Abstract
Marine flatfishes have a low metabolic rate and routinely encounter large fluctuations in salinity, and are therefore of interest in the study of diffusive water flux (a proxy for transcellular water permeability), oxygen consumption (ṀO2), ammonia excretion and urea-N excretion as a function of salinity and seawater [Ca2+]. These parameters were measured in two coastal marine flatfishes, Pacific sanddab and Rock sole acclimated to 31 ppt and exposed acutely (for up to 3 h), to environmentally relevant salinities of 45, 15.5, or 7.5 ppt. In both species, diffusive water flux and ammonia excretion rates increased as salinity decreased. ṀO2 and urea-N excretion rates remained relatively unchanged. Nitrogen quotient analysis indicated increased oxidation of protein at lower salinity. A second experimental series was performed on Rock sole to separate the effects of salinity from those of ambient [Ca2+]. In direct contrast to the significant increase seen at 7.5 ppt, reducing salinity from 31 ppt to 7.5 ppt while maintaining [Ca2+] at 10 mM or increasing it to 20 mM resulted in no change in diffusive water flux rate, demonstrating that reduced [Ca2+], rather than reduced salinity itself, is the primary cause for the increases in diffusive water flux. However, ammonia excretion rate increased when salinity was decreased and [Ca2+] was increased compared to 31 ppt with added [Ca2+]. Our results demonstrate that both diffusive water flux and ammonia excretion rates are a function of salinity, that neither are coupled to ṀO2, and that ambient [Ca2+] also plays a role in these rates.
Similar content being viewed by others
Data availability
Data are available upon request.
Code availability
Not applicable.
References
Abookire AA, Piatt JF, Robards MD (2000) Nearshore fish distributions in an Alaskan estuary in relation to stratification, temperature and salinity. Estuar Coast Shelf Sci 51(1):45–59. https://doi.org/10.1006/ecss.1999.0615
Alsop DH, Wood CM (1997) The interactive effects of feeding and exercise on oxygen consumption, swimming performance and protein usage in juvenile rainbow trout. J Exp Biol 200:2337–2346. https://doi.org/10.1242/jeb.200.17.2337
Alsop D, McGeer JC, McDonald DG, Wood CM (1999) Costs of chronic waterborne zinc exposure and the consequences of zinc acclimation on gill/zinc interactions of rainbow trout in hard and soft water. Environ Toxicol Chem 224:1014–1025
Altinok I, Grizzle J (2004) Excretion of ammonia and urea by phylogenetically diverse fish in low salinities. Aquaculture 238:499–507. https://doi.org/10.1016/j.aquaculture.2004.06.020
Armor C, Herrgesell PL (1985) Distribution and abundance of fishes in the San Francisco Bay estuary between 1980 and 1982. Hydrobiologia 129:211–227. https://doi.org/10.1007/BF00048696
Barton M, Barton AC (1987) Effects of salinity on oxygen consumption of Cyprinodon variegatus. Copeia 1:230–232. https://doi.org/10.2307/1446062
Beaudreau AH, Bergstrom CA, Whitney EJ, Duncan DH, Lundstrom NC (2022) Seasonal and interannual variation in high-latitude estuarine fish community structure along a glacial to nonglacial watershed gradient in South East Alaska. Environ Biol Fish 105:431–452. https://doi.org/10.1007/s10641-022-01241-9
Bottom DL, Jones KK, Herring MJ (1984) Fishes of the Columbia River estuary. Oregon Department of Fish and Wildlife, Columbia River Estuary Data Development Program, Corvallis, Oregon. https://docs.streamnetlibrary.org/StreamNet_References/sn68.pdf.
Boutilier RG, Heming TA, Iwama GK (1984) Appendix: Physicochemical parameters for use in fish respiratory physiology. In: Hoar WS (ed) Fish Physiology: Gills-Anatomy Gas Transfer and Acid-Base Regulation. Academic Press, London
Brett JR, Zala CA (1975) Daily pattern of nitrogen excretion and oxygen consumption of sockeye salmon (Oncorhynchus nerka) under controlled conditions. J Fish Res Bd Can 32:2479–2486. https://doi.org/10.1139/F75-285
Breves JP, Inokuchi M, Yamaguchi Y, Seale AP, Hunt BL, Watanabe S, Lerner DT, Kaneko T, Grau GE (2016) Hormonal regulation of aquaporin 3: opposing actions of prolactin and cortisol in tilapia gill. J Endocrinol 230:325–337. https://doi.org/10.1530/JOE-16-0162
Bucking C (2017) A broader look at ammonia production, excretion, and transport in fish: a review of impacts of feeding and the environment. J Comp Physiol B 187(1):1–18. https://doi.org/10.1007/s00360-016-1026-9
Burke JS, Miller JS, Hoss DE (1991) Immigration and settlement pattern of Paralichthys dentatus and P. lethostigma in an estuarine nursery ground, North Carolina, USA. Neth J Sea Res 27:393–405. https://doi.org/10.1016/0077-7579(91)90041-X
Cameron JN, Heisler N (1983) Studies of ammonia in the rainbow trout: physico-chemical parameters, acid-base behaviour and respiratory clearance. J Exp Biol 105(1):107–125. https://doi.org/10.1242/jeb.105.1.107
Cao Q, Gershunov A, Shulgina T, Ralph FM, Sun N, Lettenmaier DP (2020) Floods due to atmospheric rivers along the US west coast: The role of antecedent soil moisture in a warming climate. J Hydrometeorol 21(8):1827–1845. https://doi.org/10.1175/JHM-D-19-0242.1
Cerdà J, Finn RN (2010) Piscine aquaporins: an overview of recent advances. J Exp Zool 313A:623–650. https://doi.org/10.1002/jez.634
Chen LM, Zhao J, Musa-Aziz R, Pelletier MF, Drummond IA, Boron WF (2010) Cloning and characterization of zebrafish homologue of human AQP1: a bifunctional water and gas channel. Am J Regul Integr Comp Physiol 299(5):R1163–R1174. https://doi.org/10.1152/ajpregu.00319.2010
Cheng L, Trenberth KE, Gruber N, Abraham JP, Fasullo J, Li G, Mann ME, Zhao X, Jiang Z (2020) Improved estimates of changes in upper ocean salinity and the hydrological cycle. J Clim 33(23):10357–10381. https://doi.org/10.1175/JCLI-D-20-0366.1
Clarke A, Johnston NM (1999) Scaling of metabolic rate with body mass and temperature in teleost fish. J Anim Ecol 68:893–905. https://doi.org/10.1046/j.1365-2656.1999.00337.x
Connors DN, Kester DR (1974) Effect of major ion variations in the marine environment on the specific gravity-conductivity-chlorinity-salinity relationship. Mar Chem 2(4):301–314. https://doi.org/10.1016/0304-4203(74)90023-1
Cruz LR, Santos LN, Santos AF (2018) Changes of fish trophic guilds in Araruama Lagoon, Brazil: What can be inferred about functioning and structure of hypersaline lagoons? Estuar Coast Shelf Sci 211:90–99. https://doi.org/10.1016/j.ecss.2017.11.024
Cutler CP, Martinez AS, Cramb G (2007) The role of aquaporin 3 in teleost fish. Comp Biochem Physiol A 148:82–91. https://doi.org/10.1016/j.cbpa.2006.09.022
Dalla Via J, Thillart G, Cattani O, Cortesi P (1997) Environmental versus functional hypoxia/anoxia in sole Solea seola: the lactate paradox revisited. Mar Ecol Prog Ser 154:79–90. https://doi.org/10.3354/MEPS154079
Dalla Via J, Villani P, Gasteiger E, Niederstätter H (1998) Oxygen consumption in sea bass fingerling Dicentrarchus labrax exposed to acute salinity and temperature changes: metabolic basis for maximum stocking density estimations. Aquaculture 169:303–313. https://doi.org/10.1016/S0044-8486(98)00375-5
Driedzic WR, Hochachka PW (1978) Metabolism in fish during exercise. In: Hoar WS, Randall DJ (eds) Fish physiology. Academic Press, New York
Durkin JT, Coley TC, Verner K, Emmett RL (1981) An evaluation of aquatic life found at four hydraulic scour sites in the Colombia River estuary selected for potential sediment deposition. In Proceedings of the National Symposium on Freshwater Inflow to Estuaries Fish and Wildlife Service.
Duthie GG (1982) The respiratory metabolism of temperature-adapted flatfish at rest and during swimming activity and the use of anaerobic metabolism at moderate swimming speeds. J Exp Biol 97:359–373. https://doi.org/10.1242/jeb.97.1.359
Essington TE, Dodd K, Quinn TP (2013) Shifts in the estuarine demersal fish community after a fishery closure in Puget Sound. Washington Fish Bull 111:205–217
Evans DH (1969) Studies on the permeability to water of selected marine, freshwater and euryhaline teleosts. J Exp Biol 50:689–703. https://doi.org/10.1242/jeb.50.3.689
Evans DH (1984) The roles of gill permeability and transport mechanisms in euryhalinity. In: Hoar WS, Randall DJ (eds) Fish Physiology, XB. Academic Press, Orlando, pp 239–328
Finn RN, Rønnestad I, van der Meeren T, Fyhn HJ (2002) Fuel and metabolic scaling during the early life stages of Atlantic cod Gadus morhua. Mar Ecol Prog Ser 243:217–234
Fonds M, Cronie R, Vethaak AD, Van der Puyl P (1992) Metabolism, food consumption and growth of plaice (Pleuronectes platessa) and flounder (Platichthys flesus) in relation to fish size and temperature. Neth J Sea Res 29:127–143. https://doi.org/10.1016/0077
Giacomin M, Onukwufor JO, Schulte PM, Wood CM (2020) Ionoregulatory aspects of the hypoxia-induced osmorespiratory compromise in the euryhaline killifish (Fundulus heteroclitus): the effects of salinity. J Exp Biol 223:216–309. https://doi.org/10.1242/jeb.216309
Gibson RN (1994) Impact of habitat quality and quantity on the recruitment of juvenile flatfishes. Neth J Sea Res 32:191–206. https://doi.org/10.1016/0077-7579(94)90040-X
Herrera M, Aragão C, Hachero I, Ruiz-Jarabo I, Vargas-Chacoff L, Mancera JM, Conceição LE (2012) Physiological short-term response to sudden salinity change in the Senegalese sole (Solea senegalensis). Fish Physiol Biochem 38:1741–1751. https://doi.org/10.1007/s10695-012-9671-8
Holmes WN, Donaldson EM (1969) Body compartments and distribution of electrolytes. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol 1. Academic Press, New York, pp 1–89
Huang Q, Riviere J (2014) The application of allometric scaling principles to predict pharmacokinetic parameters across species. Expert Opin Drug Metab Toxicol 10:1–13. https://doi.org/10.1517/17425255.2014.934671
Hunn JB (1985) Role of calcium in gill function in freshwater fishes. Comp Biochem Phys A 82:543–547. https://doi.org/10.1016/0300-9629(85)90430-X
Ip YK, Chew SF, Randall DJ (2001) Ammonia toxicity, tolerance, and excretion. In: Anderson AJ (ed) Wright PA. Nitrogen excretion. Fish physiology. Academic Press Inc., San Diego
Ip YK, Soh MMLXL, Chen K, Ong JLY, Chng YR, Ching B, Wong WP, Lam SH, Chew SF (2013) Molecular characterization of branchial aquaporin 1aa and effects of seawater acclimation emersion or ammonia exposure on its mRNA expression in the gills, gut, kidney and skin of freshwater climbing perch. Anabas Testudineus Plos 8(4):61162. https://doi.org/10.1371/journal.pone.0061163
Isaia J (1984) Water and nonelectrolyte permeability. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol 10B. Academic Press. San Diego, CA, pp 1–38
Isaia J, Masoni A (1976) The effects of calcium and magnesium on water and ionic permeabilities in the sea water adapted eel. Anguilla Anguilla l J Comp Physiol 109(2):221–233. https://doi.org/10.1007/BF00689420
Jobling M (1994) Biotic factors and growth performances. In: Jobling M (ed) Fish Bioenergetics, Fish and Fisheries series. Chapman and Hall, USA
Jung D, Sato JD, Shaw JR, Stanton BA (2012) Expression of aquaporin 3 in gills of the Atlantic killifish (Fundulus heteroclitus): Effects of seawater acclimation. Comp Biochem Physiol A 161(3):320–326. https://doi.org/10.1016/j.cbpa.2011.11.014
Kieffer JD, Alsop D, Wood CM (1998) A respirometric analysis of fuel use during aerobic swimming at different temperatures in rainbow trout (Oncorhynchus mykiss). J Exp Biol 201:3123–3313
Kjerfve B (1994) Coastal lagoons. In Elsevier Oceanograp Series 60:1–8
Kolarevic J, Takle H, Felip O, Ytteborg E, Selset R, Good CM, Baeverfjord GT, Asgard T, Terjes BF (2012) Molecular and physiological responses to long term sublethal ammonia exposure in Atlantic salmon (Salmo salar). Aquat Toxicol 124(125):48–57. https://doi.org/10.1016/j.aquatox.2012.07.003
Lauff RF, Wood CM (1996) Respiratory gas exchange, nitrogenous waste excretion, and fuel usage during starvation in juvenile rainbow trout, Oncorhynchus mykiss. J Comp Physiol B 165:542–551. https://doi.org/10.1007/BF02338293
Lignot JH, Cutler CP, Hazon N, Cramb G (2002) Immunolocalisation of aquaporin 3 in the gill and the gastrointestinal tract of European eel Anguilla Anguilla. J Exp Biol 205:2653–2663. https://doi.org/10.1242/jeb.205.17.2653
Madsen SS, Engelund MB, Cutler CP (2015) Water transport and functional dynamics of aquaporins in osmoregulatory organs of fishes. Biol Bull 229:70–92. https://doi.org/10.1086/BBLv229n1p70
Marshall WS (2012) Osmoregulation in estuarine and intertidal fishes. In: McCormick SD (ed) Fish Physiology, Euryhaline Fishes. Elsevier, New York
Marshall WS, Nishioka RS (1980) Relation of mitochondria-rich chloride cells to active chloride transport in the skin of a marine teleost. J Exp Zool 214:147–156. https://doi.org/10.1002/jez.1402140204
Maxime V, Pichavant K, Boeuf G (2000) Effects of hypoxia on respiratory physiology of turbot. Scophthalmus Macimus. Fish Physiol Biochem. 22:51–59
McDonald DG (1983) The interaction of environmental calcium and low pH on the physiology of the rainbow trout, Salmo gairdneri: I Branchial and renal net ion and H+ fluxes. J Exp Biol 102(1):123–140. https://doi.org/10.1242/jeb.102.1.123
McDonald DG, Rogano MS (1986) Ion regulation by the rainbow trout, Salmo gairdneri, in ion-poor water. Physiol Zool 59(3):318–331. https://doi.org/10.1242/jeb.83.1.181
McDonald MD, Wood CM (2003) Differential handling of urea and its analogues suggests carrier-mediated urea excretion in the freshwater rainbow trout. Physiol Biochem Zool 76:791–802. https://doi.org/10.1086/378919
McDonald MD, Wood CM, Wang Y, Walsh PJ (2000) Differential branchial and renal handling of urea, acetamide and thiourea in the gulf toadfish, Opsanus beta: evidence for two transporters. J Exp Biol 203:1027–1037. https://doi.org/10.1242/jeb.203.6.1027
McDonald MD, Smith CP, Walsh PJ (2006) The physiology and evolution of urea transport in fishes. J Membr Biol 212(2):93–107. https://doi.org/10.1007/s00232-006-0869-5
McDonald MD, Gilmour KM, Walsh PJ (2012) New insights into the mechanisms controlling urea excretion in fish gills. Respirat Physiol Neurobiol. 184(3):241–248. https://doi.org/10.1016/j.resp.2012.06.002
McNeil D, Westergaard S, Cheshire K, Noell C, Ye, Q (2013) Effects of hyper-saline conditions upon six estuarine fish species from the Coorong and Murray Mouth. Report number: SARDI Publication No. F2013/000020–1. SARDI Research Report Series No. 758.Affiliation: South Australian Research and Development Institute (Aquatic Sciences)
McWilliams PG (1982) The effects of calcium on sodium fluxes in the rainbow trout Salmo trutta, in neutral and acid media. J Exp Biol 96:436–442. https://doi.org/10.1242/jeb.96.1.439
McWilliams PG, Potts WTW (1978) The effects of pH and calcium concentrations on gill potentials in the brown trout, Salmo trutta. J Biol Chem 126:277–286. https://doi.org/10.1007/BF00688938
Minami T, Tanaka M (1992) Life history cycles in flatfish from the northwestern Pacific, with particular reference to their early life histories. Neth J Sea Res 29:35–48. https://doi.org/10.1016/0077-7579(92)90006-Z
Mistry AC, Honda S, Hirata T, Kato A, Hirose S (2001) Eel urea transporter localized to chloride cells and is salinity dependent. Am J Physiol Regul 281:R1594–R1604. https://doi.org/10.1152/ajpregu.2001.281.5.R1594
Moran D, Wells RMG (2007) Ontogenetic scaling of fish metabolism in the mouse-to-elephant mass magnitude range. Comp Biochem and Physiol A 148(3):611–620. https://doi.org/10.1016/j.cbpa.2007.08.006
Motais RJ, Isaia JC, Rankin J (1969) Adaptive changes of the water permeability of the teleostean gill epithelium in relation to external salinity. J Exp Biol 51(2):529–546. https://doi.org/10.1242/jeb.51.2.529
Nawata CM, Hung CCY, Tsui TKN, Wilson JM, Wright PA, Wood CM (2007) Ammonia excretion in rainbow trout (Oncorhynchus mykiss): Evidence for Rh glycoprotein and H+ -ATPase involvement. Physiol Genomics 31:463–474. https://doi.org/10.1152/physiolgenomics.00061.2007
Németh-Cahalan KL, Hall JE (2000) pH and calcium regulate the water permeability of aquaporin. J Biol Chem 275(10):6777–6782. https://doi.org/10.1074/jbc.275.10.6777
Németh-Cahalan KL, Kalman K, Hall JE (2004) Molecular basis of pH and Ca2+ regulation of aquaporin water permeability. J Gen Physiol 123(5):573–580. https://doi.org/10.1085/jgp.200308990
Oduleye SO (1975) The effects of calcium on water balance of the brown trout Salmo trutta. J Exp Biol 63(2):343–356. https://doi.org/10.1242/jeb.63.2.343
Olson KR (1992) Blood and extracellular fluid volume regulation. In: Hoar WS, Randall DJ, Farrell AP (eds) Fish Physiology. Academic Press, San Diego, CA
Onukwufor JO, Wood CM (2018) The osmorespiratory compromise in rainbow trout (Oncorhynchus mykiss): The effects of fish size, hypoxia, temperature and strenuous exercise on gill diffusive water fluxes and sodium net loss rates. Comp Biochem Physiol A 219–220:10–18. https://doi.org/10.1016/j.cbpa.2018.02.002
Onukwufor JO, Wood CM (2020a) Reverse translation: effects of acclimation temperature and acute temperature challenges on oxygen consumption, diffusive water flux, net sodium loss rates, Q10 values and mass scaling coefficients in the rainbow trout (Oncorhynchus mykiss). J Comp Physiol B. https://doi.org/10.1007/s00360-020-01259-4
Onukwufor JO, Wood CM (2020b) Osmorespiratory compromise in zebrafish (Danio rerio): effects of hypoxia and acute thermal stress on oxygen consumption, diffusive water flux and sodium net loss rates. Zebrafish 17(6):400–411
Onukwufor JO, Wood CM (2022) The osmorespiratory compromise in marine flatfish: differential effects of temperature, salinity, and hypoxia on diffusive water flux and oxygen consumption of English sole (Parophrys vetulus) and Pacific sanddab (Citharichthys sordidus). Mar Biol 169(51):1–15. https://doi.org/10.1007/s00227-022-04040-z
Pelster B, Wood CM, Braz-Mota S, Val A (2020) Gills and air-breathing organ in O2 uptake, CO2 excretion, N-waste excretion, and ionoregulation in small and large pirarucu (Arapaima gigas). J Comp Physiol B 190:569–583. https://doi.org/10.1007/s00360-020-01286-1
Potts WTW, Fleming WR (1970) The effects of prolactin and divalent ions on the permeability to water of Fundulus kansae. J Exp Biol 53(2):317–327. https://doi.org/10.1242/jeb.53.2.317
Potts WTW, Foster MA, Rudy PP, Howells GP (1967) Sodium and water balance in the cichlid teleost. Tilapia Mossambica J Exp Biol 47(3):461–470. https://doi.org/10.1242/jeb.47.3.461
Preston GM, Carroll TP, Guggino WB, Agre P (1992) Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science 256:385–387. https://doi.org/10.1126/science.256.5055.385
Rackowski JP, Pikitch EK (1989) Species profiles: Life histories and environmental requirements of coastal fishes and invertebrates (Pacific Southwest), Pacific and speckled sanddabs. Biological Report 82(11.107), Fish and Wildlife Service, US. Department of the Interior
Rahmatullah M, Boyde TR (1980) Improvements in the determination of urea using diacetyl monoxime; methods with and without deproteinisation. Clinca Chimica Acta 107(1–2):3–9. https://doi.org/10.1016/0009-8981(80)90407-6
Rasmussen AD, Bjerregaard P (1995) The effect of salinity and calcium concentration on the apparent water permeability of Cherax destructor, Astacus astacus and Carcinus maenas (Decapoda, Crustacea). Comp Bio Physiol A 111(1):171–175. https://doi.org/10.1016/0300-9629(95)98534-N
Rocha AJS, Gomes V, Phan VN, Passos MJ, Furia RR (2005) Metabolic demand and growth of juveniles of Centropomus parallelus as function of salinity. J Exp Mar Biol Ecol 316:157–165. https://doi.org/10.1016/j.jembe.2004.11.006
Rocha AJS, Gomes V, Ngan PV, Passos MJ, Furia RR (2007) Effects of anionic surfactant and salinity on the bioenergetics of juveniles of Centropomus parallelus (Poey). Ecotoxicol Environ Saf 68:397–404. https://doi.org/10.1016/j.ecoenv.2006.10.007
Rogers SG, Targett TE, van Sant SB (1984) Fish-nursery use in Georgia salt-marsh estuaries: The influence of springtime freshwater conditions. In Trans Am Fish Soc 113:595–606. https://doi.org/10.1577/1548-8659(1984)113%3c595:FUIGSE%3e2.0.CO;2
Rooper CN, Gunderson DR, Armstrong DA (2006) Evidence for resource partitioning and competition in nursery estuaries by juvenile flatfish in Oregon and Washington. Fish Bull 104(4):616–622
Ruhr IM, Wood CM, Schauer KL, Wang Y, Mager EM, Stanton B, Grosell M (2020) Is aquaporin-3 involved in water-permeability changes in the killifish during hypoxia and normoxic recovery, in freshwater or seawater? J Exp Zool 333:511–525. https://doi.org/10.1002/jez.2393
Ruiz-Jarabo I, Herrera M, Hachero-Cruzado I, Vargas-Chacoff L, Mancera JM, Arjona FJ (2015) Environmental salinity and osmoregulatory processes in cultured flatfish. Aquac Res 46:10–29. https://doi.org/10.1111/are.12424
Schreiber AM (2001) Metamorphosis and early larval development of the flatfishes (Pleuronectiformes): an osmoregulatory perspective. Comp Biochem Physiol B 129(2–3):587–595. https://doi.org/10.1016/S1096-4959(01)00346-3
Sobocinski KL, Ciannelli L, Wakefield WW, Yergey ME, Johnson-Colegrove A (2018) Distribution and abundance of juvenile demersal fishes in relation to summer hypoxia and other environmental variables in coastal Oregon, USA. Estuar Coast Shelf Sci 205:75–90. https://doi.org/10.1016/j.ecss.2018.03.002
Stagl J, Mayr E, Koch H, Hattermann FF, Huang S (2014) Effects of Climate Change on the Hydrological Cycle in Central and Eastern Europe. In: Rannow S, Neubert M (eds) Managing Protected Areas in Central and Eastern Europe Under Climate Change Advances in Global Change Research. Springer, Dordrecht, USA
Steffensen JF, Lomholt JP, Johansen K (1982) Gill ventilation and O2 extraction during graded hypoxia in two ecologically distinct species of flatfish, the flounder (Platichthys flesus) and the plaice (Pleuronectes platessa). Environ Biol Fish 7:157–163. https://doi.org/10.1007/BF00001786
Thornburgh K (1980) Patterns of resource utilization in flatfish communities. Dissertation 90 p. Univ. Washington, Seattle, WA, USA
Tingaud-Sequeira A, Calusinska M, Finn RN, Chauvigne F, Lozano J, Cerdà J (2010) The zebrafish genome encodes the largest vertebrate repertoire of functional aquaporins with dual paralogy and substrate specificities similar to mammals. BMC Evol Biol 10(1):38. https://doi.org/10.1186/1471-2148-10-38
Tipsmark CK, Sørensen KJ, Madsen SS (2010) Aquaporin expression dynamics in osmoregulatory tissues of Atlantic salmon during smoltification and seawater acclimation. J Exp Biol 213:368–379. https://doi.org/10.1242/jeb.034785
Valenti G, Procino G, Tamma G, Carmosino M, Svelto M (2005) Minireview: aquaporin 2 trafficking. Endocrinology 146(12):5063–5070. https://doi.org/10.1210/en.2005-0868
Van den Thillart G, Kesbeke F (1978) Anaerobic production of carbon dioxide and ammonia by goldfish Carassius auratus (L). Comp Biochem Physiol A 59(4):393–400. https://doi.org/10.1016/0300-9629(78)90185-8
Van Waarde A (1983) Aerobic and anaerobic ammonia production by fish. CompBiochem Physiol B 74(4):675–684. https://doi.org/10.1016/0305-0491(83)90127-X
Verdouw H, Echteld C, Dekkers E (1978) Ammonia determination based on indophenol formation with sodium salicylate. Water Res 12:399–402. https://doi.org/10.1016/0043-1354(78)90107-0
Walsh P, Wang Y, Campbell C, Boeck DG, Wood C (2001) Patterns of nitrogenous waste excretion and gill urea transporter mRNA expression in several species of marine fish. Mar Biol 139(5):839–844. https://doi.org/10.1007/s002270100639
Weihrauch D, Wilkie MP, Walsh PJ (2009) Ammonia and urea transporters in gills of fish and aquatic crustaceans. J Exp Biol 212:1716–1730. https://doi.org/10.1242/jeb.024851
Wendelaar Bonga SE, Van der Meiji CA (1981) Effect of ambient osmolarity and calcium on prolactin cell activity and osmotic water permeability of the gills in teleost Sarotherodon mossambicus. Gen Comp Endocrin 43:432–442. https://doi.org/10.1016/0016-6480(81)90227-6
Wilkie MP (1997) Mechanisms of ammonia excretion across fish gills. Comp Biochem Physiol A 118:39–50. https://doi.org/10.1016/S0300-9629(96)00407-0
Wilkie MP (2002) Ammonia excretion and urea handling by fish gills: Present understanding and future research challenges. J Exp Zool 293:284–301. https://doi.org/10.1002/jez.10123
Wood CM (1992) Flux measurements as indices of H+ and metal effects on freshwater fish. Aquat Toxicol 22:239–264. https://doi.org/10.1016/0166-445X(92)90043-M
Wood CM (1993) Ammonia and urea metabolism and excretion. In: Evans DH (ed) The Physiology of Fishes. CRC Press. USA, Boca Raton, FL
Wood CM, Eom J (2021) The osmorespiratory compromise in the fish gill. Comp Biochem Physiol A 254:110895. https://doi.org/10.1016/j.cbpa.2021.110895
Wood CM, Marshall WS (1994) Ion balance, acid-base regulation, and chloride cell function in the common killifish, Fundulus heteroclitus a euryhaline estuarine teleost. Estuaries 17:34–52. https://doi.org/10.2307/1352333
Wood CM, Nawata CM (2011) A nose-to-nose comparison of the physiological and molecular responses of rainbow trout to high environmental ammonia in seawater versus freshwater. J Exp Biol 214:3557–3569. https://doi.org/10.1242/jeb.057802
Wood CM, McMahon BR, McDonald DG (1979) Respiratory gas exchange in the resting starry flounder, Platichthys stellatus: a comparison with other teleosts. J Exp Biol 78:167–179. https://doi.org/10.1242/jeb.78.1.167
Wood CM, Robertson LM, Johannsson OE, Val AL (2014) Mechanisms of Na+ uptake, ammonia excretion, and their potential linkage in native Rio Negro tetras (Paracheirodon axelrodi, Hemigrammus rhodostomus, and Moenkhausia diktyota). J Comp Physiol B 184(7):877–890. https://doi.org/10.1007/s00360-014-0847-7
Wood CM, Ruhr IM, Schauer KL, Wang Y, Mager EM, McDonald D, Stanton B, Grosell M (2019) The osmorespiratory compromise in the euryhaline killifish: water regulation during hypoxia. J Exp Biol 222:204818. https://doi.org/10.1242/jeb.204818
Wright PA, Wood CM (2009) A new paradigm for ammonia excretion in aquatic animals: role of Rhesus (Rh) glycoproteins. J Exp Biol 212:2303–2312. https://doi.org/10.1242/jeb.023085
Wright PA, Wood CM (2012) Seven things fish know about ammonia and we don’t. Respir Physiol Neurobiol 184:231–240. https://doi.org/10.1016/j.resp.2012.07.003
Zimmer A, Baracolli IF, Wood CM, Bianchini A (2012) Waterborne copper exposure inhibits ammonia excretion and branchial carbonic anhydrase acitiviy in euryhaline guppies acclimated to both fresh water and sea water. Aquat Toxicol 122–123:172–180
Acknowledgements
We thank the Bamfield Marine Sciences Centre staff, especially the Research Co-ordinator, Tao Eastham, for excellent assistance, and two anonymous reviewers whose constructive comments improved the paper.
Funding
Supported by an NSERC (Canada) Discovery Grant (RGPIN-2017–03843) to CMW.
Author information
Authors and Affiliations
Contributions
The project was jointly conceived by CM and CMW. CM did the experiments under the supervision of CMW. CM wrote the first draft of the paper, and CMW edited it.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Ethical approval
Animals were collected under Fisheries and Oceans Canada collection permit XR 136 2021. The University of British Columbia Animal Care Committee (AUP A18-0271) and the Bamfield Marine Science Centre Animal Care Committee (AUP RS-21(19)-01)) approved all experimental procedures, in accordance with the Canadian Council on Animal Care guidelines.
Additional information
Responsible Editor: H.-O. Pörtner.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Morris, C., Wood, C.M. The effect of salinity and calcium on diffusive water flux, oxygen consumption, and nitrogenous waste excretion rates in Pacific sanddab (Citharichthys sordidus) and Rock sole (Lepidopsetta bilineata). Mar Biol 170, 108 (2023). https://doi.org/10.1007/s00227-023-04245-w
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-023-04245-w