Cephalopod Culture

Cephalopod biology is briefly surveyed in the context of cephalopod culture, considering its promises and limits. The motivations for undertaking culture work vary greatly, both in a basic and applied science perspective. Under most circumstances, the outcome of an experimental culture remains uncertain until a second generation is achieved. Culture conditions of benthic, shallow-water species are more easily reached in captivity than the living conditions of offshore, pelagic and deep-sea cephalopods. In general terms, difficulties in launching a culture from eggs are inversely proportional to the size of the hatchlings involved. Although cephalopod hatchlings are always actively foraging predators equipped with the organ systems typical of the adults, a combination of very small size and a pelagic lifestyle represents a challenge for their culture, particularly to satisfy their nutritional requirements.

The coleoid cephalopods, typified by cuttlefish, squid, and octopuses, are carnivorous molluscs. Of the better-known coastal cephalopods, many live in shallow water, are short-lived, physiologically efficient, and nocturnal. The behaviour of cephalopods overall is poorly known: a basic ethogram is available for one cuttlefish and one octopus species. Cuttlefish and squid eat primarily fish and crustaceans; the octopus diet includes crustaceans and molluscs. Most cephalopods prefer live natural food and prepared diets reduce growth compared to natural food. Cephalopods are generally solitary. A semelparous life history, parental care of eggs only in the octopuses (and a few squid) and no overlap of generations restrict the opportunity for social behaviour. Cuttlefish reproductive tactics may be complex, and squid swim with conspecifics in schools. Smaller cephalopods are at risk for cannibalism from larger ones (common in 59 % of species and high in 24 %). Cephalopods use visual displays, and some have size-based social hierarchies in captivity. Coastal coleoid cephalopods grow rapidly (live only 1–2 years), mature at an early age, and many die shortly after laying eggs. Many species of squid and cuttlefish aggregate for spawning, while male octopuses locate receptive females by chemoreception. Most young hatch at a small size, are planktonic, and must hunt live appropriate-sized prey. Major challenges to mariculture include keeping tiny planktonic paralarvae alive, providing adequate diet for growth, and avoiding cannibalism within high density captive populations.

Since 1983, when Caddy was able to state that ‘… except in a few ocean regions, they (cephalopods) are not subject to exploitation’, the decline in many finfish stocks has led to increased attention on other groups such as cephalopods, the increasing economic importance of which is evidenced by the rapid rise in their global landings over recent decades. World cephalopod landings (capture fisheries) rose from 500,000 t in 1950 to a peak of more than 4 million t in 2007, with landings increasing in most regions with the exception of the Northeast Atlantic. New regions such as the Southwest Atlantic and the Southeast Pacific subsequently became important cephalopod fishery areas, supplying new abundant species to world markets (notably Illex argentinus and Dosidicus gigas). In Europe, the potential expansion of cephalopod fishing will require a new focus on monitoring, assessment and management of these fisheries, taking into account the differences in life history between cephalopods and fish. The increasing demand for cephalopods on the international markets has stimulated research on rearing and ‘ongrowing’ of cephalopods (mainly common octopus) as an alternative to reliance on fisheries.

This chapter reviews the history of cephalopod culture since the 1960s until 2000, compiling the most important contributions in each decade and identifying key research laboratories and researchers. The literature found is vast in cephalopod species, methodologies and technology. Hence, this chapter focuses mainly on those species with an established aquaculture potential. It includes a description of the evolving seawater systems, broodstock acclimatisation to captivity and rearing/culture methodologies of different life stages.

Cephalopods are fast-growing animals, active swimmers and top predators, which require substantial amounts of food. As such, they show high metabolic rates dependent on a carnivorous diet, thus hypothetically linked to a predominant amino acid metabolism. Their body composition is mainly constituted by high levels of total protein, and their lipids, although quantitatively low, reveal the presence of substantial amounts of long-chain polyunsaturated fatty acids. All in all, little is known about their nutritional requirements, especially during the early stages, very prone to high mortalities under culture. This chapter is a brief account of key information concerning relevant points linked to the nutritional requirements that cephalopods have for proteins, lipids, carotenoids, carbohydrates, minerals and vitamins. Moreover, some considerations on populational metabolism are also presented.

This chapter reviews the welfare and diseases that have been reported since cephalopods are maintained, reared or cultured in captivity. Although cephalopod welfare is only going to be assured in terms of the European Union (EU) legislation from January 2013, it has long been enforced in other regions or countries all over the world. Pathologies registered under captive conditions derive, most of the times, from bad welfare practices. A revision of cephalopods’ immune system and the most important pathologies are presented, which are divided into viral, bacterial, fungal and parasitic pathogenic agents as well as chemical and mechanical damages. In addition, information regarding healing, antibiotics application and surgery is provided. Welfare under research and commercial culture conditions is discussed in terms of the use of anaesthesia and euthanasia agents and their assessment in terms of effectiveness. Further research on the different aspects considered is suggested.

Restocking of cephalopods originated from the awareness of the depletion of natural resources and a need for conservation from stakeholders, public and private sectors. The concept of cephalopod restocking activities is to produce the cephalopod seeds and then release them back into the habitat where the species occur. The process of seed production comprises the collection of broodstocks from the wild, incubation of egg masses, post-hatching management and releasing the seeds at selected locations. The aquaculture methodology that enhances the hatching rate of the eggs and survival rate of the hatchling must produce high yields for the success of restocking. The neritic species, particularly Sepioteuthis lessoniana, Sepia spp. and Octopus vulgaris have been one key focus for restocking due to its success in previous studies on aquaculture as well as their importance to fisheries. The success of aquaculture restocking, supported by the public sector, has been outstanding in Japan and Thailand with a long historical background. Millions of cephalopod seeds were annually released during the peak activities. Although the biological significance of restocking activities to natural stocks requires further research and evaluation, the activities are considered to have produced a significant social success.

The worldwide catch of cephalopod species (squid, cuttlefish and octopuses) was close to 4 million t in 2008. The utilization and the processing of cephalopods result in the generation of a large amount of by-products. Generated by-products represent 35 % of the total mass caught and these include head, viscera, skin, bone, etc. These wastes are currently unvalued. Serious environmental problems can be created without appropriate management. Numerous studies have demonstrated that cephalopod by-products are suitable for human consumption, animal food and other applications with high market value. Indeed, cephalopod by-products are a source of interest for molecules such as polyunsaturated acids, chitin, collagen, etc. This chapter provides an overview of the extraordinary potential of cephalopod by-products and their applications.

Nautiluses are remnants of an ancient lineage that dates back nearly 500 million years. Extant nautiluses still exhibit many traits characteristic of the ancestral species. Nautilus culture systems should therefore take into account both the similarities between nautiloids and modern coleoids and the differences. Nautilus culture systems should be designed to maintain excellent water quality through effective filtration to promote good health. Nautiluses and coleoids differ primarily in their reproductive strategies. Whereas most coleoids are fast growing and semelparous, nautiluses grow slowly, mature later, and are iteroparous. Therefore, nautiluses may necessitate several years of care before becoming sexually mature. Successful reproduction and egg laying by a female yield only a maximum of ten eggs which take up to 1 year to develop and hatch. Currently, nautilus hatchlings have only been reared up to 1 year. The future of nautilus culture systems depends upon a better understanding of both wild and captive reproduction. The success of these culture systems would open up a brand new area of research utilizing different age groups and generations to investigate current and novel questions.

The spineless cuttlefish, Sepiella inermis, is an economic species of the Indian Ocean. S. inermis habit is bentho-nektonic but active in a higher degree compared to Sepia cuttlefish. This species can tolerate environment fluctuations and culture conditions very well, which favour aquaculture. S. inermis can be cultured through several consecutive generations in open seawater systems. The culture methodology is comparable to other sepiid cuttlefish, particularly Sepia pharaonis, comprising collection of live broodstocks, incubation of egg masses, nursing of young and growout phase. The planktonic phase of hatchling is different from Sepia cuttlefish. The moderate final size of 50–100 g is appropriate to frozen food product packaging and maintenance in home aquarium.

The spineless cuttlefish Sepiella japonica has been cultured in China in recent years. After acclimatization to captivity, spawning induction and mating of the broodstock, the females lay eggs attaching to the artificial substratum. Seawater temperature and salinity of hatching are 20–26 °C and 25.0–32.0 psu, respectively. The hatching period lasts for 17–26 days. Hatchlings are planktonic, with approximately 4 mm mean mantle length (ML). The initial feedings are live cladoceran, copepods and enriched Artemia nauplii. The spineless cuttlefishes are sexually mature after 90–120 days, and mating is observed after that. Twenty-thousand mature individuals are obtained, and survival rate from the juvenile to adult phase is about 60 %. The mean weight of adult is 100 g. ML is 50 mm in the smallest sexually mature individual. Spawning occurs as early as day 120. The amount of spawned eggs is 300–500 per individual.

Bobtail squids of the genus Euprymna are small in size with a benthic habit. Such small size results in their insignificance in fisheries and aquaculture focused for human consumption. The unique ability of the voluntary adhesion system and symbiotic bacteria used for bioluminescence is now a primary research focus with potential industrial and biomedical applications. Their small size is well suited for the home aquarium with small volume. Culture of this cephalopod group can therefore serve both research and recreational purposes. Aquaculture in the laboratory provides valuable information for culture methodology that is utilized throughout the entire life cycle of several consecutive generations. This small size and benthic habit of Euprymna are advantageous for small-scale closed or open seawater culture systems. Major trends for culturing Euprymna are similar to other cephalopod groups, particularly benthic octopus that also produce planktonic hatchlings. Reduction of the cost of production is necessary for future large-scale production, with novel protocols for live feed requirements of planktonic young in the nursing phase.

The medium-sized loliginid squids Loligo vulgaris and Doryteuthis opalescens have a long record as experimental models in cephalopod culture. The respective size of eggs (2.0–2.5 mm) and of hatchlings (2.5–3.5 mm mantle length) make them an interesting material for small-scale culture, but the high requirements for live food (copepods, crustacean larvae and/or mysids at early juvenile stages), highly active swimming behaviour and the relatively modest adult size have prevented them from becoming target species in commercial culture projects. The inherent difficulties and costs in providing food and large volume tanks to hold groups of schooling squid have an impact on profitability. However, the data obtained in culture experiments involving these species have been useful in a wider biological context. This chapter summarizes our present knowledge of their culture potential refraining from suggesting standardized methodologies.

Sepioteuthis lessoniana is a demersal neritic species that inhabits coral and rock reefs, seaweed, sea grass beds, and estuaries. Due to its wide distribution range in the Indo-Pacific region, S. lessoniana is an economically important resource of many countries. S. lessoniana has been successfully cultured through multiple generations since the 1960s in both open and closed seawater systems in Thailand, Japan, and the USA. The objectives of aquaculture studies are the production of human food in tropical countries and experimental animals in temperate countries. S. lessoniana hatchlings are larger than other loliginid squids, which enables good adaptation to culture conditions and a very high growth rate through the entire life cycle. In tropical waters, individuals can grow to 500 g in less than 150 days. This rapid growth results from a high feeding rate and requires a massive supply of live feed organisms during the early phase of life. The grow-out phase begins after S. lessoniana can accept dead feed. Further studies of artificial feed or mass production of live feed is required in order to make aquaculture of S. lessoniana economically viable on a large scale. The method and studies of S. lessoniana culture in tropical and temperate waters are reviewed.

The marbled octopus, Amphioctopus aegina, is a moderately sized benthic octopus, inhabiting muddy substrates in the coastal zone of the Indian and Western Pacific Ocean. Capture fishing of octopus in these regions includes this species. The aquaculture methodology comprises collection of broodstocks from the wild, nursing of the eggs and brooding females, nursing of the planktonic young and growout of the benthic young. All phases of the culture process prior to growout can be performed on a small scale with a 50-L tank. The general task for feeding is to feed planktonic food to the planktonic young for about 30 days, and to then provide benthic food after the settling stage. Culturing of Amphioctopus aegina as a model for scientific experiments and home aquaria is the future commercial task.

Advances in controlled cultivation of Patagonian red octopus Enteroctopus megalocyathus (Gould 1852) have fostered biological, physiological and nutritional studies of the species. Research on cultivation of E. megalocyathus is focused on obtaining juveniles under controlled cultivation conditions because it would be the only way to obtain a sustainable octopus production.

Currently, further investigations are needed on the physiology and growth of this species to determine the time and conditions required to obtain juvenile octopuses of 50 or 100 g to start the ongrowing, and to complete the total life cycle of the species.

Octopus maya culture is being developed at the Universidad Nacional Autónoma de México at pilot scale. A closed culture system of O. maya is operating at out of Yucatán facilities, in Sisal. Adult O. maya were obtained after 7 months of culture. O. maya broodstock is renewed every year with adults from the wild population. Spawns are artificially incubated at 25 °C during 45–50 days. Hatchlings pass through a post-embryonic phase that lasts approximately 10 days until they reach the juvenile stage. During the first 15 days after hatch, territorialism and cannibalism are absent and animals practically do not grow. After that age, increments on ingested food are observed together with an exponential growth rate. The culture system has been organized in two steps: (1) ongrowing of hatchlings and (2) ongrowing of juveniles. In the first step, hatchlings are cultured in indoor 7.5 m² tanks at a density of 50–60 individuals m^− 2 for 60 days. During this time, every 20 days animals are weighed and separated according to size to avoid cannibalism. At this phase, survival varies between 75 and 80 %. The juvenile ongrowing phase occurs in outdoor 6 m diameter tanks where juveniles are maintained at a density of 10–25 individuals m^− 2, depending on whether a semi-intensive or intensive culture is applied. Juveniles are cropped when they reach between 80 and 150 g in wet weight (WW), and are sold to the gourmet market. Detailed seawater characteristics and other useful data are included in the present chapter in an attempt to offer an overview of O. maya culture.

Octopus mimus (Gould 1852) is a member of the Octopodidae family. Its distribution includes intertidal and subtidal rocky shore habitats along the Southeast Pacific from northern Perú to Central Chile. The commercial supply of octopus has been diminished due to overfishing in many key fisheries. This chapter presents the results of the research on the reproduction of O. mimus in natural and captive conditions and the application of this knowledge for the potential of aquaculture at a commercial level. This species is particularly suitable for aquaculture; however, commercial cultures cannot be conducted until sound knowledge about cultivation technology and the physiology of the feeding processes in paralarvae are available. On the other hand, our studies have demonstrated that adequate growth rates of O. mimus reared in captivity can be obtained by feeding animals using a diet based on a mix of fish, mollusc and crustacean blended in sausages.

Octopus minor (Sasaki 1920) is widely distributed along the coastal waters of China, Korean Peninsula, as well as south of Sakhalien to Japan. As an important economic cephalopod, culture of O. minor has been attempted in recent years. After capture and broodstock acclimatization to captivity, spawning induction and mating, eggs are spawned at the artificial substratum. Females are responsible for protecting the eggs. The embryonic development lasts for 72–89 days before hatching under the conditions of a seawater temperature of 21–25 °C and a salinity of 28–31 psu. The mantle length and total length of new hatchlings range from 8.5 to 11.5 mm and from 25 to 31 mm, respectively. Hatchlings are benthic, going directly to the tank bottom. Two different types of shelters are provided for this species: ceramic pots of 8–12 mm inner diameter or 10-mm-diameter polyvinyl chloride (PVC) tubes. Cladocerans, copepods and enriched Artemia nauplii are adequate initial feeds for the hatchling rearing. Hemigrapsus sanguineus of less than 4 mm body width are also used to feed 10-day-old hatchlings. Using these prey, the survival rate is 75 % after 1 month of culture. After that, a mixed fresh diet such as juvenile crab, shellfish and shrimp becomes the main feed. After 6–7 months of culture indoors, juveniles of about 100 g can be considered as commercial specification, and they are then transferred to outdoor ponds to continue the ongrowing process, or to be released to the sea for stocking or enhancement programmes. Under indoor culture conditions, the average weights of males and females at 250 days are 122.9 and 197.1 g, respectively.

In laboratory trials, the best growth and survival of the paralarval phase is currently achieved by feeding a mixed live diet composed of enriched Artemia and crustacean zoeae. However, this method is not transferable to a commercial scale as there is limited availability of live zoeae. In order to advance from a research to an industrial scale, it is essential to develop an inert diet with the appropriate nutritional composition to be supplied from an age of 1 month onwards. Another option would be to develop an appropriate enrichment protocol for Artemia so that its composition simulates more closely that of crustacean larvae or wild zooplankton.

A protocol for the first month of O. vulgaris paralarvae culture, which allows the production of good-quality individuals (in terms of dry weight and survival) to start the settlement process, is proposed. Relatively high survival rates and paralarvae dry weights of 1.3–1.8 mg can be attained after 1 month on a sole diet of Artemia. These weights are increased to 2.5–3.5 mg when that diet is supplemented with zoeae.

Robsonella fontaniana (d’Orbigny 1834) is a moderate-sized octopus that inhabits the subantarctic region of South America. This benthic resource has been considered as a potential species for aquaculture diversification, mainly focused on the Asian “baby octopus” market. Most of the information about this species comes from the natural populations in Argentina and Chile, and from its experimental rearing in Chile. This chapter describes the major advances achieved in reproductive biology, ontogenetic development and hatchery cultivation under laboratory conditions of R. fontaniana.

This chapter presents an overall perspective on the current status of cephalopod culture, its bottlenecks and future challenges. It focuses on the species that have received more research effort and consequently accumulated more scientific literature during the present century, namely Sepia officinalis, Sepioteuthis lessoniana, Octopus maya and Octopus vulgaris. Knowledge regarding physiology, metabolism and nutrition of different species is still lacking. Two main challenges are identified: the development of a sustainable artificial diet and the control of reproduction. Understanding cephalopod physiology and nutrition will probably be the biggest challenge in developing the large-scale culture of this group of molluscs on a medium to long term. In addition, zootechnical parameters need future research and improvement. The performance of an ethical experimentation with cephalopods is strongly encouraged and any zootechnical development should be performed and adapted accordingly. The potential of cephalopod culture extends far beyond its use for research and human consumption and probably it will be translated in a remarkable production in the coming years.