Elsevier

Aquaculture

Volume 261, Issue 1, 16 November 2006, Pages 225-240
Aquaculture

Composition in essential and non-essential elements of early stages of cephalopods and dietary effects on the elemental profiles of Octopus vulgaris paralarvae

https://doi.org/10.1016/j.aquaculture.2006.07.006Get rights and content

Abstract

During the present study, we aimed at providing a first look at the elemental composition of the early stages of cephalopods as an approach to their elemental requirements in culture. Essential and non-essential elemental profiles of the European cuttlefish Sepia officinalis, the European squid Loligo vulgaris and the common octopus Octopus vulgaris laboratory hatchlings and wild juveniles were analysed. In addition, for O. vulgaris we determined elemental profiles of mature ovary, eggs in different stages of development and followed possible effects of four dietary treatments during paralarval rearing, also analyzing elemental content of the live preys Artemia nauplii and Maja brachydactyla hatchling zoeae. Content was determined for essential (As, Ca, Cr, Co, Cu, Fe, K, Mg, Mn, Na, Ni, P, Rb, S, Sr, Zn) and non-essential (Ag, Al, Ba, Cd, Hg, Pb) elements. The content in non-essential elements found in hatchlings and juveniles of the three species analyzed here seems to be far lower in comparison with subadult and adult stages of coastal cephalopods. In the octopus eggs, the non-essential element concentrations remained globally low compared to hatchlings and juveniles indicating the absorption of these elements along the ontogenetic development. The elemental composition of the octopus ovary and of the eggs, hatchlings and juveniles of the three cephalopod species analyzed here showed a high content in S. As expected, the calcified internal shell of the cuttlefish, rich in Ca and Sr, originates the main difference between species. It is remarkable the richness in Cu of hatchling octopus, that may indicate a particular nutritional requirement for this element during the planktonic life. The reared octopus paralarvae feed on Artemia nauplii, a prey with relatively low Cu content, showed nearly half Cu content that the “natural” profile of octopus hatchlings or wild juveniles. This suggests a dietary effect and/or an indication of the poor physiological stage of the Artemia-fed paralarvae. At the present, the percentage of essential element absorption by food or seawater is unknown for cephalopods and should be determined in the future to understand their feeding requirements in culture.

Introduction

Minerals are required for the maintenance of normal metabolic and physiological functions of living organisms. The main functions of essential elements in the animal body include the formation of skeletal structure, maintenance of colloidal systems, regulation of acid–base equilibrium and they are important components of hormones, enzymes and structural proteins (e.g. Simkiss, 1979, Williams, 1981, Lall, 2002). The present knowledge of the elemental composition of cephalopods mainly comes from subadult and adult forms and has focused on selected organs or body portions (see between others, Miramand and Bentley, 1992, Bustamante et al., 2000, Ichihashi et al., 2001a, Napoleao et al., 2005a). Most of these studies have highlighted the very high ability of cephalopods to concentrate various toxic elements such as Ag or Cd (e.g. Martin and Flegal, 1975, Bustamante et al., 1998a, Bustamante et al., 2002a, Bustamante et al., 2004) and radionuclides such as 241Am, 60Co, 137Cs, 210Po and 237Pu (Suzuki et al., 1978, Guary et al., 1981, Smith et al., 1984, Yamada et al., 1999).

Cephalopods are carnivorous, active predators and the environmental induced toxic elements have been the subject of recent research regarding detoxification processes (Tanaka et al., 1983, Finger and Smith, 1987, Castillo et al., 1990, Castillo and Maita, 1991, Craig and Overnell, 2003, Bustamante et al., 2002b). However, the elemental requirements of this group of molluscs are poorly known and few studies have been done in relation with the elemental content of early stages of cephalopods and their possible role for the development of embryos and growth of paralarvae and juveniles (Decleir et al., 1970, Miyazaki et al., 2001). For example, it clearly appears that Sr is of ground importance for the shell and statolith development and thus normal swimming behaviour and survival of hatchling cephalopods (Hanlon et al., 1989).

Because cuttlefish are among the easier cephalopod species to rear, several experimental investigations have been carried out on the incorporation of trace elements by their eggs. These studies have shown that the eggshell prevents the incorporation of some non-essential metals such as Cd, Pb, or V and of essential Cu and Zn as well (Paulij et al., 1990, Bustamante et al., 2002a, Miramand et al., 2006). But at the same time, other elements such as Ag and Cs can pass through the eggshell and become incorporated in embryonic tissues (Bustamante et al., 2004, Bustamante et al., 2006). Element transport selectivity through the eggshell is apparently not determined by the metabolic needs of the embryo for essential elements, since the non-biologically essential element Ag is well known for its enhanced embryotoxicity (Calabrese et al., 1973, Martin et al., 1981, Warnau et al., 1996). By another hand, no information exist on the incorporation of elements by eggs in cephalopod species that lack eggshell, as in the incirrate octopods (in ex., Octopus vulgaris) which egg chorion is in direct contact with seawater. Overall, after the hatchling, accumulation of toxic elements shows two patterns with 1) metals such as Ag which is accumulated immediately since juveniles are in direct contact with seawater 2) metals such as Cd or Pb which are significantly incorporated only once the cephalopods start to feed (Miramand et al., 2006). After first feeding most part of the elements can be assumed to be incorporated from the diet and it is known that in juvenile cuttlefish Sepia officinalis the diet influences the elemental composition of the calcareous statoliths (Zumholz et al., in press). However, the behaviour of most of essential elements remains poorly understood to date according to the bioaccumulation processes or to the nutritional needs of cephalopod paralarvae and juveniles.

Due to their rapid growth and market price, the culture of cephalopods has been an increasing area of interest (Walsh et al., 2002, García García et al., 2004, Nabhitabhata et al., 2005, Sykes et al., 2006). However, the rearing of the delicate early stages seems to be the main bottleneck to develop the aquaculture of some species such as S. officinalis (Domingues et al., 2001, Domingues et al., 2003, Koueta et al., 2002, Koueta and Boucaud-Camou, 2003) and O. vulgaris (Itami et al., 1963, Villanueva, 1994, Villanueva, 1995, Carrasco et al., 2003, Iglesias et al., 2004, Okumura et al., 2005). The artificial feeding of the early stages of cephalopods is an unresolved problem and to the present only cultures at experimental scale using natural prey has been successful. Aside from the problems related to food size and quantity, there seem to be other problems associated with food quality. Previous studies on the biochemical composition of the early stages of cephalopods have been developed as first approaches to determine their feeding requirements for lipids and amino acids, trying to design possible co-feeding techniques using Artemia and microdiets suitable for the paralarval feeding behaviour (Villanueva et al., 1995, Villanueva et al., 1996, Villanueva et al., 2004, Rosenlund et al., 1997, Hernández-García et al., 2000, Navarro and Villanueva, 2000, Navarro and Villanueva, 2003). The present work follows this research topic aiming at taking a first insight on the elemental requirements of the paralarval and juvenile stages of cephalopods in culture.

First, we determined the elemental composition of laboratory hatchlings and wild juveniles of three shallow water cephalopod species that represent the main cephalopod orders, all of them of high commercial interest: the European cuttlefish S. officinalis, the European squid Loligo vulgaris and the common octopus, O. vulgaris. Second, for O. vulgaris we determined the same elemental profiles in mature ovary, eggs in different stages of development, hatchlings fasted during 4 days, paralarvae reared to 20 days with four dietary treatments, and the Artemia nauplii used as food during these experiments. In addition, we analyzed hatchling zoeae of the spider crab Maja brachydactyla, a prey that has been successfully used previously as food resource for rearing O. vulgaris during the planktonic stage (Carrasco et al., 2003, Iglesias et al., 2004).

Following Mason and Jenkins (1995), we divided here the analyzed elements as essential elements (As, Ca, Cr, Co, Cu, Fe, K, Mg, Mn, Na, Ni, P, Rb, S, Sr, Zn) and non-essential elements (Ag, Al, Ba, Cd, Hg, Pb). Even Sr is generally reported as a non-essential element for biota, it is essential for cephalopods according to Hanlon et al. (1989) (see above). The knowledge about the essential character and function of each element in cephalopods is poorly known and this classification may change according with future research.

Section snippets

Cephalopod hatchlings and wild juveniles

Specimens analyzed here were used also to obtain their amino acid composition in a previous published study (Villanueva et al., 2004) where detailed information on the collection of material is indicated. In short, egg masses of S. officinalis and L. vulgaris were collected off Barcelona (NW Mediterranean) and egg masses of Octopus vulgaris were obtained from a broodstock maintained in the Institut de Ciències del Mar (ICM), Barcelona. Healthy individuals of all three species were preserved

Results

Elemental composition of S. officinalis, L. vulgaris and O. vulgaris hatchlings are shown in Table 1. Sulphur, Na, K, P, and Mg were the main elements present in the three species. The calcified, large internal shell of the cuttlefish originates the main structural difference among species. As a result, levels of Ca in S. officinalis hatchlings reached more that 5 times that of the other species. Consistently, Sr also showed the higher content as this element has a close behaviour as Ca. In O.

Elemental content profiles of early stages of cephalopods

First investigations about trace elements in cephalopods have focused on essential elements, particularly on Cu because of its role in the haemocyanin (Ghiretti-Magaldi et al., 1958, Rocca, 1969, Nardi et al., 1971, Nardi and Steinberg, 1974) and to the interactions with non-essential elements (e.g., Martin and Flegal, 1975, Miramand and Guary, 1980, Smith et al., 1984, Finger and Smith, 1987, Miramand and Bentley, 1992). Most of these studies concerned a single organ, mainly the digestive

Acknowledgements

We appreciate the technical assistance of J. Riba and M. Baeta during the rearing experiences. Elemental analyses were carried out at the Serveis Cientificotècnics, Universitat de Barcelona and we appreciate the technical assistance and advices of E. Pelfort and G. Lacort during the course of the work. This study was funded by the Centre de Referència de Recerca i Desenvolupament en Aquicültura, CIRIT, Generalitat de Catalunya; the Planes Nacionales JACUMAR, Ministerio de Agricultura, Pesca y

References (96)

  • N. Koueta et al.

    Combined effects of photoperiod and feeding frequency on survival and growth of juvenile cuttlefish Sepia officinalis L. in experimental rearing

    J. Exp. Mar. Biol. Ecol.

    (2003)
  • N. Koueta et al.

    Effect of enriched natural diet on survival and growth of juvenile cuttlefish Sepia officinalis L

    Aquaculture

    (2002)
  • P. Miramand et al.

    Variation of heavy metal concentrations (Ag, Cd, Co, Cu, Fe, Pb, V, Zn) during the life cycle of the common cuttlefish Sepia officinalis

    Sci. Total Environ.

    (2006)
  • P. Napoleao et al.

    Elemental characterization of tissues of Octopus vulgaris along the Portuguese coast

    Sci. Total Environ.

    (2005)
  • P. Napoleao et al.

    Morphologic characterisation and elemental distribution of Octopus vulgaris Cuvier, 1797 vestigial shell

    Nucl. Instr. Methods B

    (2005)
  • G. Nardi et al.

    Isolation and distribution of adenochrome(s) in Octopus vulgaris

    Comp. Biochem. Physiol.

    (1974)
  • G. Nardi et al.

    Ferritin in the hepatopancreas of Octopus vulgaris Lam

    Comp. Biochem. Physiol.

    (1971)
  • J.C. Navarro et al.

    Lipid and fatty acid composition of early stages of cephalopods: an approach to their lipid requirements

    Aquaculture

    (2000)
  • J.C. Navarro et al.

    The fatty acid composition of Octopus vulgaris paralarvae reared with live and inert food: deviation from their natural fatty acid profile

    Aquaculture

    (2003)
  • S. Okumura et al.

    Improved survival and growth in Octopus vulgaris paralarvae by feeding large type Artemia and Pacific sandeel, Ammodytes personatus

    Aquaculture

    (2005)
  • E. Rocca

    Copper distribution in Octopus vulgaris Lam. hepatopancreas

    Comp. Biochem. Physiol.

    (1969)
  • G. Rosenlund et al.

    Co-feeding marine fish larvae with inert and live diets

    Aquaculture

    (1997)
  • C. Sarzanini et al.

    Metal content in Sepia officinalis melanin

    Mar. Chem.

    (1992)
  • S. Seixas et al.

    Interannual patterns of variation in concentrations of trace elements in arms of Octopus vulgaris

    Chemosphere

    (2005)
  • D.I. Skonberg et al.

    Nutrient composition of green crab (Carcinus maenas) leg meat and claw meat

    Food Chem.

    (2002)
  • K. Simkiss

    Metal ions in cells

  • B. Tan et al.

    Response of juvenile abalone, Haliotis discus hannai, to dietary calcium, phosphorus and calcium/phosphorus ratio

    Aquaculture

    (2001)
  • R. Villanueva

    Decapod crab zoeae as food for rearing cephalopod paralarvae

    Aquaculture

    (1994)
  • R. Villanueva et al.

    Growth and proteolytic activity of Octopus vulgaris paralarvae with different food rations during first-feeding, using Artemia nauplii and compound diets

    Aquaculture

    (2002)
  • R. Villanueva et al.

    Amino acid composition of early stages of cephalopods and effect of amino acid dietary treatments on Octopus vulgaris paralarvae

    Aquaculture

    (2004)
  • L.S. Walsh et al.

    Mariculture of the loliginid squid Sepioteuthis lessoniana through seven successive generations

    Aquaculture

    (2002)
  • T. Watanabe et al.

    Trace minerals in fish nutrition

    Aquaculture

    (1997)
  • S.L. White et al.

    On the metabolic requirements for cooper and zinc in molluscs and crustaceans

    Mar. Environ. Res.

    (1985)
  • M. Yamada et al.

    239 + 240Pu and 137Cs concentrations in fish, cephalopods, crustaceans, shellfish, and algae collected around the Japanese coast in the early 1990s

    Sci. Total Environ.

    (1999)
  • R. Blust et al.

    Effect of pH on the biological availability of cooper to the brine shrimp Artemia franciscana

    Mar. Biol.

    (1988)
  • S.V. Boletzky

    Effets de la sous-nutrition prolongée sur le développment de la coquille de Sepia officinalis L. (Mollusca, Cephalopoda)

    Bull. Soc. Zool. Fr.

    (1974)
  • Bustamante, P., 1998. Etude des processus de bioaccumulation et de détoxication d'éléments traces (métaux lourds et...
  • P. Bustamante et al.

    Cadmium, copper and zinc in octopuses from Kerguelen Islands, Southern Indian Ocean

    Polar Biol.

    (1998)
  • P. Bustamante et al.

    Biokinetics of zinc and cadmium accumulation and depuration at different stages in the life cycle of the cuttlefish Sepia officinalis

    Mar. Ecol., Prog. Ser.

    (2002)
  • P. Bustamante et al.

    Uptake, transfer and distribution of silver and cobalt in tissues of the common cuttlefish Sepia officinalis at different stages of its life cycle

    Mar. Ecol., Prog. Ser.

    (2004)
  • P. Bustamante et al.

    Contrasting bioaccumulation and transport behaviour of two artificial radionuclides (241Am and 134Cs) in cuttlefish eggshell

    Vie Milieu

    (2006)
  • Bustamante, P., Lahaye, V., Durnez, C., Churlaud, C., Caurant, F., in press. Total and organic Hg concentrations in...
  • A. Calabrese et al.

    The toxicity of heavy metals to embryos of the American oyster Crassostrea virginica

    Mar. Biol.

    (1973)
  • J.F. Carrasco et al.
  • L.V. Castillo et al.

    Isolation and partial characterisation of cadmium binding proteins from the oceanic squid, Ommastrephes bartrami

    Bull. Fac. Fish., Hokkaido Univ.

    (1991)
  • L.V. Castillo et al.

    Evidence for the presence of heavy metal binding proteins in the squid, Onychoteuthis borealijaponica

  • A. D'Aniello et al.

    Electrolytes and nitrogen compounds of body fluids and tissues of Octopus vulgaris Lam

    J. Comp. Physiol.

    (1986)
  • W. Decleir et al.

    Determination of copper in embryos and very young specimens of Sepia officinalis

    Mar. Biol.

    (1970)
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