sign in sign up
<<
Home , Australostichopus, Holothuria fuscogilva, Holothuria scabra, Kappaphycus, Litopenaeus

Journal of Survey in Sciences 4(2) 5-25 2018

A review on the recent advances in the biology and technology of scabra

Junus S.1*; Kwong P.J.1; Khoo G.2

Received: March 2017 Accepted: December 2017

Abstract The highly valued is currently listed as endangered (EN) in the IUCN Red List due to overfishing in most of its native locations, spurring the development of H. scabra aquaculture to ensure sustainability of the industry and species in the wild. This review presents a summary on the biology of Holothuria scabra and recent advancements of its aquaculture technology. The life cycle, morphology and internal anatomy of H. scabra are discussed. Recent findings on the reproductive behavior and mechanism of the population are reviewed together with the possible factors that influence gamete maturation and spawning events. This review also covers the notable recent advances on H. scabra aquaculture technology such as the studies on broodstock diet which indicated bacteria and carbonate minerals to be the main diets; the favorable polyculture results of H. scabra juveniles with red tilapia and striatum; and the discovery and subsequent patent of H. scabra oocyte maturation inducing substance prepared from spawns.

Keywords: Holothuria scabra, sea cucumber, , broodstock, reproductive biology, aquaculture technology

______1-Department of Agricultural and Food Science, Faculty of Science, Universiti Tunku Abdul Rahman, 31900 Kampar, Malaysia 2-Department of Biological Science, Faculty of Science, Universiti Tunku Abdul Rahman, 31900 Kampar, Malaysia *Corresponding author’s Email: [email protected] 6 Junus et al., A review on the recent advances in the biology and aquaculture technology …

Introduction The biology of H. scabra had been The sea cucumber Holothuria scabra studied extensively for decades; the Jaeger, commonly known as sandfish or earliest mention was in a literature by trepang, has become one of the highly Jaeger (1833, cited in Hamel et al., valued species in the food industry 2001). Yet for many years the existing since the 1980’s especially in the Asian information was not readily accessible market. It is currently valued at more to researchers due to the publication than USD1000 per kg dry weight, just a and language barriers. In 2001, Hamel little under the market value of et al. compiled many of the then Apostichopus japonicus, also dubbed existing references into one the Japanese sea cucumber. Therefore, comprehensive review on H. scabra. it is not surprising that H. scabra has The 16-year-old literature was a great become overfished in most of its natural help in the advancement of H. scabra habitats resulting in the species being research, either for fundamental studies listed as endangered (EN) under the or for the aquaculture application and International Union for Conservation of technology. A more recent review was Nature (IUCN) Red List (Purcell et al., compiled and edited by Brown and 2014). In Sri Lanka, the unregulated Eddy (2015) covering the advancement overfishing of sea cucumbers has of echinoderm aquaculture in general. resulted in the collapse of the industry This paper aims to present a current (Kumara et al., 2005), and fishing summary on the biology of H. scabra activities have recently been restricted and the advancement of its aquaculture to the north, east, and north-western technology and management in the past coastal waters (Dissanayake and sixteen years. Stefansson, 2012). Other countries like India (Sakhtivel and Swamy, 1994) and The Biology of Holothuria scabra Papua New Guinea have imposed a ban or moratorium on sandfish trading The holothurians can be grouped and (Purcell et al., 2014; Purdy et al., 2017) differentiated from other in an effort to prevent the impending based on the existence of a calcareous collapse. The need to enhance the ring located anterior to the oesophagus natural stocks of H. scabra in its native as well as the buccal tentacles that location has helped to spur the extend out of the pharynx and serve as development of sea cucumber feeding apparatus. Unlike other aquaculture technology. Fortunately, echinoderms, the holothurians also just like the sea cucumber Apostichopus possess an outer skeleton (test) japonicus, its temperate counterpart, H. consisting of microscopic ossicles and a scabra is also one of the more well-developed haemal system. adaptable species for aquaculture Holothurians are further classified into production due to its biology and six orders based on the anatomy of the natural habitat (Hamel et al., 2001). Journal of Survey in Fisheries Sciences 4(2) 2018 7 calcareous ring, the shape and Natural Habitat arrangement of the ossicles, the number In his review, Hamel et al. (2001) and form of the buccal tentacles explained observations from various extending out of the mouth, and the researchers concerning the habitat presence of respiratory trees. Of the six preference of H. scabra. In its natural holothurian orders, only two orders are habitat across the region, adult H. known to be exploited commercially scabra is observed to prefer calm (Hamel et al., 2001; Slater and Chen, coastal areas with sandy muddy 2015). The minority comes from the substrate instead of coral reefs. They order Dendrochirotida, which is are also observed to be able to tolerate associated with 10 buccal tentacles. low salinities, and are sometimes even Only one species, Cucumaria frondosa, found near estuaries. A study by is commercially exploited within this Mercier et al. (1999a, b; 2000a) showed order mainly for the extraction of its the ability of H. scabra to tolerate as bioactive compound, frondoside A low as 20 p.s.u water salinity by (Takashi et al., 2005; Slater, 2015). burrowing into the sediment. The Most of the commercial sea cucumbers juveniles are also observed to prefer belong to the order Aspidochirotida, medium-sized grains (0.4 mm) as which has 18-30 buccal tentacles. substrate and areas where seagrasses Within the Aspidochirotida, the are plentiful, especially of the species commercially exploited sea cucumber Thalassia hemprichii and Enhalus comes only from two families, acoroides. and . In The sandfish H. scabra can be found terms of aquaculture production, there across various regions in the Indo- is only one species from each family Pacific which encompasses the latitude currently produced in aquaculture range of 30 N to 30 S (Massin, 1999; hatcheries namely the temperate species, Massin et al., 2009; Hamel et al., 2001). Apostichopus japonicus, and the warm Native populations have been studied in water species, Holothuria (Metriatyla) India, Sri Lanka, New Caledonia, scabra reported by Jaeger (1833). The Solomon Islands, Ecuador, Vietnam, taxonomic classification of H. scabra is Indonesia, the Philippines, Australia, as follows (Massin et al., 2009): Madagascar, and China (Hamel et al., Kingdom : Animalia 2001; Dissanayake and Stefansson, Phylum : Echinodermata 2012). Extensive aquaculture and Class : Holothuroidea farming systems of H. scabra have Order : Aspidochirotida been growing for the past 7 years and Family : Holothuriidae are currently on-going in Madagascar, : Holothuria Philippines, Vietnam and Fiji which Species : scabra mainly supply the commercial demand (Hair et al., 2012; Purdy et al., 2017). 8 Junus et al., A review on the recent advances in the biology and aquaculture technology …

Anatomy during handling, the incidence of The morphology and internal anatomy is more common among H. of Holothuria scabra had been covered scabra compared to other species extensively by various researchers, (Conand, 1989) cited in Hamel et al. most notably Bai (1971, 1978, 1980, 2001). and 1994), Conand (1989 cited in Bai (1980) revealed that the Hamel et al., 2001), James (1989), and digestive tract of H. scabra, comprising Baskar (1994). The species is usually the oesophagus, stomach, small and identified by its smooth, elongated large intestines, is supported by a tubular body along the oral-aboral axis, mesentery. The digestive tract ends into being gray or black at the convex dorsal a wide cloacal chamber that terminates side, and always white and flat at the at the anus (Slater and Chen, 2015). ventral side. The dorsal body is There is currently no detailed study on sometimes peppered with speckles of the physiology of digestion and black, yellow and/or white patterns. nutritional requirements of H. scabra. The white ventral side is usually The respiratory system of H. scabra peppered with black or brown dots is an intricate network of tubules or which are the tube feet. Located vessels formed from the cloacal wall in ventrally at one end of the tubular body one common main stem that branches is the oval mouth encircled by 20 to the left and right into many finer tentacles (Conand, 1989 cited in Hamel branches. Two or three shorter branches et al., 2001). At the opposite end of the may also form out of the base of the body and located somewhat dorsally is common stem. This network of tubules the anus or cloaca which rhythmically is the respiratory tree that terminates pumps water in and out of the body. into the perivisceral coelom and are The creeping movement of H. scabra is always covered in coelomic fluid (Bai, regulated by five pairs of muscular lines 1980; Slater and Chen, 2015). The along the body length (Bai, 1980). cloaca also plays an important role in The internal anatomy or viscera of H. the respiratory system by drawing sea scabra consists of two tubular branches water in and out of the cloacal chamber of gonads with one end connected to and respiratory trees with its rhythmical the gonopore, the digestive organs pumping (Bai, 1980). Gas exchange which end with the anus, and occurs through the thin tubular wall into respiratory trees. H. scabra is able to the coelomic fluid that is circulated eviscerate most to all of its digestive around the body through the water and respiratory organs as a method of vascular and haemal system. However, self-preservation. These organs will gas exchange also occurs throughout fully regenerate in about one to two the integument and tube feet which months (Cannon and Silver, 1987; Bai, explains the ability of H. scabra to 1994). When the are agitated eviscerate all its internal organs Journal of Survey in Fisheries Sciences 4(2) 2018 9 including the respiratory trees when to Saito et al. (2002) the main protein necessary. component of the body wall is the collagen fibrils containing glycine, Body wall composition glutamic acid, proline, and aspartic acid. The integument of H. scabra is The structure of these collagen fibrils is composed mainly of collagenous what gives the body wall its texture, an proteins and connective tissues. This important component for the use of sea body wall or dermis is the main body cucumber in the culinary field. The part desired as food of which content of carbohydrates and lipids in characteristics and texture determines the body wall of A. japonicus is found the value of the sea cucumber as a to be low. Most of the lipids are commodity. The Holothuriidae possess contained in the gonads, being the a thin epidermis composed of reproductive organs, especially when microscopic calcareous ossicles. they are mature. Saito et al. (2002) also Getting rid of this part is one of the found thiamine, riboflavin, carotenoid, most labor intensive and time and niacin in A. japonicus body wall as consuming activities in the traditional well as various minerals and trace processing of sea cucumbers. elements. The studies on the composition of H. A number of studies had been done scabra body wall are few, covering on the extraction of various bioactive only the gross composition and done compounds with pharmacological mostly on dried specimens. They properties from various sea cucumber generally agreed that H. scabra contain species, including H. scabra (Slater, around 30-60% (DW) crude protein and 2015). A recent study by around 2% (DW) of fat (Springhall and Assawasuparerk et al. (2016) on H. Dingle, 1967; Ozer et al., 2004; scabra, showed that the body wall Ibrahim et al., 2015). Springhall and extract contains scabraside D, a sulfated Dingle (1967) also showed the body triterpene glycoside, found to inhibit wall containing calcium, sodium, tumor growth in mice. Other bioactive potassium, and phosphorus in small compounds found in H. scabra extract amounts. A study conducted by are echinoside A (Collin and Adrian, Yahyavi et al. (2012) showed higher 2010), saponins (Yibmantasiri et al., content (>36%) of polyunsaturated fatty 2012) and chondroitin sulfates (Takashi acids (PUFA) in the lipid profile of H. et al., 2005) that show active scabra body wall compared to the antioxidant and antimicrobial activities. monounsaturated fatty acids (MUFA) at 25%. In comparison, the much studied Reproductive biology composition of A. japonicus body wall The H. scabra has separate sexes but also showed protein as the highest exhibit monomorphism. It is a component of the body wall. According broadcast spawner, known for biannual 10 Junus et al., A review on the recent advances in the biology and aquaculture technology … seasonal mass spawning in the natural (2006) showed that the tubular habitat. The peak spawning seasons development is synchronous across the across various populations seemed to gonads and consists of only a single tuft fall in October to January and March to for each spawning cycle. Tubules are July (Hamel et al., 2001). Nevertheless, reabsorbed after spawning, thus some studies also observed that certain signifying a resting stage in which the small populations of H. scabra gonads are not visible. The study all year long. These studies give rise to showed that it may take as long as 12 the possibility that these H. scabra months for the developing tubules to populations may have an asynchronous reach fecund stage. gonadal development that enables them Both studies by Conand (1993) and to breed all year long (Purwati, 2006; Purwati (2006) showed that the gonadal Slater and Chen, 2015). The most index (GI) for both males and females notable study that supports this notion indicated large variations across the is by Purwati (2006) which investigated same population at the same sampling the tubules and gonadal indices of occasion. This seemed to confirm the Indonesian H. scabra populations from asynchronous gonadal development three vastly different regions. The study model in H. scabra populations. showed that during each sampling However, Purwati (2006) did find that occasion the researchers would always the GI values of H. scabra population find animals with fecund gonadal stage, in Indonesian waters peaked at two with after-spawned gonads, and without different periods in a year, specifically visible gonads. at the end of each monsoon season, Male and female gonads comprise indicating a bi-annual spawning season. filamentous tubules that are elongated, This finding was in agreement with the branched, and with variable sizes and H. scabra population study in India by colors depending on the maturity state Khrisnaswamy and Krishnan (1967), in of the gonads. According to Bai (1980) Australia by Harriot (1980), in New and James (1989), the female gonads Caledonia by Conand (1989, 1990, are said to be thick, brown tubules with 1993), in Sri Lanka by Moiyadeen visible eggs that appear as white dots (1994), and in Solomon Islands by when ripe. However, Conand (1993) Battaglene (1999b, c). Several described ripe female gonads as environmental factors were proposed by translucent and the mature female various studies as to be the cue for gonadal tubules are shorter, heavier, gamete maturation and spawning event. and bigger in diameter than those of the These factors include the fluctuating males. Mature female tubules have been water temperature during the observed to contain vitellogenic oocytes, transitional period of monsoon seasons while mature male tubules contain only (Conand, 1993; Battaglene, 1999c), spermatozoa (Tuwo, 1999). Purwati change in photoperiod (Morgan, 2000), Journal of Survey in Fisheries Sciences 4(2) 2018 11 lunar influence (Mercier, 1999c, 2000b), in Solomon Islands (Battaglene, 1999a, and the change in water salinity c; Battaglene and Bell, 1999; (Khrisnaswamy and Krishnan, 1967; Battaglene et al., 1999). The Battglene, 1999a, 2000). development of H. scabra can be The heterogeneity of gonadal summarized in stages as shown in Fig. development across the population 1. makes the duration of gametogenesis There are variations in the findings stages difficult to be concluded. of H. scabra oocyte diameter and time However, most studies agree that H. frame of blastula formation reported by scabra gametogenesis include different researchers in the past. Oocyte immature and mature gonadal stages, diameter was claimed to be in various followed by spawning, after-spawning sizes ranging from 70 µm (Ong Che or spent, and resting stages where and Gomez, 1985) to 210 µm (Conand, tubules are reabsorbed (Ong Che and 1993). The varying results may be Gomez, 1985; Conand, 1993; Tuwo, caused by the non-uniformity in the 1999; Morgan, 2000, Purwati, 2006). research protocols across the studies The development and maturity of (Hamel et al., 2001). Blastula formation gonadal tubules seemed to be was reported to be completed in 40 determined by the protein and lipid minutes (Battaglene, 1999a, c; storage in the intestines (Khrisnaswamy Battaglene and Bell, 1999) to 3 hours and Krishnan, 1967). Conversely, a (James et al., 1988, 1994). Personal study by Morgan (1999) seemed to observation of the embryonic stage of H. indicate that the opposite may also be scabra seemed to confirm the latter. true. The growth and metabolism in food-deprived H. scabra actually utilize Larval stage the nutrients from the gonads and The size of fertilized H. scabra eggs are gametes. observed to be around 100-200 µm (Slater and Chen, 2015). Fertilization Life cycle usually occurs immediately upon Various researchers have conducted contact with the sperms. studies on the life cycle development of In captive breeding, polyspermy is H. scabra. The collected results from usually a problem and must be avoided these studies corroborate each other in by controlling the sperm concentration general except on few details. In the in the water. This is done by removing published article, Hamel et al. (2001) the spawned males from the spawning compiled and summarized the two tank once the desired sperm major sources of information on H. concentration is achieved. Polyspermy scabra life cycle studies conducted in is also avoided by washing the fertilized India (James et al., 1988, 1994; James eggs gently before stocking them in the and James 1993) and studies conducted hatching tanks. 12 Junus et al., A review on the recent advances in the biology and aquaculture technology …

A B . .

C .

F D . .

E

Figure 1: A. Mature broodstock and spawning activity.. B. Fertilized egg and cell division (48 hours). C. Planktonic stage (10-14 days) consists of three different stages (Top left clockwise: Gastrula, Auricularia larvae, Doliolaria). D. Benthic stage consists of two different stages (left-right: Pentactula, early juvenile). E. Juvenile at 1 g. F. Juvenile at 10 g (4 months). (Pictures are from personal collection.)

Under the optimal condition of 27C, larval development can be divided into fertilized eggs developed into blastula the early (300-400 µm length), middle in 3-5 hours. Eggs hatch in 24-48 hours (400-700 µm length), and late as gastrula, the non-feeding planktonic auricularia (700-1000 µm length). The larvae stage, which then develop into three stages of auricularia are auricularia larvae (Hamel et al., 2001). differentiated through body length and Auricularia larvae are the feeding width, feed type, size and quantity, and planktonic larvae that generally develop an increasingly defined body structure. within 36-48 hours after fertilization. The late auricularia has pronounced Auricularia feeds on microalgae and its arms and hyaline spheres. The hyaline Journal of Survey in Fisheries Sciences 4(2) 2018 13 spheres are postulated to be a lipid- At this stage, the pentactula will based energy storage that is crucial for continue its development by body the survival of the next larval stage elongation. Further development would (Battaglene, 1999a, c). In an optimum show the larva moving about and its rearing condition, the auricularia larvae movement can be traced from the develop for 10-14 days before “trail” of feces it leaves behind. This transforming into the doliolaria larvae. larval stage usually continues for 15-18 Doliolaria is the non-feeding days in which the pentactula larvae planktonic larval stage. At this stage the gradually transform into a juvenile larvae are looking for a suitable stage (James et al., 1994). substrate to settle on. This stage is one of the bottlenecks in sea cucumber Juveniles hatcheries with high mortality rate as The juvenile stage can be recognized by doliolaria are known to float around and the disappearance of the tentacles under never settle when a suitable substrate is the mouth hood and the further not found. They appear as black dots in definition of tubular and elongated the water to the naked eyes and can be body shape bearing the varietal found floating near the surface and tank coloration and specific patterns of the walls. They are also reported to be adults. Reports vary, but approximately phototactic (Battaglene, 1999a, c). In a 30-45 days after fertilization, the 1 cm suitable environment, doliolaria is long juvenile sea cucumbers emerge known to settle within 24-48 hours, (James and James, 1993; James et al., however, they have been observed to 1994; James, 1996). delay settlement up to 96 hours when The development of juvenile stage to there is no suitable substratum (Mercier adult stage is known to require the et al., 2000a). A study by Mercier et al. introduction of sandy substrates. Based (2000a) showed strong preference by on personal observation, the juveniles’ doliolaria larvae to settle on the blades body size increased sharply after the of the Thalassia hemprichii and introduction of sandy substrates. Enhalus acoroides seagrass species as Studies by Mercier et al. (1999a, b) compared to other substrates such as found that juveniles prefer muddy artificial leaves, crushed corals, or other sandy substrates especially sand with an plant species. Upon finding the average grain size of 0.4 mm. A later preferred substratum for settlement, the study showed juveniles to remain planktonic doliolaria larvae would among the seagrass up to 10 cm body transform into the benthic pentactula size before migrating out into open larvae. sandy areas (Mercier et al., 2000a). The pentactula larva is the feeding This study and several others (James et benthic stage, possessing tentacles that al., 1994; Uthicke and Benzie, 1998 are used in grabbing food and feeding. cited in Hamel et al., 2001; Uthicke and 14 Junus et al., A review on the recent advances in the biology and aquaculture technology …

Benzie, 1999) seemed to indicate a H. scabra first spawning occurred when downward migration behavior of H. the animals were about 200-230 mm scabra in the wild. More studies are body length. Yet other study by Harriot needed in order to confirm this (1980) recorded first sexual maturity of hypothesis. H. scabra at 184 g of body weight Reports on the growth rate of instead of length. The inconsistent juveniles vary and many of the studies reports on first sexual maturity may be are conducted in a laboratory setting. due to the non-uniform methods of Two studies conducted in the field defining first sexual maturity across the showed a big difference in the growth different studies. rates of juvenile H. scabra. Mercier et The life span of H. scabra is al. (2000b) stated a growth rate of 10- unconfirmed but James et al. (1994) 15 cm/month from an initial size of 65 and the Marine Products Exports mm while Manikandan (2000) observed Development Authority (MPEDA) a growth rate of only 1.4 cm/month (1989) suggested that it could be more from an initial size of 15 mm. It is thus than 10 years. Fecundity and speculated that the growth rate reproductive viability of adult sea increases with the size of the . cucumber throughout its lifespan is yet to be studied in detail. Adults The subadult H. scabra can be Advancement in the Aquaculture differentiated from juveniles through Technology and Management of H. their behavior as well as the body scabra weight and size. In the wild, it is On broodstock nutrition common to find adults of up to 2 kg The study on the effect of sea cucumber body weight and 30 cm long, although farming on sediment by Plotieau et al. these are getting rare due to (2013) showed a great reduction of overexploitation. Sexually mature bacterial population, reduced fine grain adults, however, are difficult to (<250 um), big reduction in the determine just from body weight and concentration of photosynthetic bacteria, size because H. scabra as small as 200- and reduced carbonate proportion 250 g can spawn successfully and be as (aragonite, calcite, magnesian calcite) fecund as those double in body weight in the sediment, but not much change (Harriot, 1980). The size of first sexual was found in the total organic matter. It maturity has been studied but results could be inferred from this study that vary greatly. Studies by Shelley (1981) adult sandfish live mainly on bacteria and Lokani (1995) observed that H. rather than organic matter. The study scabra becomes sexually mature at also showed that sandfish is able to around 140 mm body length. However, digest the inorganic materials of the Baskar and James (1995) observed that sediments. This observation was Journal of Survey in Fisheries Sciences 4(2) 2018 15 confirmed by Schneider et al. (2013) In relation to broodstock feed, a and Collard et al. (2014) who showed study by Asha and Muthiah (2007) on that the dissolution of CaCO3 into juvenile growth showed the researchers seawater in the ocean is greatly helped coming up with their own induction- by sea cucumbers which secrete stimulating feed formulation. This feed digestive acids to dissolve the minerals was composed of rice bran, soya in their gut. Besides the mineral content powder, and Sargassum spp. powder at in the substrate, a study by Shi et al. 4:1:2 ratio. The feed was given at 5% (2015) also showed that the size of sand body weight daily. In the area of feed particles have a cumulative effect on supplement, a preliminary study by Ko feed nutrient absorption and growth rate et al. (2009) had shown that the of the sea cucumber. addition of -tocopherol or Vitamin E Another possible diet formulation had a positive impact on weight gain, for intensive land-based culture of H. feed conversion rate and survival of scabra may be gleaned from studies juvenile A. japonicus. The optimum conducted on Apostichopus japonicus, a dietary level of -tocopherol is found to species of temperate sea cucumber be between 23.1-44 mg/kg diet. More commercially farmed for consumption. studies are needed to conclude the One of the related studies was effect of dietary vitamin E in the whole performed by Yuan et al. (2006) using body lipid and protein contents of sea feed formulated with 75% dried bivalve cucumbers, particularly H. scabra. feces and 25% powdered algae. The Such studies may also be able to answer study found a conflict between using whether vitamin E supplementation in dried material (feces and algae) which sea cucumber diet can improve its had been naturally stripped of any reproductive ability. bacteria population and using fresh material which may still contain On captive broodstock management beneficial bacteria. The dried feed and farming enabled easy feed preparation and The poor sustainability of broodstock storage, but the powdered algae or dried viability in captivity is well feces alone was shown to be an documented (Morgan, 2000; Mercier unsuitable diet for growth. Fermented and Hamel, 2013). The use of captive- powdered algae, however, was shown bred or F1 broodstock in sea cucumber to perform better as a food source for hatchery so far was only implied in Pitt sea cucumbers. This study seemed to and Duy (2004) and Agudo (2006). affirm the hypothesis of Plotieau et al. Generally, in captivity, broodstock (2013) that bacteria may comprise the would start losing weight and majority portion of what sea cucumbers decreasing in reproductive productivity actually feed on. after a few cycles. The population would also see an increasing mortality 16 Junus et al., A review on the recent advances in the biology and aquaculture technology … due to diseases. Attempts had been Although the polyculture of A. made for inland polyculture of sea japonicus with bivalves such as cucumber with other aquatic species but (Kang et al., 2003) has been successful most studies focused on juvenile H. in China (Mercier and Hamel, 2013), it scabra rather than broodstock is worth noting that, to date, no study management. The co-culture of juvenile could be found with regards to the H. scabra with juvenile blue shrimp polyculture of tropical abalone with H. ( stylirostris) showed no scabra. positive results (Purcell et al., 2006), and was even found to be inviable since Effect of environmental factors on the survival of H. scabra was observed reproductive biology to be very low (Bell et al., 2007). Mills A study by Collard et al. (2014) noted et al. (2012) studied the polyculture of that in a short period of less than 12 H. scabra with monodon in days, the ocean acidification in which Vietnam which gave disastrous results the sea water pH dropped to around 7.4- due to sea cucumber by the 7.7, caused acidosis of the coelomic prawns. A more promising result was fluids (CF) in H. scabra. However, the found in the polyculture of juvenile sea acidosis of CF in the short-term did not cucumber with red tilapia (Sithisak, seem to affect the respiration process Pongtippatee, and Withyachumnarnkul, and ammonia secretion. Further studies 2013) in 30 ppt seawater. Sea need to be carried out to determine cucumbers were found to grow faster in whether long term CF acidosis will polyculture ponds than in monoculture eventually affect the reproductive ponds. ability and viability in a negative Beltran-Gutierrez (2012) and manner. Beltran-Gutierrez et al. (2016) A study by Battaglene et al. (2002) investigated the polyculture of sea on wild caught broodstock presented an cucumber with red , overview into the spawning methods Kappaphycus striatum, which produced and peak periods of H. scabra, acceptable results since no negative Holothuria fuscogilva and effects were observed on sea cucumber mauritiana. This study showed that H. growth albeit without a positive effect scabra could be induced to spawn as well. Another study by Namukose et throughout the year as compared to al. (2016) demonstrated an integrated other species in the study but the mariculture system of H. scabra with percentage of successfully spawned seaweed denticulatum which broodstock was the greatest only in could enhance the growth rate of the August to November with September seaweed as well as reduce the organic being the most productive month. Even matter in the sediments at medium H. so, the percentage of successfully scabra stocking densities. spawned broodstock in the month of Journal of Survey in Fisheries Sciences 4(2) 2018 17

September amounted to only 35%. Assisted fertilization of extracted sea Various environmental factors are cucumber oocytes has not been suspected to act as or have influence on successful due to the unique two the spawning cues for H. scabra in the maturation steps in which the first wild. The environmental factors include oocyte maturation phase is stopped at the change in temperature, photoperiod first meiotic phase specifically at and its intensity, the lunar cycle which prophase-I stage (Leonet et al., 2009). influences tidal fluctuations, and the Oocytes would only mature when the availability of certain types of food. meiotic phase resumes just before The change in temperature or thermal spawning presumably due to the stimulation is quite a common cue for activation of a gonad-stimulating spawning events of invertebrates, and substance (GSS), which would then this is also the case with H. scabra stimulate the production of a (Morgan, 2000). Battaglene et al. (2002) maturation-inducing substance (MIS) also reported that spontaneous such as 1-methyl-adenine (1-Me-A) in spawning occurred following capture sea stars (Yamashita et al., 2000). In the and transport stress on the broodstock. case of the sea cucumber, the MIS is an Concerning captive broodstock, there unknown endocrine substance. have been reports of successful However, Leonet et al. (2009) claimed spawning following physical and to have successfully discovered a thermal stimulation on H. scabra held complex substance, termed as the in tanks (Morgan, 2000). maturation-inducing fractions (MIF), which could be prepared from sea On broodstock sex differentiation, sex urchin () spawns, hormones and oocyte maturation that allowed the maturation of 28-90% One of the difficulties in breeding H. of extracted H. scabra oocytes. An scabra is in determining the sex of the international patent had been filed for broodstock since H. scabra is a this finding which indeed was a monomorphic species. Sex can only be significant breakthrough. determined through a biopsy of the Currently, there is a scarcity of gonads, dissection of the animals, and studies on the putative sex spawning (Hamel et al., 2001). The chromosomes of H. scabra or even the difficulty of sex identification general chromosome number of the combined with the difficulty in species. Chromosome studies had been determining gamete maturity make it performed on other echinoderm species necessary to obtain a sufficiently large which generally showed a range of 36 population of wild stock for each to 46 diploid chromosome numbers spawning attempt (Mercier and Hamel, (Colombera and Venier, 1976, 1980). A 2013). study by Okumura et al. (2009) showed a diploid number of 44 for A. japonicus 18 Junus et al., A review on the recent advances in the biology and aquaculture technology … which is the same as the other two cholangiocarcinoma xenografts in species that belong to different families. mice. Asian Pacific Journal of This suggests that chromosome number Cancer Prevention, 17(2), 511-517. may similar or vary only slightly among Bai, M.M., 1971. Regeneration in the animals within the class Holothuroidea. holothurian Holothuria scabra There is also no detailed study on Jaeger. Indian Journal of the sex-related hormones, sex-related Experimental Biology, 9, 467-471. chemical cues, or maturity-related Bai, M.M., 1978. The anatomy and chemical cues of H. scabra. Such histology of the digestive system of studies may be fundamental in the Holothuria scabra Jaeger. Journal of development of a field test-kit to ease the Marine Biological Association sex identification of H. scabra India, 20, 22-31. broodstocks. In contrast, various such Bai, M.M., 1980. Monograph on studies had been carried out on A. Holothuria (Metriatyla) scabra japonicus. A study by Katow and Jaeger. Memoirs of the Zoological Katow (2014) has resulted in the Survey of India, 16, 1-75. development of a detection kit for Bai, M.M., 1994. Studies on mature A. japonicus females by regeneration in the holothurian measuring their gonad-stimulating Holothuria (Metriatyla) scabra substance-like (GSSL) peptide Jaeger. Bulletin of the Central immunochromatography. Marine Fisheries Research Institute, 46, 44-50. References Baskar, B.K., 1994. Some observation Agudo, N., 2006. Sandfish Hatchery on the biology of the holothurian Techniques. Noumea: Australian Holothuria (Metriatyla) scabra Centre for International Agricultural (Jaeger). Bulletin of the Central Research (ACIAR). 45P. Marine Fisheries Research Institute, Asha, P.S. and Muthiah, P.S., 2007. 46, 39-43. Growth of the hatchery‐produced Baskar, B.K. and James, D.B., 1995. juveniles of commercial sea Studies on the biology, ecology and cucumber Holothuria (Theelothuria) of the sea-cucumber spinifera Theel. Aquaculture Holothuria (Metriatyla) scabra Research, 38(10), 1082-1087. Jaeger from southeast coast of India. Assawasuparerk, K., Vanichviriyakit, Central Marine Fisheries Research R., Chotwiwatthanakun, C., Institute Special Publication, 61, 13- Nobsathian, S., Rawangchue, T. 17. and Wittayachumnankul, B., 2016. Battaglene, S.C., 1999a. Culture of Scabraside D extracted from tropical sea cucumbers for the Holothuria scabra induces apoptosis purposes of stock restoration and and inhibits growth of human enhancement. In: Baine, M., ed. The Journal of Survey in Fisheries Sciences 4(2) 2018 19

Conservation of Sea Cucumbers in Bell, J.D., Agudo, N.N., Purcell, S.W., Malaysia, Their taxonomy, ecology Blazer, P., Simutoga, M., Pham, D. and trade – Proceedings of an and Patrona, L.D., 2007. Grow-out International conference. Heriot- of sandfish Holothuria scabra in Watt University and the Fisheries ponds shows that co-culture with Research Institute, Kuala Lumpur, shrimp Litopenaeus stylirostris is not Malaysia, pp. 11-25. viable. Aquaculture, 273, 509-519. Battaglene, S.C., 1999b. Progress in Beltran-Gutierrez, M., 2012. the production of tropical sea Integrated multi-trophic aquaculture cucumber Holothuria scabra and of seaweed Kappaphycus striatum Holothuria fuscogilva for stock and sea cucumber Holothuria scabra, enchancement. In: World Zanzibar, Tanzania. M.Sc. Aquaculture Society Conference, University of Bremen, Germany. Sydney, Australia, April 1999. Beltran-Gutierrez, M., Ferse, S.C.A., Battaglene, S.C., 1999c. Culture of Kunzmann, A., Stead, S.M., tropical sea cucumbers for the Msuya, F.E., Hoffmeister, T.S. and purposes of stock restoration and Slater, M.J., 2016. Co-culture of sea enhancement. NAGA ICLARM cucumber Holothuria scabra and red Publication, 22, 4-11. seaweed Kappaphycus striatum. Battaglene, S.C. and Bell, J.D., 1999. Aquaculture Research, 47, 1549- Potential of the tropical Indo-Pacific 1559. Available at sea cucumber, Holothuria scabra, doi:10.1111/are.12615 for stock enhancement. In: Howell, Brown, N.P. and Eddy, S.D. eds., B.R., Moskness, E., Svåsand, T., eds. 2015. Echinoderm Aquaculture. Stock Enhancement and Sea New Jersey: Wiley-Blackwell. 384P. Ranching. Oxford: Blackwell Cannon, L.R.G. and Silver, H., 1987. Science, pp. 478-490. Sea cucumbers of northern Australia. Battaglene, S.C., Seymour, J.E. and South Brisbane: Queensland Ramofafia, C., 1999. Survival and Museum (Queensland Cultural growth of cultured juvenile sea Centre). 60P. cucumbers Holothuria scabra. Collard, M., Eeckhaut, I., Dehairs, F. Aquaculture, 178, 293-322. and Dubois, P., 2014. Acid-base Battaglene, S.C., Seymour, T.E., physiology response to ocean Ramofafia, C. and Lane, I., 2002. acidification of two ecologically and Spawning induction of three tropical economically important holothuroids sea cucumbers, Holothuria scabra, from contrasting habitats, Holothuria fuscogilva and Holothuria scabra and Holothuria Actinopyga mauritiana. Aquaculture parva. Environmental Science and 207, 29–47. Pollution Research, 21(23), 13602- 13614. 20 Junus et al., A review on the recent advances in the biology and aquaculture technology …

Collin, P.D. and Adrian, T.E., 2010. cucumber aquaculture. In: The sea cucumber-derived anti- Proceedings of an International cancer triterpenoid, Frondoside A Symposium held in Noumea, New blocks angiogenesis. In: Proceedings Caledonia, 15-17 February, 2011. of the American Association for Australian Centre for International Cancer Research Annual Meeting, Agricultural Research. 209P. 51, pp. 333. Washington, DC, 17–21 Hamel, J-F., Conand, C., Pawson, April. D.L. and Mercier, A., 2001. The Colombera, D. and Venier, G., 1976. I sea cucumber Holothuria scabra cromosomi degli Echinodermi. (Holothuroidea: Echinodermata): its Caryologia, 29(1), 35-40. biology and exploitation as beche- Colombera, D. and Venier, G., 1980. de-mer. Advances in Marine Biology, Il numero dei chromosomi di cinque 41, 129-223. specie di echinodermi. Caryologia, Harriot, V.J., 1980. Ecology of the 33, 503-507. holothurian fauna of Heron reef and Conand C., 1989. Les holothuries Moreton Bay. M.Sc. University of aspidochirotes du lagon de Nouvelle- Queensland, Brisbane, Australia. Calédonie: biologie, écologie et Ibrahim, M.Y., Elamin, S.M., Gideiri, exploitation. Etudes et Thèses, Y.B.A. and Ali, S.M., 2015. The O.R.S.T.O.M., Paris, 393P. proximate composition and the Conand, C., 1990. The fishery nutritional value of some sea resources of Pacific island countries. cucumber species inhabiting the Part 2: Holothurians. In: Food and Sudanese Red Sea. Food Science Agriculture Organization of the and Quality Management, 41, 11-16. United Nations, No. 272.2, Rome, Jaeger, G.F., 1833. Dissertatio de Italy. Holothuriis. Turici. Conand, C., 1993. Reproductive James, D.B., 1989. Beche-de-mer – its biology of the holothurians from the resources, fishery and industry. major communities of the New Marine Fisheries Information Caledonia lagoon. Marine Biology, Service, 92, 1-30. 116, 439-450. James, D.B., 1996. Culture of sea- Dissanayake, D.C.T. and Stefansson, cucumber. Bulletin of the Central G., 2012. Present status of the Marine Fisheries Research Institute, commercial sea cucumber fishery off 48, 120-126. the north-west and east coasts of Sri James, D.B., Gandhi, A.D., Lanka. Journal of the Marine Palaniswamy, N. and Rodrigo, Biological Association of the United J.X., 1994. Hatchery techniques and Kingdom, 92(4), 831-841. culture of the sea-cucumber Hair, C., Pickering, T. and Mills, D., Holothuria scabra. Central Marine 2012. Asia-Pacific tropical sea Journal of Survey in Fisheries Sciences 4(2) 2018 21

Fisheries Research Institute Special japonicus. Journal of the World Publication No. 57. 40P. Aquaculture Society, 40(5), 659-666. James, D.B., Rajapandian, M.E., Kumara, P.B.T.P, Cumaranathunga, Baskar, B.K. and Gopinathan, P.R.T. and Linden, O., 2005. C.P., 1988. Successful induced Present status of the sea cucumber spawning and rearing of the fishery in southern Sri Lanka: A holothurian Holothuria (Metriatyla) resource depleted industry. SPC scabra Jaeger at Tuticorin. Marine Beche-de-mer Information Bulletin, Fisheries Information Service, 87, 22, 24-29. 30-33. Leonet, A., Rasolofonirina, R., James, P.S.B.R. and James, D.B., Wattiez, R., Jangoux, M. and 1993. Ecology, breeding, seed Eeckhaut, I., 2009. A new method production and prospects for farming to induce oocyte maturation in of sea cucumbers from the sea holothuroids (Echinodermata). around India. Fishing Chimes, 13, Invertebrate Reproduction and 28-34. Development, 53(1), 13-21. Kang, K.H., Kwon, J.Y. and Kim, Lokani, P., 1995. Fisheries dynamics, Y.M., 2003. A beneficial coculture: ecology and management of beche- charm abalone Haliotis discus de-mer at the Warrior Reef, Torres hannai and sea cucumber Stichopus Straits Protected Zone, Papua New japonicus. Aquaculture, 216, 87–93. Guinea. M.Sc. James Cook Katow, H. and Katow, T., 2014. One- University, Australia. step detection of matured females Manikandan, K.P., 2000. From K.P. using immunochromatography Manikandan. SPC Beche-de-mer measuring kit for aquaculture of the Information Bulletin, 13, 33-34. sea cucumber Apostichopus Marine Products Exports japonicus (Selenka). Egyptian Development Authority (MPEDA), Journal of Aquatic Research, 40, 1989. Handbook on aquafarming: 317-324. sea weed, sea urchin, and sea Khrisnaswamy, S. and Krishnan, S., cucumber. Marine Products Export 1967. A report on the reproductive and Development Authority, pp. 33- cycle of holothurian Holothuria 47. scabra Jaeger. Current Science, 36, Massin, C., 1999. Reef-dwelling 155-156. Holothuridea (Echinodermata) of the Ko, S.H., Go, S., Okorie, E.O., Kim, Spermonde Archipelago (South- Y.C., Lee, S., Yoo, G.Y. and Bai, West Sulawesi, Indonesia). S.C., 2009. Preliminary study of the Zooligische Verhandelingen (Leiden) dietary -tocopherol requirement in 329, 1-144. sea cucumber, Apostichopus Massin, C., Uthicke, S., Purcell, S.W., Rowe, F.W.E. and Samyn, Y., 22 Junus et al., A review on the recent advances in the biology and aquaculture technology …

2009. Taxonomy of the heavily the tropical sea cucumber Holothuria exploited Indo-Pacific sandfish scabra. Journal of Experimental complex (Echinodermata: Marine Biology and Ecology, 249, Holothuriidae). Zoological Journal 89-110. of the Linnean Society, 155, 40-59. Mercier, A., Battaglene, S.C. and Mercier, A. and Hamel, J-F., 2013. Hamel, J.F., 2000b. Periodic Sea cucumber aquaculture: hatchery movement, recruitment and size- production, juvenile growth and related distribution of the sea industry challenges. In: Allan, G. cucumber Holothuria scabra in and Burnell, G., eds. Advances in Solomon Islands. Hydrobiologia, Aquaculture Hatchery Technology. 440, 81-100. Cambridge: Woodhead Publishing. Mills, D.J., Duy, N.D.Q., Juinio- pp. 431-454. Meñez, M.A., Raison, C.M. and Mercier, A., Battaglene, S.C. and Zarate, J.M., 2012. Overview of sea Hamel, J.F., 1999a. Daily cucumber aquaculture and sea burrowing cycle and feeding activity ranching research in the South-East of juvenile sea cucumbers Asian region. In: Hair, C.A, Holothuria scabra in response to Pickering, T.D. and Mills, D.J. eds. environmental factors. Journal of Asia-Pacific Tropical Sea Cucumber Experimental Marine Biology and Aquaculture. ACIAR Proceedings Ecology, 239, 125-156. No. 136, pp. 22-32. Mercier, A., Battaglene, S.C. and Moiyadeen, N.M., 1994. The biannual Hamel, J.F., 1999b. Daily activities reproductive activity in Holothuria of the juvenile sea cucumbers (Metriatyla) scabra (Jaeger, 1833) Holothuria scabra in response to the most abundant commercial environmental factors. In: Abstracts holothuroid of the north-western 34th European Marine Biology coastal waters. In: Proceedings of Symposium, Ponta Delgada, 13-17 the First Annual Scientific Sessions, September. 83P. NARA, Colombo, Sri Lanka, 2 Mercier, A., Battaglene, S.C. and November 1993. pp. 123-129. Hamel, J.F., 1999c. Distribution and Morgan, A.D., 1999. Husbandry and population structure of the sea spawning of sea cucumber cucumber Holothuria scabra in the Holothuria scabra (Echinodermata: Solomon Islands. In: Abstracts 34th Holothuroidea). SPC Beche-de-mer European Marine Biology Information Bulletin, 12, 35. Symposium, Ponta Delgada, 13-17 Morgan, A.D., 2000. Aspects of the September, 88P. reproductive cycle of the sea Mercier, A., Battaglene, S.C. and cucumber Holothuria scabra Hamel, J.F., 2000a. Settlements (Echinodermata: Holothuroidea). preferences and early migration of Journal of Survey in Fisheries Sciences 4(2) 2018 23

Bulletin of Marine Science, 66(1), Paper No. 463. Rome: FAO, pp. 47-57. 333-346. Namukose, M., Msuya, F.E., Ferse, Plotieau, T., Baele, J.-M., Vaucher, F.C.A., Slater, M.J. and R., Hasler, C.-A., Koudad, D. and Kunzmann, A., 2016. Growth Eeckhaut, I., 2013. Analysis of the performance of the sea cucumber impact of Holothuria scabra Holothuria scabra and the seaweed intensive farming on sediment. Eucheuma denticulatum: integrated Cahiers de Biologie Marine, 54(4), mariculture and effects on sediment 703-711. organic characteristics. Aquaculture Purcell, S.W., Patrois, J. and Fraisse, Environment Interactions, 8, 179- N., 2006. Experimental evaluation of 189. co-culture of juvenile sea cucumbers, Okumura, S., Kimura, K., Sakai, M., Holothuria scabra (Jaeger), with Waragaya, T., Furukawa, S., juvenile blue shrimp, Litopenaeus Takahashi, A. and Yamamori, K., stylirostris (Stimpson). Aquaculture 2009. Chromosome number and Research, 37(5), 515-522. telomere sequence mapping of the Purcell, S.W., Polidoro, B.A., Hamel, Japanese sea cucumber Apostichopus J-F., Gamboa, R.U. and Mercier, japonicus. Fisheries Science, 75(1), A., 2014. The cost of being valuable: 249-251. predictors of extinction risk in Ong Che, R.G. and Gomez, E.D., marine invertebrates exploited as 1985. Reproductive periodicity of luxury seafood. Proceedings of the Holothuria scabra Jaeger at Royal Society: Biological Science, Calatagan, Batangas, Philippines. [online] Available at Asian Marine Biology, 2, 21-29. http://rspb.royalsocietypublishing.or Ozer, N.P., Mol, S. and Varhk, C., g/content/281/1781/20133296 2004. Effect of the handling [Accessed 05 April 2017]. procedures on the chemical Purdy, D.H., Hadley, D.J., Kenter, composition of sea cucumber. J.O., Kinch, J., 2017. Sea cucumber Turkish Journal of Fisheries and moratorium and livelihood diversity Aquatic Sciences, 4, 71-74. in Papua New Guinea. Coastal Pitt, R. and Duy, N.D.Q., 2004. Management 12, 1-17. Available at Breeding and rearing of the sea http://dx.doi.org/10.1080/08920753. cucumber Holothuria scabra in Viet 2017.1278147 Nam. In: Lovatelli, A., Conand, C., Purwati, P., 2006. Reproductive Purcell, S., Uthicke, S., Hamel, J-F pattern of Holothuria scabra and Mercier, A. eds. Advances in (Echinodermata: Holothuroidea) in Sea Cucumber Aquaculture and Indonesian waters. Marine Research Management, Fisheries Technical in Indonesia, 30, 47-55. 24 Junus et al., A review on the recent advances in the biology and aquaculture technology …

Saito, M., Kunisaki, N., Urano, N. Slater, M. and Chen, J., 2015. Sea and Kimura, S., 2002. Collagen as cucumber biology and ecology. In: the major edible component of sea Brown, N.P. and Eddy, S.D., eds. cucumber (Stichopus japonicus). Echinoderm Aquaculture. New Journal of Food Science, 67, 1319- Jersey: Wiley-Blackwell. pp. 47-56. 1322. Slater, M., 2015. Use and exploitation Sakthivel, M. and Swamy, P.K., 1994. of sea cucumbers. In: Brown, N.P. International trade in sea cucumbers. and Eddy, S.D., eds. Echinoderm Bulletin of the Central Marine Aquaculture. New Jersey: Wiley- Fisheries Research Institute, 46, 91- Blackwell, pp. 57-73. 98. Springhall, J.A. and Dingle, J.G., Schneider, K., Silverman, J., Kravitz, 1967. Growth and pathology of B., Rivlin, T., Schneider-Mor, A., chicks fed beche-de-mer meal. Barbosa, S., Byrne, M. and Australian Veterinarian Journal, 43, Caldeira, K., 2013. Inorganic 298-303. carbon turnover caused by digestion Takashi, H., Nobuhiro, Z., Kyoko, Y., of carbonate sands and metabolic Ryoko, N., Xue, C. and Tatsuya, S., activity of holothurians. Estuarine, 2005. Recent advances in researches Coastal and Shelf Science, 133, 217- on physiologically active substances 223. in holothurians. Journal of Ocean Shelley, C.C., 1981. Aspects of the University of China, 4, 193–197. distribution, reproduction, growth, Tuwo, A. 1999. Reproductive cycle of and fishery potential of Holothurians the holoturian Holothuria scabra in (beche-de-mer) in the Papuan coastal Saugi Island, Spermonde lagoon. M.Sc. University of Papua Archipelago, Southwest Sulawesi, New Guinea. Indonesia. SPC Beche-de-mer Shi, C., Dong, S., Wang, F., Gao, Q. Information Bulletin, 11, 9-12. and Tian, X., 2015. Effects of the Uthicke, S. and Benzie, J.A.H., 1998. sizes of mud or sand particles in feed Improving the conservation on growth and energy budgets of management of the commercial sea young sea cucumber (Apostichopus cucumber Holothuria scabra japonicus). Aquaculture, 440, 6-11. (Sandfish). Final report produced Sithisak, P., Pongtippatee, P. and for the Australian National Parks Withyachumnarnkul, B., 2013. and Wildlife Service. Project No. Improving inland culture WRCP-019. Australian Institute of performance of juvenile sea Marine Science. 20P. cucumbers, Holothuria scabra, by Uthicke, S. and Benzie, J.A.H., 1999. co-culture with red tilapia. Allozyme variation as a tool for Songklanakarin Journal of Science beche-de-mer fisheries management: and Technology, 35(5), 501-505. a study on Holothuria scabra Journal of Survey in Fisheries Sciences 4(2) 2018 25

(sandfish). SPC Beche-de-mer Information Bulletin, 12, 18-23. Yahyavi, M., Afkhami, M., Javadi, A., Ehsanpour, M., Khazaali, A., Khoshnood, R. and Mokhlesi, A., 2012. Fatty acid composition in two sea cucumber species, Holothuria scabra and Holothuria leucospilata from Qeshm Island (Persian Gulf). African Journal of Biotechnology, 11, 2862-2868. Yamashita, M., Mita, K., Yoshida, N. and Kondo, T., 2000. Molecular mechanisms of the initiation of oocyte maturation: general and species-specific aspects. Progress in Cell Cycle Research, 4, 115-129. Yibmantasiri, P., Leahy, D.C., Busby, B.P., Angermayr, S.A., Sorgo, A.G., Boeger, K., Heathcott, R., Barber, J.M., Moraes, G., Matthews, J.H., Northcote, P.T., Atkinson, P.H. and Bellows, D.S., 2012. Molecular basis for fungicidal action of neothyonidioside, a triterpene glycoside from the sea cucumber, Australostichopus mollis. Molecular Biosystems, 8, 902-912. Yuan, X.T., Yang, H.S., Zhou, Y., Mao, Y.Z., Zhang, T. and Liu, Y., 2006. The influence of diets containing dried bivalve feces and/or powdered algae on growth and energy distribution in sea cucumber Apostichopus japonicus (Selenka) (Echinodermata: Holothuroidea). Aquaculture, 256, 457-467.