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Effects of salinity on snow crab (Chionoecetes opilio) larval survival and development under laboratory conditions.

ABSTRACT To better understand the factors influencing larval dispersal and settlement of the snow crab Chionoecetes opilio in its natural habitats, we tested the effects of salinities ranging from 18 to 38 and 20-38 on the survival and developmental duration of snow crab larvae in the zoeal and megalopal stages, respectively. Survivals to second-stage zoeae and to megalopae were highest at salinities of 20-38 and 26-38, respectively. There were no significant differences in survival among megalopae reared at salinities between 24 and 38, although survival tended to be higher at salinities range 28-36. The mean periods from hatching to the second zoeal and megalopal stages, and from the megalopal to first crab stage, were shortest at salinities of 30, 30, and 32, respectively, and progressively increased at salinities above and below these values.

KEY WORDS: Chionoecetes opilio, snow crab, rearing salinity, larval duration, larval survival

INTRODUCTION

The pelagic phase of the crustacean life history plays an important role in sustaining populations by facilitating larval dispersal and recruitment (e.g., Sulkin 1984, Anger 2001, 2006). The larvae exhibit rapid growth and undergo morphogenetic changes in metamorphosis into the megalopal stage. This developmental process is influenced by environmental factors such as water temperature, salinity, food availability and quality, predation, and ocean currents (e.g., Sulkin 1984, Anger 2001, Forward 2009).

Snow crab Chionoecetes opilio is one of the five species belonging to the genus Chionoecetes (Brachyura, Oregoniidae); it occurs on the continental shelf throughout the cold waters of the northern hemisphere and is an important fishery resource (e.g., Elner 1982,Sinoda 1982, Jadamec et al. 1999, Azuma et al. 2011). A number of researchers have studied the general biology of snow crab larvae with a focus on managing stocks or evaluating the mechanism underlying fluctuations in stock abundance (e.g., Kon 1980, Davidson & Chin 1991, Incze et al. 1984, Lovrich & Oullet 1994). The entire duration of the larval period from hatching to first crab stage ranges from 74 to 123 d (~2.5-4 mo) and is dependent on water temperature (Yamamoto et al. 2014).

Other environmental factors may also influence survival and larval development in the snow crab. For example, salinity affects the duration of larval developmental and larval survival rates in many decapod crustaceans (Anger 2003). Snow crab larvae are typically found in environments that do not experience large salinity fluctuations, including the Sea of Japan and the southeastern Bering Sea (Kon 1980. Incze et al. 1987). Nevertheless, snow crab zoeae are also found at salinities ranging from 24 to 32 in the Gulf of St. Lawrence (Conan et al. 1996) and in very shallow water (2.5-3 m) (Sainte-Marie & Dufour 1988, Lovrich et al. 1995), where salinity might fluctuate. To date, two studies have evaluated the effect of salinity on larval survival and development in the snow crab (Kon 1973, Charmantier & Charmantier-Daures 1995). The analysis by Kon (1973) included data from larvae that died during or immediately after molting, thereby making it difficult to draw accurate conclusions concerning the effect of salinity on survival or on the duration of the developmental periods. In additiona, Charmantier and Charmantier-Daures (1995) determined only the lethal salinity for first-stage zoeae. Our objective was to evaluate the effects of salinity on the survival and development of snow crab larvae during the entire period of larval development.

MATERIALS AND METHODS

Source of Larvae

A total of 185 ovigerous females were caught in November 2011 in the Sea of Japan off Ishikawa Prefecture, Japan. They were transferred to the Obama Laboratory at the Japan Sea National Fisheries Research Institute, Fisheries Research Agency, Fukui Prefecture, and reared at 3[degrees]C in one 4-kL (1.3 x 3.9 x 0.85 m) rectangular tank with recirculating seawater (salinity ~33), as described by Morita and Nogami (2003). Females were fed frozen Antarctic krill Euphausia superba twice weekly. The main hatching season was from February to March 2012; often several females released their larvae on the same day.

Larval Rearing Experiments

Larval rearing experiments were conducted during the zoeal stages (i.e., from hatching to metamorphosis to the megalopa) and during the megalopal stage (i.e., from metamorphosis to the molt to the first crab stage). The first zoeae hatched on February 9, 2012. Megalopae that metamorphosed on March 16, 2012 from zoeae that hatched on February 9 and 10, 2012 were used in experiments. Larval culture was carried out in 1-L plastic beakers that were placed in temperature-controlled baths. The water temperature was maintained at 11[degrees]C during the zoeal stage and 8[degrees]C during the megalopal stage. These temperatures were chosen based on the thermal distribution in the natural habitat (Kon et al. 2003) and the optimum temperatures for larval survival (Yamamoto et al. 2014). Zoeae were reared at 11 experimental salinities: 18, 20, 22, 24, 26, 28, 30, 32, 34, 36, and 38 (three beakers per concentration, 20 individuals per beaker). Megalopae were reared at 10 salinities: 20, 22,24, 26,28, 30, 32, 34, 36, and 38 (five beakers per concentration, four individuals per beaker). Diluted seawater was prepared by adding freshwater to seawater, and high-salinity water was prepared by adding synthetic seawater salt (Instant Ocean, Napqo Ltd., Tokyo, Japan) to seawater. Salinity was measured using a multiparameter water-quality meter (556MPS, YSI Inc., Yellow Springs, OH). Larvae were transferred directly from the holding tank (salinity ~33) to the experimental salinity at the beginning of the experiment. Larvae were cultured at 14[degrees]C and salinity 33 to prepare test animals for the megalopal experiment.

Larval culture was based on the method of Yamamoto et al. (2014). Zoeae were fed rotifers Brachionus plica tills at a density of 20 individuals/mL. Rotifers were enriched with 0.5 mL/L commercial condensed marine phytoplankton (Nannochloropsis sp., Mercian Co., Ltd., Tokyo, Japan), 14 [micro]L/L emulsified DHA 70 G oil, and 28 [micro]L/L EPA 28 G oil (Hokkaido Fine Chemicals Co., Ltd., Hokkaido, Japan) at 16[degrees]C for 18 h before feeding. Artemia nauplii (Utah strain) were enriched with 1.5 mL/L of a commercial emulsion of n-3 polyunsaturated fatty acids (Hyper Glos, Marinetech Co., Ltd., Aichi, Japan) at 22[degrees]C for 24 h then given to megalopae at a density of five individuals/mL. The rearing water was not aerated. Baths were covered with Styrofoam boards to stabilize the water temperature. Each morning, larvae were transferred to newly prepared beakers with fresh experimental seawater and food, using a large-mouthed pipette, and the survivors were counted. Larval developmental stages were confirmed by visual examination with the unaided eye. Dead larvae were removed from the rearing beakers, and their developmental stage was recorded. After each transfer of larvae, 20 mg/L dihydrostreptomycin sulfate (Tamura-seiyaku Co., Ltd., Tokyo, Japan) was added to the rearing water to prevent bacterial attachment to the larvae. Larval rearing was terminated when all larvae had molted to the megalopal or crab stage, or had died.

Statistical Analyses

We tested for differences between the salinity treatments in the mean survival rate and the number of days (n = 3) from hatching to the second zoeal stage and to the megalopal stage, using one-way analysis of variance (ANOVA) and Tukey's post hoc test. In the calculations of survival rates and the mean number of days from megalopal to crab stage, data for the individual larvae in each treatment group (five beakers) were pooled because of the small number of larvae reared in each beaker. We tested for differences between salinity treatments in the total number of individuals developing from megalopal to crab stage using a chi-square test and Tukey's test. One-way ANOVA and Tukey's test were used to test for differences in the mean period from the megalopa to the crab stage. All statistical analyses were performed in R (R3.1.1; R Core Team 2014) with a 5% significance level.

RESULTS

The first-stage zoeae reared at salinity 18 did not molt to second-stage zoeae (Fig. 1, Table 1). Survival to the second zoeal stage was significantly higher at salinities 20-38 (>77%) than at salinity 18 (0%). Second-stage zoeae did not molt to megalopae at salinity 20. The survival to megalopae tended to be lower at salinities 20-24 (<32%) than for larvae reared at salinities 26-38 (>68%). Megalopae molted to the first crab stage at salinities 22-38 but not at salinity 20 (Fig. 2, Table 2). The survival rates of megalopae reared at salinities 24-38 did not differ significantly among treatments, although survival tended to be higher at salinities 28-36 (>75%).

The mean duration of the periods from hatching to the second zoeal stage, and from hatching to the megalopal stage, were both shortest at salinity 30. The period from the megalopa to the first crab stage was shortest at salinity 32 (Tables 1 and 2). Larvae took 20-33 days to reach the second zoeal stage at salinities 20-38 and 43-70 days to reach the megalopal stage at salinities 22-38. The duration of the megalopal stage ranged from 43 to 52 days at salinities 22-38. Thus, the total duration of the larval period ranged from 86 to 122 days at salinities 22-38.

DISCUSSION

We tested the effect of a wide range of salinities (18-38 for zoeae and 20-38 for megalopae) and demonstrated that salinity influenced the survival and developmental rates of snow crab larvae. Kon (1973) reared snow crab zoeae in seawater with specific gravities ranging from 1.015 to 1.030 (salinities 19.8-39.1, calculated from Millero et al. 1980) and concluded that the optimal salinities for molting from the first to second zoeal stage and from the second zoeal to megalopal stage were 1.022-1.027 (salinities 28.9-35.3) and 1.019-1.026 (salinities 25.0-34.0), respectively. This author also reared megalopae at specific gravities ranging from 1.016 to 1.029 (salinities 21.1-37.9) and noted that the molting rate from megalopa to first crab stage increased with decreasing salinity. Nevertheless, the analysis in this early study was confounded by including data from larvae that died during or immediately after molting. Despite this, the results are generally consistent with our observations. Charmantier and Charmantier-Daures (1995) evaluated the salinity tolerance of snow crab first-stage zoeae and concluded that the lower and upper median lethal salinities were ~10 and ~42 at 24 h, 18 and ~41 at 48 h, and 22-25 and ~38 at 96 h, respectively. In this study, we did not test the effect of salinity levels below 10 or above 38. Nevertheless, the survival rates at the lower and upper median lethal salinities reported by Charmantier and Charmantier-Daures (1995) were lower than in our study (i.e., survival rates for first-stage zoeae were 98.5% at salinity 18 after 48 h. 96.5%-98.5% at salinities 22-26, and 98.5% at salinity 38 after 96 h). In this study, larvae were transferred directly from seawater (salinity ~33) to the appropriate test concentration at the beginning of the rearing experiments. Generally, survival rates are lower and development times are longer for larvae that are directly transferred compared with larvae that are gradually acclimated to test conditions (e.g., Baylon & Suzuki 2007, Baylon 2010). Thus, our results should be interpreted accordingly.

Zoeae and megalopae were unable to molt to the next stage when reared at salinities 18 and 20. Furthermore, the range of salinities associated with high survival became narrower during larval development; that is, the rates of survival to the second zoeal, megalopal, and first crab stages were high at salinities of 20-38, 26-38, and 28-36, respectively. This phenomenon is consistent with observations in other decapod crustacean species, including the mud crab Rhithropanopeus harrisii (Costlow et al. 1966), the red king crab Paralithodes camtschaticus (Kurata 1960), the fiddler crab Uca subcylindrica (Rabalalis & Cameron 1985), the Chinese mitten crab Eriocheir sinensis (Anger 1991), the red frog crab Ranina ranina (Minagawa 1992), the grapsid crab Armases miersii (Anger 1996), the mangrove crab Sesarma curacaoense (Anger & Charmantier 2000), the crucifix crab Charybdis feriatus (Baylon & Suzuki 2007), the mud crab Scylla serrata (Baylon 2010, Dan & Hamasaki. 2011), and the horsehair crab Erimacrus isenbeckii (Jinbo et al. 2012).

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

The Sea of Japan contains two Chionoecetes species, Chionoecetes opilio and Chionoecetes japonicus, whereas the southeastern Bering Sea primarily contains C. opilio and Chionoecetes bairdi (Chionoecetes angulatus and Chionoecetes tanneri are also found but are rare). The distribution of Chionoecetes larvae has been documented without distinguishing between these species because of their morphological similarity (Incze 1981, Incze et al. 1987, Kon et al. 2003). Snow crab zoeae occur at salinities 24-32 in the Gulf of St. Lawrence (Conan et al. 1996). In the Sea of Japan, snow crab larvae (including C. opilio and C. japonicus) are found from early spring to early summer at 0-400 m depths (Kon et al. 2003). In this season, the salinities range from ~33 to 34.5 at these depths (Naganuma 2000). In the southeastern Bering Sea, zoeae (only C. opilio) are found primarily from April to June in the upper 40 m and megalopae (C. opilio and C. bairdi) are present from July to September in the upper 60 m (Incze 1981, Incze et al. 1987). The surface salinity is ~32 in April (Incze et al. 1987). Thus, the salinity in these regions matches the optimum salinity range for survival of snow crab larvae in our study. Moreover, the lower limit of the vertical distribution of Chionoecetes larvae becomes deeper during development (Incze 1981, Conan et al. 1996, Kon et al. 2003). Thus, the decrease in the optimum salinity range for survival with the progression of larval development may be an adaptation to the shift in vertical distribution of larvae in the water column.

The periods from hatching to the second zoeal stage, from hatching to the megalopal stage, and from the megalopal to the first crab stage were shortest at salinities 30, 30, and 32, respectively, and increased outside these salinities. This appears to be a general phenomenon in decapod crustaceans and has been reported in several species, including Rhithropanopeus harrisii (Costlow et al. 1966), the southern king crab Lithodes antarcticus (Vinuesa et al. 1985), Eriocheir sinensis (Anger 1991), Ranina ranina (Minagawa 1992), the giant spider crab, Macrocheira kaempferi (Okamoto 1995), Armases miersii (Anger 1996), Sesarma curacaoense (Anger & Charmantier 2000), and Erimacrus isenbeckii (Jinbo et al. 2012). Kon (1973) reported that the minimum intermolt periods for the first and second zoeal stages and the megalopal stage were 210 day-degrees (~19 days at 11[degrees]C) at specific gravities of 1.022-1.024 (salinities 29-31), 210 day-degrees (~19 days at 11[degrees]C) at 1.020-1.022 (salinities 26-29), and 390 day-degrees (~35 days at 11[degrees]C), respectively. These values are consistent with our observations in the current study.

The effect of salinity on larval survival is important information for inferring larval distribution in natural habitats. Such information could also be incorporated into biophysical modeling (Parada et al. 2010, Szuwalski & Punt 2013, Mullowney et al. 2014) to more accurately infer the larval distribution and transport of snow crabs in their natural habitat.

ACKNOWLEDGMENTS

We thank all members of the Obama Laboratory of the JSNFRI, FRA for assistance with laboratory work. We are grateful to Dr. Sandra E. Shumway and an anonymous reviewer for suggestions and comments on the manuscript.

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TAKEO YAMAMOTO, (1) * TATSUYA YAMADA, (1) HIROSHI FUJIMOTO (2) AND KATSUYUKI HAMASAKI (3)

(1) Obama Laboratory, Japan Sea National Fisheries Research Institute, Fisheries Research Agency (FRA), Obama, Fukui 917-0117, Japan; (2) Shibushi Laboratory, National Research Institute of Aquaculture, FRA, Shibushi, Kagoshima 899-7101, Japan; (3) Graduate School of Marine Science and Technology, Tokyo University of Marine Science and Technology, Minato, Tokyo 108-8477, Japan

* Corresponding author. E-mail: takeoy@affrc.go.jp

DOI: 10.2983/035.034.0234
TABLE 1.
Survival rates and number of days from hatching to the second zoeal
stage and the megalopal stage in snow crab Chionoecetes opilio larvae
reared at 11 salinities.

                        Survival rate (%)

Salinity      To second zoea              To megalopa

18.0        0.0 (a)
20.0       76.7 [+ or -] 2.9 (b)    0.0 (a)
22.0       85.0 [+ or -] 5.0 (b)    3.3 [+ or -] 2.9 (a)
24.0       93.3 [+ or -] 5.8 (b)   31.7 [+ or -] 2.9 (b)
26.0       95.0 [+ or -] 5.0 (b)   93.3 [+ or -] 7.6 (c,d,e)
28.0       93.3 [+ or -] 2.9 (b)   88.3 [+ or -] 2.9 (c,d,e)
30.0       93.3 [+ or -] 2.9 (b)   88.3 [+ or -] 2.9 (c,d,c)
32.0       95.0 [+ or -] 8.7 (b)   90.0 [+ or -] 8.7 (c,d,e)
34.0       95.0 [+ or -] 8.7 (b)   86.7 [+ or -] 2.9 (c,d,e)
36.0       91.7 [+ or -] 2.9 (b)   75.0 [+ or -] 5.0 (c,d)
38.0       81.7 [+ or -] 7.6 (b)   68.3 [+ or -] 2.9 (c)

                        Days

Salinity           To second zoea

18.0
20.0       33.0 [+ or -] 3.1 (f)     (29-11)
22.0       27.2 [+ or -] 3.5 (e)     (21-37)
24.0       22.2 [+ or -] 2.8 (b,c)   (19-31)
26.0       20.5 [+ or -] 2.0 (a)     (17-30)
28.0       20.4 [+ or -] 1,8 (a)     (17-27)
30.0       20.3 [+ or -] 2.1 (a)     (18-30)
32.0       21.1 [+ or -] 1.9 (a,b)   (18-27)
34.0       22.2 [+ or -] 2.8 (b,c)   (18-35)
36.0       23.1 [+ or -] 2.1 (c,d)   (19-30)
38.0       24.7 [+ or -] 3.5 (d)     (20-43)

                        Days

Salinity             To megalopa

18.0
20.0
22.0       69.5 (f)                  (69-70)
24.0       58.4 [+ or -] 5.5 (c)     (51-78)
26.0       47.0 [+ or -] 4.9 (b,c)   (40-62)
28.0       44.3 [+ or -] 3.7 (a,b)   (40-61)
30.0       43.3 [+ or -] 2.1 (a)     (41-54)
32.0       45.4 [+ or -] 2.5 (a,b)   (41-54)
34.0       46.7 [+ or -] 2.8 (b,c)   (43-58)
36.0       48.9 [+ or -] 3.0 (c,d)   (44-59)
38.0       52.2 [+ or -] 3.6 (d)     (46-62)

Each value is the mean [+ or -] SD of three replicates (one replicate
is the mean value of all surviving zoeae per beaker). Values in
parentheses represent the range. Values with different superscript
letters in the same column are significantly different (P < 0.05).

TABLE 2.
Survival rates and number of days to develop from the
megalopal to first crab stage in the snow crab Chionoecetes
opilio reared at 10 salinities.

Salinity   Survival rate (%)                  Days

20.0            0.0 (a)
22.0           30.0 (b)        51.8 [+ or -] 8.3 (c)       (40-61)
24.0           60.0 (b,c)      47.5 [+ or -] 4.5 (a,b,c)   (42-59)
26.0           55.0 (b,c)      47.5 [+ or -] 4.6 (a,b,c)   (42-57)
28.0           80.0 (c)        44.8 [+ or -] 5.2 (a,b)     (39-56)
30.0           85.0 (c)        43.4 [+ or -] 3.8 (a)       (36-52)
32.0           85.0 (c)        42.6 [+ or -] 2.8 (a)       (37-49)
34.0           75.0 (b,c)      44.6 [+ or -] 2.9 (a,b)     (39-50)
36.0           75.0 (b,c)      46.5 [+ or -] 3.1 (a,b,c)   (41-51)
38.0           55.0 (b,c)      49.2 [+ or -] 6.4 (b,c)     (44-63)

Each value for number of days is the mean [+ or -] SD of individual
larvae in each salinity group. Values in parentheses represent the
range. Values with different superscript letters in the same column
are significantly different (P < 0.05).
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Article Details
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Author:Yamamoto, Takeo; Yamada, Tatsuya; Fujimoto, Hiroshi; Hamasaki, Katsuyuki
Publication:Journal of Shellfish Research
Article Type:Report
Date:Aug 1, 2015
Words:4550
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