Reviews in Aquaculture (2014) 6, 1–21 doi: 10.1111/raq.12068

Rearing European brown shrimp (Crangon crangon, Linnaeus 1758): a review on the current status and perspectives for aquaculture Daan Delbare1, Kris Cooreman1 and Guy Smagghe2

1 Animal Science Unit, Research Group Aquaculture, Institute for Agricultural and Fisheries Research (ILVO), Ostend, Belgium 2 Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium

Correspondence Abstract Daan Delbare, Animal Science Unit, Research Group Aquaculture, Institute for Agricultural The European brown shrimp, Crangon crangon, is a highly valued commercial and Fisheries Research (ILVO), Ankerstraat 1, species fished in the north-eastern Atlantic, especially the North Sea. The shrimp 8400 Ostend, Belgium. fisheries are mainly coastal and exert high pressures on the local ecosystems, Email: [email protected] including estuaries. The culture of the species provides an alternative to supply a niche market (large live/fresh shrimps) in a sustainable manner. However, after Received 5 February 2014; accepted 5 June more than a century of biological research on this species, there is still little 2014. knowledge on its optimal rearing conditions. C. crangon remains a difficult spe- cies to keep alive and healthy for an extended period of time in captivity. This review is based on a comprehensive literature search and reflects on the current status of experimental rearing techniques used for this species, identifies the prob- lems that compromise the closing of the life cycle in captivity and provides exam- ples on how these problem issues were solved in the culture of commercial shrimp species or other crustaceans. The ability to consistently produce high- quality offspring could initiate the commercial production of this valuable shrimp. A further advantage of the ability to consistently produce high-quality offspring of this species would facilitate research on the development of new bio- assays with this ecologically and economically important species in a wide variety of biochemical and physiological studies.

Key words: cannibalism, Crangon crangon, disease, formulated feed, nutritional requirements, production techniques.

reach 80 individuals per m2 in intertidal pools and shallow Introduction water; Boddeke et al. 1986) and as epibenthic predator on a The European brown shrimp, Crangon crangon, is an omni- wide range of organisms, such as worms, amphipods, present inhabitant of the shallow coastal shelf region in the schizopods, copepods, cyprid larvae of Balanus, snails, north-eastern Atlantic from northern Norway to the Atlan- young mussels and even juvenile fish (Ehrenbaum 1890; tic coast of Morocco, including the White Sea, the Baltic Herdman 1892; Havinga 1930; Plagmann 1939; Van der Sea, the Mediterranean Sea and the Black Sea (Plagmann Veer & Bergman 1987). 1939; Tiews 1970; Kuipers & Dapper 1984; Gibson et al. Crangon crangon is also economically a valuable target 1995; Spaargaren 2000). Recently (first observations in species. A fishing fleet of more than 600 vessels from six 2003), C. crangon has also colonized the west and south countries (Belgium, Denmark, France, Germany, the Neth- coasts of Iceland (Gunnarsson et al. 2007). erlands and the UK) lands annually more than 30 000 tons Crangon crangon is ecologically an important species, of commercial shrimp (>50 mm total length, TL), repre- due to its central place in the food web: as prey organism senting approximately € 100 million (Hufnagl 2009; FAO for many marine species and birds within its distribution 2013). The primary product is shrimp that was boiled on area (Herdman 1892; Gilis 1952; Kuhl€ 1956, 1961, 1963a,b, board in a traditional way in sea water with addition of salt, 1964a,b; Tiews 1965), as competitor for spawning area, subsequently resulting in a limited product range (boiled food supply and shelter space (juvenile abundance can shrimp) which is very sensitive to spoilage and has a short

© 2014 Wiley Publishing Asia Pty Ltd 1 D. Delbare et al. shelf life. Traditional peeling is carried out on a small-scale, ing water temperature (Fig. 1) within the range of 6–21°C local and immediately transported for consumption, but (Wear 1974). the bulk of the boiled product is transported for peeling The duration of the larval development is also positively (using hand or peeling machine) within or outside Europe. correlated with the water temperature. But according to The processed shrimp require therefore a thorough conser- Criales and Anger (1986), this is only true for temperatures vation treatment to prolong the shelf life (Broekaert et al. between 9 and 18°C. They observed that at 9°C, the survival 2011). The processed product is sold at a retail price rate was 32% with a moulting frequency of 5 times, while between 21.1 and 39.9 € kg 1 in Belgium, the Netherlands at 15°C, it took between 5 and 9 moults before reaching the and Luxembourg (Aviat et al. 2011). first juvenile stage with a survival of 70%, but with Despite the high commercial value of the species, little increased frequency of stunted forms. attention has been given to improve the breeding tech- niques. This paper reviews the current status of rearing Salinity C. crangon, by combining the existing knowledge on its Although C. crangon is generally considered as an euryha- reproduction biology and breeding techniques. We also line species, this is only true for the juveniles (75% sur- tried to identify gaps of knowledge and major problems to vival at a salinity of 5 ppt; Cieluch et al. 2004) and succeed in closing the life cycle in captivity, and where pos- adults. Hagerman (1970) observed that the haemolymph sible, we provided solutions by proposing techniques and of adult C. crangon was almost iso-osmotic with the med- husbandry strategies that are used in the intensive culture ium at a salinity of 21–23 ppt. On the other hand, larvae of commercial crustaceans. The aquaculture production of exhibit a much narrower salinity tolerance, with high sur- C. crangon has the opportunity to continuously supply the vival rates between 17 and 32 ppt. Slower development market with big size and high-quality live specimens in a rates were observed at salinities below 25 ppt (Criales & sustainable manner. Anger 1986) and survival decreased rapidly in media below 10 ppt (Cieluch et al. 2004). According to Criales and Anger (1986), the optimum salinity for larvae at Husbandry conditions 12°C was 32 ppt, while survival was significant lower and Water quality and light regime the periods between development stages longer at 25 and 37 ppt, respectively. Temperature The maturation process is also influenced by the salinity. Temperature has a major influence on the development In experiments carried out by Gelin et al. (2001), adult and metabolic rate of poikilothermal organisms, such as females reared at 25 ppt became ovigerous after 32 days, crustaceans, with higher metabolic rates at higher tempera- while it took 80 days at 15 ppt and no female became ovi- tures, within an optimal range. Subsequently, temperature gerous at 5 ppt. The fecundity was also higher in females significantly influences embryogenesis, larval and juvenile reared at 25 ppt, compared with specimens reared at growth, feeding incidence, moulting, reproduction and sur- 15 ppt. vival. As in most crustaceans, copulation takes place just after the female has moulted (Nouvel 1939; Lloyd & Yonge 1947; Tiews 1954). Subsequently, the frequency of moulting and its incubation period will determine the number of spawns within the breeding period. Meixner (1966) observed that females can spawn up to five times (with an average of 3.6 times) within 5 months in captivity at a constant water temperature of 14°C. Hufnagl and Temming (2011) found a clear relation between the moult interval (mi), tempera- ture (T,in°C) and total length (TL, in mm) under labora- tory conditions:

0:7364 0:09363T mi ¼ 5:7066TL e ð1Þ

During spawning, the female transfers the fertilized eggs from the genital opening to the pleopods (Lloyd & Yonge Figure 1 Incubation period of C. crangon eggs in relation to tempera- 1947), where the eggs are kept until hatching. The length of ture (after (♦) Havinga 1930; (○) Tiews 1954; (●) Meixner 1969 and (■) the incubation period decreases exponentially with increas- Redant 1978).

Reviews in Aquaculture (2014) 6, 1–21 2 © 2014 Wiley Publishing Asia Pty Ltd Rearing techniques for Crangon crangon pH that this can also result in gas bubble disease in crustaceans Studies on effects of abnormal pH values on the develop- (Weitkamp & Katz 1980). ment of crustaceans are scarce. At increased pCO2 levels (1200 latm and pH below 7.8), larvae of Homarus gamma- Light rus (Linnaeus 1758) showed significant higher number of Crangon crangon is mainly active during the night, espe- deformities, such as curled carapace and bent rostrum cially at dusk and dawn (Pihl & Rosenberg 1984; Feller (Agnalt et al. 2013). Under the same conditions, the calcifi- 2006). Dalley (1980) investigated the influence of a circa- cation rate in the larval stages 3 and 4 was significantly dian (12L/12D) and two non-circadian (8L/8D and LD reduced, although there was no direct effect on growth random) light–dark cycles on C. crangon from hatching to (Arnold et al. 2009). As growth in crustaceans occurs the late juvenile stage and observed that during the larval directly after moulting, after which the new shell hardens phase, the survival under non-circadian regimes was signif- with the deposition of calcium carbonate (CaCO3) and icantly lower, 45.6% and 20.8%, respectively, vs. 52.1% at magnesium carbonate (MgCO3), deformities of the cara- circadian regime. This observation supports the hypothesis pace and extremities could be caused by changes in energy that light is an important factor in various physiological fluxes to maintain homoeostasis, which disrupt the normal processes within the animal. There was, however, no evi- deposition of these salts. Particularly, C. crangon seems to dence that growth or morphological development was be very sensitive to small pH decreases and reacts rapidly affected under non-circadian regimes. A light cycle of 10L/ with increased avoidance behaviour (Almut & Bamber 14D was successfully used on C. crangon from Zoea III 2013). onwards (Meixner 1966) and 14L/10D was used positively These experiments show that it is important to keep the on larvae (Costlow & Bookout 1971) as well as on adults pH as stable and as close as possible to the natural pH levels (Taylor & Collie 2003). In conclusion, although C. crangon of sea water. This is particularly of great importance in is night active, a circadian light cycle is preferred. intensive culture, because higher pCO2 levels are inherently related to high stocking densities and the use of recirculat- Noise ing aquaculture systems—RAS, where acidification of the Decapod crustaceans have sensory hairs on their body culture medium could hamper normal development in lar- and appendages. These mechanosensory setae enable the vae and affect normal behaviour of the shrimps in general. organism to detect vibrations and collect information This can be prevented by securing the natural buffering from the environment. Electrophysiological studies on capacity of sea water, for example by washing out CO2 these mechanoreceptors showed that these react to a from the medium with the use of agitators, periodic addi- narrow frequency band (40–70 Hz) (Tazaki 1977). For tion of sodium hydrogen carbonate (NaHCO3) or with the obvious reasons, the ambient noise in culture conditions use of a calcium carbonate reactor on CO2. (pumps, machinery, compressors, etc.) is usually much higher than that in natural conditions. Sound pressure Oxygen levels (SPL) in commercial aquaculture systems were At rest, the oxygen consumption rate (OCR) of C. crangon found to be 125–135 dB in the 25–100 Hz range, and 1 1 ranges between 0.62 and 1.56 mg O2 h g wet weight 100–115 dB in the 1–2 kHz (Bart et al. 2001). Experi- for 1.2 and 0.01 g individuals (at a salinity of 24 g kg 1 ments on the effects of noise on C. crangon showed that and a water temperature of 20°C), respectively (Van Donck high SPLs cause modifications in behaviour (increased & De Wilde 1981). Similar OCRs were observed by Hager- cannibalism) and a significant reduction in growth man (1970), who also demonstrated an increased OCR and reproduction rates (Lagardere & Sperandio 1981; during swimming or moulting with a factor 2.5–3.0. When Lagardere 1982), and increased oxygen consumption and the oxygen level decreases, C. crangon initially raises its ammonia release (Lagardere & Regnault 1980). These front end out of the sand, to ventilate more efficiently. At symptoms are very similar to those induced by adapta- 40–50% of the normal partial oxygen pressure in the water tion to stress (Regnault & Lagardere 1983).

(pO2), the shrimps emerge from the sand and act ‘restless- As to optimize the breeding conditions for C. crangon,it ness’. At lower pO2 levels in the water, e.g. 30% of the nor- will be necessary to maximally reduce ambient noise in the mal pO2 or lower, the shrimps become apathic (Hagerman tanks, for example by installing piping without direct con- & Szaniawska 1986). These data are useful for the construc- tact to the tank, e.g. suspended inlets, effluent pipes discon- tion of production tanks to guarantee oxygen levels of more nected from the drain, expansion couplings between PVC than 50% pO2 during active or stress periods, according to piping and pumps, and installation of noise suppressors the stocked biomass in the tank. But also oxygen supersatu- and sound insulation material between tanks and support ration must be avoided, because it has been demonstrated (Davidson et al. 2007).

Reviews in Aquaculture (2014) 6, 1–21 © 2014 Wiley Publishing Asia Pty Ltd 3 D. Delbare et al.

tial for the use of formulated feeds as larval feed in Food requirements crustaceans (Table 2). Larval diet From earlier studies (Wehrtmann 1991; Kattner et al. 1994; Nursery and on-growing diet Paschke et al. 2004), it seems essential that first feeding The effects of feed in C. crangon on growth were discussed must take place within the first 24 h after hatching to guar- by Hufnagl et al. (2010). Protein requirements decrease antee high survival and development rate. In most of the during growing, with an optimal protein content of 60% in larval rearing experiments with C. crangon, Artemia nauplii 19 mm shrimp to 30% in 30 mm shrimp (Regnault & Lu- were used successfully without prior enrichment (Table 1). quet 1974). Although it is believed that shrimps have no But Criales and Anger (1986) observed a higher survival specific requirements for carbohydrates, Regnault (1981) with rotifers in Zoea I–III larvae. observed that C. crangon uses carbohydrates for short-term According to Figueiredo et al. (2012), the fatty acid pro- energy boosts. But lipids are the main source of energy in file of the eggs can be used to determine the nutritional the shrimp’s diet and provide essential fatty acids, which requirements during larval development, as the yolk are structural compounds of the cell membrane, aid in the reserves are the main source of energy and building blocks absorption of fat-soluble vitamins and serve as well as pre- during embryonic and pre-feeding larval development. Fur- cursor for metabolic regulators (such as hormones). From thermore, Urzua and Anger (2013) demonstrated ‘carry- several studies, it became clear that decapod crustaceans over effects’ from the embryonic to the larval stage in Euro- require HUFA, such as EPA, DHA and arachidonic acid pean brown shrimp. The use of fatty acids during the (ARA) (Mourente 1996), phospholipids and sterols (Harri- embryonic phase could therefore give useful information son 1990), as these were found to be the first used during on the requirements for essential fatty acids in maturation, food deprivation. They were furthermore identified as the eggs and during the early larval phase. Pandian (1967) essential compounds during development and transforma- followed the chemical composition of C. crangon during tion (Perez-Velazquez et al. 2003; Maazouzi et al. 2007). embryogenesis and observed a relative increase in proteins Cholesterol was observed to be an essential component as a from 58.7% to 69.3% and a decrease in fat from 32.6% to precursor of steroid hormones, such as sex and moulting 15.6% per unit of dry weight, indicating that lipids are the hormones, adrenal corticoids, bile acids and vitamin D main energy source during egg development. Kattner et al. (Holme 2008). (1994) investigated the fatty acid composition in eggs and In captivity, juveniles and adults have been fed success- several larval stages of C. crangon and observed that the fully on a wide range of fresh and/or frozen organisms major fatty acids in the eggs were palmitic acid (16:0) and (Table 1), but live copepods resulted in the best growth stearic acid (18:0), palmitoleic acid (16:1n-7), vaccenic acid and survival rate (Uhlig 2002; Hufnagl & Temming 2011). (18:1n-7), oleic acid (18:1n-9), eicosapentaenoic acid The disadvantages of the use of fresh/frozen feed are (i) (20:5n-3, EPA) and docosahexaenoic acid (22:6n-3, DHA). fluctuation in availability and nutritional value, (ii) rapid Other highly unsaturated fatty acids (HUFAs) detected water quality deterioration and (iii) risk of introducing were linoleic acid (18:2n-6) and arachidonic acid (20:4n-6, pathogens in the culture system. To rule out these problems ARA), although at lower percentages. The percentage of and risks, the use of an artificial diet is essential. Further- myristic acid (14:0) remained constant throughout more, such formulated diets make it much easier to incor- embryogenesis, while 16:0 showed a decrease and 18:0 an porate specific ingredients, such as immune stimulants, increase. The monounsaturated fatty acids 16:1n-7 and 18: therapeutics, hormones and attractants. n-7 increased, while 18:1n-9 decreased to approximately Experiments with C. crangon on artificial diets are rare. half of the original content in the eggs. The concentration From previous (Regnault et al. 1975) and our own prelimin- of EPA increased, while there was a slight decrease in DHA ary experiments, it is clear that C. crangon does not readily content (Table 4). As the fatty acid profiles from eggs and ingest dry pellets. Sharawy (2012) used an experimental diet larvae revealed a low consumption of EPA and DHA, this based on 56% proteins and 12% lipids, which resulted in might indicate that these HUFAs are indeed not essential lower growth rates and condition factors, higher mortalities for the larvae. This confirms the fact that larvae of C. cran- and longer intermoult periods, indicating a lack of certain gon can be reared successfully on Artemia nauplii (poor in essential components in the diet or a general unattractive- DHA and EPA). A similar finding was demonstrated for ness of the pellet. On the other hand, Hufnagl and Temming the rearing of wharf crab (Armases cinareum, Bosc 1802) (2011) obtained a good survival (80%) and growth rate â (Figueiredo et al. 2012). (0.2 mm per day) on commercial pellets (Dana feed ). Fur- Feeding experiments on formulated diets have never ther research is therefore needed to improve diet composi- been carried out for rearing larvae of C. crangon, but sev- tion, with focus on essential nutrients and palatability eral experiments on other shrimp species indicated a poten- through the use of chemical attractants and/or texture.

Reviews in Aquaculture (2014) 6, 1–21 4 © 2014 Wiley Publishing Asia Pty Ltd © eiw nAquaculture in Reviews Table 1 Housing and confinement conditions (stocking density, water parameters, feed and frequency) are given in relation to survival and growth rate for C. crangon, according to the author. NM: 04WlyPbihn saPyLtd Pty Asia Publishing Wiley 2014 not mentioned, because this was not within the scope of the study

Stage Housing Density Water parameters Feed (frequency) Survival Growth rate Reference mm per day

Zoea larvae (2014) Zoea III–V Glass beaker (325 mL), static NM Salinity: 30 ppt; Temperature: Artemia nauplii NM Meixner (1965) system with water renewal 14 0.5°C; Light cycle: 10L (45 6 1–21 , (29 per week) Lux)/14D Zoea I–V Glass beaker (500 mL), static 50 ind. L 1 Salinity: 30–32 ppt; Temperature: Rotifers & Artemia nauplii (10 64–76% 0.01–0.14 Criales and system with water renewal 12°C ind. cm 3 ) Anger (1986) (every 2nd day); 1 lm filtered seawater Zoea I–V 80-mL glass beaker; 1-lm Individually Salinity: approximately 32 ppt; Artemia nauplii 96–100% NM Paschke filtered seawater Temperature: 15°C; Light cycle: et al. (2004) 12L/12D Zoea larvae 100-mL plastic beaker, static Individually Salinity: 25 ppt, Temperature: 18°C Artemia nauplii (daily) NM NM Cieluch system (1-lm filtered and and Light cycle: 12L/12D et al. (2004) UV-sterilized seawater (changed daily) Juveniles Juveniles Glass beaker, static with Individually Salinity: 30 ppt; Temperature: 14°C; Artemia biomass NM 0.39–0.63 Meixner (1969) (20 mm) water renewal (29 per Light cycle: 10L (45 Lux)/14D week) Juveniles 2-L aquaria, static system with Individually Salinity: 20 ppt; Temperature: 5– Nematods (Panagrellus NM 0.02–0.14 Gerlach (14 mm water renewal (monthly), no 25°C; Light cycle: NM redivivus) and Schrage and larger) sand (1969) Juveniles 50-L aquarium with 60 Individually Temperature: 20°C Artificial diet (daily) 65–78% NM Regnault (9–17 mm) compartments, flow-through (30 days) et al. (1975) system (50 L h 1 ) 44–54% (60 days) Juveniles 3-L aquarium 3.33–6.66 ind. L 1 Temperature: 15–17°CNM81–87% NM Regnault for techniques Rearing (16–22 mm) (30 days) et al. (1975) Juveniles 1–4-L Perspex chamber, 6–25 ind. L 1 Salinity: 35 ppt; Temperature: Frozen Crangon crangon and NM 0.03 Edwards (1978) (20–30 mm) recirculation system 10, 15 & 20°C; Light cycle: 14L/10D macerated clupeid teleost Juveniles 1.8-L Perspex chamber with Individually Salinity: 35 ppt, Temperature: 20°C, Artemia nauplii NM 0.53 Dalley (1980) (20–35 mm) sand Light cycle: 12L/12D, 8L/8D, Random Juveniles Temperature: 16–17°C Live zooplankton 0.56 Uhlig (2002) (20–40 mm) Smelt 0.25 crangon Crangon Juveniles 10-L plastic aquarium + petri 1 ind. L 1 Salinity: 31.7 0.05 ppt; Frozen sprat (Sprattus 60% 0 Hufnagl and (18 mm) dish with sand, in a Temperature: 14.9 0.1°C; Light sprattus) Temming (2011) recirculation system (40 m3) cycle: 12L/12D Fresh cockle meat 60% 0.1 (Cerastoderma edule) 5 6 Delbare D. tal. et Table 1 (continued)

Stage Housing Density Water parameters Feed (frequency) Survival Growth rate Reference mm per day

with protein skimmer and Fresh periwinkle meat 70% 0.1 aerated wet biofilters (Littorina littorea) Frozen Crangon crangon 60% 0.2 Dana feed pellets 80% 0.2 Artemia nauplii 70% 0.2 Juveniles 50-L basin + sand (500– 0.36 ind. L 1 Salinity: 31.6 0.76 ppt; 35 days fresh cockle meat NM 0.09 Hufnagl and (20 mm) 1000 lm), in a recirculation Temperature: 18.2 0.3°C; Light (C. edulis) & Dana feed Temming (2011) system (1 m3) cycle: 12L/12D pellets 10 days adult Acartia tonsa NM 0.21 0.18 (280 per shrimp daily) Back on Dana feed pellets & NM 0.13 0.15 Arenicola marina Juveniles 132-L tanks in a recirculation Individually or in Temperature: 17.6 0.4°C; Light Artificial diet (at 10% wet 42–63% 0.13–0.16 Sharawy (2012) (30–35 mm) system group at 0.09 cycle: 10L/14D weight once per day at 6 pm ind. L 1 Adults Adults 5.5-L tanks, static system NM Salinity: 18–30 ppt; Temperature Artemia NM 2–5 spawns Meixner (1969) (49.5–58.5 14°C; Light cycle: 10L/14D in 5 months mm) Adults Aquaria + sand, static system NM Salinity: 30 ppt; Temperature: 15°C Arenicola sp. and fish (twice a NM NM Sartoris and (50–70 mm) with water renewal (every week) Portner€ (1997) second day) Ovigerous 5-L aquarium, flow-through Individually Salinity: 32 ppt; Temperature: 15°C; Thawed blue mussel NM NM Cieluch females system (1 lm filtered sea Light cycle: 12L/12D (Mytilus edulis) (every second et al. (2004) water) day) Sexually Aquarium on a flow-through Two females & Salinity: approximately 32 ppt; Mussel meat (Mytilus edulis) Egg laying Paschke °

eiw nAquaculture in Reviews mature system, with sand three males Temperature: 15 C; Light cycle: (every 2nd day) within 5 et al. (2004) © females 12L/12D days after 04WlyPbihn saPyLtd Pty Asia Publishing Wiley 2014 catch (2014) 6 1–21 , © eiw nAquaculture in Reviews Table 2 Use of replacement diets in larval culture of different species and development stages with their result in growth and survival (where available) compared with a control diet with Artemia 04WlyPbihn saPyLtd Pty Asia Publishing Wiley 2014

Species Diet Artemia Larval Result compared with Artemia control References replacement (%) stages

Farfantepenaeus Liquid feeds EpifeedTM & LiqualifeTM 50, 100 M-PL Decreased survival (except Liqualife TM at 50%), growth & Robinson et al. (2005) aztecus stress resistance

(2014) MBD ZeiglerTM E-Z larvae, 50, 100 M-PL Decreased survival, growth and stress resistance Robinson et al. (2005) ZeiglerTM Z-Plus and E-Z Artemia 6

1–21 , Litopenaeus Microencapsulated diet + algae 100 Z-PL 80% at PL7 Jones and Kurmaly (1987) vannamei Microbounded diet 100 47% at M1 Galgani and Aquacop (1988) Microencapsulated diet 70–100 Z-PL 80% survival compared with 90% survival in live food Jones et al. (1979) control (commercial scale) Crumbled microbounded 25, 50, 75, 100 M-PL Decreased growth rates at 50, 75 and 100% and Samocha et al. (1999) diet – microfeast decreased survival at 100% Microencapsulated diet 100 PZ3-M 97.3% and 98.6% (+algae) at mysis Pedroza-Islas et al. (2004) Crumbled microbounded diet 100 PL Similar survival and growth in trial 1, lower survival and Robinson et al. (2005) â Frippak RW+ higher growth in trial 2 (98% survival in Artemia shellfree control) Litopenaeus Crumbled experimental 40, 60, 100 Z-M Decreased survival, growth, development and stress Gallardo et al. (2002) setiferus Microbounded diet resistance (but similar survival at 40 and 60% in the presence of algae) Penaeus indicus Microbounded diet 100 PL 62% at M1 Galgani and Aquacop (1988) Microencapsulated diet 100 PL 55.25% at M1 Kumulu and Jones (1995) Microbounded diet 100 PL20-PL50 100% at PL50 Immanuel et al. (2003) Penaeus japonicus Microencapsulated diet 100 Z-PL 50% at PL1 Jones et al. (1979) Microbounded diet 100 Z-PL 90% at PL1 Kanazawa et al. (1982) Microbounded diet 100 Z-PL 80% at PL Kanazawa et al. (1985) Microbounded diet 100 Z-PL 75% at PL1 Kanazawa (1990) Microencapsulated diet + algae 100 Z-PL 79.5% to PL1 Le Vay et al. (1993) Penaeus monodon Crumbled experimental 100 Z-PL Similar survival but lower growth Kanazawa et al. (1982) microbounded diet Crumbled experimental 100 Z-PL Similar survival but lower growth Kanazawa (1985) microbounded diet for techniques Rearing Microencapsulated diet 100 Z-PL 3–29% to PL7 Jones et al. (1987) Microbounded diet 100 PL 85% to M1 Galgani and Aquacop (1988) Microencapsulated diet 100 Z-PL 51–64% to PL Kurmaly et al. (1989) â Microencapsulated diet – Frippak 100 Z-PL Similar survival but lower growth Jones et al. (1989) Microencapsulated diet 100 Z-PL 80% at PL1 Amjad et al. 1992; Microbounded diet 100 N6-M 52% at M Paibulkichakul et al. (1998) Microencapsulated diet – 100 Z-PL Increased survival, growth and development Wouters and Van

â crangon Crangon Frippak Fresh + one Horenbeeck (2003) single dose of algae in Zoea 1 Crumbled microbounded 40 & 100 PL Lower survival, similar (100%) or improved Wouters and Van â diet + Frippak Flake (40%) growth Horenbeeck (2003) Palaemon elegans Micro-granulated diet 100 Z5-PL1 49% at PL1 Kumulu and Jones (1995)

7 Crangon nigicauda Artemia-microcapsules 100 Z None beyond Z2 Villamar and Brusca (1987) D. Delbare et al.

Experiments with Crangon septemspinosa (Say 1818) and brood stock diet (Figueiredo et al. 2012). Data on the lipid other crustaceans showed that they locate feed by a direc- and fatty acid profiles in eggs and larvae of C. crangon are tional mechanism of scent tracking (Pardi & Papi 1961; very rare (Table 4). The main n-3HUFAs in the eggs were Wilcox 1972). Balss (1931) located the chemoreceptors on EPA and DHA, with a EPA/DHA ratio of 2 (Kattner et al. the outer branch of the first antennae, but also on the pere- 1994), which seems to be a normal ratio for boreal seashore iopods and the mouth extremities. To improve palatability species (Narciso & Calado 2001). This medium EPA/DHA of commercial shrimp feed, fish protein-soluble concen- ratio indicates that C. crangon can be placed at a medium trate and attractant mix (free amino acids) are comple- trophic level, as DHA is highly conserved across the food mented to the diet. For C. crangon, Fittschen (2001) chain. Other fatty acids present in the eggs were 18:1n-7, investigated the effects of certain free amino acids as attrac- 18:1n-9 and ARA. The high percentage of 18:1n-9 is a gen- tant in C. crangon and observed the strongest effects with eral marker for carnivores (Stevens et al. 2004) and indi- L-serine (75% effect at 10 mM) and L-histidine (55% at cates that C. crangon is feeding on small invertebrates. The 0.1 mM) in comparison with mussel meat as the 100% ratio 18:1n-7/18:1n-9 in the eggs was about 0.6, but effect reference. A synergistic effect was obtained by com- increased to 1.6 during larval development, indicating a bining both L-serine and glycin, at 0.5 mM with a 100% high use of 18:1n-9 (Table 4). As these HUFAs are mainly effect (equal to the effect of mussel meat). esterified to phospholipids, which are found in high con- Next to biochemical attractants, texture plays an impor- centrations in the shrimp ovaries, this may indicate that tant role in feeding habits of shrimp, as it first investigates certain phospholipids are essential in maturation diets. the feed particles before bringing them to the mouth Kattner et al. (1994) observed that the lipids in eggs of appendages. Agglomeration techniques can produce soft C. crangon were dominated by phospholipids, more specifi- spherical diets with high levels of soluble proteins and satis- cally phosphatidylethanolamine, phosphatidylcholine and factory particle stability. phosphatidylserine at 66%, 20% and 12% of the total phos- pholipid content, respectively. In contrast to eggs of other Maturation diet shrimp species, only small amounts of triacylglycerides Until today the feed used for maturing C. crangon consists were found, while it is generally accepted that triacylglyce- mainly of frozen blue mussel (Mytilus edulis, Linnaeus rides are the main energy source in eggs and larvae of 1758) (Cieluch et al. 2004; Paschke et al. 2004) (Table 1). shrimp (Wouters & Fegan 2004). As very low levels of Also in commercial shrimp cultures (penaeid shrimps and phosphatidylcholine and phosphatidylserine were found in Macrobrachium spp.), a wide range of unprocessed and fro- the early larval stages of C. crangon, it can be assumed that zen marine organisms, including various fish, molluscs, these phospholipids were predominantly used during worms and crustaceans, are used as maturation diet. As the embryogenesis. This would mean that phosphatidylcholine maturation diet is an important factor for fecundity and and phosphatidylserine are essential in the maturation diet. egg quality (offspring performance and survival), it is often In addition, maturation involves an intensive protein administered as a mixture of different species, to increase synthesis, with subsequently higher protein requirements. the change to cover all nutritional requirements. It is therefore likely that the protein content in the matura- Research on replacing fresh maturation diets with for- tion diet should be approximately 60%, such as found in mulated diets for commercial penaeid shrimps is still scarce fresh feed. (Table 3). As DHA, EPA and ARA are abundant in the ova- Studies on vitamin and mineral requirements in C. cran- ries of shrimp and which cannot be de novo synthesized by gon are completely missing, but nutritional studies on com- the organism, it is believed that these n-3HUFAs are essen- mercial shrimp species confirm that vitamin A, C, D and E, tial in the maturation diet. Furthermore, the n-6HUFAs are as well as calcium, phosphorus, magnesium, sodium, iron, precursors of prostaglandins, which play an important role manganese and selenium should be provided in sufficient in reproduction and vitellogenesis. According to Wouters quantities (Tacon 1987). et al. (1997), the n-3/n-6HUFA ratio in the maturation diet of penaeid shrimp should be around 2/1–3/1. Hoa (2009) System design observed that diversified mixtures of squid, oyster, marine worms and pork liver formulated in such a way to reflect Substrate the ARA/EPA and DHA/EPA ratios of ovaries of wild After metamorphosis, C. crangon juveniles settle on the mature Penaeus monodon (Fabricius 1798) females, resulted bottom. During the daytime, the shrimps stay burrowed in in an enhanced growth and fecundity. the sand, while they leave the soft sediment during the To develop an appropriate maturation diet, valuable night to hunt and scavenge, with a peak in activity at dusk information can be obtained from trophic markers present and dawn (Pihl & Rosenberg 1984). It has been observed in the eggs from gravid females from the wild, reflecting the that the presence of a sand layer reduces stress and interac-

Reviews in Aquaculture (2014) 6, 1–21 8 © 2014 Wiley Publishing Asia Pty Ltd Rearing techniques for Crangon crangon

Table 3 Use of formulated maturation diet in decapod crustaceans, with effect spawning frequency, spermatophore quality, fecundity and off- spring quality (where available)

Species Formulated diet Control Comparison (significant References different)

Litopenaeus Dried diet based on freeze-dried 2.3 frozen squid: 1.4 Daily maturation frequency: Wouters et al. (2002) vannamei Artemia (ART): 50% replacement oyster: 1.3 mussel: FRE = ART < was significantly Control diet (CON): 50% replacement 1 Artemia biomass higher than in ART and FRE; (dry matter ratio) (FRE) spawn frequency and total number of spawns: FRE < CON = ART; eggs per female: FRE < CON = ART; offspring quality: FRE = CON = ART Dried diet based on freeze-dried 2.5 frozen squid: Spawn frequency and total number Artemia (ART): 50% replacement 1.5 polychaetes: of spawns: CON < FRE = ART; eggs Control diet: 50% replacement (CON) 1 enriched Artemia (FRE) per female: FRE ≤ CON ≤ ART; spermatophore quality: FRE = CON < ART; offspring quality: FRE = CON = ART Penaeus 60% Breed-S-Freshâ pellet – INVE Squid, oyster, marine Numbers of spawns: no significant Hoa (2009) monodon worms and pork liver difference; fecundity (eggs/spawning): no significant difference; hatching success: significant better than control (75% and 63%); metamorphosis success: significant better than control (96% and 93%)

tions with conspecifics, especially during moulting (Meix- a tank can, however, act as a trap for organic (waste) mate- ner 1966; Dalley 1980; Sartoris & Portner€ 1997; Taylor & rial, with bacterial proliferation (dominated by Clostridium Collie 2003; Paschke et al. 2004). Regnault (1976) studied sp., Bacillus sp., fermentative bacteria and sulphur-reducing the effect of sand in the tanks on survival and growth bacteria) and oxygen depletion, especially in the deeper (length and weight gain) of C. crangon and discovered that part of the sand layer, as result (Moriarty & Decamp 2009). although the presence of substrate did not influence the This can be very dangerous for the stock, because C. cran- survival rate, it had a clear effect on the growth rate, with gon seems to be very sensitive to H2S, with behavioural more than 1.6 times faster daily weight gain in comparison responses at a concentration of 0.1 lM in the haemolymph with shrimp without sand. As all groups (with sand and no and a median lethal time of 1 h at 20 lM in the haemol- sand) received daily feed ad libitum, the difference can only ymph (Vismann 1996). It is therefore necessary that the be explained by more energy consumption due to abnor- sand is frequently cleaned (stirred), to wash out organic mal diurnal behaviour in the absence of substrate. This matter, before its degradation. observation confirmed the results of Hagerman (1970), As C. crangon is an inhabitant of soft sediment (sandy, which demonstrated that C. crangon deprived from sand sandy-mud and muddy substrata), it is impossible to showed more swimming activity during the daytime, in increase the total surface by the introduction of three- comparison with individuals provided with sand. This dimensional structures in the culture, as is the practice in results in a higher metabolic rate and oxygen consumption, intensive penaeid and Macrobrachium cultures (Tidwell & subsequently in an increased energy expenditure at the Coyle 2008; Zhang 2011). The increase in total production expense of growth. Additionally, it is possible that meiofa- surface is, however, possible with the use of shallow race- una (copepods, nematods, worms, etc.) sand and/or bacte- way systems (see below). ria developing in and on the sand form a substantial feed resource for the shrimp. Furthermore, it is known that Tank design C. crangon consumes sand grains, which are believed to While examining the literature to find rearing techniques assist in grinding the food particles in the cardiac part of for C. crangon, it was striking that most experiments were the stomach (Tiews 1954). carried out in small aquaria or glass beakers of 100 mL– The preferential grain size was observed to be between 1 L, with few or isolated individuals and with frequent 125 and 710 lm (Pinn & Ansell 1993). Such a sand layer in (manual) water renewal (Table 1). To develop a mass cul-

Reviews in Aquaculture (2014) 6, 1–21 © 2014 Wiley Publishing Asia Pty Ltd 9 D. Delbare et al.

Table 4 Composition of different life stages of C. crangon: protein content (% DW), moisture (%), total lipids (% DW), lipid classes (% of the total lipid content) and fatty acid composition of total lipids (% weight). Where possible results are presented as means SD

References Kattner et al. (1994) Domingues et al. (2003)

Live stage Eggs Zoea I Zoea II Zoea V Zoea VII Adult

Component Total protein (lgg1 DW) 74.95 3.67 Moisture (%) 75.18 0.47 Total lipid – TL (% DW) 5.91 0.81 Sphingomyelin (% of TL) 0.22 0.08 Phosphatidylcholine (% of TL) 20 2 7 7 47 21.44 1.05 Phosphatidylserine (% of TL) 12 16 4.23 0.48 Phosphatidylinositol (% of TL) 2.21 0.57 Phosphatidylglycerol (% of TL) 3.33 0.41 Phosphatidylethanolamine (% of TL) 66 98 93 93 37 16.00 0.83 Diacylglycerol (% of TL) 2.36 0.67 Cholesterol (% of TL) 25.02 2.93 Free fatty acids (% of TL) 13.37 1.46 Triacylglycerol (% of TL) –––9.58 5.97 Esterol ester (% of TL) 2.29 0.78 Sterol (% of TL) Neutral lipids (% of TL) 52.56 1.46 Polar lipids (% of TL) 47.44 1.47 FFA (% of TL) 14:0 (% TL weight) 1.8 1.0 2.0 0.4 1.50 0.09 15:0 (% TL weight) 0.89 0.12 16:0 (% TL weight) 24.1 5.8 19.7 1.0 16.50 0.07 16:1 (% TL weight) 4.8 4.2 5.7 1.9 7.68 4.10 18:0 (% TL weight) 6.6 1.2 7.8 1.3 6.02 0.88 18:1 n-9 (% TL weight) 13.1 2.4 6.0 1.3 6.85 0.12 18:1 n-7 (% TL weight) 7.8 2.2 10.0 0.6 6.85 0.14 18:2 n-6 (% TL weight) 0.8 0.3 0.6 0.4 1.93 0.06 18:3 n-3 (% TL weight) ND ND 1.16 0.49 18:4 n-3 (% TL weight) ND 0.2 0.4 0.0 20:1 (% TL weight) 1.47 0.58 20:4 n-6 (% TL weight) 2.3 2.3 1.4 0.6 5.29 0.51 20:4 n-3 (% TL weight) 0.0 20:5 n-3 (% TL weight) 24.4 5.1 34.4 3.5 22.60 0.26 22:5 n-6 (% TL weight) 0.86 0.17 22:5 n-3 (% TL weight) 2.2 2.2 ND 2.58 0.52 22:6 n-3 (% TL weight) 11.6 4.5 12.2 2.6 10.61 0.55 UK (% TL weight) 2.74 1.02 Saturates 32.5 26.64 1.55 Monoenes 25.7 26.89 3.66 n-3 38.2 37.37 1.09 n-6 3.1 8.93 0.78 n-3 HUFA 26.6 36.05 0.83 n-3/n-6 4.20 0.24 DHA/EPA 0.5 0.4 0.47 0.03 EPA/AA 10.6 24.6 4.29 0.46 ture of this species, rearing systems must be developed with 1 Hatchery tanks considerable stocking densities and continuous water When rearing crustacean larvae, special attention should renewal, such as flow-through systems or recirculation be paid to avoid mechanical damage of the larvae (Cala- aquaculture system (RAS) (see below) that minimize han- do et al. 2008). Most commercial hatchery systems for dling. Because larvae exhibit a different behaviour (pelagic) tropical shrimp farming make use of rectangular tanks to juveniles and adults (benthic), the tank design for both with a flat or ‘V’-shaped bottom and a daily water should be different: exchange of 10–100%. Smaller hatchery systems can use

Reviews in Aquaculture (2014) 6, 1–21 10 © 2014 Wiley Publishing Asia Pty Ltd Rearing techniques for Crangon crangon

up-flow systems in cylindro-conical or cylindro-spheri- (Kuhn et al. 2009; Xu & Pan 2013), subsequently reducing cal tanks to keep the shrimp larvae and food particles the feed conversion ratio. Although no data are available

continuous homogeneously distributed in the water col- for C. crangon on the tolerance to ammonia (NH3), nitrite umn. A more advanced system, specific for the culture (NO2 ) and nitrate (NO3 ), safe levels can be found for of planktonic organisms, i.e. shrimp larvae, is the other commercial shrimp species, which can be used as ‘planktonkreisel’ which has a cylindrical compartment guidelines for good water quality management, e.g. 0.1 mg 1 1 containing the larvae and water in- and outlets that are N-NH3 L (Chin & Chen 1987), 0.18 mg N-NO2 L designed in such a way to generate a smooth rotating (Jayasankar & Muthu 1983) and 158 (at a salinity of 1 flow and thereby avoiding dead zones (Greve 1968; 25 ppt) to 232 mg N-NO3 L (at a salinity of 35 ppt) Hamner 1990). (Tsai & Chen 2002). 2 Nursery and on-growing As mentioned before, C. crangon lives mainly on and in Other factors the sand bottom. This means that the tank can be kept shallow. Therefore, this species is a perfect candidate to Stocking density and cannibalism culture in shallow raceway systems (SRS). SRS are rect- There are not much data available on the optimal stocking angular tanks with a flat bottom, narrow width relative density of C. crangon, because most experiments were car- to length and an inlet at one end and an outlet with ried out with individuals in small containers. Criales and screen at the other side. These tanks are developed for Anger (1986) observed a slight (not significant) increase in compact industrial aquaculture production for a num- intermoulting period, but with a clear higher frequency of ber of fish species (Øiestad 1998). The water column stunted forms when larval stocking densities were as high ranges from 7 mm to 25 cm, depending on the tank as 50 larvae L 1. surface and life stage of the fish. The water inlet is Cannibalism is one of the most important problems in designed in such a way to allow a homogeneous current the intensive culture of crustaceans and could be a major in the fish chamber and an efficient removal of waste obstacle in the rearing of C. crangon, as cannibalism has products from the water. Water current speeds in SRS also been observed in wild populations (Marchand 1981; are typically between 0.7 and 5 cm s 1. Due to the low Evans 1984; Feller 2006). Stomach content analysis in tank height, tanks can be stacked in a rack, maximizing shrimps from the Dutch Wadden Sea has shown that can- the production area per m2 of floor space. nibalism is the highest on newly settled juveniles of about 6 mm by shrimps bigger than 30 mm (Derks 1980; del Recirculating aquaculture system Norte-Campos & Temming 1994). Studying the diet of The use of a recirculating aquaculture system (RAS) has C. crangon, Hostens and Mees (2003) observed that canni- lots of advantages: constant water quality parameters, balism was the highest in summer and autumn in the sub- highly energy efficiency (low heating/cooling costs) and less tidal and absent in the intertidal region, although in the risk on input of diseases. Furthermore, water parameters in latter daily consumption was the highest. Pihl and Rosen- a RAS set-up can be constantly monitored, allowing for berg (1984) estimated that juvenile conspecifics can com- immediate action online, lowering the chance of losing the prise up to 20% of the diet for C. crangon in Swedish livestock. Although it is a common practice to use flow- shallow waters. No information on the effect of cannibal- through or batch culture during the hatchery phase in larvi- ism in controlling (generating interannual variability in cultures, recent research has shown that the use of RAS recruitment) or regulating recruitment (damping interan- with moderate ozonization (to 350 mV) resulted in a better nual variability in recruitment) is available (Campos & van control of the microbial community structure and could der Veer 2008). reduce proliferation of opportunistic (pathogenic) Regnault (1976) demonstrated that high stocking den- microbes in the rearing water (Attramadal et al. 2012). The sities in captivity resulted in higher mortality rates after main nitrogen excretion product in C. crangon is ammonia 4 months in captivity, approximately 66% at 291 (94–98%), released through the gill epithelium (Regnault ind. m 2 vs. 40% at 582 ind. m 2, while almost all mor- 1981). To prevent accumulation of ammonia to toxic levels, tality could be contributed to cannibalism. Extreme can- the ammonia can be converted into nitrate in a biofilter nibalistic behaviour of juveniles after metamorphosis was (Spotte 1979) or turned into bioflocs in a biofloc reactor also reported by Dalley (1980), which resulted in high (Avnimelech 2006). In the latter, ammonia is assimilated mortalities upon settlement. Because decapod crustacean by heterotrophic bacteria, which tend to aggregate and larvae exhibit a high degree of cannibalism when the lar- form bioflocs. As C. crangon is also known to feed on detri- val diet is unpalatable or insufficient (Wickins & Lee tus, it is possible to feed the bioflocs to the shrimps, as is 2002), cannibalism can also be a major problem during already carried out in intensive penaeid culture systems the larval stage. But apart from observations as these, no

Reviews in Aquaculture (2014) 6, 1–21 © 2014 Wiley Publishing Asia Pty Ltd 11 D. Delbare et al. quantitative information is yet available. It is also still diatoms to the rearing water (Table 1). But it should be unclear which factors are involved in the initiation of noted that the concentration of microalgae in their experi- cannibalism, i.e. the release of signal products during ments was far from high enough to speak of green water moulting or just the presence of newly moulted individu- technique. als (without a hard carapace). Similar problems with cannibalism were found in cul- Diseases and profylaxis tures of penaeids and Macrobrachium spp. In P. monodon, Crangon crangon in the wild is susceptible to many dis- a clear positive relationship between stocking density and eases, which can also proliferate under culture conditions the rate of cannibalism, and a negative relationship between and wipe out complete stocks (Table 5). Black spot dis- feeding frequency and the rate of cannibalism were found ease is a necrotic shell disease in C. crangon, with a high (Abdussamad & Thampy 1994). But even at low stocking prevalence of sometimes more than 50% of the popula- densities and high feeding frequencies, cannibalism was still tion (Knust 1990; Dyrynda 1998), but is also known to observed, probably due to the aggregation behaviour, for affect numerous other crustaceans (Getchell 1989). The example in corners, which increases the chance of agonistic disease is characterized by melanisation around lesions interactions. Therefore, next to low stocking densities, through the cuticle. The disease starts after an penetra- other factors such as tank design, water current and intro- tion of the epicuticula through mechanical abrasion duction of substrate are important to distribute the larvae, (abrasive action of sediment or fishing activities), juveniles and adults in a more homogeneous manner, and wounding (predatory or cannibalistic attack), chemical to decrease the encounter frequency between individuals, or microbial attack (Vogan et al. 2002) after which the in an attempt for reducing cannibalism (Forster 1970; San- exposed chitinous endocuticle is colonized by chitinolytic difer & Smith 1975; Van Wijk 1999). bacteria (see Getchell 1989 for review) and degrades the exoskeleton. Pereiopods and pleopods are observed to be Green water technique the most affected organs and to a lesser extend the The green water technique, i.e. the addition of unicellular abdominal segments, antenullae and antennae (Vervoort microalgae to the culture water, can also contribute to a et al. 1980). Infections can cause impairment of better homogeneous distribution of the larvae in the tank functions or compromise the integrity of the exoskeletal due to diffusion of the light and reduction in interactions (Dyrynda 1998), giving the opportunity for secondary between siblings. This technique was specifically devel- infections of the underlying tissues. In case the damage oped to improve survival and growth rate of shrimp lar- is not inflicted the newly formed cuticle, the symptoms vae under intensive production conditions. Microalgae of black spot necrosis will be disappeared after moulting serve as a direct food source for the larvae or the prey (Vervoort et al. 1980). organisms (to keep their nutritional value high), but also Another disease with a high prevalence in the wild is the function as stabilizer of the culture, because phytoplank- C. crangon Baculo Virus (CcBV). Although in some cases it ton (i) assimilates carbon dioxide and nitrogenous com- can appear at a high incidence level (sometimes 100%), this pounds from the water, subsequently enhancing the disease does not causes long-term declines of the host pop- water quality, (ii) can excrete antibacterial or probiotic ulation. Stentiford and Feist (2005) showed that CcBV can components to inhibit growth of certain micro-organ- become virulent, when the shrimps are under stress. This isms, (iii) increase the contrast between the water column means that the rearing husbandry conditions and feeding and prey items by light diffraction and (iv) decrease the regime should be optimized to avoid stress, as the starting light intensity by light diffusion (Naviner et al. 1999; material for a culture of C. crangon will always be from the Muller-Feuga et al. 2003a,b; van der Meeren et al. 2007; wild. Natrah et al. 2013). Because the green water technique As shrimp aquaculture is changing to more intensive requires a parallel culture of microalgae next to the rou- and even superintensive systems, the frequency of inci- tine hatchery practices, it increases labour and costs for dents with infectious diseases increases, which hamper larval production. Therefore, recent research is focusing larval production and cause mass stock mortalities. The to reduce the need of live algae through partial substitu- prevention and control of these diseases is therefore the tion by dry algae or by adding an inert substance, like number one priority in the shrimp farming industry. clay, to increase turbidity and diffusion of the light Different strategies have been developed for disease con- (Rieger & Summerfelt 1997). trol. As reviewed by Hauton (2012), promising tech- There is no information on the effect of the green water niques are either the strengthening of the immune state technique on the rearing of C. crangon larvae, although of the shrimp with the administration of glucans or Criales and Anger (1986) observed improved morphologi- poly-beta-hydroxybutyrate, through the enhancement of cal development, but no increase in survival when adding Hsp70 synthesis, or by decreasing the virulence of patho-

Reviews in Aquaculture (2014) 6, 1–21 12 © 2014 Wiley Publishing Asia Pty Ltd © eiw nAquaculture in Reviews 04WlyPbihn saPyLtd Pty Asia Publishing Wiley 2014 Table 5 Diseases infecting C. crangon in the wild (pathogenic agent, specific symptoms, incidence level in the wild and authors)

Disease Agent Symptoms Incidence level in References the wild

(2014) Viruses Crangon crangon The majority of all hepatopancreatic tubules contain Up to 100% Stentiford et al. (2004), – 6 BaciloVirus CcBV cells with numerous aberrant nuclei, separation and Stentiford and Feist (2005) 1–21 , apparent apoptosis of large numbers of infected cells, large numbers of epithelial cells are sloughed into lumen, and the tubules appear to degenerate, often involving epithelial cells of the midgut White spot syndrome White spot syndrome White spot disease causes death in juvenile and adult This ‘tropical shrimp Stentiford et al. (2009) virus – WSSV crustaceans. Infected animals die within 3–10 days disease’ was shown of the appearance of the disease. Affected individuals to be infectious, exhibit a decreased appetite, with white spots on the cause disease and carapace, a white gut content and a red hepatopancreas kill C. crangon Bacteria Black necrosis Aeromonas, Beneckea, Is caused by chitin digesting bacteria resulting in Up to 87% of the Perkins (1967), or black spot disease Alteromonas, exoskeletal erosion, mainly at the antennae, pereiopods sampled population Abbot (1977), Ayres and Flavobacterium, Moraxella, and pleopods, especially the outermost sections of these Edwards (1982), Getchell Pasteurella, Photobacterium appendages. This disease is thought to be the result of (1989), Dyrynda (1998) Pseudomonas, Spirillum injuries inflicted by predatory and cannibalistic and Vibrio interactions combined with a high level of organic enrichment (both natural and anthropogenic) Filamentous bacterial Leucothrix mucor Infected shrimps have filamentous bacterium present on de Figueiredo and Vilela disease the aesthetasc setae, but was also found on live eggs (1972), Shelton et al. (1975), Agnalt et al. (2013) Dinoflagellates Milky disease Hematodinium sp. Infected C. crangon are characterized by a loss of 1.6% in the wash Meyers et al. (1987), Taylor transparency of the cuticle, particularly visible in the and Khan (1995), Stentiford ern ehiusfor techniques Rearing appendages, which is caused by large numbers of et al. (2012a,b) parasite life stages within the haemolymph (milky) of infected shrimp. Atrophied skeletal musculature and enlarged haemal sinuses. The infection also results in a bitter flavour after cooking, making the product unmarketable Microspores –

Cotton shrimp disease Thelohania giardia, Vavraia Infected shrimps show opaque white spots or lines in 5% 15% Henneguy and Thelohan (1892), crangon Crangon mediterranica the muscle tissue of the legs (especially thoracic legs) Sprague and Couch (1971), and the abdomen. In heavily infected individuals, the Azevedo (2001) whole body has a whitish appearance 13 D. Delbare et al. gens through the disruption of bacterial communication and decreasing to 15°C when the body size reaches or quorum sensing. 50–60 mm. Observations of pathogen control in wild populations, such as the prevalence of CcBV in C. crangon, could lead What is needed to culture C. crangon? to mitigation methods under farming conditions. A good example is the increase in RNA interference (RNAi) Technologies used in the culture of commercial species response in shrimp, to suppress virus infections (Barthol- could be introduced in the rearing of C. crangon without omay et al. 2012). This method involves the introduction major modifications, but special attention should be paid of short fragments of RNA (RNAi triggers) that bind to stocking density, tank design, water current, ambient complimentary RNA sequences, subsequently preventing noise and substrate, to reduce cannibalism and optimize specific gene expression in the pathogen. Natural RNAi development rate. Larvae can be reared in high cylindro- pathways, as in C. crangon, could therefore play a critical conical or cylindro-spherical tanks at densities below 50 role in the innate immune response to virus infections in larvae L 1, with open air tubes to provide enough turbu- crustaceans. lence to avoid larvae to aggregate in certain spots and to keep the food in a homogeneous manner in the water col- umn. At this stage, techniques to increase turbidity and Outlook and prospects for the future light diffusion can be used, to further decrease agonistic To determine whether a species is a suitable candidate for interactions between the larvae and thus avoiding canni- aquaculture, Jones (1972) proposed five criteria, to which balism. Furthermore, the feeding behaviour of the larvae the species should meet: growth rate, food conversion rate, should be investigated more closely, to set up an adequate production rate per m2, stock supply (breeding in captiv- feeding protocol. Juveniles and adults can be reared in ity) and market price. Today, sustainability is another SRSs, with stocking densities of 80 juveniles m 2 (Bod- important criterion as well. As C. crangon is sufficiently deke et al. 1986) and about 50 adults m 2. With the use abundant and a flexible organism in terms of diet (feeding of SRSs, total production area can be 5–10 times the used on a wide range of marine organisms and detritus) and floor space. The tanks should be provided with a sand other requirements (living in different habitats and display- layer with a grain size between 125 and 710 lm (Pinn & ing a large temperature and salinity tolerance,...), rearing Ansell 1993) and a high water current between feeding methods can be optimized through an approach of trial periods, to avoid agonistic interactions and accordingly and error. cannibalistic behaviour. Furthermore, the presence of a sand bottom was proven to be essential for reproduction, as females deprived from substrate did not spawn or incu- What is the potential growth rate of C. crangon? bated their eggs (Regnault 1976). During larval rearing, According to Hufnagl (2009), a 5-mm C. crangon in the the optimal water temperature ranges between 12 and wild could reach 80 mm in 650 days at maximum 15°C at a salinity of 30–32 ppt, while the water tempera- growth rate, but under controlled conditions (continuous ture for juveniles and on-growing ranges between 15 and optimal water temperature and sufficient feed availabil- 24°C at a salinity of 25–32 ppt. Dissolved oxygen should ity), the time span to grow to 80 mm could be much be as high as possible, but supersaturation should be shorter. Under laboratory conditions (water temperature avoided. pH level should be approximately 8 and as stable of 15°C and a salinity of 32 ppt), the larval phase takes as possible (Table 1). In all production set-ups, the nitrog- 30–35 days (Ehrenbaum 1890; Thorson 1946; Criales & enous compounds should be kept as low as possible. As Anger 1986), with an estimated survival of approximately wild C. crangon is a potential carrier of many diseases 70% (Criales & Anger 1986). Based on the data of Fonds (Table 5), which could have a devastating effect on the (unpublished observations cited in van Lissa 1977 and culture of this species, special attention should be paid Kuipers & Dapper 1984), shrimp of 80 mm could be during the selection and treatment of the broodstock to obtained after 15–18 months (with modest growth rates avoid introduction of disease, i.e. use of a broad spectrum of 0.08–0.325 mm per day according to the body size). antibiotic, an antibiotic cocktail or vaccination. Further- Hufnagl and Temming (2011), however, compiled growth more, efficient disinfection methods (UV and ozone) data from 16 studies from the wild and 14 studies under should be used on the sea water intake to eliminate influx laboratory conditions and showed that C. crangon could of pathogens in the culture systems. As black necrosis dis- be grown to 80 mm within 1 year (daily growth rate in ease is often the result of mechanical damage, a high pos- mm per day = 0.03054 T0.001 Le0.09984 T), with a sible incidence of this disease could be foreseen when water temperature regime optimized according to the size rearing crustaceans at high densities. Again, it is therefore of the shrimp, starting at 24°C for the early juvenile stage important to avoid cannibalism at all times.

Reviews in Aquaculture (2014) 6, 1–21 14 © 2014 Wiley Publishing Asia Pty Ltd Rearing techniques for Crangon crangon

7 Euro kg 1 in the fish auction to 23 Euro kg 1 in retail. Feed and feed conversion ratio in C. crangon? Because the collection of live shrimps is labour intensive Feeding should be administered during the shrimp’s active and only landed in limited volumes, fishermen cannot periods (at dusk and dawn) and preferably every 2 hours, meet the rising demand for live shrimp. Furthermore, the which coincides with the mean evacuation rate in C. cran- fraction of C. crangon larger than 70 mm in the catches gon (Pihl & Rosenberg 1984). Meixner (1966) estimated the is only approximately 2% of the landings in most recent feed conversion ratio (FCR) to be approximately 2.2 for the years (ICES 2013). These factors make that C. crangon is females and 3.1 for the males (from metamorphosis to the a lucrative candidate for aquaculture. The production of time of reproduction) based on Artemia (at a water temper- European brown shrimp in aquaculture could therefore ature of 14°C and a salinity of 30 ppt). But we are con- supply the market continuously with large size and fresh/ vinced that lower FCR values of approximately 1.5 are live shrimps. An optimized culture technique could also feasible with improved management, especially in combina- enhance the development of standardized bioassay tests tion with bioflocs. The biggest challenge is the development with the European brown shrimp, enabling research on of optimal artificial feeds with good palatability (effective the biological and metabolic systems of this specimen: attractants) and alluring texture, with optimal protein, reproductive traits, sex reversal, speciation, population amino acid and fatty acid profiles and contents and other dynamics, effects of contaminants and hormonal disrup- essential nutrients (e.g. cholesterol, vitamins and minerals), tors, fundamental molecular work, the immune status of not only for growth and survival, but also for optimal shrimp species, among others. innate immune response and normal pigmentation. References Is it possible to close the life cycle of C. crangon in Abbot OJ (1977) Black necrosis in brown shrimp, Crangon cran- captivity? gon. In: Nelson-Smith A, Bridges EM (eds). Problems of a An essential requisite for domestication is the ability to Small Estuary. Proceedings of the Symposium on the Burry bring the reared offspring to maturity and successful Inlet (South Wales) held at the University College of Swansea, spawning, to guaranty the supply of stock and the possibil- pp. 10. Quadrant Press Ltd, Swansea. ity to improve strains through selective breeding. Under Abdussamad EM, Thampy DM (1994) Cannibalism in the tiger culture conditions with constant water temperature of shrimp Penaeus monodon Fabricius in nursery rearing phase. 9 – 14°C and a salinity of 30 ppt, Meixner (1969) observed that Journal of Aquaculture in the Tropics :67 75. male and female C. crangon attained maturity after Agnalt A-L, Grefsrud ES, Farest E, Larsen M, Keulder F (2013) 10 months of rearing, with several consecutive successful Deformities in larvae and juvenile European lobster (Homarus gammarus) exposed to lower pH at different temperatures. spawns in the following months (Table 1). He also stated Biogeosciences 10: 7579–7615. that as the rearing of the shrimps was carried out at a con- Almut G, Bamber S (2013) Behaviourial responses of Crangon stant water temperature of 14°C, the period at maturation crangon (Crustacea, Decopoda) to reduced seawater pH fol- could be 5–6 months at 18–20°C, which is consistent with lowing simulated leakage from sub-sea geological storage. the growth rate calculated by Hufnagl and Temming Journal of Environmental Protection 4:61–67. (2011). Amjad S, Jones D, Chitracedivelu K (1992) Advances in pen- aeid larval feed technology. In: Cheah S, Thalathiah H Is there a market for cultured C. crangon? (eds) Proceedings of Seminar on New Technology in Aqua- culture, pp. 29–45. Malaysian Fishery Society, Serdang, So far, little attention has been given to improve the Malaysia. breeding techniques for this species, despite its high com- Arnold KE, Findlay HS, Spicer JI, Daniels CL, Boothroyd D mercial value. The main reasons for this are the year (2009) Effect of CO2-related acidification on aspects of the round availability of C. crangon, which occurs in great larval development of the European lobster, Homarus gamma- abundances in some seasons. Recently, however, there is rus (L.). Biogeosciences 6: 1747–1754. a growing market in Europe for live C. crangon, which Attramadal KJK, Salvesen I, Xue R, Øie G, Strøseth Vadstein O, increases the product diversity and subsequently the culi- Olsen Y (2012) Recirculation as a possible microbial control nary possibilities. Because the catch and grading with strategy in the production of marine larvae. Aquacultural drum sieves is detrimental for the survival of the shrimp Engineering 46:27–39. € (Neudecker et al. 2006), big size live shrimp are collected Aviat D, Diamantis C, Neudecker T, Berkenhagen J, Muller M manually, usually at the last trawl and stored in livestock (2011) The North Sea Brown Shrimp Fisheries. Study tanks on board. Live specimens are marketed up to 30% requested by the European Parliament’s Committee on Fish- more than their freshly cooked counterparts, e.g. eries. 106 pp. http://www.europarl.europa.eu/studies

Reviews in Aquaculture (2014) 6, 1–21 © 2014 Wiley Publishing Asia Pty Ltd 15 D. Delbare et al.

Avnimelech Y (2006) Bio-filters: the need for a new comprehen- cadian light-dark cycles. Journal of Experimental Marine Biol- sive approach. Aquaculture Engineering 34: 172–178. ogy and Ecology 47: 101–112. Ayres PA, Edwards E (1982) Notes on the distribution of ‘Black Davidson J, Frankel AS, Ellison WT, Summerfelt S, Popper AN, Spot’ shell disease in crustacean fisheries. Chemistry in Ecology Mazik P et al. (2007) Minimizing noise in fiberglass aquacul- 1: 125–130. ture tanks: noise reduction potential of various retrofits. Azevedo C (2001) Ultrastructural aspects of a new species, Vav- Aquacultural Engineering 37: 125–131. raia mediterranica (Microsporidia, Pleistophoridae), parasite Derks P (1980) Kwantitatieve bepaling van de dagelijkse voeds- of the French mediterranean shrimp, Crangon crangon (Crus- elopname van garnalen, Crangon crangon (L.), volgens het tacea, Decapoda). Journal of Invertebrate Pathology 78: 194– Bajkov-principe met een schatting van de jaarlijkse consump- 200. tie en produktie van de populatie op het Balgzand, een droog- Balss H (1931) Uber die Chemorezeption bei Garnelen. Biolo- vallend getijdengebied, en enige gegevens omtrent het gisches Zentralblatt 33: 508–511. voedselzoeken en de voedselsamenstelling. Nederlands Insti- Bart AN, Clark J, Young J, Zohar Y (2001) Underwater ambient tuut voor Onderzoek der Zee Internal Report (unpublished), noise measurements in aquaculture systems: a survey. Aqua- 1–31. culture Engineering 25:99–110. Domingues P, Poirier R, Dickel L, Almansa E, Sykes A, Andrade Bartholomay LC, Loy DS, Loy JD, Hariis DLH (2012) Nucleic- JP (2003) Effects of culture density and live prey on the acid based antivirals: augmentating RNA interference to “vac- growth and survival of juvenile cuttlefish, Sepia officinalis. cinate” Litopenaeus vannamei. Journal of Invertebrate Pathol- Aquaculture International 11: 225–242. ogy 110: 261–266. Dyrynda EA (1998) Shell disease in the common shrimp Cran- Boddeke R, Driessen G, Doesburg W, Ramaekers G (1986) Food gon crangon: variations within an enclosed estuarine system. availability and predator presence in a coastal nursery area of Marine Biology 132: 445–452. the brown shrimp (Crangon crangon). Ophelia: International Edwards RRC (1978) Effects of water soluble oil fractions on Journal of Marine Biology 26:77–90. metabolism, growth and carbon budget in the shrimp Cran- Broekaert K, Heyndrickx M, Hoffman S, Devlieghere F, Her- gon crangon. Marine Biology 46: 259–265. man L, Vlaemynck G (2011) The microbiota of common Ehrenbaum E (1890) Zur Naturgeschichte von Crangon vulgaris shrimps (Crangon crangon) from catch to consumer. In: Fabr. Berlin, Dtsch. Seefisch.- Verein, Mittl. Sekt. Kusten-€ Ho- Mees J, Seys J (eds) Book of Abstracts VLIZ Young Scien- chseefisch., Sonderbeilage: 9–124. tists’ Day, Brugge, Belgium, 25 February 2011, pp. 16. Evans S (1984) Energy budgets and predation impact of domi- VLIZ Special Publication 48. Vlaams Instituut voor de Zee nant epibenthic carnivores on a shallow soft bottom commu- (VLIZ), Oostende, Belgium. nity at the Swedish west coast. Estuarine, Coastal and Shelf Calado R, Pimentel T, Vitorino A, Dionısio G, Dinis MT (2008) Science 18: 651–672. Technical improvements of a rearing system for the culture of FAO (2013) Fisheries and Aquaculture Department. Species Fact decapod crustacean larvae, with emphasis on marine orna- Sheets: Crangon crangon. http://www.fao.org/fishery/species/ mental species. Aquaculture 285: 264–269. 3435/en Campos J, van der Veer HW (2008) Autecology of Crangon Feller RJ (2006) Weak meiofaunal trophic linkages in Crangon crangon (L.) with an emphasis on latitudinal trends. Oceanog- crangon and Carcinus maenas. Journal of Experimental Marine raphy and Marine Biology: An Annual Review 46:65–104. Biology and Ecology 330: 274–283. Chin T-S, Chen J-C (1987) Acute toxicity of ammonia to larvae de Figueiredo MJ, Vilela MH (1972) On the artificial culture of of the tiger prawn, Penaeus monodon. Aquaculture 66(3–4): Nephrops norvegicus reared from the egg. Aquaculture 1: 173– 247–253. 180. Cieluch U, Charmantier G, Grousset E, Charmantier-Daures M, Figueiredo J, Lin J, Anto J, Narciso L (2012) The consump- Anger K (2004) Osmoregulation, immunolocalization of Na+/ tion of DHA during embryogenesis as an indicative of the K+-ATPase, and ultrastructure of branchial epithelia in the need to supply DHA during early larval development: a developing brown shrimp, Crangon crangon (Decapoda, Cari- review. Journal for Aquaculture Research & Development 3: dea). Physiological and Biochemical Zoology 78 (6): 1017–1025. 140. Costlow JD, Bookout CG (1971) The Effect of Cyclic Temperature Fittschen UEA (2001) Identifizierung von Naturstoffprofilen aus on Larval Development in the Mud Crab Rhithropanopeus har- der Nordseekrabbe Crangon crangon. Dissertation zur Erlan- risii. In: Crisp DJ (ed.) Proceedings of the 4th European Marine gung des Doktorgrades des Fachbereichs Chemie der Univer- Biology Symposium 1971, pp. 211–220.Cambridge University sit€at Hamburg, 229 pp. Press, Cambridge. Forster JRM (1970) Further studies on the culture of the prawn Criales MM, Anger K (1986) Experimental studies on the larval Palaemon serratus Pennant, with emphasis on the post-larval development of shrimps Crangon crangon and C. allmanni. stages. Ministry of Agriculture. Fisheries and Food, Fishery Helgol€ander Meeresuntersuchungen 40: 241–265. Investigation Series II, 26 (6): 1–39. Dalley R (1980) The survival and development of the shrimp Galgani M, Aquacop (1988) Essais de substitution des algues Crangon crangon (L.), reared in the laboratory under non-cir- vivantes par des microparticules inertes pour l’alimentation

Reviews in Aquaculture (2014) 6, 1–21 16 © 2014 Wiley Publishing Asia Pty Ltd Rearing techniques for Crangon crangon

des larves zoeades crevettes peneides. Aquaculture 69: 115– tory at University College, Liverpool. Report on the Lanca- 127. shire Sea-fisheries Laboratory at the University of Liverpool, Gallardo PP, Pedrozo-Islas R, Garcia-Galano T, Pascual C, Rosas and the Sea-fish hatchery at Piel: 1–48. C, Sanchez A et al. (2002) Replacement of live food with a Hoa ND (2009) Domestication of black tiger shrimp (Peneaus microbound diet in feeding Litopenaeus setiferus (Burken- monodon) in recirculation systems in Vietnam. PhD thesis, road) larvae. Aquaculture Research 33: 681–691. Ghent University, Belgium. 186 pp. Gelin A, Crivelli AJ, Rosecchi E, Kerambrun P (2001) Can Holme M-H (2008) Towards development of a formulated diet salinity changes affect reproductive success in the brown for mud crab (Scylla serrate) larvae, with emphasis on lipid shrimp Crangon crangon. Journal of Crustacean Biology 21 nutrition. Thesis for the Doctor of Philosophy in the School (4): 905–911. of Marine & Tropical Biology, James Cook University. Gerlach SA, Schrage M (1969) Free-living nematods as food of Hostens K, Mees J (2003) The diet of brown shrimp Crangon the sand shrimp, Crangon crangon. Experiments on the role of crangon (L.) in the Westerschelde Estuary (Chapter 8). In: meiofauna as food of the marine macrobenthos. Oecologia 2: Hostens K, (ed.) The demersal fish and macro-invertebrate 362–375. assemblages of the Westerschelde and Oosterschelde estuaries Getchell RG (1989) Bacterial shell disease in crustaceans: a (Southern Bight of the North Sea). PhD Thesis, Ghent Uni- review. Journal of Shellfish Research 8:1–6. versity: 141–156. Gibson RN, Yin MC, Robb L (1995) The behavioural basis of Hufnagl M (2009) Population dynamics and lifecycle of the predator-prey size relationships between shrimp (Crangon brown shrimp Crangon crangon (Caridea, L. 1758). Experi- Crangon) and juvenile plaice (Pleuronectes Platessa). Journal of mental, biochemical and theoretical aspects. Dissertation zur the Marine Biological Association of the United Kingdom 75: Erlangung des Doktorgrades beim Department fur€ Biologie 337–349. der Fakult€at fur€ Mathematik, Informatik und Naturwissens- Gilis C (1952) La p^eche crevettiere sur la cote^ belge: son evolu- chaften der Universit€at Hamburg: 205 pp. tion au cours des annees 1935–1951 et son influence sur le Hufnagl M, Temming A (2011) Growth rates of Crangon cran- stock de la crevette. Memoires de l’Instut d’Etudes Maritimes gon. II. Meta-analysis and growth modelling? Marine Ecology d’Ostende 8:1–55. Progress Series 435: 155–172. Greve W (1968) The “planktonkreisel”, a new device for cultur- Hufnagl M, Temming A, D€anhardt A, Perger R (2010) Is Cran- ing zooplankton. Marine Biology 1: 201–203. gon crangon (L. 1758, Decapoda, Caridea) food limited in the Gunnarsson B, Asgeirsson P, Ingolfsson A (2007) The rapid col- Wadden Sea? Journal of Sea Research 64: 386–400. onization by Crangon crangon (Linnaeus, 1758) (Eucarida, ICES (2013) Report of the Working Group on Crangon fisheries Caridea, Crangonidae) of Icelandic coastal waters. Crustace- and life history (WGCRAN), 3-7 June 2013, ICES HQ, ana 80 (6): 747–753. Copenhagen, Denmark, ICES CM2013/SSGEF:12, 25 pp. Hagerman L (1970) The oxygen consumption of Crangon vulga- Immanuel G, Menethira V, Beena S, Palavesam A (2003) Influ- ris (Fabricius) (Crustacea, Natantia) in relation to salinity. ence of dietary lipid on survival, growth and moulting strate- Ophelia 7: 283–292. gies of Penaeus indicus (Milne Edwards) postlarvae. Journal of Hagerman L, Szaniawska A (1986) Behaviour, tolerance and Aquaculture in the Tropics 18:45–60. anaerobic metabolism under hypoxia in the brackish-water Jayasankar P, Muthu MS (1983) Toxicity of nitrite to the larvae shrimp Crangon crangon. Marine Ecology Progress Series 34: of Penaeus indicus H. Milne Edwards. Indian Journal of Fisher- 125–132. ies 30: 231–240. Hamner WM (1990) Design developments in the planktonkrei- Jones A (1972) Marine fish farming: An examination of the fac- sel, a plankton aquarium for ships at sea. Journal of Plankton tors to be considered in the choice of species. Laboratory leaf- Research 12 (2): 397–402. let N° 24, Fisheries Laboratory Lowstoft: 16 pp. Harrison KE (1990) The role of nutrition in maturation, repro- Jones DA, Kurmaly K (1987) Feeding and assimilation of Fri- duction and embryonic development of decapod crustaceans: ppak and other feeds by crustacean larvae. Journal of the a review. Journal of Shellfish Research 9:1–28. World Aquaculture Society 18: 17A. Hauton C (2012) The scope of the crustacean immune system Jones DA, Kanazawa A, Ono K (1979) Studies on the nutritional for disease control. Journal of Invertebrate Pathology 110: 251– requirements of the larval stage of Penaeus japonicus using mi- 260. croencapsulated diets. Marine Biology 54: 261–267. Havinga B (1930) Der Granat (Crangon vulgaris Fabr.) in den Jones DA, Kurmaly K, Aeshad A (1987) Penaeid shrimp holl€andischen Gew€assern. Journal du Conseil/Conseil Perma- hatchery trials using microencapsulated diets. Aquaculture nent International pour l’Exploration de la Mer 5:57–87. 64: 133–146. Henneguy LF, Thelohan P (1892) Myxosporidies parasites des Jones DA, Amjad S, Chitravadicelu K (1989) Comparison of muscles chez quelques Crustaces decapodes. Annales de artificial feeds used in penaeid shrimp hatcheries. In: al-Iskan- Micrographie 4: 617–641. darıyah J, al-Ziraah K (eds) Proceedings of the Third Egyptian- Herdman WA (1892) Report on the investigations carried on in British Conference on Animal, Fish and Poultry Production, pp. 1892 in connection with the Lancashire sea-fisheries labora- 15–20. Alexandria University, Alexandria, Egypt.

Reviews in Aquaculture (2014) 6, 1–21 © 2014 Wiley Publishing Asia Pty Ltd 17 D. Delbare et al.

Kanazawa A (1985) Essential fatty acid and lipid requirement of Lagardere JP (1982) Effects of noise on growth and reproduction fish. In: Cowey CB, Mackie AM, Bell JG (eds) Nutrition and of Crangon crangon in rearing tanks. Marine Biology 71 (2): Feeding in Fish, pp. 281–298. Academic Press, London and 177–185. New York. Lagardere JP, Regnault MR (1980) Influence du niveau sonore Kanazawa A (1990) Protein requirements of penaeid shrimp. de bruit ambient sur le metabolism de Crangon crangon Advance in Tropical Aquaculture, Actes de Colloques 9, IFR- (Decapoda: Natantia) en elevage. Marine Biology 57: 157–164. EMER, Plouzane, France: 261–270. Lagardere JP, Sperandio M (1981) Influence du niveau sonore Kanazawa A, Teshima S, Sasada H, Abdel-Raham S (1982) Cul- de bruit ambiant sur la croissance de la crevette Crangon cran- ture of prawn larvae with microparticulate diets. Bulletin of gon (Limne, 1758). Resultats preliminaires. Aquaculture 24: the Japan Society of Fisheries 48: 195–199. 77–90. Kanazawa A, Teshima S, Sakamoto M (1985) Effects of dietary Le Vay L, Rodriguez A, Mourente G, Jones DA (1993) Influence lipids, fatty acids and phospholipids on the growth and survival of the Diet on Digestive Activity and Growth of Penaeus Japoni- of prawn (Penaeus japonicus)larvae.Aquaculture 50:39–49. cus Larvae - Implications for Nutritional Studies. European Kattner G, Wehrtmann IS, Merck T (1994) Interannual varia- Aquaculture Society, Oostende, Belgium. tions of lipids and fatty acids during larval development of van Lissa JHL (1977) Aantallen, voedselopname, groei en prod- Crangon spp. In the German Bight, North Sea. Comparative uktie van de garnaal (Crangon crangon L.) in een getijdenge- Biochemistry and Physiology 107B (1): 103–110. bied, alsmede de voedselopname en groei onder Knust R (1990) The black spot disease in Crangon crangon (L.) laboratoriumomstandigheden. Interne Verslagen Nederlands of the German Bight. ICES Paper C.M.1990/E:32 Ref.K Mar- Instituut voor Onderzoek der Zee 10:1–100. ine Environmental Qualtity Committee: 11 pp. Lloyd A, Yonge CM (1947) The biology of Crangon crangon L. Kuhl€ H (1956) Untersuchung der Nahrung von jungen Seehasen in the Bristol channel and severn estuary. Journal of the (Cyclopterus lumpus L.) im Mundungsgebiet€ der Elbe. Archiv Marine Biological Association of the United Kingdom 26: fur€ Fischereiwissenschaft 7 (1): 40–47. 626–661. Kuhl€ H (1961) Nahrungsuntersuchungen an einigen Fischen im Maazouzi C, Massona G, Izquierdo MS, Pihan J-C (2007) Fatty Elbe-Mundungsgebiet.€ Berichte der deutschen wissenschaftli- acid composition of the amphipod Dikerogammarus villosus: chen Kommission fur€ Meeresforschung 16 (2): 90–104. feeding strategies and trophic links. Comparative Biochemistry Kuhl€ H (1963a) Uber€ die Nahrung der Scharbe (Limanda liman- and Physiology Part A: Molecular & Integrative Physiology 147 da L.). Archiv fur€ Fischereiwissenschaft 14 (½): 8–17. (4): 868–875. Kuhl€ H (1963b) Das Vorkommen von Garnelenlarven (Crangon Marchand J (1981) Observations sur l’ecologie de Crangon cran- crangon L.) in der Elbemundung€ . Archiv fur€ Fischereiwissens- gon (Linne) et Palaemon longirostris (H. Milne Edward) chaft 14 (½): 1–7. (Crustacea, Decapoda, Natantia). Estuaire interne de la Loire Kuhl€ H (1964a) Protokolle zu den Nahrungsuntersuchungen an (France). Vie et Milieu 31:83–92. einigen Fischen der Elbmundung.€ Ver€offentlichungen des In- Meixner R (1965) Eine Methode zur Aufzucht von Crangon stut fur€ Kusten-€ und Binnenfischerei 32:1–30. crangon (L.) (Crust. Decap. Natantia). Archiv fur€ Fischereiwis- Kuhl€ H (1964b) Protokolle zu den Nahrungsuntersuchungen an senschaft 17 (1): 1–4. Scharben (Limanda limanda L). Ver€offentlichungen des Instut-. Meixner R (1966) The effects of food supply on moulting, fur€ Kusten-€ und Binnenfischerei 33:1–27. growth and spawning of the shrimp Crangon crangon (L.). Kuhn DD, Boardman GD, Lawrence AL, Marsh L, Flick GJ Jr International Council for the Exploration of the Sea, Shellfish (2009) Microbial floc meal as a replacement ingredient for Committee 5:1–7. fish meal and soybean protein in shrimp feed. Aquaculture Meixner R (1969) Wachstum, H€autung, und Fortpflanzung von 296:51–57. Crangon crangon (L.) bei Einzelaufzucht. Berichte der deuts- Kuipers BR, Dapper R (1984) Nursery function of Wadden Sea chen wissenschaftlichen Kommission fur€ Meeresforschung 20: tidal flats for the brown shrimp Crangon crangon. Marine 93–111. Ecology Progress Series 17: 171–181. Meyers TR, Koeneman TM, Botelho C, Short S (1987) Bitter Kumulu M, Jones DA (1995) The effect of live and artificial crab disease: a fatal dinoflagellate infection and marketing diets on growth, survival and trypsin activity in larvae of problem for Alaskan Tanner crabs Chionoecetes bairdi. Dis- Penaeus indicus. Journal of the World Aquaculture Society eases of Aquatic Organisms 3: 195–216. 26: 406–415. Moriarty DJW, Decamp O (2009) Strategies for disease preven- Kurmaly K, Jones DA, Yule AB, East J (1989) Comparative tion on shrimp farms. In: Browdy CL, Jory DE (eds) The Ris- analysis of the growth and survival of Penaeus monodon ing Tide, Proceedings of the special session on sustainable (Fabricus) larvae, from protcoea I to postlarvae I, on live shrimp farming, pp. 53–70. The World Aquaculture Society, feeds, artificial diets and on combinations of both. Aqua- Baton Rouge, LA. culture 81:27–45. Mourente G (1996) In vitro metabolism of C-14-polyunsatu- rated fatty acids in midgut gland and ovary celles from Penaeus kerathurus Forskal at the beginning of sexual mat-

Reviews in Aquaculture (2014) 6, 1–21 18 © 2014 Wiley Publishing Asia Pty Ltd Rearing techniques for Crangon crangon

uration. Comparative Biochemistry and Physiology 115B: of adult male Litopenaeus vannamei (Boone) in response to 255–266. culture temperature and food deprivation. Aquaculture Muller-Feuga A, Moal J, Kaas R (2003a) The microalgae of Research 34: 1205–1213. aquaculture. In: Støttrup JG, McEvoy LA (eds) Live Feeds in Perkins EJ (1967) Some aspects of the biology of Carcinus mae- Marine Aquaculture, pp. 253–299. Blackwell Publishing, nas (L). Transactions of the Dumfrieshire and Galloway Natu- Oxford. ral History and Antiquarian Society, 3th Series 4:46–56. Muller-Feuga A, Robert R, Cahu C, Robin J, Divernach P Pihl L, Rosenberg R (1984) Food selection and consumption of (2003b) Use of microalgae in aquaculture. In: Støttrup JG, the shrimp Crangon crangon in some shallow marine areas in McEvoy LA (eds) Live Feeds in Marine Aquaculture, pp. 253– western Sweden. Marine Ecology Progress Series 15: 159–168. 299. Blackwell Publishing, Oxford. Pinn RH, Ansell AD (1993) The effect of particle size on the Narciso L, Calado R (2001) Fatty acid profiles of some crusta- burying ability of the brown shrimp Crangon crangon. Journal cean eggs with commercial interest in Europe. In: Browdy CL, of the Marine Biological Association of the United Kingdom 73: Jory DE (eds) The New Wave. Proceedings of the special ses- 365–377. sion on sustainable shrimp farming, pp. 375. World Aquacul- Plagmann J (1939) Ern€ahrungsbiologie der Garnele (Crangon ture Society, Baton Rouge, Louisiana, USA. vulgaris Fabr.). Helgol€ander wissenschaftliche Meeresuntersuch- Natrah FMI, Bossier P, Sorgeloos P, Yusoff F, Defoirdt T (2013) ungen 2 (1): 113–162. Significance of microalgal-bacterial interactions for aquacul- Redant F (1978) Konsumptie en produktie van post-larvale ture. Reviews in Aquaculture 5:1–14. Crangon crangon (L.) (Crustacea, Decapoda) in de Belgische Naviner M, Berge JP, Durand P, Bris HL (1999) Antibacterial kustwateren, Vol. 2, pp. 444. PhD Thesis. Vrije Universiteit activity of the marine diatom Skeletonema costatum against Brussel, Brussel. aquacultural pathogens. Aquaculture 174:15–24. Regnault M (1976) Influence du substrat sur la mortaliteetla Neudecker T, Damm U, Kuhnhold€ W (2006) Fang, anlandun- croissance de la crevette Crangon crangon (L.) en elevage. gen, discard und bestand der Nordseegarnelen (Crangon cran- Cahiers de Biologie Marine Tome XVII: 347–357. gon L.). Information aus der Fishereiforschung 53:82–85. Regnault M (1981) Respiration and ammonia excretion of the del Norte-Campos AGC, Temming A (1994) Feeding and activ- shrimp Crangon crangon L.: metabolic response to prolonged ity in gobies and brown shrimp. Marine Ecology Progress Series starvation. Journal of Comparative Physiology 141B: 549–555. 115:41–53. Regnault M, Lagardere J-P (1983) Effects of ambient noise on Nouvel L (1939) Observation de l’accouplement chez une espece the metabolic level of Crangon crangon (Decapoda, Natantia). de crevette Crangon crangon. Comptes Rendus Hebdomadaires Marine Ecology Progress Series 11:71–78. des Seances de l’Academie des Sciences (Paris) 209: 639–641. Regnault M, Luquet P (1974) Besoins en proteines de la crevette Øiestad V (1998) Shallow raceway as a solution to compact grise Crangon crangon L. au cours de sa vroissance. Annales de resource-maximizing farming procedure for marine fish spe- la Nutrition et de l’Alimentation 28:6. cies. ICES C.M. 1998/L:2, 11 pp. Regnault M, Campillo A, Luquet P (1975) Croissance des cre- Paibulkichakul C, Piyatiratitivorakul S, Kittakoop P, Viyakarn vettes Crangon crangon et Palaemon serratus soumises a un V, Fast A, Menasveta P (1998) Optimal density level of leci- regime artificiel: influence du mode de presentation et du thin and cholesterol for black tiger Penaeus monodon larvae mode de sechage de l’aliment. Cahiers de Biologie Marine and postlarvae. Aquaculture 176: 273–281. Tome XVI:1–20. Pandian TJ (1967) Changes in chemical composition and caloric Rieger PW, Summerfelt RC (1997) The influence of turbidity on content of developing eggs of the shrimp Crangon crangon. larval walleye, Stizostedium vitreum, behavior and develop- Helgol€ander wissenschaftliche Meeresuntersuchungen 16 (3): ment in tank culture. Aquaculture 159:19–32. 216–224. Robinson CB, Samocha TM, Fox JM, Gandy RL, McKee DA Pardi L, Papi F (1961) Kinetic and tactic responses. In: Water- (2005) The use of inert artificial commercial food sources as man T (ed.) The Physiology of Crustacea, pp. 365–399. Aca- replacements of traditional live food items in the culture of demic Press, New York. larval shrimp, Farfantepenaeus aztecus. Aquaculture 245: 135– Paschke KA, Gebauer P, Buchholz F, Anger K (2004) Seasonal 147. variation in starvation resistance of early larval North Sea Samocha TM, Matsumoto T, Jones ER, Torano M (1999) Use of shrimp Crangon crangon (Decapoda: Crangonidae). Marine inert artificial commercial food sources as replacements of Ecology Progress Series 279: 183–191. traditional live food items in the culture of larval shrimp, Far- Pedroza-Islas R, Gallardo P, Vernon-Carter EJ, Garcia-Galano T, fantepenaeus aztecus. Aquaculture 245: 135–147. Rosas C, Pascual C et al. (2004) Growth, survival, quality and Sandifer PA, Smith TIJ (1975) Effect of population density on digestive enzyme activities of larval shrimp fed microencapsu- growth and survival of Macrobrachium rosenbergii reared in lated, mixed and live diets. Aquaculture Nutrition 10: 167– recirculating water management systems. Proceedings of the 173. World Mariculture Society 6:43–54. Perez-Velazquez M, Gonzalez-Felix ML, Lawrence AL, Gatlin Sartoris SJ, Portner€ HO (1997) Temperature dependence of the DM (2003) Changes in lipid class and fatty acid composition ionic and acid-base regulation in boreal and arctic Crangon

Reviews in Aquaculture (2014) 6, 1–21 © 2014 Wiley Publishing Asia Pty Ltd 19 D. Delbare et al.

crangon and Pandalus borealis. Journal of Experimental Marine Crangon septemspinosa preying on juvenile winter flounder Biology and Ecology 211:69–83. Pseudopleuronectes americanus. Marine Ecology Progress Series Sharawy ZZ (2012) Investigations into growth and nutritional 263: 217–234. condition of Crangon crangon (L). Dissertation zur Erlan- Taylor DM, Khan RA (1995) Observations on the occurrence of gung des Doktorgrades beim Department fur€ Biologie der Hematodinium sp. (Dinoflagellata, Syndinidae), the causative Fakult€at fur€ Mathematik, Informatik und Naturwissenschaf- agent of bitter crab disease in Newfoundland snow crab (Chin- ten der Universit€at Hamburg: 176 pp. oecetes opilio). Journal of Invertebrate Pathology 65: 283–288. Shelton RGJ, Shelton PMJ, Edwards AS (1975) Observations Tazaki K (1977) Nervous responses from mechanosensory with the scanning electron microscope on a filamentous bac- hairs on the antennal flagellum in the lobster, Homarus terium present on the aesthetasc setae of the brown shrimp gammarus (L.). Marine and Freshwater Behaviour and Phys- Crangon crangon (L.). Journal of the Marine Biological Associa- iology 5:1–18. tion of the United Kingdom 55: 795–800. Thorson G (1946) Reproduction and larval development of Spaargaren DH (2000) Seasonal and annual variations in the Danish marine bottom invertebrates, with special reference to catches of Crangon crangon (L., 1758) (Decapoda, Natantia) the planktonic larvae in the Sound (Øresund). Meddelelser fra near the coast of Texel, the Netherlands. Crustaceana 73: 547– Kommissionen for Danmarks Fiskeri og Havunders (Plankton) 563. 4 (1): 1–523. Spotte S (1979) Seawater Aquariums - The Captive Environment. Tidwell J, Coyle S (2008) Impact of substrate physical character- A Wiley-Interscience Publication, John Wiley & Sons, New istics on grow out of Macrobrachium rosenbergii, in ponds and York. pond microcosm tanks. Journal of the World Aquaculture Soci- Sprague V, Couch JA (1971) An annotated list of protozoan par- ety 39 (3): 406–413. asites, hyper-parasites and commensals of decapod Crustacea. Tiews K (1954) Die biologischen Grundlagen der Busmer€ Garne- Journal of Parasitology 18: 526–573. lenfischerei. Berichte der deutschen wissenschaftlichen Kommis- Stentiford GD, Feist SW (2005) A histopathological survey of sion fur€ Meeresforschung 13 (3): 235–269. shore crab (Carcinus maenas) and brown shrimp (Crangon Tiews K (1965) Lichtung des Nordseegarnelenbestandes (Cran- crangon) from six estuaries in the United Kingdom. Jounal of gon crangon L.) durch Wegfrass. Archiv fur€ Fischereiwissens- Invertebrate Pathology 88: 136–146. chaft 16 (2): 169–181. Stentiford GD, Bateman K, Feist SW (2004) Pathology and Tiews K (1970) Synopsis of biological data on the common ultrastructure of an intranuclear bacilliform virus (IBV) shrimp Crangon crangon (Linaeus, 1758). FAO Fisheries infecting brown shrimp Crangon crangon (Decapoda: Crang- Reports 4: 1167–1223. onidae). Diseases of Aquatic Organisms 58:89–97. PubMed Tsai S-J, Chen J-C (2002) Acute toxicity of nitrate on Penaeus Abstract. monodon juveniles at different salinity levels. Aquaculture 213 Stentiford GD, Bonami JR, Alday-Sanz V (2009) A critical (1–4): 163–170. review of susceptibility of crustaceans to Tauro syndrome, yel- Uhlig N (2002) Wachstum und ern€arhrungssituation der Nord- lowhead disease and white spot disease and implications of seegarnele Crangon crangon (L.). Diploma thesis: Institute for inclusion of these diseases in European legislation. Aquacul- Hydrobiology and fishery science, University of Hamburg, ture 291:1–17. 114 pp. Stentiford GD, Bateman KS, Small HJ, Pond M, Ungfors A Urzua A, Anger K (2013) Seasonal variations in larval biomass (2012a) Hematodinium sp. and its bacteria-like endosymbiont and biochemical composition of brown shrimp, Crangon in European brown shrimp (Crangon crangon). Aquatic Bio- crangon (Decapoda, Caridea), at hatching. Helgol€ander Marine systems 8 (24): 10. Research 67: 267–277. Stentiford GD, Neil DM, Peeler EJ, Shields JD, Small HJ, Flegel Van der Veer HW, Bergman MJN (1987) Predation by crusta- TW et al. (2012b) Disease will limit future food supply from ceans on newly settled 0-group plaice Pleuronectes platessa the global crustacean fishery and aquaculture sectors. Jounal populations in the western Wadden Sea. Marine Ecology Pro- of Invertebrate Pathology 110: 141–157. gress Series 35: 203–215. Stevens CJ, Deibel D, Parrish CC (2004) Incormporation of bac- van der Meeren T, Mangor-Jensen A, Pickova J (2007) The effect terial fatty acids and changes in wax ester-based omnivory of green water and light intensity on survival, growth and index during a long-term incubation experiment with Cal- lipid composition in Atlantic cod (Gadus morhua) during anus glacialis Jaschnov. Journal of Experimental Marine Biology intensive larval rearing. Aquaculture 265: 206–217. and Ecology 303: 135–156. Van Donck E, De Wilde AWJ (1981) Oxygen consumption and Tacon AGJ (1987) The nutrition and feeding of farmed fish and motile activity of the brown shrimp Crangon crangon related shrimp - a training manual. 1 The essential nutrients. Project to temperature and body size. Netherlands Journal of Sea GCP/RLA/075/ITA, FAO Field Document 2/E, Brasilia, Brazil: Research 15 (1): 54–64. 117 pp. Van Wijk PM (1999) Farming Marine Shrimp in Freshwater Sys- Taylor DL, Collie JS (2003) Effect of temperature on the func- tems: An Economic Development Strategy for Florida: Final tional response and foraging behavior of the sand shrimp Report. Harbor Branch Oceanographic Institution, Florida.

Reviews in Aquaculture (2014) 6, 1–21 20 © 2014 Wiley Publishing Asia Pty Ltd Rearing techniques for Crangon crangon

Vervoort D, Redant F, Declerck D (1980) Causes and incidence Wouters R, Fegan DF (2004) Shrimp broodstock nutrition: a of ‘black spot disease’ on brown shrimp (Crangon crangon). review. Global Aqculture Advocate 6:36–38. ICES (Committee Meeting Paper Report) K 34:1–14. Wouters R, Van Horenbeeck T (2003) Larval shrimp feeds: cur- Villamar D, Brusca G (1987) Survival and growth of Crangon rent status. In: Jory Darryl E (ed.) Responsible Aquaculture for nigricauda larvae (Decapoda, Caridea) raised on experimental a Secure Future: Proceedings of a Special Session on Shrimp diets. Journal of World Aquaculture Society 18:11–25. Farming, World Aquaculture 2003, pp. 90–190. The World Vismann B (1996) Sulfide species and total sulfide toxicity in the Aquaculture Society, Baton Rouge, Louisiana, USA. shrimp Crangon crangon. Journal of Experimental Marine Biol- Wouters R, Vanhauwaert A, Naessens E, Pedrazzoli A, Lavens P ogy and Ecology 204 (1&2): 141–154. (1997) The effect of dietary n-3 HUFA and 22:6n-3/20:5n-3 Vogan CL, Costa-Ramos C, Rowley AF (2002) Shell disease syn- ratio of white shrimp larvae and postlarvae. Aquaculture Inter- drome in the edible crab, Cancer pagurus – isolation, charac- national 5: 113–126. terizationand pathogenicity of chitinolytic bacteria. Wouters R, Zambrano B, Espin M, Calderon J, Lavens P, Sorge- Microbiology 148: 743–754. loos P (2002) Experimental broodstock diets as partial fresh Wear RG (1974) Incubation in British decapod crustacea and food substitutes in white shrimp Litopeneaus vannamei B. the effects of temperature on the rate and success of embry- Aquaculture Nutrition 8: 249–256. onic development. Journal of the Marine Biological Association Xu W-J, Pan L-Q (2013) Dietary protein level and C/N ratio of the United Kingdom 54: 745–762. manipulation in zero-exchange culture of Litopenaeus vanna- Wehrtmann IS (1991) How important are starvation periods in mei: Evaluation of inorganic nitrogen control, biofloc compo- early larval development for survival of Crangon septemspin- sition and shrimp performance. Aquaculture Research 2013: osa? Marine Ecology Progress Series 73: 183–190. 1–10. Weitkamp DE, Katz M (1980) A review of dissolved gas super- Zhang B (2011) Influence of the Artificial Substrates on the saturation literature. Transactions of the American Fisheries Attachment Behavior of Littopenaeus vannamei in the Inten- Society 109: 659–702. sive Culture Condition. International Journal of Animal and Wickins JF, Lee DOC (2002) Crustacean Farming, Ranching and Veterinary Advances 3 (1): 37–43. Culture, 2nd edn. Blackwell Science, Oxford. Wilcox JR (1972) The feeding habit of the sand shrimp Cran- gon setemspinosa. Ph.D. thesis. Univ. Rode Island Library: 135 pp.

Reviews in Aquaculture (2014) 6, 1–21 © 2014 Wiley Publishing Asia Pty Ltd 21