Effects of continuous and diel intermittent feedingregimes on food consumption, growth and gonadproduction of the sea urchin Strongylocentrotusintermedius of different size classes

Chong Zhao • Weijie Zhang • Yaqing Chang • Haisen Zhou •

Jian Song • Shibin Luo

Received: 7 March 2012 / Accepted: 4 October 2012 / Published online: 10 January 2013� 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 Body size � Diurnal � Feeding regime � Strongylocentrotus intermedius �Nocturnal

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; Vaıtilingon 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. ZhaoCollege of Marine Life Science, Ocean University of China, Qingdao 266003, China

C. Zhao � W. Zhang � Y. Chang (&) � H. Zhou � J. Song � S. LuoKey Laboratory of Mariculture & Stock Enhancement in North China’s Sea,Ministry of Agriculture, Dalian Ocean University, Dalian 116023, Chinae-mail: yaqingchang@hotmail.com

123

Aquacult Int (2013) 21:699–708DOI 10.1007/s10499-012-9604-7

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 pro-

duction. 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. intermediusharvested 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. inter-medius 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 inter-

mittent 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 temper-

ature (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 noc-

turnal 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

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 con-

sumption 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.

0

10

20

30

40

50

60

1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61 63 65 67 69 71 73 75 77 79 81 83

Day

Wet

wei

ght o

f th

e ke

lp (

g)

Nocturnal feeding regimeDiurnal feeding regimeDaily intermittent regimeContinuous feeding regime

Fig. 1 Mean daily food consumption of large size sea urchins in different feeding regimes

Wet

wei

ght o

f th

e ke

lp (

g)

0

10

20

30

40

50

60

1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61 63 65 67 69 71 73 75 77 79 81 83

Day

Nocturnal feeding regimeDiurnal feeding regimeDaily intermittent regimeContinuous feeding regime

Fig. 2 Mean daily food consumption of medium size sea urchins in different feeding regimes

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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 con-

tinuously 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

Wet

wei

ght o

f th

e ke

lp (

g)

Day

0

10

20

30

40

50

60

1 3 5 7 9 11 13 15 17 19 21 23 25 27 29 31 33 35 37 39 41 43 45 47 49 51 53 55 57 59 61 63 65 67 69 71 73 75 77 79 81 83

Nocturnal feeding regimeDiurnal feeding regimeDaily intermittent regimeContinuous feeding regime

Fig. 3 Mean daily food consumption of small size sea urchins in different feeding regimes

3210

5

10

15

20

Dai

ly f

ood

cons

umpt

ion

(g)

Size class

Nocturnal feeding regimeDiurnal feeding regime

Daily intermittent feeding regime Continuous feeding regime

a a ab

x

x x

x

bc

ab a

c

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 differenceaccording to Duncan’s multiple comparisons

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0

5

10

15

20

25

0 1 2 3 4 5 6 7 8 9 10 11 12

Week

Bod

y w

eigh

t (g)

Nocturnal feeding regime in class 3 Diurnal feeding regime in class 3Daily intermittent regime in class 3 Continuous feeding regime in class 3Nocturnal feeding regime in class 2 Diurnal feeding regime in class 2Daily intermittent regime in class 2 Continuous feeding regime in class 2Nocturnal feeding regime in class 1 Diurnal feeding regime in class 1Daily intermittent regime in class 1 Continuous feeding regime in class 1

Fig. 5 Mean wet body weights of three size classes sea urchins in continuous and intermittent feedingregimes. Class 1: 30 mm; Class 2: 23 mm; Class 3: 14 mm

3210.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

4.0

αα

xx

aa

Gon

ad w

et w

eigh

t (g)

Size class

Nocturnal feeding regime

Diurnal feeding regime

Daily intermittent feeding regime

Continuous feeding regime

a

b

xx

α

β

Fig. 6 Gonad wet weight regimes (Mean ± SD, N = 15) of three size classes of sea urchins in continuousand 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

704 Aquacult Int (2013) 21:699–708

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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 chal-

lenge 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

Vaıtilingon 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

3210

3

6

9

12

15

18

xx

x

αα

Nocturnal feeding regime

Diurnal feeding regime

Daily intermittent feeding regime

Continuous feeding regime

Gon

ad in

dex

(%)

Size class

xa

aa

b

α

β

Fig. 7 Gonad index (Mean ± SD, N = 15) of three size classes of sea urchins in continuous andintermittent feeding regimes. Class 1: 30 mm; Class 2: 23 mm; Class 3: 14 mm. In each size class, differentletters mean significant difference according to Duncan’s multiple comparisons

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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 inter-

mittent 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 high-

lights 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 experi-

mental 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; Kankanen 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, Mc-

Carron 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 continu-

ously 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 phenom-

enon 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 sig-

nificantly affect growth of S. intermedius compared to continuous feeding; (4) diel inter-

mittent 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). Weare grateful to Prof. John Lawrence for providing many useful editorial suggestions.

References

Barnes D, Crook A (2001) Quantifying behavioural determinants of the coastal European sea-urchinParacentrotus lividus. Mar Bio 138:1205–1212

Buurma B, Diana J (1994) Effects of feeding frequency and handling on growth and mortality of culturedwalking catfish Clarias fuscus. J World Aquacul Soc 25:175–182

Carpenter RC (1984) Predator and population density control of homing behavior in the Caribbean echinoidDiadema antillarum Phillippi. Mar Bio 82:101–108

Chang Y, Ding J, Song J, Yang W (2004) Biology and aquaculture of sea cucumbers and sea urchins. OceanPress, Beijing

Cho SH, Lim YS, Lee JH, Lee JK, Park S, Lee SM (2003) Effects of feeding rate and feeding frequency onsurvival, growth, and body composition of Ayu post-larvae Plecoglossus altivelis. J World AquaculSoc 34:85–91

Dance C (1987) Patterns of activity of the sea urchin Paracentrotus lividus in the Bay of Port-Cros (Var,France, Mediterranean). Mar Ecol 8:131–142

Ding J, Chang Y, Wang C, Cao X (2007) Evaluation of the growth and heterosis of hybrids among threecommercially important sea urchins in China: Strongylocentrotus nudus, S. intermedius and Antho-cidaris crassispina. Aquaculture 272:273–280

Dobson SH, Holmes RM (1984) Compensatory growth in the rainbow trout, Salmo gairdneri Richardson.J Fish Biol 25:649–656

Ebling FJ, Hawkins AD, Kitching JA, Muntz L, Pratt VM (1966) The ecology of Lough Ine XVI. Predationand diurnal migration in the Paracentrotus community. J Anim Ecol 35:559–566

Fuji A (1967) Ecological studies on the growth and food consumption of Japanese common littoral seaurchin, Strongylocentrotus intermedius (A. Agassiz). Memoirs of the Faculty of Fisheries HokkaidoUniversity 15:83–160

James DW (2000) Diet, movement, and covering behavior of the sea urchin Toxopneustes roseus inrhodolith beds in the Gulf of California. Mexico Mar Biol 137:913–923

Aquacult Int (2013) 21:699–708 707

123

Jobling M, Koskela J (1996) Interindividual variations in feeding and growth in rainbow trout duringrestricted feeding and in a subsequent period of compensatory growth. J Fish Biol 49:658–667

Kankanen M, Pirhonen J (2009) The effect of intermittent feeding on feed intake and compensatory growthof whitefish Coregonus lavaretus L. Aquaculture 288:92–97

LaMontagne JM, Jackson LJ, Barclay RMR (2003) Compensatory growth responses of Potamogeton pec-tinatus to foraging by migrating trumpeter swans in spring stop over areas. Aquat Bot 76:235–244

Lawrence JM, Hughes-Games L (1972) The diurnal rhythm of feeding and passage of food through the gutof Diadema setosum (Echinodermata: Echinoidea). Isr J Zool 21:13–16

Lawrence JM, Plank LR, Lawrence AL (2003) The effect of feeding frequency on consumption of food,absorption efficiency, and gonad production in the sea urchin Lytechinus variegatus. Comp BiochemPhys A 134:69–75

Lin Q, Zhang D, Lin J (2009) Effects of light intensity, stocking density, feeding frequency and salinity onthe growth of sub-adult seahorses Hippocampus erectus Perry, 1810. Aquaculture 292:111–116

McCarron E, Burnell G, Mouzakitis G (2009) Growth assessment on three size classes of the purple seaurchin Paracentrotus lividus using continuous and intermittent feeding regimes. Aquaculture288:83–91

Minor MA, Scheibling RE (1997) Effects of food ration and feeding regime on growth and reproduction ofthe sea urchin Strongylocentrotus droebachiensis. Mar Biol 129:159–167

Nelson BV, Vance RR (1979) Diel foraging patterns of the sea urchin Centrostephanus coronatus as apredator avoidance strategy. Mar Biol 51:251–258

Quinton JC, Blake RW (1990) The effect of feed cycling and ration level on the compensatory growthresponse in rainbow trout, Oncorhynchus mykiss. J Fish Biol 37:33–41

Silva CR, Gomes LC, Brandao FR (2007) Effect of feeding rate and frequency on tambaqui (Colossomamacropomum) growth, production and feeding costs during the first growth phase in cages. Aqua-culture 264:135–139

Stefansson SO, Imsland AK, Handeland SO (2009) Food-deprivation, compensatory growth and hydro-mineral balance in Atlantic salmon (Salmo salar) post-smolts in sea water. Aquaculture 290:243–249

Thornton IWB (1956) Diurnal migration of the echinoid Diadema setosum. Brit J Anim Behav 4:143–146Tian X, Qin J (2003) A single phase of food deprivation provoked compensatory growth in barramundi

Lates calcarifer. Aquaculture 224:169–179Tuya F, Martin JA, Luque A (2004) Patterns of nocturnal movement of the long-spined sea urchin Diadema

antillarum (Philippi) in Gran Canaria (the Canary Islands, central East Atlantic Ocean). Helgoland MarRes 58:26–31

Vaıtilingon D, Rasolofonirina R, Jangoux M (2003) Feeding preferences, seasonal gut repletion indices, anddiel feeding patterns of the sea urchin Tripneustes gratilla (Echinodermata: Echinoidea) on a coastalhabitat off Toliara (Madagascar). Mar Biol 143:451–458

Wang Y, Kong LJ, Li K, Bureau DP (2007) Effects of feeding frequency and ration level on growth, feedutilization and nitrogen waste output of cuneate drum (Nibea miichthioides) reared in net pens.Aquaculture 271:350–356

Weatherley AH, Gill HS (1981) Recovery growth following periods of restricted rations and starvation inrainbow trout Salmo gairdneri Richardson. J Fish Biol 18:195–208

Yamamoto T, Shima T, Furuita H, Sugita T, Suzuki N (2007) Effects of feeding time, water temperature,feeding frequency and dietary composition on apparent nutrient digestibility in rainbow trout On-corhynchus mykiss and common carp Cyprinus carpio. Fisheries sci 73:161–170

Yoshida M (1966) Photosensitivity. In: Boolootian RA (ed) Physiology of echinoderms. IntersciencePublishers, New York, pp 435–464

708 Aquacult Int (2013) 21:699–708

123