Cuttlefish Culture – State of the Art and Future Trends

Abstract

The present article provides an overview of cuttlefish culture, its current state of art, and future trends. Present cuttlefish culture related research, recently developed technologies (like culture systems, maternity/nursery and juve-nile and adult proceedings) are described. Finally, current problems and prospects for future research are discussed. The increase of the human population has led to a greater demand for fishery products, and there-fore intensified diversification of fish catches. Al-though there has been a decline in fish consump-tion and production in developed countries, global fish consumption has doubled since the beginning of the 1970's (Delgado et al. 2003). During this pe-riod, aquaculture production followed this increase and has risen from 6 to 30% of total fishery pro-duction (Delgado et al. 2003). Landings from worldwide aquaculture increased rapidly in the last decade, to approximately 10–15% per year. Ac-cording to FAO (2002), total aquaculture in 1996 was 26.7 million tons, and in 2001 increased to 37.5 million tons. Rapid growth was due to the combined effects of an increasing world popula-tion, decreasing catches from traditional fisheries (Caddy & Griffiths 1995), and changing consumer preferences in developed countries (Lem & Shehadeh 1997, Tacon 1997). Ultimately, this was reflected in world fish catches, including cephalo-pods. Between 1950 and 1970, cephalopod land-ings increased from 20 million tons (Mt) to 70 Mt (Amaratunga 1983). At present, cephalopod spe-cies represent an important seafood supply for hu-man consumption worldwide. According to FAO (FAO 2002, 2004), cephalopods contribute approx-imately 14% of the world fisheries. The fast de-cline of the worldwide fish stocks, as well as the technological advances over the last 15 years, and decreased prices of commonly cultured species, makes the development of technology for rearing and culture of new species profitable, indeed nec-essary (FAO 2004). High commercial value of the cephalopods, particularly in the Asian and Medi-terranean markets, and some aspects of cephalopod biology and physiology make them good candi-dates for aquaculture (Kunisaki 2000, Ruíz-Cappillas et al. 2002). It is also known that cephalopod consumption is increasing in the American market. Thus, an overall increase in world cephalopod consumption is predicted, since an open market with high growing potential is fore-seen in the future. These facts indicate that increas-ing efforts to start semi-intensive and intensive cul-ture of cephalopod species like the European cuttlefish (Sepia officinalis) and the common octopus (Octopus vulgaris) should be made. The top five countries in fish consumption (above 40 kg/head/year; Iceland, Japan, Portugal, Norway and Spain) (European Communities 2004) are also those searching for greater diversification of edible fish species. In these countries, there is an existing market for cephalopod catches. In fact, Japan is the principal consumer of cephalopods, with cuttlefish being the most appreciated and val-ued species (Boucaud-Camou 1990). Therefore, cephalopod production for human consumption in these countries is advantageous, since their short life cycles and fast growth rates imply lower pro-duction periods and associated costs. Also, the non-edible parts of cephalopods, which make up approximately 30% of the animal, can be used for fish meal or bait. According to Kreuzer (1984), the conversion of non-edible parts into products of higher value would also be economically beneficial. In the case of cuttlefish, there is potential for further exploitation, particularly with regard to the production of undersized individuals allowed by DGPA (Portuguese Fisheries and Agriculture De-partment), which would reduce the impact of ille-gal catches on this species from the natural envi-ronment. For example, the smallest individuals are considered a delicacy and have the highest com-mercial value in Portugal. The main reason for this increasing demand is that cephalopods in general

Full text

CUTTLEFISH CULTURE – STATE OF THE ART
AND FUTURE TRENDS
A. V. SYKES, P. M. DOMINGUES, M. CORREIA, J. P. ANDRADE
C.C.Mar – F.C.M.A.– Universidade do Algarve, Campus de Gambelas 8000, 810 Faro, Portugal
* Corresponding author’s email: asykes@ualg.pt
COMMON CUTTLEFISH
CULTURE TECHNOLOGY
SEPIA OFFICINALIS
REVIEW
ABSTRACT. – The present article provides an overview of cuttlefish culture, its
current state of art, and future trends. Present cuttlefish culture related research,
recently developed technologies (like culture systems, maternity/nursery and juve-
nile and adult proceedings) are described. Finally, current problems and prospects
for future research are discussed.
GENERAL OVERVIEW AND PAST
RESEARCH
Fisheries and Human Consumption
The increase of the human population has led to
a greater demand for fishery products, and there-
fore intensified diversification of fish catches. Al-
though there has been a decline in fish consump-
tion and production in developed countries, global
fish consumption has doubled since the beginning
of the 1970’s (Delgado et al. 2003). During this pe-
riod, aquaculture production followed this increase
and has risen from 6 to 30% of total fishery pro-
duction (Delgado et al. 2003). Landings from
worldwide aquaculture increased rapidly in the last
decade, to approximately 10–15% per year. Ac-
cording to FAO (2002), total aquaculture in 1996
was 26.7 million tons, and in 2001 increased to
37.5 million tons. Rapid growth was due to the
combined effects of an increasing world popula-
tion, decreasing catches from traditional fisheries
(Caddy & Griffiths 1995), and changing consumer
preferences in developed countries (Lem &
Shehadeh 1997, Tacon 1997). Ultimately, this was
reflected in world fish catches, including cephalo-
pods. Between 1950 and 1970, cephalopod land-
ings increased from 20 million tons (Mt) to 70 Mt
(Amaratunga 1983). At present, cephalopod spe-
cies represent an important seafood supply for hu-
man consumption worldwide. According to FAO
(FAO 2002, 2004), cephalopods contribute approx-
imately 14% of the world fisheries. The fast de-
cline of the worldwide fish stocks, as well as the
technological advances over the last 15 years, and
decreased prices of commonly cultured species,
makes the development of technology for rearing
and culture of new species profitable, indeed nec-
essary (FAO 2004). High commercial value of the
cephalopods, particularly in the Asian and Medi-
terranean markets, and some aspects of cephalopod
biology and physiology make them good candi-
dates for aquaculture (Kunisaki 2000, Ruíz-
Cappillas et al. 2002). It is also known that
cephalopod consumption is increasing in the
American market. Thus, an overall increase in
world cephalopod consumption is predicted, since
an open market with high growing potential is fore-
seen in the future. These facts indicate that increas-
ing efforts to start semi-intensive and intensive cul-
ture of cephalopod species like the European
cuttlefish (Sepia officinalis) and the common
octopus (Octopus vulgaris) should be made.
The top five countries in fish consumption
(above 40 kg/head/year; Iceland, Japan, Portugal,
Norway and Spain) (European Communities 2004)
are also those searching for greater diversification
of edible fish species. In these countries, there is
an existing market for cephalopod catches. In fact,
Japan is the principal consumer of cephalopods,
with cuttlefish being the most appreciated and val-
ued species (Boucaud-Camou 1990). Therefore,
cephalopod production for human consumption in
these countries is advantageous, since their short
life cycles and fast growth rates imply lower pro-
duction periods and associated costs. Also, the
non-edible parts of cephalopods, which make up
approximately 30% of the animal, can be used for
fish meal or bait. According to Kreuzer (1984), the
conversion of non-edible parts into products of
higher value would also be economically beneficial.
In the case of cuttlefish, there is potential for
further exploitation, particularly with regard to the
production of undersized individuals allowed by
DGPA (Portuguese Fisheries and Agriculture De-
partment), which would reduce the impact of ille-
gal catches on this species from the natural envi-
ronment. For example, the smallest individuals are
considered a delicacy and have the highest com-
mercial value in Portugal. The main reason for this
increasing demand is that cephalopods in general
VIE ET MILIEU – LIFE & ENVIRONMENT, 2006, 56 (2) : 129-137 The cuttle Sepia officinalis
(N. Koueta, J.P. Andrade, S. v. Boletzky, eds)

and cuttlefish in particular, are a good source of
protein and essential lipids (Sinanoglou &
Miniadis-Meimaroglou 2000). According to
Boucaud-Camou (1990), cuttlefish is composed
mainly of water (81%) and protein (16.1%); it has
no carbohydrates and less than 1% lipids. It is also
a source of mineral salts and vitamins, and is
highly digestible. Its nutritional profile, as a high
protein and EPA/DHA lipid source, makes it one of
the most suitable and healthy forms of human food.
Cephalopods can be consumed in a variety of
forms: eaten raw as sashimi or sushi, cooked as
tempura or deep-fried, boiled as nimono,orpro
-
cessed into delicacies like surume (dried squid),
smoked squid, and saki-ika (shredded dried squid)
(Kunisaki 2000).
The European cuttlefish have been reared in ex-
tensive aquaculture for a number of years. Eggs are
collected and left in ponds for 3 months during
spring-summer, after which grown animals are cap-
tured and sold for human consumption. According
to DGPA data, until 1996, this production did not
exceed 1 ton.year-1 of cuttlefish biomass produced.
According to Rodger & Davies (2000), Tunisia has
also been producing S. officinalis since 1990. Nev-
ertheless, it must be noted that there is a lack of ac-
curate data on this type of production, since most
of these captures are not declared.
Culture related research until present
The introduction of a new species in aquaculture
requires a series of preliminary studies related to
the biology and the ecology of the species. These
studies can be performed in the wild or in the labo-
ratory. For the cuttlefish, both approaches were
conducted simultaneously and allowed not only the
culture technology to be developed but also the
knowledge related to local stock dynamics.
The first reports on experimental culture of
cephalopods are dated from the 1960’s, by the Ko-
rean and Japanese on species of the Sepiidae fam-
ily. These pioneer studies by Choe & Ohshima
(1963) and Choe (1966) were then followed and
complemented by Richard (1971) at the end of the
1960’s.
Richard (1971), Pascual (1978) and Boletzky
(1979) were among the first researchers who suc-
ceeded in culturing European cuttlefish in the labo-
ratory for one or more consecutive generations.
From these works, essential information on growth
and feeding under different culture conditions was
made available. Richard (1971) extended data re-
garding various aspects of culture, but also in-
cluded data on the population inhabiting the
English Channel. Boucaud-Camou (1973) and
Boucaud-Camou & Péquignat (1973) studied the
digestive apparatus and its biochemical processes,
and Yim (1978) addressed the development of the
digestive gland in the post-embryonic phase.
From 1980 onwards, research concerning the
possibility of using cuttlefish as a candidate spe-
cies for aquaculture rapidly expanded. Initial ex-
periments utilizing this species in coastal lagoons
were employed by Italians (see Palmegiano &
Sequi 1984, for a review) and Portuguese
(Gonçalves 1989, Coelho & Martins 1991).
Other contributions on feeding and digestion
were made by Boucaud-Camou et al. (1985),
Nixon (1985), and Guerra et al. (1988); on fecun-
dity by Boletzky (1987); and alternative prey items
by DeRusha et al. (1989).
A review on the laboratory maintenance, rear-
ing, and culture of cephalopod molluscs was pre-
sented by Boletzy & Hanlon (1983). Forsythe et al.
(1987) published the first synopsis of cephalopod
pathology in captivity. Boletzky (1983) also ad-
dressed the biology and ecology of S. officinalis,
while a review on the early stages, life cycle pro-
cesses, trophic relations, and exploitation of cepha-
lopods in general can be found in Boyle (1987). In
the 1990’s, further information was published on
rearing, culture and production of the European
cuttlefish (Forsythe et al. 1991, 1994, Loi &
Tublitz 1998, Warnke 1994).
The first reports on the use of pellet diets and
surimi in cephalopods (Lee et al. 1991) and espe-
cially cuttlefish (Castro 1991, Castro & Lee 1994,
Castro et al. 1993) demonstrated poor results in
growth and survival (e.g. 67.5% and 22.5% sur-
vival rates for pellets and surimi, respectively).
Use of artificial diets promoted cannibalism. An
approach to the nutritional requirements of cepha-
lopods by Lee (1994) revealed high amino acid
(AA) metabolism and the importance of protein/en-
ergy ratio. Complementary data were published re-
garding nutritional characterization of free l-amino
acids (D’Aniello et al. 1995) and lipid changes
during starvation (Castro et al. 1992).
Several articles regarding social and sexual be-
haviour (Adamo & Hanlon 1996, Boal 1996, 1997,
Boal & Marsh 1998, Hanlon et al. 1999) and
crowding (Boal et al. 1999) under culture condi-
tions contributed to increased knowledge of the
sexual behaviour of the cuttlefish in captivity and
spawning methodologies. Furthermore, Hanlon &
Forsythe (1990a, 1990b) described cephalopod dis-
eases, while Forsythe et al. (1990) published a
formulary for disease treatment.
Contributions to development of artificial sur-
faces for egg deposition and collection (Blanc &
Daguzan 1998) and the influence of temperature
(Bouchaud & Daguzan 1990, Bouchaud & Galois
1990), photoperiodicity (Paulij et al. 1991), and
energy consumption (Bouchaud 1991) during em-
bryonic development were published. A report on
the postembryonic predatory behaviour and its
130 A.V. SYKES, P.M. DOMINGUES, M. CORREIA, J.P. ANDRADE

relation to the maturation of the brain was pub-
lished by Dickel et al. (1997).
During recent years, the amount of published in-
formation on cephalopod and especially cuttlefish
culture steadily increased. Growth (IGR) and feed-
ing rates (FR) in hatchlings were studied by Koueta
& Boucaud-Camou (2001), while Domingues et al.
(2001a) extended this knowledge by culturing
hatchlings at the upper end of the biological tem-
perature (30ºC) and salinity range (37±3‰) with
good results. Grigoriou & Richardson (2004) pro-
vided new data on IGR and FR from cultured popu-
lations from the North Atlantic. Domingues et al.
(2002) also studied the effects of temperature in
the life cycle of cuttlefish with respect to growth,
extension of the cycle, and several reproductive as-
pects, while Boyle et al. (2001) described a model
system for partitioning environmental and genetic
effects on development and hatching of cephalopod
eggs. All these reports support the hypothesis of
the existence of different populations, thus
enhancing the probability that sub-species exist.
Several papers were also published regarding
the use of live and dead feeds for hatchlings
(Domingues et al. 2001b, Fuentes & Iglesias 2001,
Koueta et al. 2002; Perrin et al. 2004) and juve-
niles (Domingues et al. 2003b, 2004). Moreover,
Perrin et al. (2004) continued the work on diges-
tive enzymes, but related to alternative feeding of
hatchlings. Culture densities/crowding in hatch-
lings, juveniles, and adults and throughout the life
cycle was studied by Correia et al. (2005),
Domingues et al. (2003a), Forsythe et al. (2002)
and Sykes et al. (2003). The latter authors also
studied the effects of using sand in hatchling tanks
on growth and mortality of newly hatched individ-
uals of cuttlefish. Hunting behaviour and prey pref-
erence were addressed by Cole & Adamo (2005)
and Darmaillac et al. (2004), respectively.
STATE OF THE ART OF CUTTLEFISH
CULTURE AND ASSOCIATED
TECHNOLOGY
All technology described below has allowed cut-
tlefish culture at the University of the Algarve for
the last 6 years and its use in a first RTD contract
with an aquaculture enterprise. Currently, facilities
have been utilized as hatchery and grow out loca-
tions, while the company is conducting grow out
experiments to determine the viability of introduc-
ing the species as a new product.
Hatchery Technology
Spawners
Spawners should be captured from the wild
and/or selected from the most fit juvenile individu-
als cultured, which will be those displaying no dis-
ease or skin damage, and achieving the best
growth. After capture and/or selection, animals
should be conditioned in 2000-10000 l round
shaped tanks of a flow-through system. These
tanks should have a bumper system (Hanley et al.
1999) or large soft-plastic wall pools should be
used. Tanks should also be placed in a low distur-
bance zone inside the hatchery. Large bottom areas
should be used, and density should be low (Correia
et al. 2005, Sykes et al. unpublished results).
Eggs
Eggs can be obtained either by collection from
the wild, possibly using artificial surfaces for eggs
designed by Blanc & Daguzan (1998), or by repro-
duction in captivity. Preferably, eggs should be col-
lected in the laboratory rather than from the wild,
since there will be an advantage in knowing spawn
date and establishing correct incubation condi-
tions. Collection in the laboratory should be made
using a plastic rectangular supportive net (1 cm2
holes), suspended inside the spawners tank. This
net should be checked daily, and if eggs are pres-
ent, they should be carefully removed (since
freshly laid eggs are very soft and gelatinous) and
individualized. Subsequently, eggs should be
counted and weighed (50%, if n<100 or 30% if
n>100). Also, eggs should be separated according
to shape and colour. Black oval eggs are consid-
ered to be viable while eggs of any other shape
should be discarded.
Embryonic development should be completed in
bowl-shaped tanks with clean natural seawater. At
this phase, type of seawater system (open, closed
or semi-closed) can be used as long as it provides
clean water (with low concentrations of ammonia,
nitrites, and nitrates). Nevertheless, the use of
flow-through (open) seawater systems is advisable.
Tank setup should be as follows: 2 airlifts on the
side walls of the tank, and also medium to strong
aeration from the middle of the tank produced by a
wood air bubbler. This procedure ensures a maxi-
mization of hatching efficiency (creating an oxy-
gen-enriched environment), to allow hatchlings to
have a bottom where they may settle before being
removed for experiments or hatchling culture
tanks. It also keeps eggs moving in an elliptical
fashion, thus preventing necrosis by either lack of
oxygen or fungal/bacterial growth (originated by
no movement at all). To ensure normal hatching,
all physical parameters should be kept at a constant
level, including temperature, salinity, pH, nitroge-
nous compounds, daily photoperiod and light in-
tensity (Hanlon 1990, Forsythe et al. 1991). Ac-
cording to Boletzky (1983), water maintenance
limits for the species are as follows: between 9-
30ºC of temperature, 25-38‰ salinity, ammonia,
nitrites below 0.1mg/l and nitrates below 80mg/l.
REVIEW ON THE CULTURE OF SEPIA OFFICINALIS 131

Light intensity should be lower than 200 lux at the
top of the water column of the hatching tank, and
photoperiod should resemble natural conditions in
spring. A maximum number of 2000 eggs, col-
lected during 5-7 days, can be incubated in a 250 l
tank using this setup. For tanks using higher vol-
umes, the number of eggs still must be determined.
After being placed in the tank, disturbance of the
eggs should be avoided in order to prevent prema-
ture hatching that may result in mass mortality.
Embryonic development is temperature dependant,
but without any linear correlation (Richard 1971,
Sykes et al. unpubl results). Due to the fact that
temperature varies in different geographical areas,
it is suggested that temperature should resemble lo-
cal spring to summer conditions in the culture fa-
cility. This means that cuttlefish eggs from the
Mediterranean and South Portugal should be incu-
bated at temperatures between 18-25ºC (at these
temperatures hatching will occur 30-25 days after
being laid, respectively). Length of time to hatch-
ing can double when temperatures fall to 15ºC (60
days) and hatching will not occur below 12ºC.
Cuttlefish eggs from the North Atlantic are usually
big (they are laid by bigger females) and take
longer to hatch at the same temperatures (15ºC =
87 days)(see Richard 1971 or Boletzky, 1983 for
hatching table and graphics).
Hatchlings
After hatching in bowl-shaped tanks, hatchlings
will settle on the bottom of the tank. In this phase,
floating egg cases should be removed daily. Eggs
that do not hatch in the following 10 days should
be removed and considered non viable. The 250 l
tank used for egg incubation will now function as a
grow-out tank for the hatchling stage during the
next 30 DAH. Depending on the size of the eggs,
hatchling mean weight can vary between
0.233±0.050g (English Channel) or 0.090±0.030g
(South Portugal). Densities (500 hatchlings) and
minimal bottom areas (600 cm2) should be taken
into account (Sykes et al. 2003). For instance, a
250 l tank will only suffice for 2000 hatchlings for
about 15 days (T= 22.5±2.5ºC). After that, hatch-
lings are separated into 2 similar 250 l tanks (1000
hatchlings each).
Live food should be supplied ad libitum and wa-
ter quality must be similar to that of the egg stage.
At this phase, growth and feeding rates are the
highest of the whole life cycle, but they are still
temperature dependant.
Until now, high growth rates and low mortality
have been obtained by feeding live mysid shrimp
during the first 10 to 20 days of the life cycle
(Domingues et al. 2001b, 2001c, Koueta et al.
2002). Nevertheless, culture thorugh all phases of
the cuttlefish life cycle has been accomplished by
Sykes (2003) using a diet exclusively based on live
grass shrimp (P. varians). The effects of a single
prey diet are similar to those of using more than
one prey species (Sykes et al. unpubl results). The
use of a sole prey species for cuttlefish culture
drastically reduces costs associated with mysid
shrimp production or catching them from the wild,
and solves the problem of low mysid fecundity
(Domingues et al. 1998, Domingues et al. 2000),
which is considered a bottleneck in the first stage
culture of the species.
Grow out of juveniles and adult stages
After being reared for the first 20-30 DAH in the
250 l tanks, cuttlefish hatchlings should have at-
tained a mean weight of 5g; they are now juveniles,
ready for a transfer to a larger bottom area tank.
This new tank may be a saline pond, research fiber
or plastic tank. At this time, new spawners should
be selected from fast growers. Spawners will now
remain in the hatchery facilities, and those that are
grown and sold should be conditioned to outside
tanks. Nevertheless, densities (120 juveniles) and
minimal bottom areas (1100 cm2) should be taken
into account (Sykes et al. 2003). Since there is no
surimi diet or a dry pellet known to generate simi-
lar growth and survival, live or dead shrimp should
be used to accomplish this stage. If the individuals
are to be cultured in ponds, then extensive culture
should be used. In this case, live prey should be
naturally present or deliberately introduced. De-
pending on the final size needed and the culture
temperature, it can take approximately 50-60 days
to obtain individuals of 50g (T= 25.0±5.0ºC).
CURRENT PROBLEMS AND FUTURE
TRENDS
Sepia officinalis has several characteristics that
make it one of the most promising species for fu-
ture commercial aquaculture. Among them are:
large eggs, which are easily transported and main-
tained; hatchlings resembling miniature adults in
shape; many habits and behaviour being under-
stood; ability to handle relatively large prey (some-
times twice as big as themselves); high survival
rates of hatchlings, compared to other species of
cephalopods; resistance to crowding, disease and
handling, so they can be easily shipped; fast
growth and short life cycle, in some geographical
regions, allowing more than one generation every
year.
However, S. officinalis culture shows several
problematic factors keeping it out of commercial
culture, so they represent bottlenecks. Those are:
lower fertility and fecundity under culture condi-
tions; semelparous life history, therefore requiring
a new group of breeders for each cycle; hatchlings
132 A.V. SYKES, P.M. DOMINGUES, M. CORREIA, J.P. ANDRADE

requiring live food and juveniles and adult stages
refusing dry pellets; the species is cannibalistic;
production of the live food required is not yet de-
veloped, so the cost of food supply is high; and a
basic immunological system (Forsythe et al. 1987
1990) which may generate problems in intensive
culture.
In order to establish correct methodologies for
cuttlefish culture, the determination of Mediterra-
nean and NE Atlantic subspecies is of extreme im-
portance. Published and unpublished data regard-
ing life cycles, reproduction, and initial hatchling
weight seem to indicate that there are, at least, 2
different subspecies. Nevertheless, more compre-
hensive studies elaboring on Pérez-Losada et al.
(1999) will solve this problem. Otherwise, culture
methodologies and their results will inevitably
differ, thus varying in different geographical
locations.
The existence of appropriate and inexpensive ar-
tificial diets is a vital requirement for the viability
of commercial aquaculture. The inability to grow
cephalopods on an inexpensive and storable artifi-
cial diet has inhibited cephalopod mariculture on a
commercial basis (Lee et al. 1991). Therefore, for-
mulation of such a diet is one of the primary and
achievable goals for a successful large-scale cul-
ture of cephalopods (Lee 1994). Furthermore, an
artificial diet with known composition can be of
extreme importance to understanding the physio-
logical and especially absorption processes of the
species in question, which contributes to the
knowledge and understanding of the nutrition
physiological processes in cephalopods.
Artificial diets for cephalopods have been tested
over the past few years in order to lower the costs
of mariculture (Lee et al. 1991, Domingues 1999).
The majority of the artificial diets so far used have
been based on shrimp paste (Lee et al. 1991). In
the last few years, feeding experiments have been
conducted with either moist or dry pellets (Lee
et al. 1991, Castro et al. 1993) or surimi (fish
myofibrillar protein concentrate; Castro et al.
1993, Castro & Lee 1994, Domingues 1999), dem-
onstrating that cuttlefish readily accept prepared
diets. S. officinalis has been maintained with artifi-
cial diets (Castro 1991, Hanlon et al. 1991, Castro
et al. 1993, Castro & Lee 1994, Domingues 1999),
yielding very low growth rates (frequently with
negative growth rates). Recently, juvenile Octopus
maya have been maintained with artificial diets
during periods of up to 2 months with significant
growth, although it was lower than growth ob-
tained with natural diets (Domingues et al. unpub-
lished data). Until now, feeding, growth, and sur-
vival of cephalopods fed with artificial diets are
comparable to fish larvae being weaned from natu-
ral to artificial diets (Lindberg & Doroshov 1986).
Despite the moderate acceptance of artificial diets
by cephalopods, the highest growth rates obtained
(<0.5% BW d-1) were at least 7 times lower than
growth rates recorded during normal laboratory
maintenance of this species (>3.5% BW d-1)
(Forsythe et al. 1994, Domingues et al. 2003,
2004). Growth rates higher than 5% BW d-1 for
similar size cuttlefish were obtained by Domingues
et al. (2002) when using live shrimp as food. Even
higher growth rates (> 20% BW d-1) were reported
by Domingues et al. (2001a) for juveniles.
Future research efforts should now be directed
to the knowledge of nutritional profiles of prey,
hatchlings, and eggs. Additionally, studies should
explore whether the production of grass shrimp as
first feed is economically viable. The technology
of producing grass shrimp as an easy and low cost
feeding method is under study. Results obtained
will provide data that will be used to compose a
dry pellet, different from those tried previously
(which gave some disappointing results). More-
over, the study of the number of generations
achievable until eggs become infertile is of ex-
treme importance to determine brood stock re-
newal. Further research regarding the viability of
different eggs in terms of colour and shape
combinations is also needed.
In order to successfully design artificial diets for
cephalopods, their particular metabolism has to be
taken into consideration. Cephalopods are com-
posed mainly of protein (75-85% dry weight)
(Iwasaki & Harada 1985, Boucaud-Camou 1990),
suggesting that this is an extremely important nu-
trient in their development. According to Lee
(1994), cephalopod metabolism is mainly protein
and amino acid driven. Contrary to fish and crusta-
ceans, cephalopods exclusively use protein for
both growth and energy supply. So, total protein
content and AA composition are considered key
factors in the design of artificial diets for this spe-
cies. Besides, higher grow rates (between 3 and
15% BW d-1) imply an elevated AA requirement
for protein synthesis during the life cycle (Lee
1994). Protein digestibility of the diet is also a rel-
evant factor to be considered in diet formulation.
Related to AA composition (D’Aniello et al.
1995), proportions of essential AA (which cannot
be synthesised from their precursors) should cover
requirements in all stages of cuttlefish develop-
ment. Also, levels of proline and alanine (non-es-
sential AA) in the diet must be reinforced, given
that both AA represent one of the most important
energy resources in cephalopods with a production
not sufficient to cover catabolic demands (Lee
1994).
Lipids represent less than 2% DW (Boucaud-
Camou 1990) and are considered to be of lower im-
portance in energy metabolism (Lee 1994). Be-
cause of this, research on lipid and fatty acid re-
quirements has been neglected, and there is little
knowledge at present (Navarro & Villanueva
2000). Nevertheless, the importance of lipids for
REVIEW ON THE CULTURE OF SEPIA OFFICINALIS 133

cephalopod nutrition, especially during early de-
velopment, has been shown by several authors
(Bouchaud & Galois 1990, Boucher-Rodoni et al.
1987, Castro et al. 1992, Domingues et al. 2003b,
2004, Koueta et al. 2002, Navarro & Villanueva
2000, Perrin et al. 2004, Sinanoglou & Miniadis-
Meimaroglou 2000). Cuttlefish hatchlings and ju-
veniles require prey rich in PUFA, phospholipids
and cholesterol, and a moderate content in neutral
lipids. Within PUFA, the fatty acids eicosapentaenoic
acid (20:5n-3, EPA), docosahexaenoic acid (22:6n-3,
DHA) and arachidonic acid (20:4n-6, AA) are very
important for development, growth, reproduction,
and other physiological functions in marine species
(Sargent et al. 1995). These fatty acids are essential
since they cannot be synthesised from their precur-
sors (linolenic acid - 18:3n-3 for EPA and DHA or
linoleic acid - 18:2n-6 for AA) and must be included
in the diet of these species (Sargent et al. 1995, Arts
et al. 2001).
Another important nutrient is carotenoids that
must be incorporated in the diet, since they are not
produced by cephalopods. Carotenoids are widely
distributed in nature and have shown their influ-
ence on growth in marine species. The antioxidant
effect of these pigments is one of the main reasons
for their importance, especially in PUFA- rich tis-
sues, to avoid lipid peroxidation (Liebler 1993). In
cephalopod nutrition, crustacean species are the
main source of carotenoids.
Finally, to formulate an optimal diet, other nutri-
ents and micronutrients such as carbohydrates, vi-
tamins, and minerals must be taken into consider-
ation to satisfy the main nutritional requirements
for the cuttlefish. Experimental design of diets
should not only take nutrient profiles and propor-
tion into consideration, but also nutrient sources
and the protein/energy ratio. Other aspects are also
important, such as different palatability, texture,
colour, form, and moisture content, all of which
can influence the acceptability and performance of
the designed diet.
The development of artificial diets for the Euro-
pean cuttlefish will open the doors to cephalopod
commercial aquaculture, and will be eventually re-
quired with increasing demand of fishery products
and shortage of fish stocks.
AKNOWLEDGEMENTS. – This work was funded by a
FCT PhD grant (SFRH/BD/12409/2003) to António Sy-
kes. The author’s are indebted to Dr A Guerra (CSIC,
Vigo, Spain) for his valuable comments which really im-
proved the manuscript.
REFERENCES
Adamo SA, Hanlon RT 1996. Do cuttlefish (Cephalopo-
da) signal their intentions to conspecifics during ago-
nistic encounters? Anim Behav 52: 73-81.
Amaratunga T 1983. The role of cephalopods in the ma-
rine ecosystem In Caddy JF ed Advances in the as-
sessment of world cephalopod resources. FAO Fish
Tech Paper 231: 379-412.
Arts MT, Ackman RG, Holub BJ 2001. Essential fatty
acids. In: Aquatic ecosystems. A crucial link between
diet and human health and evolution. Can J Fish
Aqua Sci 58: 122-137.
Blanc A, Daguzan J 1998. Artificial surfaces for cuttle-
fish eggs (Sepia oficinalis L.) in Morbihan Bay,
France. Fish Res 38: 225-231.
Boal JG 1996. Absence of social recognition in laborato-
ry-reared cuttlefish, Sepia officinalis L. (Mollusca:
Cephalopoda). Anim Behav 52: 529-537.
Boal JG 1997. Female choice of males in cuttlefish
(Mollusca: Cephalopoda). Behaviour 134: 975-988.
Boal JG, Marsh SE 1998. Social recognition using che-
mical cues in cuttlefish (Sepia officinalis Linnaeus,
1758). J Exp Mar Biol Ecol 230: 183-192.
Boal JG, Hylton RA, Gonzalez SA, Hanlon RT 1999.
Effects of crowding on the social behavior of cuttle-
fish (Sepia officinalis). Contemp Topics 38(1): 49-55.
Boletzky Sv 1979. Growth and life-span of Sepia offici-
nalis under artificial conditions. Rapp Comm Intern
Mer Médit 25/26(10): 159-168.
Boletzky Sv 1983. Sepia officinalis.In Boyle PR ed, Ce-
phalopod life cycles. I. – Species Accounts. Acade-
mic Press, London: 31-52.
Boletzky Sv 1987. Fecundity variation in relation to in-
termittent or chronic spawning in the cuttlefish, Sepia
officinalis L. (Mollusca, Cephalopoda). Bull Mar Sci
40(2): 382-387.
Boletzky Sv, Hanlon RT 1983. A review of the laborato-
ry maintenance, rearing and culture of cephalopod
molluscs. Mem Nat Museum Victoria 44: 147-187.
Boucaud-Camou E 1973. Étude de l’appareil digestif de
Sepia officinalis L. (Mollusque Céphalopode). Essai
d’analyse expérimentale des phénomènes digestifs.
Thèse Doct ès Sci Nat, Univ Caen, France, 208p.
Boucaud-Camou E 1990, La Seiche, un animal d’avenir.
La Pêche Maritime 69 (1342): 321-329.
Boucaud-Camou E, Péquignat E 1973. Etude expérimen-
tale de l’absorption digestive chez Sepia officinalis L.
Form funct 6: 93-112.
Boucaud-Camou E, Yim M, Tresgot A 1985. Feeding
and digestion of young Sepia officinalis L. (Mollusca:
Cephalopoda) during post-hatching development. Vie
Milieu 35(3/4): 263-266.
Bouchaud O 1991. Energy consumption of the cuttlefish
Sepia officinalis L. (Mollusca: Cephalopoda) during
embryonic development, preliminary results. Bull
Mar Sci 49(1-2): 333-340.
Bouchaud O, Daguzan J 1990. Etude expérimentale de
l’influence de la température sur le déroulement du
développement embryonnaire de la Seiche Sepia offi-
cinalis L. (Céphalopode, Sepioidae). Cah Biol Mar
31: 131-145.
Bouchaud O, Galois R 1990. Utilization of egg-yolk li-
pids during the embryonic development of Sepia offi-
cinalis L. in relation to temperature of the water.
Comp.Bioch.Physio.97B (3): 611-615.
Boucher-Rodoni R, Boucaud-Camou E, Mangold K
1987. Feeding and digestion. In Boyle, PR ed, Cepha-
lopod Life Cycles Vol. II Academic Press, London:
85-108.
134 A.V. SYKES, P.M. DOMINGUES, M. CORREIA, J.P. ANDRADE

Boyle PR 1987. Cephalopod Life Cycles. Vol. II. Com-
parative Reviews. Academic Press, London, 441p.
Boyle PR, Noble L, Emery AM, Craig S, Black KD,
Overnell J 2001. Development and hatching in cepha-
lopod eggs: a model system for partitioning environ-
mental and genetic effects on development. In D
Atkinson & Thorndyke ed, Environment and Animal
Development, Life Histories and Plasticity, Oxford
Bios Scientific: 251-267.
Caddy JF, Griffiths RC 1995. Living marine resources
and their sustainable development. FAO Fish Tech
Paper 353, 167p.
Castro B 1991. Can Sepia officinalis L. be reared on arti-
ficial food? Mar Behav Physiol 19: 35-38.
Castro BG, Lee PG 1994. The effects of semi-purified
diets on growth and condition of Sepia officinalis L.
(Mollusca: Cephalopoda). Comp Bioch Physio 109A:
1007-1016.
Castro BG, Garrido JL, Sotelo CG 1992. Changes in the
composition of digestive gland and mantle muscle of
the cuttlefish Sepia officinalis during starvation. Mar
Biol 114: 11-20.
Castro BG, DiMarco FP, DeRusha RH, Lee PG 1993.
The effects of surimi and pelleted diets on the labora-
tory survival, growth and feeding rate of the cuttle-
fish Sepia officinalis L.. J Exp Mar Biol Ecol 170:
241-252.
Choe S 1966. On the eggs, rearing, habits of the fry and
growth of some Cephalopoda. Bull Mar Sci 16: 330-
348.
Choe S, Ohshima Y 1963. Rearing of cuttlefishes and
squids. Nature 197: 307.
Coelho M L, Martins C 1991. Preliminary observations
on the biology of Sepia officinalis in the Ria Formo-
sa, Portugal. In Boucaud-Camou E ed, La seiche.
Centre Publ Univ Caen: 131-139.
Cole PD, Adamo SH 2005. Cuttlefish (Sepia officinalis:
Cephalopoda) hunting behaviour and associative lear-
ning. Anim Cogn 8: 27-30.
Correia M, Domingues PM, Sykes A, Andrade JP 2005.
Effects of culture density on growth and broodstock
management of the cuttlefish, Sepia officinalis (Lin-
naeus, 1758). Aquacult 245: 163-173.
D’Aniello A, Nardi G, De Santis A, Vetere A, Cosmo A
de, Marchelli R, Dossena A, Fisher G 1995. Free L-
amino acids and D-aspartate content in the nervous
system of Cephalopoda. A comparative study. Comp.
Biochem Physiol l12B( 4): 661-666.
Darmaillacq AS, Chichery R, Poirier R, Dickel L 2004.
Effect of early feeding experience on subsequent prey
preference by Cuttlefish, Sepia officinalis.Dev Psy-
chobiol 45: 239-244.
Delgado CL, Wada N, Rosegrant MW, Meijer S, Ahmed
M 2003. Fish to 2020. Supply and Demand in Chan-
ging Global Markets. WorldFish Center Technical
Report 62. International Food Policy Research Insti-
tute and WorldFish Center. International Food Policy
Research Institute, Washington, D.C. & WorldFish
Center Penang, Malaysia. 236p.
DeRusha RH, Forsythe JW, DiMarco FP, Hanlon RT
1989. Alternative diets for maintaining and rearing
cephalopods in captivity. Lab Anim Sci 39: 306-312.
Dickel L, Chichery MP, Chichery R 1997. Postembryo-
nic Maturation of the Vertical Lobe Complex and
Early Development of Predatory Behavior in the Cut-
tlefish (Sepia officinalis). Neurobio Learn Mem 67:
150-160.
Domingues PM 1999. Development of alternative diets
for the mass culture of the European cuttlefish Sepia
officinalis. Ph D Thesis Univ Algarve, 95p.
Domingues PM, Turk PE, Andrade JP, Lee PG 1998. Pi-
lot-scale production of mysid shrimp in a static water
system. Aquacult Int 6: 387-402.
Domingues PM, Fores R, Turk PE, Lee PG, Andrade JP
2000. Mysid culture: Lowering costs with alternative
diets. Aquacult Res 31: 719-728.
Domingues PM, Kingston T, Sykes A, Andrade JP
2001a. Growth of young cuttlefish, Sepia officinalis
(Linnaeus, 1758) at the upper end of the biological
distribution temperature range. Aquacult Res 32: 923-
930.
Domingues PM, Sykes A, Andrade JP 2001b. The use of
artemia or mysids as food for hatchlings of the cuttle-
fish Sepia officinalis Linnaeus, 1758; effects on
growth and survival throughout the life cycle. Aqua-
cult Int 9: 319-331.
Domingues PM, Sykes A, Andrade JP 2002. The effects
of temperature in the life cycle of two consecutive ge-
nerations of the cuttlefish Sepia officinalis (Linnaeus,
1758), cultured in the Algarve (South Portugal).
Aquacult Int 10: 207-220.
Domingues PM, Poirier R, Dickel L, Almansa E, Sykes
A, Andrade JP 2003a. Effects of culture density and
live prey on growth and survival of juvenile cuttle-
fish, Sepia officinalis.Aquacult Int 11: 225-242.
Domingues P, Sykes A, Sommerfield A, Andrade JP
2003b. The effects of feeding live or frozen prey on
growth, survival and the life cycle of the cuttlefish,
Sepia officinalis (Linnaeus, 1758). Aquacult Int 11:
397-410.
Domingues P, Sykes A, Sommerfield A, Almansa E, Lo-
renzo A, Andrade JP 2004. Growth and survival of
cuttlefish, Sepia officinalis (Linnaeus, 1758) of diffe-
rent ages fed crustaceans and fish. Effects of frozen
and live prey. Aquacult 229: 239-254.
European Communities 2004. Facts and Figures on the
CFP. Basic data on the Common Fisheries Policy.
Luxemburg: Office for Official Publications of the
European Communities, 40p.
FAO 2002. The State of World Fisheries and Aquacul-
ture. FAO Fisheries Department. Food and Agricul-
ture Organization of the United Nations. Rome, Italy,
150p.
FAO 2004. The State of World Fisheries and Aquacul-
ture. FAO Fisheries Department. Food and Agricul-
ture Organization of the United Nations. Rome, Italy,
153p.
Forsythe JW, Hanlon RT, Lee PG 1987. A synopsis of
cephalopod pathology in captivity. Intern Assoc Aqua
Anim Med 1(4): 130-135.
Forsythe JW, Hanlon RT, Lee PG 1990. A formulary for
treating cephalopod mollusc diseases. In FOPerkins
& T C Cheng ed, Pathology in Marine Science.San
Diego, Academic Press: 51-63.
REVIEW ON THE CULTURE OF SEPIA OFFICINALIS 135

Forsythe JW, Hanlon RT, DeRusha RH 1991. Pilot
large-scale culture of Sepia in biomedical research. In
Boucaud-Camou E ed, The Cuttlefish. Centre publ
Univ Caen: 313-323.
Forsythe JW, DeRusha RH, Hanlon RT 1994. Growth,
reproduction and life span of Sepia officinalis (Ce-
phalopoda: Mollusca) cultured through seven conse-
cutive generations. J Zool London 233: 175-192.
Forsythe JW, Lee PG, Walsh L, Clark T 2002. The ef-
fects of crowding on growth of the European cuttle-
fish, Sepia officinalis Linnaeus, 1758 reared at two
temperatures. J Exp Mar Biol Ecol 269: 173-185.
Fuentes L, Iglesias J 2001. Influencia del tipo de presa
viva en las primeras fases del cultivo de sepia Sepia
officinalis L., 1758. Boletin Inst Esp Oceano 17: 327-
331.
Gonçalves JMA 1989. Perspectivas de Repovoamento e
Aquacultura de Sepia officinalis (Mollusca: Cephalo-
poda) em Sistemas Lagunares Costeiros. Açoreana
7(1): 143-152.
Grigoriou P, Richardson CA 2004. Aspects of the
growth of cultured cuttlefish Sepia officinalis (Lin-
naeus,1758). Aquacult Res 35: 1141-1148.
Guerra A, Nixon M, Castro BG 1988. Initial stages of
food ingestion by Sepia officinalis (Mollusca: Cepha-
lopoda). J Zool London 214: 189-197.
Hanley JS, Shashar N, Smolowitz R, Mebane W, Hanlon
RT 1999. Soft-sided tanks improve long-term health
of cultured cuttlefish. Biol Bull Mar Biol Lab Woods
Hole 197: 237-238.
Hanlon RT 1990. Maintenance, rearing and culture of
teuthoid and sepioid squids. In DL Guilbert, Adelman
Jr, WJ & Arnold JM eds. Squid as Experimental Ani-
mals, New York, Plenum Press: 35-61.
Hanlon RT, Forsythe JW 1990a. 1: Diseases of Mollus-
ca: Cephalopoda. 1.1. Diseases caused by microorga-
nisms. In O Kinne ed Diseases of Marine Animals.
III. Cephalopoda to Urochardata, Hamburg, Biol
Anstalt Helgoland. 3: 23-46.
Hanlon RT, Forsythe JW 1990b. 1.3. Structural abnor-
malities and neoplasia. O. Kinne ed.Diseases of Ma-
rine Animals, Vol 3: Cephalopoda to Urochardata,
Hamburg, Biol Anstalt Helgoland. 3: 203-204.
Hanlon RT, Turk PE, Lee PG 1991. Squid and cuttlefish
mariculture: An updated perspective. JCephBiol2:
31-40.
Hanlon RT, Ament SA, Gabr H 1999. Behavioral aspects
of sperm competition in cuttlefish, Sepia oficinalis
(Sepioidea: Cephalopoda). Mar Biol 134: 719-728.
Iwasaki M, Harada R 1985. Proximate and amino acid
composition of the roe and muscle of selected marine
species. J Food Sci 1585 (50).
Koueta N, Boucaud-Camou E 2001. Basic growth rela-
tions in experimental rearing of early juvenile cuttle-
fish Sepia officinalis L. (Mollusca: Cephalopoda).
J Exp Mar Biol Ecol 265: 75-87.
Koueta N, Boucaud-Camou E, Noel B 2002. Effect of
enriched natural diet on survival and growth of juve-
nile cuttlefish Sepia officinalis L. Aquacult 203: 293-
310.
Kreuzer R 1984. Cephalopods: handling, processing and
products. FAO Fish Tech Paper 254, 108p.
Kunisaki N 2000. Nutritional Properties of Squid and
Cuttlefish. In Okuzumi M & Fujii T ed Nutritional
and Functional Properties of Squid and Cuttlefish.
National Cooperative Association of Squid Proces-
sors. Japan, 218p.
Lee PG 1994. Nutrition of cephalopods: fuelling the sys-
tem. Mar Freshw Behav Physiol 25: 35-51.
Lee PG, Forsythe JW, DiMarco FP, DeRusha RH, Han-
lon RT 1991. Initial palatability and growth trials on
pelleted diets for cephalopods. Bull Mar Sci 49: 362-
372.
Lem A, Shehadeh ZH 1997. International trade in aqua-
culture products. FAO Aquaculture Newsletter 17: 3-
6.
Liebler DC 1993. Antioxidant reactions of carotenoids.
Ann NY Acad. Sci 691, 20-31.
Lindberg JC, Doroshov SI 1986. Effects of diets switch
between natural and prepared foods on growth and
survival of white sturgeon juveniles. Trans Am Fish
Soc 115: 166-171.
Loi PK, Tublitz NJ 1998. Long term rearing of cuttlefish
in a small scale facility. Aquarium Sci Cons 2: 1-9.
Navarro JC, Villanueva R 2000. Lipid and fatty acid
composition of early stages of cephalopods: an ap-
proach to their lipid requirements. Aquacult 183: 161-
177.
Nixon M 1985. Capture of prey, diet and feeding of Se-
pia officinalis and Octopus vulgaris from hatchling to
adult. Vie Milieu 35: 255-261.
Pascual E 1978. Crecimiento y alimentacion de tres ge-
neraciones de Sepia officinalis en cultivo. Inv Pesque-
ra 42: 421-442.
Paulij WP, Herman PMJ, Roozen MEF, Denucé, JM
1991. The influence of photoperiodicity on hatching
of Sepia officinalis.J Mar Biol Assoc UK 71: 665-
678.
Pecl GT, Steer MA, Hodgson KE 2004. The role of hat-
chling size in generating the intrinsic size-at-age va-
riability of cephalopods: extending the Forsythe
Hypothesis. Mar Freshw Res 55: 387-394.
Péres-Losada M, Guerra A, Sanjuan A 1999. Allozyme
differentiation in the cuttlefish Sepia officinalis (Mol-
lusca: Cephalopoda) from the NE Atlantic and Medi-
terranean. Heredity 83: 280-289.
Perrin A, Le Bihan E, Koueta N 2004. Experimental stu-
dy of enriched frozen diet on digestive enzymes and
growth of juvenile cuttlefish Sepia officinalis L.
(Mollusca Cephalopoda). J Exp Mar Biol Ecol 311:
267-285.
Richard A 1971. Contribution à l’étude expérimentale de
la croissance et de la maturation sexuelle de Sepia of-
ficinalis L. (Mollusque, Céphalopode). Thèse État no
248, Univ Lille, 264 p.
Rodger GK, Davies IM 2000. Summary of mariculture
production in countries neighbouring the European
Union. J Appl Ichthyol 16: 224-229.
Ruíz-Capillas C, Moral A, Morales J, Montero P 2002.
Characterization of non-protein nitrogen in the Ce-
phalopods volafor (Illex coindetii), pota (Todaropsis
eblanae) and octopus (Eledone cirrhosa). Food Che-
mistry 76: 165-172.
Sargent JR, Bell MB, Bell JG, Henderson RJ, Tocher DR
1995. Origins and function of n-3 polyunsaturated
fatty acids in marine organisms. In Cebe G & Paltauf
F ed, Phospholipids: charaterization, metabolism and
novel biochemical applications. American Oil Chemi-
cal association Press, Champaign, IL., USA, 248:
259.
136 A. V. SYKES, P. M. DOMINGUES, M. CORREIA, J. P. ANDRADE

Sequi R, Palmegiano GB 1984. Some alternatives for the
use of the cuttlefish (Sepia officinalis L.) resources in
coastal lagoons. GFCM Studies and Reviews. Mana-
gement of Coastal Lagoons Fisheries, 61 (2), FAO,
Rome: 607-614.
Sinanoglou VJ, Miniadis-Meimaroglou S 2000. Phos-
pholipids in Mediterranean cephalopods. J. Biosci.
55: 245-255.
Sykes A 2003. On the use of live grass shrimp (Palae-
monetes varians) as the only prey for cuttlefish (Sepia
officinalis) cultured throughout the life cycle. Msc
thesis. Univ Porto, Portugal, 61 p.
Sykes A, Domingues P, Loyd M, Sommerfield A,
Andrade P 2003. The influence of culture density and
enriched environments on the first stage culture of
young cuttlefish, Sepia officinalis (Linnaeus, 1758).
Aquacult Int 11: 531-544.
Warnke K 1994. Some aspects of social interaction du-
ring feeding in Sepia officinalis (Mollusca: Cephalo-
poda) hatched and reared in the laboratory. Vie
Millieu 44(2): 125-131.
Yim M 1978. Développement post-embryonnaire de la
glande digestive de Sepia officinalis L. (Mollusque
Céphalopode). Thèse Doct Spécialité Biol Animale,
Univ Caen, France, 81p.
Received October 19, 2005
Accepted November 3, 2005
REVIEW ON THE CULTURE OF SEPIA OFFICINALIS 137