McCormick and Saunders

7/30/2019 McCormick and Saunders

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AmericanFisheriesSocietySymposium1.211-229, 1987

Preparatory PhysiologicalAdaptations for Marine Life ofSalmonids:Osmoregulation,Growth, and MetabolismSTEPHEN D. MCCORMICK I AND RICHARD L. SAUNDERS

Department of Fisheries and Oceans, Biological StationSt. Andrews, New Brunswick EOG 2XO, CanadaAbstract.--Atlantic salmonSalmo salar, steelheadS. gairdneri, and several speciesof Pacificsalmon Oncorhynchus pp. undergo ransformation rom stream-dwellingparr to seaward-mi-gratingsmolts.Physiological, ehavioral,morphological, nd biochemical hanges ccur in freshwater in preparation or marine ife. The preparatorynatureof theseadaptationss reviewed anddiscussedwith particular emphasis on osmomgulation,metabolism, and growth. Functionalchanges n gill, kidney, gut, and urinary bladder result in increased salinity tolerance andhypoosmomgulatorybility. Someor all of thesepreparatory hysiological hangesmay reverse nthe absenceof exposure o seawater.Changes n lipid, protein, and carbohydratemetabolism,oxygenconsumption, nd aerobic espiratory nzymeactivity suggestncreased atabolism uringparr-smolt ransformation. hese ransient hangesn catabolismmay reflectenergetic emands f

the extensivedifferentiation ccurringduring ransformation.Although hem is increasedgrowthduring parr-smolt transformation,evidence or a hypothesized ncrease n scope or growth aftertransformations not convincing.We suggesthat differentaspectsof the transformation avedifferent developmentalpatterns, the timing of which is species-dependentnd responsive oenvironmental hange.Phylogenetic omparison f the differentiation f salmonidhypoosmomgu-latory mechanismsand migratory behavior suggests hat their evolution has occurred throughheterochrony.Transformation of the stream-dwellingparr to

the seaward-migratingsmolt is a significant ifehistory event in many salmonids. Various mor-phological,physiological, nd behavioralchangesoccur seasonally usually n spring),develop overa period of 1-2 months, and are presumablyadaptive for downstreammigrationand residencein the marine environment (see Table 1 and re-views by Hoar 1976; Folmar and Dickhoff 1980;Wedemeyer et al. 1980). Parr-smolt transforma-tion has for some time been of interest as adevelopmental process (Hoar 1939; Bern 1978)and recently has come under more intense scru-tiny as an important actor in the performanceofhatchery-rearedsalmonids n ocean ranchingandintensiveaquaculture Wedemeyer et al. 1980).In the presentundertaking,we review changesin osmoregulation,metabolism, and growth thatoccur during the parr-smolt transformation andthat are to some degree interrelated. Substantialinformation exists concerningchanges n salinitytolerance and metabolism, hough much remainsto be done in this area. Less is known concerninggrowth, and our discussion enterson what is notknown. By stating hypotheses concerning theinterrelationships f physiological hangesduring

Ipresentaddress: epartment f Zoology,Universityof California, Berkeley, California 94720, USA.211

the parr-smolt transformation, we hope to spurmore focused research in this most fascinatingand important area. In reviewing each of theseareas we develop a commonhypothesis:physio-logicalchangesduring the parr-smolt transforma-tion are preparatory adaptations,preparatory be-cause hey anticipatea change n environmentandadaptive because hey increase survival and fit-ness in a new environment.

Experiments conducted on the parr-smolttransformationhave, of necessity, examined iso-lated aspectsof development.Evidence for devel-opmental changesare then unified under the sin-gle term "smoltification." This has often led totwo disparate views that are equally wrong: thatthe transformation s a single and common proc-ess, or that it is a series of unconnectedchanges.Simpson 1985) stated the problem the followingway:

Perhapswe shouldalso be concerned est our use ofthe term "smoltification" encouragesa predilectionto the belief that the process s a single one with asingleor organically inked set of effectors. Stooltingought ather o be seenas the resultof a largenumberof distinct processes--the hange o particular pat-ternsof growth, the elaborationof neuronsassociatedwith long-termmemory, he development f differentpatternsof behaviour,major changes n metabolismand, finally, those changes n gill structure whichpermit he fish to pass rom a hypo- to a hypertonic


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212 MCCORMICKAND SAUNDERS

environment.There seems o me no a priori reasonfor supposing hat these processes volved simulta-neously,or for supposinghat they are linearly nter-dependentor have functionally inked endocrineme-diators.If we are successful n this review, we shall

have shown or suggestedboth the distinctionbetween these processes nd their interrelations.By adoptinga comparativeview, we hope toestablish hat differentaspectsof the parr-smolttransformationare present in different salmonidspecies nd hat heirpresence nddevelopmentalpattern are related to the timing and duration ofanadromyof a populationor species.Osmoregulation

Ontogenyof Salinity ToleranceOntogeneticchanges n salinity tolerance de-fined here as the ability to survive seawater>30%o) have been found in virtually all salmonidspeciesnvestigated.Whereassalmonid ggs an-not survivemore than a few days n seawater, heposthatchalevin has even poorer survival, pre-sumably due to loss of the chorion (Weisbart1968). Salinity toleranceof Atlantic salmonSaltnosalar alevinsdecreases s the water-impermeablevitelline membrane decreases in favor of a water-

permeable epithelium (Parry 1960; Talbot et al.1982). In contrast, salinity tolerance of chumsalmon Oncorhynchus eta increasesduring de-velopment of the alevin (Kashiwagi and Sato1969).After resorptionof the yolk sac, salinity oler-anceof all salmonidsncreaseswith size and age,and is closely tied to, and probablycausedby,increasedability to regulateplasma ons and os-molarity ollowingexposure o seawater (Parry1958, 1960; Houston 1961; Conte and Wagner1965; Conte et al. 1966; Wagner 1974b; McCor-mick and Naiman 1984b;Ouchi 1985).Conte andWagner (1965) and McCormick and Naiman(1984b)concluded hat size, not age, is the pri-mary determinant of increased seawater survivalfor steelhead Saltno gairdneri and brook troutSalvelinus ontinalis, respectively. Size-depen-dent salinity tolerance may be due to a more

Chinooksalmon 0. tshawytscha)re an apparentexception to this rule. Whereas other Oncorhynchusspeciesdevelop increased salinity tolerance throughincreased ability to regulate plasma ions, chinooksalmon develop an increased tolerance of elevatedplasma ons (Weisbart 1968).

favorablesurface-area-to-volumeatio for largerfish, or to a progressive evelopment f hypoos-moregulatory mechanismswith size, or to both.By comparingstudiesof similar design, McCor-mick andNaiman 1984b) oncludedhat salinitytolerance was also related to genus: the size atwhich seawater survival occurs is smallest forOncorhynchuspecies,arger or Saltnospecies,and largest or Salvelinus pecies.This phyloge-netic relationship ollows closely he durationofmarine esidenceshortestor Salvelinus pecies)characteristic f each genus,as pointed out byRounsefell 1958) and Hoar (1976).There is substantial vidence ndicating hatsize-dependenthanges n salinity tolerancearedistinctrom he more apid,seasonallyccurringchanges n salinity tolerance associatedwith theparr-smolt transformation.Salinity tolerance ofseasonally migrating Atlantic salmon, rainbowtrout Saltno gairdneri and coho salmon On-corhynchus isutch ncreases apidly over a pe-riod of 1-2 months, coincidingwith the normalperiod of migration and visible smolt characteris-tics Conteand Wagner1965;Komourdjian t al.1976; Clarke et al. 1978; Saunderset al. 1983,1985;McCormicket al. 1987).Thesechanges reindependent f temperatureexceptas it affectsdevelopmentalate), and are responsiveo photo-periodic cues (Saunders and Henderson 1970;Wagner 1974a;Komourdjianet al. 1976;Clarke etal. 1978; Johnstonand Saunders 1981; Clarke etal. 1985; Saunders et al. 1985; McCormick et al.1987).Althoughsomeseasonal eriodicity n salinitytolerancemay occur at all life stages Hoar 1965;Wagner 1974a), he ability to manifest arge sea-sonalchangesn salinity olerances size-depen-dent. Rainbow trout do not respond o seasonalcues with increased alinity toleranceuntil theyare at least i0 cm long (Conte and Wagner 1965).Similarsize-relatedimitations n the expressionof parr-smolt transformationhave been found forcoho salmon (Clarke et al. 1978) and Atlanticsalmon Elson 1957;Parry 1960).In distinguishing between size-dependentchangesn salinity oleranceand the size-depen-dent parr-smolt transformation, he degree ofsalinity tolerance becomes mportant. Atlanticand coho salmonparr of 10-12 cm can routinelytolerate i.e., survive or many days)a salinityof30%o Saundersand Henderson 1969; Clarke andNagahama1977).These ish may begin o die afterseveralweeks,however,and growth s inevitablypoor. Such differencesn the degreeof salinity


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PHYSIOLOGY OF THE SALMONID PARR--SMOLT TRANSFORMATION 213

tolerance are not limited to the parr stage. Smolt-size (14-17 cm) Atlantic salmon that are deniedseasonal cues through exposure to continuouslight can adapt to 30%oseawater, but cannotsurvive in 40%oas can normal smolts, and exhibitpoor feedingand growth n seawater Saunders tal. 1985; McCormick et al. 1987). This distinctionbetween the merely adequate or short-term sea-water survivalof parr and the completeadaptabil-ity of smolts s an important one. Its basis ies inthe increased hypoosmoregulatory ability ofsmolts (Parry 1960; Conte and Wagner 1965;Clark et al. 1978; Boeuf et al. 1978; SaundersandHenderson 1978; Hogstrand and Haux 1985) andperhaps other transport-relatedphenomenasuchas food conversion efficiency. Since parr cansurvive n seawater or extendedperiodsof time,however, one can justifiably ask what the adap-tive basis of increasedsalinity tolerance s at thetime of smolting. Rapid acclimation to highersalinities with fewer osmotic perturbationsmaypermit rapid movement hroughestuaries Cher-nitsky 1983; McCormick et al. 1985), and imme-diate resumptionof physiological nd behavioralprocesses hat might otherwiseresult n increasedpredationand interrupted eedingand growth.The developmentalprocesseshat result in sea-sonally increasedsalinity tolerance and hypoos-moregulatoryability are apparently reversible ffish remain in fresh water. Rapid summer de-creases n salinity tolerancehave been observedin rainbow trout (Conte and Wagner 1965), cohosalmon (Mahnken et al. 1982), and Atlanticsalmon Evropeytseva 1962). Generally known as"desmolting," this process may also result inreversion o a parr-like appearance see Folmar etal. 1982). Whether or not "desmolting" results na reversal of all physiological hanges ssociatedwith the parr-smolt transformation will be dis-cussed below.Functional Changes n OsmoregulatoryOrgans

Teleosts normally maintain their plasma osmo-!arity within a narrow range 290-340 mOsmol/L)irrespective of the salinity of the external me-dium, and failure to do so for prolongedperiodsresults in death. The transition from fresh water toseawaterrequiresa reversal rom net ion influx tonet ion efflux which is regulatedprimarily by thegills but also involves the kidney, gut and urinarybladder (for a review of osmoregulation n tel-eosts, see Evans 1979; Foskett et al. 1983). Inmost eleosts his reversal s initiatedby exposure

to a hyperosmoticenvironment. As the followingdiscussion houlddemonstrate,seasonalchangesin structure or function (differentiation) of theosmoregulatorymachinery, which occur prior toand in anticipation of exposure to seawater, areresponsibleor increased alinity oleranceduringthe parr-smolt transformation.This seasonaldif-ferentiation s likely to be the result of qualitativeand quantitativechanges n gene expression, hehormonal control of which has yet to be eluci-dated (Dickhoff and Sullivan 1987, this volume).In considering he mechanismsof osmoregula-tory change as well as metabolismand growth),we shall consider only those salmonid specieswhich show a rapid (1-2 month), reversible, sea-sonallycued increase n salinity tolerance. In thisgroup, Atlantic, coho, and masu salmon On-corhynchus nasou and steelhead have receivedthe greatestattention. There are, however, inher-ent difficulties n conducting nd comparingstud-ies on a developmental phenomenon that occursover many weeks but which has no absolutemorphological criterion (Gorbman et al. 1982).Many researchers have used appearance (oftenthe degreeof silveringor fin darkening) as a solecriterion to distinguish molts rom nonsmolts. naddition o the subjectivenature of this criterion,it has proved o be highly variable under artificialculture conditionsand is often "uncoupled" fromother aspects of the parr-smolt transformation(Wedemeyer et al. 1980). Seasonal changes intemperaturemay introducephysiologicalchangesindependentof developmental phenomena (Vir-tanen and Oikari 1984). Differences in methodol-ogy, species, and size further increase the diffi-culties of assessing xperimental results. In mostcases, he developmental rocess s clear enough(or the experimental onditioncontrolledenough)in spite of these confounding actors. We shallattempt to point out the exceptions,particularlywhen conflicting esults are apparent.Gills.--For a variety of euryhaline teleosts, gillNa+,K+-ATPase activity increasesafter transferfrom fresh water to seawater Epstein et al. 1967;Kirschnet 1980). Ionic and electrical gradientsgenerated by this enzyme are central to currentmodels of branchial ion fluxes (Maetz and Garcia-Romeau 1964; Silva et al. 1977). Increases n gillNa+,K+-ATPase occur in several salmonid spe-cies in freshwater prior to seawater entry. Suchincreases in coho salmon (Zaugg and McLain1970; Giles and Vanstone 1976a; Lasserre et al.1978), chinook salmon (Hart et al. 1981; Buckmanand Ewing 1982), rainbow trout (Zaugg and Wag-


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214 MCCORMICK AND SAUNDERS

her 1973), and Atlantic salmon McCartney 1976;Saundersand Henderson 1978; Boeuf et al. 1985;McCormick et al. 1987) occur seasonallyand inphasewith migration and increasedsalinity toler-ance (Figure 1). Most of the gill Na+,K+-ATPaseactivity and ion transport capacity resides inmitochondria-rich chloride cells (Epstein et al.1980; Foskett and Scheffey 1982). Chloride cellsincrease in number in gill opercular epithelium(Loretz et al. 1982)and changemorphology n gillfilaments (Richman 1985) of freshwater cohosalmonsmolts.Langdonand Thorpe (1985) oundincreased size and number of chloride cells inAtlantic salmon n early spring ust before attain-ment of maximum salinity tolerance.D. R. N. Primmett, F. B. Eddy, M. S. Miles,C. Talbot, and J. E. Thorpe (personalcommuni-cation)measuredwhole-bodyNa + fluxes n juve-nile Atlantic salmon; these fluxes are generallyassumed o reflect the function of gill epithelium.During parr-smolt transformation, Na + fluxchanged from net influx (characteristicof fresh-water teleosts) to net efflux. However, net Na +efflux is not an absolute equirement or increasedsalinity tolerance since maximum salinity toler-ance was achieved after Na + flux had returned toa net influx. Iwata et al. (in press) ound develop-mental changes in whole-animal transepithelialpotential (TEP) of coho salmon. The TEP of coho

salmon n fresh water decreased radually rom 6mV in early February to -12 mV in mid-April. Infish transferred to seawater for 12 h, TEP was 5mV in February and increased to 16-18 mV inApril throughAugust. Taken together, these re-sults indicate that developmental changes inmechanismsor ion transport ound n freshwater-adaptedsmoltsare important or seawateradap-tation.Kidney and urinary bladder.--The urine flowand water excretory rates of rainbow trout smolts

in fresh water decrease relative to those in bothpre- and postsmolts and are due entirely to areduction in glomerular filtration rate (Holmesand Stainer 1966). Urine excretory rates of so-dium and potassium nd total osmolarityare alsoreduced in smolts. (Decreased urine flow andglomerular iltration occur in euryhaline eleostsafter exposure o seawater Hickman and Trump1969],and the resultsof Holmes and Stainer maybe interpretedas a preparatoryadaptation.) How-ever, the "seasonal" temperatures, variable tim-ing of measurements, nd use of appearanceasthe sole smolt criterion make it difficult to inter-pret these results. Recent work by Eddy andTalbot (1985) indicates hat urine productionbyjuvenile Atlantic salmon(> 15 cm) increasesdur-ing springcoincidentwith increasing ill Na +,K +-ATPase activity. These conflicting results con-

MaximumSalinity

ToleranceI.W Seawater

%%

(Fresh Water)

Seawater

Fresh WaterMarch I April I MayParr Smolt

FIGURE 1.--Functional changes n osmoregulatory rgans during the parr-smolt transformation.Functionalchanges normally associated with osmoregulation n seawater occur in fresh water and result in increasedhypoosmoregulatorybility and salinity tolerance. n the absenceof exposure o seawater, hese changesarereversible.


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cerning alteration of kidney function during parr-smolt ransformationare, at present,unexplained.Declines n kidney Na +,K+-ATPase activity injuvenile Atlantic salmon n springwere reportedby McCartney (1976). Virtanen and Soivio (1985)reported hat kidney Na+,K+-ATPase activity ofjuvenile Atlantic salmon aised n brackishwaterfluctuates considerablyduring spring, falling inearly spring hen rising o high evels n mid springand falling again n late spring.S. D. McCormickand R. L. Saunders (unpublisheddata) found noseasonal hange n kidney Na+,K+-ATPase activ-ity in freshwater-rearedAtlantic salmon, nor wasthe activity level of this enzyme different fromthat in fish exposed o continuous ight (conditionsthat inhibit physiological hanges ssociatedwithtransformation). It should be noted that, unlikegill Na+,K+-ATPase activity, kidney Na+,K +-ATPase activity of Atlantic salmon changesslightly or not at all following increases n envi-ronmentalsalinity Virtanen and Oikari 1984;Mc-Cormick et al., unpublisheddata).Loretz et al. (1982) found that Na + and Cl-reabsorptionby the urinary bladderof freshwater-adapted coho salmon did not change betweenMarch and June. However, developmentalchanges in the urinary bladder were detectedwhen coho salmon were experimentally adaptedto seawaterover this sameperiod. In May, whenseawater survival was low, Na + and Cl- reab-sorption by the urinary bladder of seawater-adapted fish was at high levels characteristicofsalmon in fresh water. In June, when seawatersurvivalwas high, Na + and Cl- reabsorptionwasabolished. While no functional differentiation ofthe urinary bladder was apparent n fresh water, aclear increase in its capacity to respond to seawater had occurred.Gastrointestinal ract.--Increased drinking rateand absorption of water and salts across gutepitheliaoccur followingadaptationof euryhalinetelosts to seawater. Collie and Bern (1982) foundthat the capacity for net fluid absorptionof theintestine ncreased wofold in freshwater-adaptedjuvenile coho salmon between March and May,and that high values n May were similar to thoseof salmon adapted to seawater. Reversion ofintestinal net fluid absorption o prespring evelsoccurred in early autumn in fish held in freshwater. Developmental changes in drinking rateassociated with the parr-smolt transformationhave yet to be investigated.

Consequences f Developmental Changeson Osmoregulation n Fresh WaterThe previous section has established hat sea-sonal ncreases n salinity tolerance and hypoos-moregulatory ability occur in conjunction with

increases n gill Na+,K+oATPase activity, quan-tity of gill chloride cells, intestinal net fluid ab-sorptionand other osmoregulatory hanges hatare characteristic f seawater-adaptedeleostsbutwhich occurprior to seawaterentry (Figure 1). Ifthese mechanisms are detectable in smolts infresh water, are they also fully functional in vivo,and do they, therefore, produce osmoregulatorydifficulties (water gain and ion loss) for smolts infresh water? D. N. R. Primmett, F.B. Eddy,M. S. Miles, C. Talbot, and J. E. Thorpe (per-sonal communication)have recently argued thatincreases n ion fluxes across the body surface,which are presumablyhormone-induced, recedeand are responsibleor increases n gill Na +,K +-ATPase activity and other osmoregulatorychangesduring transformation. Whereas we havestressedthe adaptive nature of these changes,these researchers suggest hey are primarily aconsequenceof the loss of freshwater osmoregu-latory capacity (see also Langdon and Thorpe1985; Simpson 1985). It shouldbe stressed,how-ever, that in each of these scenarios a seasonaldifferentiation occurs that results in increasedsalinity olerance, which is clearly adaptive for aseaward-migrating ish. It is still unclear that allthe osmoregulatory hangesportrayed n Figure 1are functional in the freshwater smolt (e.g.,Na+,K+-ATPase ncreasesmay be demonstrableby enzymologicalassay of gill homogenates utthe enzyme may not be functionally active invivo), or whether hey require nductionby expo-sure to seawater. In either event, we emphasizethat the physiologicalmechanismsnecessary orlong-term survival in seawater take several daysto develop in euryhaline species (Foskett et al.1983); in smolts, these adaptations are already inplace and may be rapidly induced to becomefunctional upon exposure to seawater.Decreases n plasma chloride (in the late parrstage:Houston and Threadgold1963)and musclechloride (in migratingsmolts: Fontaine 1951) oc-cur in Atlantic salmon in fresh water. Plasmaosmolarityhas been reported to decreaseduringsmoltingof masu salmon Kubo 1953), to be morevariable in smolting Atlantic salmon (Koch andEvans 1959), and to increaseabsolutely n post-smolt Atlantic salmon Parry 1961). On the other


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hand, a number of studies ailed to find significant'changes n plasmaor muscle onscoincidentwiththe parr-smolt transformation see Folmar andDickhoff 1980).The variety and conflict of results in the inves-tigationscited above suggest hat environmental,experimental, and speciesdifferencesmay haveinfluenced the results. Indeed, regulation ofplasma and cellular ions of salmonids n freshwater can be affected by temperature (Kubo1955), size (McCormick and Naiman 1984a), ac-

tivity (Wood and Randall 1973), water quality(Eddy 1982),pH (Saunderset al. 1983),and stress(Schreck 1982). We have recently conducted astudy in which rearing temperature for Atlanticsalmon was held constant (5-8C) from Februaryto August (McCormick and Saunders, unpub-lished data). The interaction of seasonaland de-velopmentalphenomenawas controlledby exam-ining fish under both a simulatednatural photope-riod and continuous ight. (Atlantic salmon aisedunder continuous ight grow normally but do notundergoa parr-smolt transformation:Saunders tal. 1985;McCormick et al. 1987.) A slight


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observations n changes n body composition,oxygen consumption, and mitochondrial enzymeactivity. We wish to addresswo generalhypoth-eses during the review of this evidence. First,doesa metabolic ncreaseoccur during he parr-smolt transformation.'?Second, is such a meta-bolic increasedue to energetic equirementsofdifferentiation or to increased anabolism associ-ated with growth or to both (Figure 2).Changes n Body Composition

Several changes n carbohydrate metabolismare concurrent with the parr-smolt transforma-tion. Reduction of liver and muscle glycogenoccurs in spring n Atlantic and coho salmon nboth the presenceand absenceof migratoryactiv-ity (Fontaine and Hatey 1953; Malikova 1957;Wendt and Saunders 1973; Woo et al. 1978).Blood glucosehas been reported to increase nAtlantic salmon (Wendt and Saunders 1973) andto decrease n coho salmon (Woo et al. 1978) at

Differentiation

Growth

DifferentiationrowthGi I I i i iMarch April May June JulyParr SmoltFIGURE 2.--Possible causes of metabolic increase

during the parr-smolt transformation. ncreases n met-abolic rate due to differentiationand growth can beassociatedwith catabolism nd anabolism, espectively.Increased growth rate (which occurs in both parr andsmolts in spring) will, a priori, result in increasedmetabolic rate. There also is evidence for increasedmetabolic ate due to differentiation.Arrows suggesthemagnitudes f the influence n metabolic ate exertedbydifferentiationD) and growth G) actingseparately rtogether.

the time of the parr-smolt transformation. Fon-taine et al. (1963) reported that the powerfulhyperglycemic agents adrenaline and noradrena-line are at their highest evels in Atlantic salmonduring he final stages f smoltingn April-May.'With heexceptionf decreasedlood lucose,the abovechanges re often associatedwith short-term stress Schreck1981).The increased uscep-tibility of smolts to stress has been noted byseveral authors (Wendt and Saunders 1973;Schreck1982).Seasonal hangesn enzymeactiv-ity associatedwith glycogenolysisnd glycoge-nesis,however,suggest morepermanent hangethat is unrelated o stress.Sheridan et al. (1985b)found that liver phosphorylase-a ctivity (glyco-genolysis)of coho salmon ncreasesby 64% be-

tween March and April, while uridine phosphateformation (glycogenesis) ecreasesby 54% fromMarch to June.Total body protein decreasedby 10% betweenFebruary and April in large (>14 cm)juvenilerainbow trout, but not in smaller fish under thesame conditions Fessler and Wagner 1969). Incontrast, Woo et al. (1978) found no change nliver and muscleprotein content of coho salmonparr and smolts. Serum protein content of cohosalmon smolts was 15% lower than in parr orpostsmolts Woo et al. 1978). Cowey and Parry(1963) found a 30% increase n muscle content ofnonprotein nitrogenous constituents of smoltsover that in parr, due almost entirely to increasedcreatine content. The authors suggested hat in-creased reatinemay be due to greateravailabilityof N-phosphorylcreatine or endergonic eactionsor to increased metabolism of several amino acids

for which creatine s an end product.Cowey and Parry (1963) and Fontaine and Mar-chelidon (1971) could find no differences n totalamino acid content of the brain or muscle betweenAtlantic salmonparr and smolts they were able tosampleboth laboratory-rearedand wild fish). Thelevels of particularamino acids did change,how-ever. Threonine and glutamine contents of thebrains of smolts ncreased,while muscle glycineand taurine decreased (Fontaine and Marchelidon1971). Decreased muscle taurine content of Atlan-tic salmonsmoltswas also found by Cowey andParry (1963). Fontaine and Marchelidon (1971)explained these changesas ramificationsof sev-eral physiological hangesduring the parr-smolttransformation.G!ycine (a precursorof purines)may be involved n events eading o deposition fguanine and hypoxanthine in skin and scales,which results in silvering (Johnstonand Eales


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1967). Taurine is important for intracellular sos-motic regulation in teleosts (increasing whenplasma osmolarity increases:King and Goldstein1983) and may be lowered in response o osmo-regulatorychanges n fresh water or be distributedto other more sensitive issues n preparation orhyperosmotic regulation. Increases in threoninein the brain, which is under insulin control inmammals (Okumura et al. 1959), may be a by-product of increased nsulinconcentration esult-ing from glycemic fluctuations. While these in-triguing suppositions ave yet to be given exper-imental support, hey underline he importanceofdistinguishingcause and effect in this complexdevelopmentalprocess.Total body and muscle lipid decreasesmark-edly in spring n juvenile Atlantic, coho, and masusalmon and in rainbow trout coincident with otherparr-smolt changes Vanstone and Markert 1968;Fessler and Wagner 1969; Saundersand Hender-son 1970, 1978; Ota and Yamada 1974a, 1974b;Komourdjian et al. 1976;Farmer et al. 1978;Wooet al. 1978; Sheridan et al. 1983). These changesdo not occur in small juveniles (parr), are notdependenton changes n activity or temperature,and return to prespring levels by late summerwhen fishes are retained in fresh water (Malikova1957; Fessler and Wagner 1969; Ota and Yamada1974a, 1974b; Farmer et al. 1978; Saunders andHenderson 1978; Woo et al. 1978). Moisture con-tent of muscle varies inversely with lipid content(Farmer et al. 1978; Saunders and Henderson1978;Woo et al. 1978) hough his appears o be acommon eature of teleostsand not peculiar o theparr-smolt transformation Phillips 1969).Sheridan and co-workers (Sheridan et al. 1983,1985a, 1985b; Sheridan and Allen 1983) haveexamined lipid dynamics of coho salmon andrainbow trout in some detail. Lipid content ofserum, liver, and muscle (white and red) is de-pleted by up to 60% in spring.Mesenteric at doesnot fluctuate. Large amounts of triacylglycerol(normally used as energy storage) n muscle andliver are reducedmore than other lipid classes.Areorganization of the fatty acid composition alsooccurs. Increased amounts of long-chainpolyun-saturated atty acids and decreased inoleic acid,characteristic of marine teleosts, occur in freshwater during the parr-smolt transformation. Sim-ilar changes n lipid compositioncoincidentwiththe migratory period were observed n juvenileAtlantic and masu salmon (Lovern 1934; Ota andYamada 1974a, 1974b). The adaptive value ofthese changes s as yet unknown, though sugges-

tions for a role in osmoregulationhave been made(Sheridan et al. 1985a).The biochemical asesof changes n lipid me-tabolismhave also been nvestigated Sheridanetal. 1985b).Lipolytic rate (measuredby the releaseof 4C-oleic cid rom 14C-triolein)ncreases ne-to three-fold in liver, red muscle, and mesentericfat in coho salmon over a 4-month period inspring.During his sameperiod3H20 ncorpora-tion into fatty acids of liver and mesenteric at washalved, though no difference in lipogenesis ofneutral ipids was detected.These resultssuggestboth a reorganizationof lipid composition for amarine existence and increased catabolism asso-ciated with the parr-smolt transformation.Oxygen Consumption

Direct measurement f oxygenconsumptionsdifficult to assessbecause of the relatively highindividual variation, dependenceon temperatureand size (often requiringuse of regressions,whichcan obscuredata), effectsof variousactivity lev-els, and differential response o handlingstressorconfinement.Baraduc and Fontaine (1955) foundresting, weight-specificoxygen consumptionofwild Atlantic salmon parr at 8C was 25% lowerthan for wild smolts.Power (1959), working withAtlantic salmon from an Arctic environment,found a temperaturedivergence n oxygen con-sumption:smoltshad lower oxygen consumptionthan parr below 13.5C, but higher oxygen con-sumption bove his temperature.This may be theresultof increased ctivity in responseo temper-ature. Higgins (1985) reported oxygen consump-tion as a function of differential growth and theparr-smolt transformation in Atlantic salmon.When oxygen consumption per animal was re-gressed o a common size, rapidly growing fishhad higher oxygen consumptionat 7.5C thanslower growing fish. Smolts (based on externalappearance),however, had lower weight-specificoxygenconsumption han nonsmolts. n one of thefew reported studies n which activity levels weretaken into account, Withey and Saunders 1973)found that postsmoltAtlantic salmonhad higherrates of oxygen consumption than nonsmolts.Without more critical studies aking activity levelinto consideration, t is difficult to arrive at a firmconclusionconcerningchanges n oxygen con-sumptionduring the parr-smolt transformation.Respiratory EnzymesMitochondrial enzyme activities are indicativeof tissue espiratory ate or respiratorypotential,


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though some enzymes are more representativethan others (Ericinska and Wilson 1982). Succi-nate dehydrogenase Chernitsky and Shterman1981;Langdonand Thorpe 1985),citrate synthaseand cytochrome-c oxidase activities (S. D. Mc-Cormick and R. L. Saunders,unpublisheddata)increase n gill homogenates f Atlantic salmonconcurrentwith the parr-smolt transformation.At first glance, these results would appear tocoincide with the observed increase in numbers ofmitochondria-rich chloride cells discussed earlier.Although chloride cells have greater respiratoryenzyme activity than other gill cells (Sargentet al.1975), whole-gill homogenatesof fish which areacclimated to seawater do not have different res-piratory enzyme activities (Epstein et al. 1967;Conte 1969;McCormick et al., unpublished ata;for exceptions, see Sargent et al. 1975; Langdonand Thorpe 1984). Increases n gill respiratoryenzyme activity observed during the parr-smolttransformation ppear o go beyondwhat may berequired for steady-state osmoregulationonceseawater acclimation has occurred. The increasemay be required or preparatorydifferentiationofthe gills, or perhapsmay aid in seawateradapta-tion during initial acclimation.Blake et al. (1984) ound up to 50% increasesnmitochondrial concentration, and in the activitiesof succinate dehydrogenaseand cytochrome-coxidase, in the livers of large (>16 cm), silveryAtlantic salmon relative to those of parr. Simi-larly, McCormick and Saunders (unpublisheddata) found that liver citrate synthase ctivity ofsmolt-size Atlantic salmon increased 25% be-tween March and June (coincident with increasesin gill Na +,K+-ATPaseactivity)and subsequentlydeclined to basal levels in August. These results,in combinationwith increasedipolyticand glycoogenolyticenzyme activities n coho salmon ivers,suggest hat increased catabolism occurs in theliver during the parr-smolt transformation.The evidence summarized here indicates thatthere is both reorganizationand enhancementofmetabolicactivity during he parr-smolt ransfor-mation. Unfortunately, there is relatively littleinformationon the reversibilityof these changes.Metabolic alterationswhich are adaptations orseawaterentry, suchas changesn lipid composi-tion, are analogous o preparatory osmoregula-tory changes nd are probably ost if the animalsare maintained in fresh water. Metabolic in-creases appear to be at least partly catabolic,owing possibly o the energeticdemandsof differ-entiation. Recovery of pretransformationbody

compositionMalikova 1957;Woo et al. 1978)andreturn of liver respiratory enzyme activity topresmolt evel in summer ndicate hat increasedcatabolismsubsides fter the transformation, irre-spectiveof the environmentalsalinity.Growth

The apparent size threshold of the parr-smolttransformationmay rule out growth rate as theprimary stimulus or differentiation.Yet patternsof growth will undoubtedlyaffect the year ofoccurrenceof the parr-smolt transformationandperhaps also its timing and intensity (Clarke1982). The bimodal growth pattern of Atlanticsalmon s a goodexampleof the complex elation-shipbetweengrowthand transformation.Bimodallength-frequency distributions of laboratory-reared Atlantic salmoncan be distinguisheddur-ing the first autumn following hatching and havebeen attributed to an increase in growth rate ofupper-mode ish (Kristinssonet al. 1985)and to adecline n growth rate owing to reducedappetiteof lower-mode fish (Thorpe et al. 1982; Higgins1985; Thorpe 1987a). Though these distinctionsare controversial, t is clear that upper-and lower-mode fish do not further subdivide even after thefish in each mode are placed in separate tanks(Thorpe 1977). Upper-mode fish invariably be-come smolts in I year, while lower-mode malesundergoa high rate of sexual maturation duringtheir first autumn and normally require anotheryear to achieve smolt size. Existence n the lowermode, however, does not preclude undergoingtransformation; levatedearly winter temperatureresulting n higher growth and a greater size inearly spring will result in normal smolt appear-ance and performance (Saunders et al. 1982;Kristinsson1984).The relationshipbetween highgrowth rates of upper-mode ish and the parr-smolt transformation may be indirect, coupledonly by the size dependence f the transformation(Thorpe et al. 1982). Alternatively, bimodalitymaybe an early manifestation f parr-smolt rans-formationsuch hat changes aking place n springare the climax of processeswhich have beenproceedingsince the previous autumn (Thorpe1986).Under natural conditions, juvenile Atlanticsalmonmay beginseawardmigrationat 2-4 yearsof age, and at weightsof 30-50 g. They frequentlyattain weights of 1.5-2.5 kg in their first year atsea. Increasedgrowth is undoubtedlydue in largepart to increasedquantityand quality of food andmore favorable year-round emperatures Gross


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1987, his volume). It is presentlyunclearwhethersmoltsundergoa physiological hange esulting nincreased cope or growth (maximum ood ntakeminus hat necessary or maintenance:Brett 1979)at temperatureand ration levels characteristicofthe marine environment.

Increased growth of juvenile salmon occurs nspring concurrent with other transformation-re-lated changesand in direct response o increasingphotoperiod (Saunders and Henderson 1970;Knutsson and Grav 1976; Komourdjian et al.1976; Clarke et al. 1978; Johnston and Saunders1981; Higgins 1985). Though evidence or a com-mon growth responseof all salmonids o increas-ing photoperiods lacking Brett 1979), ncreasedgrowth under increasingphotoperiodalso occursin Atlantic salmonparr (Higgins 1985).One pecu-liar aspectof growth during he parr-smolt trans-formation is a decrease in condition factor (100 weight/length3;eeWedemeyer t al. 1980).Thismay be the result of a relative weight loss due tocatabolism, or to an increased growth in length,such that increase in length outstrips growth inweight. Several authors have suggested n adap-tive change n morphology o explain the latterhypothesis Thorpe 1982).In the absenceof salinity effects, are parr andsmolt distinguishable n their scope for growtheither during or after the parr-smolt transforma-tion? Higgins (1985) found that, at maximumration and identical thermal regimes, Atlanticsalmon in the upper size mode (incipient smolts)had a higher instantaneousgrowth rate in springthan lower-mode fish (parr), despite the smallersize of lower-mode ish which would, other thingsbeingequal, result n higher nstantaneous rowthrates (Brett 1979). It is unclear, however, whetherthis result is a function of the bimodal-growthpattern, the parr-smolt transformation,or both.We have recently compared the summer growthin fresh water of Atlantic salmon smolts (50 g)with juveniles (50 g) exposed o continuous ightthat inhibited at least the osmoregulatoryaspectsof the transformation (McCormick et al. 1987).Instantaneousgrowth rate of smoltsand of fish ncontinuous ight over a 6-week period at constanttemperature (13C) was the same (1.8%/d). Wehave concluded hat either continuous-lightreat-ment doesnot inhibit all aspectsof the parr-smolttransformation, or that an increase in scope forgrowth (at maximum ration and at 13C)does notaccompany ransformation n Atlantic salmon.This limited evidence does not favor eitheracceptanceor rejection of an increasedscope or

growth accompanyinghe parr-smolt transforma-tion. If it does ndeedoccur, it is likely to be largeand more easily detected in species such as At-lantic salmon which spend longer periods (2-5years) in fresh water. Environmental effects ongrowth and scope for growth may also changeafter transformation. There is indirect evidencethat the optimum emperature or marine growthof Atlantic salmon s lower than that for presmoltgrowth in fresh water (Reddin and Shearer 1987,this volume; Saunders 1987). Many fishes showreduced hermal optima for growth after the earlyjuvenile stage (Hokanson 1977; Brett 1979; Mc-Cauley and Huggins 1979; Jobling 1981). Photo-periodic response may also change. Whereasgrowth of Atlantic salmonparr drops sharply inearly autumn (decreasingphotoperiod), despitefavorable temperature and ration levels (R. L.Saunders, unpublisheddata), postsmolts n seacagesappear to continue growing rapidly in au-tumn until temperatures all below 4C (Sutterlinet al. 1981).Suchan alteration n growth responseto photoperiodhas been observed n the bimodalgrowth pattern of juvenile Atlantic salmon(Kristinsson1984;Higgins 1985;Kristinssonet al.1985; Thorpe 1987a). Substantiationor rejectionof these suppositions ould greatly increase ourunderstandingof ontogeneticand environmentalinfluenceson growth in teleosts.

ComparativeAspectsof the Parr SmoltTransformationThe variety of differentiativeprocesseswhichoccur and their responsivenesso photoperiodiccues underline the developmental nature of theparr-smolt transformation.This developmenthasoften been viewed as a single, size-related eventwhich occurs seasonallyand is reversible in theabsenceof sea water (Figure 3A). Although thismay be true for some aspectsof the transforma-tion, other aspects, such as silvering, salinitytolerance, ndgill Na +,K+-ATPase ctivity,oftendisplay slight but significantseasonal hythms inthe absenceof "real" or "total" changesassoci-ated with transformation Hoar 1965, 1976; Saun-ders and Henderson 1978; Langdon and Thorpe1985; McCormick et al. 1987). Perhaps we canmore correctly view these developmental pro-cessesas an interactionor synergism Figure 3D)between prior development Figure 3B) and sea-sonal rhythms (Figure 3C) which manifests tself

in a critical size and season for transformation.Each componentof the parr-smolt transformationmay possess differentgradientof thesedevelop-


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PHYSIOLOGY OF THE SALMONID PARR-SMOLT TRANSFORMATION 221

mental ypes. The existenceof differentdevelop-mental patternsemphasizes he adaptivevalue oftemporal orchestrationof the many changes hatoccur during the transformation.Otherwise, theymay occur as isolated events or physiologicaldevelopmentswhich fall short of the attributesrequired for long-term marine residence.

ATime

FIGURE3.--Developmental patterns that may occur fordifferent aspects of the parr-smolt transformation.A:Seasonal occurrence of physiological change that isdependenton seasonalcues and prior development acritical size). B: Differentiation hat is independentofseason.A change rom B to B' may representa changein ontogeny (i.e., increased growth rate resulting inincreaseddifferentiationat any time) or phylogeny i.e.,a differentrate of differentiation elative to size resultingin increased salinity tolerance at any given size). C:Seasonalchange hat is independentof size, such as aphotoperiod-cued ncrease n growth rate. D: Interac-tion of seasonand developmental ate. In this pattern,aspectsof the parr-smolt transformation re an intensi-fication and synchronizationof seasonalchanges hatare also dependenton prior development.D and D'represent, for instance, segmentsof a population hatwill undergo he parr-smolt transformation n the yearsn and n + 1, respectively. Analogouschanges n devel-opmental timing may have occurred in the course ofsalmonidevolution (see Figure 4). S representsphysio-logical differencesbetween parr and smolt; SW is sea-water and FW is fresh water.

Analysisof the parr-smolt transformationas adevelopmental process consisting of numerouscomponents an facilitate comparisons mongsal-monid species. Osmoregulatoryphysiology hasreceived the most attention and can be morethoroughly explored. Brook trout, a member ofthe genus (Salvelinus) that has the least-devel-oped capacity for marine residence n the sub-family Salmoninae Rounsefell ! 958; Hoar 1976),migrates nto seawaterat a relatively large size(>17 cm) and shows variability in the seasonofmigration (White 1940; Wilder 1952; Castonguayet al. 1982;Montgomeryet al. 1983). The devel-opment of salinity tolerance and hypoosmoregu-latory ability in brook trout occursat a larger sizethan in speciesof Salmo or Oncorhynchus e.g.,Figure 3, B versus B'; see also McCormick andNaiman 1984b).The osmoregulatory spectof theparr-smolt transformation,as characterized byseasonaldifferentiationof osmoregulatoryorgansresulting n increasedsalinity tolerance, is unde-veloped n brook trout (McCormick and Naiman1984b; McCormick et al. 1985a). It should benoted, however, that seasonalsilvering occurs inanadromous rook trout populations though hisis not necessarilyassociatedwith seawater entry:Black 1981), ndicating hat differentphysiologicalchanges ssociatedwith the parr-smolt transfor-mation can occur independentlyof one another.Pink salmon Oncorhynchus gorbuscha andchum salmon represent the opposite end of thesalmonid spectrum, often spendingas little as amonth or two in fresh water after hatchingbeforemigrating to sea. Salinity tolerance in these twospecies s incomplete n the posthatchalevin stagebut increases rapidly, permitting survival in seawater at sizes ess han 5 cm long (Weisbart 1968).It seemsprobable hat sucha rapid attainmentofsalinity tolerance will preclude a photoperiodi-cally cued differentiation ypical of other Onocorhynchusand Salmo species which undergotransformationand migrate at larger sizes. Withthe exceptionof changesn gill Na +,K+-ATPaseactivity (Sullivan et al. 1983)and kidney morphol-ogy (Ford 1958), little is known of the differenti-ation of osmoregulatory rgans n pink and chumsalmon. As in seasonally ransforming salmonids,prolonged rearing of pink and chum salmon infresh water results in substantial oss of salinitytolerance (Kashiwagi and Sato 1969; Iwata et al.1982).A phylogenetic comparison of the minimumsize at which seawater entry occurs in salmonidspeciess presented n Figure4. The developmen-


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E 20--

, 5-o.;;o lO-o

Eo 5 --

.//Salvelinusontinalis'o / SalmoairdneriSalmo salar Oncorhynchusisutch/ Oncorhynchusshawytscha

Onc orhynchus gorbuscha Oncorhynchus keta

SeasonalDifferentiation

7

=8

.4, 10lO

FIGURE .--Phylogeneticcomparison f the minimumsizeat which he development f salinity oleranceoccursin the subfamilySalmoninae. alinity olerance s defined sgreater han75% survival n seawater 29%o or at least14 d. Seasonaldifferentiation +) is definedas a photoperiod-controlledifferentiationof osmoregulatory rgansresulting n increased alinity olerance.With the exceptionof brook trout, reversibleontogenetic ifferentiationshave been shown to occur in the depicted species.Phylogenetic elationshipssuggest hat heterochronyhasoccurredeither through paedomorphosisincreasingsize at differentiation)or recapitulation decreasingsize atdifferentiation). his hypothesis houldnot imply existence f a linear salmonidineagebut rather hat, in the courseof salmonid evolution, heterochrony has occurred in differentiation of osmoregulatoryorgans. References(superscripts): , Kashiwagiand Sato (1969);2, Weisbart 1%8); 3, Wagneret al. (1969); 4, Conte et al. (1966); 5,Johnston nd Saunders 1981);6, Conte and Wagner 1965);7, McCormick and Niaman (1984a, 1984b);8, Wagner(1974b);9, Saunders nd Henderson 1970); 10, Clarke et al. (1978).tal nature of the attainment of salinity toleranceand the correspondenceof this phylogeny tomorphometrica!!y nd geneticallybasedphyloge-hies of the subfamily Salmoninae especially nthat Salrno is intermediate between Salvelinusand Oncorhynchus;see Neave 1958 for review)leads us to conclude hat heterochrony3n differ-entiationof hypoosmoregulatoryapacity and tsunderlying physiological mechanisms) has oc-curred during the evolution of these species(Figure 4; see Balon 1979, 1980 and Thorpe 1982for earlier discussionsof heterochrony in salmo-nids). The direction of heterochrony,either pae-domorphic increasedsize at attainmentof salin-ity tolerance with advancingphylogeny)or reca-pitulatory decreased izeat attainment f salinitytolerance) has yet to be established. It seemslikely that paedomorphosiswould be associatedwith an ancestral seawater origin for salmonids,

3Heterochrony s definedas changes n the timing ofdevelopment, ollowing he terminologyof Gould(1978).

and recapitulationwith a fleshwater origin. Argu-ments based on fossil and extant species havebeen given for freshwater (Tchernavin 1939; Hoar1976)and seawater Day 1887;Regan 1911;Balon1968; Thorpe 1982) origins of salmonids. Devel-opmental conflict between transformation andmaturation,arguedby Thorpe (1987, this volume)underlines he importanceof changesn the timingof development n establishing life history pat-tern. Viewing the parr-smolt transformationas adevelopmental rocess ubject o changesn tim-ing during the course of salmonid evolutionshould acilitate species omparison nd help gen-erate hypotheses oncerning he adaptive mecha-nisms or seawater entry and their hormonal con-trol. Indeed, it seems likely that changes in thetiming of expression of endocrine mechanismscontrolling he transformationare responsible orthe observed heterochrony.In a "common strategies" symposium, a finalstatement on comparative physiological tacticsmay seem nappropriatelybrief, yet a longer oneis precludedby the limited stateof our knowledge

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