(Paralithodes Platypus) with Improved Nutrition

AKCRRAB Draft Study Plan 2012

Increasing hatchery production of blue king crab (Paralithodes platypus) with improved nutrition

Ben Daly, Jim Swingle, Courtney Lyons, Ginny Eckert, Jeff Hetrick September 2011

ABSTRACT The Alaska King Crab Research Rehabilitation and Biology (AKCRRAB) program was formed in 2006 with the goal of investigating the feasibility of hatchery rearing of Alaskan king crab species for the purpose of population rehabilitation. Large-scale larval culture has been conducted at the Alutiiq Pride Shellfish Hatchery from 2007 to 2010 using red king crab (Paralithodes camtschaticus) and blue king crab (Paralithodes platypus). Culture of red king crab has been increasingly successful. Experiments in 2007 yielded survival to the first juvenile stage of less than 1%, however improvements in rearing techniques and hatchery infrastructure yielded survival to glaucothoe of over 50% in 2009 and 2010 producing over 100,000 first stage juveniles in both years. Hatchery production technology of blue king crab is behind that of red king crabs for a variety of reasons that include 1) broodstock acquisition is more logistically and financially difficult, and 2) blue king crab larvae in the hatchery experienced high rates of mortality from 2009 to 2011 using rearing conditions similar to those used successfully for red king crab. We are planning blue king crab larval rearing experiments in 2012 to improve survival through modifications of larval feeding and rearing conditions. Additionally, juvenile experiments will investigate effects of habitat and temperature on predation rates. Each year improvements in culture technology are made with the understanding that fine tuning larval and juvenile husbandry techniques are an ongoing process. This research will give further insight into the feasibility of mass culture of king crab in terms of methodology, crab survival, and costs incurred which are critical to assess the feasibility of rehabilitation.

INTRODUCTION Hatchery rearing has the potential to be an effective tool for rehabilitation of depleted stocks and for fishery management and is currently in progress for crab and lobster species in the US and worldwide (Secor 2002, Stevens 2006c). However, before implementation, research is needed to assess the feasibility, effectiveness, and possible consequences of a rehabilitation program (Leber 1999, 2002). The Alaska King Crab Research and Rehabilitation and Biology (AKCRRAB) Program was created in 2006 as a partnership between the University of Alaska Fairbanks, Alaska Sea Grant, the Alutiiq Pride Shellfish Hatchery (APSH), NOAA Fisheries, and several community-based groups to begin the necessary research to assess the feasibility of rehabilitation for king crabs in Alaska. Commercial harvest of Alaskan king crab was for decades active and lucrative. However, many stocks declined drastically over 20 years ago and have not rebounded, even in the absence of fishing. We propose to study the early life history of blue king crab to develop methods and determine feasibility of hatchery rearing. This study plan

1 addresses methods for culture of larvae in the Alutiiq Pride Shellfish Hatchery in Seward, Alaska.

The life histories of red king crab (Paralithodes camtschaticus) and blue king crab (Paralithodes platypus) are similar (Stevens et al., 2008), with differences that may be the result of the different habitats of the two species. Female red king crab reproduce annually and hold their fertilized eggs for 11 months, releasing them as zoeae over a period of 2-3 weeks between January and March, depending on environmental and physiological factors (Stevens and Swiney, 2007). In contrast, large-sized female blue king crab reproduce biannually and hold their fertilized eggs for approximately 14 months (Somerton and Macintosh, 1985: Jensen and Armstrong, 1989), releasing larvae over a period of 3-7 weeks between January and May (Stevens, 2006a, 2006b). Both species release planktotrophic larvae that molt through their four zoeal stages (Z1-Z4) lasting approximately 40 days, followed by a non-feeding glaucothoe (G) stage that lasts 30-40 days. Survival of red king crab larvae from Z1 to glaucothoe in the wild was estimated from plankton samples and ranged from 0.7% to 3% over four years (Shirley and Shirley, 1989a). The glaucothoe stage seeks structurally complex habitat and metamorphoses into a first-instar juvenile crab (C1) (Stevens and Kittaka, 1998; Stevens, 2003). Both species have a relatively long juvenile period and mature at approximately 5-7 years of age and recruit to the fishery at 7-9 years of age (Jensen and Armstrong, 1989; Stevens, 1990; Zhou et al., 1998; Loher at al., 2001; Stevens et al., 2008).

Laboratory culture of Paralithodes sp. to the C1 stage has been extensively investigated in Japan (Kurata, 1960; reviewed by Stevens, 2006d), Russia (Kovatcheva et al., 2006), and Alaska (Shirley and Shirley, 1989b; Persselin, 2006a; Stevens et al., 2008; Daly et al., 2009). Red king crab larvae are especially vulnerable to stress, and relatively high mortality has been observed throughout larval development, especially during molting (Stevens, 2006d; Kovatcheva et al., 2006). Although methods for large-scale rearing of king crab were developed several decades ago in Japan (Nakashani and Naryu, 1981), hatchery production was highly variable from year to year, and from 1982 to 1996, production of Hanasaki king crab (P. brevipes) ranged from 0 to 800,000 C1 per year, with an average survival of about 42% (Stevens 2006d). Survival to the C1 stage for red and blue king crab in small-scale culture experiments in Kodiak has also been highly variable (Persselin, 2006a, 2006b; Stevens et al., 2008). In an experiment that examined the effect of diet, temperature, and larval density, blue king crab larval survival to C1 varied from 27% to 91% dependent on treatment (Stevens et al., 2008).

Several other species of crab are cultured at the hatchery scale. Successful techniques for rearing larval crabs at the hatchery scale were developed 30 years ago for swimming crab (Portunus trituberculatus) in Japan, more recently for Chinese mitten crab (Eriocheir sinensis) in China (Zhang et al. 1998, Li et al. 2001), and blue crab (Callinectes sapidus) in Chesapeake Bay (Secor et al. 2002, Zmora et al. 2005). During four culturing cycles from February through September 2002, the hatchery in Chesapeake Bay produced 40,000 juvenile blue crabs, of which 25,000 were released in the wild (Zmora et al. 2005). Researchers working on blue crab have developed tagging techniques (Davis et al. 2004a), investigated fitness of hatchery-raised individuals (Davis et al. 2004b), and developed techniques for morphological conditioning to improve juvenile fitness (Davis et al. 2005a). Estimated survival to maturity of hatchery-raised blue crab released

2 into the wild was 5 to 20% during initial investigations, indicating that rehabilitation may be possible for this species (Davis et al. 2005b).

2007 - 2011 RESULTS Large-scale culturing techniques have been developed at the Alutiiq Pride Shellfish Hatchery for red king crab. Survival rates from Z1 to the glaucothoe stage have increased from 1% in 2007 to over 50% in 2009 and 2010 producing over 100,000 first stage juveniles in both years. This increase in survival and production is primarily due to improvements in rearing techniques and hatchery infrastructure. With the exception of 2008 experiments, in which survival to the C1 stage was 5% large-scale culture of blue king crab has been less successful. Access to broodstock is limited by the fact that many blue king crab fisheries are currently closed to fishing, and their remote location is logistically difficult to reach. Additionally, blue king crab larvae have experienced high rates of mortality from 2009 to 2011, proximally from increased sensitivity to bacterial infections such as Vibrio sp. and ultimately from poor condition larvae. Generally, filamentous bacteria is problematic but can be controlled by increasing rearing temperature and molting frequency to reduce the degree of shell infestation. However, Vibrio sp. infect the larvae internally and are much more problematic once present in a tank.

OBJECTIVES AND METHODS: Experiments in 2012 will focus on improving larval nutrition in an effort to improve larval condition and vulnerability to disease. Additionally, effects of habitat complexity and temperature on predation rates of juvenile survival may be explored.

Objectives include the following: • Improve larval health through diet • Determine effects of habitat and temperature on predation rates of juvenile survival

BROODSTOCK ACQUISITION We will collect 20 ovigerous female blue king crabs from St Matthews Island during the commercial fishery (pending permits, boat TBD). Crabs will be shipped to the Alutiiq Pride Shellfish Hatchery in Seward.

EXPERIMENT 1: LARVAL REARING: Improving larval nutrition

We propose refining rearing technology to improve larval health, reduce bacterial infections, and increase survival by improving larval diet. Previous hatchery-scale experiments with BKC conducted in 2009 and 2010 yielded poor survival to the glaucothoe stage (<10%). In both these years, high mortality occurred during the zoeal stages. In 2011, survival to glaucothoe was greater than 50%; however, catastrophic mortality occurred about one week into the glaucothoe stage resulting in <1% survival to the first juvenile stage. In all three years, swarming internal bacteria (presumably Vibrio sp.) were observed in dead and dying larvae and glaucothoe. In all three years, the larval diet consisted of DC DHA SELCO enriched Artemia, which has proven effective in larval rearing of RKC (survival to C1 of ~20%), it may not be adequate for BKC. During 2008, we achieved our best results to date with BKC (~50% survival to glaucothoe and 5% survival to C1) by feeding them a diet of enriched Artemia and Chaetoceros muelleri

3 microalgae As such, we plan to revisit the use of microalgae and other Artemia enrichments in larval rearing.

Hypothesis H10: There will be no difference in larval survival when microalgae is used as a dietary supplement. H1a: Survival is higher with microalgae.

H20: There will be no difference in larval survival when an alternate enrichment media is used as a dietary supplement. H2a: Survival is higher with an alternate enrichment media.

Experimental design Larvae will be collected from at least three females and mixed randomly. Larvae will be stocked at densities of 25 larvae L-1in twelve 190 L tanks at the Alutiiq Pride Shellfish Hatchery. Treatments will consist of Artemia enriched with DC DHA Selco, Artemia enriched with an alternate enrichment media (Spriulina or other TBD), and Artemia (enriched with DC DHA Selco) supplemented with either of two species of microalgae (see below). Chaetoceros muelleri and another species (TBD) of microalgae will be added to the standard Artemia diet daily at approximately 50,000 cells ml-1. These four treatments will be replicated four times. Water will be maintained at 8-10°C. Incoming water filtration will be flow through with particle filtration to 5 µm, a carbon filter, and an ultraviolet light sterilizer. Food will be retained and flushed on a daily cycle using 105 and 500 µm screens. Artemia will be fed at a density of 2 ml-1. This density falls into suggested feeding ranges based on daily feeding rates of P. camtschaticus in laboratory conditions (Epelbaum and Kovatcheva 2005). Feeding will be terminated when all zoeae in the tank molt to the glaucothoe stage.

EXPERIMENT 2: JUVENILE EXPERIMENTS: Effects of habitat complexity and temperature on groundfish predation of juvenile blue king crabs

Note: This experiment may be conducted in 2011 with juveniles cultured in 2011, if enough juveniles survive to the start of the experiment.

Increases in groundfish predation brought about by the mid-1970s climate regime shift are currently posited as one of the main drivers behind declines in numerous Bering Sea crab fisheries (e.g., Zheng and Kruse 2000, Zheng and Kruse 2006). However, groundfish abundance was not the only major ecological change brought about by the regime shift. Other changes tied to the regime shift include reorganization and decline in productivity of benthic communities (Grebmeier et al. 2006, Hunt et al. 2002), northward-shifts in the distribution of numerous species, and increases in trophic level, species diversity and total biomass in specific northern regions of the Bering Sea (Mueter and Litzow 2008, Conners et al. 2002).

As global climate change leads to further increases in ocean temperature, the Bering Sea ecosystem is likely to change even more. Predicted physical changes include increases in winds, storm intensity, salinity, stratification, pH, and abundance of suitable physical habitat, though the exact spatial and temporal scales of these changes are uncertain (Brander 2010, Hoegh-Guldberg

4 and Bruno 2010). Sub-arctic species will continue to extend northward, altering community structure and trophic interactions in the northern Bering Sea (Mueter and Litzow 2008). Ocean acidification will increase, harming numerous important arctic and sub-arctic species including: pteropods, foraminifers, cold-water corals, sea urchins, molluscs, and coralline alga (Fabry et al. 2009). Warmer air and water temperatures will also affect the winter sea ice extent. Annual sea ice melt creates the Bering Sea cold pool, an important oceanographic feature that marks the boundary between arctic and sub-arctic communities (Aydin and Mueter 2007). Hence, changes in the location and size of the cold pool will alter community composition (Mueter and Litzow 2008). Blue king crab prefer colder waters than redking crabs (Jensen and Armstrong 1989) and so are especially vulnerable to changes in the cold pool extent.

These predictions indicate that it is not sufficient to understand the current mechanisms behind the PIBKC decline. Successful long-term management requires the examination of how these mechanisms will change in response to climate forcing. We propose to investigate the potential of groundfish predation as a limit to PIBKC recovery by examining predation rates in response to different substrates and the presence of a crab competitor. I will then assess how increases in water temperature alter these relationships.

The objectives of this research project are: 1. To document groundfish predation rates on blue king crab and how they are affected by habitat complexity and the presence of competitor (red king crab; Paralithodes camtschaticus) 2.) To understand how increases in temperature alter these relationships.

Methods and Materials We will conduct a series of laboratory experiments on juvenile king crab at the Alaska Fisheries Science Center (NOAA/NMFS) Hatfield Marine Science Center in Newport, Oregon. Cultured juvenile crabs will be shipped to the facilities in Newport, Oregon just prior to the experiment. Pacific halibut (Hippoglossus stenolepis) used in predation trials will be drawn from supplies available at the Hatfield Marine Science Center laboratory. We will create microcosms consisting of sand or shell hash substrates with artificial seaweed (Fukui) added for structural complexity. Pairs of Pacific halibut will be added to the microcosms and allowed 10 days to acclimate before predation trials begin. Fish pairs will be fed to satiation 48 h before the experiment to standardize hunger levels and to insure that fish are uniformly motivated to feed. We will distribute ten juvenile blue king crabs over the middle half of each tank, allowing the crabs to settle into preferred microhabitats. After a one-hour acclimation period for the crabs, I will allow fish access to the entire tank. We will return the room lights to standard illumination over a period of around 60 s and begin video recording at this time. Trials will last approximately 60 min and be recorded for the entirety. Trapping fish under an acrylic column (28 cm diameter) will terminate trials. Afterward, we will determine survival rates, noting locations of remaining crabs. Surviving crabs will not be reused in subsequent trials.

We will repeat experiments at three different temperatures (3°C, 4°C, 5°C). The first temperature (3°C) is the lower limit for seawater temperature at the Newport facility. Based on average eastern Bering Sea benthic temperature data collected during summer trawl surveys from 1982-

5 2004, average benthic temperature was 2.5°C (s.d.=1.6;), so 3°C is representative of recent environmental conditions.

Data analysis We will review video recordings for the predation trials to assess time to first motion (after full light) and time to first strike on a crab for each fish. We will assess the following for each 5- minute block of time for each 60 min trial: general index of fish activity (summing the number of fish that actively move about the tank during each 5-min period; possible range=0 to 24) and the number of strikes on crabs. Strikes per target, crabs eaten per target, and crabs eaten per strike will be tabulated for each run. We will calculate differences in crab survival rates, predator performance (attack rates, attack success rates), and substrate use with contingency table analyses (for frequency data) or t-tests (for continuous data).

QUARANTINE PROCEDURES For each of the previously described hatchery experiments, quarantine precautions will include disinfection of transport containers with 100 ppm iodophore or 200 ppm bleach, control of aerosolization from the broodstock holding containers either by placement in a separate room or placing lids over the tanks, controlled access to the tanks either by separate room or visqueen barrier, use of disinfectant footbath in the controlled access corridor, use of separate utensils for the king crabs, and disinfection of the effluent with ozone and/or chlorine.

ADDITIONAL PROJECTS Mass culture of king crab larvae provides the opportunity to investigate other features of early life history with hatchery-produced larvae and juveniles. Larvae and juveniles for additional studies will be provided by the larval culture described here. Additional projects may include genetic analyses, behavioral experiments to determine fitness of hatchery-reared individuals, and studies of molting, growth and habitat selection. These projects will require that hatchery- produced individuals be sent to research labs of collaborators to include Ginny Eckert (UAF Juneau), Al Stoner (NOAA Newport), Pam Jensen (NOAA Seattle), David Tallmon (UAS Juneau), and Sherry Tamone (UAS Juneau). Transport permits will be requested as needed for these projects.

FUNDING Completion of this study plan will be dependent on the availability of funding.

LITERATURE CITED Aydin K, Mueter F, 2007. The Bering Sea- A dynamic food web perspective. Deep Sea Res Part II 54:2501-2525. Brander K, 2010. Impacts of climate change on fisheries. J Mar Syst 79:389-402. Conners ME, Hollowed AB, Brown E, 2002. Retrospective analysis of Bering Sea bottom trawl surveys: regime shift and ecosystem reorganization. Prog Oceanogr 55:209-222Daly, B., J.S. Swingle, G.L. Eckert. 2009. Effects of diet, stocking density, and substrate on survival and growth of hatchery-cultured red king crab (Paralithodes camtschaticus) juveniles in Alaska, USA. Aquaculture 293, 68-73. Daly, B., J.S. Swingle, G.L. Eckert. In prep. Astaxanthin and calcium as dietary supplements for hatchery-cultured red king crab (Paralithodes camtschaticus) juveniles. Aquaculture

6 Davis, J. L. D., A. C. Young-Williams, A. H. Hines, and O. Zmora. 2004a. Comparing two types of internal tags in juvenile blue crabs. Fisheries Research 67, 265-274. Davis, J.L.D., A.C. Young-Williams, R.Aguilar, B.L. Carswell, M.R. Goodison, A.H. Hines, M.A. Kramer, Y. Zohar, and O. Zmora. 2004b. Differences between hatchery-raised and wild blue crabs: Implications for stock enhancement potential. Transactions of the American Fisheries Society 133, 1-14. Davis, J. L. D., M. G. Eckert-Mills, A. C. Young-Williams, A. H. Hines, Y. Zohar. 2005a. Morphological conditioning of a hatchery-raised invertebrate, Callinectes sapidus, to improve field survivorship after release. Aquaculture 243, 147-158. Davis, J. L. D., A. C. Young-Williams, A. H. Hines, Y. Zohar. 2005b. Assessing the potential for stock enhancement in the case of the Chesapeake Bay blue crab (Callinectes sapidus). Canadian Journal of Fisheries and Aquatic Sciences 62, 109-122. Epelbaum, A.B., N.P. Kovatcheva. 2005. Daily food intakes and optimal food concentrations for red king crab (Paralithodes camtschaticus) larvae fed Artemia nauplii under laboratory conditions. Aquaculture Nutrition 11, 455-461. Grebmeier JM, Overland JE, Moore SE, Farley EV, Carmack EC, Cooper LW, Frey KE, Helle JH, McLaughlin FA, McNutt SL, 2006. A major ecosystem shift in the northern Bering Sea. Science 311:1461-1464. Hoegh-Guldberg O, Bruno JF, 2010. The impact of climate change on the world’s marine ecosystems. Science 328:1523-1528. Hunt GL, Stabeno P, Walters G, Sincllair E, Brodeur RD, Napp JM, Bond NA, 2002. Climate change and control of the southeastern Bering Sea pelagic ecosystem. Deep-Sea Res Part II 49:5821-5853. Jensen, G.C., D.A. Armstrong. 1989. Biennial reproductive cycle of blue king crab, Paralithodes platypus , at the Pribilof Islands, Alaska, and comparison to a congener, P. camtschatica. Can. J. Fish. Aquat. Sci. 46, 932-940. Kovatcheva, N., Epelbaum, A., Kalinin, A., Borisov, R., and Lebedev, R. 2006. Early Life History Stages of the Red King Crab Paralithodes camtschaticus (Tilesius, 1815) Biology and Culture. VINRO Publishing. Kurata, H. 1960. Studies on the larva and postlarva of Paralithodes camtschaticus. III. Effects of water temperature and salinity on larval survival and speed of development. Bulletin Hokkaido Reg. Fish. Res. Lab. 21, 9-14. Leber, K.M. 1999. Rationale for an experimental approach to stock enhancement. In: B.R. Howell, E. Moksness, and T. Svasand, (eds) Stock enhancement and sea ranching. p 63- 75. Oxford, UK, Fishing News Books, Blackwell Science Ltd. 606 pp. Leber, K.M. 2002. Advances in marine stock enhancement: shifting emphasis to theory and accountability. In: R. Stickney and J. McVey, (eds) Responsible Aquaculture, p 79-90. Abingdon, UK, CABI. Li, C., Li, S., Xing, Y., Hu, B., Zhao, S., and Wu, Z. 2001. Growth and survival variations and genotype-environment interaction analysis of two populations of pond cultured Chinese mitten crabs Eriocheir sinensis. Aquaculture: Book of Abstracts. p 372. Loher, T., Armstrong, D.A., Stevens, B.G. 2001 Growth of juvenile red king crab (Paralithodes camtschaticus) in Bristol Bay (Alaska) elucidated from field sampling and analysis of trawl survey data. Fish Bull 99, 572-587 Mueter FJ, Litzow MA, 2008. Sea ice retreat alters the biogeography of the Bering Sea continental shelf. Ecol App 18:309-320.

7 Nakanishi, T. and Naryu, M. 1981. Some Aspects of Large-Scale Rearing of Larvae and Post- Larvae of the King Crab (Paralithodes camtschaticus). Bull. Jap. Sea. Reg. Fish. Res Lab. 32, 39-47. Persselin, S. 2006a. Cultivation of king crab larvae at the Kodiak Fisheries Research Center, Kodiak, Alaska. pp 9-14. in B. G. Stevens, Ed. Alaskan Crab Stock Enhancement and Rehabilitation Workshop, Kodiak, AK, University of Alaska Sea Grant. Persselin, S. 2006b. Enriched Artemia nauplii as diet for red (Paralithodes camtschaticus) and blue (P. platypus) king crab larvae in the laboratory. J. Shell. Res. 25, 762. Secor, D. H., A. H. Hines, and A. R. Place. 2002. Japanese Hatchery-based Stock Enhancement: Lessons for the Chesapeake Bay Blue Crab. UM-SG-TS-2002-02, Maryland Sea Grant, College Park, MD. Sharp, W.C., Lellis, W.A., Butler, M.J., Herrnkind, W.F., Hunt, J.H., Pardee-Woodring, M., Matthews, T.R. 2000. The use of coded microwire tags in mark-recapture studies of juvenile Caribbean spiny lobsters, Panulirus argus. J. Crust. Biol. 20, 510-521. Shirley, S. M. and Shirley, T. C. 1989a. Interannual variability in density, timing, and survival of Alaskan red king crab Paralithodes camtschatica larvae. Mar. Ecol. Prog. Ser. 54, 51-59. Shirley, T. C. and Shirley, S. M. 1989b. Temperature and salinity tolerances of red king crab larvae. Mar. Behav. Physiol. 16, 19-30. Somerton, D. A., and R. A. MacIntosh. 1985. Reproductive biology of the female blue king crab Paralithodes platypus near the Pribilof Islands, Alaska. Journal of Crustacean Biology 5, 365-376. Stevens, B. G. 2003. Settlement, substratum preference, and survival of red king crab Paralithodes camtschaticus (Tilesius, 1815) glaucothoe on natural substrata in the laboratory. J. Exp. Mar. Biol. Ecol. 283, 63-78. Stevens, B.G., Swiney, K.M., 2005. Post-settlement effects of habitat type and predator size on cannibalism of glaucothoe and juveniles of red king crab Paralithodes camtschaticus. J. Exp. Mar. Biol. Ecol. 321, 1–11. Stevens, B. G. 2006a. Embryonic development and morphometry in the blue king crab Paralithodes platypus studied by using image and cluster analysis. Journal of Shellfish Research. 25, 569-576. Stevens, B. G. 2006b. Timing and duration of larval hatching for blue king crab Paralithodes platypus Brandt, 1850 held in the laboratory. Journal of Crustacean Biology. 26, 495-502. Stevens, B. G., editor. 2006c. Alaska Crab Stock Enhancement and Rehabilitation: Workshop Proceedings. Alaska Sea Grant College Program AK-SG-06-04. Stevens, B. G., 2006d. King crab cultivation and stock enhancement in Japan and the United States: A brief history. In: Stevens, B. G., (ed.) Alaska Crab Stock Enhancement and Rehabilitation: Workshop Proceedings. P. 23-31. Alaska Sea Grant College Program AK- SG-06-04. Stevens, B. G., Persselin, S., Matweyou, J. 2008. Survival of blue king crab larvae, Paralithodes platypus, in cultivation: Effects of diet, temperature, and density. Aq. Res. 39, 390-397. Stevens, B. G. Swiney, K. M. 2007. Hatch timing, incubation period, and reproductive cycle for primiparous and multiparous red king crab Paralithodes camtschaticus (Tilesius, 1815). Journal of Crustacean Biology. 27, 37-48.

8 Zhang, J., Rao, G., Wang, Z., Meng, X., Kong, L., Xuan Z., Cao, Z., Yang D. 1998. Production effect of Eriocheir sinensis larvae culture with micro-capsulated diets to replace living foods. J. Shanghai Fish. Univ./Shanghai Shuichan Daxue Xuebao 7, 235-240. Zheng J, Kruse G, 2000. Recruitment patterns of Alaskan crabs in relation to decadal shifts in climate and physical oceanography. ICES J Mar Sci 57:438-451. Zheng J, Kruse G, 2006. Recruitment variation of eastern Bering Sea crabs: Climate forcing or top-down effects? Prog Oceanogr 184-204. Zhou, S., Shirley, T.C., Kruse, G.H. 1998. Feeding and growth of the red king crab Paralithodes camtschaticus under laboratory conditions. J Crustac Biol 18, 337-345 Zmora, O., Findiesen, A., Stubblefield, J., Frenkel, V. and Zohar, Y. 2005. Large-Scale Juvenile Production of the Blue Crab Callinectes sapidus. Aquaculture 244, 129-139.