Osmoregulation in elasmobranchs: a review for fish biologists, behaviourists and ecologists
01 Sep 2006-Marine and Freshwater Behaviour and Physiology (Taylor & Francis Group)-Vol. 39, Iss: 3, pp 209-228
TL;DR: A broad review of osmoregulation in elasmobranchs for non-specialists, focusing on recent advances, is provided, highlighting the contribution of drinking and eating processes in maintaining osmotic consistency.
Abstract: This article provides a broad review of osmoregulation in elasmobranchs for non-specialists, focusing on recent advances. Marine and euryhaline elasmobranchs in seawater regulate urea and other body fluid solutes (trimethylamine oxide (TMAO), Na+, Cl−) such that they remain hyper-osmotic to their environment. Salt secretions of the rectal gland and excretions in the urine compensate for continuous inward diffusion of environmental salts. Freshwater and euryhaline elasmobranchs in fresh water synthesise less urea and retain less urea and other body fluid solutes compared to marine elasmobranchs and thus have relatively lower osmolarity. Electrolyte uptake at the gills and kidney reabsorption of salts maintain acid–base balance and ionic consistency. The role of the gills, kidney, liver and rectal gland in elasmobranch osmoregulation is reviewed. The ontogeny of osmoregulatory systems in elasmobranchs and the contribution of drinking and eating processes in maintaining osmotic consistency are discussed. Rec...
Citations
More filters
TL;DR: Nitrogen stable isotope values of skate blood and skate and dogfish white muscle were not affected by tissue urea content, suggesting that available diet–tissue discrimination estimates for teleost fishes with similar physiologies would provide accurate estimates for elasmobranchs.
Abstract: Carbon and nitrogen stable isotope analyses have improved our understanding of food webs and movement patterns of aquatic organisms. These techniques have recently been applied to diet studies of elasmobranch fishes, but isotope turnover rates and isotope diet-tissue discrimination are still poorly understood for this group. We performed a diet switch experiment on captive sandbar sharks (Carcharhinus plumbeus) as a model shark species to determine tissue turnover rates for liver, whole blood, and white muscle. In a second experiment, we subjected captive coastal skates (Leucoraja spp.) to serial salinity reductions to measure possible impacts of tissue urea content on nitrogen stable isotope values. We extracted urea from spiny dogfish (Squalus acanthias) white muscle to test for effects on nitrogen stable isotopes. Isotope turnover was slow for shark tissues and similar to previously published estimates for stingrays and teleost fishes with low growth rates. Muscle isotope data would likely fail to capture seasonal migrations or diet switches in sharks, while liver and whole blood would more closely reflect shorter term movement or shifts in diet. Nitrogen stable isotope values of skate blood and skate and dogfish white muscle were not affected by tissue urea content, suggesting that available diet-tissue discrimination estimates for teleost fishes with similar physiologies would provide accurate estimates for elasmobranchs.
175 citations
Cites background from "Osmoregulation in elasmobranchs: a ..."
...Isotope turnover rates thus appear to be similar for two elasmobranch species with differing life history strategies and tissue urea retentions (Hammerschlag, 2006), but similarly low growth rates (Casey et al., 1985; MacNeil et al., 2006)....
[...]
...Nitrogen isotope ratios in animal tissues increase with trophic position due to the preferential excretion of 14N as nitrogenous waste (Steele & Daniel, 1978), but elasmobranch fishes retain urea in their tissues to osmoregulate (Smith, 1929, 1936; Karnaky, 1998; Hammerschlag, 2006)....
[...]
...Isotope turnover rates thus appear to be similar for two elasmobranch species with differing life history strategies and tissue urea retentions (Hammerschlag, 2006), but similarly low growth rates (Casey et al....
[...]
...Nitrogen isotope ratios in animal tissues increase with trophic position due to the preferential excretion of (14)N as nitrogenous waste (Steele & Daniel, 1978), but elasmobranch fishes retain urea in their tissues to osmoregulate (Smith, 1929, 1936; Karnaky, 1998; Hammerschlag, 2006)....
[...]
TL;DR: It is indicated that urea affects isotope ratios and that water treatment removes urea without altering muscle protein composition, and this study begins to address the need for elasmobranch-specific methods.
Abstract: Stable isotope analysis has the potential to expand our understanding of elasmobranch ecology. However, elasmobranchs share unique traits (i.e., retention of urea, lack of adipose tissue, cartilaginous skeletons) that require modified preparation techniques. Alternative tissue collection and preservation methods would allow sampling from ichthyology collections and at remote locations. We compared different collection, preservation, and preparation techniques to identify treatments that yielded robust isotopic data. Blood components collected in tubes coated with lithium heparin (an anti-coagulant) were not isotopically distinct from blood collected in no-additive tubes. Compared to frozen muscle, ethanol-treated muscle had altered δ13C values, but similar δ15N values. Finally, we removed lipids and urea with petroleum ether and deionized water, respectively. Although untreated and treated muscle had similar amino acid compositions, treated muscle preferentially lost 14N and had greater C:N ratios. These results indicate that urea affects isotope ratios and that water treatment removes urea without altering muscle protein composition. Although not exhaustive, our study begins to address the need for elasmobranch-specific methods.
148 citations
Cites background from "Osmoregulation in elasmobranchs: a ..."
...The concentrations of urea and TMAO in body tissues fluctuate depending on ambient salinity (Ballantyne 1997; reviewed by Hazon et al. 2007; reviewed by Hammerschlag 2006; Wood et al. 2007)....
[...]
TL;DR: Mechanisms used by hagfishes, lampreys, elasmobranchs, and teleosts to maintain ionic and osmotic homeostasis in changing environmental salinity are summarized.
Abstract: Euryhaline fishes live in a wide salinity range from freshwater to seawater and hypersaline environments. Euryhaline fishes such as salmon, eels, and tilapia are economically important in worldwide fisheries and aquaculture. This chapter summarizes mechanisms used by hagfishes, lampreys, elasmobranchs, and teleosts to maintain ionic and osmotic homeostasis in changing environmental salinity. Hyperosmoregulation in dilute environments uses gills for active ion uptake, intestine for dietary ion uptake, and kidneys for renal uptake. Extrarenal NaCl uptake occurs via high-affinity uptake mechanisms or low-affinity Na+/Cl− cotransport. In seawater, hypoosmoregulation involves reflexive drinking, intestinal absorption of salts and water, NaCl secretion at the gills, and renal ion excretion. Na+ and Cl− excretion occurs through Na+/K+-ATPase, the Na+/K+/2Cl− cotransporter, and apical cystic fibrosis transmembrane conductance regulator. These mechanisms are magnified in hypersaline conditions. Active extrarenal salt transport takes place through mitochondrion-rich ionocytes in skin and gill epithelia. The mechanisms of ion and water transport are summarized, with models presented for seawater, marine, and euryhaline conditions.
123 citations
TL;DR: The roles of the thyroid axis in fish and its contributions to growth and development, metamorphosis, reproduction, osmoregulation, as well as feeding and nutrient metabolism are discussed.
Abstract: In all vertebrates, the thyroid axis is an endocrine feedback system that affects growth, differentiation, and reproduction, by sensing and translating central and peripheral signals to maintain homeostasis and a proper thyroidal set-point. Fish, the most diverse group of vertebrates, rely on this system for somatic growth, metamorphosis, reproductive events, and the ability to tolerate changing environments. The vast majority of the research on the thyroid axis pertains to mammals, in particular rodents, and although some progress has been made to understand the role of this endocrine axis in non-mammalian vertebrates, including amphibians and teleost fish, major gaps in our knowledge remain regarding other groups, such as elasmobranchs and cyclostomes. In this review, we discuss the roles of the thyroid axis in fish and its contributions to growth and development, metamorphosis, reproduction, osmoregulation, as well as feeding and nutrient metabolism. We also discuss how thyroid hormones have been/can be used in aquaculture, and potential threats to the thyroid system in this regard.
83 citations
TL;DR: Model predictions for small, medium, and large wild leopard sharks indicate the time to isotopic equilibrium is from one to several years, which dif- fers from most reports for young marine teleosts.
Abstract: There are very few studies reporting isotopic trophic discrimination factors and turnover rates for marine elasmobranchs. A controlled laboratory experiment was conducted to estimate carbon and nit...
80 citations
References
More filters
TL;DR: The fish gill is a multipurpose organ that, in addition to providing for aquatic gas exchange, plays dominant roles in osmotic and ionic regulation, acid-base regulation, and excretion of nitrogenous wastes.
Abstract: The fish gill is a multipurpose organ that, in addition to providing for aquatic gas exchange, plays dominant roles in osmotic and ionic regulation, acid-base regulation, and excretion of nitrogenous wastes Thus, despite the fact that all fish groups have functional kidneys, the gill epithelium is the site of many processes that are mediated by renal epithelia in terrestrial vertebrates Indeed, many of the pathways that mediate these processes in mammalian renal epithelial are expressed in the gill, and many of the extrinsic and intrinsic modulators of these processes are also found in fish endocrine tissues and the gill itself The basic patterns of gill physiology were outlined over a half century ago, but modern immunological and molecular techniques are bringing new insights into this complicated system Nevertheless, substantial questions about the evolution of these mechanisms and control remain
2,371 citations
"Osmoregulation in elasmobranchs: a ..." refers background or result in this paper
...Marine teleosts drink to maintain ionic and water balance, with excess ions being excreted (reviewed by Evans 1993 and Evans et al. 2005)....
[...]
...This is in contrast to teleosts, which principally use only sodium and chloride ions to maintain osmotic consistency through functions of the gill, kidney and by drinking processes (sees reviews by Evans 1993 and Evans et al. 2005)....
[...]
...Although there have been several recent reviews of elasmobranch osmoregulation (Hazon et al. 2003; Evans et al. 2004, 2005), these have restricted focus to selected aspects of osmoregulation and tended to be highly technical....
[...]
...…across the apical membrane is lowered by active transport of intracellular urea across the basolateral membrane via a Naþ: urea antiporter, energised by the continual removal of Naþ from the gill via basolateral Naþ, Kþ-ATPases (Fines et al. 2001; reviewed by Wilkie 2002 and Evans et al. 2005)....
[...]
...…gill is involved with salt ion uptake and acid–base balance, particularly important for maintaining ionic homeostasis in a freshwater environment (Perry 1997; Wilson et al. 1997; Piermarini and Evans 2000; Piermarini et al. 2002; Wood et al. 2002; Evans et al. 2005; Tresguerrers et al. 2005)....
[...]
Book•
21 Jun 1984
TL;DR: This volume discusses water-Solute Adaptations: The Evolution and Regulation of the Internal Milieu, and the influence of Oxygen Availability on the Diving Response and Its Evolution.
Abstract: 1. The Goals and Scope of This Volume 2. Cellular Metabolism, Regulation, and Homeostasis 3. Influence of Oxygen Availability 4. The Diving Response and Its Evolution 5. Human Hypoxia Tolerance 6. Water-Solute Adaptations: The Evolution and Regulation of the Internal Milieu 7. Temperature
1,831 citations
"Osmoregulation in elasmobranchs: a ..." refers background in this paper
...Intracellular concentrations of TMAO approach 200 mM, approximately 50% of urea levels, a ratio that is generally consistent in most elasmobranchs (Hochachka and Somero 2002)....
[...]
TL;DR: In this article, the authors discuss the effects of stress on the human body, including muscle plasticity, muscle strength, and endocrine function, as well as the role of stress in these processes.
Abstract: Muscle Plasticity Grant B. McClelland and Graham R. Scott Cardiovascular System A. Kurt Gamperl and Holly A. Shiels Membranes and Metabolism James S. Ballantyne Oxygen Sensing Michael G. Jonz Intestinal Transport Martin Grosell Gill Ionic Transport, Acid-Base Regulation, and Nitrogen Excretion Pung-Pung Hwang and Li-Yih Lin Endocrine Disruption Heather J. Hamlin Thermal Stress Suzanne Currie and Patricia M. Schulte Physiology of Social Stress in Fishes Christina Sorensen, Ida Beitnes Johansen, and Oyvind Overli Pain Perception Victoria A. Braithwaite Chemoreception Warren W. Green and Barbara S. Zielinski Active Electroreception Signals, Sensing, and Behavior John E. Lewis Cardiac Regeneration Viravuth P. Yin Neuronal Regeneration Ruxandra F. Sirbulescu and Gunther K.H. Zupanc
1,400 citations
TL;DR: The regulation of specific Na pump isozymes gives cells the ability to precisely coordinate Na-K-ATPase activity to their physiological requirements.
Abstract: The Na-K-ATPase is characterized by a complex molecular heterogeneity that results from the expression and differential association of multiple isoforms of both its α- and β-subunits. At present, a...
1,150 citations
TL;DR: Under certain conditions that challenge ion regulation, chloride cells proliferate on the lamellae, which causes a thickening of the blood-to-water diffusion barrier and thus impedes respiratory gas transfer.
Abstract: This review focuses on the structure and function of the branchial chloride cell in freshwater fishes. The mitochondria-rich chloride cell is believed to be the principal site of trans-epithelial Ca2+ and Cl- influxes. Though currently debated, there is accruing evidence that the pavement cell is the site of Na+ uptake via channels linked electrically to an apical membrane vacuolar H(+)-ATPase (proton pump). Chloride cells perform an integral role in acid-base regulation. During conditions of alkalosis, the surface area of exposed chloride cells is increased, which serves to enhance base equivalent excretion as the rate of Cl-/HCO3- exchange is increased. Conversely, during acidosis, the chloride cell surface area is diminished by an expansion of the adjacent pavement cells. This response reduces the number of functional Cl-/HCO3- exchangers. Under certain conditions that challenge ion regulation, chloride cells proliferate on the lamellae. This response, while optimizing the Ca2+ and Cl- transport capacity of the gill, causes a thickening of the blood-to-water diffusion barrier and thus impedes respiratory gas transfer.
543 citations