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Unidirectional Na and Ca 2+ Xuxes in Two Euryhaline Teleost Wshes

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Unidirectional Na and Ca 2+ Xuxes in Two Euryhaline Teleost Wshes J Comp Physiol B (2007) 177:519–528 DOI 10.1007/s00360-007-0150-y ORIGINAL PAPER Unidirectional Na+ and Ca2+ Xuxes in two euryhaline teleost Wshes, Fundulus heteroclitus and Oncorhynchus mykiss, acutely submitted to a progressive salinity increase Viviane Prodocimo · Fernando Galvez · Carolina A. Freire · Chris M. Wood Received: 15 September 2006 / Revised: 30 January 2007 / Accepted: 30 January 2007 / Published online: 22 February 2007 © Springer-Verlag 2007 Abstract Na+ and Ca2+ regulation were compared in rainbow trout experienced a dramatic increase in Na+ two euryhaline species, killiWsh (normally estuarine- inXux (50-fold relative to FW values), but not Na+ resident) and rainbow trout (normally freshwater-resi- eZux between 40 and 60% SW, resulting in a large net dent) during an incremental salinity increase. Whole- loading of Na+ at higher salinities (60–100% SW), and body unidirectional Xuxes of Na+ and Ca2+, whole body increases in plasma Na+ and whole body Na+ at 100% Na+ and Ca2+, and plasma concentrations (trout only), SW. KilliWsh were in negative Ca2+ balance at all salini- were measured over 1-h periods throughout a total 6-h ties, whereas trout were in positive Ca2+ balance protocol of increasing salinity meant to simulate a nat- throughout. Ca2+ inXux rate increased two- to threefold ural tidal Xow. KilliWsh exhibited signiWcant increases in killiWsh at 80 and 100% SW, but there were no con- in both Na+ inXux and eZux rates, with eZux slightly comitant changes in Ca2+ eZux. Ca2+ Xux rates were lagging behind eZux up to 60% SW, but net Na+ bal- aVected to a larger degree in trout, with twofold ance was restored by the time killiWsh reached 100% increases in Ca2+ inXux at 40% SW and sevenfold SW. Whole body Na+ did not change, in agreement increases at 100% SW. Again, there was no change in with the capacity of this species to tolerate daily Ca2+ eZux with salinity, so plasma Ca2+ concentration salinity Xuctuations in its natural habitat. In contrast, increased in 100% SW. As the killiWsh is regularly sub- mitted to increased salinity in its natural environment, it is able to rapidly activate changes in unidirectional Communicated by G. Heldmaier. Xuxes in order to ensure ionic homeostasis, in contrast V. Prodocimo (&) · C. A. Freire to the trout. Departamento de Fisiologia, Setor de Ciências Biológicas, Universidade Keywords Calcium · Ion Xuxes · KilliWsh · Federal do Paraná, Centro Politécnico, Curitiba, Paraná 81531-990, Brazil Rainbow trout · Salinity · Sodium e-mail: [email protected] F. Galvez · C. M. Wood Introduction Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4K1Canada Marine teleosts are strongly hypotonic to seawater, resulting in a tendency for solutes to move passively F. Galvez into the animal. In contrast, freshwater teleosts tend to Department of Biological Sciences, Louisiana State University, 216 Life Sciences Building, lose ions to the hypotonic aquatic environment Baton Rouge, LA 70803, USA (reviews in Jobling 1995; Evans et al. 1999, 2005; Marshall 2003; Kirschner 2004; Marshall and Grosell C. M. Wood 2005). Many teleosts are extremely euryhaline, displaying Department of Marine Biology and Fisheries, Rosenstiel School of Marine and Atmospheric great capacity to tolerate and adapt to wide variations Sciences, University of Miami, Miami, FL 33149, USA in salinity, reducing and even reversing net Xuxes of 123 520 J Comp Physiol B (2007) 177:519–528 ions through their surface epithelia (Potts and Evans the hypothesis that a euryhaline freshwater species and 1967; Bath and Eddy 1979a, b; Perry and Flik 1988; a euryhaline estuarine resident species would display Wood and Marshall 1994; Goss et al. 1998; Marshall diVerent patterns of ion Xux modulation when faced 2003; Wood and Laurent 2003). with the same stress of rapid salinity increase. Two such teleosts are the killiWsh Fundulus hetero- clitus (Family Cyprinodontidae) and the rainbow trout Oncorhynchus mykiss (Family Salmonidae). Fundulus Materials and methods heteroclitus is normally resident in the intermediate salinities of estuaries and salt marshes and is extremely Animals euryhaline, being exposed to daily salinity changes throughout the tidal cycle. This species also tolerates Adult specimens of F. heteroclitus (northern race, abrupt changes of water salinity between 0 and 120‰ sometimes classiWed as the sub-species macrolepidotus; (GriYth 1974) and has been a preferred model for the mean weight = 2.7 § 0.08 g) were obtained from the study of euryhalinity in teleost Wsh (e.g., Jacob and estuaries of Antigonish, NS, Canada, and Hampton, Taylor 1983; Marshall et al. 1999, 2000; Daborn et al. NH, USA. Fish were air-shipped to McMaster Univer- 2001; Katoh et al. 2003; Marshall 2003; Wood and sity, Hamilton, ON, Canada, where they were main- Laurent 2003). Oncorhynchus mykiss is normally resi- tained in 500-l tanks of recirculated water with a dent in freshwater, but may enter brackish and marine salinity of 10% of full-strength seawater (SW) (»3.5‰) waters to feed, and some strains go to sea for pro- for at least 2 weeks prior to experimentation. This longed periods (Sedgewick 1982). This species is also water was made up using commercial sea salts (Instant considered to be very euryhaline, and has been a com- Ocean™, Aquarium Systems Inc., Mentor, OH, USA) mon model used in euryhalinity studies (e.g., Gordon appropriately diluted in Lake Ontario water (composi- 1959, 1963; Bath and Eddy 1979a, b; Eddy and Bath tion as shown below). Water was maintained at 1979; Richards et al. 2003; Hawkings et al. 2004). approximately 20°C with constant aeration. Fish were A direct positive relationship between unidirectional fed daily with Wsh food in Xakes (Wardley Total Tropi- Na+ (and Cl¡) Xuxes and salinity has already been dem- cal Gourmet Flake Blend, Hartz Mountain Corp., onstrated for the killiWsh F. heteroclitus exposed to Secausus, USA), and frozen brine shrimp (San Francisco diVerent salinities for few hours (»3–4 h) up to several Bay Brand, Newark, USA). days or weeks of exposure/acclimation (Motais et al. Adult rainbow trout (O. mykiss) (mean 1966; Potts and Evans 1967; Pic 1978; Wood and weight = 169.5 § 10.6 g) were purchased from Humber Marshall 1994; Wood and Laurent 2003). Studies have Springs Trout Hatchery (Orangeville, ON, Canada), also been conducted with the rainbow trout O. mykiss, and taken to McMaster University, where they were mostly employing 7 or more days of acclimation to held in 500-l tanks supplied under Xow-through condi- diVerent salinities (Gordon 1963; Bath and Eddy 1979a; tions with moderately hard fresh water from Lake Eddy and Bath 1979; Perry and Laurent 1989), and Ontario (in mM: Ca2+ =1.0, Mg2+ = 0.2, Na+ =0.6, have also shown increased Xuxes associated with Cl¡ = 0.8, K+ = 0.05; pH = 7.9–8.0). The Wsh were accli- greater salinity. Unidirectional Ca2+ Xux measurements mated for at least 2 weeks prior to experimentation. in F. heteroclitus (Mayer-Gostan et al. 1983) and Water temperature was maintained at 15°C under con- O. mykiss (Perry and Flik 1988) are fairly rare; to our stant aeration. Trout were fed daily (ad libitum) with knowledge, they have never been determined while commercial trout chow (Martin Mills Inc., Canada). imposing salinity changes for these species. Note that while the size of killiWsh and trout obvi- However, at present, there is almost no information ously diVered, our goal was to compare adult animals on what happens when euryhaline Wsh experience fairly of the two species. Also, the acclimation temperatures, rapid and progressive salinity changes, as might happen 20°C for the killiWsh and 15°C for the trout, and salini- during a tidal cycle in an estuary or salt marsh, or during ties, 3.5‰ (10% seawater) for the killiWsh and 0‰ migration through these environments. The goal of the (freshwater) for the trout diVered, reXecting their present study was to Wll the gap in the literature, deter- normal environments. mining unidirectional Xuxes of Na+ and Ca2+ in the whole Wsh (killiWsh and rainbow trout) during a pro- Determination of unidirectional sodium gressive increase in salinity by small step changes over and calcium Xuxes 6 h, simulating the challenges imposed by the tidal cycle in an estuarine environment. The results have been ana- Flux experiments were conducted using the radioiso- lyzed comparatively between trout and killiWsh, under topes 22Na+ (Perkin Elmer, Wellesley, MA, USA) or 123 J Comp Physiol B (2007) 177:519–528 521 24Na+ (McMaster University Nuclear Reactor) and SW (for O. mykiss experiments), 40 Ci in 80% SW, 45Ca2+ (Perkin Elmer). and 50 Ci in 100% SW. The increased amounts of radioactivity added to higher salinity waters kept spe- InXux experiments ciWc activities between treatments as close as economi- cally feasible. Water was sampled (5 ml) at the start Fish were submitted to a progressive, step-wise rise in (time 0 min) and after 30 min (for 24Na+), and 60 min salinity to simulate seawater entry in estuaries during (for 45Ca2+) for each salinity. Water samples for 24Na+ tidal Xow. All salinities were again made up with com- detection were placed in 20 ml polypropylene tubes, mercial sea salts (Instant Ocean™) diluted with Lake whereas those sampled for 45Ca2+ were stored in 20 ml Ontario water. The measured ion compositions are glass vials. Immediately following water sampling, Wsh shown in Table 1. Using a standard value of Na+ for were transferred to non-radioactive water (of the full strength seawater (470.2 mM/l; Barnes, 1954), the same salinity) for 5 min in order to remove any radio- nominal and actual values were: 10% = 15.6% SW, activity adsorbed to the external surface of the Wsh, 20% = 23.4% SW, 40% = 43.2% SW, 60% = 57.4% then terminally anesthetized in 0.5 g/l MS-222, SW, 80% = 75.5% SW, 100% = 93.4% SW.
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