Sea Urchin Aquaculture

Home , Echinidae, Echinometridae, Hemicentrotus, Heterocentrotus, Loxechinus albus, Lytechinus

SUSAN C. MCBRIDE1 University of California Sea Grant Extension Program, 2 Commercial Street, Suite 4, Eureka, California 95501, USA

Introduction and History South America. The correct color, texture, size, and taste are factors essential for successful sea The demand for fish and other aquatic prod- urchin aquaculture. There are many reasons to ucts has increased worldwide. In many cases, develop sea urchin aquaculture. Primary natural fisheries are overexploited and unable among these is broadening the base of aquac- to satisfy the expanding market. Considerable ulture, supplying new products to growing efforts to develop marine aquaculture, particu- markets, and providing employment opportu- larly for high value products, are encouraged nities. Development of sea urchin aquaculture and supported by many countries. Sea urchins, has been characterized by enhancement of wild found throughout all oceans and latitudes, are populations followed by research on their such a group. After World War II, the value of growth, nutrition, reproduction, and suitable sea urchin products increased in Japan. When culture systems. Japan’s sea urchin supply did not meet domes- Sea urchin aquaculture first began in Ja- tic needs, fisheries developed in North America, pan in 1968 and continues to be an important where sea urchins had previously been eradi- part of an integrated national program to de- cated to protect large kelp beds and lobster fish- velop food resources from the sea (Mottet 1980; eries (Kato and Schroeter 1985; Hart and Takagi 1986; Saito 1992b). Democratic, institu- Sheibling 1988). As North American fishery tionalized, and exclusive control over fishing stocks were reduced, sea urchin fisheries ex- grounds, including some aquaculture rights, panded in South America (Vasquez 1992). In favor and support fishery enhancement and Europe, fishery stocks have also been depleted aquaculture activities to increase production and aquaculture systems have been developed. in Japan’s coastal waters. An extensive program Sea urchins have been important since the 19th of research, education, and extension services century for developmental research, and large- support the national program, as Japanese con- scale laboratory systems for maintenance of sumption of seafood is the highest per capita broodstock are found in many universities (Leahy in the world. et al. 1978, 1981). Many species of sea urchins Sea urchin aquaculture began with manage- are currently fished or cultured (Table 1). ment of fishery resources where adult animals Sea urchins are an unusual candidate for were transplanted to more favorable habitats. aquaculture as they are harvested for their go- This fishery management tool led to sea urchin nads. Both male and female sea urchin gonads aquaculture research. These activities occurred are consumed, usually uncooked, but some are mainly in Kyushu, Tohoku, and Hokkaido, the salted, pickled, or made into paste. Processed regions with sea urchin fisheries. The objective sea urchin gonads remain one of the most valu- was to increase gonad production and supply able seafood products valued over US$100/kg high value products to a human population on wholesale markets (www.nmfs.gov/ows- where the standard of living was continuing to trade). Whole, live sea urchins, or processed improve. Sea urchin fisheries in Japan began gonads are sold in Asia, Europe, and North and showing signs of depletion in 1967 and efforts to culture sea urchins to supplement natural populations began in the early 1960s (Saito 1 E-mail: [email protected] 1992a, 1992b). To meet the demand for sea ur-

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Table 1.—Species, range, and countries where the species is cultured or where research projects are currently in process. Species Family Range Country Anthocidaris crassipina Echinometridae mid-Honshu to Kyushu, South Japan Japan Heterocentrotus pulcherrimus Strongylocentrotidae North Honshu to Kyushu, South Japan Japan Pseudocentrotus depressus Toxopneustidae Tokoyo Bay to Kyushu, South Japan Japan Strongylocentrotus intermedius Strongylocentrotidae Tohoku to Hokkaido, North Japan, Korea, China, Russia (Kamchatka) Japan S. nudus Strongylocentrotidae Sagami Bay to Hokkaido, North Japan, Korea, China, Russia (Kamchatka) Japan Lytechinus variegatus Toxopneustidae Subtropical–Tropical Americas USA Loxechinus albus Echinidae South Peru, Chile Chile S. droebachiensis Strongylocentrotidae Circumpolar and south to Washington, New Hampshire, and Norway USA, Canada S. franciscanus Strongylocentrotidae Alaska to Baja California, East Pacific USA, Canada S. purpuratus Strongylocentrotidae Alaska to Baja California, East Pacific USA Heliocidaris erythrogramma Echinometridae Australia Australia Evechinus chloroticus Echinometridae New Zealand New Zealand Tripneustes gratilla Toxopneustidae Indo-Pacific Japan, Taiwan, and Philippines T. ventricosus Toxopneustidae Atlantic South America to Gulf of Mexico USA Paracentrotus lividus Echinidae North Atlantic–Mediterranean France, Belgium, Italy, Ireland, and Israel Psammechinus miliaris Echinidae North Atlantic–Mediterranean (Norway and Iceland to Morocco) Scotland chin roe products, the Japanese government sup- most cultured sea urchins are released as ju- ported basic and applied research on the feed- veniles (Table 2). ing habits, reproductive cycle, and environmen- Japanese demand for sea urchin products tal requirements. Initial research led to additional increased dramatically during the 1980s and and ongoing studies of nutrition, environmen- domestic production was able to supply about tal control, culture systems, and control of the one-half the consumer demand. This led to reproductive system (Imai 1978; Agatsuma rapid development and expansion of sea urchin 1998). fisheries in North and South America. Early Since 1970, approximately 55 prefectural warnings from fishermen and resource manag- hatcheries have produced small sea urchins for ers warned of fishery declines. Aquaculture re- cooperative units, which have collective rights search was rapidly initiated in many countries. over local aquatic resources. The production Sea urchin aquaculture in countries with fish- laboratories are responsible for supplying sea eries followed the same pattern as that seen in urchins to cooperative associations. The coop- Japan during the 1960s. Fishermen and scien- erative associations manage the land-based tists initially worked with sea urchins from the nursery units and restocking programs in suit- fishery populations and developed methods able coastal habitats. The coastal areas are man- and diets to enhance gonad production. These aged by predator removal, addition of algae, studies included holding sea urchins in sus- and sometimes habitat improvements, until pended cages or on the sea floor and transplant- harvest, usually 2 to 5 years later. More recently, ing urchins to habitats with more natural algal some cultured sea urchins are reared in cage food. Today, sea urchin aquaculture research systems at high density and fed cultured sea- often utilizes sea urchins collected from the weed until they are large enough for market- ocean in laboratory studies. ing (Mottet 1976, 1980; Doumenge 1990; T. In Europe, there is also a long history of Horii, National Research Institute of Fisheries sea urchins used as food. Sea urchins are eaten Science, Nagai, Japan, personal communica- whole and fresh in southern Europe, in contrast tion). Large-scale aquaculture of sea urchins to the processed roe products popular in Japan. to harvest size is not popular in Japan, and Sea urchins are sold through the fisheries sec- SEA URCHIN AQUACULTURE 181

Table 2.—Production of sea urchin seed for release and aquaculture in Japan for fiscal year April 1999 to March 2000 (data from T. Horii, National Research Institute of Fisheries Science, Nagai, Japan,). The number of product organizations that cultured or cooperative fishery associations that released each species and areas where species were released are also shown. The number of seeds produced is the total for the year and the number released is the actual amount released during this fiscal year. (org. = organizations, n.a. = not applicable) Seed Seed produced released Production size (mm) # of # of seed size (mm) # seed # of # of Species type mean range org. produced mean range released org. areas Tripneustes gratilla release 11 1–25 3 136,000 14 3–50 99,000 3 20 aquaculture n.a. Pseudocentrotus depressus release 16 3–29 11 9,460,000 12 3–30 3,739,000 79 25 aquaculture 8 3–17 2 152,000 n.a. Heterocentrotus pulcherrimus release 9 3–15 3 590,000 11 3–27 489,000 10 47 aquaculture 10 8–12 1 10,000 n.a. Strongylocentrotus intermedius release 11 2–49 28 64,985,000 12 2–106 57,895,000 94 486 aquaculture 8 3–22 2 6,696,000 n.a. S. nudus release 18 6–46 10 6,718,000 18 7–50 7,120,000 11 302 aquaculture 11 6–31 3 366,000 n.a. tor network by auction. Cultured sea urchins ment of wild populations with supplemental could be sold at a fixed price, which would re- feeding, transplanting of sea urchins to favor- quire management of harvesting, production, able habitat, and research scale hatcheries indi- and shipping. Much of the European sea urchin cate aquaculture production of sea urchins is supply is not eaten locally and the diversity of biologically possible, but the economics are regional preferences must be considered for unclear. Providing a consistent supply of a qual- industry expansion (Birulés 1990). ity product is essential for the sea urchin roe South Americans, particularly in Chile, market. The proper balance between identify- also enjoy fresh whole sea urchins. Chile cur- ing market potential, research priorities, and the rently produces 50% of the world’s harvested eventual production of a consistent supply of a sea urchins with approximately 10% of the pro- superior product are among the criteria essen- duction consumed in Chile (Roa 2003). In tial for successful aquaculture of sea urchins. North America, approximately 5–10% of pro- Some of these criteria have been met for sea ur- duction from California fisheries is sold do- chins, but many remain to be explored. mestically. These markets, though small, are expanding. Most sea urchin roe, called uni in Taxonomy and Anatomy Japan, is sold at sushi bars as topping for cooked rice wrapped in seaweed. People seem Sea urchins are members of the Phylum Echi- to either love or hate the taste of uni, which nodermata. Sea urchins are entirely marine and has been described as “ocean bubble gum,” free-living. Most edible sea urchins are adapted better than caviar, tastes like custard or a mild for life on hard, benthic surfaces and generally pate. It is not to everyone’s taste, but it is a live in areas with algal food available. They tend delicacy and worth a try. to live in shallow waters, usually from mid to Countries now looking to sea urchin aquac- low intertidal zones to depths of about 50 m. ulture for stock enhancement of depleted fish- Commercially important sea urchins are eries include Canada, Chile, New Zealand, and spherical but slightly flattened and with mov- the United States. Sea urchin aquaculture in able spines. Each spine fits neatly into a socket these countries and others is repeating the pat- joint in the shell and can be used to move verti- tern of the early Japanese research. Enhance- cally and horizontally. Tubular feet or podia are 182 MCBRIDE found in rows alternating with the spines and have well-developed suckers for attachment. Podia are also sensitive to chemicals and touch, absorb oxygen, catch drifting algae for food, and keep the body clean. The spines are controlled by muscles and are used for protection, to cap- ture and hold food, and for locomotion. Healthy sea urchins can right themselves using the spines and podia. In between the spines and also attached to the calcified body wall or test, are pedicellaria, small, stalked, appendages used for defense, capturing small prey or to clean the body surface. The body is radically symmetrical. Exter- nally, sea urchins are extremely colorful due to skin pigments and can be pale yellow, green, pink, purple, red, or black. Internally, the gonads are also colorful due to carotenoid pigments and desirable gonad colors are yellow and orange. Undesirable gonad colors are white, tan, brown, black, or green. Figure 1.—Internal and external anatomy of a sea The sea urchin body has an oral (bottom) urchin. Upper drawing shows external spine attach- and aboral (top) surface. The aboral surface con- ments, pedicellaria, and tube feet. The mouth and tains the anal region where excretory products teeth (Aristotle’s lantern) and internal digestive sys- and gametes are released and water vascular tem are shown in the lower drawing. The five gonads of sea urchins can be seen in the upper draw- system is controlled (Figure 1). ing (from Mottet 1976). The spherical body surface covered with movable spines comprises 50% of the live sea urchin body weight. The oral surface includes sea urchins progresses through reproductive the mouth, which can be protruded, a peristomal stages that include gonads in the mature, spent, membrane allowing movement of the mouth, regenerating, growing, and premature condi- short spines, and podia. The mouth or “Aris- tion. Commercial harvest is optimal when the totle’s lantern,” named in honor of the Greek gonads are in the growing or premature stage. naturalist and philosopher, is effective at tear- Gonads in this condition contain a majority of ing algae into manageable pieces. It is composed nongerminal, nutritive cells filled with glyco- of five calcareous plates and teeth that are con- gen, protein, and lipid. They are firm, have good trolled by muscles. The mouth leads to the tu- color and texture, and are large. Gonads are bular digestive system, which is intimately con- equally large or larger during the mature phase, nected to the five gonads by mesenterial and but moisture content is higher, the texture is very hemal strands. Between the five gonads are soft, and the gonads tend to fall apart. Gonads structures of the water vascular system. When that are spent or regenerating are too small, of- sea urchins are harvested, gonads must be 10– ten very dark, and are not marketable (Figure 14% of the body weight for successful process- 2a, 2b). ing and marketing. Aquaculture of sea urchins has developed Reproduction in sea urchins is a complex partly because the annual reproductive cycle process involving nutrient accumulation in the limits availability. The mature and growing sea- gonads, transfer of the accumulated nutrients sons each last about 1 to 6 months, depending from nutritive cells to gametogenic cells, stor- on the species. Seawater temperature, food age of the gametes, and spawning either through availability, photoperiod, and sea urchin den- a series of dribbling releases or a mass spawn- sity effect timing of the annual reproductive ing at one time (Pearse and Cameron 1991; cycle. Gonad production in sea urchins is mea- Walker et al. 2001). Gonad production in edible sured by the gonad index. Throughout this pa- SEA URCHIN AQUACULTURE 183

could not be harvested as part of the commer- a cial fishery. The transplanted sea urchins were moved when the gonads were in the growing stage of their annual reproductive cycle. With sufficient food, these urchins were harvested 3 months later. In some cases, the transplanted sea urchins were fed fish or algae at the new site. The main species involved in transplants were Pseudocentrotus depressus and Strongylocentrotus pulcherrimus in southern Japan and S. intermedius and S. nudus in the north (Saito 1992a). Mortality was generally low, 1–2%, and as a re- b sult many fishing areas depended heavily on this method. Approximately 20 metric tons (mt) of sea urchins had been transplanted before 1969 (Takagi 1986). Transplanting of wild sea urchins remains an important fishery management tool in Japan. A field test to examine transplanting sea urchins was completed in California in 1997. Strongylocentrotus franciscanus measuring 25– 70 mm in test diameter were transplanted from an area devoid of algae to dense kelp beds. Fish- ermen and scientists moved approximately Figure 2.—Adult red sea urchin Strongylocentrotus 34,000 urchins. The transplant site was 0.24 ha franciscanus with (a) low gonad index of 2% and (b) (0.6 acres) and had a standing population esti- with full gonads and a gonad index of 20%. mated at 2,100. The area where the urchins were collected was the same size and had about 42,000 sea urchins. After 1 year at the new site, per, unless otherwise stated, gonad index is many sea urchins have grown to nearly 90 mm, given as a percentage [(wet gonad weight/ the legal size for harvest. A conservative esti- whole animal live weight) × 100]. mate of survival, not taking into consideration Some innovative, intermediate forms of animals that have moved from the study site, is aquaculture have been developed for sea urchins 60% of the original transplants. The transplant to increase productivity of wild populations. was cost effective at US$3,500 or $0.10 per urchin and the high recapture rate was encourag- Intermediate Stages of ing for the future of the California sea urchin industry (Schroeter and Steele 1998). Aquaculture—Transplanting In Japan, the next intermediate phase was Adults and Collecting Juveniles collection of naturally set larvae. The first experimental collection of larvae was completed In Japan, reduction of fishery stocks resulted in in 1967 with P. depressus. Early larval collectors activities focused on maintaining sea urchin used nylon threads for settlement. Other in- populations and increasing production from water and benthic larval collectors were devel- populations in less favorable areas. Transplants oped and included transparent polyvinyl chlo- of adult sea urchins were conducted under the ride (PVC) plates with a corrugated surface and assumption that some populations were lim- enclosed gravel beds (Takagi 1986). After 8 ited by the amount of food or habitat available. months, an average of 1,200 sea urchins mea- Sea urchins from overgrazed areas devoid of suring 2 mm in test diameter was harvested algae were moved to areas with more food avail- from the in-water collectors. The small urchins able. These sea urchins were of poor quality were moved to suitable habitat or prepared with virtually no gonadal development and gravel beds (Mottet 1980). Small urchins tended 184 MCBRIDE to fall off the in-water collectors, and preda- Mexico, ownership and environmental modifi- tion was a problem in the benthic systems. Col- cations of the sea floor are not legal and associ- lection of natural seed in Hokkaido was not ated issues of multiple use of coastal areas have pursued due to fluctuation in the supply of not been addressed (Tegner 1989). natural seed. Most cooperative associations carried out some form of adult or juvenile transplanting or collection between 1967 and 1984. Development of Cultured sea urchin seed production began at Sea Urchin Aquaculture the national level in 1984. In California, transplants of juvenile S. Sea urchin rearing developed in several loca- franciscanus with a mean size of 25 mm in test tions for a variety of reasons. In university labo- diameter were completed between 1992 and 1998 ratories, holding adult sea urchin broodstock, at four sites. Survival at two sites was greater usually S. purpuratus, for embryology and toxi- than 50%, and at the other two sites, it was less cology research is widespread. The sea urchin than 10% after 1 year. Survival after 5 years was embryo is important because of the ease of han- between 6% and 11%. About half the survivors dling and observing early development. Cul- were large enough for harvest. The work was not turing a variety of sea urchin species for fishery continued because there was no source of com- production enhancement has been practiced in mercially available sea urchins for additional Japan since 1968. More recently, aquaculture of stock enhancement (Dixon et al. 1998). sea urchins for food production is under intense In Ireland, Paracentrotus lividus has been research in Canada, the United States, Mexico, fished for decades with minimal fishery man- Chile, Scotland, Belgium, France, Ireland, Nor- agement. Transplanting of animals from way, Israel, New Zealand, and Japan. Very re- grounds with poor growth rates to areas with cently, research projects have begun in Austra- more food available is done with subcommer- lia, China, and the Philippines. cial size animals, 35–45 mm. In general, these animals reach good market size and condition Japan after 1 year. This type of work has been carried out by fishermen with little data available, but Extensive studies of naturally setting S. inter- anecdotal evidence shows small urchins (10 medius larvae resulted in rearing the small ur- mm) grow to 50+ mm in 2–2.5 years (Leighton chins in land-based hatcheries until they were 1995). Natural seed collection trials based on large enough for outplanting (Kawamura 1973). techniques used in Japan collected P. lividus and Aquaculture of sea urchins was first conducted Psammechinus miliaris juveniles. The results were in the Yamaguchi Prefecture in 1968 with P. encouraging but have not been continued depressus and H. pulcherrimus and was soon fol- (Moylan 1997). lowed by work with H. crassispina. During these The next phase of in-water sea urchin studies, the phytoplankton Chaetocerous gracilis aquaculture is feeding seaweed to animals en- was used successfully to feed the larvae. The closed in cages or on the sea floor. In Japan, the first cultured sea urchin seed of 10-mm test di- United States, Canada, Scotland, Ireland, and ameter were stocked in prepared gravel beds Mexico, experimentation with this type of in- on the sea floor in 1974. Survival for the first year termediate culture has been completed but it was between 65% and 75% (Takagi 1986). is not used on a commercial basis. Enclosures In the early 1980s, projects were organized on the sea floor near Southern California kelp at the Hokkaido Institute of Mariculture to de- beds were used to feed groups of S. purpuratus velop techniques of mass seed production of and S. franciscanus. Some groups were fed with S. intermedius under a 3-year plan. The national, kelp; Macrocystis pyrifera and others were unfed. prefectural, local governments and the local Gonad production was significantly increased cooperative association contributed to the pro- in groups that received supplemental feeding gram. Generally, the national government (Leighton and Johnson 1992). This project was funds about 50%, the prefectural government expensive and cumbersome. Gonad production about 25%, and the local government and co- can be enhanced quickly, but in California and operative association provide the remaining SEA URCHIN AQUACULTURE 185

25%. There are regulations for administration the gonoduct and gonopores and are collected of the research station, hatchery, and nursery. at the bottom of the beaker. Males are inverted Profits to the program come from sales of the over Petri dishes and the sperm is collected sea urchin seed to fishermen and cooperative “dry” (that is without mixing in seawater). Fer- associations that release them to fishery tilization is done by mixing 1 mL of concentrated grounds. Often the facility does not earn a sperm with 50 mL of seawater and mixing this profit, but as long as the cooperative fishery with the eggs from one female. After fertiliza- association earns a profit from fishery harvest tion, the entire mixture is diluted to 5 L. or sales to fishermen, the government contin- Fertilization is assessed every 30 min when ues to support the facility. the eggs are washed to remove excess sperm and The Hokkaido Experimental Fish Station prevent polyspermy. This continues for 2.5 h. The and its associated sea urchin culture program fertilized eggs are then further diluted to 20 L, has been especially important since 1989 when and the eggs are left undisturbed for 20 h or un- Japanese fishery production dropped below til the larvae hatch out. The hatched out larvae 20,000 mt. With foreign imports and low domes- or dipleurula do not increase in size until they tic harvest, the national government policy con- are able to feed, about 3 or 4 d later. The feeding tinues to support this program. Production of pluteus shows complete gut development and cultured sea urchin seed expanded rapidly. In a single pair of arms in early stages and four arms Hokkaido, 8 million S. intermedius and S. nudus in later stages. The pluteus continues to add arms seed were produced in 1986 and 30 million in as the rudiment of the juvenile sea urchin devel- 1989. The 1989 sea urchin seed production was ops inside the larva. The echinoplutei is the fi- 70% of the national total. The remainder of the nal stage before settlement and metamorphosis. sea urchin seed production was southern species (Saito 1992b). In 1989, there were 17 sea urchin hatcheries and 27 in 2000 with annual production of 100 million in the 10–20-mm size range (Y. Agatsuma, Tohoku University, Aoba, Japan, personal communication) Some new sea urchin hatcheries were con- structed, and some abalone hatcheries were con- verted to sea urchin culture. The objectives of the program were to collect wild broodstock, cultivate planktonic algae to feed the larvae, rear the planktonic sea urchin larvae, and grow the a urchins to a size suitable for release to appropriate habitat. The technique of mass seed production had been developed at southern hatcheries prior to the Hokkaido expansion. Broodstock are collected from the wild populations when they are mature. Broodstock management is not well developed, but water temperature, food availability, and photoperiod have been studied in southern species. Reproductive development of Pseudocentrotus depressus and Hemicentrotus pulcherrimus (Yamamoto et al. 1988) and Anthocidaris crassispina (Sakairi et al. 1989) is b determined by temperature, not photoperiod. Spawn induction is done by removing the Figure 3.—Larval stages of Strongylocentrotus mouthparts and inverting the sea urchins over purpuratus. (a) 3 d pluteus or nonfeeding larvae. (b) a 300-mL beaker containing seawater filtered 23 d echinopluetei larvae with rudiment of juvenile through 1-m mesh. The ova leave the urchin via sea urchin visible. 186 MCBRIDE

Larval development takes 3 to 4 weeks in the hatchery, depending on the seawater tempera- a ture and species (Figure 3a, 3b). Larvae are cultured in 600-L flow-through tanks receiving 1-m filtered seawater and are gently aerated. The incoming water is introduced to larval rearing tanks from a header tank where temperature is maintained at 18°C. Five larval tanks receive water from one header tank. Water enters the larval tanks at the bottom and exits through a centrally placed column with a mesh of 50, 90, or 150 m, depending on the size and age of the larvae. Larval density is 1–2 larvae/ mL. Batch culture of Chaetocerous gracilis are fed b to the sea urchin larvae, providing 5,000 cells/ mL/d, initially, and 20,000 cells/mL when larvae reach the eight-arm + rudiment stage. Heteroshigma akashiwo are also fed to the larvae at 500 cells/mL and 2,000 cells/mL at the beginning and end of larval rearing. Other algae that have been tested, but are not widely used are Dunaliella salina, Monochrysis lutheri, and Phaeocay- tylum tricornatum (Naidenko 1983). Water flow is also increased during larval culture. Approxi- mately 60–68% survive the larval rearing process, and of these, 50% survive settlement and meta- Figure 4.—(a) Juvenile Strongylocentrotus intermedius morphosis to become juveniles (Saito 1992b). rearing tanks at the Shikabe hatchery in Japan, Larvae are ready for settlement and meta- showing the wavy plate inserts. (b) close-up of morphosis at the eight-arm echinoplutei stage young sea urchins on the wavy plates. when the rudiment is approximately 300–350 m in diameter, depending on the species. An- other indicator of larval competence is the abil- The next nursery phase is removal of the ity to bend the arms, and podia may occasion- small urchins from the wavy plates and trans- ally be seen protruding from the larvae. Settle- ferring them to baskets (65 × 65 cm), which are ment is induced using the single-celled Chlor- suspended in the 5-m tanks or in long-line sys- ophyte Ulvella lens (Saito 1992b) or the diatom tems in the sea. The small sea urchins are then Navicula ramosissima (Ito et al. 1987) that have been fed kelp Laminaria japonica, the terrestrial knot- cultured on vinyl wavy plates. Ulvella lens is suc- weed Polygonum sachaliense, or a prepared diet cessfully mass cultured as food source for aba- until they reach 15–20 mm in test diameter about lone, Haliotis spp., and sea urchins. It releases 6 months later. spores that attach to surfaces on a permanent Sea urchin seed is released when they are basis and serve as a food source. Ulvella lens re- 15 mm or larger in test diameter and are ap- duces the high costs of diatom culture for the proximately 1 year old. If seed is held in land- early nursery phase in sea urchin culture. based systems with heated water, 15 mm seed The plates with cultured U. lens or N. may be released after 5 months of rearing. The ramosissima are held in racks of 24 plates in 5-m seeds are released by broadcasting them from rectangular tanks. The newly settled sea urchins fishing vessels over suitable habitat. After 1 year, are held in these large tanks until they reach 5 survival of the seed averages 40%. Predation is mm in test diameter, approximately 3–4 months usually minimal on seed 15 mm or larger as later. Sometimes soft algae such as Ulva lactuca predators are removed from the release sites are added to tanks where small urchins are (Miyamota et al. 1985). Cultured seed of S. in- settled on the wavy plates (Figure 4a, 4b). termedius reached 40 mm and had a 37.8% sur- SEA URCHIN AQUACULTURE 187 vival (Omi 1987) compared to wild S. interme- rearing system. Understanding larval develop- dius, which took a minimum of 5 years to reach ment and response to food quantity and qual- 60 mm (Fuji 1967). Cultured seed of S. interme- ity contributed significantly to development of dius grew faster than natural populations for the sea urchin culture systems in France (Fenaux et first 14 months and then growth rate decreased al. 1988, 1994; Strathmann et al. 1992). Later work and was lower than native stock after 3 years by Fenaux et al. (1994) showed P. lividus reaches (Agatsuma and Momma 1988). In recent years, 16 mm after 1 year of culture on optimal diets sea urchin seeds have been produced for release compared to 12.3 mm reported by Le Gall and to coastal areas with and without existing popu- Bucaille (1989) in heated seawater. Both of these lations and for culture to adult or market size. growth rates compare well with fishery calcu- In addition to research directly applicable lations (Turon et al. 1995). to sea urchin culture, a wealth of research has The recirculation system developed by Le examined aspects of sea urchin biology and ecol- Gall and Bucaille (1989) has been used and re- ogy that are often used by current aquaculture fined to culture Paracentrotus lividus from fer- researchers. Key papers examine reproductive tilization to harvest. The system utilizes one cycles, energetics of growth and ecological rela- area for spawning, larval and algal cultures, and tionships (Fuji 1967), and population modeling, a separate rearing system for P. lividus from habitat requirements, and energy needs of sea settlement and metamorphosis to adult market- urchin populations (Fuji and Kawamura 1970a, size animals. Spawning is induced with potas- 1970b). It is important to note that despite this sium chloride (KCl); fertilization is checked af- huge effort, Japanese fishery harvest has contin- ter 4 h at 20°C. Fertilized eggs are placed in 200- ued to decline. Annual harvest for the last 10 years L tanks at a low density (250 larvae/L) for the has been between 10 and 15 mt. The cause of the duration of larval culture. Larvae are fed decline is unknown, but reduced food availabil- Phaeodactylum tricornatum once a day with 600 ity, decreases in juvenile recruitment, and fish- mL of a 10 × 106 cells/mL concentration. The ing pressure must play a role. larval culture system is maintained on a 12/12 photoperiod with gentle mixing from aeration. Europe When 80% of the larvae are ready to settle, they are transferred to the pregrowth portion of the Europe is a valuable market for aquaculture rearing system. Transfers of larvae are done products and sea urchins have been harvested using 10-m screens to prevent larval arms from for thousands of years from many nearshore entering the mesh and breaking. areas. Currently, no commercial aquaculture The pregrowth area contains sieves with production of sea urchins occurs in Europe, but 500-m screens. The early postmetamorphic stage sea urchin research is at an exciting stage. As- lasts about 8 d when the young sea urchins do pects of the biology and culture parameters of not feed. As the mouth and digestive system Paracentrotus lividus are well documented and reorganize, fresh Enteromorpha linza is fed to the Psammechinus miliaris is under investigation. sea urchins. The sieves are cleaned weekly and the animals are sorted and graded monthly. France Animals larger than 5 mm are transferred to 1- mm sieves. In France, natural sea urchin fisheries collapsed When P. lividus reach 10 mm in test diam- in the 1970s (Southward and Southward 1975) eter, they are cultured in baskets until they reach leading to development of a recirculating sea market size of 40 mm. Sea urchin growth in bas- urchin culture system (Le Gall 1990; Blin 1997; kets submerged in shallow troughs takes ap- Grosjean et al. 1998). proximately 2.7–3.5 years. When the sea urchins Larval diets and culture were studied in reach 40 mm, some are prepared for harvest by detail by Fenaux et al. (1985a, 1995b). A small a 1- to 2-month period of starvation followed scale flow-through larval rearing system was by feeding of kelp, Laminaria digitata, or a pre- developed using a haptophycean flagellate, pared diet. The remaining adult P. lividus are Hymenomonas carterae, as food. This successful conditioned for spawning. These individuals method is modeled after the Japanese larval are held at 18–20°C and at either a 12/12 photo- 188 MCBRIDE period or in complete darkness. This system feet functions include respiration, feeding, and provides mature P. lividus year round. For com- locomotion. A decrease in their activity would plete description of this system, see Grosjean have a deleterious effect on the capacity for go- et al. (1998) (Figure 5). nad production and may explain the reduced The success of this system is encouraging, growth in P. lividus found in Basuyaux and and most likely, the research group will con- Mathieu (1999). tinue to improve and refine it. This recirculating system has also been tested in other areas Scotland of the world (Blin 1997; Fernadez 1998). An important factor that may influence In Scotland, where no fisheries exist, Psam- growth in the recirculating system is accumu- menchinus miliaris has been identified as an ed- lation of ammonia, nitrate, or nitrite. Echinoids ible sea urchin with good potential for aquac- excrete urea. In an important study (Basuyaux ulture. Mass rearing of P. miliaris was success- and Mathieu 1999), the ammonia and nitrate ful using culture methods developed for tolerance of P. lividus was measured in 20-L static Paracentrotus lividus (Kelly et al. 2000). Larval tanks with the test solutions changed daily. growth and survival was optimal using Weight gain was used to determine the effects Duniella tertiolecta and low larval-rearing den- over 15 d. The safe ammonia level determined sities of 1 larvae/mL. Small (1-mm test diameter), cultured for P. lividus was 1 mg N-NH3–4/L (or 0.045 mg N-NH3/L) and a slight toxicity was found at 5 Psammenchinus miliaris grew equally well when mg N-NH3–4/L (or 0.226 mg N-NH3/L). fed a prepared salmon diet or Ulva lactuca. The Behavior was used to test sublethal effects small urchins grew to 8 mm in test diameter in on four species of sea urchins to ammonia con- 6 months. Mortalities were 18.7% in the U. centrations between 12.5 and 100 mg NH4Cl/ lactuca and 37.4% in the prepared diet treatment. L (Lawrence et al. 2003). Tube feet were more Morphologically, P. miliaris fed U. lactuca had sensitive than spines or the Aristotle’s lantern, longer spines and a more flattened test com- probably due to their higher permeability. Tube pared to those fed the prepared diet (Cook et al. 1998). High stocking density (four individuals/L) compared to lower stocking density (two individuals/L) were significantly smaller after 6 months. Mean initial size was 9-mm test diameter and final size was 14 and 15 mm for high and low stocking densities, respectively (Kelly 2002). These studies of juvenile P. miliaris suggest more research is needed for diets that enhance somatic growth of juvenile sea urchins.

Ireland Culture research in Ireland since the decline of the fishery (Byrne 1990) has focused on larval and early juvenile growth. The violet sea urchin Paracentrotus lividus is spawned by peristomal injection of 0.5 M KCl. Flow-through and static culture systems were compared with significantly greater larval survival in the static (80– 90%) compared to the flow-through (1%) systems. Experiments testing various algae re- Figure 5. —European sea urchin culture system from Grosjean et al. (1998). This completely enclosed and sulted in a larval culture system using 500-L recirculating system has been successful used to cul- batch cultures that were fed a haptophycean ture several generations of the European sea urchin flagellate, Hymenomonas elongata. Larvae are Paracentrotus lividus. stocked at 1 larvae/mL, and each tank is lightly SEA URCHIN AQUACULTURE 189 aerated with one air stone near the bottom of hatchery in Canada Island—Scallops, Ltd., lo- the tank. Temperature is maintained between cated in Parksville, British Columbia. The com- 21°C and 24°C. Seawater introduced to the lar- pany is entering commercial production. Island val rearing tanks is filtered to 10 m. Larval sea Scallops produced 750,000 small (5 mm) green urchins are fed H. elongata in excess daily or sea urchins S. droebachiensis in 2000 for aquac- every other day. Microalgae is fed at 5,000 cells/ ulture production and fishery enhancement and larvae during the four-arm stage, 8,000 cells/ a smaller number of red sea urchins S. francis- larvae for the six-arm stage, and 12,000 cells/ canus. Expected production in 2001 is 3 million larvae for the eight-arm stage. Larvae are re- S. droebachiensis and 750,000 S. franciscanus. Is- moved from the culture tanks every 2 or 3 d, land Scallops is also working with S. droebach- collected on 10-m sieves, and placed in a clean iensis collected from wild population and con- tank. Larvae are generally ready to settle in 14– ducting gonad enhancement studies (see Nutri- 16 d (Leighton 1995). tion section). At Island Scallops, larvae are reared in a Norway static system at four larvae/mL, with single bubble aeration to maintain larval distribution University research has focused on spawning, in the water column. The size of the rudiment larval rearing, and gonad enhancement. Local is used to determine the time of metamorpho- broodstock of the green sea urchin S. droeb- sis. Larvae are settled on polycarbonate plates achiensis are spawned and reared at 10°C. Lar- held in racks. Jaw formation occurs in about 4 vae are fed supplemented Dunaliella tertiolecta d. Ambient seawater is used during culture and and reared in a modified, flow-through system ranges between 9°C and 14°C. Large diameter following the Japanese method. All work is cur- pipe is cut longitudinally and used as a nurs- rently experimental (N. Hagen, Bodø Univer- ery system (Y. Alabi, Island Scallops, Ltd., sity, Bodø, Norway, personal communication) Qualicum, Canada, personal communication). The university research group, lead by Dr. Israel Shawn Robinson, is rearing S. droebachienis for laboratory research and offshore field trials in Paracentrotus lividus has been culture for 4 years commercial grow-out facilities. The research at the National Center for Mariculture in Eilat, group has already completed preliminary go- Israel (M. Shipgel, National Center for Maricul- nad maturation studies and juvenile rearing ture, Eilat, Israel, personal observation) Spawn- methods (Morgan 2000; S. Robinson, Depart- ing and larval rearing are done according to ment of Fisheries and Oceans, St. Andrews, Leighton (1995) in winter months when ambi- Canada, personal communication). ent seawater temperatures are 20–21°C. Settle- De Jong-Westman et al. (1995a) examined ment of competent larvae is done when the ru- the effects of adult diet on egg size and num- diment is greater than 320 m in diameter and ber, larval development, survival, and metamor- the larvae are between 14 and 17 d old. Larvae phic success for S. droebachiensis. Adults were are settled on cultured benthic diatoms Navicula conditioned for 9 months with eight experimen- spp. in 100-L tanks of 1 m diameter. A few days tal diets: 1) Low protein: (LoPro < 10% protein); after settlement, cultured red alga Gracilaria 2) High protein: (Hi Pro > 20%); 3) LoPro + M conferta is added to the tanks. Young P. lividus (with mannitol 9.7%); 4) LoPro + A (with 9.75% quickly move onto the algae. About 1 week algin); 5) Hi Pro +C (with 0.5% cholesterol); 6) later, small amounts of cultured U. lactuca are Hi Pro + b (with 0.006% b -carotene); 7) HiPro C added also. Growth to 30-mm test diameter + b (with 0.5% cholesterol and 0.006% b -caro- takes about 2 years. tene); and 8) Air dried kelp: Nereocystis luetkeana. Spawn induction during the natural spawn- Canada ing season (March) was conducted using 0.1 M acetylcholine through the peristomal mem- Currently, there is one research laboratory at St. brane. Diet had no effect on egg size or fertili- Andrews Biological Station, New Brunswick, zation rate. Egg energy content was lowest on working with larvae and one private sea urchin LoPro and highest on HiPro with no difference 190 MCBRIDE in the other diets. Larval culture was completed for diets 1, 2, 6, 7, and 8. Fertilization did not differ among the five diet treatments. Larval development had no pattern, but larvae fed diet 7 formed the eight-arm stage 3 d earlier than other treatments. Larvae from parents fed diet 8 were abnormal, and developmental stages could not be determined. Larval survival at the six-arm stage was 92–95% on diets 1, 2, 6, and 7. Diet 8 had high mortality with 15% survival on day 20. Only larvae from diet 6 consistently showed faster larval development from embry- onic stages. Larvae from diets 6 and 7 were also 13–18% larger than those reared by McEdward (1986) from broodstock fed algae. Overall, this Figure 6. —Juvenile Loxenchinus albus at the Instituto study showed the diet of the adult may influ- de Fomento Pesquero hatchery in Huehue, Chile. ence the larvae and that larva like adults respond to their environment by changes in shape. Other larval research in Canada has shown diet of both algal species in flow-through sys- S. droebachiensis growth is most rapid at 14°C tems. Seawater is filtered to 1 m and flow rates (Hart and Sheibling 1988); growth can be accu- are low; about one-third to two-thirds of the rately compared measuring the oral arms water is exchanged in 24 h. Larvae fed the mixed (McEdward 1984); settlement with developed diet completed metamorphosis after 33 d at 10– microbial films induced more settlement than 12°C and after 20 d at 18–20°C. Larvae were plates without films (Pearce et al. 1990). settled with benthic diatoms, Navicula spp., Nitzchia spp., and Cocconeis spp., in 2-L, clear Chile plastic containers. Young L. albus reach 500– 7,200 µ after 76 d (Gonzales et al. 1987; Bustos Chile has a highly regulated aquaculture indus- and Olave 2001). try with over 13 species of fishes, algae, and in- Mass culture of newly settled L. albus is con- vertebrates commercially cultured. The com- ducted in large rectangular tanks (5.2 × 1.3 × mercially important sea urchin Loxechinus albus 0.65 m, 4,400 L) with fiberglass plates inoculated is cultured on a research and development scale with pinnate diatoms. When sea urchins reach at government (Instituto Fomento Pesquero at 5 mm in test diameter, some are moved to sus- Huehue and Putemún) and university research pended long-line and cage systems. Loxechinus facilities (Universidad Catolico del Norte, albus reaches commercial size, 50–55 mm, in Universidad de Conceptión, Universidad about 30 months. Chile has a patented prepared Andres Bello) and several private hatcheries diet used to feed L. albus during the long grow- (Fundacion Chile, Palo Colorado Cultivos out period (Bustos and Olave 2001). Costeras, and others) (Norambuena and Lemb- eye 2003). Of these facilities, government and Mexico private operations produce about 3 million seed per year but have an estimated total seed In 1994, the Universidad Autónoma de Baja production capacity of 18 million seed (Letelier California began research and production of 2003) (Figure 6). juvenile S. franciscanus and S. purpuratus on an Loxechinus albus is successfully cultured experimental scale. The program started in re- using established methods. Adults are induced sponse to declining fishery harvests. Approxi- to spawn with 0.5 M KCl and reared in a labo- mately 15,000 juveniles are produced each year. ratory system to the eight-arm echinoplutei The juvenile sea urchins are used for labora- stage. Metamorphosis was induced with bacte- tory research, cage culture grow-out research, rial films. Larvae are fed Dunaliella tertiolecta, and have been seeded to artificial reefs. The Chateoceros gracilis, Isochrysis galbana, or a mixed white sea urchin Lytechinus pictus is cultured for SEA URCHIN AQUACULTURE 191 research on G-proteins and signal transduc- over 2 to 3 weeks with high rates of metamor- tion mechanisms between the sperm and egg phosis, 60–90%. Newly settled S. franciscanus (E. Carpizo, University of Hawaii, Honolulu, were 0.40 mm ± 0.038 (mean ± SD) in test diam- personal communication). eter. At settlement, juveniles lacked functional jaws. When the jaws emerged, diatoms, red turf United States algae, and kelp Macrocystis pyrifera were placed in the settlement tanks. At 6 months of age, the Some important laboratory studies were com- juveniles averaged 10.0 ± 2.6 mm, at 9 months pleted in relation to embryological studies of 16.4 ± 5.4 mm. One year later, approximately sea urchins in universities. Hinegardner (1969), 1.7% survived from fertilized embryos. Survival who studied several species from the east and estimates, calculated from the end of the larval West Coast of North America, comprehensively rearing period (with 32% surviving) was 5.3%. described sea urchin larval rearing and meta- The laboratory-cultured sea urchins were used morphosis (Figure 4). Cameron and Hine- for fishery enhancement experiments (Rogers- gardner (1971) identified key factors that induce Bennett et al. 1994). sea urchin larval settlement. In New Hampshire and Maine, cultivation In California, the sea urchin fishery funded and growth studies with S. droebachiensis have aquaculture research for S. franciscanus at the been conducted for several years (Harris et al. University of California Davis Bodega Marine 2003). Sea urchins are produced for laboratory Laboratory. The sea urchins produced from the research, stock enhancement, and sea ranching. system were used in stock enhancement experi- Adult sea urchins are spawned with standard ments. Wild, adult broodstock were induced to spawning and fertilization techniques (Hine- spawn with 0.5 M KCl. Eggs were collected in gardner 1969; Strathman 1987). Laboratory re- filtered seawater and sperm was collected in search with S. droebachiensis testing several al- chilled bowls without seawater. Eggs were fer- gal diets during larval rearing found Nano- tilized using 1,000 sperm/egg. Fertilized eggs chloropsis superior to Dunaliella tertiolecta and were placed in 1,500 mL of 5-m filtered seawa- Isochrysis galbana. Survival and settlement were ter. Larvae were cultured at high densities, 5– low compared to other studies, but the re- 7/mL, in a static system using 1,500-mL glass searchers plan to expand the culture research containers with stir paddles moving at 25–30 (Lake et al. 1998). Juveniles are settled in fi- rpm (revolutions per minute). Larvae were fed berglass tanks with microalgal films and grown a single-celled algae Rhodomonas lens at 60– to approximately 15 mm in test diameter. Nu- 10,000 cells/mL. Algae were cultured in heat merous experiments indicate outplanting in sterilized (70°C) seawater and Prvaosoli- winter months is most successful as natural Guillard culture medium (Guillard 1975). Trans- predators are less active (Harris and Chester ferred cultures took about 5 d to bloom to high 1996). enough densities for feeding (>500,000 cells/ Water flow in rearing containers is also im- mL) under grow lights at 22°C. Cultures were portant for sea urchin gonad growth. Feed in- reared in 17-, 23-, and 100-L containers. Cultures gestion did not vary when S. droebachiensis were attained peak densities of 1.25 million cells/mL held in 350 mL/min compared to 219 mL/min, around day 10 and exhibited a dark red color. but somatic and gonad growth was greater in They were used until densities declined, the lower flow rate (Tollini et al. 1997). around day 13. Adult Lytechinus variegatus were fed a pre- Larval urchin survival was variable among pared diet for 10 months (George et al. 2000). spawn cohorts and within each spawn. Bacte- Following spawn induction, egg size, and time rial contamination was initially a problem but to metamorphosis showed the prepared diet was controlled by rinsing larvae onto 10-m supported development similar to those from screens and cleaning the jars daily with fresh- field populations. water. Over time, larval survival averaged 61– Large-scale culture work with sea urchins 66% at day 16 postfertilization and 32% on day is in the initial stages in several universities in 22, 1 d prior to settlement. Canada, the United States, New Zealand, Nor- Settlement of larvae varied and occurred way, and Scotland. Undoubtedly, new culture 192 MCBRIDE systems will emerge as additional sea urchin nile and adult sea urchin nutrition studies us- species are cultured. ing both wild and cultured animals is presented. Nutrition Gonad Growth and Studies of sea urchin nutrition using natural Enhancement Studies and prepared diets and examination of the associated somatic or gonadal growth have been Algal Diets active areas of research for the past century. Much of the earlier research resulted from in- The scientific literature on ecological relation- terest in these extraordinary animals, and, ships between sea urchins and algae in the natu- more recently, nutritional research has over- ral environment is enormous. Here, I will re- lapped with fishery depletions and the mar- view only those studies with objectives relevant ket demand for sea urchin products. Somatic to aquaculture. growth and annual gonadal growth patterns The European edible sea urchin Para- complicate sea urchin nutrition. Somatic centrotus lividus was fed 12 macroalgae ad libi- growth is slow after metamorphosis to about tum for a 6-month period to examine gonadal 5 mm, rapid juvenile growth to about 15–30 growth. Findings related food ingestion to go- mm, and then slow growth in the adult stage. nadal growth where P. lividus, which digested The annual reproductive cycle results in sea- more than 3 g of organic matter per day, showed sonal gonadal growth. These patterns suggest gonadal growth. Above this food intake rate, the sea urchins may have different nutritional re- species of macroalgae did not have a signifi- quirements during their life history as well as cant effect on gonadal growth. Absorption rates seasonal differences. were strongly correlated with food preferences. The normal food of edible sea urchins is The algae species included three red, six brown, algae, but numerous studies have shown that and three green algae, all of which were domi- they may also act as carnivores or scavengers. nant in the natural habitat of the P. lividus col- Sea urchins apparently feed continuously if lected. The highest gonadal growth was found food is available. Digestibility is generally on the Rhodophyte species Rissoella verruculosa high (>80%) for organic matter, protein, energy, and the lowest on the red algae Asparagopsis and soluble carbohydrates, but may be low for armata and the brown algae Dilophus spiralis. Dif- lipid and insoluble carbohydrates (about 50%) ferences in ingestion rates were attributed to (Klinger et al. 1998; Lares 1999). Digestive pro- attraction factors and chemical defenses of the cesses include enzymes and gut bacterial com- algal species tested (Frantzis and Grémare 1992). munities that break down dietary components. Two interesting studies have examined the Many questions remain regarding the transfer feasibility of out-of-season gonad enhancement of nutrients from the digestive system to the of S. droebachiensis. One study was conducted hemal system and gonads. The sea urchin di- in the laboratory and compared to natural gestive system and gonads respond to food populations (Hagen 1998), and the second study availability by increasing or decreasing in size. was conducted in cages held near the shore Sea urchins may utilize nutrient reserves in any (Vadas et al. 2000). Both studies collected S. body tissue during starvation or may show droebachiensis from barren ground habitat de- rapid growth with high quality food available. void of macroalgal species during the post- There is no discrete nutrient storage site or spawn or summer season. In the laboratory sites of nutrient reserves in the digestive sys- study (Hagen 1998), S. droebachiensis were fed tem, and the conspicuous gonads are believed Laminaria hyperborea, L. digitata, L. saccharina, and to partly serve this function. Alaria esculenta and attained maximal gonad size Excellent reviews of sea urchin nutrition before field populations. This study also exam- for wild populations can be found in Ander- ined optimal size for gonad enhancement and son (1966), Lawrence (1975), and Lawrence and found S. droebachiensis of 50–60 mm in test di- Lane (1982). In this section, a review of juve- ameter would provide aquaculturists with SEA URCHIN AQUACULTURE 193 maximal gonad yield for the time and food in- fresh kelp was used in a 54-d experiment with vested. large, 95–110-mm animals and resulted in a Four algal species, A. esculenta, L. digitata, doubling of the gonad index (5.5% to 10.3%) Palmaria palmata, and Ulva lactuca were fed indi- between September and November. Trials with vidually, and a fifth treatment of a mixed diet frozen kelp were longer, 150 d, and tested three that included all algal species was used to ex- size-classes of S. franciscanus, 15–26 mm, 47–56 amine gonad production to S. droebachiensis in mm, and 70–110 mm, between October and April. sea cages (Vadas et al. 2000). The red alga P. For this experiment, laboratory results were com- palmata induced the most rapid and greatest pared to the field population where the urchins gonadal production and was equivalent to the were collected. Gonad indices increased from mixed diet. Alaria esculenta and L. saccharina pro- 0.04% to 12.4%, 4.2–12.4%, and 6.5–22.1% for duced the lowest yields. The yields after 3 small, medium, and large S. franciscanus, respec- months were significantly greater in the experi- tively. Gonad indices for field populations were mental animals (10%) compared to field much lower: 0.01%, 0.8%, and 5.5% for small, samples (4–6%). Both studies suggest out-of- medium, and large urchins, respectively. Costs season gonad enhancement using algal diets is of freezing large amounts of kelp (150 kg in this possible with S. droebachiensis. study) need to be analyzed for economic feasi- Single and multiple algal diets were also bility, but it appears gonad enhancement of this tested with S. droebachiensis in Atlantic Canada species is feasible (Bureau et al. 1997). (Hooper et al. 1997). Adult S. droebachiensis of Also on the West Coast of North America, 45–55 mm in diameter were fed one of four di- S. purpuratus were held in nearshore cages and ets: 1. Individual species of algae: Agarum fed Macrocystis pyrifera (Hudson 1991). This clathratum, Alaria esculenta, Fucus vesiculosus, study tested the feasibility of developing a com- Ascophyllum nodusum, Laminaria longicruris, or L. mercial product from S. purpuratus collected digitata; 2. L. digitata at 100%, 75%, 50%, 25%, or from food-limited barren areas. When removed 0% of satiation; 3. A 50:50 mixture of L. digitata from the sea cages, 30- and 45-kg samples were and L longicruris;or 4. fresh frozen herring. commercially processed. Gonad weight in- The algal species Agarum clathratum, Alaria creased at rates greater than 1% per week over esculenta, Fucus vesiculosus, and Ascophyllum 10-week trials. The improvement in yield and nodusum produced little gonad growth and were quality were confirmed when the samples were unsuitable for commercial quality require- sold in Japan as grade A ($17.00/lb) and grade ments. Laminaria digitata increased gonad yields B ($7.50/lb), both 1991 prices. This trial was later to 10% in 4–6 weeks. Laminaria longicruris pro- expanded to a commercial operation on a 31.16 duced similar gonad yield over an 8–10-week acre offshore lease, which successfully fattened period. Gonad yield was not different between S. purpuratus until a large winter storm de- treatments in the ration experiment, suggesting stroyed the long-line system in 1998 (J. Hudson, assimilation was increased in the lower rations. commercial sea urchin fisherman, Santa Barbara, The mixed diet (3) showed no significant dif- California, personal communication). ferences in gonad yield compared to either spe- In Scotland, polyculture of Psammechinus cies fed individually. This result provides the miliaris with Atlantic salmon Salmo salar net-pen aquaculturist with more choice when planning systems was examined by rearing the urchins an urchin feed lot. The fish diet resulted in un- (11–16 mm diameter) in lantern or pearl nets. acceptable gonad yield and high mortalities. The lantern nets were placed in salmon cages Seasonal feeding trials using diet 3 and started and under walkways connecting the cages. Lan- in June, July, August, and September had simi- tern net mesh was large enough to allow salmon lar results as those from the first experiment. A pellets to enter, and pearl net mesh was not. A trial started in October had low feed ingestion control group of sea urchins was fed Laminaria rates and low gonad production. There would saccharina. P. miliaris in the lantern nets had sig- appear to be little advantage to winter feed lots nificantly greater somatic growth and gonad in this northern region. indices than animals in the pearl nets (19.08% In western Canada, S. franciscanus were fed vs. 10.35%). This result suggests it is advanta- fresh or frozen kelp, Nereocystis luetkeana. The geous to locate the urchin net culture systems 194 MCBRIDE where they have access to uneaten salmon pel- gonad indices were 32% and 39% for LoPro lets (Kelly et al. 1998). and HiPro, respectively. There were no signifi- The Japanese red sea urchin Pseudocentrotus cant effects of diet on somatic growth, gonad depressus from two cultured populations were lipid, or dry matter content. fed the brown algae Eisenia bicyclis for 1 year. Adult S. droebachiensis (40–60 mm) were col- Field samples were compared to the laboratory lected by scuba diving and sorted into 15 animals, in which monthly subsamples mea- groups. Three agar-based diets were compared sured somatic growth, gonad index, and histo- to Laminaria longicruris in cages suspended from logical analysis (Unuma et al. 1996). Laboratory a long-line system. The sea urchins were fed populations maintained a higher gonad index approximately 10 kg every 2 weeks over a 3- over the year with significantly less decrease month period. Gonad production was greatest following spawning than field populations (5% on a prepared diet containing carrots, cabbage, vs. 2%). The laboratory group did not increase soy meal, potato starch, seawater, and guar gum in gonad index as rapidly as the field popula- as a binder (Diet A). The other two diets con- tion; however, gametogenesis was delayed tained the same ingredients with poultry meal about 2 months and was sustained longer. The substituted for soy meal (Diet B) or raw potato authors suggest environmental factors in the instead of raw cabbage (Diet C). The initial laboratory study are probably responsible for sample and samples from the wild population the differences between the two populations. had gonad indices of 4.3–4.9% at the beginning From an aquaculture perspective, the sustained and end of the experiment. The prepared diets mature condition of the gonads should be showed final gonad indices of 9.8% and 8.0% avoided. Shortening the mature period by con- for prepared diets A and B and 7.5% for pre- trolling the environment or changes in the feed pared diet C and L. longicruris. Similar to other may provide methods to maintain the imma- studies, the prepared diets showed greater go- ture gonadal condition (Unuma et al. 1996). nad production than macroalgae but suggest Overall, algal diets successfully enhance sea that refinement of prepared diets for improved urchin gonadal growth. The main concerns are gonad production is essential for successful sea the costs of natural algae, availability of algae, urchin aquaculture (Robinson and Colborne and possible negative impacts to the natural 1997). environment. Comparison of algal and pre- Between 1991 and 1994, several 4- to 5-week pared diets was a natural follow up to testing studies were completed with S. droebachiensis algal diets, and several studies have done this. fed semimoist prepared diets or dried Laminaria longicrispus. Diets were formulated with algae, Comparison of Algal and Prepared Diets wheat gluten, starch, calcium phosphate, calcium carbonate, calcium sulfate, vitamins, cho- Several published studies have compared go- line chloride, and vitamin C into rubbery, sink- nadal growth for sea urchins fed natural algal ing pellets. Sea urchins were collected by divers diets and prepared diets. Seven prepared diets and experiments conducted in laboratory tanks and air-dried Nereocystis luetkeana were fed to at densities of 40–50 g/L of seawater. Condi- adult S. droebachiensis (50–70 mm) collected from tioning in January was inconclusive with sea- a population near Vancouver Island. The com- water temperatures below 6°C. Gonad indices position of the diets is the same as those shown between 11% and 12% from initial values of 3.4– in the “Development of Aquaculture” (de Jong- 6.4% were found in May, July, August, and Oc- Westman et al. 1995a) section. The experiment tober trials for prepared and algal diets. These was conducted from July 1991 to March 1992 studies again showed it is possible to increase with subsamples taken from each treatment the gonad index in a relatively brief period every 6 weeks. All of the HiPro diets and N. (Motnikar et al. 1997). luetkeana had higher gonad indices than S. Cultured Loxechinus albus were maintained droebachiensis fed the LoPro diets. It is impor- in cages on a long-line system and in labora- tant to note that gonad indices were calculated tory aquaria. Four diets were tested: two ex- as wet gonad mass/drained test mass × 100. truded feeds, one with and one without kelp, Initial gonad indices were 15.9–17.8% and final and Macrocystis pyrifera and Ulva lactuca. The SEA URCHIN AQUACULTURE 195 experiment was conducted for two 4-month not the field samples in the postspawn season. periods, one during the summer (December to During gonad growth and late gametogenesis, March) and one during the spring (August to large E. chloroticus gonad indices were larger for November). Whole live weight was 72 g at the urchins fed the prepared diets compared to al- start of both experiments. Gonad index was sig- gal diet treatments and the field samples (Barker nificantly greater for L. albus fed the prepared et al. 1998). diet in the spring for both culture systems com- In Scotland, polyculture of Psammechinus pared to the algae diets (19% vs. 8%) and had miliaris and Atlantic salmon showed some inter- significantly increased from the initial sample. esting results. The sea urchins efficiently utilized In the summer, gonad index results showed the a prepared salmon diet rich in protein and lipid same pattern, but gonadal growth was greater. resulting in acceptable somatic and gonadal Sea urchins fed the prepared diet increased from growth. In another study, gonadal production 5.5% to 20% compared to a gonad index of 11.7% was greatest for P. miliaris-fed salmon feed (20– found in the algal diet treatments (Lawrence et 57%) compared to natural algal diets (2–12%) over al. 1997). This study confirmed that for some a 12-month period (Cook et al. 1998). The gonad species, gonad production is greater with pre- indices of monthly subsamples showed a large pared diets than algal diets or fishery yields. gonad mass with negligible decline after spawn- Large S. franciscanus collected from a natu- ing and an extended spawning period for urchins ral population off northern California had an fed the prepared diet treatment. The sea urchins initial gonad index of 3.4% and weighed 248 g. fed an algal diet, Laminaria saccharina, had a Sea urchins were fed the prepared diet with kelp spawning period of 8 weeks with substantial (as for L. albus, Lawrence et al. 1997) or fresh declines in gonad mass, lipid, and protein con- Nereocystis luetkeana from June to November at tent. The elevated gonad production results sug- two seawater temperatures, 12.9°C and 16.1°C. gest a more refined diet could result in success- Final gonad production was not significantly ful aquaculture for this valuable species. The different between treatments and was 19.2% pattern of extended spawn season and no large (McBride et al. 1997). For this species, it appears changes in gonad index during the annual re- high gonad indices are possible from both al- productive cycle is validated in studies with gal and prepared diets. other prepared diets. A very comprehensive study with three sizes of Evechinus chloroticus examined four prepared Prepared Diet Only diets and a combination algal diet of Macrocystis pyrifera and Ulva lactuca. This study was con- The suggestion to develop prepared diets for ducted during three stages of the reproductive sea urchin nutrition research (Lawrence 1975) season, postspawning (February to May), go- has been a stimulus for many studies. Agar- nadal growth (June to September), and late ga- based research diets and extruded pellets have metogenesis (October to December). The three been developed and tested with many sea ur- size-classes were small (30–40 mm), medium chin species. So far, most of these studies have (50–60 mm), and large (70–80 mm). All compari- been on nutrition using wild sea urchins, not sons included an initial and final sample from cultured ones. This situation is changing rap- the natural population. Field samples from the idly as many research laboratories are devel- small size-class did not develop gonads. Gonad oping mass culture techniques. indices from small and medium urchins were The first published study using a prepared generally similar in the postspawning and late diet was Nagai and Kaneko (1975). Strong- gametogenic stages, and the prepared diets sup- ylocentrotus pulcherrimus was fed a prepared diet ported greater gonadal growth than algae. Be- to examine feed ingestion and assimilation ef- tween June and September, there were no sig- ficiencies. The prepared diet contained 23.3% nificant differences in gonad indices between the each of fish, soy, corn, yeast, and 0.1% vitamins prepared and algal diet for small and medium and was bound by cooking with agar. Mortali- E. chloroticus, but they were all greater than the ties were dissected and found to have a gonad field samples. Large E. chloroticus gonad indices index of 20–25%. were greater in the prepared diets than algae but Since Nagai and Kaneko’s study, sea urchin 196 MCBRIDE prepared diets have been used in Japan (Hagen U.S. Department of Agriculture. In the follow- 1996). The preferred food for cultured sea ur- ing section, these diets are referred to as the chins is kelp, but prepared pellets are used pellet diet. when algae are not available. Adult S. droebachiensis (50.4 ± 3.9 mm, 47 ± Gonad production of small (5 g) and large 2 g) were fed the pellet diet during two sea- (60 g) Paracentrotus lividus was examined using sons, prior to the annual spawning (8-week ex- agar-based diets that were similar except for the periment) and after spawning (12 week). Two protein source. One diet utilized fish and the pellet diets were used: one with fish meal as other soybean. Groups of each size-class of P. the protein source, and a second using soy lividus were fed the diets either continuously or were fed ad libitum. Sea urchins were collected every 3–4 d. Gonad index increased from 0.5% from natural populations and the experiment to 4.4% and was similar in both feed regimes was conducted in a recirculation system at 34 for small P. lividus. Gonad index for large P. parts per thousand, 6–8°C, and 12/12 photo- lividus increased from 0.8% to 5.5% and was not period. In the winter prespawn study, initial significantly different between diets or feed gonad index was 17.1% and increased slightly schedules. These results suggest the protein to 19.7% in both diet treatments. In the sum- available from both fish and soy is suitable for mer post-spawn study, initial gonad index was gonad enhancement (Lawrence et al. 1989). 4.9% and increased to 20%, comparable to In a large and complex study, small cul- maximum gonad production for this species tured and large wild P. lividus were fed three from natural populations. Both feeds were suf- prepared diets or an algal diet Cymodocea nodosa ficient to support gonad growth (Klinger et al. in laboratory tanks with recirculating seawater 1998). or fresh incoming seawater. The diets contained The same diet was tested with S. droebachiensis fish, vegetable or mixed protein sources. Tem- collected by diving and placed in ambient photo- perature was controlled at 18–20°C or main- period or a photoperiod set four months ahead tained at ambient seawater temperature. Tanks using artificial lights. The experiment began in were either in total darkness or natural photo- March and the altered photoperiod treatment set period. Mixed diets, fresh seawater, and natu- for July sunrise and sunset was a 4-month photo- ral temperatures resulted in higher gonad indi- period advance. A subsample from each tank was ces for all size-classes and ranged from 11% to taken monthly. All subsamples resulted in gonad 15%. These values were higher than natural indices around 20%, significantly higher than populations or P. lividus fed C. nodosa. In the re- those taken from concurrent field samples. Results circulating system, final gonad indices were 5– of the reproductive condition of these sea urchins 7% in all treatments. Interactions between diet- will be presented in the Reproduction section recirculation versus continuous flow and size (Walker and Lesser 1998). shows that a mid-size-class, 20–25 mm diam- A ration study with a soy-based pellet was eter P. lividus had the highest gonad indices. tested with wild S. franciscanus. Adult S. Gonad index results can be grouped into three franciscanus, 91 mm, 295 g, were fed 1 g/d, 3 categories: 1. sea urchins fed C. nodosa, 2. all g/d, or not fed. Initial gonad index was 3.3% diets and light conditions at the controlled tem- and increased to 7.1% and 12% in the low and perature and 3. all diets and light treatments high rations, respectively. There was no change with flowing seawater. Groups 1 and 2 had in the gonad index of unfed urchins. The ex- similar gonad indices and group 3 had the periment lasted 60 d. The results show S. higher value (Fernandez and Pergent 1998). franciscanus can also be fed pellet diets and that Three papers have tested extruded pellet gonadal production may be controlled by food diets developed by Dr. John M. Lawrence (De- ration (McBride et al. 1999). partment of Biology, University of South In the recirculation system described by Florida) and Dr. Addison L. Lawrence (Texas Grosjean et al. (1998), Paracentrotus lividus were A & M Shrimp Mariculture Project) and manu- fed a pellet diet for 1 month (30 d). In each 48 h factured by Wenger International, Inc. (Kansas period, diets were fed ad libitum for 8, 16, 24, City, Missouri). The pellets are approved by 32, 40, or 48 h. Paracentrotus lividus with food the U.S. Food and Drug Administration and the available for 35 h or more had the highest go- SEA URCHIN AQUACULTURE 197 nad production. These results suggest P. lividus almost black or brown. In some species, this does not feed continually to produce large go- dark color persists after feeding for 2 to 3 nads and that the quantity of food can be esti- months. Research on pigments that influence mated to prevent waste (Spirlet et al. 1998). gonad color has not been successful (Motnikar Agar-based diets have also been used to test et al. 1997), as the pigments tested have gener- effects of protein on gonad enhancement. Diets ally had no influence on gonad color. An inno- with 30%, 40%, or 50% protein were fed to small vative method to investigate the efficiency of S. franciscanus for 10 months. Initially, the sea transfer of pigment from prepared diets to go- urchins were immature and had very small gonads, used reflected light fiber optic spectro- nads. This range of diet protein content was rela- photometer using CIE (Commission Inter- tively high and did not impact gonad produc- nationale de l’Eclairage) L * a * b * units of mea- tion. Gonad index increased equally in all diet surement (Robinson et al. 2002). This method treatments to 16% (McBride et al. 1998). Gonad improves on previous approaches of determin- index was not significantly different for S. ing gonad color by comparison with color droebachiensis-fed agar based diets with protein swatches. Distinct pigment sources can be quali- concentration ranging from 19% to 29% (Pearce tatively and definitively measured using the et al. 2002). CIE system. Robinson et al. (2002) found a natu- Adult Lytechinus variegatus (37–64 mm, 30– ral source of b-carotene from dry Duneliella salina 110 g) were fed one of two prepared diets for 10 produced the most acceptable color in S. weeks. Diet 1 was a pellet diet from Wenger droebachiensis. International, Inc. Diet 2 was agar-based and similar to a catfish diet. Both diets resulted in equally large gonad production (Watts et al. Feed Ingestion Rates 1998). Reports of sea urchin feed ingestion rates are As can be seen from studies with algal or given in most of the studies presented in the prepared diets, sea urchin gonad enhancement Nutrition section and are summarized in Table is quite readily achieved. Laboratory and in- 3. Trends seen include the inverse relationship water studies feeding sea urchins algal or pre- of protein content and feed ingestion. A word of pared diets have shown an average increase caution, most sea urchin studies cited here do gonad size of about 1% per week. The difficult not consider energy content of the diets. Since part is controlling the quality of the gonads. energy is the first limiting factor in biological Often when sea urchins are fed in a controlled systems, the feed ingestion rates presented environment, the gonad becomes soft or an un- should be considered with this in mind. desirable color. Researchers are now examin- ing additional quality aspects that can be improved or manipulated by diet. Among the im- Control of Reproduction portant factors under consideration are color and reproductive stage. Many elegant studies have described the annual reproductive cycle of a wide variety of edible and other species of sea urchins. In gen- Gonad Color eral, edible sea urchins reach sexual maturity at about 1–2 years of age and 25–30 mm in test Color is among the most important appearance diameter or when they reach approximately factors in sea urchin roe products and was rec- 30% of their adult size (Pearse and Cameron ognized as an early challenge to sea urchin 1991; Lawrence 1982; Walker et al. 2001). How- aquaculture (Matsui 1968). Prepared diets tend ever, sustainable sea urchin aquaculture re- to give a light tan or pale gonad color. This has quires maintenance of breeding populations been noted by nearly every study mentioned in addition to understanding the natural repro- above in the nutrition section. Algal diets tend ductive cycle. The development of sea urchin to give excellent color unless the urchins are aquaculture has been primarily focused on collected from an extremely food limited envi- gonad production. Regulation of gonadal ronment where the gonads tend to be very dark, growth and gamete development has been 198 MCBRIDE et al. 1998 Klinger et al. 1997 ased research diet, no data = ased research d ingested/animal/d. Size is given 0.09–0.4 0.16–0.54 Food ingested Study 0.1–0.2 0.1–0.24 0.05–0.06 0.04–0.12 0.04–0.18 0.100.05 Nagai and Kaneko 1975 Lawrence et al. 1991 0.310.34 0.47 0.18 Klinger et al. 1994 0.14 0.63 16° C23° C 0.05 0.08 Klinger et al. 1986 lib. 0.09–0.12 Barker ad lib.ad 0.1–0.14 ad libitum 0.4 Frantis and Grémare 1992 prespawn postspawnprespawn 0.44 type Food offered Macrocystis pyrifera agar agarRisoella verruculosa ab lib. agar ad lib., agaragar ad lib. kelp meal ad lib. pellet without kelp postspawn lipid ash Food 25–54 1–4 20–40 carb. Diet composition (% dry matter) 5–10 protein 40 31 7 n.d. agar ad lib. 40 (soy) 32 5.1 17 50–60 mm 70–80 mm 30–40 mm 30–40 mm 20 64 7 9 pellet ad Size 30 mm4.4 g 36 37 36 5 49 0.5 n.d. n.d. agar adlib. 50–60 mm 70–80 mm 30–40 mm50–60 mm 70–80 mm 37 494.4 g60 g 0.5n.d. n.d. 12.4 41.7 n.d 21.3 every 3–4 d every 2–3 d 0.05 0.10 n.d. 37 49 0.5 n.d. agar ad lib., 51 mm, 63 g 40 (fish + soy) 3237–64 mm 5.147 mm, 50 g 23 23 17 64 64 1 2 n.d. 9 pellet pellet with ad lib. 0.44 et al. 1998 Watts Evechinus chloroticus Table 3.—Diet composition and feeding rates of sea urchins fed natural or prepared diets (pellet = extruded diet, agar agar-b fed natural or prepared 3.—Diet composition and feeding rates of sea urchins Table as test diameter (mm) or whole animal weight (g). Species n.d., carbohydrate = carb, ad libitum lib.). Algal diets are given as genus and species. Food ingested is dry fee Strongylocentrotus pulcherrimus Paracentrotus lividus P. lividus P. Lytechinus variegatus L. variegatus L. variegatus L. S. droebachiensis SEA URCHIN AQUACULTURE 199 Floreto et al. 1996 Agatsuma et al. 1993 McBride et al. 1997 McBride et al. 1999 Food ingested Study 0.06 0.05 0.07 0.5–1.0 2.75 1.421.25 0.89 0.55 McBride et al. 1998 ad lib. ad lib. ad lib. ad lib. ad.lib., 12°C 16°Cad lib., 16°Cad lib., 4.0 1.31 3 g/d3 1.42 type Food offered Ulva pertusa Gloio peltis furcata Undaria pinnatifida mixed algaeLaminaria ad religiosa lib. 0.08 Nereocystis luetkeana agaragaragarpellet ad lib. ad lib. ad lib. 1 g/d 0.5–1.5 lipid ash Food 0.05 8.8 carb. .5–4.9 23–54 1.4–4.4 27–49 Diet composition (% dry matter) protein 23.3 35.6 3.1 n.d. 22.125.5n.d. 43.9 1.4 7.4 n.d. 6.9 n.d. n.d. n.d. n.d. 234050 14 0.05 30.7 2.5 20.2 7.0 7.0 8.7 pellet 9.0 12°C ad.lib., 0.99 Size 16 mm, 2 g 25 mm, 8.6 g 15 mm, 2 g n.d. 33 mm, 19.7 g40 mm, 37.8 g54 mm, 76.8 g90 mm, 248 g 2 0.6–1.8 1.0–2.5 1.0–4.0 91 mm, 295 g 20 64 35 mm, 20 g 30 42.2 7.0 8.4 Table 3.—Continued. Table Species gratilla Tripnuestes S. nudus S. franciscanus S. franciscanus S. franciscanus 200 MCBRIDE studied for several sea urchin species. In stud- stores are generally depleted during gameto- ies that have focused on reproduction, diet, genesis and after spawning (Giese 1966; Hol- temperature, and photoperiod have been inland and Holland 1969; Fernandez 1998). vestigated. Seasonally, changes of seawater tempera- The recirculating system developed and ture are also often suggested to be responsible used in France has resulted in a successful for annual reproductive cycles. However, there breeding method (Grosjean et al. 1998). Brood- is little relationship between temperature and stock has also been maintained in laboratory spawning season for many species. In areas populations by holding the animals in dark- with little or no changes in seasonal tempera- ness with controlled temperature (Leahy et al. tures, such as the Antarctic or deep sea, annual 1978). Both of these systems feed the adult sea reproductive cycles are found in sea urchins. urchins ad libitum, either kelp or prepared Both field and laboratory studies show seawa- diet. Both algal diets and prepared diets have ter temperature had little effect on gametoge- been shown to produce healthy viable larvae nesis of S. purpuratus (Pearse et al. 1986; Bay- (de Jong-Westman et al. 1995a; George et al. Schmidt and Pearse 1987). 2000) when adults were held in ambient light. Seawater temperature may initiate gameto- Size at sexual maturity is an important genesis out of season, such as in the laboratory component of reproduction. Well-fed, labora- systems of Grosjean et al. (1998) and Leahy et al. tory-reared sea urchins can have huge gonads (1978) and in areas where seawater temperatures year round and may also develop gonads at a have strong seasonal variation. Also, gametoge- very small size. S. purpuratus were full of ga- nesis has been induced using temperature for metes by 6 months of age when they were only Anthocidaris crassispina, Hemicentrotus pulch- 10 mm in test diameter (Pearse et al. 1986) com- errimus, and Pseudocentrotus depressus (Yamamoto pared to wild populations where gonads were et al. 1988; Sakairi et al. 1989). not found until S. purpuratus versus 25–40 mm Photoperiodic control of annual reproduc- (Gonor 1972). tive cycles in sea urchins was first suggested The effect of diet on sea urchin reproduc- by Giese et al. (1958). These observations were tion is mostly seen in the size of the gonads and confirmed for S. purpuratus in an 18-month labo- does not effect gametogenesis. Sea urchins pro- ratory study (Pearse et al. 1986). For this spe- duce large gonads when a preferred food is cies, when animals were held in a photoperiod available, which results in high food ingestion. regime 6 months out of phase with laboratory In wild and laboratory populations, high feed- and field samples held at ambient photope- ing rates often result in extended gametogen- riod, S. purpuratus developed a gametogenic esis and spawning activity. Reproductive de- cycle 6 months out of phase. Individual S. velopment is often inversely related to somatic purpuratus that were moved between photope- growth in wild populations (Fuji 1967; Gonor riod regimes so that they experienced less than 1972; Pearse et al. 1986) and in laboratory stud- 12 h of daylight for 12 months had continuous ies (Unuma et al. 1996; Cook et al. 1998; Klinger gametogenesis. These results suggested either et al. 1998). In poor food conditions, natural short days stimulated gametogenesis or long populations tend to allocate more resources to days inhibited it. Confirmation of gametoge- reproduction than somatic growth (Thompson nic stimulation from short days was shown by 1982). Laboratory ration studies with sea ur- Bay-Schmith and Pearse (1987). chins have resulted in lower gonadal indices Commercially important, edible sea ur- but similar reproductive development (McBride chins appear to vary in response to photope- et al. 1999). When starved, sea urchins can de- riod manipulations. Applications of this con- crease in overall size and in gonad size cept to aquaculture include timing of product (Lawrence and Lane 1982; Levitan 1988). available for markets and sustaining breeding Diet does not appear to influence gameto- populations. In a study with S. droebachiensis, genesis except to possibly extend the mature groups of mature adults were held at ambient stage. Gonadal changes during the reproduc- photoperiod, in a 4-month advanced photope- tive cycle result in reorganization of nutrient riod, and fed an extruded pellet diet. Only males stores in the body wall and gonad. Nutrient showed gametogenesis stimulated by the ad- SEA URCHIN AQUACULTURE 201 vanced photoperiod. The ambient seawater tem- Processing and Marketing peratures used in these studies did not influence gametogenesis (Walker and Lesser 1998). Prior to 1985, a substantial amount of sea ur- In another study with S. droebachiensis, chin roe was salted, steamed, baked, or frozen adults were held in total darkness or all light for Japanese markets. The product is now sold for 8 months and fed L. digitata and L. hyper- primarily fresh. Sea urchins are stored in large borea. The natural population was used as the refrigerated rooms near 0°F for up to 3 d before control group. The number of mature males in processing, if necessary. Longer storage is the dark treatment was significantly greater avoided because it causes the gonads to get soft than the controls, but the reproductive condi- and dark. tion of S. droebachiensis held in the light treat- Processing consists of several steps. The ment was not significantly different than the test is split open and the roe is removed with a controls (Hagen 1997). It appears that males of spoon and placed in plastic strainers. The vis- S. droebachiensis have been more sensitive to the cera and other extraneous material is carefully photoperiod manipulations examined so far. removed from the gonads. For fresh uni, the plastic containers are placed in large tanks of 1 m by 3 m containing chilled seawater or brine Diseases and Parasites and a solution of anhydrous potassium alum,

KAl (SO4)2, until the roe becomes firm. Concen- Sea urchins are known hosts of over 100 patho- tration of alum vary between 0.4% and 0.7% and gens and parasites (Jangoux 1987a, 1987b, soak times vary between 15 min and 1 h. The 1987c, 1987d). Diseases caused by microorgan- roe is then drained, placed on absorbent mate- isms are usually bacteria or fungi. Sporozoans rial, and stored in a clean refrigerated room until are the most common cause of protistan dis- final cleaning and packing. Final cleaning is eases. Lesions of the body wall associated with done with tweezers or small forks to remove bacteria and mass mortalities of natural popu- attached membranes. Roe is packed in 150- or lations have been reported (Pearse et al. 1977; 250-g wooden boxes or bulk packs in larger Pearse and Hines 1979). Injury or other stress styrofoam trays. Boxes and trays are packaged is necessary for the formation of body wall le- with gonads of the same size and color together. sions (Gilles and Pearse 1986). Symbiotic tur- Whole, firm roe is placed on the top layer. The bellarians have been reported in echinoids and packaging process is critical. Workers who occur in the gut and coelm. Sea urchins act as package the gonads into boxes are the highest secondary hosts for trematodes, serving mainly paid in the plant and have a good eye for color as a vector and are passed to fish predators. and excellent manual dexterity. The best qual- During culture of sea urchin larvae, bac- ity roe is kept for the fresh market and highest terial contamination may occur. Larvae be- prices. Broken gonads, off color, large or soft come less robust or may die entirely and lar- roe are used for secondary products. Bulk- val arms regress. Bacterial diseases also in- packed roe is usually made into other products fect juvenile sea urchins in Japanese culture such as salted, steamed, baked, preformed, or systems (Tajima and Lawrence 2001). Mass frozen roe. After packaging, the boxes or trays mortalities occur in summer when seawater are placed into insulated cartons that fit into temperatures were greater than 20C°. Symp- foam boxes. Artificial coolant is added, the car- toms include black or green spots on body tons sealed and air freighted to Japan. Sanita- surfaces, partial spine loss, and discoloration tion is critical for the fresh roe product. Ultra- of the peristomium. The spring bacterial dis- violet treated water and good refrigeration ease occurs when seawater temperatures are maintains a clean environment. Labor costs are between 11° C and 13°C. rather high as all the work is done by hand Disease will be an important consideration (Kramer and Nordin 1979; Kato and Schroeter in sea urchin aquaculture as the experiences 1985). with bacteria diseases in juvenile S. intermedius The primary market for sea urchin roe is in Japan may be found with adults in grow-out Japan, where an auction system determines systems also. price daily. Color is extremely important for 202 MCBRIDE marketing. Up to eight grades of roe are used and sea urchin biology are necessary to develop by processors, and all dark or discolored roe is large scale enhancement operations. discarded. Texture and firmness are also criti- In Chile, hatchery construction and equip- cal marketing factors. Once the roe arrives in ment were estimated at $106,000 for larval rear- Japan, it is auctioned at the Tsukiji Market in ing and $7,000 for land-based grow-out tanks Tokyo. The prices depend on supply and de- to rear sea urchins 15 mm in test diameter. An- mand. Domestic roe always brings the highest nual costs were estimated at $23,000 for sala- price, but during winter months when domes- ries, $33,000 for fixed costs, and $9,100 for en- tic roe is not available, imported products fill ergy. If 15-mm juvenile Loxechinus albus are sold the demand and may receive high prices. for $0.29, the operation would be profitable. If Because sea urchin gonad products are rela- the young sea urchins were sold at $0.24, there tively expensive, many factors influence the would be no profit. This estimate requires two price. Among them are supply and demand fac- batches of 5-mm juveniles each year. Grow out tors such as Japanese domestic supply, total im- to 55 mm taking approximately 30 months is port supply, quality of imported roe, demand in estimated to cost $404,000 (Gonzales 2003). various markets, seasonal demand cycles, com- petition with other foods, and the exchange rate. Lower grade product may become more popu- The Future lar as more people eat in fast food sushi shops where preformed sushi is sold, rather than in Worldwide demand for edible seafood prod- expensive sushi bars where it is made to order. ucts, including sea urchin roe, is expected to The amount of imported urchin roe contin- continue increasing. Total world fishery har- ues to increase as the Japanese economy de- vests of edible products have stabilized around clines (Sonu 1995; Jones 1998). Sales of Japanese 70 mt since 1995. Sea urchin fishery harvests roe declined and so did that of imports, but the will probably remain around 100,000 mt per declines were due to decreased supply of ur- year or decline (Andrew et al. 2002). Fishery chins. However, lower price and take-away resource conditions fluctuate year to year due sushi shops are more popular in Japan today. to oceanographic events such as El Niño, food This low-end market increased dramatically in availability, and natural recruitment. There are response to economic recession in Japan over opportunities for sea urchin aquaculture un- the past 10 years or so. The Japanese public ac- der these conditions but development requires cepts the 100-g plastic cups that originated in several key pieces of information. Maine. This new packaging style has now Suitable diets for somatic and gonadal spread to other nontraditional exporting coun- growth and appropriate feeding regimes with tries such as Norway, Peru, and Chile. This prod- high feed efficiencies will be needed for gonadal uct targets supermarket chains and less expen- and somatic growth through the culture period sive restaurants. and to avoid environmental degradation. Com- With the steady demand for sea urchin plete feed programs addressing nutrition, physi- products in Japan, Europe, and North and South cal characteristics of the feed, and feed manage- America, interest in sea urchin aquaculture is ment will be essential for successful sea urchin growing worldwide. Although there are few aquaculture (Lawrence and Lawrence 2004). Pro- commercial operations at present, the experi- duction scale culture systems that include effec- mental projects investigating gonad enhance- tive broodstock maturation methods will reduce ment will probably lead to fully integrated cul- reliance on natural populations and must be ture operations. perfected. Aspects of sea urchin biology that have A preliminary economic feasibility study not been considered for aquaculture are behav- in Canada examined costs, stocking density, ioral considerations such as density, feed man- mortality rate, feeding, and operating costs for agement, and growth interactions for these gre- a land-based or in-water gonad enhancement garious animals. New product development in business (Burke 1997). Premium quality and response to changing consumer lifestyle and pref- high gonad yield are required for success in erences will make the industry more economi- such an endeavor. Knowledge of market factors cally effective and profitable. SEA URCHIN AQUACULTURE 203

Evaluating the costs to develop a sea ur- Agatsuma, Y., and H. Momma. 1988. Release of cultured chin aquaculture industry in a number of coun- seeds of the sea urchin Strongylocentrotus interme- tries must be analyzed given current and ex- dius (A. Agassiz) in the Pacific coastal waters of southern Hokkaido. I. Growth and reproductive cycle. pected markets. Appropriate sea urchin species Bulletin of Hokkaido Fisheries Research Station to culture should be given serious consider- 31:15–25. ation. Most studies have been on species cur- Anderson, J. M. 1966. Aspects of nutritional physiol- rently harvested in fisheries. These may not be ogy. Pages 329–358 in R. A. Boolootian, editor. the best species for aquaculture (Lawrence Physiology of Echinodermata. Wiley, New York. 1998). Relatively reliable methods to culture Andrew, N. L., Y. Agatsuma, E. Ballesteros, D. K. A. tens of thousands of sea urchins to juvenile size Barnes, A. G. Bazhin, L. W. Botsford, A. Bradbury, A. Campbell, E. P., Creaser, J. D. Dixon, are well established. However, grow-out meth- S. Einarsson, P. Gerring, K. Hebert, M. Hunter, S. ods are not well described. B. Hur, C. R. Johnson, M. A. Juinio-Menez, P. Development of sea urchin aquaculture Kalvass, R. J. Miller, C. A. Moreno, J. S. Palleiro, will also rely on positive interactions of the com- D. Rivas, S. M. L. Robinson, S. C. Schroeter, R. mercial fisheries and aquaculturists. Fishery S. Steneck, R. I. Vadas, D. A. Woodby, and Z. harvesters may participate in aquaculture of sea Xiaoqi. 2002. Status and management of world urchins by supplying broodstock animals for sea urchin fisheries. Oceanography and Marine Biology Annual Review 40:343–425. enhancement programs. Aquaculture of sea ur- Barker, M. F., J. A. Keogh, J. M. Lawrence, and A. L. chins would have many benefits relative to Lawrence. 1998. Feeding rate, absorption efficien- quality requirements for sea urchin products, cies, growth, and enhancement of gonad produc- as quality control will be easier to manage. And tion in the New Zealand sea urchin Evechinus given the increasing demand for the expensive chloroticus Valenciennes (Echinoidea: Echinoder- sea urchin products, successful aquaculture mata) fed prepared and natural diets. Journal of Shellfish Research 17(5):1583–1590. ventures are likely to develop in many coun- Basuyaux, O., and M. Mathieu. 1999. Inorganic ni- tries. trogen and its effect on growth of the abalone Strong aquaculture research programs cur- Haliotis tuberculata Linnaeus and the sea urchin rently exist in many countries. It will be the re- Paracentrotus lividus Lamark. Aquaculture sponsibility of scientists, fishermen, students 174:95–107. and other sea urchin enthusiasts to utilize these Bay-Schmidt, E., and J. S. Pearse. 1987. Effect of fixed funds effectively with the objective of develop- dlengths on photoperiodic regulation of gametogenesis in the sea urchin Strongylocentrotus ing a profitable and environmentally sound sea purpuratus. International Journal of Invertebrate urchin aquaculture industry. Reproduction and Development 11:287–294. Birulés, A. 1990. Marketing of aquaculture products. Pages 44–49 in R. Flos, L. Tort, and P. Torres, Acknowledgments editors. Mediterranean aquaculture. Ellis Hor- wood, New York. This chapter was supported by the National Blin, J. L. 1997. Culturing the purple sea urchin, Sea Grant College Program of the U.S. Depart- Paracentrotus lividus, in a recirculating system. Bulletin of the Aquaculture Association of Canada ment of Commerce’s National Oceanic and 97(1):8–13. Atmospheric Administration under NOAA Bureau, D., A. Campbell, and E. B. Hartwick. 1997. Grant #NA06RG0142, Project Number A/EA-1 Roe enhancement in the red sea urchin Strong- through the California Sea Grant College Pro- ylocentrotus franciscanus fed the bull kelp gram. The views expressed herein do not nec- Nereocystis luetkeana. Bulletin of the Aquacul- essarily reflect the views of any of those organi- ture Association of Canada 97(1):26–29. Burke, B. 1997. Sea urchin gonad enhancement: pre- zations. liminary economic feasibility analysis. Bulletin of the Aquaculture Association of Canada 97(1):45– 50. References Bustos, E., and S. Olave. 2001. Manual: sea urchin culture (Loxechinus albus). Instituto de Fomento Agatsuma, Y. 1998. Aquaculture of the sea urchin Pesquero FONDEF D96 I 1101, Puerto Montt, (Strongylocentrotus nudus) transplanted from cor- Chile. alline flats in Hokkaido. Japanese Journal of Shell- Byrne, M. 1990. Annual reproductive cycles of the fish Research 17(5):1541–1547. commercial sea urchin Paracentrotus lividus from 204 MCBRIDE

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