Blue Crabs Is an Osmoregulator Most of the Time but Becomes a Conformer During a Moult
A comparative study of two sympatric species within the genus Callinectes: osmoregulation, long-term acclimation to salinity and the effects of salinity on growth and moulting
Abstract
Juvenile blue crabs, Callinectes sapidus Rathbun, and lesser blue crabs, C. similis Williams, were exposed to a range of salinities for 67 days to determine if salinity exerted species specific differential effects on growth and moulting. Growth was measured in terms of carapace width, wet weight, dry weight and ash-free dry weight. Growth rates of the two species (% increase in dry weight/day) were differentially affected by salinity. C. similis juveniles exposed to 5‰ grew significantly slower than those exposed to 10‰, with those at 30‰ exhibiting intermediate growth rates. Salinity had no effect on growth rates of C. sapidus by any measure of weight or carapace width. C. sapidus grew at faster rates than C. similis at low salinity as measured by wet and dry weight, and at all treatments as measured by carapace width. Growth per moult (wet weight) of C. similis was greater than that of C. sapidus. However, intermoult periods of C. similis were longer and exhibited a more pronounced effect of salinity than those of C. sapidus. Feeding rates and hemolymph osmolalities were measured at the beginning and end of the 67 day exposure period. Weight-adjusted feeding rate of C. sapidus increased significantly after 67 days exposure to low salinity, whereas that of C. similis decreased significantly. Each species exhibited a decline in hemolymph osmolality at low salinities by the end of the exposure period. In order to determine if either species exhibits an ontogenetic shift in ability to regulate hemolymph osmolality, juvenile and adult C. sapidus and C. similis were collected and exposed to a range of salinities for measurement of hemolymph osmolalities. These crabs were collected and exposed separately from those used in the 67 day exposure. Adult C. sapidus maintained higher hemolymph osmolalities than juveniles when exposed to low salinities (≤25‰). Hemolymph osmolalities of adult C. similis exposed to low salinity varied with salinity of collection site. Those from a high salinity site (30‰) exhibited hemolymph osmolalities no different than juveniles when exposed to salinities of 2.5 and 10‰. Those from a lower salinity site (22‰) exhibited greater hemolymph osmolalities than juveniles, osmoregulating at levels insignificantly different from adult C. sapidus. Results of this study indicate that although previously published studies may have overestimated the effects of low salinity on C. similis relative to it`s more euryhaline congener C. sapidus, effects of salinity alone are probably sufficient to limit this species' distribution to waters of 10‰ or greater.
Introduction
The blue crab Callinectes sapidus and the lesser blue crab C. similis are congeners existing sympatrically throughout the latter's geographic range, in coastal waters of North America from Delaware Bay to the Yucatan peninsula (Williams, 1974). The geographic range of C. sapidus extends further north to Nova Scotia, south to Argentina, and throughout the Caribbean islands. Additional records of C. sapidus from the Mediterranean and western European coasts are most likely due to larval introductions via ballast water in ships. C. sapidus and C. similis exhibit similar life cycles (Millikin and Williams, 1984; Hsueh et al., 1993). Egg-carrying females migrate to the mouth of estuaries to spawn, releasing larvae (zoeae) in high salinity waters. An offshore planktonic existence follows, consisting of 6–8 zoeal stages lasting a total of 1–1.5 months (Bookhout and Costlow, 1977, Millikin and Williams, 1984). Larvae metamorphose into megalopae and reinvade estuaries, and early crab stages feed in coastal marshes or begin migrating upstream to lower salinity waters.
While the species co-occur within estuaries, C. sapidus inhabits a wider range of salinities, has been reported in waters as low as 0‰ and generally prefers low salinity, whereas C. similis is usually restricted to waters above 15‰ (Williams, 1984Hsueh et al., 1993). Hsueh et al. (1993)report that C. similis inhabiting shallow, low salinity marshes were exclusively juveniles (≤40mm carapace width). Adult and sub-adult C. similis inhabited only higher salinity, open bay habitats of Mobile Bay. Our observations in the Port Fourchon, LA area agree with these findings, in that adult C. similis are never found inshore, whereas both juvenile and adult C. sapidus are common in shallow marshes.
The distributional pattern exhibited by C. sapidus and C. similis within estuaries of the southeastern United States is repeated by other members of the genus throughout their geographic range. Based on morphological and physiological characteristics, Norse and Fox-Norse (1982)have proposed evolutionary relationships within the genus Callinectes (Fig. 1). These proposed relationships place most members of the genus within two groups: the `danae' group, consisting of smaller, offshore dwelling species less tolerant of low salinity (including C. similis) and the `bocourti' group, consisting of larger, inshore dwelling species more tolerant of low salinity (including C. sapidus).
Engel (1977)and Piller et al. (1995)reported that adult C. sapidus were superior hyperosmoregulators to adult C. similis at 5‰. Guerin and Stickle (in press)and Hsueh et al. (1992a)demonstrated that C. sapidus is more tolerant of low salinity than C. similis, at both the juvenile and adult stage. These studies demonstrated, however, that C. similis can survive for extended periods in the laboratory at salinities below 15‰, suggesting that other factors such as competition and sub-lethal effects on growth may contribute to distributional differences observed within estuaries.
Salinity has been shown to affect scope for growth (energy accumulated for growth and reproduction) of juvenile C. sapidus and C. similis, with C. sapidus exhibiting highest scope for growth at 10–25‰ (Guerin and Stickle, 1992) and C. similis at 35‰ (Guerin and Stickle, in press). However, calculation of actual growth rates from short term studies is difficult due to the incremental growth pattern of crustaceans. The above bioenergetics experiments were carried out for 28 days, and many crabs moulted only once or not at all. Exposing crabs to a range of salinities over a longer time period allows calculation of growth rates, thus making it possible to determine if the scope for growth differences mentioned above are reflected by differences in actual growth.
Cadman and Weinstein (1988)concluded that the effect of temperature on growth of juvenile C. sapidus was greater than that of salinity. However, since salinity is considered to be the most important factor influencing distribution within estuaries and since we are investigating possible factors affecting distributional differences of C. similis and C. sapidus within an estuarine system, we chose to limit this study to an investigation of the effects of salinity alone (with all other environmental variables being maintained at constant levels). Still, it should be noted that growth rates at other latitudes or throughout the year may vary greatly from those reported here due to temperature differences, and this should be considered in all studies of growth.
In the present study, juvenile C. sapidus Rathbun and C. similis Williams were exposed to three salinities each for 67 days. Growth and moulting were monitored throughout the exposure period for calculation of growth rates in terms of carapace width, wet weight, dry weight and ash-free dry weight. Feeding and hemolymph osmolality were measured at the beginning and end of the study to determine if long term exposure could result in acclimation (i.e., do feeding or hemolymph osmolality recover with extended exposure to low salinities?). Separate measurements of hemolymph osmolalities of juvenile and adult C. sapidus and C. similis, exposed to a range of salinities, were also taken to determine if an ontogenetic shift may contribute to differences in distribution seen within and between the species.
Section snippets
Collection and maintenance
Juvenile C. sapidus and C. similis were collected in April 1992 and June 1993, respectively. All crabs were collected by dip net in the vicinity of the Louisiana Universities Marine Consortium (LUMCON) laboratory at Port Fourchon, LA, USA. Salinity at the time of collection was 25‰ for C. sapidus and 21‰ for C. similis. Carapace width of C. sapidus averaged 19.04 mm (range=12.50–27.50 mm), while that of C. similis averaged 29.83 mm (range=23.90–36.65mm). Juvenile crabs of these sizes are likely
Long term study – growth
Percent survival of C. sapidus in each treatment was 41 (2.5‰), 66 (10‰) and 75% (30‰). Percent survival of C. similis in each treatment was 39 (5‰), 26 (10‰) and 45% (30‰).
Two-way analysis of variance (species × salinity) revealed no significant effect of salinity on overall growth rate (% increase/day) of C. sapidus or C. similis over the 67 day period, as measured by carapace width or any measure of weight. However, the species × salinity interaction term was significant (p<0.05) for growth
Discussion
Our data show that salinity exerted a more pronounced effect on growth of juvenile C. similis than on juvenile C. sapidus. While growth (as measured by dry weight) of C. similis at 5‰ was roughly half that of crabs at 10‰, salinity had no effect on growth of C. sapidus as calculated by carapace width or any measure of weight (Fig. 2). Cadman and Weinstein (1988)reported a significant effect of salinity on growth of juvenile C. sapidus averaged over five temperature treatments, but this effect
Acknowledgements
We thank Dr. J. Fleeger, Dr. K. Brown, Dr. D. Foltz and Dr. J. Siebenaller for their editorial comments and advice. Instruction from Dr. S. Wang and Dr. S. Sarver in techniques and procedures required for this experiment is greatly appreciated. We also thank P. Culley, Dr. P. Rutledge and Dr. M. Hollay for their help with statistical analyses. The following people were invaluable in aiding with sample collections of adult C. similis: R. Burns at the Gulf Coast Research Laboratory, R. Allemand
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Since osmoregulation and growth are both processes that require energy (Schmidt-Nielsen, 1997), osmoregulation will affect the energy budget of aquatic organisms (Mu et al., 2005; Hulathduwa et al., 2007; Urbina et al., 2010) and ultimately might determine the energy available for growth (Urbina and Glover, 2015). For example crabs and shrimps exposed to suboptimal salinities present an increase in the production of ammonia (Rosas et al., 1999, 2002; Urbina et al., 2010), as well as an increase in metabolic rate (Aguilar et al., 1998; Urbina et al., 2010), which leads to an alteration in their growth potential (Guerin and Stickle, 1997a, 1997b; Gillikin et al., 2004; Urbina et al., 2010). Crustaceans are one of the marine invertebrate taxa that are able to inhabit coastal regions and tidal estuaries across the globe, and are thus able to occupy habitats with low and/or fluctuating salinities (Anger, 1995; Charmantier and Anger, 2011).
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Most marine species are essentially isosmotic with their surrounding medium and are osmoconformers, not supporting strong fluctuations or lengthy exposure to dilute media [28,33–37]. In contrast, hyperosmoregulating crustaceans ably confront osmotic challenge, maintaining hemolymph osmolality fairly constant and well above that of dilute media [28,34–36,38–40]. When hyperosmoregulating crabs are exposed to dilute media, (Na+, K+)-ATPase activity in the posterior gill epithelia quickly increases [28,33–35,40–42].
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Euryhaline crustaceans like brachyuran crabs adjust to ambient salinity changes employing an efficient ensemble of posterior gill ion transporters that maintains hemolymph osmolality and ion concentrations within a range compatible with normal cell function. Callinectes danae Smith 1869 is a hyperosmoregulating euryhaline swimming crab that inhabits a wide range of ambient salinities and is distributed from Florida, USA to southern Brazil [23,24]. The crabs occur on silt/sand substrates and migrate freely among water masses of moderate salinity (28 to 35‰), often impacted by freshwater runoff during the rainy southern summer [25].
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Upon the salinity challenge offered here, the two species behaved essentially the same in their extracellular fluid (ECF) homeostasis of osmolality and chloride. The hemolymph dilution noted when the two crabs were submitted to low salinity (Ho) was also very similar to that shown by Callinectes sapidus and C. similis, also ~ 600–700 mOsm/kg H2O when in dilute SW of salinity 10‰ for 14–67 days (Piller et al., 1995; Guerin and Stickle, 1997). It is important to highlight that, despite this hemolymph dilution, all these crabs remain significantly hyper-osmotic to the water of salinity ~ 10‰ (~ 300 mOsm/kg H2O).
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