Abstract
We measured the ontogeny of salinity tolerance and the preparatory hypo-osmoregulatory physiological changes for seawater entry in green sturgeon (Acipenser medirostris), an anadromous species occurring along the Pacific Coast of North America. Salinity tolerance was measured every 2 weeks starting in 40-day post-hatch (dph) juveniles and was repeated until 100% survival at 34‰ was achieved. Fish were subjected to step increases in salinity (5‰ 12 h−1) that culminated in a 72-h exposure to a target salinity, and treatment groups (0, 15, 20, 25, 30, 34‰; and abrupt exposure to 34‰) were adjusted as fish developed. After 100% survival was achieved (134 dph), a second experiment tested two sizes of fish for 28-day seawater (33‰) tolerance, and gill and gastrointestinal tract tissues were sampled. Their salinity tolerance increased and plasma osmolality decreased with increasing size and age, and electron microscopy revealed three types of mitochondria-rich cells: one in fresh water and two in seawater. In addition, fish held on a natural photoperiod in fresh water at 19°C showed peaks in cortisol, thyroid hormones and gill and pyloric ceca Na+, K+-ATPase activities at body sizes associated with seawater tolerance. Therefore, salinity tolerance in green sturgeon increases during ontogeny (e.g., as these juveniles may move down estuaries to the ocean) with increases in body size. Also, physiological and morphological changes associated with seawater readiness increased in freshwater-reared juveniles and peaked at their seawater-tolerant ages and body sizes. Their seawater-ready body size also matched that described for swimming performance decreases, presumably associated with downstream movements. Therefore, juvenile green sturgeon develop structures and physiological changes appropriate for seawater entry while growing in fresh water, indicating that hypo-osmoregulatory changes may proceed by multiple routes in sturgeons.
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Abbreviations
- BML:
-
Bodega Marine Laboratory
- CF:
-
Condition factor
- Dph:
-
Days post-hatch
- FW:
-
Fresh water
- GIT:
-
Gastrointestinal tract
- MRC:
-
Mitochondria-rich cell
- NKA:
-
Na+, K+-ATPase
- SW:
-
Seawater
- TL:
-
Total length
References
Adams PB, Grimes C, Hightower JE, Lindley ST, Moser ML, Parsley MJ (2007) Population status of North American green sturgeon, Acipenser medirostris. Environ Biol Fish 79:339–356
Allen PJ, Cech JJ Jr (2007) Age/size effects on juvenile green sturgeon, Acipenser medirostris, oxygen consumption, growth, and osmoregulation in saline environments. Environ Biol Fish 79:211–229
Allen PJ, Hodge B, Werner I, Cech JJ Jr (2006a) Effects of ontogeny, season, and temperature on the swimming performance of juvenile green sturgeon (Acipenser medirostris). Can J Fish Aquat Sci 63:1360–1369
Allen PJ, Nicholl M, Cole S, Vlazny A, Cech JJ Jr (2006b) Growth in larval to juvenile green sturgeon in elevated temperature regimes. Trans Am Fish Soc 135:89–96
Allen PJ, Cech JJ Jr, Kültz D (2009a) Mechanisms of seawater acclimation in a primitive, anadromous fish, the green sturgeon. J Comp Physiol B 179:903–920
Allen PJ, Hobbs JA, Cech JJ Jr, Van Eenennaam JP, Doroshov SI (2009b) Using trace elements in pectoral fin rays to assess life history movements in sturgeon: estimating age at initial seawater entry in Klamath River green sturgeon. Trans Am Fish Soc 138:240–250
Altinok I, Galli SM, Chapman FA (1998) Ionic and osmotic regulation capabilities of juvenile Gulf of Mexico sturgeon, Acipenser oxyrinchus desotoi. Comp Biochem Physiol A Comp Physiol 120:609–616
Amiri BM, Baker DW, Morgan JD, Brauner CJ (2009) Size dependent early salinity tolerance in two sizes of juvenile white sturgeon, Acipenser transmontanus. Aquaculture 286:121–126
Baker DW, Matey V, Huynh KT, Wilson JM, Morgan JD, Brauner CJ (2009) Complete intracellular pH protection during extracellular pH depression is associated with hypercarbia tolerance in white sturgeon, Acipenser transmontanus. Am J Physiol Regul Integr Comp Physiol 296:R1868–R1880
Barry TP, Lapp AF, Kayes TB, Malison JA (1993) Validation of a microtitre plate ELISA for measuring cortisol in fish and comparison of stress responses of rainbow trout (Oncorhynchus mykiss) and lake trout (Salvelinus namaycush). Aquaculture 117:351–363
Billard R, Lecointre G (2001) Biology and conservation of sturgeon and paddlefish. Rev Fish Biol Fish 10:355–392
Boeuf G (1993) Salmonid smolting: a pre-adaptation to the oceanic environment. In: Rankin JC, Jensen FB (eds) Fish ecophysiology. Chapman & Hall, London, pp 105–135
Brown K (2007) Evidence of spawning by green sturgeon, Acipenser medirostris, in the upper Sacramento River, California. Environ Biol Fish 79:297–303
Burke CN, Geiselman CW (1971) Exact anhydride epoxy percentages for electron microscopy embedding (Epon). J Ultrastruct Res 36:119–126
Carmona R, Garcia-Gallego M, Sanz A, Domenzain A, Ostos-Garrido MV (2004) Chloride cells and pavement cells in gill epithelia of Acipenser naccarii: ultrastructural modifications in seawater-acclimated specimens. J Fish Biol 64:553–566
Cataldi E, Ciccotti E, Di Marco P, Di Santo O, Bronzi P, Cataudella S (1995) Acclimation trials of juvenile Italian sturgeon to different salinities: morpho-physiological descriptors. J Fish Biol 47:609–618
Cataldi E, Barzaghi C, Di Marco P, Boglione C, Dini L, McKenzie DJ, Bronzi P, Cataudella S (1999) Some aspects of osmotic and ionic regulation in Adriatic sturgeon Acipenser naccarii. I: ontogenesis of salinity tolerance. J Appl Ichthyol 15:57–60
Chang IC, Lee TH, Yang CH, Wei YW, Chou FI, Hwang PP (2001) Morphology and function of gill mitochondria-rich cells in fish acclimated to different environments. Physiol Biochem Zool 74:111–119
Chang IC, Wei YW, Chou FI, Hwang PP (2003) Stimulation of chloride uptake and morphological changes in gill mitochondria-rich cells in freshwater tilapia (Oreochromis mossambicus). Physiol Biochem Zool 76:544–552
Clarke WC, Blackburn J (1977) A seawater challenge test to measure smolting of juvenile salmon. Fisheries and Marine Service Research and Development Technical Report 705
Daborn K, Cozzi RRF, Marshall WS (2001) Dynamics of pavement cell-chloride cell interactions during abrupt salinity change in Fundulus heteroclitus. J Exp Biol 204:1889–1899
Deng X, Van Eenennaam JP, Doroshov SI (2002) Comparison of early life stages and growth of green and white sturgeon. In: Van Winkle W, Anders PJ, Secor DH, Dixon DA (eds) Biology, management, and protection of North American sturgeon. American Fisheries Society, Symposium 28, Bethesda, Maryland, pp 237–248
Eales JG (2006) Modes of action and physiological effects of thyroid hormones in fish. In: Reinecke M, Zaccone G, Kapoor BG (eds) Fish endocrinology, vol 2. Science Publishers, Enfield, pp 767–808
Evans DH, Piermarini P, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid-base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177
Hanaichi T, Sato T, Iwamoto T, Malavasi-Yamashiro J, Hoshino M, Mizuno N (1986) A stable lead stain by modification of Sato’s method. J Electron Microsc 35:304–306
He X, Zhuang P, Zhang L, Xie C (2009) Osmoregulation in juvenile Chinese sturgeon (Acipenser sinensis Gray) during brackish water adaptation. Fish Physiol Biochem 35:223–230. doi:10.1007/s10695-008-9230-5
Hoar WS (1988) The physiology of smolting salmonids. In: Hoar WS, Randall DJ (eds) Fish physiology, vol XI. Academic Press, Inc., San Diego, pp 275–343
Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford University Press, New York
Holmes WN, Donaldson EM (1969) The body compartments and the distribution of electrolytes. In: Hoar WS, Randall DJ (eds) Fish Physiology, vol 1. Academic Press, New York, pp 1–89
Hossler FE, Ruby JR, Mcilwain TD (1979) Gill arch of the mullet Mugil cephalus. 2: modification in surface ultrastructure and Na, K-ATPase content during adaptation to various salinities. J Exp Zool 209:399–405
Hossler FE, Musil G, Karnaky KJ, Epstein FH (1985) Surface ultrastructure of the gill arch of the killifish Fundulus heteroclitus, from seawater and fresh water, with special reference to the morphology of apical crypts of chloride cells. J Morphol 185:377–386
Hwang P-P, Lee T-H (2007) New insights into fish ion regulation and mitochondrion-rich cells. Comp Biochem Physiol Part A 148(2007):479–497
Johnson SL, Ewing RD, Lichatowich JA (1977) Characterization of gill (Na + K)-activated adenosine triphosphatase from chinook salmon, Oncorhynchus tshawytscha. J Exp Zool 199:345–354
Jorgensen EH, Arnesen AM (2002) Seasonal changes in osmotic and ionic regulation in Arctic charr, Salvelinus alpinus, from a high- and a sub-arctic anadromous population. Environ Biol Fish 64:185–193
Karnaky KJ Jr, Kinter LB, Kinter WB, Stirling CE (1976a) Teleost chloride cell: II. Autoradiographic localization of gill Na, K-ATPase in killifish, Fundulus heteroclitus adapted to low and high salinity environments. J Cell Biol 70:157–170
Karnaky KJ Jr, Ernst SA, Philpott CW (1976b) Teleost chloride cell: I. Response of pupfish Cyprinodon variegatus gill Na, K-ATPase and chloride cell fine structure to various environments. J Cell Biol 70:144–156
Katzman S, Cech JJ (2001) Juvenile coho salmon locomotion and mosaic muscle are modified by 3′,3′,5′-tri-iodo-l-thyronine (T3). J Exp Biol 204:1711–1717
Kieffer MC, Kynard B (2011) Pre-spawning and non-spawning spring migrations, spawning, and effects of hydroelectric dam operation and river regulation on spawning of Connecticut River shortnose sturgeon. In: World Sturgeon Conservation Society Spec Publ (ed) (in press)
Krayushkina LS, Dyubin VP (1974) The reaction of juvenile sturgeon to alteration of environmental salinity. J Ichthyol 14:971–977
Kültz D, Jürss K, Jonas L (1995) Cellular and epithelial adjustments to altered salinity in the gill and opercular epithelium of a cichlid fish (Oreochromis mossambicus). Cell Tissue Res 279:65–73
Kynard B, Parker E, Parker T (2005) Behavior of early life intervals of Klamath River green sturgeon, Acipenser medirostris, with a note on body color. Environ Biol Fish 72:85–97
LeBreton GTO, Beamish FWH (1998) The influence of salinity on ionic concentrations and osmolarity of blood serum in lake sturgeon, Acipenser fulvescens. Environ Biol Fish 52:477–482
Lee TH, Hwang PP, Feng SH (1996a) Morphological studies of gill and mitochondria-rich cells in the stenohaline cyprinid teleosts, Cyprinus carpio and Carassius auratus, adapted to various hypotonic environments. Zoological Studies 35:272–278
Lee TH, Hwang PP, Lin HC, Huang FL (1996b) Mitochondria-rich cells in the branchial epithelium of the teleost, (Oreochromis mossambicus) acclimated to various hypotonic environments. Fish Physiol Biochem 15:513–523
Lin LY, Hwang PP (2004) Mitochondria-rich cell activity in the yolk-sac membrane of tilapia (Oreochromis mossambicus) larvae acclimatized to different ambient chloride levels. Journal Experimental Biology 207:1335–1344
Madsen SS (1990) The role of cortisol and growth hormone in seawater adaptation and development of hypoosmoregulatory mechanisms in sea trout parr (Salmo trutta trutta). Gen Comp Endocrinol 79:1–11
Martinez-Alvarez RM, Hidalgo MC, Domezain A, Morales AE, Garcia-Gallego M, Sanz A (2002) Physiological changes of sturgeon Acipenser naccarii caused by increasing environmental salinity. J Exp Biol 205:3699–3706
Martinez-Alvarez RM, Sanz A, Garcia-Gallego M, Domezain A, Domezain J, Carmona R, AE Morales, Ostos-Garrido MV (2005) Adaptive branchial mechanisms in the sturgeon Acipenser naccarii during acclimation to saltwater. Comp Biochem Physiol Part A 141(2):183–190
McCormick SD (1994) Ontogeny and evolution of salinity tolerance in anadromous salmonids: hormones and heterochrony. Estuaries 17:26–33
McCormick SD (1995) Hormonal control of gill Na+, K+-ATPase and chloride cell function. In: Wood CM, Shuttleworth TJ (eds) Fish physiology: cellular and molecular approaches to fish ionic regulation. Academic Press, San Diego, pp 285–315
McCormick SD (2001) Endocrine regulation of osmoregulation in teleost fish. Am Zool 41:781–794
McDowall RM (1988) Diadromy in fishes. Timber Press, Portland
McEnroe M, Cech JJ Jr (1985) Osmoregulation in juvenile and adult white sturgeon, Acipenser transmontanus. Environ Biol Fish 14:23–30
McEnroe M, Cech JJ Jr (1987) Osmoregulation in white sturgeon: life history aspects. Am Fish Soc Symp 1:191–196
McKenzie DJ, Cataldi E, Romano P, Taylor EW, Cataudella S, Bronzi P (2001) Effects of acclimation to brackish water on tolerance of salinity challenge by young-of-the-year Adriatic sturgeon (Acipenser naccarii). Can J Fish Aquat Sci 58:1113–1121
Moyle PB (2002) Inland fishes of California. University of California Press, Berkeley
Munro C, Stabenfeldt G (1985) Development of a cortisol enzyme immunoassay in plasma. Clin Chem 31:956
Nakamoto RJ, Kisanuki TT, Goldsmith GH (1995) Age and growth of Klamath River green sturgeon (Acipenser medirostris). U.S. Fish and Wildlife Service. Klamath River Fishery Resource Office, Yreka
Perry SF (1997) The chloride cell: structure and function in the gills of freshwater fishes. Annu Rev Physiol 59:325–347
Pisam M, Rambourg A (1991) Mitochondria-rich cells in the gill epithelium of teleost fishes an ultrastructural approach. Int Rev Cytol 130:191–232
Radtke LD (1966) Distribution of smelt, juvenile sturgeon, and starry flounder in the Sacramento-San Joaquin Delta with observations on food of sturgeon. In: Turner JL, Kelley DW (eds) Ecological studies of the Sacramento-San Joaquin Delta, Part II: Fishes of the Delta. California Fish and Game Bulletin 136, pp 115–129
Richards JE, Beamish FWH (1981) Initiation of feeding and salinity tolerance in the Pacific lamprey Lampetra tridentata. Mar Biol 63:73–77
Rodriguez A, Gallardo MA, Gisbert E, Santilari S, Ibarz A, Sanchez J, Castello-Orvay F (2002) Osmoregulation in juvenile Siberian sturgeon (Acipenser baerii). Fish Physiol Biochem 26:345–354
Sardella BA, Kültz D (2009) Osmo- and ionoregulatory responses of green sturgeon (Acipenser medirostris) to salinity acclimation. J Comp Physiol B 179:383–390
Sardella BA, Cooper J, Gonzalez RJ, Brauner CJ (2004) The effect of temperature on juvenile Mozambique tilapia hybrids (Oreochromis mossambicus x O. urolepis hornorum) exposed to full-strength and hypersaline seawater. Comp Biochem Physiol A 137:621–629
Schall RL, Henderson EB, Glebe BD (1978) A sensitive manual enzyme immunoassay for thyroxine. Clin Chem 24:1801–1804
Schreiber AM, Specker JL (1999) Metamorphosis in the summer flounder, Paralichthys dentatus: thyroidal status influences salinity tolerance. Endocrinology 284:414–424
Subash Peter MC, Lock RAC, Wendalaar Bonga SE (2000) Evidence for an osmoregulatory role of thyroid hormones in the freshwater Mozambique tilapia Oreochromis mossambicus. Gen Comp Endocrinol 120:157–167
Tsai JC, Hwang PP (1998) Effects of wheat germ agglutinin and colchicines on microtubules of the mitochondria-rich cells and Ca2+ uptake in tilapia (Oreochromis mossambicus) larvae. J Exp Biol 201:2263–2271
USFWS (U. S. Fish and Wildlife Service) (1998) Juvenile salmonid monitoring on the mainstem Klamath River at Big Bar and mainstem Trinity River at Willow Creek, 1992–1995. Annual Report of the Klamath River Fisheries Assessment Program. Arcata, CA
USFWS (U. S. Fish and Wildlife Service) (2001) Juvenile salmonid monitoring on the mainstem Klamath River at Big Bar and mainstem Trinity River at Willow Creek, 1997–2000. Annual report of the Klamath River Fisheries Assessment Program. Arcata, CA
USGS (U.S. Geological Survey) (2011) Klamath River temperature data. In: National Weather Information Service surface water data for California. http://nwis.waterdata.usgs.gov/ca/nwis
Van Eenennaam JP, Webb MAH, Deng X, Doroshov SI, Mayfield RB, Cech JJ Jr, Hillemeier DC, Willson TE (2001) Artificial spawning and larval rearing of Klamath River green sturgeon. Trans Am Fish Soc 130:159–165
Varsamos S, Connes R, Diaz JP, Barnabe G, Charmantier G (2001) Ontogeny of osmoregulation in the European sea bass Dicentrarchus labrax L. Mar Biol 138:909–915
Varsamos S, Nebel C, Charmantier G (2005) Ontogeny of osmoregulation in postembryonic fish: a review. Comp Biochem Physiol Part A 141:401–429
Watanabe WO, Kuo CM, Huang MC (1985) The ontogeny of salinity tolerance in the tilapias Oreochromis aureus, O. niloticus, and an O. mossambicus x O. niloticus hybrid, spawned and reared in freshwater. Aquaculture 47:353–368
Wedemeyer GA (1996) Physiology of fish in intensive culture systems. Chapman and Hall, New York
Wu YC, Lin LY, Lee TH (2003) Na+, K+, 2Cl− cotransporter: a novelmarker for identifying freshwater- and seawater-type mitochondria-rich cells in gills of the euryhaline tilapia tilapia, Oreochromis mossambicus. Zool Stud 42:186–192
Ziegeweid JR, Jennings CA, Peterson DL, Black MC (2008) Effects of salinity, temperature, and weight on the survival of young-of-year shortnose sturgeon. Trans Am Fish Soc 137:1490–1499
Zydlewski J, McCormick SD (1997) The ontogeny of salinity tolerance in the American shad, Alosa sapidissima. Can J Fish Aquat Sci 54:182–189
Acknowledgments
We thank the Yurok Tribal Council and the Yurok Fisheries Program for broodstock fish; S. Doroshov, J. Van Eenennaam, and J. Linares-Casenave for providing larval fish from the broodstock; P. Lutes, E. Hallen, K. Menard, J. Newman, B. Myers, M. Paulson, K. Brown, and W. Newman for facility assistance and recommendations; T. Allen, B. J. Zamora, N. Ponferrada, B. Hodges, R. Kaufman, D. Cocherell, T. Matsumoto, K. Jasperson, D. Hickey, A. Vlazny, A. Oye and B. Jang for technical assistance and insight; and S. Doroshov, P. Moyle, the students of WFA8212 and two anonymous reviewers for helpful comments on the manuscript. Financial assistance was provided by the California Bay-Delta Authority (grant no. ERP-02D-P57), the Anadromous Fish Restoration Program (US Fish and Wildlife Service, US Bureau of Reclamation; grant no. 11332-1-G005), the University of California Agricultural Experiment Station (grant no. 3455-H to JJC), the UC Davis Ecology Graduate Group (Block Grant and Jastro-Shields Scholarship to PJA), the BML (travel grant to PJA), Emily Schwalen Memorial Prize, the Marin Rod and Gun Club, the Granite Bay Flycasters, and the California Federation of FlyFishers (scholarships to PJA). TF was supported by a Purchase College Undergraduate Research Support Award, and the TEM/SEM capabilities were provided by a National Science Foundation Major Research Instrumentation Grant (No: 0116457) to J.R. Factor, Purchase College.
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Allen, P.J., McEnroe, M., Forostyan, T. et al. Ontogeny of salinity tolerance and evidence for seawater-entry preparation in juvenile green sturgeon, Acipenser medirostris . J Comp Physiol B 181, 1045–1062 (2011). https://doi.org/10.1007/s00360-011-0592-0
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DOI: https://doi.org/10.1007/s00360-011-0592-0