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The effects of temperature and salinity on the survival, growth and duration of the larval development of the common spider crab Maja brachydactyla (Balss, 1922) (Brachyura: Majidae).

ABSTRACT The effect of temperature and salinity on the larval development of the common spider crab Maja brachydactyla (Balss, 1922) were studied in the laboratory. Larvae were reared at different salinities (0 45) at constant temperature, and under six different combinations of temperature (18 and 21[degrees]C) and salinity (30, 35, and 40). The survival and developmental time from newly hatched zoeae to the megalopa stage and from megalopa to the first juvenile stage was quantified; the 24 h median lethal salinity ([LS.sub.50]) for first zoeal stage was calculated. Dry mass (DM), elemental body composition (Carbon. Hydrogen, Nitrogen) and carbon: nitrogen ratio (C:N) were determined in both starved and nourished zoeae. The lower and upper [LS.sub.50] for M. brachydactyla first zoea in 24 h were 19.9 and 56.0, respectively; similar to other marine stenohaline brachyuran larvae. The megalopa stage was reached in a salinity range from 30 to 40. The highest survival rates to the first juvenile stage were observed at salinity: 35 and temperature: 21[degrees]C. Salinity was the key parameter for the survival to first juvenile, whereas the temperature had a higher effect over the duration of the larval development. The greatest loss of DM in starving and nourished zoeae was observed at low salinity (25). No differences were found in DM or C:N during the megalopa stage. The culture and ecological implications of the salinity tolerance of M. brachydactyla larvae are discussed.

KEY WORDS: Maja brachydactyla, Brachyura, growth, larval development, salinity, temperature


The common spider crab Maja brachydactyla (Balss, 1922) is a brachyuran widely distributed in the eastern Atlantic, from the southern British Isles to the western Sahara (including Azores and Canary Islands), and southwestern Mediterranean (Abello et al. 2014). This is a species of high commercial value whose main fisheries are located in France, United Kingdom, Ireland, and Spain, with an average of total annual captures of 5,600 and 7,000 tonnes between 2008 and 2012 (FAO 2012). This species shows an abbreviated larval development, consisting of a zoeal phase with two zoeal stages and a megalopa stage. The short larval duration makes M. brachydactyla a very attractive species for aquaculture (Guerao et al. 2008). Previous studies have covered the morphological description of larval stages and molt cycles (Guerao et al. 2008, Guerao & Rotllant 2010, Guerao et al. 2010), growth patterns (Andres et al. 2008) and ontogenetic changes in biochemistry (Andres et al. 2007, Andres et al. 2010a).

In the Galician coast (NW Iberian Peninsula), the larval release and recruitment of Maja brachydactyla occur in near-shore waters (Corgos et al. 2011), where the larvae may be exposed to salinity fluctuations due to the coastal and estuarine influences (Cabanas et al. 1987, Gago et al. 2011). Since the salinity is one of the key factors affecting survival, growth, development, and distribution of aquatic crustacean larvae (Charmantier 1998, Anger 2003, Torres et al. 2011), the study of the salinity tolerance during the larval development is interesting for inferring the ecological adaptations of the larvae in the field. The range of salinities for survival and development of crustacean larvae depends on the ability and range of the osmoregulatory capacity, driven by adaptations to osmotic stress that can change drastically during the ontogeny (Charmantier 1998, Charmantier et al. 2001). According to Anger (2003), if salinity exceeds the tolerance range, there usually appears a stress response, characterized by reduced survival, prolongation of the developmental time, and a depression of the feeding and growth rates. Reductions in growth rates have also been correlated with the capacity to osmoregulate (Mikami & Kuballa 2007, Torres et al. 2011). In this sense, the precise knowledge of the range of salinity tolerance is necessary for both ecological and culture approaches.

Temperature is another factor with important implications for many ecological processes, including larval dispersal and mortality, population connectivity, and recruitment dynamics (O'Connor et al. 2007). Temperature is known to have significant influence on survival, molting intervals, and total duration of larval development (Anger 1983, Minagawa 1990, Gonzalez-Ortegon & Gimenez 2014). Many studies also have shown that temperature can modify the manner in which salinity can influence the survival and duration of the larval development of brachyuran species (Costlow Jr. et al. 1962, Costlow Jr. et al. 1966, Reed 1969, Baylon & Suzuki 2007, Nurdiani & Zeng 2007). Synergistic or other multiple stressors effects are likely to occur in coastal marine organisms as a consequence of natural variations in precipitation and estuarine discharge; they are currently an objective of intensive interest because variations caused by climate change and anthropogenic influence can also affect the capacity of organisms to cope with environmental stressors (Gonzalez-Ortegon et al. 2013, Przeslawski et al. 2015). The larvae of Maja brachydactyla develop in coastal waters where freshwater flux, evaporation, and thermal radiance create dynamic changes in temperature and salinity, all of which can cause multiple stressor effects; such effects are also of importance for the optimization of techniques in aquaculture.

Hence, the main objective of this study was to determine the short- and long-term influence of salinity and the combined effects of temperature and salinity on larval development of Maja brachydactyla to better understand the likely conditions for larval recruitment in the field and obtain valuable information for the optimization of culture techniques.


Broodslock Maintenance

The broodstock of Maja brachydactyla was captured with commercial fishery boats in the NW Iberian Peninsula coast (Ria de A Coruna, Galicia, Spain) and transported to the Institut de Recerca i Tecnologia Agroalimentaries facilities (Sant Carles de la Rapita, Tarragona, Spain) in December 2012. The broodstock was kept in 2,000 1 cylindrical tanks connected to a recirculation unit (renewal rate = 3.5 [m.sup.3] x [h.sup.-1]) maintained at controlled conditions of temperature (18 [+ or -] 1[degrees]C), salinity (35 [+ or -] 1), photoperiod (12 h light: 12 h dark), and light intensity (25 lux, fluorescent lights). The broodstock was fed daily with a combination of fresh mussels (Mytilus sp. four times per week), frozen mussels (Mytilus sp., twice per week), and frozen crabs (Liocarcinus depurator, once per week).

Larval Culture System

The designed larval culture system was a modification of a previous rearing system published by Anger et al. (1991) and Andres et al. (2010b) for experimental and small-scale culture of brachyuran larvae. Each experiment was carried out in 200 1 aquaria (100 X 40 X 50 cm) used as incubation chambers (Fig. 1). Experimental glass beakers with 600 ml capacity were located inside each aquarium. The temperature was maintained constant with calibrated submersible thermostat-controlled heaters (Eheim Jager, Finsterrot, Germany) and distributed by an air lift. Daily the temperature was measured with portable meters (precision: 0.1[degrees]C; WTW ProfiLine Oxi 3210. Weilheim, Germany). The aquaria were illuminated from above with 1,000 lux LED lights; the light intensity was measured with a light meter (precision: 1 lux; Lx-101, Lutron Electronic Enterprise, Taipei, Taiwan). The photoperiod of 12 h light: 12 h dark was controlled with 24 h programmable timers.

Low salinities were obtained by diluting filtered seawater with distilled water and higher salinities by adding sea salt (Natural Salt Mix, Oceanic, Dallas, TX). The salinity of the experimental glass beakers was measured daily using a portable handheld salinity refractometer (precision: 1, range: 0-100; Shenzhen Handsome Technology Co. Ltd., Guandong, China). The glass beakers were filled with 500 ml of the test salinities according to each treatment.

The newly hatched larvae ([ZI.sub.0]) were transferred by outflow pipe to special collectors (35 1 fiberglass cylindroconical baskets opened by 12 X 18 cm windows covered with 150 [micro]m mesh). Only actively swimming zoeae of the same hatch within a maximum ~15 h after hatching were selected for the experiments.

Following Andres et al. (2007, 2008), larvae were transferred to glass culture beakers at an initial density of 60 zoeae [1.sup.-1] without prior adaptation, the experiment continued until all the larvae died or molted to megalopa. The newly molted megalopae ([M.sub.0]) were transferred to new experimental glass beakers at an initial density of 20 megalopae [1.sup.-1] and kept under the previous experimental conditions until all the animals died or reached the first juvenile instar ([J.sub.0]). The confirmation of the death was carried out using a Nikon SMZ800 stereomicroscope; the total lack of movement of appendages and the immobility of the heart were used as criteria.

The larvae were fed daily ad libitum with fresh Artemia sp. Kellogg, 1906 nauplii and metanauplii (INVE Aquaculture Nutrition, Salt Lake, UT). Living larvae were collected daily by carefully pipetting to reserve glass beakers previously prepared at the same temperature and salinity conditions.


Acute Osmotic Stress Tolerance

This first experiment used newly hatched zoeae in starving conditions to ascertain the range of salinity tolerance. The study used six salinity treatments ranging from 0 to 55 (0, 15, 25, 35, 45, and 55 [+ or -] 1) with four replicates per treatment. The total of living and dead specimens was counted after 3 days. Samples for dry mass (DM) and elemental body composition analysis were taken. The temperature was constant at 19.7 [+ or -] 0.2[degrees]C.

Median Lethal Salinity in 24 h

In this second experiment, newly hatched zoeae in starving conditions were used to obtain more detailed information on the range of tolerance. The upper and lower median lethal salinity ([LS.sub.50]) were calculated through two separate experiments keeping larvae around the lower and upper range of tolerance: lower [LS.sub.50] (15, 17, 19, 21, 23, and 25 [+ or -] 1); upper [LS.sub.50] (51, 53, 55, 57, 59, and 61 [+ or -] 1). Three replicates per treatment were used. In both experimental sets, the total of living and dead specimens was counted after 24 h. The temperature was maintained constant at 19.7 [+ or -] 0.1[degrees]C.

Chronic Effects of Salinity on Survival and Growth

In this experiment, the long-term responses were studied within the range of salinities (20-45) that were tolerated by the starving zoea I (six salinity treatments: 20, 25, 30, 35,40, and 45 [+ or -] 1). The survival and developmental time were tested using four replicates per treatment; additional replicates for DM and elemental body composition analysis were used. The temperature was constant at 22 [+ or -] 1[degrees]C. The following response variables were studied: (1) the duration of the zoeal phase, (2) the duration of the megalopa stage, (3) the survival to the megalopa stage, and (4) the survival from the megalopa to the first juvenile stage. Since the differentiation between zoeae stages required the individual examination of the larvae under the stereomicroscope, the study was decided to focus the research in the zoeal phase to reduce the manipulation and potential damage of the larvae and increase the chances of survival until [M.sub.0] and [J.sub.0].

Combined Effects of Salinity and Temperature on Survival and Growth

This experiment was used to understand how temperature may modulate the effect of salinity on survival and growth. The experiment used two temperature regimes: 18 and 21 [+ or -] 1[degrees]C combined with three salinity levels: 30, 35, and 40 [+ or -] 1, giving a total of six temperature-salinity combinations. Four replicates per treatment were used. The response variables measured were as stated in the previous experiment.

Dry Mass and Elemental Body Composition

The DM and elemental body composition [Carbon, Hydrogen, Nitrogen (CHN)] were analyzed in Acute Osmotic Stress Tolerance and Chronic Effects of Salinity on Survival and Growth experiments to study the acute and chronic effects of the salinity on the growth. Each treatment used five replicates per zoeae phase and megalopa stage. Each analysis (DM and CHN) required five zoeae and three megalopae, respectively. The zoeae were sampled as newly hatched ([ZI.sub.0]) and in intermolt ([ZI.sub.2-3]), whereas the megalopae were sampled when newly molted ([M.sub.0]). The larvae were gently rinsed in distilled water for 10-20 sec and blotted dry on a metal sieve with filter paper. Subsequently, the larvae were transferred to preweighed tin capsules pressed for Elemental Microanalysis and stored at -20[degrees]C.

Analyses of DM and CHN were carried out at the School of Ocean Sciences (Bangor University, Menai Bridge, UK) following standard techniques (Anger & Harms 1990, D'Urban Jackson et al. 2014). Samples were freeze dried in a vacuum drier (Edwards Super Modulyo) for 24 h and DM was determined with a Mettler Toledo MX5 microbalance (precision: 1 [micro]g, capacity: 5.1 g). Elemental Analysis was performed using a CHNS-O Analyzer (FlashEA 1112 Series).

Statistical Analysis

The statistical treatment of the data was performed using R version 3.2.0 (R Development Core Team 2015). The median lethal salinity was calculated using a general linear model with the <<dosing.p>> function of the R package <<MASS 7.3-4>> (Venables & Ripley 2002). One way analysis of variance (ANOVA) was performed using salinity as factor. The combined effects of temperature and salinity were tested through two-way Type III ANOVA applying R package <<car 2.0-25>> (Fox & Weisberg 2011). Comparisons between groups after finding significant differences were performed by Tukey's honest significant difference test. Normality and homogeneity were tested by Shapiro-Wilk and Levene tests, respectively. Kruskal-Wallis test was carried out when the data did not show normality or homogeneity of variance. The critical level ([alpha]) to reject the null hypothesis was 0.05.


Acute Osmotic Stress Tolerance

All larvae exposed to a salinity of 0 and 15 died in the first 24 h. In the salinity range from 25 to 55, the survival was higher than 90% without significant differences among treatments (Kruskal-Wallis: [X.sup.2.sub.3] = 2.76, P = 0.43).

Salinity affected the DM and elemental body composition of the 3-day-old zoeae (ANOVA: [F.sub.3,15] = 32.01, P < 0.001). The stronger effect in decreasing DM was produced by the low salinity (25); whereas only a minor DM reduction was produced by the higher salinities, 45 and 55 (Table 1). Larvae reared at low and seawater salinity (35) showed higher percent carbon and nitrogen than larvae reared at extremely high salinities (C: [F.sub.3,14] = 200.9, P <0.001; N: [F.sub.3,14] = 169.9, P < 0.001). The carbon content per individual also decreased at higher salinity, but the nitrogen content per individual did not vary between treatments (C: [F.sub.3,14] = 6.11, P< 0.01; N: [F.sub.3,14] = 0.82, P = 0.51). The C:N ratio indicated that at high and low salinity, the losses of C were proportionally larger than losses of N ([F.sub.3,15] = 79.19, P< 0.001; Table 1).

Median Lethal Salinity in 24 h

The lower [LS.sub.50] was at 19.9, whereas the upper [LS.sub.50] was at 56.0 (Fig. 2). The larvae exposed at 20 or lower salinities immediately sank passively to the bottom of the culture glass beakers; those larvae exposed at 56 or higher salinities remained swimming actively in the glass culture beakers until they died.

Chronic Effects of Salinity on Survival and Growth Survival and Duration of Larval Development

Total mortality occurred after 24 h at salinity 20, after 5 days at salinity 45 and after 7 days at salinity 25, coinciding with the molt to megalopa stage (Fig. 3). The development until the megalopa stage only occurred in the salinity range from 30 to 40, but there were significant differences among treatments ([F.sub.2,9] = 16.52, P < 0.001). The highest survival was observed at salinity 35 (51.7 [+ or -] 11.4%), followed by salinity 30 (39.2 [+ or -] 9.6%), and salinity 40 (11.4 [+ or -] 9.3%; Fig. 3). The molt to zoea II occurred between the 3rd and 4th day of culture from hatching (salinity range: 25-45). The duration of the zoeal phase until M0 was on average 7.1 [+ or -] 0.8 days, but significant differences among salinity treatments were not observed ([F.sub.2,8] = 0.64, P = 0.55).

The highest survival from megalopa to first juvenile occurred at salinity 35 (37.5 [+ or -] 4.8%); and the average duration of the megalopa stage was 6.2 [+ or -] 1.1 days. High mortality rates were observed at other salinities (100% of mortality at salinity 40; only one individual reached the juvenile stage at salinity 30 after 5 days of megalopa stage).

Growth and Elemental Body Composition

Salinity had a significant effect on the larval growth and elemental body composition. Two-day-old zoeae showed a DM increment in all treatments except at salinity 25 ([F.sub.4,20] = 12.12, P < 0.001; Table 2); the carbon and nitrogen content per individual also increased in all treatments except at 25 (C: F4-20 3.53, P < 0.05; N: [F.sub.4,20] = 3.58, P < 0.05). The percent carbon and nitrogen was significantly lower at salinity of 40 and 45 (C: [F.sub.4,20] = 3.63, P< 0.05; N: [F.sub.4,20] = 4.70, P < 0.01). Although the C:N ratio differed significantly among treatments ([F.sub.4,19] = 4.65, P < 0.01), a general trend was not observed (Table 2).

Megalopa from different salinity treatments did not show significant differences in DM ([F.sub.2,11] = 0.719, P = 0.51), carbon and nitrogen content per individual (C: [F.sub.2,11] = 2.02. P = 0.18; N: [F.sub.2,11] = 2.51, P = 0.13), percent nitrogen ([F.sub.2,11] = 3.05. P = 0.09), or C:N ratio ([F.sub.2,11] = 1.16, P = 0.35). Only the percent carbon showed a significant response, consisting in decreased levels at higher salinity ([F.sub.2,11] = 6.98, P < 0.05; Table 3).

Combined Effect of Temperature and Salinity Survival and Duration of Development

The two-way ANOVA showed a significant interaction between temperature and salinity on survival from hatching to the megalopa stage ([F.sub.2,18] = 5.26, P < 0.05): survival decreased at salinity 30 and 40 with the temperature increment, but increased at salinity 35. The lowest survival occurred at the combination: salinity 40 and 18[degrees]C (22.5 [+ or -] 22.3%); but it doubled in the remaining temperature-salinity combinations (Fig. 4). Survival to the juvenile stage was significantly affected by salinity ([F.sub.2,18] = 11.54, P < 0.001), but not by temperature ([F.sub.1,18] = 2.08, P = 0.16) or the interaction of both ([F.sub.2,18] = 0.31, P = 0.73); the highest survival occurred at salinity 35 (average: 62.5 [+ or -] 21.2%; Fig. 5). In most cases, mortality occurred at the time of metamorphosis: most individuals failed to metamorphose or metamorphosed with deformities (syndrome of molt cycle).

The duration of the zoeal phase was significantly affected by temperature ([F.sub.1,17] = 87.71, P < 0.001), but not by salinity ([F.sub.2,17] = 1.06, P = 0.36) or their interaction ([F.sub.2,17] = 0.95, P = 0. 40). The zoeal phase required less time at 21[degrees]C (average 7.6 [+ or -] 0.7 days) than at 18[degrees]C (average 10.2 [+ or -] 1.0 days) to complete (Fig. 6). The duration of the megalopa was also affected by temperature ([F.sub.1,14] = 89.7, P < 0.001), whereas salinity ([F.sub.2,14] = 1.62, P = 0.23) and the interaction between temperature and salinity was not significant ([F.sub.1,14] = 2.58, P = 0.13). The megalopa stage required less time to complete at 21[degrees]C (average: 6.0 [+ or -] 0.5 days) than at 18[degrees]C (average: 8.8 [+ or -] 1.0 days; Fig. 7).


The data showed that larvae of Maja brachydactyla are strictly stenohaline. The acute stress restricted the salinity tolerance range from 20 to 56 and outside this range the larvae died in less than 24 h. Larvae tolerated salinities of 25 and 45, but the growth rate was reduced and metamorphosis to megalopae did not occur. The most suitable range for development was between 30 and 40: larvae successfully metamorphosed to the first juvenile stage. Moreover, the highest survival from newly hatched zoeae to first juvenile stage was observed at salinity 35 [+ or -] 1. The duration of larval development was not affected by salinity. On the other hand, the highest temperature showed the shorter duration of the larval development (21[degrees]C). In general terms, the larval culture of this species required a constant salinity at 35 [+ or -] 1. Contrary to other brachyuran species of interest for culture such as Scylla serrata (Nurdiani & Zeng 2007), the larval stages of M. brachydactyla were not tolerant to salinity levels below 30. These restrictions must be taken into account in the selection of sites or water sources for the culture of this species.

Previous studies that have focused on the osmoregulatory physiology of the majid crabs showed that generally they are osmoconformers or weak regulators with high sensitivity to variations in salinity (Dakin 1912, Pequeux 1995). The vulnerability of Maja brachydactyla to low salinity is also reflected in the decrement of larvae production by adults (Rotllant et al. 2015) and a narrow range of acute salinity tolerance ([LS.sub.50] >n 24 h) in newly hatched zoeae (salinity range: 20-56). A similar LS50 range was observed in the larvae of other brachyurans such as the cancroid Cancer irroratus (salinity range: 15-46: Charmantier & Charmantier-Daures 1991) or the majoid Chionoecetes opilio (salinity range: 9.5-42.5: Charmantier & Charmantier-Daures 1995). Other brachyuran larvae have a broader salinity tolerance range: for example, the grapsoid Armases miersii and the xanthoid Rhithropcmopeus harrisii can complete the larval development in a salinity range from 5 to 35 (Anger 1996; Forward Jr. 2009), whereas the first zoeae of Armases ricordi tolerate a salinity range from 5 to 55 during 6 days (Diesel & Schuh 1998). These differences in the salinity tolerance range correspond to adaptations to fluctuations in the salinity in the field (Anger 2001). Larvae with a narrow salinity tolerance inhabit waters with oceanic influence (Bigford 1979, Charmantier & CharmantierDaures 1995) whereas those with broader salinity tolerance usually inhabit environments with high salinity fluctuations, such as rocky pools or estuaries (Costlow Jr. et al. 1966, Anger 1995, Forward Jr. 2009). The Table 4 summarizes the relationship between the range of salinity tolerance of brachyuran larvae and their habitat. In some taxa, there are specializations to some environments (e.g., estuarine environments in Grapsoidea and Portunoidea and nearshore/offshore in Majoidea); but exceptions are associated with habitat specialization (e.g., Pacliygrapsus transversus in grapsoid or Halicarcinus rostratus in majoid crabs, see Table 4). Thus, it can be hypothesize that the larval tolerance to salinity is more influenced by adaptations to field conditions than by the phylogeny.

The optimal salinity for the larval development of Maja brachydactyla is 35 [+ or -] 1, coincides with the expected conditions for development in the field: the outer coast of Galicia (NW Iberian Peninsula) shows a constant salinity of ~35, whereas in the inner coast the salinity fluctuates between the 30 in winter and the 35 in summer due to estuarine influence (Cabanas et al. 1987, Corgos et al. 2011, Gago et al. 2011). Exposure of larvae to this estuarine influence cannot be discarded, because the zoeae are released in nearshore areas (Corgos et al. 2011) and they will be distributed by the marine currents as occurs with other brachyuran larvae (Peliz et al. 2007). From the standpoint of salinity, moderate to high survival would be expected because zoeae reached the megalopa stage at 30. Survival might be also maximized as a consequence of the time of release (spring and summer: Corgos et al. 2011), when the fluctuations in salinity are reduced and the average salinity is nearest to the optimal range for this species (Gago et al. 2011).

When the larvae of Maja brachydactyla were exposed to very low salinities (near or under the [LS.sub.50]), their immediate reaction was immobilization and dropping to the bottom of the glass culture beakers as observed in other brachyurans (Anger 1985, Kannupandi et al. 2000, Baylon & Suzuki 2007). Anger (1985) suggested that this behavior would enable larvae to reach the lower waters layers, where salinity is higher. This strategy may be useful for M. brachydactyla larvae, because in the Galician coast the salinity increases with depth until reaching a maximum of 35.5 (Gago et al. 2011).

The likely salinity conditions at the settlement habitat are still unknown, but the experiments suggest that megalopa would not settle in very shallow habitats, characterized by low or variable salinity. Le Foil (1993) found that juveniles (carapace length > 50 mm) of Maja brachydactyla (referred as Maja squinado) inhabit sand, mud-sand, gravel, rock, and maerl seafloors, mainly at 15 m depth; however, the habitat of younger juveniles was not found. Corgos et al. (2011) suggested that the recruitment may occur in more shallow habitats (<5 m depth). The same authors also noticed that both juveniles and adults inhabit seafloors with constant salinity around 35, in the range of optimal salinity as shown in this study. Hence, the study propose three possible hypotheses: (1) the megalopae avoid the estuarine influenced waters and their settlement occurs in coastal waters with oceanic characteristics; (2) because the settlement occurs during late spring and summer, the metamorphosis to first juvenile can take place in coastal waters with minimal estuarine influence (i.e., coinciding with a period when the drop in salinity is minimal); (3) the megalopae might tolerate short exposure to low salinity and they migrate shortly after metamorphosis into estuarine-influenced coastal areas. To evaluate these hypotheses, the settlement habitat of M. brachydactyla in the field must be determined.

The temperature mainly influences the duration of the larval development of Maja brachydactyla: the duration was significantly shorter at higher temperatures (21 versus 18[degrees]C). Temperature increases the metabolic processes, accelerates the molting cycle and reduces the duration of larval development of brachyurans (Costlow et al. 1960, Costlow Jr. et al. 1966, Ong & Costlow 1970, Minagawa 1990, Anger 1991, Mene et al. 1991, Nagaraj 1992, Larez et al. 2000, Anger 2001, Baylon & Suzuki 2007, Nurdiani & Zeng 2007, Spivak & Cuesta 2009, Hernandez et al. 2012). Low salinities increased the duration of the larval development in some brachyuran species (Anger 1985, Mene et al. 1991, Minagawa 1992, Nagaraj 1992), however, the study did not observe this phenomenon in M. brachydactyla larvae. Beside the cited studies, the salinity evokes comparatively weak effects over the duration of decapods as reviewed by Anger (2003).

The DM and elemental body composition of the zoeae of Maja brachydactyla varied with the salinity. The larvae maintained at salinity 25 in starving conditions showed higher DM losses than the larvae maintained at salinity 35 although both groups maintained similar carbon levels. Because the carbon content is a reliable expression of the biomass content in the individuals (Anger & Dawirs 1982, Anger et al. 2000, Anger 2003), it can be considered that the higher DM losses at salinity 25 could be explained by mineral losses. The larvae of another majoid, Hyas araneus, show important mineral depletion under low salinities, probably due to the depression in the mineral accumulation rate and the osmotic loss of mineral content (Anger 2003). In this sense, the higher DM and lower carbon and nitrogen percentages observed in the larvae maintained at salinity 45 and 55 could be explained by a mineral accumulation. On the contrary, well-fed 2-day-old larvae increased their DM in all the salinity treatments except at salinity 25, although similar values of percentage carbon and nitrogen were observed. Short exposures (-50% molt cycle) to low salinities may also cause reduction of DM, lipid and/or protein content in marine brachyuran larvae such as Cancerpagurus (Torres et al. 2002) or Hyas araneus (Anger 2003, Torres et al. 2011). Similar results were also reported in astacideans larvae such as Homarus gammarus and Nephrops norvegicus (Torres et al. 2002, Torres et al. 2011). A reduction of feeding (Minagawa 1992), and food conversion (Anger 2003, Torres et al. 2011) has been proposed as an explanation for the reduction in growth at low salinity.

The C:N ratio has been widely applied as an indicator of the lipid:protein ratio in the decapod larvae (Anger & Dawirs 1981, Anger & Dawirs 1982, Anger & Harms 1990, Anger et al. 1998, D'Urban Jackson et al. 2014), including Maja brachydactyla (Andres et al. 2008). Anger and Dawirs (1982) indicated that changes in the C:N ratio indicate shifts in the relative amounts of lipids (plus carbohydrates) and proteins (plus free amino acids); and a decrease in the C:N ratio can be interpreted as a degradation in lipid contents and/or a protein accumulation. In starved zoeae, the lowest C:N ratio occurred at salinity 55, intermediate values were observed at salinity 25 and 45. The reduction of the C:N ratio under unfavorable salinity conditions could be related with a degradation of the lipids due to extra energetic requirements. When larvae were fed, the C:N ratio did not show significant differences among the salinity concentrations tested.

In conclusion, the larvae of Maja brachydactyla are stenohaline with a rather narrow range of salinities where complete larval development is achieved. Such narrow limits should restrict the timing and sites of larval settlement, duration of the period of metamorphosis in coastal areas, and the water sources useful for their culture. Extreme salinities (low or high), influence the DM and the elemental body composition of the developing larvae, whereas the temperature can interact with salinity to influence the survival during the zoeal phase.


The Spanish Ministry of Economy and Competitiveness funded bench fees through the INIA project (RTA201100004-00-00) to G.G. and a predoctoral fellowship to D.C. (FPI-INIA). We would like to thank Carles Alcaraz for his advice on the data analysis and Karl B. Andree for his improvement of the article. We thank hatchery technicians at IRTA in Sant Carles de la Rapita (David Carmona, Gloria Macia, Magda Monllao and Francese X. Ingla) for the broodstock maintenance and the setup of the rearing culture system.


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(1) Subprograma Cultius Aquatics, IRTA, Ctra. de Pobre Nou, Km 5.5, Sant Carles de la Rctpita 43540, Tarragona, Spain; (2) Departament de Recursos Marins Removables, Institui de Ciencies Del Mar, CSIC, Passeig Maritim de la Barceloneta 37-49, Barcelona 08003, Spain; (3) School of Ocean Sciences, Bangor University, Menai Bridge, Anglesey, LL59 5AB, United Kingdom; (4) PS Fabra i Puig 344, Barcelona 08031, Spain

* Corresponding author. E-mail:

DOI: 10.2983/035.034.0334

Acute effects of salinity on growth under starving conditions in Maja
brachydactyla zoeae I from ~15 h after hatch (0 day) and in
intermoult (3 days from hatch).

Age (days)   Salinity        DM (ng)         ([micro]g [ind.sup.-1])

0               --      104 [+ or -] 1        35.7 [+ or -] 0.3
3               25       91 [+ or -] 1 (a)    28.3 [+ or -] 0.3 (a)
                35       93 [+ or -] 1 (b)    28.2 [+ or -] 0.4 (a)
                45       96 [+ or -] 2 (c)    28.0 [+ or -] 0.2 (ab)
                55       97 [+ or -] 1 (c)    27.4 [+ or -] 0.4 (b)

                                                Nitrogen ([micro]g
Age (days)   Salinity        Carbon (%)           [ind.sup.-1])

0               --      34.4 [+ or -] 0.1       9.20 [+ or -] 0.05
3               25      31.3 [+ or -] 0.2 (a)   7.37 [+ or -] 0.10
                35      30.2 [+ or -] 0.2 (b)   7.28 [+ or -] 0.12
                45      29.2 [+ or -] 0.3 (c)   7.32 [+ or -] 0.05
                55      28.2 [+ or -] 0.1 (d)   7.34 [+ or -] 0.09

Age (days)   Salinity        Nitrogen (%)

0               --      8.85 [+ or -] 0.08
3               25      8.14 [+ or -] 0.04 (a)
                35      7.80 [+ or -] 0.05 (b)
                45      7.64 [+ or -] 0.04 (c)
                55      7.56 [+ or -] 0.01 (c)

Age (days)   Salinity          C:N ratio

0               --      3.89 [+ or -] 0.03
3               25      3.84 [+ or -] 0.02 (ab)
                35      3.87 [+ or -] 0.01 (a)
                45      3.82 [+ or -] 0.01 (b)
                55      3.73 [+ or -] 0.02 (c)

Different letters indicate significant difference (P < 0.05) among
the treatments.

Dry mass (DM, [micro]g), carbon content ([micro]g [ind.sup.-1]),
carbon percentage (%), nitrogen content ([micro]g [ind.sup.-1]),
nitrogen percentage (%) and C:N ratio. Larvae were kept at constant
19.7 [+ or -] 0.2[degrees]C. Values are expressed as average
[+ or -] SD.

Acute effects of salinity on growth under feeding conditions in Maja
brachydactyla zoeae I from 15 h after hatch (0 days) and in
intermoult (2 days from hatch).

                                                Carbon ([micro]g
Age (days)   Salinity     DM ([micro]g)          [ind.sup.-1])

0               --       95 [+ or -] 1       30.6 [+ or -] 0.4
2               25       98 [+ or -] 3 (a)   32.1 [+ or -] 1.0 (a)
                30      110 [+ or -] 4 (b)   36.5 [+ or -] 1.6 (ab)
                35      110 [+ or -] 5 (b)   35.2 [+ or -] 2.5 (ab)
                40      113 [+ or -] 2 (b)   35.6 [+ or -] 3.1 (ab)
                45      118 [+ or -] 1 (b)   37.3 [+ or -] 2.9 (b)

Age (days)   Salinity         Carbon (%)

0               --      32.2 [+ or -] 0.3
2               25      32.7 [+ or -] 0.4 (ab)
                30      33.2 [+ or -] 0.4 (a)
                35      32.0 [+ or -] 0.7 (ab)
                40      31.5 [+ or -] 1.5 (b)
                45      31.5 [+ or -] 1.0 (b)

                          Nitrogen ([micro]g
Age (days)   Salinity        [ind.sup.-1])

0               --      8.01 [+ or -] 0.13
2               25      8.30 [+ or -] 0.26 (a)
                30      9.33 [+ or -] 0.41 (ab)
                35      9.06 [+ or -] 0.56 (ab)
                40      9.11 [+ or -] 0.73 (ab)
                45      9.56 [+ or -] 0.70 (b)

Age (days)   Salinity        Nitrogen (%)

0               --      8.45 [+ or -] 0.10
2               25      8.45 [+ or -] 0.11 (ab)
                30      8.48 [+ or -] 0.09 (b)
                35      8.26 [+ or -] 0.15 (bc)
                40      8.05 [+ or -] 0.32 (c)
                45      8.08 [+ or -] 0.25 (ac)

Age (days)   Salinity          C:N ratio

0               --      3.82 [+ or -] 0.02
2               25      3.87 [+ or -] 0.02 (ab)
                30      3.91 [+ or -] 0.01 (a)
                35      3.86 [+ or -] 0.02 (b)
                40      3.91 [+ or -] 0.03 (a)
                45      3.90 [+ or -] 0.03 (ab)

Different letters indicate significant difference (P < 0.05) among
the treatments.

Dry mass (DM, [micro]g), carbon content ([micro]g [ind.sup.-1]),
carbon percentage (%), nitrogen content ([micro]g [ind.sup.-1]),
nitrogen percentage (%) and C:N ratio. Larvae were kept at constant
22 [+ or -] 1[degrees]C. Values are expressed as average [+ or -] SD.

Chronic effects of salinity on growth under feeding conditions in
Maja brachydactyla megalopae from ~15 h after molt.

                              Carbon ([micro]g
Salinity    DM ([micro]g)      [ind.sup.-1])

30         168 [+ or -] 12   57.8 [+ or -] 4.4
35         171 [+ or -] 28   57.2 [+ or -] 10.1
40         158 [+ or -] 8    50.9 [+ or -] 2.2

                                    Nitrogen ([micro]g
Salinity         Carbon (%)           [ind.sup.-1])

30         34.3 [+ or -] 0.8 (a)    14.9 [+ or -] 1.0
35         33.4 [+ or -] 1.2 (ab)   15.0 [+ or -] 2.2
40         32.1 [+ or -] 0.8 (b)    13.3 [+ or -] 0.5

Salinity      Nitrogen (%)          C:N ratio

30         8.82 [+ or -] 0.18   3.89 [+ or -] 0.07
35         8.78 [+ or -] 0.36   3.81 [+ or -] 0.13
40         8.40 [+ or -] 0.34   3.83 [+ or -] 0.06

Different letters indicate significant difference (P < 0.05) among
the treatments.

Dry mass (DM, [micro]g), carbon content ([micro]g [ind.sup.-1]),
carbon percentage (%), nitrogen content ([micro]g [ind.sup.-1]),
nitrogen percentage (%) and C:N ratio. Larvae were kept at constant
22 [+ or -] 1[degrees]C. Values are expressed as average [+ or -] SD.

Salinity tolerance in the larvae of the brachyuran clade.

      Species              Family           Saline range

Cardisoma armatum      Gecarcinidae      15-35
  (Herklots, 1851)     Grapsoidea
Cardisoma guanhumi     Gecarcinidae      20-40
  (Latreille, 1828)    Grapsoidea
Aratus pisonii (H.     Grapsidae         25-35 * ([dagger])
  Milne Edwards,       Grapsoidea          ([double dagger])
Pachygrapsus           Grapsidae         28-34 * ([dagger])
  gracilis             Grapsoidea
  (Saussure, 1858)
Pachygrapsus           Grapsidae         >32-35 * ([dagger])
  transversus          Grapsoidea
  (Gibbes, 1850)
Armases (=Sesarma)     Sesarmidae        15-45
  miersii (Rathbun,    Grapsoidea
Armases ricordi (H.    Sesarmidae        25-40
  Milne Edwards,
  1853)                Grapsoidea
Armases roberti (H.    Sesarmidae        20-10
  Milne Edwards,
  1853)                Grapsoidea
Armases                Sesarmidae        >20-30 * ([dagger])
  (=Metasesarmu)       Grapsoidea
  rubripes (Rathbun,
Selatium (=Sesarma)    Sesarmidae        >20-30
  brockii (De Man,     Grapsosidea
Sesarma cinereum       Sesarmidae        20-27
  (Bosc, 1802)         Grapsoidea
Sesarma curacaoense    Sesarmidae        15-32
 (De Man, 1982)        Grapsoidea
Acmaeopleuraparvula    Varunidae         >27-34 * ([dagger])
  (Stimpson, 1858)     Graposidea          ([double dagger])
Eriocheir sinensis     Varunidae         15-32 ([dagger])
  (H. Milne Edwards,   Grapsoidea
Neohelice              Varunidae         15-32 * ([dagger])
  (=Chasmagnathus)     Grapsoidea
  granulata (Dana,
Pseudoheliee           Varunidae         15-25
  subquadrata (Dana,   Grapsoidea
  1851) (referred as
  Helice leachi)
Uca rapax (S. I.       Ocypodidae        25-35 * ([dagger])
  Smith, 1870)         Ocypodoidea
Uca subcylindrica      Ocypodidae        0.08-45
  (Stimpson, 1859)     Ocypodoidea
Uca tangeri (Eydoux    Ocypodidae        24-32 * ([dagger])
  1835)                Ocypodoidea
Uca vocator (J. F.     Ocypodidae        10-30 * ([dagger])
  W. Herbst, 1804)     Ocypodoidea
Menippe mercenaria     Menippidae        20-40 ([dagger])
  (Say, 1818)          Xanthoidea
Eurytium limosum       Panopeidae        20-32 ([dagger])
  (Say, 1818)          Xanthoidea
Panopeus herbstii      Panopeidae        20-31
  (H. Milne-Edwards,   Xanthoidea
Rhithropanopeus        Panopeidae        2.5-40
  harrisii (Gould,     Xanthoidea
Achelous (=Portunus)   Portunidae        30-40
  spinicarpus          Portunoidea
  (Stimpson, 1871)
Callinectes sapidus    Portunidae        20-31
  (Rathbun. 1896)      Portunoidea
Carcinus maenas        Portunidae        20-35 * ([dagger])
  (Linnaeus, 1758)     Portunoidea         ([double dagger])
Charybdis feriata      Portunidae        25-35
  (Linnaeus, 1758)     Portunoidea
Necora puber           Portunidae        30-35
  (Linnaeus, 1767)     Portunoidea
Scylla serrata         Portunidae        20-30
  (Forskal. 1775)      Portunoidea
Cancer irroralus       Cancridae         25-35 ([dagger])
  (Say, 1817)          Cancroidea
Metacarcinus           Cancridae         20-30 * ([dagger])
  (=Cancer) magister   Cancroidea
  (Dana, 1852)
Halicarcinus           Hymenosomatidae   6.4-19.3 ([dagger])
  rostratus            Majoidea
  (Haswell, 1882)
  (referred as
  H. australis)
Hymenosoma             Hymenosomatidae   21-42
  orbiculare           Majoidea
  (Desmarest, 1823)
Stenorhynchus          Inachidae         30-40 ([dagger])
  seticornis           Majoidea            ([double dagger])
  (Herbst., 1788)
Mithrax caribbaeus     Mithracidae       32-38 ([dagger])
  (Rathbun, 1920)      Majoidea            ([double dagger])
Mithrax                Mithracidae       30-35 ([dagger])
  pleuracanthus        Majoidea
  (Stimpson, 1871)
Mithrax verrucosus     Mithracidae       25-35
  (H. Milne-Edwards,   Majoidea
Chionoectes opilio     Oregoniidae       24-38 ([dagger])
  (O. Fabricius,       Majoidea
Hyas araneus           Oregoniidae       25-35 ([dagger])
  (Linnaeus, 1758)     Majoidea
Libinia emarginata     Pisidae           ~30 ([dagger])
  (Leach, 1815)        Majoidea
Maja brachydactyla     Majidae           30-40
  (Balss, 1922)        Majoidea

      Species                  Habitat                 References

Cardisoma armatum      Nearshore ([paragraph])   (Cuesta & Anger 2005)
  (Herklots, 1851)     Estuaries
Cardisoma guanhumi     Nearshore ([paragraph])   (Costlow & Bookhout
  (Latreille, 1828)    Estuaries                   1968)
Aratus pisonii (H.     Nearshore ([section])     (Diaz & Bevilacqua
  Milne Edwards,         ([paragraph])             1986)
  1837)                Estuaries ([section])
Pachygrapsus           Nearshore ([section])     (Brossi-Garcia &
  gracilis             Offshore ([section])        Rodrigues 1993)
  (Saussure, 1858)
Pachygrapsus           Nearshore ([section])     (Brossi-Garcia &
  transversus          Offshore ([section])        Rodrigues 1997)
  (Gibbes, 1850)
Armases (=Sesarma)     Rocky pools               (Anger et al. 2000)
  miersii (Rathbun,                              (Schuh & Diesel 1995)
Armases ricordi (H.    Nearshoref ([section])    (Diesel & Schuh 1998)
  Milne Edwards,         ([paragraph])
  1853)                Offshore ([section])
Armases roberti (H.    Nearshore ([section])     (Diesel & Schuh 1998)
  Milne Edwards,         ([paragraph])
  1853)                Estuaries  ([section])
Armases                Nearshore ([section])     (Luppi et al. 2003)
  (=Metasesarmu)         ([paragraph])
  rubripes (Rathbun,   Offshore ([section])
  1897)                  ([paragraph])
Selatium (=Sesarma)    Mangroves ([section])     (Kannupandi et al.
  brockii (De Man,                                 2000)
Sesarma cinereum       Nearshore ([section])     (Costlow et al. 1960)
  (Bosc, 1802)           ([paragraph])           (Seiple & Salmon 1987)
Sesarma curacaoense    Rocky pools               (Anger & Charmantier
 (De Man, 1982)                                    2000)
                       Mangroves                 (Diesel & Schuh 1998)
Acmaeopleuraparvula    Nearshore                 (Kim & Jang 1987)
  (Stimpson, 1858)     Offshore
Eriocheir sinensis     Nearshore ([paragraph])   (Anger 1991)
  (H. Milne Edwards,   Estuaries
Neohelice              Nearshore ([paragraph])   (Anger et al. 2008)
  (=Chasmagnathus)     Estuaries                 (Charmantier et al.
  granulata (Dana,                                 2002)
Pseudoheliee           Mangroves ([section])     (Mia & Shokita 2002)
  subquadrata (Dana,
  1851) (referred as
  Helice leachi)
Uca rapax (S. I.       Nearshore ([section])     (Simith et al. 2014)
  Smith, 1870)           ([paragraph])
                       Offshore ([section])
Uca subcylindrica      Rainfall puddles          (Rabalais & Cameron
  (Stimpson, 1859)                                 1985)
Uca tangeri (Eydoux    Nearshore ([section])     (Spivak & Cuesta 2009)
  1835)                 ([paragraph])
Uca vocator (J. F.     Nearshore ([section])     (Simith et al. 2012)
  W. Herbst, 1804)       ([paragraph])
                       Offshore ([section])
Menippe mercenaria     Nearshore                 (Ong & Costlow 1970)
  (Say, 1818)
Eurytium limosum       Estuaries ([section])     (Messerknecht et al.
  (Say, 1818)                                      1991)
Panopeus herbstii      Estuaries                 (Costlow Jr. et al.
  (H. Milne-Edwards,                               1962)
  1834)                                          (Dittel & Epifanio
Rhithropanopeus        Estuaries                 (Forward Jr. 2009)
  harrisii (Gould,
Achelous (=Portunus)   Nearshore                 (Bookhout & Costlow
  spinicarpus                                      Jr. 1974)
  (Stimpson, 1871)     Offshore                  (Brandao et al. 2015)
Callinectes sapidus    Nearshore ([paragraph])   (Costlow & Bookhout
  (Rathbun. 1896)                                  1959)
                       Estuaries                 (Epifanio 1995)
Carcinus maenas        Nearshore ([paragraph])   (Nagaraj 1993)
  (Linnaeus, 1758)     Estuaries
Charybdis feriata      Nearshore                 (Baylon & Suzuki 2007)
  (Linnaeus, 1758)     Estuaries                 (Fowler et al. 2011)
Necora puber           Nearshore                 (Choy 1991)
  (Linnaeus, 1767)     Offshore                  (Mene et al. 1991)
                                                 (Nagaraj 1992)
Scylla serrata         Nearshore                 (Dan & Hamasaki 2011)
  (Forskal. 1775)      Offshore
Cancer irroralus       Nearshore                 (Sastry 1970)
  (Say, 1817)          Offshore                  (Bigford 1979)
Metacarcinus           Nearshore                 (Reed 1969)
  (=Cancer) magister   Offshore
  (Dana, 1852)
Halicarcinus           Estuaries                 (Lucas & Hodgkin 1970)
  (Haswell, 1882)
  (referred as
  H. australis)
Hymenosoma             Estuaries                 (Papadopoulos et al.
  orbiculare           Nearshore                   2006)
  (Desmarest, 1823)
Stenorhynchus          Nearshore ([section])     (Hernandez et al.
  seticornis           Offshore ([section])        2012)
  (Herbst., 1788)
Mithrax caribbaeus     Nearshore                 (Larez et al. 2000)
  (Rathbun, 1920)      Offshore
Mithrax                Nearshore                 (Goy et al. 1981)
  pleuracanthus        Offshore
  (Stimpson, 1871)
Mithrax verrucosus     Nearshore                 (Rengel de Zambrano et
  (H. Milne-Edwards,   Offshore                    al. 1993)
Chionoectes opilio     Nearshore                 (Yamamoto et al. 2015)
  (O. Fabricius,       Offshore
Hyas araneus           Nearshore                 (Anger 1985)
  (Linnaeus, 1758)     Offshore
Libinia emarginata     Nearshore                 (Johns & Lang 1977)
  (Leach, 1815)        Offshore
Maja brachydactyla     Nearshore ([section])     Present study
  (Balss, 1922)        Offshore ([section])

Saline range suitable for the larval development from newly hatched
zoeae to first juvenile stage. The habitat of the larvae also was

* The data only comprise the saline range suitable for the larval
development from newly hatched zoeae to the megalopa stage,

([dagger]) Salinity higher than the highest suitable salinity was not

([double dagger]) Salinity lower than the lowest suitable salinity
was not tested.

([section]) The habitat of the larvae is extrapolated from
experimental data, confirmation with field data is required.

([paragraph]) The larvae migrate from the hatching habitat
(estuaries, mangroves, rivers or brackish waters) to nearshore and/or
offshore waters, i.e., "export strategy" (see Charmantier et al.
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Author:Castejon, Diego; Rotllant, Guiomar; Gimenez, Luis; Torres, Gabriela; Guerao, Guillermo
Publication:Journal of Shellfish Research
Article Type:Report
Date:Dec 1, 2015
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