DOI: 10.1111/are.

13492

ORIGINAL ARTICLE

Experimental rearing of the sea urchin Paracentrotus lividus

fed with discards of the lettuce Lactuca sativa in a sea-based
system

Salvatrice Vizzini1,2 | Giulia Visconti1 | Antonino Vaccaro1 | Antonio Mazzola1,2

1
Department of Earth and Marine Sciences,
University of Palermo, Palermo, Italy
2
CoNISMa, Roma, Italy
Correspondence
Salvatrice Vizzini, Department of Earth and
Marine Sciences, University of Palermo,
Palermo, Italy.
Email: salvatrice.vizzini@unipa.it
Funding information
INNOVAQUA Project; Flagship Project
RITMARE—Italian Research for the Sea
Abstract
Small-sized specimens (test diameter: 16.64
0.93 mm, mean
SE) of the sea
urchin Paracentrotus lividus were fed with fresh discards of the lettuce Lactuca sativa
during a 24-week experiment in a sea-based system. At the end of the experiment,
stock survival was high (88.8
6.6%). Sea urchin test diameter and total weight
grew by 35% and 56%, respectively, while gonad somatic index, after an initial
decrease, increased by 3.2%. Moreover, more than 90% of specimens achieved the
gonad colour that the market demands. These results support the exploitation of
L. sativa as the main ingredient in a manufactured diet for echinoculture of P. lividus.
Employing diets formulated with discard ingredients, combined with a low-cost sea-
based rearing system, could be a suitable approach for sustainable management of
echinoculture.

KEYWORDS
Echinoculture, gonad colour, gonad index, sea urchin roe

1 | INTRODUCTION gonads quantitatively and qualitatively speaking (Basuyaux & Blin,

In the Mediterranean region, roe of the sea urchin Paracentrotus livi-
dus (Lmk) is one of the most popular seafood delicacies (Barnes &
Crook, 2001; Byrne, 1990; Pais, Serra, Meloni, Saba & Ceccherelli,

gis, Pe
2012; Re
re
s & Gras, 1986). Although in Italy harvesting of this
species is regulated by a national law (D.M. 12/01/1995 in GU n.
20, 25/01/1995), which limits the harvesting period and number of
urchins collected per day, illegal fishery is practised throughout the
year to meet market demand, causing a progressive decline in natu-
ral populations (Gianguzza et al., 2006; Guidetti, 2004; Pais et al.,
2007).
Aquaculture production of sea urchins may represent a sustain-
able alternative to satisfy market demand, and at the same time pre-
serve natural populations. One of the main challenges
echinoculture to date is the formulation of a suitable diet to boost
production of gonads and obtain, in a commercially acceptable time
interval, high yields of gonads with optimal taste and colour. Notable
gaps still exist in the formulation of feeds for obtaining optimal
1998; Spirlet, Grosjean & Jangoux, 2000). Systems for mass rearing
of P. lividus are still not widely developed, although pilot-scale facili-
ties have been described (Grosjean, Spirlet, Gosselin, Vaitilingon &
Jangoux, 1998) and one company is active in Ireland (Dunmanus
Seafood Ltd). Moreover, the production of P. lividus in integrated
mariculture systems alongside both Atlantic salmon and blue mussel
culture facilities has been tested, with good results (Cook & Kelly,
2009; Kelly & Chamberlain, 2010).
The aim of obtaining a suitable diet and high-quality products
accords with the sustainable animal diets (StAnD) concept that inte-
grates the importance of protecting the environment, efficient use of
natural resources, socio-cultural benefits and ethical integrity and
sensitivity (Makkar & Ankers, 2014). In addition, it meets the current
of nutrition-based criteria for producing safe and economically viable
feed (Makkar & Ankers, 2014). The major challenges in the produc-
tion of diets for reared species are to reduce costs and environmen-
tal footprint without reducing product quantity, quality and value
(Thorarinsdottir, Jokumsen, Bjornsson & Torrissen, 2011). In most

Aquaculture Research. 2018;49:631–636. wileyonlinelibrary.com/journal/are © 2017 John Wiley & Sons Ltd | 631
632 | VIZZINI
cases, echinoculture makes use of expensive manufactured diets,
consisting of pellet formulated with high-cost ingredients, especially
when these are of animal origin (Hammer et al., 2012; McBride,
Price, Tom, Lawrence & Lawrence, 2004; McLaughlin & Kelly, 2001;
Mortensen, Siikavuopio & Raa, 2004; Pearce, Daggett & Robinson,
2002, 2003, 2004; Robinson & Colborne, 1997; Senaratna, Evans,
Southam & Tsvetnenko, 2005; Vidal, 2004; Watts, Boettger, McClin-
tock & Lawrence, 1998). Moreover, sea urchins are often fed on
other species (mainly macroalgae such as kelp and seaweed) har-
vested in marine environments, with detrimental ecological effects
(Daggett, Pearce, Tingley, Robinson & Chopin, 2005; Pearce et al.,
2002). Sea urchins fed on a manufactured diet of vegetables and
animal proteins showed higher gonadic growth than those given a
natural or vegetal manufactured diet (Carrier, Eddy & Redmond,
2017; Fernandez & Boudouresque, 2000; Fernandez & Pergent,
1998; Schlosser, Lupatsch, Lawrence, Lawrence & Shpigel, 2005;
Shpigel, McBride, Marciano, Ron & Ben-Amotz, 2005; Spirlet, Gros-
jean & Jangoux, 2001).
Recently, attention has focused on the exploitation of constantly -
available land-based vegetables, in the form of agricultural discards, as
, Vaccaro & Maz-
a dietary component for P. lividus (Vizzini, Micciche
zola, 2015). This represents a potentially successful way to decrease
the harvesting pressure on marine organisms generally included in sea
urchin diets (i.e. macroalgae and fish proteins and oils). In a laboratory
experiment, among different vegetable discards provided to P. lividus
adults, Lactuca sativa (L) gave the best results in terms of gonad weight
and colour, and gonadic index (Vizzini et al., 2015), although gonad
yield was far below values reached using diets rich in animal proteins
(Pearce et al., 2002; Phillips et al., 2010). However, this result pro-
vided evidence that L. sativa may be included in low-cost and environ-
mentally sustainable feedstuff for sea urchin aquaculture.
Following this promising result carried out on adults (>30 mm) in
the laboratory, we carried out a in situ-feeding experiment to test
the use of lettuce discards as a diet for earlier life stages (<30 mm)
of P. lividus, to investigate its exploitation and its effectiveness in
improving gonad yield and colour. The experiment was performed in
a sea-based site for the initial evaluation of the feasibility of sea
urchin rearing in in situ conditions.
2 | MATERIALS AND METHODS
Small-sized Paracentrotus lividus (16.64
0.93 mm, mean
SE) were
obtained from “Dunmanus Seafoods Ltd” (Ireland) and transported to
Sicily (Italy) in refrigerated containers in May 2011. Upon arrival at the
fish farm “Azienda Ittica S. Giorgio srl” (southern Sicily; 37°50 12.82″N–
13°560 28.69″E), the sea urchins were placed in 9 plastic cages
(600 9 500 9 200 mm; internal surface area = 1.20 m2), 200 speci-
mens in each cage. Cages were kept at a depth of 2 m, hanging from a
60 m linear rope. The rope was kept at the water surface with buoys
and the rearing system moored to the sea bottom. Sea urchins placed
in the cages were levelled off for nutritional status; they were kept
ET AL.
starved for 2 weeks prior to the feeding experiment as suggested by
Pearce et al. (2002, 2004) and McBride et al. (2004).
The experiment started on 9 June 2011 and ran until 24 Novem-
ber 2011, for a total of 24 weeks. Fresh leaves of L. sativa obtained
from unprocessed agricultural discards (fresh outermost leaves) were
provided two times per week throughout all the experiment. Chemical
composition of L. sativa in terms of protein, lipid and carbohydrate
content was analysed throughout the experiment according to Har-
tree (1972) modified by Rice (1982), Marsh and Wenstein (1966) and
Gerchacov and Hachter (1972), respectively, and expressed as %.
Before feed provision, cages were always cleaned and faeces
and any leftover feed removed when necessary.
At the end of the experiment, percentage survival rate (S, %) was
calculated as:
S ¼ ðSf =Si Þ  100 (1)
where sf is the number of surviving specimens at the end of the
experiment and si is the initial number of sea urchins.
At the beginning of the experiment (T0) and at three further
dates 50 days apart (T1, T2, and T3), test diameter (TD) was mea-
sured in 50 sea urchins per cage using a Vernier calliper (
0.1 mm).
On the same dates, three sea urchins were randomly collected from
each cage and total wet weight (TW) and gonad wet weight (GW)
measured on a Sartorius electronic balance (Genius Me
235S,
0.01 g). Gonad somatic index (GSI, %) was calculated as:
GSI ¼ ðGW=TWÞ  100 (2)
The colour quality of the sea urchin gonads was assessed at the
four sampling times (T0, T1, T2 and T3) according to Shpigel et al.
(2005) and allocated to one of three categories (E: excellent, A:
acceptable, I: inadequate) following Symonds, Kelly, Suckling and
Young (2009). The same observer used a Pantoneâ colour standards
chart (Colour Formula Guide 1000, 1991) in natural daylight to
assign each specimen to a single category.
During the entire experiment, temperature and dissolved oxygen
were recorded daily using a multi-probe (Hydrolab-DS5).
ANOVAs were used to test for differences in TD (repeated
ANOVA), TW, GW and GSI among sampling times (Factor Time, four
levels: T0, T1, T2 and T3; nine replicates: 1 cage = 1 replicate). Nor-
mality and homogeneity of variance were tested using Tukey and
Cochran’s test prior to analysis of variance. Where significant p-
values were obtained, Tukey’s post hoc comparison test was used to
evaluate pair-wise means. All analyses were carried out with STATIS-
TICA.10 software.
3 | RESULTS
Throughout the experiment, seawater temperature ranged between
19.15
0.95 °C (mean
SD) in November and 24.71
1.61 °C in
August, while dissolved oxygen was between 5.02
0.82 mg/L in
September and 7.03
0.70 mg/L in June (Figure 1).
VIZZINI ET AL. | 633

29 9

8
27

Dissolved Oxygen (mg/L)

7
25
Temperature (°C)

6
23
5

21 4

3
19
2
17
1

15 0
09/06/2011
13/06/2011
17/06/2011
21/06/2011
25/06/2011
29/06/2011
03/07/2011
07/07/2011
11/07/2011
15/07/2011
19/07/2011
23/07/2011
27/07/2011
31/07/2011
04/08/2011
07/08/2011
11/08/2011
15/08/2011
19/08/2011
23/08/2011
27/08/2011
31/08/2011
04/09/2011
08/09/2011
12/09/2011
16/09/2011
20/09/2011
24/09/2011
28/09/2011
02/10/2011
06/10/2011
10/10/2011
14/10/2011
18/10/2011
22/10/2011
26/10/2011
30/10/2011
03/11/2011
07/11/2011
11/11/2011
15/11/2011
19/11/2011
23/11/2011
T0 T1 T2 T3
Time
Temperature (°C) Dissolved oxygen (mg/L)
FIGURE 1 Seawater temperature (°C) and dissolved oxygen (mg/L) recorded during the feeding experiment (June–November 2011)

Chemical composition of L. sativa had low variability throughout
the experiment, being proteins the most abundant
(18.7
1.4%) followed by carbohydrates (12.1
2.0%) and lipids
(8.6
0.47%).
At the end of the experiment (T3), the percentage of surviving
sea urchins was 88.8
6.6%. Test diameter (TD) and total wet
weight (TW) showed a gradual, significant increase throughout the
experiment (Figure 2; Table 1), achieving a gain of 35% and 56%,
respectively, at the end of the experiment.
Gonad wet weight increased gradually and significantly during
the experiment from 0.005
0.008 g at T0 to 0.193
0.038 g at
T3 (Table 1; Figure 3). Contrarily, a decrease in GSI was recorded
from T0 to T2, followed by an increment at the end of the experi-
ment.
At the beginning of the experiment, the three colour categories
fraction (E: excellent, A: acceptable, I: inadequate) were found in comparable
percentages (E = 29.62%; A = 33.33%; I = 37.04%). During the
experiment categories E and A, which are those in demand on the
market, increased and exceeded 90% at T3 (Figure 4).
4 | DISCUSSION
Fresh leaves of Lactuca sativa obtained from agricultural discards
were employed to feed small sea urchins during a 24-week feeding
experiment, resulting in somatic growth, gonad development and
marketable gonad colour. The results highlighted the suitability of a
simple, low-cost sea-based rearing system for sea urchin aquaculture.

24 5.5
Test diameter (mm) Total wet weight (g)
23 5

22
4.5
21
Total wet weight (g)
Test diameter (mm)

4
20
3.5
19
3
18
2.5
17

16 2
F I G U R E 2 Test diameter (mm,
mean
SE) and total wet weight (g, 15 1.5
mean
SE) of sea urchins during the T0 T1 T2 T3
feeding experiment Time
634 | VIZZINI ET AL.

T A B L E 1 ANOVA results for the effects of the factor Time on 100%

test diameter (repeated ANOVA; n=50), total wet weight (n = 9),
gonad wet weight (n = 9) and gonad somatic index (n = 9) of 80%
Paracentrotus lividus during the feeding experiment
df MS F-value p-value Tukey’s test 60%

Test diameter (TD)

40%
Time 3 66.69 119.52 <.001 T0 < T1 < T2 < T3
Total wet weight (TW)
20%
Time 3 50.03 30.34 <.001 T0 < T1 < T2 < T3
Gonad wet weight (GW) 0%
T0 T1 T2 T3
Time 3 0.10 6.87 <.001 T0 < T1 < T2 < T3
Time
Gonad somatic index (GSI)
Excellent Acceptable Inadequate
Time 3 13.55 3.22 <.05 T2 < T1 < T0 < T3
F I G U R E 4 Gonad colour quality of Paracentrotus lividus during
Tukey’s post hoc tests indicate significant pair-wise differences.
the feeding experiment (E, excellent; A, acceptable; I, inadequate.)

Indeed, the survival rate of P. lividus fed with L. sativa was very high,
and comparable with previous feeding experiments using similar-
sized specimens (10–19 mm) (Cook & Kelly, 2009; McCarron, Bur-
nell, Kerry & Mouzakitis, 2010; Spirlet et al., 2000).
Environmental variables are key factors for sea urchin growth,
with different ranges of variation having different effects depend-
ing on sea urchin size. As an example, temperature is known to
either limit or boost growth in sea urchins of different size
classes. Higher temperatures (especially between 19°C and 24 °C)
enhance growth in small sea urchins (< 20 mm), while colder tem-
peratures (15°C) are more favourable to larger ones (Basuyaux &
Blin, 1998). Our results confirm that small-sized sea urchins expe-
riencing a range of seawater temperatures of between 19°C and
24°C underwent high growth rates. In addition, in agreement with
previous findings (McCarron, Burnell & Mouzakitis, 2009), the ad li-
bitum feeding regime adopted for small-sized sea urchins was
shown to be effective, with a marked increase in their somatic
growth. Evidence from other sea urchin species shows that a con-
tinuous feeding regime produced a significantly higher increase in
gonad somatic index than an intermittent provision of food (Lawr-
ence, Plank & Lawrence, 2003; Minor & Scheibling, 1997; Thomp-
son, 1983).
Generally, small sea urchins (10–19 mm) are characterized by fas-
ter somatic growth in test diameter and total weight than medium-
sized ones (20–29 mm) (Barker, Keogh, Lawrence & Lawrence, 1998;
McCarron et al., 2009). Accordingly, in this study a clear increase in
test diameter and total weight was recorded in the first part of the
experiment (100 days) when the temperature was favourable to
small specimens and they allocated more energy to somatic growth
than to gonadic development, as suggested by the decrease in gonad
somatic index. Successively, sea urchins showed a clear increase in
gonad yield and index, achieving conditions similar to those of adults
at the end of the experiment. Finally, as regards the qualitative fea-
tures, at the end of the experiment more than 90% of sea urchins
had a colour in the excellent and acceptable categories. This result
confirms a previous study on adult sea urchins fed with L. sativa in
laboratory conditions, which noticeably improved gonad colour qual-
ity (Vizzini et al., 2015), due to the high carotenoid concentration in
lettuce (Caldwell & Britz, 2006).
Although a stock of adult sea urchins (22.60
0.34 mm) with a
good, marketable gonad colour was obtained at the end of the
experiment, the overall gonadic yields and index obtained were not
satisfactory in terms of marketability. This corroborates previous
findings (Vizzini et al., 2015), confirming that L. sativa cannot be

4
Gonad somatic index (%) Gonad wet weight (g)
0.40
Gonad somatic index (%)

3
Gonad wet weight (g)

0.32

0.24
2

0.16

1
0.08
F I G U R E 3 Gonad features of sea
urchins: gonad somatic index (%,
0 0.00
T0 T1 T2 T3 mean
SE) and gonad wet weight (g,
Time mean
SE) during the feeding experiment
VIZZINI ET AL.
used as the sole diet for sea urchins. It may, however, be included
in a more balanced diet with a higher protein content to maintain
organoleptic characteristics and, in particular, the colour of the
gonads found in wild specimens. A new feedstuff, which includes a
large proportion of lettuce among other ingredients, has been for-
mulated and tested through both laboratory and in situ-trials (S.
Vizzini, G. Visconti, A. Vaccaro, A. Mazzola, in preparation). The
advantages of exploiting unprocessed agricultural discards in a pre-
pared diet are numerous and of great relevance from both the
economic and environmental points of view (Vizzini et al., 2015).
Indeed, agricultural discards are available all year round, are rich in
carotenoids (Caldwell & Britz, 2006) and easy to store. This issue
meets the StAnD concept of promoting sustainability in animal
production methods and products, embracing the socio-cultural and
environmental aspects (Brown, Mitchell & Beresford, 2004; FAO,
2011; Makkar & Ankers, 2014). Access to available, safe and
economically convenient feed ingredients is becoming one of the
most important challenges for strengthening the aquaculture indus-
try and developing more sustainable production (Thorarinsdottir
et al., 2011).
In conclusion, the results of this study are encouraging for the
exploitation of agricultural discards such as L. sativa in the formula-
tion of new sustainable diets for herbivorous and omnivorous spe-
cies such as sea urchins. Moreover, the positive response of sea
urchins in terms of growth and survival suggests that sea-based sys-
tems are a promising area for echinoculture. The rearing of sea urch-
ins may represent an additional activity and income for farmers as
well as guaranteeing a good quality product.
ACKNOWLEDGMENTS
This research was supported by INNOVAQUA Project
(PON02_00451_3362185) and Flagship Project RITMARE—Italian
Research for the Sea—both funded by the Italian Ministry of Educa-
tion, University, and Research. We are grateful to Alessandro Galioto
and “Azienda Ittica San Giorgio” of Licata (Sicily, Italy) for the oppor-
tunity to carry out the experiment in the fish farm and the logistical
 for support in the early stages of this study;
support; Luca Micciche
P. Scariano and A. Savona for assistance with experiments.
ORCID
Salvatrice Vizzini http://orcid.org/0000-0002-7127-7555
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How to cite this article: Vizzini S, Visconti G, Vaccaro A,
Mazzola A. Experimental rearing of the sea urchin
Paracentrotus lividus fed with discards of the lettuce Lactuca
sativa in a sea-based system. Aquac Res. 2018;49:631–636.
https://doi.org/10.1111/are.13492