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Ion levels in the gastrointestinal tract content of freshwater and marine–estuarine teleosts

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Ion levels in the gastrointestinal tract content of freshwater and marine–estuarine teleosts
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  Ion levels in the gastrointestinal tract content of freshwaterand marine–estuarine teleosts Alexssandro G. Becker  • Jamile F. Gonc¸alves  • Marcelo D. M. Burns  • Joa ˜ o Paes Vieira  • Joa ˜ o Radu ¨nz Neto  • Bernardo Baldisserotto Received: 29 April 2011/Accepted: 1 December 2011/Published online: 11 December 2011   Springer Science+Business Media B.V. 2011 Abstract  This study investigated the relationshipbetweenionlevels(Na ? ,Cl - ,K  ? ,Ca 2 ? ,andMg 2 ? )inthe fluid phase and total chyme of the contents of thegastrointestinal tract segments of freshwater andmarine–estuarine teleosts collected in different salin-ities (0–34 ppt) in estuarine and freshwater portions of the Sa˜o Gonc¸alo channel, southern Brazil. In addition,the relative contribution of feeding and osmoregula-tion to the ionic content of each portion of thegastrointestinal tract of fishes collected in differentambient salinities was analyzed. There was no rela-tionship between salinity and ion levels in the fluidphase and total chyme of the segments of the gastro-intestinal tract when considering all species together.However, there was a significant positive relationshipbetween salinity and ion levels in the fluid phase andtotal chyme of two fish species (  Micropogonias furnieri  and  Genidens barbus ) collected in three ormore different salinities. In most species, ion levels inthefluidphaseandtotalchymechangedthroughoutthegastrointestinal tract, suggesting absorption, but theionoregulatory mechanisms of the gastrointestinaltract seem to vary according to species. Keywords  Fish    Estuaries    Intestinal fluids   Osmoregulation    Salinity Introduction Seawater teleosts live in a constant hypoosmotic statein relation to their surrounding environment, whichresults in diffusive water loss and excess salt uptake(Evans et al. 2005). The water loss occurs through the gill surface by osmosis and through the production of isoosmotic urine and is compensated by the ingestionof seawater (Shehadeh and Gordon 1969; Carroll et al. 1994; Ando et al. 2003; Evans et al. 2005). The gastrointestinal tract absorbs approximately 60–85%of the seawater that is ingested (Shehadeh and Gordon1969; Sleet and Weber 1982; Wilson et al. 1996; Grosell et al. 1999; Grosell 2007). The esophagus absorbs large amounts of Na ? and Cl - and is imper-meable to water, resulting in lower concentrations of Na ? and Cl - and low osmotic pressure in stomachfluids compared to the ingested seawater (Smith 1930; A. G. Becker    J. F. Gonc¸alves    B. Baldisserotto ( & )Departamento de Fisiologia e Farmacologia, UniversidadeFederal de Santa Maria, Santa Maria, RS 97105-900,Brazile-mail: bbaldisserotto@hotmail.comA. G. Becker    J. Radu¨nz Neto    B. BaldisserottoPrograma de Po´s-Graduac¸a˜o em Biodiversidade Animal,Universidade Federal de Santa Maria, Santa Maria, RS,BrazilM. D. M. Burns    J. P. VieiraInstituto de Oceanografia, Universidade Federal do RioGrande, Rio Grande, RS 96201-900, BrazilJ. Radu¨nz NetoDepartamento de Zootecnia, Universidade Federal deSanta Maria, Santa Maria, RS 97105-900, Brazil  1 3 Fish Physiol Biochem (2012) 38:1001–1017DOI 10.1007/s10695-011-9585-x  Hirano and Mayer-Gostan 1976; Kirsch and Meister 1982; Parmelee and Renfro 1983; Wilson et al. 1996). Na ? , Cl - , and K  ? are absorbed in the intestine,allowing for the absorption of water (Grosell et al.1999; Grosell 2007; Grosell and Taylor 2007). On the otherhand,theintestineabsorbsdivalentionsCa 2 ? andMg 2 ? at a lesser rate, causing these ions to precipitateas carbonate deposits during the absorption process(Kirsch et al. 1984; Wilson et al. 2002; Wilson and Grosell 2003; Grosell 2007; Kurita et al. 2008). Freshwater teleosts are always in a hyperosmoticstate in relation to their surrounding environment,which, consequently, results in loss of ions by diffu-sion, and gain of water by osmosis (Baldisserotto2003). Ions are absorbed by the gills (Evans et al.2005), and excess water is eliminated through theproduction of large amounts of diluted urine (Curtisand Wood 1991). The drinking rate of freshwaterteleostsislow(Fliketal.1995).Regardlessofwhether freshwater teleosts drink water, some ambient water isinevitably ingested along with food, and the digestivetract is an important part of osmoregulation, becauseion absorption could occur in the stomach (Buckingand Wood 2006a, b) and intestine (Baldisserotto and Mimura 1994; Baldisserotto et al. 2006; Bucking and Wood 2006a, b). The intestine (or pyloric ceca, when present) absorbs Na ? , Cl - , Ca 2 ? , and Mg 2 ? (andprobablyotherions)thatispresent infood(Dabrowskietal.1986;BuddingtonandDiamond1987;Boge ´ etal.1988; Baldisserotto et al. 1993; Kerstetter and White 1994; Baldisserotto and Mimura 1995; Bijvelds et al. 1998). The intestine also reabsorbs ions discharged bygastric secretion (such as Cl - ) (Hirano and Mayer-Gostan1976)andbilewhenfatenterstheintestine.Theintestineofseveralspeciesoffreshwaterteleostseitherabsorbs (Smith 1964; Skadhauge 1969; Nakamura 1985; Baldisserotto et al. 1996) or does not transport K  ? (Dabrowski et al. 1986; Baldisserotto et al. 1993). Several studies have analyzed ion levels in thecontents of the gastrointestinal tract of freshwater andseawater fishes. In those studies, fishes receivedcommercialdiets(Dabrowskietal.1986;Baldisserotto et al. 2004a), pilchards or squids (Taylor and Grosell 2006), or fasted (Wilson et al. 1996; Bucking and Wood 2006a, b; McDonald and Grosell 2006; Genz et al. 2008). To our knowledge, only one study analyzed the ionic content of the gastrointestinal tractof fish that had been recently collected from theirnatural freshwater environment (Becker et al. 2006). Changes in the ionic concentration throughout thegastrointestinal tract had previously been reported infreshwater and seawater teleosts (Dabrowski et al.1986; Wilson et al. 1996; Baldisserotto et al. 2004a; Becker et al. 2006; Bucking and Wood 2006a, b; McDonald and Grosell 2006; Veillette et al. 2006; Grosell 2007; Genz et al. 2008), suggesting a role for the intestine in osmoregulation.Estuaries are regions where marine and freshwatermeet, and frequent changes in salinity, temperature,dissolvedoxygen,andturbiditycontributeconsiderablytothephysiologicalmechanismsofthefishesthatliveinthese systems (Whitfield 1999). Marine fishes that use estuaries as feeding or nursery grounds are necessarilyeuryhaline species and efficient osmoregulators. Theenvironment that estuarine fish occupy exhibits dailysalinity fluctuations, which could affect the physiolog-ical mechanisms of the inhabitants (Prodo´cimo andFreire 2001; Freire and Prodo´cimo 2007). In southernBrazil, the upper limit of the Patos Lagoon Estuarymigratesseasonallyina year-to-yearbase(Mo¨lleretal.2001). Patos Lagoon is connected to the Mirim Lagoonby the Sa˜o Gonc¸alo Channel, a 75-km-long, 200–500-m-wide, 6-m-deep natural channel. The channel isobstructed by the Sa˜o Gonc¸alo Dam to prevent saltwater from intruding into the Mirim Lagoon during thedry season (Burns et al. 2006; Da Rocha et al. 2009). Some physicochemical water characteristics such astemperature,salinityanddissolvedoxygenweresimilarat upstream (freshwater) and downstream (estuarine)the Dam most of the seasons, with the exception of salinity,beinghigherinsummerfortheestuarineregionwhen compared with the freshwater region (Da Rochaet al. 2009). The purposes of this study were (1) to investigate the relationship between ion levels in thecontents of the gastrointestinal tract of fishes and theambientsalinityfromwheretheywerecollectedand(2)to analyze the relative contribution of feeding andosmoregulation to the ionic content of each portion of the gastrointestinal tract of fishes collected in differentambient salinities. These results will add to knowledgeof the function of the gastrointestinal tract in theosmoregulatory process of teleost fishes. Methods On three occasions (February 2005, April and Decem-ber2006), fishwere sampledfrom water with different 1002 Fish Physiol Biochem (2012) 38:1001–1017  1 3  salinities (Table 1) at the estuarine (downstream) andfreshwater (upstream) site of the Sa˜o Gonc¸alo Dam.Freshwater and marine–estuarine teleosts were col-lected using a shrimp trawl (10.5 m head rope,0.5 cm bar mesh in the center, 1.3 cm bar mesh onthe wings) deployed for 5 min between 5 and 8 mdepth by a wood boat 60 Hp engine. Shallow watersamples (1.0–1.8 m depth) were also taken on bothsidesofthedam usingabeach seine (9 m).Field watersalinity was measured at the same depth of collec-tion before collecting fish with a handheld salinitymeter.The resulting fishes were classified into two eco-logical guilds (see Table 1) following Garcia et al.(2003a): (1) estuarine dependents—marine- or fresh-water-spawningspecies foundinlargenumberswithinthe estuary during certain periods of their life cycleand (2) first-order freshwater vagrants—typicallyconfined to freshwater habitats and rarely occurringwithin the estuary (Vieira et al. 1998).After their collection, fishes were weighed, mea-sured, and then euthanized by severing the spinal cord(Table 1). The gastrointestinal tract was removed anddivided into the following segments: stomach, pyloricceca or anterior intestine, mid- and posterior intestine.In  M. furnieri , that has pyloric ceca, the next portionwas considered mid-intestine, as stated by Menin andMimura(1992).Therefore,comparisonofioncontentsof pyloric ceca of this species was made with anteriorintestine of other species. Specimens were used only if there was any content in the stomach and intestine (orpyloric ceca). The contents of the gastrointestinal tractsegments were collected separately, placed in previ-ously weighed Eppendorf tubes, and kept refrigerated.All samples of the contents of the gastrointestinal tractwere taken to the Fish Physiology Laboratory at theUniversidade Federal de Santa Maria. The contents of the segments of the gastrointestinal tract were centri-fuged at 7,000 rpm for 5 min to separate the fluid andsolid phases. The supernatant (fluid phase) was storedinEppendorftubesat - 20  Cforlater analysis,and thesolid phase was digested with nitric acid 2N at 75  Cfor 48 h. Following digestion, the solid phase wascentrifuged to obtain a clear supernatant that was alsostored in previously weighed Eppendorf tubes for lateranalysis. The ion concentrations of the total chyme inthe different segments of the gastrointestinal tractwere calculated using the following equation:Ionconcentrationintotalchyme ð mmolkgwetchyme  1 Þ : ð SPW ½ SPC Þþð FPW ½ FP Þ = TCW ; where SPW  =  solid-phase weight in the segment;[SPC]  =  solid-phase concentration in the segment;FPW  =  fluid-phase weight in the segment; [FP]  = fluid-phase concentration in the segment and TCW  = total chyme weight in the segment.Chloride concentration was measured according toZall et al. (1956). Sodium and K  ? concentrations weremeasured with a B262 flame spectrophotometer (Mic-ronal, Sa˜o Paulo, Brazil). Calcium and Mg 2 ? concen-trations were measured using a GBC 932AA atomicabsorption spectrophotometer (GBC Scientific Equip-ment, Victoria, Australia). Standard solutions weremade with analytical grade reagents (Vetec or Merck)dissolved in deionized water, and standard curves forfive different concentrations were made for each ion.The methodology of this experiment was approved bythe Ethical and Animal Welfare Committee of theUniversidade Federal de Santa Maria (process number23081.008434/2007-85).Alldataareexpressedasthemean  ±  standarderrorof the mean (SEM). Homogeneity of variances amongdata from fishes from different salinities was tested Table 1  Freshwater and marine–estuarine teleosts collected in different salinities in the Sa˜o Gonc¸alo channelSpecies Ecological guild Salinity Weight (g) Length (cm)  N  Micropogonias furnieri  ESD 0; 5; 24; 26; 29; 34 56.15  ±  2.41 12.10  ±  1.14 12 Pimelodus pintado  FRV 0; 5 816.13  ±  3.49 30.14  ±  1.41 12 Cyphocharax voga  FRV 0; 5 155.15  ±  2.12 28.23  ±  1.23 12 Genidens barbus  ESD 5; 24; 29 570.21  ±  2.85 28.35  ±  1.18 12The specimens were also classified according to ecological guilds (Vieira et al. 1998; Garcia et al. 2003a) Values are means  ±  SEM ESD  estuarine dependents (catadromous),  FRV   first-order freshwater vagrantsFish Physiol Biochem (2012) 38:1001–1017 1003  1 3  with a Levene’s test. Relationships between ion levelsand salinity were described using Sigma Plot softwareversion 11. Comparisons among the segments of thegastrointestinal tract within the same species weremade using a one-way analysis of variance (ANOVA)and Tukey’s test using the software Statistica ver. 5.1(Stat Soft, Tulsa, Okla). The minimum significancelevel was set at  P \ 0.05. Results Relationship between ions levels in the contentsof the gastrointestinal tract and ambient salinityThere was no relationship between salinity and ionlevels in the fluid phase or total chyme in the segmentsof the gastrointestinal tract when considering allspecies together. However, a separate analysis of thetwo marine–estuarine species collected in three ormore salinities (  Micropogonias furnieri  and  Genidensbarbus ) demonstrated a significant relationshipbetween these parameters and salinity.In  M. furnieri , there was a positive relationshipbetween salinity and Na ? levels in the fluid phase andtotal chyme of the stomach and mid- and posteriorintestine. However, in the anterior intestine, there wasa negative relationship (Figs. 1a, 3a). Chloride, Ca 2 ? ,and Mg 2 ? levels in the fluid phase and total chymedemonstratedapositiverelationshipwithsalinityinallthe segments of the gastrointestinal tract (Figs. 1c, 2c, etofluidphaseand,3c,4c,etototalchyme).K  ? levelsin the fluid phase and salinity demonstrated a negativerelationship in the stomach and anterior and mid-intestine, and a positive relationship in the posteriorintestine (Figs. 2a,4a). In  G. barbus , there was a positive relationshipbetween salinity and Na ? and Cl - levels in the fluidphase and total chyme in the stomach and anteriorintestine, but a negative relationship in the mid- andposterior intestine (Figs. 1b, d to fluid phase and 3b, d to total chyme). Salinity and K  ? levels in the fluidphase and total chyme demonstrated a positive rela-tionship with salinity in the stomach and mid- andposterior intestine, and a negative relationship in theanterior intestine (Figs. 2b, 4b). There was a negative relationship between salinity and Ca 2 ? levels in thefluid phase and total chyme in all segments of thegastrointestinal tract (Figs. 2d, 4d). Mg 2 ? levelsdemonstrated a positive relationship with salinity inall segments of the gastrointestinal tract (Figs. 2f, 4f). Ion levels in different segmentsof the gastrointestinal tractConcentrations of Na ? , Cl - , and K  ? in the fluid phaseofdifferentsegmentsofthegastrointestinaltractofthestudied species were very similar to those in the totalchyme. Contrarily, Ca 2 ? and Mg 2 ? concentrations inthe fluid phase of some segments of the gastrointes-tinal tract were lower than those measured in the totalchyme, except  G. barbus  (Figs. 5, 6, 7, 8, 9). Na ? levels in the fluid phase and total chyme of allspecies (except  G. barbus ) collected from salinities upto 26 ppt were significantly lower in the stomach thanin the anterior intestine. However, at higher salinities,the highest Na ? levels in the fluid phase and totalchyme were observed in the stomach (Fig. 5). In Cyphocharax voga  (except at 5 ppt),  Pimelodus pintado  and  M. furnieri  (except at 24 ppt) Cl - levelsin the fluid phase and total chyme were highest in theanterior intestine than in other segments. In  G. barbus (except at 5 ppt), the highest Cl - levels were observedin the stomach (Fig. 6).In all studied species, K  ? levels in the fluid phaseand total chyme were highest in the stomach oranterior intestine when compared to the mid- andposterior intestine, except in  M. furnieri  collected at26–34 ppt(highestK  ? levelsintheposteriorintestine)and G.barbus  collectedat26 ppt(highestK  ? levelsinthe mid-intestine) (Fig. 7). In all studied species, Ca 2 ? levels in the fluid phase and total chyme were higherin the stomach or anterior intestine than in the mid-and posterior intestine, except in the specimens of  P. pintado  (highest Ca 2 ? levels in the mid-intestine), G.barbus collectedat5 ppt(highestCa 2 ? levelsintheposterior intestine) (Fig. 8). Magnesium levels in thefluid phase and total chyme were significantly higherin the anterior intestine than in the other segments inthree studied species, but in  G. barbus , the highestMg 2 ? levels were observedinthe posterior intestineinspecimens collected in all salinities (Fig. 9). Discussion The ecological guild approach has been used byseveral authors to simplify information, and to allow 1004 Fish Physiol Biochem (2012) 38:1001–1017  1 3  for a better comparison between different systems(freshwater, estuarine and marine) and the physiolog-ical and ionoregulatory mechanisms of the fishespresent in an estuarine region (Elliott and Dewailly1995; Prodo´cimo and Freire 2001; Garcia et al. 2003a, b,2004;Burnsetal.2006;FreireandProdo ´cimo2007;Martinho et al. 2007; Da Rocha et al. 2009). The analysis of spatiotemporal distribution patternsshowed that first-order fishes inhabiting the freshwatersite in the upper part of Patos Lagoon can be passivelyflushed into the estuarine zone during periods of highfreshwater discharge and can remain in this zone forbrief periods (Garcia et al. 2003b, 2004). However, after the estuary returns to its normal hydrologicalconditions, those first-order freshwater fishes thatremain in the estuary could suffer a high degree of physiological stress caused by intrusion of salt waterinto the estuary (Garcia et al. 2003a). Only second- order freshwater fishes are able to remain on theestuary, namely small Cyprinodontiformes and largeCichlids. Contrarily, some euryhaline estuarine fishescan move into the freshwater site of Patos Lagoonduring part of their life cycle (Chao et al. 1985; Vieiraand Castello 1996; Barletta et al. 2010). 0 7 14 21 28 35    N  a   +    (  m  m  o   l   L   -   1    ) 060120180240300 A 0 7 14 21 28 35060120180240300 B 0 7 14 21 28 35    C   l   -    (  m  m  o   l   L   -   1    ) 060120180240300 st ai mi pi C Salinity 0 7 14 21 28 35060120180240300 D Salinity Fig. 1  Na ? and Cl - levels in the fluid phase of the differentsegments of the gastrointestinal tract of   Micropogonias furnieri ( a  and  c ) and  Genidens barbus  ( b  and  d ) collected in the Sa˜oGonc¸alochannelasafunctionofsalinity. st  Stomach, ai anteriorintestine,  mi mid-intestine,  pi posterior intestine.Data expressedas mean  ±  SEM ( n  =  12). The following equations were fittedto the data.  Micropogonias furnieri : Na ? (st:  y  =  35.03  ? 5.20  x ,  r  2 =  0.71; ai:  y  =  211.39  -  1.87,  r  2 =  0.71; mi:  y  = 33.27  ?  5.55  x ,  r  2 =  0.97; pi:  y  =  42.50  ?  3.18  x ,  r  2 =  0.73).Cl - (st:  y  =  33.67  ?  6.55  x ,  r  2 =  0.97; ai:  y  =  113.86  ?  4.43, r  2 =  0.78; mi:  y  =  103.68  ?  2.32  x ,  r  2 =  0.71; pi:  y  = 58.18  ?  2.81  x ,  r  2 =  0.73).  Genidens barbus : Na ? (st:  y  = 21.58  ?  6.14  x ,  r  2 =  0.74; ai:  y  =  44.27  ?  2.56,  r  2 =  0.71;mi:  y  =  188.18  -  2.93  x ,  r  2 =  0.97; pi:  y  =  126.19  -  1.52  x , r  2 =  0.97). Cl - (st:  y  =  100.83  ?  5.08  x ,  r  2 =  0.97; ai:  y  =  165.15  ?  0.62,  r  2 =  0.88; mi:  y  =  195.43  -  3.71  x ,  r  2 = 0.72; pi:  y  =  155.93  -  3.12  x ,  r  2 =  0.71), where  x  =  salinityand  y  =  ion levels in the fluid phase (mmol L - 1 )Fish Physiol Biochem (2012) 38:1001–1017 1005  1 3
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