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Resting Metabolic Rate, Critical Swimming Speed, and Routine Activity of the Euryhaline Cyprinodontid, Aphanius Dispar, Acclimated to a Wide Range of Salinities

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Resting Metabolic Rate, Critical Swimming Speed, and Routine Activity of the Euryhaline Cyprinodontid, Aphanius Dispar, Acclimated to a Wide Range of Salinities 590 Resting Metabolic Rate, Critical Swimming Speed, and Routine Activity of the Euryhaline Cyprinodontid, Aphanius dispar, Acclimated to a Wide Range of Salinities Itai Plaut* salt marshes, intertidal pools, etc.) show physiological adap- Department of Biology, University of Haifa at Oranim, tations that enable them to tolerate and survive extreme salinity Tivon 36006, Israel levels and ¯uctuations. Most studies on the physiological and behavioral effects of Accepted 6/5/00 euryhalinity and salinity have been done either with a narrow range of salinity, usually subranges between freshwater and full- strength seawater (Igram and Wares 1979; Nelson et al. 1996; Young and Cech 1996; Morgan et al. 1997; Kolok and Sharkey ABSTRACT 1997; Morgan and Iwama 1998; Plaut 1998, 1999a, 1999b; Shi- Specimens of the euryhaline cyprinodontid ®sh, Aphanius dis- kano and Fujio 1998) or under acute exposures to salinity par, collected in salt ponds, were acclimated to salinities of ¯uctuations (Davenport and Vahl 1979; Moser and Miller !1 (freshwater), 35 (seawater), 70, 105, and 140 ppt for 4 wk 1994). Data on the effects of long-term acclimation to extreme before measurement of oxygen consumption, critical swim- salinities (above seawater) on ®sh are rare. Recent studies have ming speed, and routine activity level. Oxygen consumption included only two species, the milk®sh, Chanos chanos (Swan- was similar in !1, 35, and 70 ppt (0.18 5 0.07 , 0.17 5 0.06 , son 1998), and the sheephead minnow, Cyprinodon variegatus and0.16 5 0.04 mL h21 g21, respectively [ mean 5 SD ]) but (Haney and Nordlie 1997; Haney et al. 1999). Few ®sh species decreased in 105 and 140 ppt (0.12 5 0.02 and 0.09 5 0.2 mL can tolerate extreme salinity, which may explain the small num- h21 g21, respectively). Critical swimming speed and routine ber of studies in this area (Nordlie and Haney 1998). activity levels showed the same trend. These results suggest a The cyprinodontid, Aphanius dispar (Teleostei, Cyprinodon- general decrease in physiological function of A. dispar at ex- tidae) is a euryhaline ®sh species found in a wide range of treme salinities. salinities, from freshwater to 1500% (»175 ppt) seawater in springs around the Dead Sea and in salt ponds in Atlit, Israel (Lotan 1969, 1971; Lotan and Skadhauge 1972; Skadhauge and Lotan 1974). Lotan (1971) showed that A. dispar is capable of Introduction maintaining its plasma osmotic pressure and ionic concentra- tion when acclimated to salinities from 16 to 105 ppt. However, Teleost ®shes are osmoregulators, maintaining their body ¯uids' freshwater acclimation reduced A. dispar plasma osmotic pres- osmotic concentration within a relatively narrow range, from sure to 70% (compared with ®sh in seawater), and acclimation » 260 to 400 mOsmol (Jobling 1995), usually different from the to 140 ppt increased its plasma osmotic pressure to about 135%. osmotic concentration of their environment. To osmoregulate, The ability of A. dispar to tolerate such a wide range of salinities ®sh actively create a ¯ow of ions and water in the opposite makes it an excellent candidate for studies of salinity effects on direction to the passive ¯ow imposed by the osmotic gradient. other physiological, ecological, and behavioral traits. In addition, they may reduce their gill membrane and/or in- In this study, I examine the effects of extremely high salinity tegument permeability to passive ¯ows. Most ®shes are capable on physiological and behavioral functions of A. dispar. I ex- of tolerating only a narrow range of salinities in their natural posed A. dispar to a range of salinities, from freshwater to 175 environment (Haney and Nordlie 1997), and exposure to sa- ppt (500% seawater) for 4 wk, and then measured oxygen linities substantially outside their range may exceed their os- consumption rate, critical swimming speed, and routine activity moregulatory capabilities and reduce their performance (Beam- level. ish 1978; Webb 1994). By contrast, some ®shes from habitats characterized by a wide range of salinity ¯uctuations (estuaries, Material and Methods *E-mail: [email protected]. Fish Collection, Holding, and Acclimation Physiological and Biochemical Zoology 73(5):590±596. 2000. q 2000 by The Adult Aphanius dispar (standard length [SL],31.9 5 0.5 mm University of Chicago. All rights reserved. 1522-2152/2000/7305-0030$03.00 [mean 5 SE , range 24.6±46.3 mm], body mass [BM], Effects of Wide Salinity Range Acclimation on Aphanius dispar 591 0.72 5 0.04 g [range 0.23±1.37]) were collected in the salt surements were performed both before and after the ponds of Atlit, near Haifa, Israel, by hand net. Salinity in the measurements of oxygen consumption of the ®sh. Each ®sh salt ponds at the time of collection was »57 ppt (»160% was used only once, and after the measurement, the ®sh were seawater) and water temperature was 277C. In the laboratory, weighed (50.01 g) in a preweighed beaker with water and ®sh were divided into ®ve groups, each subdivided among transferred to a new aquarium containing ªusedº ®sh. three aquaria. These aquaria contained continuously aerated Linear regression analysis of oxygen depletion over time was water from the salt ponds. Fish were treated prophylactically performed for each ®sh, and the regression coef®cient was used for 24 h with malachite green (0.15 ppm) and with methylene to calculate oxygen consumption: blue (1 ppm). Seven percent of the ®sh died within 3 d of collection; afterward mortality was very low. Two weeks after Ç 21 p # # # # Vo22(mmol h ) a 3,600 So V Pa/760, collection, salinity acclimation was begun. Salinity was changed by addition of arti®cial sea salt (Instant Ocean) or where a is the linear regression coef®cient (percentage s21), the by dilution with distilled water. Each day, the salinity was value 3,600 converts seconds to hours, So2 is oxygen concen- increased or decreased by »9 ppt. After 14 d, there were ®ve tration at 100% saturation in the experimental salinity at 257C groups in each of ®ve different salinities: freshwater (!1 ppt at an atmospheric pressure of 760 mmHg (Green and Carritt salt), 35, 70, 105, and 140 ppt. Then, ®sh acclimated to each 1967), V is the water volume in the closed respirometry system salinity were pooled to one larger tank for the rest of the measured speci®cally for each chamber (L), and Pa is the actual acclimation period (®ve salinity groups in ®ve tanks). Salin- atmospheric pressure in mmHg. Background (bacterial) oxygen ities were then monitored daily, and distilled water was added consumption measured in the blank chamber was always below accordingly to compensate for evaporation. Fish remained in 4% of the ®sh's oxygen consumption measurements. Correc- these salinities for 4 wk before experiments were begun. The tions were made for blank oxygen consumption rates if those aquaria were equipped with biological ®lters and temperature rates exceeded 1% of the experimental values per run. control (257517C), and ®sh were fed twice a day with Te- tramin ¯akes and live Daphnia magna and Artemia salina. Critical Swimming Speed (Ucrit) Swimming performance was measured as critical swimming Oxygen Consumption Measurements speed (Ucrit) in a water tunnel described in Plaut (2000). Post- The respirometer used in this study was described in detail in absorptive ®sh (24 h) were placed in the water tunnel con- Plaut (1999a, 1999b). This is a semiclosed respirometer (Stef- taining the relevant water salinity at a temperature of fensen 1989) with eight measuring cells. Water was directed 25750.57C. Water velocity was set to 4 cm s21 (about 1 SL 21 from an aerated (100% O2 saturation), temperature-controlled s ), and the ®sh were left undisturbed for 2 h to recover reservoir containing water at the experimental salinity to the from handling (Kolok 1991; Peake et al. 1997). Water velocity respirometer chamber and back to the reservoir by peristaltic was then increased in increments of 4 cm s21 at 5-min in- pumps via c-¯ex tubing. Three-way stopcocks made it possible tervals, until the ®sh fatigued. Fatigue was determined as the to disconnect a chamber from the reservoir and to direct the situation where the ®sh could no longer maintain position water ¯ow from the respirometer chamber to a cell with an against the current and were swept downstream and held oxygen electrode and back to the chamber in closed circulation. against the mesh screen at the downstream end of the water Thus, oxygen depletion in the chamber could be measured tunnel. Ucrit was calculated according to the equation (Brett without disturbance to the ®sh. 1964) Fish were not fed for 24 h before measurement. Postab- p 1 sorptive ®sh were placed in each of seven chambers (one cham- Ucrit Uiiiiii[U (T /T )], ber was left empty as a blank control) and left for 4±5 h to recover from handling. Preliminary tests showed that oxygen where Ui is the highest velocity maintained for the whole 5 21 21 consumption was high immediately after placement of the ®sh min (cm s ), Uii is the velocity increment (i.e., 4 cm s ), Ti in the chambers and then decreased to a stable value after is the time elapsed at fatigue velocity (min), and Tii is the approximately 2 h and remained stable for more than 24 h. At interval time (5 min). Ucrit's were calculated both as absolute the beginning of the measurement, ®sh were completely qui- (cm s21) and relative (SL s21) swimming speeds. escent in the chamber, so the oxygen consumption rates are regarded as resting metabolic rate (RMR). Following the re- Routine Activity Rate covery period, oxygen consumption was measured over about 15 min, long enough to detect depletion of oxygen concentra- Routine activity rates of A.
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