Homeostasis: Osmoregulation in elasmobranchs The difference between marine, eurahyline and fresh water species

Osmoregulation The environment the organism lives in Isotonic? Relationship between solute to solvent concentrations of internal body fluids The environment the organism lives in Isotonic? Hypertonic? Hypotonic? Osmolarity = solute/solvent concentration

semipermeable membrane between two compartments water molecules protein molecules semipermeable membrane between two compartments Fig. 5-20, p.86

1 liter of distilled water 2% sucrose solution 1 liter of 10% sucrose solution 1 liter of 2% sucrose solution 1 liter of distilled water Hypotonic Conditions Hypertonic Conditions Isotonic Conditions Fig. 5-21, p.87

hypotonic solution hypertonic solution first compartment second compartment hypotonic solution hypertonic solution membrane permeable to water but not to solutions fluid volume rises in second compartment Fig. 5-22, p.87

water but not to solutes Hypotonic Solution membrane permeable to water but not to solutes Hypertonic Stepped Art Fig. 5-22, p.87

The Challenge Avoid desiccation in an aqueous environment MARINE ANIMALS Dehydration Elimination of excess salt FRESHWATER ANIMALS Conserve salts Eliminate excess water Elasmo blood and other bodily fluids separated from the surrounding environment by permeable surfaces. Marine animals face problems of dehydration and the elimination of excess salts Freshwater animals must conserve their salts and eliminate excess water.

Environmental challenges of elasmobranchs All ureotelic and ureosmotic except potamytrygonid rays Marine elasmobranchs surrounded by salt; lose water; need to get rid of excess organic and inorganic compounds Euryhaline species environment fluctuates Must handle salt and fresh conditions Freshwater species lose salt and electrolytes; need to get rid of excess water

Dealing with Environment Marine : Maintain serum osmolarity = or greater than seawater primarily w/ urea Little osmotic loss of water Dilute Seawater or Freshwater: Serum osmolarity reduced Little diffusion of water inward

Players in osmoregulation Organs Kidney, liver, gills, rectal gland Organic compounds Urea TMAO trimethylamine oxide Inorganic ions Sodium Chloride Other salts

Umanitoba - Gary Anderson

Body Fluid Marine Elasmobranchs Reabsorb & retain urea and other body fluid solutes in tissues Serum osmolarity remains just greater than external seawater (hyperosmotic) Don’t have to drink water like teleosts Water gained excreted by kidneys Marine elasmos evolved technique of reabsorbing and retaining urea & other body fluid solutes in tissues so serum osmolarity (solute/solvent concentration) remains just greater than external seawater. \ This reduces need to continuously drink seawater like teleosts do. Tri-MethylAmine Oxide (TMAO): Acts to counteract the perturbing effects of urea

Marine elasmobranchs Plasma solutes and osmoregulation Different than marine teleosts Have high osmolarity Reabsorb and retain high levels of urea and TMAO in their body fluids Osmolarity remains hyperosmotic to surrounding seawater TMAO to stabilize proteins and activate enzymes Water gained across gills is excreted by kidneys Any salt gained across gills is excreted by rectal gland and kidney

Body fluid of euryhaline elasmobranchs Ammonotelic in frehwater As salinity increases Increase urea production and retention Decrease urea excretion Increase Na+ and Cl- Decrease ammonia excretion Can not produce and retain as much urea as marine spp. (lower osmolarity) Ex. D. sabina and H. signifier

Body fluid of euryhaline elasmobranchs As salinity decreases Lower osmolarity (less urea and TMAO) than marine species Decrease amount of urea produced and reabsorbed Increased urinary excretion Loss of sodium and chloride balanced by electrolyte uptake at the gills and reabsorbed by kidneys

Bull Shark - Carcharhinus leucas Eeigen Werk

Body Fluid Fresh Water Elasmobranchs Lost ability to synthesize and retain urea or TMAO Body fluid solute concentrations relatively low Freshwater rays abandoned renal reabsorption Urine is dilute Ammonotelic Ex. Potamotrygon rays

Potamotrygonidae Raimond Spekking

Urea- production, retention and reabsorption Occurs in the liver Retention In gills Reabsorption In kidneys

Urea production in liver Ornithine-urea cycle (OUC) Glutamine synthetase is crucial enzyme needed for urea production Euryhaline spp. decrease production of urea when entering fresh water Freshwater rays lack the enzyme for the biosynthesis to occur Unsure if urea is produced in other locations Bacteria hypothesized for being responsible

Marine gills retain urea Do not lose much urea across gills Gill’s basolateral membrane has high cholesterol to phospholipid ratio levels Membrane limit diffusion Active transport of urea by Na+/ urea antiporter energized by Na+/K+ ATPases Used more for salt regulation and acid/base balance

Kidneys reabsorb urea Reabsorption contributes to high urea levels Minor site of urea loss Thought to involve active transport Use urea-sodium pump Proven in R. erinacea Second hypothesis for passive transport that has not been proven Euryhaline spp. decrease renal reabsorption of urea as enter areas of decreased salinity Increases rate of urine flow to rid system of excess urea

Salt regulation Rectal gland secretions Marine spp. surrounded by high salinity Rectal gland secretes sodium and chloride Na+/ K+ ATPases used

Osmoregulation by the Rectal Gland Rectal Gland = Salt secreting mechanism Migratory elasmos - regressive rectal gland Non-functional in freshwater rays Rectal Gland - epithelial tissue gland - concentrates & secretes excess Na & Cl in sharks. large shark liver produces copious amounts of urea, making the shark hyperosmotic to seawater, & thus a shark acts like a fresh water fish, constantly gaining water. Excess salts are concentrated by the rectal gland and secreted. Marine; diffusion of salts into the body from seawater… rectal gland secretion Freshwater movement…rectal gland becomes regressive or non-functional as in fresheater rays Potamotrygon http://fig.cox.miami.edu/~cmallery/150/physiol/rectal.htm

Salt regulation Gills Salt uptake Acid/ base balance Na+/ K+ ATPases even higher in freshwater Acid/ base balance Secrete acid H+ excreted/exchanged for Na+ Run by Na+/ K+ ATPases Responsible for ammmonia secretion

Salt regulation Kidney salt excretion Dilute environment Saltwater Urine flow increase Saltwater Not solely responsible for salt secretion

Endocrine Regulation to Regulate Body Fluid Volume and Solute Concentration CNP - Released from heart Increase urine production Stimulate salt secretion from rectal gland Inhibit drinking and relax blood vessels AVT Increase in plasma osmolality Reduces urine production RAS Antagonistic to CNP, reduces urine flow Increases drinking Constricts blood vessels Three key agents involved in regulation of body fluid volume and solute concdentration Natriuretic peptide system (NP) Neurohypophysial peptide arginine vasotocin (AVT), Renin Angiotensin system (RAS)

Feeding and osmoregulation Urea is metabolically expensive 5 umol ATP for 1 mole urea Protein in food is main source of N in urea Elasmobranches must get adequate food to produce the urea Why ureotelic and not ammonotelic???

Literture cited Hammerschlag N.2006. Osmoregulation in elasmobranches: a review for fish biologists, behaviorists and ecologists. MARINE AND FRESHWATER BEHAVIOUR AND PHYSIOLOGY 39 (3): 209-228 Speers-Roesch B, Ip YK, Ballantyne JS.2006. Metabolic organization of freshwater, euryhaline, and marine elasmobraches: implications for the evolution of energy metabolism in sharks and rays. JOURNAL OF EXPERIMENTAL BIOLOGY 209 (13): 2495- 2508 Pillans RD, Anderson WG, Good JP, et al.2006. Plasma and erythrocyte solute properties of juvenile bull sharks, Carcharhinus leucas, acutely exposed to increasing environmental salinity. JOURNAL OF EXPERIMENTAL MARINE BIOLOGY AND ECOLOGY 331 (2): 145-157 Pillans RD, Good JP, Anderson WG, et al. 2005.Freshwater to seawater acclimation of juvenile bull sharks (Carcharhinus leucas): plasma osmolytes and Na+/K+ ATPase activity in gill, rectal gland, kidney and intestine. JOURNAL OF COMPARATIVE PHYSIOLOGY B-BIOCHEMICAL SYSTEMIC AND ENVIRONMENTAL PHYSIOLOGY 175 (1): 37-44

Literature cited Pillans RD, Franklin CE.2004. Plasma osmolyte concentrations and rectal gland mass of bull sharks Carcharhinus leucas, captured along a salinity gradient. COMPARATIVE BIOCHEMISTRY AND PHYSIOLOGY A- MOLECULAR & INTEGRATIVE PHYSIOLOGY 138 (3): 363-