Swimming between salt- en freshwater: osmoregulation in the bull shark
The bull shark (Carcharhinus leucas, also called Zambesi shark in Africa) is a large and stout shark, with females being larger (around (2-3 meters) than males. Along with the tiger and great white shark, bull sharks are among the three shark species most likely to bite humans. Shark bites in shallow water, sometimes ascribed to great whites, later appeared to come from bull sharks. Remarkably, the bull shark is one of the few species of Carcharhinus that occasionally swims into fresh, brackish, and shallow water of river deltas, estuaries, and lakes that connect with the sea.
Insert: Upper panel: schematical view of the organs of the shark involved in keeping a balance between osmolarity of body fluids and the environment. Lower panel: bull shark in saltwater Bahamas (picture taken with Olympus E-PL5 and 8mm lens, natural light)
Habitats The ability of bull sharks to tolerate freshwater could be rooted in competition for scarce saltwater food resources, where perhaps bull sharks suffered and needed to develop an edge. Giving them gradually the genetic advantage of access to a greater variety of fishes in freshwater regions, where other competitive predators sharks cannot enter. Females are thought to give birth to one to 13 pups in estuaries and river mouths, from where the young migrate and may remain far upstream for up to five years In freshwater they are free from predators, similar to baby lemon sharks that often seek safety in the shallow mangroves as nurseries. Bull sharks hunt on bony fish, small sharks, and stingrays. Their diet may include turtles, crustaceans and enichoderms. They also hunt in murky waters where it is harder for the prey to see the shark coming
Osmoregulatory mechanisms in the bull shark. The most abundant dissolved salts in seawater are sodium and chloride, magnesium, sulfate, and calcium: together around 36 gram per 1000 gram seawater. Seawater is thus denser than freshwater because the dissolved salts increase the mass by a larger proportion than the volume. The fluids inside and surrounding cells in the body of the shark are composed of water, electrolytes (mostly the salt particles in the body fluid or blood that produce ions, that is an electrical charge), and nonelectrolytes. In addition to chemical compounds such as sodium and chloride, the blood plasma of sharks also contains high concentrations of organic compounds such as urea and trimethylamine oxide (TMAO) to maintain the animal's isotonicity.
In marine sharks, the watery portion of blood, the plasma, has a concentration of salt and ions that is remarkably similar, and only slightly higher than that of seawater (see insert). In more technical terms, its osmolality (the concentration of dissolved particles of chemicals and minerals per liter) is about 1070mOsm/l (=number of particles per liter of solution). Osmoregulation (or: osmosis) is the process of maintaining salt and water balance (osmotic balance) across a semi-permeable membrane (mainly the gills) within the body fluids. This allows molecules of a solvent to pass through the membrane from a more concentrated solution into a less concentrated one. This principle (called: diffusion) is of vital importance in bull sharks resident in and migrating between fresh and saltwater. The challenge for these sharks is to maintain osmotic and ionic homeostasis. that is a constant hyperosmotic value (osmolality) of around >1000 mOsm/l relative to the external milieu, over a wide breadth of conditions.
Bull sharks possess several organs that are adapted to maintain appropriate salt and water balance; these are the rectal gland, kidneys, liver, and gills epithelium (see insert for a rough sketch). All elasmobranchs have a rectal gland that functions in the excretion of excess salts accumulated as a consequence of living in seawater. Marine and euryhaline elasmobranchs in saltwater reabsorb and retain urea and other body fluid solutes such that osmolarity remains hyper-osmotic to their surrounding seawater; consequently, they experience little or no osmotic loss of water. In contrast, euryhaline elasmobranchs in freshwater, balance osmotic water gain by increased urinary excretion. Overall, plasma osmolarity in freshwater-captured animals was significantly reduced compared to saltwater-captured animals, mostly caused by the decrease of sodium, chloride and urea, excreted by higher urine flow rates in freshwater sharks. They also synthesized less urea as well as retained less urea, Na, and Cl than marine individuals such that osmolarity remains relatively low but still greater than the surrounding freshwater. In sum, this implies that euryhaline bull sharks, acclimated to freshwater have urea and TMAO levels of about a half and one-third of their marine counterparts, respectively. In addition, they have sodium, chloride, and magnesium ion concentrations about 12, 13, and 15% of levels below marine species. (Pillans & Franklin, 2004).
Buoyancy Sharks in deep saltwater use the caudal fin and pectoral fins to generate vertical forces that balance the negative buoyancy. This, in turn, results in drag due to lift by the body and pectoral fins. Negative buoyancy is favorable for marine sharks traveling fast whereas neutral buoyancy provided by large oily livers, such as in the Greenland shark, favors lower travel speeds, as a result of decreasing costs of lift production at higher speeds. Bull sharks swimming in freshwater may experience a two- to three-fold increase in negative buoyancy as a result of decreasing water density. Liver size or density offers only limited compensation for increased negative buoyancy. Suggesting that increased negative buoyancy in freshwater bull sharks might be less of a handicap when swimming in the shallow murky water of rivers and estuaries.
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