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A review of the research on the Australasian sea cucumber, Australostichopus mollis (echinodermata: holothuroidea) (Hutton 1872), with emphasis on aquaculture.

ABSTRACT The Australasian sea cucumber, Australostichopus mollis, has an extensive distribution; it is found along the coast of southern Australia and throughout New Zealand's coastal waters. This species is very similar in appearance to the highly prized Japanese sea cucumber, Apostichopus japonicus, and as a consequence has attracted increasing interest for commercial fishing and aquaculture. The sea cucumber A. mollis currently supports a small commercial fishery in New Zealand of 10-20 t/y. A review of the research on this sea cucumber indicates that the development of aquaculture for this species has been impeded by a general lack of background biological knowledge. Future research needs to be targeted toward resolving the constraints the aquaculture industry is facing for this species, including reliable methods for broodstock conditioning, mass larval rearing, juvenile nutrition and husbandry, as well as development of effective grow-out technology and identification of suitable farming sites.

KEY WORDS: sea cucumber, Australostichopus mollis, fisheries, aquaculture, sea ranching, beche-de-mer

INTRODUCTION

The commercial aquaculture of sea cucumbers has begun in relatively recent times in response to a constrained supply from wild stocks and increasing market demand, leading to a rise in prices (Toral-Granda et al. 208). Most of the sea cucumbers harvested worldwide are exported to Asian markets, especially China, where they have been regarded for centuries as a nutritious food with health-giving properties (Choo 2008). Sea cucumbers can be traded fresh or alive, but they are usually sold gutted and dried. The dried sea cucumber is often known as beche-de-mer, trepang, or haishen. There is a huge diversity of species of sea cucumbers (66 species) that are harvested commercially and traded around the world, with the majority of these species belonging to the order Aspidochirotida, and only a few to the order Dendrochirotida (Purcell et al. 2010). Most of these species come from the multispecies sea cucumber fisheries that are found throughout the tropical regions of the world (Kinch et al. 2008). In higher latitudes with temperate waters, sea cucumber fisheries tend to be monospecific (Hamel & Mercier 2008).

The price of sea cucumbers varies greatly among species and also within species, depending on the size of the animals and processing methods (Ferdouse 2004, Purcell et al. 2012b). Therefore, large-scale commercial aquaculture has only been developed for a small number of the most valuable species: the temperate Japanese sea cucumber, Apostichopusjaponicus; and the tropical sandfish, Holothuria scabra (Hulling et al. 2004, Renbo & Yuan 2004, Xiyin et al. 2004, Duy 2012, Gamboa et al. 2012). Both species can fetch more than US$300/kg (dried) at retail markets for large and well-processed specimens (Purcell et al. 2010). Aquaculture technology (hatchery and grow-out technology) is also being developed for several other temperate and tropical sea cucumber species around the world, such as Isostichopus fuscus, Athyonidium chilensis, Cucumaria frondosa, Parastichopus californicus, Stichopus horrens, Holothuria fuscogilva, and Actynopiga spp. (Paltzat et al. 2008, Guisado et al. 2012, Jimmy et al. 2012, Mercier et al. 2012, Nelson et al. 2012). Another such species is the Australasian sea cucumber, Australostichopus mollis. This is an aspidochirotid sea cucumber that is very similar in appearance to the valuable Japanese species, A. japonicus, and, as a consequence, can be sold into the same markets at good prices.

Despite the strong commercial interest in the development of fisheries, sea ranching, and aquaculture of the Australasian sea cucumber, progress has been slow because of a lack of comprehensive knowledge about the biology of this species. Although a considerable amount of research has been conducted on this sea cucumber, much of this information is widely dispersed and contained in unpublished reports and research theses mainly from New Zealand, with very few studies in Australia. Therefore, the aim of this review is to collate the available information on Australostichopus mollis and identify those knowledge gaps creating difficulties for the commercial aquaculture development of this species.

TAXONOMY

The sea cucumber Australostichopus mollis is the most conspicuous sea cucumber species in shallow waters along the coastlines of New Zealand and southern Australia. It is commonly known as the brown sea cucumber because of its coloration, or as the Australasian sea cucumber because of its distributional range. This species was first described as Holothuria mollis (Hutton 1872). Subsequently, other specific names were applied, such as Holothuria robsoni (Hutton 1878), Stichopus sordidus (Theel 1886), Holothuria victoriae (Bell 1887), Stichopus mollis (Dendy 1896), and Stichopus simulans (Dendy & Hindle 1907), with the assignment of the various names based mostly on comparisons of the morphology of ossicles in the body wall. Of all these names, Stichopus mollis has been most widely accepted and used for this species. Recently, this species was reclassified as Australostichopus mollis because of differences in morphology (including ossicles) and chemical composition, a taxonomic distinction that has subsequently been supported by analyses of genetic markers (Moraes et al. 2004, Byrne et al. 2010).

BIOLOGY AND ECOLOGY

Distribution and Habitat

The sea cucumber Australostichopus mollis can be found all along the coast of New Zealand, including The Snares Islands and Chatham Rise, as well as along the southern coast of Australia, including all of Tasmania (Fig. 1) (Joshua 1914, Clark 1922, Hickman 1962, Pawson 1970, Fenwick &Horning 1980, Lawler 1998, Cohen et al. 2000, Fromont et al. 2005, Shears & Babcock 2007). However, there is some doubt whether the individuals found along the southwestern coast of Australia correspond to A. mollis (Maria Byrne, The University of Sydney, Australia; pers. comm. 2013).

The sea cucumber Australostichopus mollis is a subtidal animal that is typically found in shallow waters of sheltered coastlines and occasionally in intertidal pools, but it has also been recorded at depths of up to 1,000 m (Dawbin 1949a, Dawbin 1950, Pawson 1970, Sewell 1990). It can inhabit a wide range of substrates, such as rocky reefs and biogenic reefs (beds of mussels, polychaetes, and bryozoans), as well as sediments of a range of grain size from gravel to mud (Dawbin 1949a, Dawbin 1950, Pawson 1970, Probert et al. 1979, Sewell 1990, Smith et al. 2005, Wing et al. 2008, Slater et al. 2010, Morgan 2011). Juveniles and adults generally occupy different habitats. This pattern of distribution is possibly related to the cryptic behavior of the juveniles, which are often found under boulders in shallow waters, whereas adults tend to be found out in the open and in deeper waters than juveniles (Joshua 1914, Sewell 1990). Occasionally, juveniles and adults can be found together in high numbers in habitats where suitable juvenile shelter

is available within adult habitats, such as where large, curved shell fragments from horse mussels (Atrina zelandica) are overlying areas of organically enriched mud substrate (Slater et al. 2010).

External Appearance

The sea cucumber Australostichopus mollis is a medium-size species of sea cucumber, reaching up to 300 g in wet weight and up to 25 cm in length (Dawbin 1949a, Sewell 1990). This species has the typical cylindrical shape of sea cucumbers, with the mouth located anteriorly, facing the seafloor, and the anus positioned at the posterior end. The dorsal surface of this species is characterized by a series of irregularly positioned papillae of different sizes and shapes (Dendy 1896, Sewell 1987), although the ventral surface is smoother, with the presence of ambulacral podia, or tube feet, which are used for locomotion (Dendy 1896, Sewell 1987). The coloration of this species varies significantly among individuals; they can be either a single color (from dark brown to white) or may have a combination of different brown, yellow, and cream--white tones, but usually they are dominated by the brown tones (Dendy 1896, Sewell 1987). Some individuals are mottled, but in most, the coloration of the ventral and dorsal surfaces are different, with the color of the ambulacral podia varying widely among individuals (Dendy 1896, Sewell 1987). The highly individual patterns of coloration permits the use of reliable photo identification of individual sea cucumbers for research of this species; they are difficult to tag using conventional physical marking methods (Raj 1998a, Stenton-Dozey 2007b).

Internal Anatomy

The internal anatomy has been described as being similar to other sea cucumbers of the Stichopus genus, with a large and undivided coelom filled with fluid (Sewell 1987). The coelom volume of this species can change by as much as 5% as a result of the exchange of seawater in the coelom, facilitated by cloacal pulsations used to ventilate the respiratory trees (Robertson 1972).

The circulation of oxygen and nutrients is achieved by the perivisceral coelomic fluid, as well as the hemal and water vascular systems, which are associated with the digestive system and the major sites of oxygen uptake in the respiratory trees, body wall, and podia (Fig. 2) (Robertson 1972, Lawrence 1987). Oxygen transportation is facilitated by hemoglobin in dendrochirotid and molpadiid sea cucumbers; however, the presence of any such respiratory pigment is yet to be described in Australostichopus mollis (Baker & Terwilliger 1993, Hoffmann et al. 2012). The water vascular system of this species is comprised of a circular canal as well as 5 radial canals, canals to the ambulacra, oral tentacles with their ampullae, a stone canal, and a madreporite (Fig. 2) (Sewell 1987). This species has a single polian vesicle, an elongated digestive system (folded twice to fit inside the coelom), a pair of well-developed respiratory trees, gonads (consisting of branched tubes divided in 2 parts), and no cuverian organs (Fig. 2) (Sewell 1987). Most of these internal organs are suspended in the coelom by mesenteries (Sewell 1987). Under situations of extreme stress, rarely encountered in their natural environment, this species can undergo autotomy and evisceration of their digestive tract and respiratory trees (Dawbin 1949a, Dawbin 1949b, Sewell 1990). Both small juveniles (around 8 g) and large adults (up to 300 g) are able to recover from this, and in adequate conditions it takes around 110 days to recommence feeding, and more than 145 days to regenerate the full extent of the alimentary canal, whereas the full recovery of the respiratory trees takes longer (Dawbin 1949a).

Reproduction and Early Development

The sea cucumber Australostichopus mollis is dioecious and reaches sexual maturity at more than 75 g wet weight (Sewell 1987, Raj 1998b). It has an annual reproductive cycle, spawning synchronously during the austral summer (Sewell 1990, Sewell 1992, Sewell & Bergquist 1990, Archer 1996, Raj 1998b). Individuals from different latitudes have shown different patterns of gonad maturation, with populations in northern New Zealand completely reabsorbing their gonads after spawning, whereas individuals in southern parts of the country do not completely reabsorb the gonad and, instead, have progressive gonadal maturation during the winter (Sewell & Bergquist 1990, Sewell 1992, Archer 1996, Sewell et al. 1997, Raj 1998b). The sea cucumber A. mollis has nocturnal spawning behavior, which has been observed in the wild, with individuals reaching their anterior end up into the water column while releasing their gametes (Archer 1996). This species has indirect development with more than one larval stage, starting with a swimming and feeding auricularia larva, which after around 2 wk develops into a nonfeeding doliolaria larva (Table 1) (Archer 1996, Stenton-Dozey & Heath 2009). Then, the doliolaria metamorphoses into a pentactula larva, which settles to the seafloor at around 25 days after fertilization and starts deposit-feeding as a competent juvenile sea cucumber (Table 1) (Archer 1996, Stenton-Dozey & Heath 2009). There is no clear evidence whether there is any preferred substrate for settling juveniles in the wild, because newly settled individuals are very cryptic and are rarely found (Joshua 1914, Sewell 1990). However, juvenile recruitment appears to be highly localized and is thought to be related to patterns of larval settlement, rather than restricted availability of suitable juvenile habitat (Slater & Jeffs 2010).

Feeding Behavior

As a deposit-feeding sea cucumber, Australostichopus mollis uses its oral tentacles to feed on the organic particles accumulated on the seafloor by gathering the particles with shield-shaped tentacles and bringing them inside the mouth as the animal moves forward along the seafloor (Roberts et al. 2000). This species has the capability of exploiting different food sources in different habitats by ingesting inorganic particles of a wide range of sizes and by actively selecting the associated organic material, including live microorganisms, decaying material of plant and animal origin, and the feces of other marine organisms (Roberts et al. 2000, Wing et al. 2008, Slater et al. 2009, Slater & Jeffs 2010, Slater et al. 2011a, Zamora & Jeffs 2011, MacTavish et al. 2012). On sediments with relatively low levels of organic food availability (around 1%), individuals actively seek out patches with greater organic content; however, at greater organic levels (around 3%), this behavior is greatly diminished (Slater et al. 2011a). Most individuals of A. mollis are nocturnally active feeders, although feeding during day has been observed on occasion for both juveniles and adults (Slater 2006, Zamora & Jeffs 2011).

Predators, Parasites, and Commensals

Predation of Australostichopus mollis in the wild has been poorly documented, with only a small number of predation events being reported by the asteroid Luidia varia (Sewell 1990), and by the giant boarfish Paristiopterus labiosus (Russell 1983). Under laboratory holding conditions, the omnivorous crab Notomithrax ursus has also been observed preying on A. mollis (Woods 1993).

This sea cucumber can serve as host for symbiotic organisms, such as a group of subcuticular bacteria living between the epidermal cells and the outer cuticle (Lawrence et al. 2010), an isopod that can be found on the skin of the sea cucumber (Menzies & Miller 1955), a platyhelminth that lives in the coelom (Cannon 1990), and turbellarian parasites that live in its intestine (Hickman 1955, Jondelius 1996).

FISHERIES

Fishing History in Australasia

There is no history of traditional or recreational fishing of Australostichopus mollis in New Zealand or Australia. In more recent years, these sea cucumbers have been harvested increasingly by Asian immigrants at coastal locations around major urban centers in New Zealand, a localized activity which is poorly represented in recreational fishing surveys (Ministry of Fisheries 2011). This species is the only sea cucumber fished commercially in New Zealand, and despite being present in significant quantities in southern parts of Australia, it is not harvested commercially. Inquiries with Australian state fisheries management agencies indicate they do not intend to allow the commercial fishing of this species in their waters because of a lack of commercial interest and concerns about the difficulty of managing new fisheries of this kind (Kim Evans, Department of Primary Industries, Parks, Water and Environment, Tasmania; pers. comm. 2013).

Most of the commercial landings of sea cucumbers in New Zealand are a result of bycatch in other fisheries, such as scallop dredging and bottom trawling (Ministry of Fisheries 2011). The annual commercial landings have been relatively low (<10 t) since landing records began to be recorded in 1991, when the value of this species in export markets was first recognized (Fig. 3) (Ministry of Fisheries 2011). During the early 2000s, there was a significant increase in total annual landings of these sea cucumbers before they were included in the quota management system for fisheries in 2004, after which time the annual landings fluctuated (Fig. 3) (Ministry of Fisheries 2011).

Stock Assessment and Management

There has only ever been one systematic attempt at stock assessment in southwestern New Zealand, in four fiords: Thompson Sound, Bradshaw Sound, Charles Sound, and Doubtful Sound (Mladenov & Guerring 1997, Mladenov & Campbell 1998). This assessment resulted in an estimate of an average of 1,574 kg sea cucumbers/km of coastline within the surveyed fiords. On this basis, the estimate for the total sea cucumber biomass present within in a depth range of 0-20 m all of Fiordland was at around 1,950 t (Mladenov & Guerring 1997, Mladenov & Campbell 1998). There has been only one attempt to measure population parameters such as size at age, growth, and mortality of a small population in shallow coastal waters in northern New Zealand (Morgan 2012).

Because of the lack of abundance and distribution information of wild stocks in New Zealand, fisheries managers established conservative harvesting limits when sea cucumbers where incorporated into the quota management system (Ministry of Fisheries 2011). A total allowable commercial catch of 35 t was established, which is comparatively small when considering the magnitude of the landings for Apostichopus japonicus (1,000 t and 6,000 t for Japan and the Republic of Korea, respectively) and Parastichopus californicus (around 400 t for Canada, British Columbia) (Choo 2008, Hamel & Mercier 2008). This 35-t total allowable commercial catch was allocated into 15 arbitrary fishery management areas in which sea cucumbers can only be harvested commercially by free diving (Fig. 4) (Ministry of Fisheries 2011). Of these fishery management areas, the northeastern and southeastern New Zealand areas, together with the Cook Strait area (SSC 1B, 3, and 7A, respectively) consistently have the highest reported annual landings in recent years, with typically more than 2 t each (Fig. 4) (Ministry of Fisheries 2011). However, there are no further harvesting controls on the commercial fisheries of this species, such as minimum legal size, fishing season, or protected nursery zones (Ministry of Fisheries 2011). There are currently no controls on the recreational harvesting of sea cucumbers. The effect of marine protected areas on sea cucumber populations cannot be assessed because of the low fishing pressure in unprotected areas, as seen in a study that included Australostichopus mollis in Tasmania (Barrett et al. 2009).

Processing and Market Value

Most of the sea cucumbers harvested in New Zealand are processed locally and exported to Asia. Usually, the sea cucumbers are gutted, boiled for up to 20 min in saltwater, and then air-dried while covered in salt (Andrew Jeffs, pers. obs.). The highest prices are paid for dried sea cucumbers that are larger in size, evenly dark brown, and with large and erect papillae. There is considerable individual variability in terms of the final appearance of dried sea cucumbers after processing, which is addressed through careful grading. The dry weight recovery of sea cucumbers of this species is around 9% of the wet weight of the freshly landed sea cucumbers, depending on the extent of drying and the addition of salt during processing (Zamora unpubl. data).

This sea cucumber is considered a medium- to high-value species; however, it can reach market values more than US$275/kg dry weight (Purcell et al. 2012b). There is the potential to add further value to this species through the extraction of bioactive compounds for manufacturing high-value biopharmaceuticals or human health supplements (Kelly 2005, Bordbar et al. 2011). Some of the bioactive compounds that have been described from Australostichopus mollis include long-chain fatty acids, collagens, complex carbohydrates, and triterpene glycosides (Freeman & Simon 1964, Baker 1998, Moraes et al. 2004, Moraes et al. 2005, Liu 2010, Yibmantasiri et al. 2012). There is also an opportunity to develop additional high-value products from the viscera (i.e., digestive tract, respiratory trees, and gonads) that is usually discarded during processing (Morgan & Archer 1999, Morgan 2000c).

AQUACULTURE ADVANCES, CONSTRAINTS, AND FUTURE DIRECTIONS

Interest in the aquaculture of Australostichopus mollis started during the early 2000s as a result of the high value of the species in Asian markets, and the discovery of the possibility of co-culturing with other aquaculture species in New Zealand, such as the green-lipped mussel, Perna canaliculus, and the native abalone, Haliotis iris (Morgan & Archer 1999, Morgan 2000a, Morgan 2000b, Morgan 2000c, Morgan 2001, Maxwell 2006, Stenton-Dozey 2007a, Morgan 2009a). Information useful for the development of the aquaculture of this species is scarce, especially in relation to effective hatchery technology and the biology and ecology of postsettlement juveniles (i.e., nursery). Therefore, in the following sections, the available information is summarized, with emphasis on identifying knowledge gaps for the aquaculture of A. mollis.

Hatchery and Nursery Technology Development

Using current hatchery and nursery culture methods for this sea cucumber, it can take almost a year after larval settlement to raise small Australostichopus mollis juveniles with a mean weight of 0.05 g, and with only a few individuals reaching 2-5 g (Stenton-Dozey & Heath 2009, Heath et al. unpub). The efficiency of production of juvenile A. mollis could be greatly improved through the development of more cost-effective technology customized for this species (Morgan 2002, Morgan 2004a, Morgan 2005a, Morgan 2005b, Morgan 2008a). This becomes evident when considering that the nursery production of Apostichopus japonicus and Holothuria scabra requires only a few months after settling, and 1 or 2 y of subsequent grow-out to reach commercial sizes of around 300 g in China and Vietnam, respectively (Pitt & Duy 2004, Renbo & Yuan 2004). For these species, the reduction in the nursery production time came after many years of research and development to establish the efficient hatchery and nursery techniques used today. This research and development has been conducted since the 1950s for A. japonicus and since the 1990s for H. scabra (James et al. 1994, Pitt & Duy 2004, Renbo & Yuan 2004, Xiyin et al. 2004, Duy 2012, Juinio-Menez et al. 2012b, Mills et al. 2012). These improvements allowed the production of large numbers of juveniles in a simplified and cost-effective manner, stabilizing the production and allowing the expansion of the commercial grow-out of these species. The development of broodstock management, larval rearing, nursery culture, and techniques for transporting juveniles were key to this successful commercial aquaculture development of A. japonicus and H. scabra, and require marked improvement for A. mollis, and are discussed further in the following subsections.

Broodstock Management

Broodstock for Australostichopus mollis are currently obtained from the wild during their natural spawning season (Sewell 1990, Sewell & Bergquist 1990, Sewell 1992, Archer 1996, Morgan 2003). Spawning is enhanced by collecting individuals within 1 wk after the full moon and exposing them to seawater temperatures of around 3-5[degrees]C above ambient (Archer 1996, Maxwell 2006, Morgan 2007d, Morgan 2009b). This approach to broodstock management is unreliable, because not all individuals have mature gonads or respond to the spawning stimulus, which affects the number and quality of the gametes obtained (Battaglene et al. 2002, Hamel & Mercier 2004, Eeckhaut et al. 2012). The use of wild broodstock is also a limitation in terms of introducing effective selective breeding through the careful broodstock selection from superior-performing aquaculture stock. Being confined to the short, natural breeding season is also inefficient in terms of the effective use of hatchery and nursery infrastructures. Therefore, there is a need for a more reliable method for obtaining good-quality female and male gametes throughout the year in large numbers (Morgan 2005c). This can be achieved through conditioning captive broodstock by manipulating diet and holding conditions to obtain mature gonads with high-quality gametes, and by developing more reliable spawning methods (Hamel & Mercier 2004, Morgan 2004b, Agudo 2006, Leonet et al. 2009, Gamboa et al. 2012). An alternative to unreliable forced spawning induction is in vitro fertilization, which has been tested successfully in Holothuria scabra; however, its effectiveness in A. mollis has to be proved (Eeckhaut et al. 2012).

Retaining individual broodstock that respond well to spawning stimuli and yield large numbers of good-quality gametes with the highest fertilization rates has been shown to be a rapid route for improving broodstock performance in Australostichopus mollis (Morgan 2007a, Morgan 2007b, Morgan 2007c, Morgan 2009d). The development of complete control over broodstock will allow for selective breeding, the application of which has considerable potential to improve the value of this species. Selective breeding could improve traits related to production and market appeal, such as fast growth and dark body coloration with large papillae. However, first it will be necessary to determine the extent that these commercially important traits are genetically determined in A. mollis.

Larval Rearing

The food requirements of the planktotrophic larvae of Australostichopus mollis is poorly understood, despite it being critical to effective hatchery production, because larvae in poor nutritional condition fail to complete metamorphosis to post-settled juvenile (Archer 1996, Morgan 2007a, Morgan 2007c). Researchers have raised A. mollis larvae (auricularia) with mono and mixed cultures of microalgal species, including Dunaliella sp., Phaedoctylum sp., Nannochloropsis oculata, Isochrysis (T-iso), and Chaetoceros muelleri, at different concentrations, with the best results obtained with a mixture of microalgae (N. oculata, Isochrysis (T-iso), and C. muelleri) supplied at concentrations between 3,000 cells/mL and 5,000 cells/mL (Archer 1996, Maxwell 2006, Morgan 2008b, Heath et al. unpub). To reduce costs and use cultured microalgal feeds efficiently, the feeding rate of the auricularia should be adjusted carefully as they grow by checking the presence of microalgae in the digestive tract of the larvae (Renbo & Yuan 2004). More efficient larval production for A. mollis may also be possible by using 1 species of cultured microalgae or commercially available algal pastes, which have been shown to be effective in the larviculture of Holothuria scabra (Hair et al. 2011, Duy 2012, Gamboa et al. 2012). Resolving these larviculture issues should be relatively straightforward, because it appears that the timing of larval development is associated with the nutritional status of the larvae, which can be evaluated indirectly by checking the readily visible hyaline spheres in the transparent larvae of A. mollis (Archer 1996, Morgan 2008b, Morgan 2009c, Stenton-Dozey & Heath 2009, Morgan 2010, Peters-Didier & Sewell 2012). In addition, to determine optimum larval feeding regimes, a variety of other standard larviculture husbandry parameters also need to be optimized, such as larval stocking densities, seawater exchange, temperature, oxygen, salinity, and pH levels, as these are poorly understood in this sea cucumber species but have been shown to be critical in the larviculture of other commercially important sea cucumber species (Battaglene et al. 1999, Kashenko 2000, Renbo & Yuan 2004, Li & Li 2010, Duy 2012).

Induction of larval settlement in Australostichopus mollis has been achieved successfully using methods that are identical to those used for Apostichopus japonicus. This involves the use of polycarbonate and polyethylene sheets preconditioned in seawater to develop a natural biofilm that promotes larval settlement in the sea cucumbers (Xiyin et al. 2004, Heath et al. unpub). However, simplified methods for larval settlement that have been described for Holothuria scabra and A. japonicus could also be tested to reduce operational costs and the chances of introducing harmful animals, such as copepods (Xilin 2004, Juinio-Menez et al. 2012b, Mills et al. 2012). One of these methods consists of using clean settlement plates and then providing food for the sea cucumbers after they have settled to the plates (Xilin 2004). Alternatively, the settlement plates could be covered with a paste of Spirulina sp. that induces settlement and serves as an initial food for the settled individuals (Juinio-Menez et al. 2012b, Mills et al. 2012).

Nursery Culture of Postsettled Juveniles

The nursery culture of postsettled juveniles of Australostichopus mollis is a significant bottleneck to the development of commercial aquaculture of this species. Only one study reports the nursery rearing of large numbers of early juveniles (Heath et al. unpub). In that study, the postsettlement juveniles were taken from the settlement plates and placed into tanks where they were fed with an artificial diet consisting of fine sediment mixed with powdered macroalgae and benthic diatoms (Heath et al. unpub). However, the growth rate of these juveniles was very poor using these nursery culture methods (Heath et al. unpub). Therefore, alternative ways to culture the postsettlement juveniles should be tested to improve nursery production. The early juveniles could be held in tanks with or without sediment (Pitt & Duy 2004, Xilin 2004, Xiyin et al. 2004), or they could be placed in earthen ponds or at sea (e.g., inside floating or bottom-set fine-mesh cages ("hapas"), or in bottom cages or in pens), all of which have proved successful in other species of sea cucumber (Pitt & Duy 2004, Lavitra et al. 2010, Duy 2012, Juinio-Menez et al. 2012b). Depending on the system used, it may also be necessary to supply additional food for the juvenile sea cucumbers (Pitt & Duy 2004, Xilin 2004, Xiyin et al. 2004). The lack of availability of earthen ponds in New Zealand and Australia that would be suitable for culturing early juvenile A. mollis means that the early nursery culture will need to be developed in indoor tanks, as it is in Apostichopus japonicus (Xilin 2004, Xiyin et al. 2004). However, the potential for nursery culture in ponds or in the sea should not be dismissed, because these culture methods could reduce production costs substantially, especially in terms of the costs of supplying food, provided adequate nursery locations are selected (Pitt & Duy 2004, Duy 2012, Juinio-Menez et al. 2012b). Alternatively, finding more effective feeds, either natural or artificial, for the early juveniles in nursery culture is also important because it is likely to accelerate growth rates and reduce production times substantially (Hulling et al. 2004, Watanabe et al. 2012). For example, early postsettlement juvenile A. mollis of around 100 mg increased their weight on average by 3-fold over 6 wk when feeding on mussel waste compared with barely any growth on artificial diets (Zamora et al. in prep.). Although effective feed is the primary determinant for improving the performance of nursery cultured A. mollis, a range of other husbandry variables also warrant further research, including the determination of optimum stocking densities and seawater parameters (Pitt & Duy 2004, Renbo & Yuan 2004, Xiyin et al. 2004, Agudo 2006, Mercier et al. 2012). The development of adequate grading techniques to separate the fast-growing juveniles, and releasing the growth potential of smaller individuals, are also needed (Battaglene & Seymour 1998, Yin-Geng et al. 2004).

Transportation of Juveniles for Grow-out

The transport of juvenile sea cucumbers from nursery facilities to grow-out locations has proved problematic in other species of sea cucumbers (Purcell et al. 2006a, Sun et al. 2006). Transportation of juvenile Australostichopus mollis can be done with or without seawater for different amount of times (Zamora & Jeffs, unpub.). The juveniles can be transported without seawater only if desiccation is avoided, and for short periods of time (up to 8 h), whereas transportation with seawater can be done for longer periods of time, although careful monitoring of oxygen and pH levels is required (Zamora & Jeffs, unpubl.). However, it is still not known whether hatchery-reared juveniles of this species of sea cucumbers require acclimation prior to release into grow-out sites (Dance et al. 2003, Purcell et al. 2006a, Purcell & Simutoga 2008). In this regard, the size of A. mollis juveniles used for stocking grow-out sites is critical because, in other species of sea cucumbers, larger juveniles have proved consistently to have better chances of survival, growing faster than smaller ones (Purcell 2004, Renbo & Yuan 2004, Purcell & Simutoga 2008, Mills et al. 2012, Purcell 2012).

Alternatives for Grow-out of Sea Cucumbers

Sea cucumbers produced in hatchery and nursery facilities can be grown-out in a variety of different ways, such as releasing them into the wild to restore the depleted spawning biomass of a wild population (i.e., restocking) or to increase the fishery yield of overfished populations of sea cucumbers (i.e., stock enhancement) (Purcell 2004, Bell et al. 2005, Purcell 2012). Currently, this is not the case for Australostichopus mollis, but it may be necessary if demand and commercial awareness of the market potential of this species increases, leading to a reduction of the natural stocks through increased commercial harvesting (Bell & Nash 2004). The most commonly used grow-out systems for sea cucumbers are earthen ponds, sea pens, sea cages, and release into delimited areas of seabed (i.e., sea ranching) (Chen 2004, Renbo & Yuan 2004, Yaqing et al. 2004, Purcell & Simutoga 2008, Agudo 2012, Duy 2012, Mills et al. 2012). An alternative grow-out method that has gained interest recently is the feasibility of using sea cucumbers as a critical component of integrated multi-trophic aquaculture systems by using their capacity to feed on organic waste generated by the aquaculture of other species, such as shellfish or fish (Ahlgren 1998, Kang et al. 2003, Zhou et al. 2006, Bell et al. 2007, Slater & Carton 2007, Paltzat et al. 2008, Maxwell et al. 2009, Ren et al. 2012, Yokoyama 2013).

All these methods of grow-out could potentially be used in Australostichopus mollis; however, further research is needed regarding the optimal seawater parameters for the growth of this species. So far, it is known that the growth and feeding activity of juveniles of A. mollis from northern New Zealand become negatively affected when temperature increases from 15-21[degrees]C, and that temperatures around 24[degrees]C are lethal (Zamora & Jeffs 2012a). In southern populations, negative effects of seawater temperature manifest around 18[degrees]C, which suggests there are latitudinal differences in temperature tolerance in this species (Maxwell et al. 2009). Salinity also affects feeding activity and survival, with juvenile sea cucumbers found to decrease their feeding activity as salinity decreased from 34 ppt to 24 ppt, and dying after 5 days of exposure to seawater at 28 ppt (Zamora unpubl, data). Oxygen levels may also become a problem under confined culture situations (e.g., earthen ponds) when sea cucumbers are cultured at higher densities, despite A. mollis having a low metabolic rate and corresponding oxygen demand (Robertson 1972, Maxwell et al. 2009, Zamora & Jeffs 2012a). However, in these situations, organic loading may place additional pressures on oxygen demand at the sediment--seawater interface where sea cucumbers dwell (Renbo & Yuan 2004). The effect of pH has not been researched in A. mollis, but research in Apostichopus japonicus suggests that pH levels should not go below a pH of 7.9 (Renbo & Yuan 2004). Overall, increasing the knowledge of how A. mollis responds to environmental variables in the laboratory and under culture conditions is essential for the development of the aquaculture of this species. This information will be particularly important for the selection of the most suitable grow-out locations and culture system to be used.

Pond Culture

Pond culture of sea cucumbers is common practice in China (>7,000 ha) as well as in other tropical regions of the world, because abandoned shrimp ponds can often be adapted for growing sea cucumbers, thus saving in construction costs (Renbo & Yuan 2004, Yaqing et al. 2004, Agudo 2012, Duy 2012). However, not all sea cucumbers perform well under pond culture conditions, with some species found to lose weight and die because the culture conditions do not resemble their natural habitat (Mercier et al. 2012, Purcell et al. 2012a). The muddy floor of earthen ponds should not be problematic for Australostichopus mollis because this species can be found naturally in high numbers in shallow waters with fine sediment (Slater et al. 2010). However, because typically there is no continuous water flow in pond culture, the sea cucumbers may be exposed to water stratification and even to daily and seasonal fluctuations in seawater temperature and salinity, which may impact their growth and survival (Pitt & Duy 2004, Renbo & Yuan 2004, Yaqing et al. 2004, Bell et al. 2007, Yuan et al. 2010, Agudo 2012, Bowman 2012). Usually, in ponds, there is some natural supply of food for the sea cucumbers; however, depending on the pond conditions and stocking densities, a supply of additional food may be needed (Renbo & Yuan 2004, Qin et al. 2009, Ren et al. 2010, Sun et al. 2013). Stocking densities of ponds could also be increased by adding artificial substrates to increase the surface area (Renbo & Yuan 2004). Determining the relative importance of all these variables would be necessary for advancing the pond culture of A. mollis, and may involve adjustments at different growing latitudes (Purcell et al. 2012a).

Sea Pens and Sea Cage Culture

A common method for growing out sea cucumbers is in the sea, inside cages or pens, which have been used in China and tropical regions of the world (Chen 2004, Renbo & Yuan 2004, Mills et al. 2012). The use of these confinement structures prevents the sea cucumbers from migrating to other places, and helps to designate ownership of stocks and prevent theft of the cultured sea cucumbers (Purcell et al. 2012a). There is a need to determine effective sea culture systems (sea pens, bottom cages, or floating cages) to enhance growth, reduce mortality, and escapes (Chen 2004, Renbo & Yuan 2004, Purcell & Simutoga 2008, Hair 2012, Robinson & Pascal 2012). The sea cucumber Australostichopus mollis grows well when enclosed in small, plastic mesh cages fixed to the seafloor at relatively high densities, provided the cages are placed where there is a high ongoing organic food input, such as beneath shellfish farms (Slater & Carton 2007, Slater & Jeffs 2010, Zamora & Jeffs 2012b). However, using methods of containment for juvenile sea cucumbers with more extensive benthic area, such as sea pens and ponds, would provide a greater surface area for the animals to forage (Purcell & Simutoga 2008, Robinson & Pascal 2012). The use of sea pens and sea cages, despite ensuring confinement of the sea cucumbers, can be expensive to establish and maintain, and also constrain the stocking density (Purcell et al. 2012a).

Sea Ranching

The release of juvenile sea cucumbers without any confinement into a specific coastal location with the intention of subsequent harvesting has been researched recently for a number of sea cucumber species (Purcell & Simutoga 2008, Bowman 2012, Fleming 2012, Juinio-Menez et al. 2012a, Purcell 2012). The research shows that successful sea ranching of sea cucumbers relies on the selection of an area of adequate size and with the correct environmental conditions for the sea cucumbers to survive and grow, thereby reducing mortality and migration. It has been shown in Australostichopus mollis, as well as in Holothuria scabra, that if the habitat conditions are adequate at the site where the juvenile sea cucumbers are released, they will not move great distances before they are harvested years later (Mercier et al. 2000, Purcell & Kirby 2006, Slater & Carton 2010). Survival of the released juveniles is a major concern because the majority of them do not survive to a market size in the wild (Purcell & Simutoga 2008, Juinio-Menez et al. 2012a). Survival could be increased by increasing the size of the released animals, improving transport conditions, and acclimating the juveniles better to the conditions at the site of their release (Pitt & Duy 2004, Purcell et al. 2006a, Purcell & Simutoga 2008, Robinson & Pascal 2012). Predation of juveniles at the release site is also important and should be mitigated if possible by providing refuges or through timing the release at periods when low predation risk is expected (Purcell et al. 2012a). However, this would require further research given the lack of information regarding natural predation in A. mollis (Sewell 1990).

In addition, before applying this kind of sea ranching system, care should be taken with the possible genetic pollution and transfer of diseases from hatchery-produced individuals to the local wild population (Purcell 2004, Purcell 2012). The released juveniles should, ideally, be tagged to distinguish them from the wild conspecifics, providing a proof of ownership and a means to evaluate the effectiveness of the release (Purcell 2012). Several tagging methods have been tested in Australostichopus mollis, such as the use of freeze branding, microsand blasting, pit-tagging, T bars. and visible implant fluorescent elastomer (Archer 1996, Stenton-Dozey 2007b). Of these methods the visible implant fluorescent elastomer had the highest retention (87%) after 3 mo (Stenton-Dozey 2007b). However, other cost-effective methods such as fluorochromes, which mark the sea cucumbers ossicles for a longer period, should not be dismissed as being a potentially useful marking method (Purcell et al. 2006b, Purcell & Blockmans 2009).

Integrated Multi-trophic Aquaculture Systems

Integrated multi-trophic aquaculture is the culture of 2 or more compatible species together, which maximizes production by using organisms that occupy different trophic levels and niches (Bardach 1986). Culture of Australostichopus mollis with other economically important aquaculture species shows some considerable promise for further advancement toward commercial production, as it has been revealed in other sea cucumber species (Ahlgren 1998, Kang et al. 2003, Zhou et al. 2006, Bell et al. 2007, Paltzat et al. 2008, Ren et al. 2012, Yokoyama 2013).

The culture of Australostichopus mollis together with the New Zealand abalone Haliotis iris in land-based aquaculture systems revealed that the waste from cultured abalone has sufficient energy to support growth in juvenile sea cucumbers, but not for adults (Maxwell et al. 2009). Culture of A. mollis with oysters appears to have promise, as it has been shown to be effective in Apostichopus japonicus and Parastichopus californicus (Zhou et al. 2006, Paltzat et al. 2008). Caged juvenile A. mollis can grow well in sites nearby oyster farms compared with sites farther away from the farms (Slater & Jeffs 2010). Initial experiments, co-culturing juvenile A. mollis in cages beneath oyster farms has shown their growth depends on a combination of stocking density, food availability, and seawater temperature (Zamora & Jeffs unpubl, data). The possibility for culturing A. mollis beneath salmon farms in Australasia should also be evaluated, considering the extensive sea cage salmonid production in the region, and given that other sea cucumbers species have performed well in co-culture with finfish (Ahlgren 1998, Yokoyama 2013). co-culturing A. mollis with other aquaculture species, such as scallops and crustaceans, should also be considered (Zhou et al. 2006, Bell et al. 2007, Ren et al. 2012).

The most promising and therefore most studied co-culture option for Australostichopus mollis is with mussels (Perna canaliculus and Mytilus galloprovincialis), of which there is extensive production in New Zealand and Australian waters (Slater 2006, Slater & Carton 2007, Slater & Carton 2009, Slater et al. 2009, Slater & Carton 2010, Zamora & Jeffs 2011, Zamora & Jeffs 2012a, Zamora & Jeffs 2012b, MacTavish et al. 2012). The sea cucumber A. mollis has been observed to occur naturally in high numbers beneath some mussel farms in New Zealand, presumably attracted by the organic enrichment of the seabed (Gribben & Bell 2000, Gribben & Bell 2001). co-culturing sea cucumbers beneath mussel farms will not only provide a second crop for the mussel industry, but also will help to reduce the impact of the organic loading on the sediments beneath the farms (Slater & Carton 2009, MacTavish et al. 2012). Caged adult sea cucumbers can survive and grow at high densities when caged on the sediments under mussel farms; however, as the sea cucumbers grow, the food availability in the cages becomes a limiting factor (Slater & Carton 2007), possibly because the distribution of mussel waste under mussel farms is patchy (Zamora & Jeffs 2012b). A possible solution would be to place the sea cucumbers under the mussel farms without cages, allowing them to forage freely, being retained by their behavioral attraction to the organically enriched seabed beneath the mussel farm (Slater & Carton 2010). However, the success of this type of co-culture will depend on the abundance of mussel waste in the sediment, as well as the seawater temperature and salinity, which together can greatly influence sea cucumber feeding behavior and growth (Slater et al. 2009, Zamora & Jeffs 2012a, Zamora & Jeffs 2012b, Zamora unpubl, data). Therefore, to optimize growth and survival of the sea cucumbers cultured beneath mussel farms, it is useful to know the temperature and salinity of the seawater to which the mussel farm is exposed throughout the year, and estimates of mussel waste biodeposition can be used to help manage the stocking densities of A. mollis.

Artificial Diet Development

The development of an artificial diet for the culture of Australostichopus mollis has been slow, mainly because of limited information about the nutrient requirements and digestive capabilities of this species, which are likely to involve differences between nursery and grow-out stages of production (Maxwell et al. 2009, Slater et al. 2009, Slater et al. 2010, Slater et al. 2011b, Zamora & Jeffs 2012a). Consequently, artificial diet development has been a specific focus for recent research. In terms of nutrients, protein and lipid are the most important structural and energy reserve components for adult A. mollis (Liu 2010). However, juveniles of this species appear to rely more on protein than both lipid and carbohydrate as a source of metabolic energy (Gay & Simon 1964, Zamora & Jeffs 2012a). When feeding on mussel waste, juvenile A. mollis absorb lipid more efficiently than protein and carbohydrate: however, the total quantity of carbohydrate and protein absorbed from this food source are substantially higher (Zamora & Jeffs unpubl.). Juveniles of this species are able to digest, absorb, and grow on a wide variety of artificial sources of protein and carbohydrate, which is an important prerequisite for developing artificial feeds (Slater 2010, Slater et al. 2011b). Several potential artificial diet ingredients such as fishmeal, mussel meal, dried seaweed (Sargassum policystum), Spirulina sp., fish oil, and even artificial diets formulated for abalone and carnivorous fish have proved to be palatable to the juveniles of A. mollis when offered in the correct proportions with sand or diatomaceous earth (Maxwell et al. 2009, Slater et al. 2009, Slater 2010, Slater et al. 2011b, Zamora unpubl. data). However, further research is needed in terms of the selection of adequate feed ingredients, feed attractants, ingestion stimulants, and feed presentation to develop an effective artificial diet for A. mollis (Lawrence et al. 2007). For example, in Australostichopus japonicus, several artificial feed ingredients have been evaluated, and detailed nutrient requirements are available, even to the level of specific amino acid requirements (Huiling et al. 2004, Yuan et al. 2006, Okorie et al. 2008, Liu et al. 2009, Okorie et al. 2011, Seo & Lee 2011, Xia et al. 2013). Improved artificial diets can enhance growth as well as give the sea cucumbers greater tolerance to survive stressful conditions (Qin et al. 2009, Wang et al. 2009, Zhang et al. 2010, Seo et al. 2011, Ma et al. 2013).

CONCLUSIONS

Considering the high value and the growing market demand for sea cucumbers, wild populations of Australostichopus mollis may face increasing fishing pressure, and further commercial interest in the development of their aquaculture production. Considering the current state of the fisheries for this species throughout its natural range, it is unlikely that A. mollis could face overexploitation in the near term. However, stock identification and biomass estimations together with more biological and ecological data are required for a better management of this species. Aquaculture development seems to be a more likely route for increasing the supply of this sea cucumber to meet international market demand. However, further information is needed in some key areas to provide a reliable basis for proceeding with sustainable commercial aquaculture at any scale. Major research priorities for improving the development prospects of the commercial aquaculture of this species are improving hatchery and nursery technology (e.g., broodstock management, larval rearing, postsettlement culture), and identifying the most suitable grow-out systems and locations (e.g., pond culture, sea pens and cages, sea ranching, integrated multi-trophic aquaculture). Initial research has indicated that broodstock of this species do have the potential to be manipulated into reproductive condition (Morgan, pets. comm. 2013), but reliable broodstock conditioning techniques need to be researched further and developed for commercial application. Methods used for commercial hatchery-reared larvae of Apostichopus japonicus in China have recently been proved to be effective for A. mollis on a pilot commercial scale conducted by a company in New Zealand (Heath et al. unpub. Maxwell pers. comm. 2013). However, weaning and early nursery methods have proved problematic because of a lack of knowledge of the types of suitable foods and the manner of their presentation. This is an area in great need of research if effective nursery production methods for A. mollis are to be established to support commercial-scale production of juveniles. Research to date shows that A. mollis can tolerate a variety of grow-out conditions and regimes. However, their growth and survival varies enormously in response to ambient conditions and is frequently suboptimal, especially with poor-quality or low availability of food. Therefore, defining optimal growing conditions for A. mollis under aquaculture conditions is now critical for advancing the commercial grow-out of this species.

ACKNOWLEDGMENTS

This research was supported by the University of Auckland in New Zealand, the Glenn Family Foundation, and the Comision Nacional de Investigacion Cientifica y Tecnologica of Chile.

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LEONARDO N. ZAMORA * AND ANDREW G. JEFFS

Leigh Marine Laboratory, Institute of Marine Science, University of Auckland, PO Box 349, Warkworth 0941, New Zealand

* Corresponding author. E-mail: lzam004@aucklanduni.ac.nz

DOI: 10.2983/035.032.0301

TABLE 1.
Timetable of embryonic and larval development of
Australostichopus mollis from 2 different studies
(Archer 1996, Stenton-Dozey & Heath 2009).

                                        Archer (1996)

                                                       Size
                                                     ([micro]m
Developmental stage                Time             [+ or -] SD)

Release (polar bodies)           <65 min                 --
First cleavage                    90 min                 --
Second cleavage                  140 min           185 [+ or -] 6
Third cleavage                   225 min           188 [+ or -] 13
Fourth cleavage                  290 min           195 [+ or -] 11
Blastula                           6 h             189 [+ or -] 11
Initiating gastrulation            9 h             154 [+ or -] 10
Gastrula                          14 h             171 [+ or -] 11
Very small auricularia              --                   --
Early auricularia                  1 day           404 [+ or -] 40
Small auricularia                   --                   --
Medium auricularia                  --                   --
Late auricularia                  17 days          686 [+ or -] 72
Large auricularia                   --                   --
Early doliolaria                  22 days          454 [+ or -] 50
Doliolaria                          --             450 [+ or -] 69
Early pentactula                  23 days                --
Pentactula                          --             344 [+ or -] 68
Settlement                        25 days                --

                               Stenton-Dozey and
                                  Heath (2009)

Developmental stage          Time      Size ([micro]m)

Release (polar bodies)    20-30 min        140-145
First cleavage            40-60 min        140-145
Second cleavage               --             --
Third cleavage                --             --
Fourth cleavage               --             --
Blastula                   5-6 h           140-150
Initiating gastrulation       --             --
Gastrula                  25-36 h          150-200
Very small auricularia    56-60 h          350-380
Early auricularia             --             --
Small auricularia          4-5 days        450-500
Medium auricularia         8-11 days       600-700
Late auricularia              --             --
Large auricularia         12-16 days       800-980
Early doliolaria              --             --
Doliolaria                18-20 days       330-500
Early pentactula              --             --
Pentactula                21-23 days       320-200
Settlement                24-27 days       165-280

In the first study, fertilized eggs were obtained from a naturally
occurring spawning event of broodstock in northeastern New Zealand
and were incubated at 19 [+ or -] 0.5[degrees]C (Archer 1996). In the
second study, fertilized eggs from artificially induced spawning
events in broodstock collected from Wellington Harbour and
Marlbourough Sounds in southern New Zealand were incubated at
18[degrees]C (Stenton-Dozey & Heath 2009).
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Author:Zamora, Leonardo N.; Jeffs, Andrew G.
Publication:Journal of Shellfish Research
Geographic Code:8AUST
Date:Dec 1, 2013
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