AmericanFisheriesSocietySymposium1.211-229, 1987
Preparatory PhysiologicalAdaptations for Marine Life of
Salmonids:Osmoregulation,Growth, and Metabolism
STEPHEN D. MCCORMICK I AND RICHARD L. SAUNDERS
Department of Fisheries and Oceans, Biological Station
St. Andrews, New Brunswick EOG 2XO, Canada
Abstract.--Atlantic salmonSalmo salar, steelheadS. gairdneri, and severalspeciesof Pacific
salmon Oncorhynchusspp. undergotransformationfrom stream-dwellingparr to seaward-migratingsmolts.Physiological,behavioral,morphological,and biochemicalchangesoccur in fresh
water in preparationfor marinelife. The preparatorynatureof theseadaptationsis reviewed and
discussedwith particular emphasis on osmomgulation,metabolism, and growth. Functional
changes in gill, kidney, gut, and urinary bladder result in increased salinity tolerance and
hypoosmomgulatory
ability. Someor all of thesepreparatoryphysiologicalchangesmay reversein
the absenceof exposureto seawater.Changesin lipid, protein, and carbohydratemetabolism,
oxygenconsumption,and aerobicrespiratoryenzymeactivitysuggestincreasedcatabolismduring
parr-smolttransformation.
Thesetransientchangesin catabolismmayreflectenergeticdemandsof
the extensivedifferentiationoccurringduringtransformation.Althoughthem is increasedgrowth
during parr-smolt transformation,evidencefor a hypothesizedincreasein scopefor growth after
transformationis not convincing.We suggestthat differentaspectsof the transformationhave
different developmentalpatterns, the timing of which is species-dependent
and responsiveto
environmentalchange.Phylogeneticcomparisonof the differentiationof salmonidhypoosmomgulatory mechanismsand migratory behavior suggeststhat their evolution has occurred through
heterochrony.
Transformation of the stream-dwellingparr to
the seaward-migratingsmolt is a significantlife
history event in many salmonids. Various morphological,physiological,and behavioralchanges
occur seasonally(usually in spring),develop over
a period of 1-2 months, and are presumably
adaptive for downstreammigrationand residence
in the marine environment (see Table 1 and reviews by Hoar 1976; Folmar and Dickhoff 1980;
Wedemeyer et al. 1980). Parr-smolt transforma-
the parr-smolt transformation, we hope to spur
more focused research in this most fascinating
and important area. In reviewing each of these
areaswe develop a commonhypothesis:physiologicalchangesduringthe parr-smolt transformation are preparatory adaptations,preparatory becausethey anticipatea changein environmentand
adaptive becausethey increase survival and fitness in a new environment.
Experiments conducted on the parr-smolt
transformationhave, of necessity, examined isodevelopmental process (Hoar 1939; Bern 1978) lated aspectsof development.Evidence for develand recently has come under more intense scru- opmental changesare then unified under the sintiny as an importantfactor in the performanceof gle term "smoltification." This has often led to
hatchery-rearedsalmonidsin ocean ranchingand two disparateviews that are equally wrong: that
intensiveaquaculture(Wedemeyeret al. 1980).
the transformationis a single and common procIn the presentundertaking,we review changes ess, or that it is a seriesof unconnectedchanges.
in osmoregulation,metabolism, and growth that Simpson(1985) statedthe problem the following
occur during the parr-smolt transformation and way:
that are to some degree interrelated. Substantial
Perhapswe shouldalso be concernedlest our use of
information exists concerningchangesin salinity
the term "smoltification" encouragesa predilection
tolerance and metabolism,though much remains
to the belief that the processis a single one with a
to be done in this area. Less is known concerning
singleor organicallylinked set of effectors.Stoolting
growth, and our discussioncenterson what is not
oughtratherto be seenas the resultof a largenumber
of distinctprocesses--thechangeto particularpatknown. By stating hypotheses concerning the
ternsof growth, the elaborationof neuronsassociated
interrelationshipsof physiologicalchangesduring
tion has for
some time
been of interest
as a
Ipresentaddress:Departmentof Zoology,University
of California, Berkeley, California 94720, USA.
211
with long-termmemory,the developmentof different
patternsof behaviour,major changesin metabolism
and, finally, those changesin gill structure which
permitthe fish to passfrom a hypo- to a hypertonic
212
MCCORMICKAND SAUNDERS
environment.There seemsto me no a priori reason favorablesurface-area-to-volume
ratio for larger
for supposingthat these processesevolved simulta- fish,or to a progressive
developmentof hypoosneously,or for supposing
that they are linearlyinter- moregulatory mechanismswith size, or to both.
dependentor have functionallylinked endocrinemediators.
By comparingstudiesof similar design,McCor-
mickandNaiman(1984b)concludedthat salinity
If we are successfulin this review, we shall tolerance was also related to genus: the size at
have shown or suggestedboth the distinction which seawater survival occurs is smallest for
between theseprocessesand their interrelations. Oncorhynchus
species,largerfor Saltnospecies,
By adoptinga comparativeview, we hope to and largestfor Salvelinusspecies.This phylogeestablishthat differentaspectsof the parr-smolt netic relationshipfollows closelythe durationof
transformationare present in different salmonid marineresidence(shortestfor Salvelinusspecies)
speciesandthattheirpresence
anddevelopmental characteristicof each genus,as pointed out by
pattern are related to the timing and duration of Rounsefell(1958) and Hoar (1976).
anadromyof a populationor species.
There is substantialevidenceindicatingthat
size-dependent
changesin salinitytoleranceare
distinct
from
the
morerapid,seasonally
occurring
Osmoregulation
changesin salinity tolerance associatedwith the
Ontogenyof Salinity Tolerance
parr-smolt transformation.Salinity tolerance of
Ontogeneticchangesin salinity tolerance(de- seasonally migrating Atlantic salmon, rainbow
fined here as the ability to survive seawater trout Saltno gairdneri and coho salmon Onkisutchincreasesrapidly over a pe>30%o) have been found in virtually all salmonid corhynchus
speciesinvestigated.Whereassalmonideggscan- riod of 1-2 months, coincidingwith the normal
not survivemore than a few daysin seawater,the period of migrationand visible smolt characterisposthatchalevin has even poorer survival, pre- tics(ConteandWagner1965;Komourdjianet al.
sumably due to loss of the chorion (Weisbart 1976; Clarke et al. 1978; Saunderset al. 1983,
1968).Salinity toleranceof Atlantic salmonSaltno 1985;McCormicket al. 1987).Thesechangesare
of temperature(exceptas it affects
salar alevinsdecreasesas the water-impermeable independent
vitelline membrane decreases in favor of a waterdevelopmental
rate), andare responsiveto photopermeable epithelium (Parry 1960; Talbot et al. periodic cues (Saundersand Henderson 1970;
1982). In contrast, salinity tolerance of chum Wagner 1974a;Komourdjianet al. 1976;Clarke et
salmonOncorhynchusketa increasesduring de- al. 1978; Johnstonand Saunders 1981; Clarke et
velopment of the alevin (Kashiwagi and Sato al. 1985; Saunderset al. 1985; McCormick et al.
1969).
1987).
After resorptionof the yolk sac, salinitytoleranceof all salmonidsincreaseswith sizeandage,
and is closely tied to, and probablycausedby,
increasedability to regulateplasmaions and osmolarityfollowingexposureto seawater
2 (Parry
1958, 1960; Houston 1961; Conte and Wagner
1965; Conte et al. 1966; Wagner 1974b;McCormick and Naiman 1984b;Ouchi 1985).Conte and
Althoughsomeseasonalperiodicityin salinity
tolerancemay occurat all life stages(Hoar 1965;
Wagner1974a),the ability to manifestlarge seasonalchangesin salinitytoleranceis size-dependent. Rainbow trout do not respondto seasonal
cueswith increasedsalinitytoleranceuntil they
are at least i0 cm long (Conte and Wagner 1965).
Similarsize-relatedlimitationsin the expression
of parr-smolt transformationhave been found for
coho salmon (Clarke et al. 1978) and Atlantic
salmon(Elson 1957;Parry 1960).
In distinguishing between size-dependent
changesin salinitytoleranceand the size-dependent parr-smolt transformation,the degree of
salinity tolerance becomesimportant. Atlantic
and coho salmonparr of 10-12 cm can routinely
tolerate(i.e., survivefor manydays)a salinityof
30%o(Saundersand Henderson 1969; Clarke and
Nagahama1977).Thesefishmay beginto die after
severalweeks,however,andgrowthis inevitably
poor. Such differencesin the degreeof salinity
Wagner (1965) and McCormick and Naiman
(1984b)concludedthat size, not age, is the primary determinant of increased seawater survival
for steelhead Saltno gairdneri and brook trout
Salvelinusfontinalis, respectively. Size-dependent salinity tolerance may be due to a more
•Chinooksalmon(0. tshawytscha)
are an apparent
exception to this rule. Whereas other Oncorhynchus
speciesdevelop increasedsalinity tolerance through
increased ability to regulate plasma ions, chinook
salmon develop an increased tolerance of elevated
plasmaions (Weisbart 1968).
PHYSIOLOGY OF THE SALMONID PARR--SMOLT TRANSFORMATION
toleranceare not limited to the parr stage.Smolt-
213
to a hyperosmoticenvironment. As the following
discussionshoulddemonstrate,seasonalchanges
seasonal cues through exposure to continuous in structure or function (differentiation) of the
light can adapt to 30%oseawater, but cannot osmoregulatorymachinery, which occur prior to
survive in 40%oas can normal smolts, and exhibit and in anticipation of exposure to seawater, are
poor feedingand growthin seawater(Saunderset responsible
for increasedsalinitytoleranceduring
al. 1985; McCormick et al. 1987). This distinction the parr-smolt transformation.This seasonaldifbetween the merely adequate or short-term sea- ferentiationis likely to be the result of qualitative
water survivalof parr and the completeadaptabil- and quantitativechangesin gene expression,the
ity of smoltsis an importantone. Its basislies in hormonal control of which has yet to be elucithe increased hypoosmoregulatory ability of dated (Dickhoff and Sullivan 1987, this volume).
smolts (Parry 1960; Conte and Wagner 1965;
In consideringthe mechanismsof osmoregulaClark et al. 1978; Boeuf et al. 1978; Saundersand tory change(as well as metabolismand growth),
Henderson 1978; Hogstrand and Haux 1985) and we shall consider only those salmonid species
perhaps other transport-relatedphenomenasuch which show a rapid (1-2 month), reversible, seaas food conversion efficiency. Since parr can sonallycued increasein salinity tolerance. In this
survive in seawaterfor extendedperiodsof time, group, Atlantic, coho, and masu salmon Onhowever, one can justifiably ask what the adap- corhynchusrnasou and steelhead have received
tive basis of increasedsalinity tolerance is at the the greatestattention. There are, however, inhertime of smolting. Rapid acclimation to higher ent difficultiesin conductingand comparingstudsalinities with fewer osmotic perturbationsmay ies on a developmental phenomenonthat occurs
permit rapid movementthroughestuaries(Cher- over many weeks but which has no absolute
nitsky 1983; McCormick et al. 1985), and imme- morphologicalcriterion (Gorbman et al. 1982).
diate resumptionof physiologicaland behavioral Many researchers have used appearance (often
processesthat might otherwiseresult in increased the degreeof silveringor fin darkening)as a sole
predationand interruptedfeedingand growth.
criterion to distinguishsmoltsfrom nonsmolts.In
The developmentalprocessesthat result in sea- additionto the subjectivenature of this criterion,
sonally increasedsalinity toleranceand hypoos- it has provedto be highly variableunder artificial
moregulatoryability are apparentlyreversible if culture conditionsand is often "uncoupled" from
fish remain in fresh water. Rapid summer de- other aspects of the parr-smolt transformation
creasesin salinity tolerancehave been observed (Wedemeyer et al. 1980). Seasonal changes in
in rainbow trout (Conte and Wagner 1965), coho temperaturemay introducephysiologicalchanges
salmon (Mahnken et al. 1982), and Atlantic independentof developmental phenomena (Virsalmon(Evropeytseva 1962).Generally known as tanen and Oikari 1984). Differences in methodol"desmolting," this process may also result in ogy, species, and size further increase the diffireversionto a parr-like appearance(seeFolmar et culties of assessingexperimentalresults. In most
al. 1982). Whether or not "desmolting" resultsin cases,the developmentalprocessis clear enough
a reversalof all physiologicalchangesassociated (or the experimentalconditioncontrolledenough)
with the parr-smolt transformation will be dis- in spite of these confoundingfactors. We shall
cussed below.
attempt to point out the exceptions,particularly
when conflictingresultsare apparent.
Functional Changesin Osmoregulatory
Gills.--For a variety of euryhalineteleosts, gill
Organs
Na+,K+-ATPase activity increasesafter transfer
Teleosts normally maintain their plasmaosmo- from fresh water to seawater(Epstein et al. 1967;
!arity within a narrow range(290-340 mOsmol/L) Kirschnet 1980). Ionic and electrical gradients
irrespective of the salinity of the external me- generated by this enzyme are central to current
dium, and failure to do so for prolongedperiods models of branchial ion fluxes (Maetz and Garciaresults in death. The transition from fresh water to
Romeau 1964; Silva et al. 1977). Increasesin gill
seawaterrequiresa reversalfrom net ion influx to Na+,K+-ATPase occur in several salmonidspenet ion efflux which is regulatedprimarily by the cies in freshwater prior to seawater entry. Such
gills but also involves the kidney, gut and urinary increases in coho salmon (Zaugg and McLain
bladder (for a review of osmoregulationin tel- 1970; Giles and Vanstone 1976a; Lasserre et al.
1978), chinook salmon (Hart et al. 1981; Buckman
eosts, see Evans 1979; Foskett et al. 1983). In
mostteleoststhis reversalis initiatedby exposure and Ewing 1982), rainbow trout (Zaugg and Wagsize (14-17 cm) Atlantic salmon that are denied
214
MCCORMICK AND SAUNDERS
her 1973), and Atlantic salmon(McCartney 1976; salmonin fresh water decreasedgraduallyfrom 6
Saundersand Henderson 1978; Boeuf et al. 1985; mV in early Februaryto -12 mV in mid-April. In
McCormick et al. 1987) occur seasonallyand in fish transferred to seawater for 12 h, TEP was 5
phasewith migrationand increasedsalinity toler- mV in February and increased to 16-18 mV in
ance(Figure 1). Most of the gill Na+,K+-ATPase April throughAugust. Taken together, these reactivity and ion transport capacity resides in sults indicate that developmental changes in
mitochondria-rich chloride cells (Epstein et al. mechanismsfor ion transportfound in freshwater1980; Foskett and Scheffey 1982). Chloride cells adaptedsmoltsare importantfor seawateradapincrease in number in gill opercular epithelium tation.
(Loretz et al. 1982)and changemorphologyin gill
Kidney and urinary bladder.--The urine flow
filaments (Richman 1985) of freshwater coho and water excretory rates of rainbow trout smolts
salmonsmolts.Langdonand Thorpe (1985)found in fresh water decrease relative to those in both
increased size and number of chloride cells in
pre- and postsmolts and are due entirely to a
Atlantic salmonin early springjust before attain- reduction in glomerular filtration rate (Holmes
ment of maximum salinity tolerance.
and Stainer 1966). Urine excretory rates of soD. R. N. Primmett, F. B. Eddy, M. S. Miles, dium and potassiumand total osmolarityare also
C. Talbot, and J. E. Thorpe (personalcommuni- reduced in smolts. (Decreased urine flow and
cation)measuredwhole-bodyNa + fluxesin juve- glomerularfiltration occur in euryhalineteleosts
nile Atlantic salmon; these fluxes are generally after exposureto seawater[Hickman and Trump
assumedto reflect the functionof gill epithelium. 1969],and the resultsof Holmes and Stainermay
During parr-smolt transformation, Na + flux be interpretedas a preparatoryadaptation.)Howchanged from net influx (characteristicof fresh- ever, the "seasonal" temperatures, variable timwater teleosts) to net efflux. However, net Na + ing of measurements,and use of appearanceas
efflux is not an absoluterequirementfor increased the sole smolt criterion make it difficult to intersalinity tolerance since maximum salinity toler- pret these results. Recent work by Eddy and
ance was achieved after Na + flux had returned to
Talbot (1985) indicatesthat urine productionby
a net influx. Iwata et al. (in press)found develop- juvenile Atlantic salmon(> 15 cm) increasesdurmental changes in whole-animal transepithelial ing springcoincidentwith increasinggill Na +,K +potential (TEP) of coho salmon. The TEP of coho ATPase activity. These conflicting results con-
Maximum
Salinity
Tolerance
I.
W Seawater
%
%
(Fresh Water)
Seawater
Fresh
March
Parr
Water
I
April
I
May
•
Smolt
FIGURE 1.--Functional changesin osmoregulatoryorgansduring the parr-smolt transformation.Functional
changes normally associated with osmoregulationin seawater occur in fresh water and result in increased
hypoosmoregulatory
ability and salinity tolerance.In the absenceof exposureto seawater,these changesare
reversible.
PHYSIOLOGY OF THE SALMONID PARR--SMOLT TRANSFORMATION
cerningalteration of kidney function during parrsmolttransformationare, at present,unexplained.
Declinesin kidney Na +,K+-ATPase activity in
juvenile Atlantic salmonin springwere reported
by McCartney (1976). Virtanen and Soivio (1985)
reportedthat kidney Na+,K+-ATPase activity of
juvenile Atlantic salmonraisedin brackishwater
fluctuates considerablyduring spring, falling in
early springthen risingto highlevelsin mid spring
and falling againin late spring.S. D. McCormick
and R. L. Saunders (unpublisheddata) found no
seasonalchangein kidney Na+,K+-ATPase activity in freshwater-rearedAtlantic salmon,nor was
the activity level of this enzyme different from
that in fishexposedto continuouslight (conditions
that inhibit physiologicalchangesassociatedwith
transformation). It should be noted that, unlike
gill Na+,K+-ATPase activity, kidney Na+,K +ATPase activity of Atlantic salmon changes
slightly or not at all following increasesin environmentalsalinity(Virtanen and Oikari 1984;McCormick et al., unpublisheddata).
Loretz et al. (1982) found that Na + and Clreabsorptionby the urinary bladderof freshwateradapted coho salmon did not change between
March and June. However, developmental
changes in the urinary bladder were detected
when coho salmon were experimentally adapted
to seawaterover this sameperiod. In May, when
seawater survival was low, Na + and Cl- reabsorption by the urinary bladder of seawateradapted fish was at high levels characteristicof
salmon in fresh water. In June, when seawater
survivalwas high, Na + and Cl- reabsorptionwas
215
Consequencesof Developmental Changes
on Osmoregulationin Fresh Water
The previous sectionhas establishedthat seasonalincreasesin salinity toleranceand hypoosmoregulatory ability occur in conjunction with
increasesin gill Na+,K+oATPase activity, quantity of gill chloride cells, intestinal net fluid absorptionand other osmoregulatorychangesthat
are characteristic
of seawater-adapted
teleostsbut
which occurprior to seawaterentry (Figure 1). If
these
mechanisms
are detectable
in smolts
in
fresh water, are they also fully functional in vivo,
and do they, therefore, produce osmoregulatory
difficulties(water gain and ion loss) for smolts in
fresh water? D. N. R. Primmett, F.B. Eddy,
M. S. Miles, C. Talbot, and J. E. Thorpe (personal communication)have recently argued that
increasesin ion fluxes across the body surface,
which are presumablyhormone-induced,precede
and are responsiblefor increasesin gill Na +,K +ATPase activity and other osmoregulatory
changesduring transformation. Whereas we have
stressedthe adaptive nature of these changes,
these researchers suggestthey are primarily a
consequenceof the loss of freshwater osmoregulatory capacity (see also Langdon and Thorpe
1985; Simpson 1985). It shouldbe stressed,however, that in each of these scenarios a seasonal
differentiation
occurs
that
results
in increased
salinitytolerance,which is clearly adaptivefor a
seaward-migratingfish. It is still unclear that all
the osmoregulatorychangesportrayed in Figure 1
are functional in the freshwater smolt (e.g.,
Na+,K+-ATPaseincreasesmay be demonstrable
by enzymologicalassayof gill homogenatesbut
abolished. While no functional differentiation of
the enzyme may not be functionally active in
the urinary bladder was apparentin fresh water, a vivo), or whetherthey requireinductionby expoclear increase in its capacity to respondto sea sure to seawater. In either event, we emphasize
water had occurred.
that the physiologicalmechanismsnecessaryfor
Gastrointestinaltract.--Increased drinkingrate long-term survival in seawater take several days
and absorption of water and salts across gut to develop in euryhaline species (Foskett et al.
epitheliaoccur followingadaptationof euryhaline 1983); in smolts, these adaptationsare already in
telosts to seawater. Collie and Bern (1982) found place and may be rapidly induced to become
that the capacity for net fluid absorptionof the functional upon exposure to seawater.
intestine increasedtwofold in freshwater-adapted
Decreasesin plasma chloride (in the late parr
juvenile coho salmon between March and May,
stage:Houstonand Threadgold1963)and muscle
and that high valuesin May were similar to those chloride (in migratingsmolts: Fontaine 1951) ocof salmon adapted to seawater. Reversion of cur in Atlantic salmon in fresh water. Plasma
intestinalnet fluid absorptionto prespringlevels osmolarityhas been reported to decreaseduring
occurred in early autumn in fish held in fresh smoltingof masusalmon(Kubo 1953), to be more
water. Developmental changes in drinking rate variable in smolting Atlantic salmon (Koch and
associated with the parr-smolt transformation Evans 1959), and to increaseabsolutelyin posthave yet to be investigated.
smolt Atlantic salmon(Parry 1961). On the other
216
MCCORMICK AND SAUNDERS
hand, a numberof studiesfailed to find significant tween downstreammigrationand water temperature for Atlantic salmon (Fried et al. 1978; Jonsson and Rudd-Hansen 1985). Kubo (1955) found
Dickhoff 1980).
that depressionof plasma osmolarity during the
The variety and conflict of results in the inves- parr-smolt transformationof masusalmonclosely
tigationscited above suggestthat environmental, paralleledincreasesin water temperature.
experimental, and speciesdifferencesmay have
Since a variety of other physiologicaland beinfluenced the results. Indeed, regulation of havioral changessuch as buoyancy, swimming
plasma and cellular ions of salmonidsin fresh ability, and orientation also occur during the
water can be affected by temperature (Kubo parr-smolt transformation (Table 1), it seems
1955), size (McCormick and Naiman 1984a), ac- likely that a variety of factors will be important in
tivity (Wood and Randall 1973), water quality initiatingmigration.While we have suppliedsome
(Eddy 1982),pH (Saunderset al. 1983),and stress suppositions,it is clear that the primary cue(s)of
(Schreck 1982). We have recently conducted a downstream migration and their relationship to
study in which rearing temperature for Atlantic osmoregulatorydifferentiationhave yet to be essalmon was held constant (5-8øC) from February tablished.In salmonidpopulationswhichundergo
to August (McCormick and Saunders, unpub- prolonged downstream migration there is evilished data). The interaction of seasonaland de- dence that migratory behavior and osmoregulavelopmentalphenomenawas controlledby exam- tory differentiationdo not occur together (Ewing
ining fish under both a simulatednatural photope- et al. 1980; Bradley and Rourke 1984). This pheriod and continuouslight. (Atlantic salmonraised nomenonmay be due to the length and variability
under continuouslight grow normally but do not of migration, which might precludeaccurate anundergoa parr-smolt transformation:Saunderset ticipation of seawaterentry.
al. 1985;McCormick et al. 1987.)A slight(<5%)
decrease in plasma Na +, CI-, and osmolarity
Metabolism
occurredin each group betweenMarch and April.
'changesin plasmaor muscleionscoincidentwith
the parr-smolt transformation(see Folmar and
There is substantial evidence of a metabolic
No changein plasmaNa +, CI-, Mg++, K +, or
reorganization
during the parr-smolt transformaosmolarityoccurredduringthe periodwhen salintion.
This
evidence
is derived primarily from
ity tolerance and gill Na+,K+-ATPase activity
increased (May and June) and subsequentlydecreased (August) in Atlantic salmon reared under
TABLE I.---Some behavioral and physiological
natural photoperiod;nor were the levelsof plasma changescoincident with the parr-smolt transformation
in salmonids.
ions and osmolarity different from those in fish
reared under continuouslight, in which increases Behavioral or physiologicalchange
Reference
in gill Na +,K+-ATPaseactivityand salinitytolerance did not occur.
These results indicate that
changesin plasma ions are not a necessaryconsequenceof differentiationin osmoregulatoryorgansduringthe parr-smolt transformation.
The aboveconclusiondoesnot imply, however,
that changesin plasma or muscle ions do not
occurin responseto environmentalchangeduring
the parr-smolt transformation. Several authors
have suggested a direct connection between
downstream migration and osmoregulatorydysfunction in fresh water caused by preparatory
differentiation (Fontaine 1975; D. R. N. Primmett, M. S. Miles, C. Talbot, and J. E. Thorpe,
personalcommunication).We suggestthat preparatory physiologicalchangesfollowed by environmental change (such as increasedtemperature or
water flow) may be required for osmoregulatory
perturbation,which may, in turn, be connectedto
migratorybehavior. Strongcorrelationsexist be-
Increaseddepositionof guanineand Johnstonand Eales
hypoxanthinein skin and scales
(1967)
(silvering)
Increasedbuoyancy due to
increased air volume of
swimbladder
Saunders (1965); Pinder
and Eales (1969)
Alterations
in blbodhemoglobins Vanstone et al. (1964);
(rapid increasein adult forms)
Giles and Vanstone
(1976b); Koch (1982);
Sullivan et al. (1985)
Increasedschoolingbehavior
Kalleberg (1958)
Increasedsalinity preference
Baggerman(1960);
Mclnerney (1964)
Negative rheotaxis
Wagner (1974b);
Eriksson and
Lundqvist (1982);
Lundqvist and
Eriksson (1985)
Decreasedswimmingability
Glova and Mclnerney
(1977); Smith (1982)
PHYSIOLOGY
OF THE SALMONID
PARR--SMOLT TRANSFORMATION
217
observationson changesin body composition, the time of the parr-smolt transformation. Fontaine et al. (1963) reported that the powerful
activity. We wishto addresstwo generalhypoth- hyperglycemic agents adrenaline and noradrenaeses during the review of this evidence. First, line are at their highestlevels in Atlantic salmon
doesa metabolicincreaseoccurduringthe parr- duringthe final stagesof smoltingin April-May.
oxygen consumption, and mitochondrial enzyme
smolt transformation.'?Second, is such a meta-
bolic increasedue to energeticrequirementsof
differentiation
or to increased anabolism associ-
ated with growth or to both (Figure 2).9
Changesin Body Composition
'Withtheexception
of decreased
bloodglucose,
the abovechangesare often associatedwith shortterm stress(Schreck1981).The increasedsusceptibility of smolts to stress has been noted by
several authors (Wendt and Saunders 1973;
Schreck1982).Seasonalchangesin enzymeactiv-
Several changesin carbohydrate metabolism ity associatedwith glycogenolysis
and glycogeare concurrent with the parr-smolt transforma- nesis,however,suggesta morepermanentchange
tion. Reduction of liver and muscle glycogen that is unrelatedto stress.Sheridanet al. (1985b)
occurs in springin Atlantic and coho salmonin found that liver phosphorylase-aactivity (glycoboth the presenceand absenceof migratoryactiv- genolysis)of coho salmonincreasesby 64% beity (Fontaine and Hatey 1953; Malikova 1957; tween March and April, while uridine phosphate
Wendt and Saunders 1973; Woo et al. 1978). formation (glycogenesis)decreasesby 54% from
Blood glucosehas been reported to increasein March to June.
Atlantic salmon (Wendt and Saunders 1973) and
Total body protein decreasedby 10% between
to decreasein coho salmon (Woo et al. 1978) at February and April in large (>14 cm)juvenile
rainbow trout, but not in smaller fish under the
same conditions(Fessler and Wagner 1969). In
Differentiation
contrast,Woo et al. (1978) found no changein
liver and muscleprotein content of coho salmon
parr and smolts. Serum protein content of coho
salmon smolts was 15% lower than in parr or
postsmolts(Woo et al. 1978). Cowey and Parry
(1963) found a 30% increase in muscle content of
nonprotein nitrogenous constituents of smolts
over that in parr, due almostentirely to increased
creatine content. The authors suggestedthat increasedcreatinemay be due to greateravailability
of N-phosphorylcreatinefor endergonicreactions
Growth
or to increased metabolism of several amino acids
for which creatineis an end product.
Cowey and Parry (1963) and Fontaine and Mar-
Differentiation
&
Growth
chelidon (1971) could find no differences in total
amino acid content of the brain or muscle between
Atlantic salmonparr and smolts(they were able to
sampleboth laboratory-rearedand wild fish). The
i
I
I
i
i
i
levelsof particularamino acidsdid change,howMarch
April
May
June
July
ever. Threonine and glutamine contents of the
Parr
•
Smolt
brainsof smoltsincreased,while muscleglycine
and taurine decreased(Fontaine and Marchelidon
FIGURE 2.--Possible
causes of metabolic increase
duringthe parr-smolt transformation.Increasesin met- 1971). Decreased muscle taurine content of Atlanabolic rate due to differentiationand growth can be tic salmonsmoltswas also found by Cowey and
associatedwith catabolismand anabolism,respectively. Parry (1963). Fontaine and Marchelidon (1971)
Increased growth rate (which occurs in both parr and explained these changesas ramificationsof sevsmolts in spring) will, a priori, result in increased
eral physiologicalchangesduring the parr-smolt
metabolic rate. There also is evidence for increased
transformation.
G!ycine (a precursorof purines)
metabolicrate due to differentiation.Arrows suggestthe
magnitudesof the influenceon metabolicrate exertedby maybe involvedin eventsleadingto depositionof
guanine and hypoxanthine in skin and scales,
differentiation(D) and growth(G) actingseparatelyor
together.
which results in silvering (Johnstonand Eales
IG
218
MCCORMICK AND SAUNDERS
1967). Taurine is important for intracellular isosmotic regulation in teleosts (increasing when
plasma osmolarity increases:King and Goldstein
1983) and may be lowered in responseto osmoregulatorychangesin freshwater or be distributed
to other more sensitivetissuesin preparationfor
hyperosmotic regulation. Increases in threonine
in the brain, which is under insulin control in
mammals (Okumura et al. 1959), may be a byproductof increasedinsulinconcentrationresulting from glycemic fluctuations. While these intriguing suppositionshave yet to be given experimental support,they underlinethe importanceof
distinguishingcause and effect in this complex
developmentalprocess.
Total body and muscle lipid decreasesmarkedly in springin juvenile Atlantic, coho, and masu
salmon and in rainbow trout coincident with other
parr-smolt changes(Vanstone and Markert 1968;
Fessler and Wagner 1969; Saundersand Henderson 1970, 1978; Ota and Yamada 1974a, 1974b;
Komourdjian et al. 1976;Farmer et al. 1978;Woo
et al. 1978; Sheridan et al. 1983). These changes
do not occur in small juveniles (parr), are not
dependenton changesin activity or temperature,
and return to prespring levels by late summer
when fishes are retained in fresh water (Malikova
1957; Fessler and Wagner 1969; Ota and Yamada
1974a, 1974b; Farmer et al. 1978; Saunders and
Henderson 1978; Woo et al. 1978). Moisture con-
tent of muscle varies inversely with lipid content
(Farmer et al. 1978; Saunders and Henderson
1978;Woo et al. 1978)thoughthis appearsto be a
commonfeatureof teleostsand not peculiarto the
parr-smolt transformation(Phillips 1969).
Sheridan and co-workers (Sheridan et al. 1983,
1985a, 1985b; Sheridan and Allen 1983) have
examined lipid dynamics of coho salmon and
rainbow trout in some detail. Lipid content of
serum, liver, and muscle (white and red) is depletedby up to 60% in spring.Mesentericfat does
not fluctuate. Large amounts of triacylglycerol
(normally used as energy storage) in muscle and
liver are reducedmore than other lipid classes.A
reorganization of the fatty acid compositionalso
occurs. Increasedamountsof long-chainpolyunsaturatedfatty acids and decreasedlinoleic acid,
tions for a role in osmoregulationhave been made
(Sheridan et al. 1985a).
The biochemicalbasesof changesin lipid metabolismhave also been investigated(Sheridanet
al. 1985b).Lipolytic rate (measuredby the release
of •4C-oleicacidfrom 14C-triolein)
increases
oneto three-fold in liver, red muscle, and mesenteric
fat in coho salmon over a 4-month period in
spring.Duringthis sameperiod3H20 incorporation into fatty acidsof liver and mesentericfat was
halved, though no difference in lipogenesis of
neutrallipids was detected.These resultssuggest
both a reorganizationof lipid composition for a
marine existence and increased catabolism
asso-
ciated with the parr-smolt transformation.
Oxygen Consumption
Direct measurementof oxygenconsumptionis
difficult to assessbecauseof the relatively high
individual variation, dependenceon temperature
and size (often requiringuse of regressions,which
can obscuredata), effectsof variousactivity levels, and differentialresponseto handlingstressor
confinement.Baraduc and Fontaine (1955) found
resting, weight-specificoxygen consumptionof
wild Atlantic salmonparr at 8øC was 25% lower
than for wild smolts.Power (1959), working with
Atlantic salmon from an Arctic environment,
found a temperaturedivergencein oxygen consumption:smoltshad lower oxygen consumption
than parr below 13.5øC, but higher oxygen consumptionabovethis temperature.This may be the
resultof increasedactivity in responseto temperature. Higgins (1985) reported oxygen consumption as a function of differential growth and the
parr-smolt transformation in Atlantic salmon.
When oxygen consumptionper animal was regressedto a common size, rapidly growing fish
had higher oxygen consumptionat 7.5øC than
slower growing fish. Smolts (based on external
appearance),however, had lower weight-specific
oxygenconsumptionthan nonsmolts.In one of the
few reported studiesin which activity levels were
taken into account, Withey and Saunders(1973)
found that postsmoltAtlantic salmonhad higher
rates of oxygen consumption than nonsmolts.
Without more critical studiestaking activity level
into consideration,it is difficult to arrive at a firm
conclusionconcerningchangesin oxygen consumptionduringthe parr-smolt transformation.
characteristic of marine teleosts, occur in fresh
water during the parr-smolt transformation. Similar changesin lipid compositioncoincidentwith
the migratory period were observed in juvenile
Atlantic and masu salmon (Lovern 1934; Ota and Respiratory Enzymes
Yamada 1974a, 1974b). The adaptive value of
Mitochondrial enzyme activities are indicative
these changesis as yet unknown, though sugges- of tissuerespiratoryrate or respiratorypotential,
PHYSIOLOGY OF THE SALMONID PARR--SMOLT TRANSFORMATION
219
though some enzymes are more representative composition
(Malikova1957;Woo et al. 1978)and
than others (Ericinska and Wilson 1982). Succi- return of liver respiratory enzyme activity to
nate dehydrogenase(Chernitsky and Shterman presmoltlevel in summerindicatethat increased
1981;Langdonand Thorpe 1985),citrate synthase catabolismsubsidesafter the transformation, irreand cytochrome-c oxidase activities (S. D. Mc- spectiveof the environmentalsalinity.
Cormick and R. L. Saunders,unpublisheddata)
Growth
increase in gill homogenatesof Atlantic salmon
The apparent size threshold of the parr-smolt
concurrentwith the parr-smolt transformation.
At first glance, these results would appear to transformationmay rule out growth rate as the
coincide with the observed increase in numbers of
primary stimulusfor differentiation.Yet patterns
mitochondria-rich chloride cells discussed earlier.
of growth will undoubtedlyaffect the year of
Althoughchloride cells have greater respiratory occurrenceof the parr-smolt transformationand
enzyme activity than other gill cells(Sargentet al. perhaps also its timing and intensity (Clarke
1975), whole-gill homogenatesof fish which are 1982). The bimodal growth pattern of Atlantic
acclimated to seawater do not have different ressalmonis a goodexampleof the complexrelationpiratory enzyme activities (Epstein et al. 1967; shipbetweengrowthandtransformation.Bimodal
Conte 1969;McCormick et al., unpublisheddata; length-frequency distributions of laboratoryfor exceptions, see Sargent et al. 1975; Langdon reared Atlantic salmoncan be distinguisheddurand Thorpe 1984). Increasesin gill respiratory ing the first autumn following hatchingand have
enzyme activity observed during the parr-smolt been attributed to an increase in growth rate of
transformationappearto go beyondwhat may be upper-modefish (Kristinssonet al. 1985)and to a
required for steady-state osmoregulationonce declinein growth rate owing to reducedappetite
seawater acclimation has occurred. The increase
of lower-mode fish (Thorpe et al. 1982; Higgins
may be requiredfor preparatorydifferentiationof 1985; Thorpe 1987a). Though these distinctions
the gills, or perhapsmay aid in seawateradapta- are controversial,it is clear that upper-and lowermode fish do not further subdivide even after the
tion during initial acclimation.
Blake et al. (1984)foundup to 50% increasesin fish in each mode are placed in separate tanks
mitochondrial concentration, and in the activities (Thorpe 1977). Upper-mode fish invariably beof succinate dehydrogenaseand cytochrome-c come smolts in I year, while lower-mode males
oxidase, in the livers of large (>16 cm), silvery undergoa high rate of sexual maturation during
Atlantic salmon relative to those of parr. Simi- their first autumn and normally require another
larly, McCormick and Saunders (unpublished year to achievesmolt size. Existence in the lower
data) found that liver citrate synthaseactivity of mode, however, does not preclude undergoing
smolt-size Atlantic salmon increased 25% betransformation;elevatedearly winter temperature
tween March and June (coincident with increases resultingin higher growth and a greater size in
in gill Na +,K+-ATPaseactivity)andsubsequently early springwill result in normal smolt appeardeclined to basal levels in August. These results, ance and performance (Saunders et al. 1982;
in combinationwith increasedlipolyticandglycoo Kristinsson1984).The relationshipbetween high
genolyticenzyme activities in coho salmonlivers, growth rates of upper-modefish and the parrsuggestthat increased catabolism occurs in the smolt transformation may be indirect, coupled
liver duringthe parr-smolt transformation.
only by the sizedependenceof the transformation
The evidence summarized here indicates that
(Thorpe et al. 1982). Alternatively, bimodality
there is both reorganizationand enhancementof maybe an early manifestation
of parr-smolttransmetabolicactivity duringthe parr-smolttransfor- formationsuchthat changestakingplacein spring
mation. Unfortunately, there is relatively little are the climax of processeswhich have been
informationon the reversibilityof thesechanges. proceedingsince the previous autumn (Thorpe
Metabolic alterationswhich are adaptationsfor 1986).
Under natural conditions, juvenile Atlantic
seawaterentry, suchas changesin lipid composition, are analogousto preparatory osmoregula- salmonmay beginseawardmigrationat 2-4 years
tory changesand are probablylost if the animals of age, and at weightsof 30-50 g. They frequently
are maintained in fresh water. Metabolic inattain weights of 1.5-2.5 kg in their first year at
creases appear to be at least partly catabolic, sea. Increasedgrowth is undoubtedlydue in large
owing possiblyto the energeticdemandsof differ- part to increasedquantityand quality of food and
entiation. Recovery of pretransformationbody more favorable year-roundtemperatures(Gross
220
MCCORMICK AND SAUNDERS
1987,this volume). It is presentlyunclearwhether
smoltsundergoa physiologicalchangeresultingin
increasedscopefor growth(maximumfood intake
minusthat necessaryfor maintenance:Brett 1979)
at temperatureand ration levels characteristicof
the marine environment.
Increased growth of juvenile salmonoccurs in
spring concurrent with other transformation-related changesand in direct responseto increasing
photoperiod (Saunders and Henderson 1970;
Knutsson and Grav 1976; Komourdjian et al.
1976; Clarke et al. 1978; Johnston and Saunders
1981; Higgins 1985). Though evidencefor a common growth responseof all salmonidsto increasing photoperiodis lacking(Brett 1979),increased
growth under increasingphotoperiodalso occurs
in Atlantic salmonparr (Higgins 1985).One peculiar aspectof growth duringthe parr-smolt transformation is a decrease in condition factor (100 ß
weight/length3;
seeWedemeyeret al. 1980).This
may be the result of a relative weight loss due to
catabolism, or to an increased growth in length,
such that increase in length outstrips growth in
weight. Several authors have suggestedan adaptive change in morphologyto explain the latter
hypothesis(Thorpe 1982).
In the absenceof salinity effects, are parr and
smolt distinguishablein their scope for growth
either during or after the parr-smolt transformation? Higgins (1985) found that, at maximum
ration and identical thermal regimes, Atlantic
salmon in the upper size mode (incipient smolts)
had a higher instantaneousgrowth rate in spring
than lower-mode fish (parr), despite the smaller
size of lower-modefish which would, other things
beingequal, resultin higherinstantaneous
growth
rates (Brett 1979). It is unclear, however, whether
this result is a function of the bimodal-growth
pattern, the parr-smolt transformation,or both.
We have recently compared the summergrowth
in fresh water of Atlantic salmon smolts (50 g)
with juveniles (50 g) exposedto continuouslight
that inhibited at least the osmoregulatoryaspects
of the transformation (McCormick et al. 1987).
Instantaneousgrowth rate of smoltsand of fish in
continuouslight over a 6-week period at constant
temperature (13øC) was the same (1.8%/d). We
have concludedthat either continuous-lighttreatment doesnot inhibit all aspectsof the parr-smolt
transformation, or that an increase in scope for
growth (at maximum ration and at 13øC)does not
accompanytransformationin Atlantic salmon.
This
limited
evidence
does not favor
either
acceptanceor rejectionof an increasedscopefor
growthaccompanyingthe parr-smolt transformation. If it doesindeedoccur, it is likely to be large
and more easily detected in speciessuch as Atlantic salmon which spend longer periods (2-5
years) in fresh water. Environmental effects on
growth and scope for growth may also change
after transformation.
There
is indirect
evidence
that the optimumtemperaturefor marine growth
of Atlantic salmonis lower than that for presmolt
growth in fresh water (Reddin and Shearer 1987,
this volume; Saunders 1987). Many fishes show
reducedthermal optima for growth after the early
juvenile stage (Hokanson 1977; Brett 1979; McCauley and Huggins 1979; Jobling 1981). Photoperiodic response may also change. Whereas
growth of Atlantic salmonparr drops sharply in
early autumn (decreasingphotoperiod), despite
favorable temperature and ration levels (R. L.
Saunders, unpublisheddata), postsmolts in sea
cagesappear to continuegrowing rapidly in autumn until temperaturesfall below 4øC (Sutterlin
et al. 1981).Suchan alterationin growthresponse
to photoperiodhas been observedin the bimodal
growth pattern of juvenile Atlantic salmon
(Kristinsson1984;Higgins 1985;Kristinssonet al.
1985; Thorpe 1987a). Substantiationor rejection
of these suppositionscould greatly increase our
understandingof ontogeneticand environmental
influenceson growth in teleosts.
ComparativeAspectsof the Parr Smolt
Transformation
The variety of differentiativeprocesseswhich
occur and their responsiveness
to photoperiodic
cues underline the developmental nature of the
parr-smolt transformation.This developmenthas
often been viewed as a single, size-related event
which occurs seasonallyand is reversible in the
absenceof sea water (Figure 3A). Although this
may be true for someaspectsof the transformation, other aspects, such as silvering, salinity
tolerance,andgillNa+,K+-ATPaseactivity,often
display slight but significantseasonalrhythms in
the absenceof "real" or "total" changesassociated with transformation(Hoar 1965, 1976; Saunders and Henderson 1978; Langdon and Thorpe
1985; McCormick et al. 1987). Perhaps we can
more correctly view these developmental processesas an interactionor synergism(Figure 3D)
between prior development(Figure 3B) and seasonal rhythms (Figure 3C) which manifestsitself
in a critical size and season for transformation.
Each componentof the parr-smolt transformation
may possessa differentgradientof thesedevelop-
PHYSIOLOGY OF THE SALMONID PARR-SMOLT TRANSFORMATION
mentaltypes. The existenceof differentdevelopmental patternsemphasizesthe adaptivevalue of
temporal orchestrationof the many changesthat
occur during the transformation.Otherwise, they
may occur as isolated events or physiological
developmentswhich fall short of the attributes
required for long-term marine residence.
221
Analysisof the parr-smolt transformationas a
developmental process consisting of numerous
componentscan facilitate comparisonsamongsalmonid species. Osmoregulatoryphysiology has
received
the most attention
and can be more
thoroughly explored. Brook trout, a member of
the genus (Salvelinus) that has the least-developed capacity for marine residencein the subfamily Salmoninae(Rounsefell ! 958; Hoar 1976),
migratesinto seawaterat a relatively large size
(>17 cm) and shows variability in the seasonof
migration (White 1940; Wilder 1952; Castonguay
et al. 1982;Montgomeryet al. 1983). The development of salinity tolerance and hypoosmoregulatory ability in brook trout occursat a larger size
than in speciesof Salmo or Oncorhynchus(e.g.,
Figure 3, B versus B'; see also McCormick and
Naiman 1984b).The osmoregulatoryaspectof the
parr-smolt transformation,as characterized by
seasonaldifferentiationof osmoregulatoryorgans
resultingin increasedsalinity tolerance, is undeveloped in brook trout (McCormick and Naiman
1984b; McCormick et al. 1985a). It should be
noted, however, that seasonalsilvering occurs in
anadromousbrook trout populations(thoughthis
is not necessarilyassociatedwith seawater entry:
Black 1981),indicatingthat differentphysiological
changesassociatedwith the parr-smolt transformation can occur independentlyof one another.
Pink salmon Oncorhynchus gorbuscha and
chum salmon represent the opposite end of the
salmonidspectrum, often spendingas little as a
month
or two in fresh water after hatchingbefore
Time
migrating to sea. Salinity tolerance in these two
FIGURE3.--Developmental patterns that may occur for
speciesis incompletein the posthatchalevin stage
different aspectsof the parr-smolt transformation.A: but increases rapidly, permitting survival in sea
Seasonal occurrence of physiologicalchange that is water at sizeslessthan 5 cm long (Weisbart 1968).
dependenton seasonalcues and prior development(a
It seemsprobablethat sucha rapid attainmentof
critical size). B: Differentiationthat is independentof
season.A changefrom B to B' may representa change salinity tolerance will preclude a photoperiodically cued differentiationtypical of other Ono
in ontogeny (i.e., increased growth rate resulting in
corhynchusand Salmo species which undergo
increaseddifferentiationat any time) or phylogeny(i.e.,
a differentrate of differentiationrelative to size resulting transformationand migrate at larger sizes. With
in increased salinity tolerance at any given size). C: the exceptionof changesin gill Na +,K+-ATPase
Seasonalchangethat is independentof size, such as a
activity (Sullivan et al. 1983)and kidney morpholphotoperiod-cuedincrease in growth rate. D: Interaction of seasonand developmentalrate. In this pattern, ogy (Ford 1958), little is known of the differentiaspectsof the parr-smolt transformationare an intensi- ation of osmoregulatoryorgansin pink and chum
fication and synchronizationof seasonalchangesthat salmon. As in seasonallytransformingsalmonids,
are also dependenton prior development.D and D'
prolonged rearing of pink and chum salmon in
represent, for instance, segmentsof a populationthat fresh water results in substantialloss of salinity
will undergothe parr-smolt transformationin the years tolerance(Kashiwagi and Sato 1969; Iwata et al.
n and n + 1, respectively.Analogouschangesin devel1982).
opmental timing may have occurred in the course of
A phylogenetic comparison of the minimum
salmonidevolution (see Figure 4). S representsphysiological differencesbetween parr and smolt; SW is sea- size at which seawater entry occurs in salmonid
water and FW is fresh water.
speciesis presentedin Figure4. The developmen-
A
222
MCCORMICK AND SAUNDERS
Seasonal
Differentiation
E 20--
7
.•/•/Salvelinus
fontinalis
•
.•½'
o• / Salmo
gairdneri
•
•, •5o
=•8
Salmo salar •
.;
;o
lO-
/
o
'• Oncorhynchus
tshawytscha
•
E
o
Oncorhynchus
kisutch•
5
.•4, 10
lO
--
Onc orhynchus gorbuscha •
Oncorhynchus
keta •
FIGURE4.--Phylogeneticcomparisonof the minimumsizeat whichthe developmentof salinitytoleranceoccurs
in the subfamilySalmoninae.Salinitytoleranceis definedasgreaterthan75% survivalin seawater(29%ofor at least
14 d. Seasonaldifferentiation(+) is definedas a photoperiod-controlled
differentiationof osmoregulatoryorgans
resultingin increasedsalinitytolerance.With the exceptionof brooktrout, reversibleontogeneticdifferentiations
have been shown to occur in the depicted species.Phylogeneticrelationshipssuggestthat heterochronyhas
occurredeither through paedomorphosis
(increasingsize at differentiation)or recapitulation(decreasingsize at
differentiation).This hypothesisshouldnot imply existenceof a linearsalmonidlineagebut ratherthat, in the course
of salmonid evolution, heterochrony has occurred in differentiation of osmoregulatoryorgans. References
(superscripts):1, Kashiwagiand Sato (1969);2, Weisbart(1%8); 3, Wagneret al. (1969);4, Conte et al. (1966); 5,
Johnstonand Saunders(1981);6, Conte and Wagner(1965);7, McCormick and Niaman (1984a, 1984b);8, Wagner
(1974b);9, Saundersand Henderson(1970); 10, Clarke et al. (1978).
tal nature of the attainment of salinity tolerance and recapitulationwith a fleshwater origin. Arguand the correspondenceof this phylogeny to ments based on fossil and extant species have
morphometrica!!yand geneticallybasedphyloge- beengiven for freshwater (Tchernavin 1939;Hoar
hies of the subfamily Salmoninae(especiallyin 1976)and seawater(Day 1887;Regan 1911;Balon
that Salrno is intermediate between Salvelinus
1968; Thorpe 1982) origins of salmonids.Develand Oncorhynchus;see Neave 1958 for review) opmental conflict between transformation and
leads us to concludethat heterochrony3in differ- maturation,arguedby Thorpe (1987, this volume)
entiationof hypoosmoregulatory
capacity(andits underlinesthe importanceof changesin the timing
underlying physiological mechanisms)has oc- of developmentin establishinga life history patcurred during the evolution of these species tern. Viewing the parr-smolt transformationas a
(Figure 4; see Balon 1979, 1980and Thorpe 1982 developmentalprocesssubjectto changesin timfor earlier discussionsof heterochrony in salmo- ing during the course of salmonid evolution
nids). The direction of heterochrony,either pae- shouldfacilitatespeciescomparisonand helpgendomorphic(increasedsize at attainmentof salin- erate hypothesesconcerningthe adaptivemechaity tolerancewith advancingphylogeny)or reca- nismsfor seawater entry and their hormonal conpitulatory(decreasedsizeat attainmentof salinity trol. Indeed, it seems likely that changes in the
tolerance) has yet to be established. It seems timing of expression of endocrine mechanisms
likely that paedomorphosiswould be associated controllingthe transformationare responsiblefor
with an ancestral seawater origin for salmonids, the observed heterochrony.
In a "common strategies" symposium,a final
3Heterochronyis definedas changesin the timing of statement on comparative physiological tactics
may seeminappropriatelybrief, yet a longer one
development,followingthe terminologyof Gould
(1978).
is precludedby the limited stateof our knowledge
PHYSIOLOGY
OF THE SALMONID
concerningthe osmoregulatoryphysiologyof diadromous fishes which, with the exception of
salmonidsand anguillids, have been little studied.
The seaward migration of salmon and eels, despitethe many differencesbetweenthesefishes,is
accompaniedby morphologicalchange(such as
silvering) and increasesin salinity tolerance and
gill Na+,K+-ATPase activity (Fontaine 1975;
PARR--SMOLT TRANSFORMATION
223
Fishes 4:193-198.
Balon, E. K. 1980. Comparative ontogeny of charrs.
Pages703-720 in E. K. Balon, editor. Charrs:salmonidfishesof the genusSalvelinus.Dr. W. Junk,
The Hague, The Netherlands.
Baraduc, M. M., and M. Fontaine. 1955. Etude com-
parre du mrtabolismerespiratoiredujeune saumon
srdentaire (parr) et migrateur (smolt). Compte
Rendu des Searicesde !a Socirt6 de Biologie Paris
149:1327-1329.
Thomson and Sargent 1977). The common
"strategy" of these two groups is to make a Bern, H. A. 1978. Endocrinologicalstudieson normal
and abnormalsalmonsmoltification.Pages77-100
single, seasonal seaward migration during their
in P. J. Gaillard and H. H. Boer, editors.Comparlifetime, and they display a "tactic" of undergoative endocrinology.Elsevier/North-Holland Bioing preparatory physiologicaladaptations.This is
medical Press, Amsterdam, The Netherlands.
in contrast to euryhaline species (such as Fun- Black, G. A. 1981.Metazoan parasitesas indicatorsof
dulusspp.) which make repeated,lesspredictable
movementsof anadromousbrook charr (Salvelinus
movements into seawater. These fishes must have
fontinalis) to sea. CanadianJournalof Zoology 59:
1892-1896.
the capacity to alter osmoregulatoryphysiology
more frequently, and it is generallybelievedthat Blake, R. L., F. L. Roberts, and R. L. Saunders. 1984.
Parr-smolt
transformation
of Atlantic
salmon
these changesare induced by environmentalsa(Saltnosalar):activitiesof two respiratoryenzymes
linity (Karnaky 1986). One might predict, thereand concentrations of mitochondria in the liver.
fore, that preparatory physiologicaladaptations
CanadianJournalof Fisheriesand Aquatic Sciences
41:199-203.
.for seawater entry entailing ontogeneticdifferentiation would occur in specieswhich make a single Boeuf, G., P. Lasserre, and Y. Harache. 1978. Osmotic
adaptationof Oncorhynchuskisutch Walbaum. II.
seaward migration. Conversely, diadromous or
Plasma osmotic and ionic variations, and gill
nondiadromousfisheswhich make repeated seaNa+,K+-ATPase activity of yearling coho salmon
water entries seem less likely to display such a
transferredto seawater.Aquaculture 15:35-52.
tactic and may rely more heavily on inductionby Boeuf,G., A. LeRoux, J. L. Gaignon,and Y. Harache.
external salinity of a perpetualhypoosmoregula1985.Gill (Na+,K+)-ATPase activity and stoolting
in Atlantic salmon(Saltno salar) in France. Aquatory capacity.
culture 45:73-8
Acknowledgments
This paper was greatly improvedby the critical
comments of Howard
A.
Bern, Richard S.
Nishioka, Arthur W. Rourke, Robert L. Stephenson, Clive Talbot, John E. Thorpe, and Graham
Young. William McMullon and Franklin Cunningham drew the figures, and Jeanine Hurley typed
the manuscript.S. D. McCormick was supported
by a postdoctoralfellowship from the Natural
Sciences and Engineering Research Council of
Canada and the Department of Fisheries and
Oceans.
I.
Bradley, T. M., and A. W. Rourke. 1984. An electrophoretic analysisof plasma proteinsfrom juvenile
Oncorhynchustshawytscha(Walbaum). Journal of
Fish Biology 24:703-709.
Brett, J. R. 1979. Environmental factors and growth.
Pages599-677 in W. S. Hoar, D. J. Randall, and
J.R. Brett, editors. Fish physiology, volume 8.
Bioenergeticsand growth. Academic Press, New
York, New York, USA.
Buckman, M., and R. D. Ewing. 1982. Relationship
betweensize and time of entry into the seaand gill
(Na+-K+)-ATPase activity for juvenile springchinook salmon. Transactions
of the American
Fish-
eries Society l I 1:681-687.
Castonguay,M., G. J. Fitzgerald,and Y. C6tr. 1982.
References
Baggerman,B. 1960. Salinity preference, thyroid activity and the seaward migrationof four speciesof
Pacificsalmon(Oncorhynchus).
Journalof the Fisheries Research Board of Canada 17:295-322.
Balon, E. K. 1968. Notes to the origin and evolutionof
trouts and salmonswith special reference to the
Danubian trouts. Vestnik Ceskolovenske Spolecnosti Zoologicke32:1-21.
Balon, E. K. 1979. The juvenilization process in phy!ogeny and the altricial to precocial forms in the
ontogeny of fishes. Environmental Biology of
Life history movements of anadromous brook
charr, Salvelinusfontinalis, in the St. Jean river,
Gaspr, Qurbec. CanadianJournal of Zoology 60:
3084-3091.
Chernitsky,A. G. 1983.Adaptive significanceof smoltification in the Atlantic salmon, Salmo salar. Journal of Evolutionary Biochemistryand Physiology
19:186-190.
Chernitsky, A. G., and L. Ya. Shterman. 1981. Peculiarities of osmoregulationin the migratingjuvenile
Atlantic salmons.Voprosy lkhtiologii 21:497-502.
Clarke, W. C. 1982. Evaluation of the seawater chal-
lengetest as an index of marine survival. Aquacul-
224
MCCORMICK AND SAUNDERS
ture 28:177-183.
Ericinska, M., and F. F. Wilson. 1982. Regulation of
cellular energy metabolism.Journal of Membrane
Clarke, W. C., H. Lundqvist,and L.-O. Eriksson.1985.
Biology 70:1-14.
Accelerated photoperiodadvances seasonalcycle
of seawater adaptation in juvenile Baltic salmon, Eriksson, L.-O., and H. Lundqvist. 1982. Circannual
Saltno salar L. Journalof Fish Biology 26:29-35.
rhythms of growth and smoltingin Baltic salmon.
Clarke, W. C., and Y. Nagahama. 1977. Effect of preAquaculture28:113-122.
mature transfer to sea water on growth and mor- Evans, D. H. 1979. Fish. Pages305-390 in G. M. O.
Maloiy, editor. Osmotic and ionic regulation in
phology of the pituitary, thyroid, pancreas,and
animals, volume 1. Academic Press, London, Eninterrenal in juvenile coho salmon (Oncorhynchus
kisutch). Canadian Journal of Zoology 54:
gland.
1620-1630.
Evropeytseva,N. V. 1962.[Comparativeanalysisof the
Clarke, W. C., J. E. Shelbourn, and J. R. Brett, Jr.
desmoltificationprocessamong the young of different ecological forms of Atlantic salmon.]
1978.Growth and adaptationto sea water in underUchenye Zapiski LeningradskogoGosudarstrenyeafling sockeye(Oncorhynchusnerka) and coho
nogo Universiteta311:46-76. Translatedfrom Rus(0. kisutch) salmon subjectedto regimesof consian: Fisheries Research Board of Canada Translastant or changingtemperatureand daylength.Cation Series 431, Ottawa, Canada.
nadian Journalof Zoology 56:2413-2421.
Collie, N. L., and H. A. Bern. 1982.Changesin intes- Ewing, R. D., C. A. Fustich, S. L. Johnson,and H. J.
tinal fluid transport associatedwith smoltification
Pribble. 1980. Seaward migrationof juvenile chinook salmonwithout elevatedgill (Na+ K)-ATPase
and seawater adaptation in coho salmon, Onactivities. Transactions of the American Fisheries
corhynchus kisutch (Walbaum). Journal of Fish
Society 109:349-356.
Biology 21:337-348.
Conte, F.P. 1969. The biochemicalaspects of salt Farmer, G.J., J.A. Ritter, and D. Ashfield. 1978.
secretion. Pages 105-120 in O. W. Neuhaus and
Seawateradaptationand parr-smolt transformation
J. E. Haiver, editors. Fish in research. Academic
of juvenile Atlantic salmon,Saltnosalar. Journalof
the Fisheries Research Board of Canada 35:93-100.
Press, New York, New York, USA.
Conte, F. P., and H. H. Wagner. 1965.Developmentof Fessler,J. L., and H. H. Wagner. 1969. Some morphological and biochemicalchangesin steelheadtrout
osmotic and ionic regulationin juvenile steelhead
trout Saltno gairdneri. ComparativeBiochemistry
during the parr-smolt transformation.Journal of
the Fisheries Research Board of Canada 26:
and Physiology14:603-620.
2823-2841.
Conte, F. P., H. H. Wagner, J. Fessler,and C. Gnose.
1966. Developmentof osmoticand ionic regulation Folmar, L. C., and W. W. Dickhoff. 1980. The parrsmolt transformation(smoltification) and seawater
in juvenile coho salmon (Oncorhynchuskisutch).
adaptationin salmonids.A review of selectedliterComparativeBiochemistryand Physiology18:1-15.
ature. Aquaculture 21:1-37.
Cowey, C. B., and G. Parry. 1963. The non-protein
nitrogen constituentsof the muscle of parr and Folmar, L. C., W. W. Dickhoff, C. V. M. Mahnken,
smolt stagesof the Atlantic salmon(Saltno salar).
and F. W. Waknitz. 1982. Stuntingand parr-reverComparativeBiochemistryand Physiology8:47-51.
sion during smoltificationof coho salmon (Oncorhynchuskisutch). Aquaculture 28:91-104.
Day, F. 1887. British and Irish salmonidae.Williams
Fontaine, M. 1951. Sur la diminution de la teneur en
and Norgate, London, England.
Dickhoff, W. W., and C. Sullivan. 1987. Involvement of
chlore du muscledesjeunes saumons(smolts)1ors
de la migrationd'avalaison.ComptesRendusHebthe thyroid gland in smoltificationwith special
domadaires des S•ances de l'Acad•mie
des Scireference to metabolic and developmentalproences 232:2477-2479.
cesses. American Fisheries Society Symposium
1:197-210.
Fontaine, M. 1975. Physiological mechanisms in the
migration of marine and amphihaline fish. AdEddy, F.B. 1982. Osmotic and ionic regulation in
captive fish with particular referenceto salmonids.
vancesin Marine Biology 3:241-355.
Fontaine, M., andJ. Hatey. 1953.Contribution/• !'•tude
Comparative Biochemistry and Physiology B,
Comparative Biochemistry73:125-141.
du m•tabolismeglucidiquedu saumon(Salmo salar
Eddy, F. B0, and C. Talbot. 1985. Urine productionin
L.)/• diverses•tapes de son d•velopment et de ses
smoltingAtlantic salmon,Saltno salar L. Aquaculmigrations.PhysiologiaComparataet Oecologia3:
ture 45:67-72.
36-52.
Elson, P. F. 1957.The importanceof size in the change Fontaine, M., and J. Marchelidon. 1971. Amino acid
from parr to smolt in Atlantic salmon. Canadian
contents of the brain and the muscle of young
Fish Culturist 21:1-6.
salmon(Saltno salar L.) at parr and smolt stages.
Epstein, F. H., A. I. Katz, and G. E. Pickford. 1967.
Comparative Biochemistry and Physiology A,
Sodiumand potassium-activated
adenosinetriphosComparativePhysiology40:127-134.
phataseof gills: role in adaptationof teleoststo salt Fontaine, M., M. Mazeaud, and F. Mazeaud. 1963.
water. Science(Washington,D.C.) 156:1245-1247.
L'adr•nalin•mie du Saltno salar L. /• queiques
Epstein, F. H., P. Silva, and G. Kormanik. 1980. Role
•tapes de son cycle vital et de ses migrations.
of Na-K-ATPase
in chloride cell function. AmeriComptesRendusHebdomadairesdes S•ances de
!'Acad•mie des Sciences 256:4562-4565.
can Journalof Physiology238:R246-R250.
PHYSIOLOGY OF THE SALMONID PARR-SMOLT TRANSFORMATION
Ford, P. 1958.Studieson the developmentof the kidney
of the Pacific pink salmon(Oncorhynchusgorbuscha (Walbaum). Il. Variation in glomerularcountof
the kidney of the Pacific salmon.CanadianJournal
of Zoology 36:45-47.
Foskett, J. K., H.A.
Conner.
Bern, T. E. Machen, and M.
1983. Chloride
cells and the hormonal
control of teleost fish osmoregulation.Journal of
Experimental Biology 106:255-281.
Foskett, J. K., and C. Scheffey.1982.The chloridecell:
definitive identificationas the salt-secretorycell in
teleosts. Science(Washington,D.C.) 215:164-166.
Fried, S. M., J. D. McCleave, and G. W. LaBar. 1978.
Seaward migration of hatchery-reared Atlantic
salmon, Salrno salar, smolts in the PenobscotRiver
estuary, Maine:riverine movements.Journal of the
Fisheries Research Board of Canada 35:76-87.
Giles, M. A., and W. E. Vanstone. 1976a. Changesin
ouabain-sensitiveadenosinetriphosphataseactivity
in gills of coho salmon (Oncorhynchuskisutch)
during parr-smolt transformation. Journal of the
Fisheries Research Board of Canada 33:54-62.
225
Hoar, W. S. 1976. Smolt transformation:evolution, behavior and physiology. Journal of the Fisheries
Research Board of Canada 33:1233-1252.
Hogstrand, C., and C. Haux. 1985. Evaluation of the
seawaterchallengetest on sea trout, Salmo trutta.
Comparative Biochemistry and Physiology A,
ComparativePhysiology82:261-266.
Hokanson,K. E. F. 1977.Temperaturerequirementsof
somepercidsand adaptationsto the seasonaltemperaturecycle. Journalof the FisheriesResearch
Board of Canada 34:1524-1550.
Holmes, W. N., and I. M. Stainer. 1966. Studies on the
renal excretion of electrolytes by the trout Salmo
gairdneri. Journal of Experimental Biology 44:
33-46.
Houston, A. H. 1961. Influenceof size upon the adaptation of steelhead trout (Salrno gairdneri) and
chum salmon (Oncorhynchusketa) to sea water.
Journal of the Fisheries Research Board of Canada
18:401-415.
Houston,A. H., and L. T. Threadgold.1963.Body fluid
regulationin stooltingAtlantic salmon. Journal of
the Fisheries Research Board of Canada 20:
Giles, M. A., and W. E. Vanstone. 1976b.Ontogenetic
1355-1369.
variation in the multiple hemoglobinsof coho
salmon (Oncorhynchuskisutch) and the effect of lwata, M., S. Hasegawa, and T. Hirano. 1982. Deenvironmentalfactors on their expression.Journal
creasedseawateradaptabilityof chum salmon(Onof the Fisheries Research Board of Canada 33:
corhynchusketa) fry followingprolongedrearingin
freshwater.
1144-1149.
GIova, G. J., and J. E. Mclnerney. 1977.Critical swimming speedsof coho salmon (Oncorhynchuskisutch) fry to smolt stagesin relationto salinity and
temperature. Journal of the Fisheries Research
Board of Canada 34:151-154.
Gorbman, A., W.W. Dickhoff, J. L. Mighell, E. F.
Prentice, and F. W. Waknitz. 1982. Morphological
indicesof developmentalprogressin the parr-smolt
coho salmon, Oncorhynchuskisutch. Aquaculture
28:1-19.
Canadian
Journal
of Fisheries
and
Aquatic Sciences39:509-514.
lwata, M., R. S. Nishioka, and H. A. Bern. In press.
Whole animal transepithelial potential (TEP) of
coho salmonduringthe parr-smolt transformation
and effects of thyroxine, prolactin and hypophysectomy.Fish Physiologyand Biochemistry.
Jobling, M. 1981. Temperature tolerance and the final
preferendure--rapidmethodsfor the assessment
of
optimumgrowth temperatures.Journalof Fish Biology 19:439-455.
Gould, S. J. 1978. Ontogeny and phylogeny. Harvard Johnston, C. E., and J. G. Eales. 1967. Purines in the
University Press, Cambridge, Massachusetts,
integumentof the Atlantic salmon (Salrno salar)
USA.
during parr-smolt transformation. Journal of the
Fisheries Research Board of Canada 24:955-964.
Gross, M. A. 1987. Evolution of diadromy in fishes.
Johnston,C. E., and R. L. Saunders. 1981. Parr-smolt
American FisheriesSociety Symposium1:14-25.
Hart, C. E., G. Concannon, C. A. Fustish, and R. D.
transformationof yeafling Atlantic salmon (Salrno
salar) at several rearing temperatures. Canadian
Ewing. 1981. Seawardmigrationand gill (Na+K)Journal of Fisheries and Aquatic Sciences 38:
ATPase activity of spring chinook salmon in an
artificial
stream.
Transactions
of the American
1189-1198.
FisheriesSociety 110:44-50.
Hickman, C. P., and B. F. Trump. 1969. The kidney.
Pages 91-239 in W. S. Hoar and D.J. Randall,
editors. Fish physiology, volume 1. Excretion,
ionic regulation,and metabolism.AcademicPress,
Jonsson,B., and J. Rudd-Hansen. 1985. Water temperature as the primary influenceof timingof seaward
migrationsof Atlantic salmon(Saltno salar) smolts.
CanadianJournalof Fisheriesand AquaticSciences
New York, New York, USA.
Higgins, P. J. 1985. Metabolic differencesbetween Atlantic salmon(Salmo salar) parr and smolts.Aqua-
Kalleberg, H. 1958. Observationsin a stream tank of
territorialityandcompetitioninjuvenile salmonand
trout (Saltno salar L. and S. trutta L.). Institute of
Freshwater Research Drottningholm Report 39:
culture 45:33-54.
Hoar, W. S. 1939. The thyroid gland of the Atlantic
salmon.Journalof Morphology65:257-295.
Hoar, W. S. 1965. The endocrinesystemas a chemical
link between the organismand its environment.
Transactionsof the Royal Society of Canada 3:
175-200.
42:593-595.
55-98.
Karnaky, K.J.
1986. Structure and function of the
chloride cell of Fundulus heteroclitus
and other
teleosts.AmericanZoologist26:209-224.
Kashiwagi, M., and R. Sato. 1969. Studies of the
osmoregulationof chum salmon, Oncorhynchus
226
MCCORMICK AND SAUNDERS
keta (Walbaum). I. The toleranceof eyed period of
eggs,alevinsand fry of the chum salmonto seawater. Tohoku Journal of Agricultural Research 20:
of the salmonin its youngfreshwaterstages.Biochemical Journal 28:1961-1963.
Lundqvist, H., and L.-O. Eriksson. 1985. Annual
41-47.
rhythmsof swimmingbehaviorand seawateradapKing, P. A., and L. Goldstein.1983.Organicosmolytes
tationin youngBaltic salmon,Salmosalar, associand cell volumeregulationin fish. MolecularPhysated with smolting. Environmental Biology of
Fishes 14:259-267.
iology 4:53-66.
Kirschher, L. B. 1980. Comparison of vertebrate salt- Maetz, J., and F. Garcia-Romeau. 1964. The mechanism
of sodiumand chloride uptake by the gills of a
excretingorgans.AmericanJournalof Physiology
238:R219-R223.
freshwaterfish, Carassiusauratus. II. Evidence for
Knutsson,S., and T. Grav. 1976. Seawateradaptation
NHn+/Na+ and HCO3-/Cl- exchanges.Journalof
in Atlantic salmon(Salrnosalar) at differentexperGeneral Physiology47:1209-1227.
imental temperaturesand photoperiods.Aquacul- Mahnken, C., E. Prentice, W. Waknitz, G. Moran, C.
ture 8:169-187.
Sims, and J. Williams. 1982. The applicabilityof
recent smoltificationresearch to public hatchery
Koch, H. J. 1982.Hemoglobinchangeswith sizein the
Atlantic salmon (Salrno salar L.). Aquaculture 28:
releases:anassessmentof size/time requirements
231-240.
for Columbia River hatchery coho salmon (Oncorhynchuskisutch). Aquaculture 28:251-268.
Koch, H. J., and J. C. Evans. 1959.Sodiumregulation
in the bloodof parr and smoltstagesof the Atlantic Malikova, E. M. 1957. Biochemicalanalysisof young
salmon at the time of their transformation to a
salmon. Nature (London) 184:283-284.
Komourdjian,M. P., R. L. Saunders,and J. C. Fernconditioncloseto the smoltstageand duringreten-.
wick. 1976. Evidence for the role of growth hortion of smolts in fresh water. Trudy Latviiskovo
Otdeleniia VNIRO 2:241-255.
mone as a part of a 'light-pituitaryaxis' in growth
and smoltificationof Atlantic salmon(Salrnosalar). McCartney, T. H. 1976. Sodium-potassiumdependent
CanadianJournalof Zoology54:544-551.
adenosinetriphosphataseactivity in gills and kidneys of Atlantic salmon (Salmo salar). ComparaKristinsson,J. B. 1984. Factorsinfluencingthe growth
of juvenile Atlantic salmon.Doctoral dissertation.
tive Biochemistry
andPhysiology
A, Comparative
Physiology53:351-353.
University of New Brunswick, Fredericton, Canada.
McCauley, R. W., and N. W. Huggins. 1979. Ontogenetic and non-thermal seasonal effect on thermal
Kristinsson, J. B., R. L. Saunders,and A. J. Wiggs.
1985.Growth dynamicsduringthe developmentof
preferendaof fish. AmericanZoologist19:267-271.
bimodal length-frequencydistribution in juvenile McCormick,S. D., andR. J. Naiman.1984a.OsmoregAtlantic salmon (Salrno salar L.). Aquaculture 45:
ulation in the brook trout, Salvelinusfontinalis. I.
1-20.
Diel, photoperiodand growth relatedphysiological
Kubo, T. 1953.On the bloodof salmonidfishesof Japan
changesin freshwater.ComparativeBiochemistry
duringmigration.I. Freezingpointof blood.Bulleand Physiology A, Comparative Physiology 79:
7-16.
tin of the Faculty of FisheriesHokkaido University
4:138-148.
McCormick,S. D., andR. J. Naiman. 1984b.OsmoregKubo, T. 1955. Changes of some characteristicsof
ulation in the brook trout, Salvelinusfontinalis. II.
blood of smolts of Oncorhynchus masou during
Effects of size, age and photoperiodon seawater
seawardmigration. Bulletin of the Faculty of Fishsurvival and ionic regulation. Comparative Bioeries Hokkaido University 6:201-207.
chemistryand PhysiologyA, ComparativePhysiology 79:17-28.
Langdon,J. S., and J. E. Thorpe. 1984.Responseof the
gill Na+-K + ATPase, succinicdehydrogenase
ac- McCormick,S. D., R. J. Naiman,and E. T. Montgomtivity and chloride cells to saltwateradaptationin
ery. 1985. Physiologicalsmolt characteristicsof
Atlantic salmon, Salmo salar L., parr and smolt.
anadromousand non-anadromousbrook trout (Salvelinus fontinalis) and Atlantic salmon (Salmo
Journalof Fish Biology24:323-331.
Langdon, J. S., and J. E. Thorpe. 1985. The ontogeny
salar). CanadianJournal of Fisheriesand Aquatic
Sciences 42:529-538.
of smoltification:developmentalpatterns of gill
McCormick, S. D., R. L. Saunders,E. B. Henderson,
Na+/K+-ATPase, SDH, and chloridecells in juvenile Atlantic salmon, Salmo salar L. Aquaculture
and P. R. Harmon. 1987. Photoperiod control of
45:83-96.
parr-smolt transformation in Atlantic salmon
Lasserre, P., G. Boeuf, and Y. Harache. 1978. Osmotic
(Salmo salar): changesin salinity tolerance, gill
adaptation of Oncorhynchuskisutch Walbaum. I.
Na+,K+-ATPase and plasma thyroid hormones.
Seasonalvariationsof gill Na+-K + ATPaseactivity
CanadianJournalof Fisheriesand AquaticSciences
44:1462-1468.
in coho salmon, 0+-age and yearling, reared in
freshwater. Aquaculture 14:365-382.
Mclnerney, J. E. 1964. Salinity preference:anorientaLoretz, C. A., N. L. Collie, N. H. Richman,and H. A.
tion mechanismin salmonmigration.Journalof the
Fisheries Research Board of Canada 21:995-1018.
Bern. 1982. Osmoregulatorychangesaccompanying smoltificationin coho salmon.Aquaculture28: Montgomery,W. L., S. D. McCormick,R. J. Naiman,
67-74.
F. G. Whoriskey, and G. A. Black. 1983. Spring
Lovern, J. A. 1934. Fat metabolismin fishes.V. The fat
migratorysynchronyof salmonid,catostomioland
PHYSIOLOGY OF THE SALMONID PARR--SMOLT TRANSFORMATION
cyprinid fishes in Rivib•re a 1• Truite, Qu6bec.
CanadianJournalof Zoology61:2495-2502.
Neave, F. 1958.The originand speciationof Oncorhynchus.Transactionsof the Royal Societyof Canada,
Section 5:BiologicalSciences52:25-39.
Okumura, N.,
S. Otsuki, and H. Nasu. 1959. The
227
eels(Anguilla anguilla). ComparativeBiochemistry
and PhysiologyB, Comparative Biochemistry51:
75-79.
Saunders,R. L. 1965.Adjustmentof buoyancyin young
Atlantic salmon and trout by changesin swimbladder volume. Journal of the Fisheries Research
Board of Canada 22:335-352.
influencesof hypoglycaemiccoma, repeated electroshocks and chlorpromazine or fl-phenyliso- Saunders,R. L. 1987. The thermal biology of Atlantic
propylmethylamine administration on the free
salmon:influenceof temperature on salmon culture
amino acids in the brain. Journalof Biochemistry
with particularreferenceto constraintsimposedby
47:207-247.
low temperature.Institute of FreshwaterResearch
Ota, T., and M. Yamada. 1974a.Lipids of masusalmon.
DrottningholmReport 65.
II. Seasonalvariationsin the lipidsof masusalmon Saunders, R. L., and E. B. Henderson. 1969. Survival
parr during the life in freshwater. Bulletin of the
and growth of Atlantic salmon parr in relation to
JapaneseSocietyof ScientificFisheries40:699-706.
salinity. FisheriesResearchBoard of CanadaTechOta, T., and M. Yamada. 1974b.Lipids of masusalmon.
nical Report 147.
Ill. Differencesin the lipids of residualtype and Saunders, R. L., and E. B. Henderson. 1970. Influence
seawardmigrationtype of masusalmonparr during
of photoperiodon smoltdevelopmentandgrowthof
the period of seaward migration. Bulletin of the
Atlantic salmon(Salmo salar). Journalof the Fisheries Research Board of Canada 27:1295-1311.
JapaneseSociety of Scientific Fisheries40:707-713.
Ouchi, K. 1985. Effect of cortisolon the salinitytoler- Saunders,R. L., and E. B. Henderson. 1978. Changes
ance of masu salmon (Oncorhynchusrnasou)parr
in gill ATPase activity and smolt statusof Atlantic
adapted to different salinities. Bulletin of the Nasalmon (Saltno salar). Journal of the Fisheries
Research Board of Canada 35:1542-1546.
tional ResearchInstitute of Aquaculture7:21-27.
Parry, G. 1958. Size and osmoregulationin salmonid Saunders, R. L., E. B. Henderson, and B. D. Glebe.
1982. Precocious sexual maturation and smoltificafishes. Nature (London) 181:1218-1219.
Parry, G. 1960.The developmentof salinitytolerancein
tion in male Atlantic salmon(Salmo salar). Aquaculture 28:211-229.
the salmon, Saltno salar (L.), and some related
species. Journal of Experimental Biology 37: Saunders, R. L., E. B. Henderson, and P. R. Harmon.
425-434.
1985.Effectsof photoperiodonjuvenile growthand
Parry, G. 1961.Osmoticand ionic changesin blood and
smoltingof Atlantic salmon and subsequentsurmuscle of migratingsalmonids.Journal of Experivival and growth in sea cages. Aquaculture 45:
55-66.
mental Biology 38:411-427.
Phillips, A.M. 1969. Nutrition, digestion and energy Saunders, R.L., E.B. Henderson, P.R. Harmon,
C. E. Johnston, and J. G. Eales. 1983. Effects of
utilization. Pages391-432 in W. S. Hoar and D. J.
Randall, editors. Fish Physiology,volume 1. Excrelow environmental pH on smolting of Atlantic
tion, ionic regulation, and metabolism.Academic
salmon(Saltno salar). CanadianJournalof FisherPress, New York, New York, USA.
ies and Aquatic Sciences40:1203-1211.
Pinder, L., and J. G. Eales. 1969. Seasonalbuoyance Schreck, C. B. 1981. Stress and compensationin telchangesin Atlantic salmon(Saltno salar) parr and
eosteanfishes:response
to social and physical facsmolt. Journal of the Fisheries Research Board of
tors. Pages 295-321 in A.D. Pickering, editor.
Canada 26:2093-2100.
Stress and fish. Academic Press, New York, New
York, USA.
Power, G. 1959.Field measurementof the basaloxygen
consumptionof Atlantic salmon parr and smolts. Schreck, C. B. 1982. Stress and rearing of salmonids.
Arctic 12:195-202.
Aquaculture 128:241-249.
Reddin, D. G., and W. M. Shearer. 1987. Sea-surface
temperature and distribution of Atlantic salmon in
the northwest Atlantic Ocean. American Fisheries
Society Symposium1:262-275.
Regan, C. T. 1911. The freshwater fishesof the British
Isles. Methuen, London, England.
Richman,N. H. 1985.Hormonesand osmoregulationin
developing coho salmon (Oncorhynchuskisutch).
Doctoral dissertation. University of California,
Berkeley, California, USA.
Rounsefell, G. A. 1958. Anadromy in North American
Salmonidae.U.S. Fish and Wildlife ServiceFishery
Bulletin 58(131):171-185.
Sargent, J. R., A.J. Thompson, and M. Bornancin.
1975. Activities and localization of succinic dehydrogenase and Na+/K+-activated adenosine triphosphatasein the gills of freshwaterand seawater
Sheridan, M. A., and W. V. Allen. 1983. Wax esters in
the liver andserumof steelheadtrout, Salmogairdneri Richardson. Comparative Biochemistry and
Physiology B, Comparative Biochemistry 74:
251-253.
Sheridan, M. A., W. V. Allen, and T. H. Kerstetter.
1983.Seasonalvariationsin the lipid compositionof
the steelheadtrout, Salmo gairdneri Richardson,
associated with the parr-smolt transformation.
Journalof Fish Biology 23:125-134.
Sheridan, M. A., W. V. Allen, and T. H. Kerstetter.
1985a. Changes in the fatty acid composition of
steelheadtrout, Salmo gairdneri Richardson,associated with parr-smolt transformation.Comparative Biochemistryand PhysiologyB, Comparative
Biochemistry80:671-676.
Sheridan, M.A.,
N. Y. S. Woo, and H.A.
Bern.
228
MCCORMICK AND SAUNDERS
1985b.Changesin the ratesof glycogenesis,
glycogenolysis,lipogenesisand !ipolysisin selectedtissues of the coho salmon (Oncorhynchuskisutch)
associatedwith parr-smolt transformation.Journal
of Experimental Zoology 236:35-44.
Silva, P., R. Solomon, K. Spokes, and F. H. Epstein.
1977. Ovabain inhibitionof gill Na-K-ATPase relationship to active chloride transport. Journal of
Experimental Zoology 199:419-426.
Simpson,T. H. 1985.Epilogue.SalmonidSmoltification
Workshop. Aquaculture45:395-398.
Smith, L. S. 1982.Decreasedswimmingperformanceas
a necessarycomponentof the smolt migration in
salmon in the Columbia River. Aquaculture 28:
sity Press, Ames, Iowa, USA.
Thorpe, J. E. 1987b.Smoltingversusresidency:developmentalconflict in salmonids.American Fisheries
SocietySymposium1:244-252.
Thorpe, J. E., C. Talbot, and C. Villareal. 1982. Bimodality of growth and stooltingin Atlantic salmon,
Salmo salar L. Aquaculture 28:123-132.
Vanstone, W. E., and J. R. Markert. 1968. Some morphological and biochemical changes in coho
salmon, Oncorhynchuskisutch, during the parr-smolt transformation. Journal of the Fisheries Research Board of Canada 25:2403-2418.
Vanstone, W. E., E. Roberts, and H. Tsuyuki. 1964.
Changes in the multiple hemoglobin patterns of
153-162.
somePacificsalmon,genusOncorhynchus,during
Sullivan, C. V., W. W. Dickhoff, S. D. Brewer, and
the parr-smolttransformation.CanadianJournalof
G.P. Johnston. 1983. Plasma thyroid-hormone
Physiologyand Pharmacology42:697-703.
concentrationsand gill (Na+K)-ATPase activities Virtanen, E., and A. Oikari. 1984. Effects of low accliin postemergentpink salmon. Transactionsof the
mation temperature on salinity adaptation in the
American FisheriesSociety 112:825-829.
presmoltsalmon,Salmo salar L. ComparativeBioSullivan, C. V., W. W. Dickhoff, C. V. W. Mahnken,
chemistryand PhysiologyA, ComparativePhysiology 78:387-392.
and W. K. Hershberger.1985.Changesin hemoglobin system of the coho salmon (Oncorhynchus Virtanen, E., and A. Soivio. 1985. The patterns of
kisutch during smoltificationand triiodothyronine
T3,T4, cortisoland Na+-K+-ATPase during smoltification of hatchery-rearedSalmo salar and comand prophthiouraciltreatment. Comparative Biochemistryand PhysiologyA, ComparativePhysiolparisonwith wild smolts.Aquaculture45:97-109.
ogy 81:807-813.
Wagner, H.H. 1974a. Photoperiod and temperature
Sutterlin, A.M., E. B. Henderson, S. P. Merrill, R. L.
regulation of smolting in steelhead trout (Salmo
Saunders,and A. A. MacKay. 1981.Salmonidreargairdneri). Canadian Journal of Zoology 52:219234.
ing trials at Deer island, New Brunswick, with
some projections of economic viability. Canadian Wagner,H. H. 1974b.Seawateradaptationindependent
TechnicalReportof FisheriesandAquaticSciences
of photoperiodin steelheadtrout (Salmo gairdneri).
1011.
CanadianJournalof Zoology 52:805-812.
Talbot, C., F. B. Eddy, and J. Johnston. 1982. Osmo- Wagner, H. H., F. P. Conte, and J. L. Fessler. 1969.
regulationin salmonand sea trout alevins. Journal
Developmentof osmoticand ionic regulationin two
of Experimental Biology 101:61-70.
races of chinook salmonO. tshawytscha.ComparTchernavin,V. 1939.The originof salmon.Salmonand
ative Biochemistryand Physiology29:325-341.
Trout Magazine 95:120-140.
Wedemeyer,G. A., R. L. Saunders,and W. C. Clarke.
Thomson,A. J., and J. R. Sargent.1977.Changesin the
1980.Environmentalfactorsaffectingsmoltification
and early marine survival of anadromous salmolevels of chloride cells and (Na+,K+)-dependent
nids. U.S. National Marine Fisheries Service MaATPase in the gills of yellow and silver eels adaptrine Fisheries Review 42(6): 1-14.
ing to seawater. Journal of Experimental Zoology
200:33-40.
Weisbart, M. 1968. Osmotic and ionic regulation in
Thorpe, J. E. 1977. Bimodal distribution of length of
embryos, alevins, and fry of the five species of
juvenile Atlantic salmon (Salmo salar L.) under
Pacific salmon. Canadian Journal of Zoology 46:
385-397.
artificial rearingconditions.Journalof Fish Biology
11:175-184.
Wendt, C. A. G., and R. L. Saunders.1973.Changesin
Thorpe, J. E. 1982.Migrationin salmonids,with special
carbohydratemetabolismin youngAtlantic salmon
in responseto variousforms of stress.international
reference to juvenile movements in freshwater.
Pages 86-97 in E. L. Brannon and E.O. Salo,
Atlantic Salmon Foundation Special Publication
Series 4:55-82.
editors. Proceedingsof the salmonand trout migratory behavior symposium.University of Washing- White, H. C. 1940. Life-history of sea-runningbrook
ton, School of Fisheries, Seattle, Washington,
trout (S. fontinalis) of Moser River, N. S. Journal
USA.
of the Fisheries
Research
Board of Canada
5:
176-186.
Thorpe, J. E. 1986. Age at first maturity in Atlantic
salmon, Salmo salar:freshwaterperiod influences Wilder, D.G. 1952. A comparative study of anadroand conflictswith smolting.CanadianSpecialPubmous and freshwater populations of brook trout
(Salvelinus fontinalis (Mitchell)). Journal of the
lication of Fisheriesand Aquatic Sciences89:7-14.
Fisheries Research Board of Canada 9:169-202.
Thorpe, J.E. 1987a. Environmental regulation of
growth patterns in juvenile Atlantic salmon.Pages Withey, K. G., and R. L. Saunders. 1973. Effect of a
463-474 in R. C. Summerfelt and G. E. Hall, edireciprocalphotoperiodregimeon standardrate of
tors. Age and growthin fishes.Iowa State Univeroxygenconsumptionof postsmoltAtlantic salmon
PHYSIOLOGY OF THE SALMONID PARR--SMOLT TRANSFORMATION
(Salrno salar). Journal of the Fisheries Research
Board of Canada 30:1898-1900.
Woo, W. Y. S., H. A. Bern, and R. S. Nishioka. 1978.
Changesin bodycompositionassociated
with smolt-
ificationandprematuretransferto seawaterin coho
salmon (Oncorhynchuskisutch) and king salmon
(0. tschawytscha).Journal of Fish Biology 13:
421-428.
Wood, C. M., and D. J. Randall. 1973.The influenceof
swimming activity on sodium balance in the rainbow trout (Salmo gairdneri). Journal of Comparative Physiology82:207-233.
229
Zaugg, W.S., and L.R. McLain. 1970. Adenosine
triphosphatase
activity in gills of salmonids:seasonal variations and salt water influences in coho
salmon,Oncorhynchuskisutch. ComparativeBiochemistryand Physiology35:587-596.
Zaugg, W. S., and H. H. Wagner. 1973. Gill ATPase
activity related to parr-smolt transformationand
migration in steelhead trout (Salmo gairdneri):
influenceof photoperiodandtemperature.Comparative Biochemistryand PhysiologyB, Comparative
Biochemistry45:955-965.