins consumed significantly more food in continuous feeding regime than those in other feeding regimes. The amount of food consumed by all size classes fed during the day or during the night did not differ significantly. Nocturnal feeding regime Diurnal feeding regime Daily intermittent regime Continuous feeding regime
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Fig. 1 Mean daily food consumption of large size sea urchins in different feeding regimes
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Fig. 2 Mean daily food consumption of medium size sea urchins in different feeding regimes
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Fig. 3 Mean daily food consumption of small size sea urchins in different feeding regimes Nocturnal feeding regime Diurnal feeding regime Daily intermittent feeding regime Continuous feeding regime
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Size class Fig. 4 Average daily food consumption of different size sea urchins in different feeding regimes. Class 1: 30 mm; Class 2: 23 mm; Class 3: 14 mm. In each size class, different letters indicate significant difference according to Duncan’s multiple comparisons
Growth (wet body weight) of sea urchins in the four feeding regimes is shown in Fig. 5. One-way ANOVA showed no significant difference between all feeding regimes in all size classes (p [ 0.05). Gonad growth (wet weight) was significantly affected by feeding regimes in large and small sea urchins (p \ 0.05). In both large and small size classes, sea urchins fed continuously had significantly greater gonad wet weight than those fed intermittently (p \ 0.05, Fig. 6). However, no significant difference in gonad wet weight was found in medium size class (p [ 0.05). There was no significant difference of gonad wet weight between nocturnal and diurnal feeding regimes in all size classes of sea urchins (p [ 0.05). In large and small size classes, sea urchins fed continuously had a higher gonad index than those fed intermittently (p \ 0.05, Fig. 7). In medium size class, however, the gonad index of sea urchins fed continuously was not significantly different from that of those fed
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Fig. 5 Mean wet body weights of three size classes sea urchins in continuous and intermittent feeding regimes. Class 1: 30 mm; Class 2: 23 mm; Class 3: 14 mm
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Size class Fig. 6 Gonad wet weight regimes (Mean ± SD, N = 15) of three size classes of sea urchins in continuous and intermittent feeding regimes. Class 1: 30 mm; Class 2: 23 mm; Class 3: 14 mm. In each size class, different letters indicate significant difference according to Duncan’s multiple comparisons
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705 Nocturnal feeding regime Diurnal feeding regime Daily intermittent feeding regime Continuous feeding regime
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Size class Fig. 7 Gonad index (Mean ± SD, N = 15) of three size classes of sea urchins in continuous and intermittent feeding regimes. Class 1: 30 mm; Class 2: 23 mm; Class 3: 14 mm. In each size class, different letters mean significant difference according to Duncan’s multiple comparisons
intermittently (p [ 0.05). No significant difference of gonad index was found between nocturnal and diurnal feeding regimes in all size classes of sea urchins (p [ 0.05).
Discussion S. intermedius has been thought to have higher food consumption during the night because of its higher nocturnal activity and negative phototactic feeding behavior (Fuji 1967; Chang et al. 2004). However, it is not known if greater nocturnal feeding contributes to growth and gonad performance. The lack of information on the effect of diel feeding and on food consumption, growth and gonad performance greatly limits our understanding of sea urchin feeding behavior and consequently hampers the development of sea urchin aquaculture. To our knowledge, the present study is the first report on the effect of diurnal and nocturnal feeding regimes on food consumption, growth and gonad performance in cultivated S. intermedius. Fuji (1967) reported that sea urchins fed more actively at night after a bright day. In the present study, contrary to our expectation, we found no significant effect of nocturnal and diurnal feeding regimes on food consumption, growth and gonad production of S. intermedius under laboratory culture condition. These results suggest that S. intermedius has no diel rhythm at least in laboratory culture and to some extent challenge our former paradigm considering S. intermedius as a nocturnal marine organism (Fuji 1967). The present study agrees with studies by Lawrence and Hughes-Games (1972) and Vaı¨tilingon et al. (2003), who documented the presumed nocturnal rhythm of feeding associate with activity by measuring the amount of gut contents in Diadema antillarum and Tripneustes gratilla, respectively. These observations indicate sea urchins can function both diurnally and nocturnally. The observations in Fuji (1967) lasted for only 2 days and
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did not indicate the immediate past conditions of the sea urchins. It is possible very bright light and abrupt changes in light intensity may inhibit feeding. The different observations on diel rhythm of sea urchins may be because the sea urchins can learn to associate light with predation. Nocturnal and diurnal feeding regimes might be expected to have an effect in wild sea urchins because of this learned association of light with potential predation. In the present study, however, nocturnal and diurnal feeding regimes had no effect on gonad production probably because feeding did not differ with regime in laboratory. This could enrich our understanding of diurnally feeding deprivation of sea urchins and provide direct application to the aquaculture of S. intermedius. The present study is helpful to overcome the paradigm in sea urchin aquaculture. In the sea urchin P. lividus, McCarron et al. (2009) pointed out that even when food is continuously available and the environmental conditions remain unchanged, sea urchins may not necessarily feed continuously. In the present study, however, we found that large and small sea urchins fed significantly more in continuous feeding regimes than in intermittent feeding regimes. This agrees with the study by Lawrence et al. (2003), who reported the total amount is greater because their food is always available although the daily amount of food consumed by urchins fed continuously may be less than those fed intermittently. This suggests that S. intermedius feeds continuously when food is always available. This increases our knowledge on the feeding habit of S. intermedius and highlights the potential risk of degeneration and desertification of macro-algae habitat for releasing S. intermedius. In the present study, daily food consumption irregularly fluctuated during the experimental period of 12 weeks (Figs. 1, 2, 3). These results suggest feeding rhythm of S. intermedius is not dependent on size or feeding regimes. Compensatory growth is the increase in growth rate when animals are returned to full rations following food restriction (Weatherley and Gill 1981; McCarron et al. 2009). This phenomenon has been reported frequently in marine organisms with different time periods of food restriction (Dobson and Holmes 1984; Quinton and Blake 1990; Jobling and Koskela 1996; LaMontagne et al. 2003; Tian and Qin 2003; Ka¨nka¨nen and Pirhonen 2009; Stefansson et al. 2009). However, compensatory growth and its potential application in aquaculture have not been studied in commercial sea urchins. Compensatory growth was not observed in the present study in spite of short feeding intervals. This might be due to the limited duration of the experiment and the short period of food restriction. In the present study, we found no significant difference in wet body weight of sea urchins between urchins fed continuously and intermittently. In P. lividus, however, McCarron et al. (2009) reported that weekly intermittent feeding did not significantly affect the body weight of large sea urchins but significantly affected that of small and medium individuals. The disagreement might be due to different feeding intervals and species. In the present study, diel intermittent feeding significantly affected the gonad production of sea urchins. The gonad wet weight or gonad index of large and small sea urchins fed continuously was significantly larger than those fed intermittently. However, no significant difference was found on the body weight of sea urchins among feeding regimes. This agrees with the former opinion that a decrease in frequency of food availability results in use of a greater proportion of the food consumed for maintenance and less for gonad production (Lawrence et al. 2003). The present study with S. intermedius supports the conclusion of the study by McCarron et al. (2009) that intermittent feeding regime decreases gonad production of sea urchins. However, no significant difference of wet gonad weight and gonad index was found between the medium sea urchins fed continuously and intermittently. This is a very strange and inexplicable result. A similar
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phenomenon was also found by McCarron et al. (2009) with P. lividus. In their study, gonad wet weight and index showed no significant difference between medium size sea urchins fed continuously and intermittently, although those of urchins fed continuously were slightly higher than those fed intermittently. However, McCarron et al. (2009) did not provide any explanation for this strange phenomenon. We also cannot explain it. Further study is necessary to provide more information to confirm or reject the strange phenomenon found both by McCarron et al. (2009) and the present study. We are aware that the present study only involved laboratory sea urchins under the condition of laboratory. There is no evidence whether laboratory cultured sea urchins have innate nocturnal behavior. Therefore, further studies should be carried out on the wild collected sea urchins to compare with the present study for better understanding of the feeding behavior of S. intermedius. In conclusion, the present study indicates (1) food consumption of S. intermedius did not significantly differ between diurnal and nocturnal feeding regimes; (2) feeding regimes significantly affected food consumption of sea urchins in the large and small size classes, but not in medium size class; (3) diurnal and nocturnal intermittent feeding did not significantly affect growth of S. intermedius compared to continuous feeding; (4) diel intermittent feeding regimes significantly affected gonad wet weight and gonad index of small and large S. intermedius compared to the continuous feeding regime; (5) gonad production of S. intermedius did not significantly differ between diurnal and nocturnal feeding regimes; (6) diel intermittent feeding regimes seem not appropriate for aquaculture of S. intermedius. Acknowledgments This work was supported by the Chinese National 863 Project (2012AA10A412). We are grateful to Prof. John Lawrence for providing many useful editorial suggestions.
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