Pacific salmon (Oncorhynchus spp.) early marine feeding patterns based on 15N/14N and 13C/12C in...

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Pacific salmon (Oncorhynchus spp.) early marine

feeding patterns based on 15 N/ 14N and 13 C/ 12 C in

Prince William Sound, Alaska

Thomas C. Kline, Jr., and T. Mark Willette

Abstract: Nitrogen and carbon mass and stable isotope composition among cohorts of Pacific salmon ( Oncorhynchus

spp.) released from Prince William Sound, Alaska, hatcheries in 1994 varied widely, suggesting a range in early marine

feeding patterns. Analyses consisted of whole-body stable carbon and nitrogen mass and stable isotope composition of

selected release-date cohorts that had been identified by implanted coded wire tags (CWT). Nitrogen isotopic and mass

shifts suggested that the initial protein pool within individual fish was replaced at different rates among cohorts. There

was a notable difference in carbon source dependency among hatcheries. Salmon from the hatchery closest to the Gulf

of Alaska had a 13C-depleted carbon signature consistent with Gulf carbon, whereas salmon from the other hatcheries

had Sound signatures. Differences in early marine feeding histories among 1994 hatchery-release-date cohorts recon-

structed from the stable isotope composition of fry bore no relationship to marine survival pattern. Varied survival rates

of 1994 Prince William Sound hatchery salmon were more likely related to the fry size at time of release, the observeddifferences in growth rate among release cohorts, and predation refuge effects of pen-rearing.

Résumé : Les masses d’azote et de carbone et la composition en isotopes stables varient considérablement d’une

cohorte à l’autre chez les saumons du Pacifique (Oncorhynchus spp.) provenant de piscicultures du détroit du Prince

William, Alaska, ce qui laisse croire qu’ils possèdent une gamme de patterns alimentaires différents au début de leur

vie en mer. Nous avons déterminé les masses d’azote et de carbone stables dans le corps entier, ainsi que la composi-

tion en isotopes stables, chez des cohortes choisies en fonction de la date de leur mise en eau et dont les individus

avaient été marqués par l’implantation de fils de fer codés par couleur. Les variations des isotopes et de la masse

d’azote indiquent que le pool initial d’azote est remplacé à des taux divers chez les poissons des différentes cohortes.

Il y a des différences appréciables entre les sources de carbone utilisées par les poissons des différentes piscicultures.

Les saumons provenant de la pisciculture la plus proche du golfe de l’Alaska ont une signature de carbone appauvrie

en 13C, ce qui correspond au carbone présent dans le golfe, alors que les saumons des autres piscicultures ont une

signature de carbone correspondant au carbone du détroit. Les variations de l’alimentation durant les premiers temps en

mer chez les cohortes de pisciculture de dates de libération différentes en 1994, telles que révélées par l’étude de lacomposition en isotopes stables des alevins, ne sont pas reliées aux patterns de survie en mer. Les taux variables de

survie des saumons provenant des piscicultures du détroit du Prince William en 1994 sont plus probablement reliés à la

taille des alevins au moment de leur libération, aux différences observées dans les taux de croissance chez les cohortes

libérées et aux effets de refuge dus à l’élevage en enclos.

[Traduit par la Rédaction] Kline and Willette 1638

Introduction

Approximately 500 million Pacific salmon (Oncorhynchusspp.) fry are released into the waters of Prince William Sound(PWS), Alaska, each year from five private nonprofit hatch-eries (Cooney 1993). These salmon initially feed withinPWS, then migrate into the Gulf of Alaska (GOA), returningto PWS as maturing fish one or more (depending upon thespecies) years later. Survivorship of maturing salmon return-ing to PWS hatcheries has declined in recent years. Presently,survival rates, which are based on comparing population size

at date of release with return, generally range between 3 and5% (Willette et al. 1999b). Survival of salmon from juvenileto adult stages is thought to be determined by mortality oc-curring during early marine life history (Parker 1968; Hartt1980; Bax 1983). Manipulating time of release by PWShatchery managers was explored as a means for increasingmarine survival rate (Willette et al. 1995, 1996). In 1994,pink salmon (Oncorhynchus gorbuscha, the numerically dom-inant Pacific salmon species in the study area) fry that werereleased in June at two PWS hatcheries, at a larger size, hadsurvival rates of 7 and 22% compared with 1% survival for

Can. J. Fish. Aquat. Sci. 59: 1626–1638 (2002) DOI: 10.1139/F02-126 © 2002 NRC Canada

1626

Received 29 March 2001. Accepted 17 July 2002. Published on the NRC Research Press Web site at http://cjfas.nrc.ca on11 October 2002.J16292

T.C. Kline, Jr. Prince William Sound Science Center, 300 Breakwater Ave., P.O. Box 705, Cordova, AK 99574, U.S.A.T.M. Willette. Alaska Department of Fish and Game, 43961 Kalifornsky Beach Road Suite B, Soldotna, AK 99835-7563, U.S.A.

1Corresponding author (e-mail: [email protected]).



those released during the conventional period of April toMay (Table 1).

Processes leading to fish mortality are frequently dicho-tomized into “bottom up” versus “top-down” control, whichin this case, is the relative importance of salmon forage ver-sus salmon-as-forage, respectively. The availability of zoo-plankton forage, especially Neocalanus copepods, is

important also because it may cause a shift in the behaviorof salmon predators, in addition to being important as salmonprey (Cooney et al. 2001; Willette et al. 2001). Neocalanusand other zooplankton from PWS were found to be distin-guishable by their stable carbon isotope ratio content fromthose from the adjacent GOA during 1994 (Kline 1999). Ju-venile salmon sampled off Vancouver Island appeared tohave fed on isotopically distinctive food sources (Perry et al.1996). We determined whether natural stable isotope abun-dance based trophic differences in early marine stage salmon,suggested by a pilot study (Kline 1996), were important formarine survival.

There is a predictable relationship between the isotopiccomposition of a consumer and that of its diet (reviewed by

Michener and Schell 1994). A secondary consumer’s isoto-pic signature reflects that of its diet, but with a consistent in-crease in the heavy isotopes 15N and 13C relative to diet(Vander Zanden and Rasmussen 2001). Isotopic compositionshifts occurring at low trophic levels can thus propagate tohigher trophic levels. A change in diet to one of differingisotopic composition can thus be measured in a secondaryconsumer like salmon. The approach taken here was to de-termine whether carbon or nitrogen isotopic compositionpatterns paralleled observed survival patterns for certainidentifiable (by tagging) hatchery-produced salmon cohortsfrom 1994. If it could be shown that isotopic and survivalpatterns were concordant, then it could be argued that preywas a factor affecting survival, since isotopic signatures de-

rive from diet.

Materials and methods

Study areaSalmon naturally migrate into PWS from adjacent natal

(mostly intertidal and short streams) and juvenile rearing(lakes and streams) habitats or are released into PWS fromhatcheries during April–May. This time period in PWS ismarked by energy-rich diatom and Neocalanus blooms, whichare food sources for juvenile salmon production (Cooney etal. 2001). Salmon then rear in PWS during the transitionfrom winter to summer conditions (Cooney et al. 2001). Ac-cordingly, seasonal transitioning, including a concomitantcomplex of oceanographic processes, in part due to the fjordand estuarine nature of PWS, alters the distribution of poten-tial food sources for salmon and salmon predators (Gay andVaughan 2001; Vaughan et al. 2001; Wang et al. 2001). Thisearly marine life-history phase when salmon are rearingwithin PWS, which is thought to be important for determin-ing year-class strength and has been the subject of recent in-tensive investigation (Cooney et al. 2001), was the focus of this study. Following PWS rearing, salmon emigrate to thegreater Gulf of Alaska, only returning to spawn as a matur-ing fish one or more years later (Cooney et al. 2001).

© 2002 NRC Canada

Kline and Willette 1627

H a t c h e r y r e

l e a s e s

I s o t o p e s

a m p l e - s p e c i f i c r e l e a s e s

S a l m o n

s p e c i e s

H a t c h e r y

R e l e a s e

p e r i o d

N u m b e r r e l e a s e d

( m i l l i o n s ) a

W e t m a s s

a t r e l e a s e a

S u r v

i v a l t o

a d u l

t ( % ) a

R e l a t i v e

s u r v i v a l

b

C o h o r t

c o d e

R e l e a s e d a t e s

W e t m a s s

a t r e l e a s e a

S u r v i v a l t o

a d u l t ( % ) a

C a p t u r e d a t e s c

N

P i n k

W H N

L a t e A p r i l

4 8 . 0

0 . 4

1 . 0

L o w

A

2 5 A p r i l

0 . 4

1 . 0

8

M a y t o 1 6 J u l y

4 8

P i n k

W H N

E a r l y M a y

1 5 4 . 7

0 . 4

0 . 4

L o w

B

7 M a y

0 . 4

0 . 2

8

M a y t o 1 0 J u l y

3 9

P i n k

W H N

E a r l y J u n e

7 . 7

1 . 4

2 2 . 1

H i g h

C

1 1 J u n e

1 . 4

2 2 . 3

2 6

J u n t o 1 2 J u l y

4 3

P i n k

A F K

E a r l y M a y

8 4 . 8

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0 . 4

L o w

D

1 0 a n d 1

7 M a y

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1 . 0

7

a n d 8 J u l y

6

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7

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4


1 5

N o t e : T h e s u r v i v a l r a t e o f c h u m s a l m

o n w a s n o t t r a c k e d . W H N , W . H . N o e r e n b e r g

h a t c h e r y ; A F K , A . F . K o e r n i g h a t c h e r y ; M B ,

M a i n B a y h a t c h e r y ; N D , n o t d e t e r m i n e d .

a D a t a f r o m W i l l e t t e e t a l . ( 1 9 9 6 ) , J o y

c e a n d R i f f e ( 1 9 9 5 ) , a n d p r o v i d e d b y t h e P r i n

c e W i l l i a m S o u n d A q u a c u l t u r e C o r p .

b A m o n g p i n k s a l m o n r e l e a s e s .

c D e t a i l e d l i s t i n g s s h o w i n g s a m p l e s i z

e f o r e a c h s p e c i e s , h a t c h e r y , r e l e a s e d a t e , a n d

c a p t u r e d a t e c o m b i n a t i o n a r e g i v e n i n T a b l e A 1 a m o n g p i n k s a l m o n r e l e a s e s .

T a b l e 1 . S u r v i v a l r a t e s a n d s a m p l i n g i n f o r m a t i o n o f s e l e c t P r i n c e W i l l i a m

S o u n d h a t c h e r y s a l m o n r e l e a s e c o h o r t s .



SamplingThe sampling of CWT-marked salmon by Willette et al.

(2001) enabled us to perform this study. Approximately onein every 600 salmon released from PWS hatcheries in 1994was labeled with a CWT indicating release date and hatch-ery of origin, thus enabling the selection of specific cohorts(Willette et al. 1999a). Fine-mesh purse seines were used to

sample juvenile salmon during their migration from westernPWS hatchery-release sites from early May throughmid-July 1994 (Willette et al. 1999a, 2001). Schools of fishwere targeted for seining after being located visually innear-shore nursery habitats. CWT fish were immediatelyidentified using a portable CWT detector. Samples werelogged into a database that included release cohort informa-tion for each fish. Samples were stored frozen (–20°C) orga-nized by capture date.

The CWT samples selected for this study were based onrelease cohorts that yielded samples over the May to Julysampling period, as well as samples analyzed in a pilot study(Table 1, Table A1; Kline 1996). Salmon selected for thisstudy originated primarily from the Wallace H. Noerenberg

(WHN) hatchery (Fig. 1) because the migration path of thesesalmon within PWS was known (Willette et al. 1999a,2001). Furthermore, their route along Knight Island Passagewithin PWS enabled multiple recapture of the individual re-lease cohorts over the spring to summer out-migration pe-riod (Fig. 1, Willette et al. 1999a; see Table A1 for samplingdates). However, sampling was destructive (fish caught wereremoved from the pool) and characterized by decreasingprobability of resampling over time owing to dispersion (aftera few days from release, frequently only one individual froma given cohort was found in a day of sampling, Table A1),which is a function of zooplankton density (Willette 2001).

This study focused on pink salmon because they dominateboth natural and artificial salmon production in PWS (Cooney

1993). A total of 1192 pink salmon fry with CWT were re-covered from the 1 199 348 individuals that were sampledfrom May to July 1994 (Willette et al. 1995). Marine sur-vival (total number returning as maturing fish minus numberof fry released) rates of pink salmon hatchery releases weredichotomized into high (>5% survival) or low (1% survival)relative survival from provided data (Table 1). To also pro-vide a comparison by species, a majority of the recoveredCWT chum salmon fry (Oncorhynchus keta; 93 CWT recov-ered, all from WHN hatchery) and sockeye salmon fry(Oncorhynchus nerka; 23 CWT recovered, all from MainBay (MB) hatchery; Fig. 1) were also analyzed. Data from apilot study (Kline 1996) that included pink salmon fry fromthe Armin F. Koernig (AFK) hatchery (Fig. 1) are included

here for comparison with pink salmon fry from the WHNhatchery.

Laboratory analysisCWT fry samples were stored frozen (–20°C) in their

sampling vials until they were selected for analysis. Selectedsamples were thawed, fork length was measured to nearest0.5 mm, and then samples were refrozen and freeze-dried.Freeze-dried weight was determined and then samples wereground to a fine powder with a dental amalgamator. Pilotstudy (Kline 1996) samples followed the same protocolomitting the length and weight measurements (these samples

are indicated in Table A1). Powdered samples were sent tothe University of Alaska Fairbanks Stable Isotope Facilityfor analysis. A mass spectrometric analysis generated thefollowing data: 13C/ 12C and 15N/ 14N ratios expressed in stan-dard delta units, δ

13C and δ15N, respectively; and %C and

%N. The delta notation used to express stable isotope ratiosis reported as the per mil (‰) deviation relative to an inter-national standard, air for nitrogen, and Vienna Pee Dee bel-emnite (VPDB) for carbon. By definition, the isotopestandards have delta values of zero, i.e., δ15N = 0‰ for at-mospheric N2. Mass spectrometric analysis quality assuranceprotocols consisted of running of laboratory standards beforeand after groups of five “unknowns” and duplicate analysesof each sample. Samples were run again when duplicateanalyses differed by more than 0.6‰.

Data analysisData used for analysis consisted of mean δ

13C, δ15N, andN and C mass, and C/N of the duplicate determinationsmade for each fish. The %C and %N data were used to cal-culate C/N atom ratios. Nitrogen and carbon mass was cal-culated by multiplying the freeze-dried weight by the %Nand %C, respectively. Stable carbon isotope ratios were nor-malized for lipid content following the methods of McConnaughey and McRoy (1979) and expressed as δ13C′

following Kline (1999).Release date was subtracted from capture date to calculate

“days since release” for use as an independent variable foreach fish. Data were computer fitted using Graphpad Prism3.0 (GraphPad Software, Inc., San Diego, Calif.) to simplemathematical models (Table A2) according to fit determinedby R2, and when appropriate, P value (significance level was0.05) and the ratio of predicted half-time (half-life or dou-bling time) confidence intervals (the smaller the ratio thebetter the fit).

Considering only mass-balance constraints, growth in Nand C mass was expected to “dilute” the original isotopic

© 2002 NRC Canada

1628 Can. J. Fish. Aquat. Sci. Vol. 59, 2002

Fig. 1. Map of the Prince William Sound study area showing

locations of salmon hatcheries and its geographic location within

Alaska, U.S.A. (insert).



composition in proportion to mass increase. For example, if a salmon with initial isotopic composition A grew on a dietthat resulted in isotopic composition B, the isotopic compo-sition would be halfway between A and B when the initialmass was doubled, i.e., the fish would consist of 50% initialmaterial and 50% new material. Once a fish increased inmass by an order of magnitude, the isotopic composition

would equal 10% initial material plus 90% new material.Accordingly, isotopic estimates were made for an initialδ

15N of 13.0 and a δ15N of 10.0 for a salmon virtually rid of

its initial N mass, i.e., 100% new material, as B, above. Thevariable initial condition was N mass. Starting mass valueswere 5, 7.5, 10, 15, and 20 mg N. The terminology “isotopedilution model” is used herewith to refer to the results of this predictable shift.

Salmon isotopic patterns were characterized and comparedqualitatively among high and low survival cohorts. Mean co-hort δ13C′ values were characterized as “high” or “low”, de-pending on whether they were greater than or less thanδ

13C′ = –22.0 after showing evidence of growth, i.e., havingturned over their initial natal or hatchery signature (Kline et

al. 1993). A cohort’s nitrogen isotope turnover was charac-terized as “rapid” when the regression line of δ15N vs. timecrossed δ

15N = 11.5 before 30 days, and “slow” when the co-hort crossed it 30 days after release and later. Similar isotopicpatterns would be conferred if all cohorts within a survivalcategory (low vs. high marine survival) had either slow orrapid nitrogen turnover or all had either high or low δ13C′.

Results

Following release into Prince William Sound from hatcher-ies, carbon and nitrogen mass increased exponentially (Fig. 2).Salmon released on later dates, between 30 May and 11 June(all chum and sockeye fry and June WHN pink fry), attained

~200 mg N and ~1000 mg C in 30–40 days compared with60–70 days for the April and May releases. An overall de-cline in C/N atom ratio with time suggested a difference inC and N mass turnover (Fig. 2c). The C/N ratios of WHNpink salmon fry released in April and May declined moreslowly than the chum salmon fry released from WHN fromlate May to June (Fig. 2c). Data points for June WHN pink and MB sockeye fry (Fig. 2c) occur near the WHN chum re-gression, whereas May AFK pink fry fell in with the Apriland May WHN regressions and June AFK pink fry fell inbetween conferring a speedier C/N decline for late spring re-leases.

Fry 13C content depended upon location (AFK is located~80 km south of the WHN hatchery), whereas 15N content

depended upon growth (change of the fry mass with time).From initial δ15N values of ~+13‰, 15N content declinedrapidly during the first two to three weeks following release,then appeared to become asymptotic at values ranging fromapproximately +10 (e.g., May WHN pink salmon) to about+11‰ (e.g., April WHN pink salmon; Fig. 3a). While therapid increase in mass was reflected by a concomitantchange in 15N composition, 13C composition remained ap-proximately constant (regression lines ranged up to ~1‰;Fig. 3b). Although C/N declined, the C/N-based lipid nor-malization (only normalized data are shown) changed pink,chum, and sockeye salmon δ13C′ values by just 0.4‰ (stan-

dard deviation, SD = 0.5), 0.5‰ (SD = 0.3), and 0.2‰ (SD= 0.2), respectively, compared with the raw data. The 13Ccomposition of early and late releases from a given hatcheryranged about 2‰. Nevertheless, there was a significant cor-relation for δ13C′ vs. time (Fig. 3b, Table A2). AFK salmonfry were 13C depleted by 3–4‰ compared with those fromthe other hatcheries (Fig. 3b).

Ontogenetic shifts in15

N content were suggested frommost x– y plots of δ15N and N mass (Fig. 4a). The very rapiddecline in δ15N (Fig. 3a) corresponded to when fry N masswas <~50 mg. Salmon fry appear to have reached a δ15Nminimum when N mass was between ~50 and 150 mg. MayWHN fry were 15N depleted by about 0.5‰ compared withApril and June releases when in the 15N-minimum sizerange. Fry >~150 mg N (corresponding to length >~90 mm)appear to have increased in 15N. Many of the larger fish, par-ticularly those with δ

15N values >~11.5‰, were sockeyesalmon.

Data aggregated into 10-day averages enabled simulta-neous elucidation of the effects of calendar date, number of days since release, and cohort, suggesting that N mass and

δ15N decreased more slowly for salmon released before day130 compared with those released later (Table 2). For exam-ple, April salmon exceeded 200 mg N and had δ15N values<11.0‰ after about two months compared with about onemonth for those released on day 150 and later.

The isotope dilution model results fitted a hyperbolic modelwith R2 > 0.99. The effect of increased starting mass on theisotope dilution model was to shift the curves upwardly(Fig. 4a). The May WHN pink cohort fitted well to the iso-tope dilution model, whereas the others did not. However,their asymptote was closer to 10.4, rather than 10.0 as usedin the model calculations.

Shift in δ15N values among cohorts was correlated to C/N

decline (Fig. 4b). When salmon fry approached asymptotic

δ15N values (Fig. 3a), C/N ratios were ~4.5 to 4.0 (Fig. 2c),suggesting that C/N could be used as an independent vari-able to ascertain turnover of initial material (Fig. 4b). Arange in asymptotic δ15N values can be seen in the right por-tion of Fig. 4b above the abscissa for the C/N range <4.5;the slopes for April and May WHN pink and sockeyesalmon were similar, ranging from ~1 to 1.3 (Fig. 4b, TableA2). The apparent lesser slope and lower R2 for chumsalmon may, in part, have reflected their lower initial C/N(cf. Fig. 2c).

The ratio C/N was used as an independent variable to dis-tinguish salmon that had turned over their natal C (Fig. 5).Species other than chum salmon with C/N <4.5 ranged inδ13C′ value from about –19.0 to –24.0 (Fig. 5). The δ13C′ di-chotomy of ~3‰ between AFK salmon and the others oc-curred at C/N values consistent with initial material turnover.Accordingly, only AFK salmon were categorized as having“low” δ

13C′ (Table 3).Qualitative assessment suggested that there were both

high and low δ13C′ and both rapid and slow δ15N turnoverrates within each survival category (Table 3). Of the highmarine survival cohorts (Table 1), only MB sockeye salmonhad sufficient data to ascertain slow turnover from the re-gression of δ15N with days since release, crossing the +11.5line at the 30-day mark. Because the δ

15N June WHN pink salmon was already +11 before 20 days, they must have

© 2002 NRC Canada




crossed +11.5 earlier, assuming they had starting δ15N values

similar to the other cohorts. Their turnover was thus catego-rized as rapid. Because the δ

15N values of June AFK pink

salmon were about +11.5 before 30 days, their turnover ratewas categorized as rapid. It is assumed that their startingδ

15N was similar to WHN salmon. April and May WHN

© 2002 NRC Canada


Fig. 2. (a) Coded wire tagged (CWT) fry nitrogen mass in relation to time, in days since release from hatcheries, for three W.H.

Norenberg (WHN) hatchery pink salmon (Oncorhynchus gorbuscha) release dates (25 April, 7 May, and 11 June 1994; indicated by

Apr WHN Pink, May WHN Pink, and June WHN Pink, respectively), WHN hatchery chum salmon (Oncorhynchus keta) released from

30 May to 3 June (indicated by WHN Chum), and Main Bay (MB) hatchery sockeye salmon (Oncorhynchus nerka) released from 28

to 31 May 1994 (indicated by MB Sockeye). (b) CWT salmon fry carbon mass in relation to time, in days since release from hatcher-

ies, for the same cohorts as shown in a. (c) CWT salmon fry C/N atom ratio in relation to time, in days since release from hatcheries,

for the same cohorts as shown in a with the addition of data for the A.F. Koernig (AFK) hatchery pink salmon releases of 10 and 17

May 1994, which are indicated in the legend as May AFK Pink, and the AFK pink salmon hatchery release of 13 June, which isindicated as June AFK Pink.



pink salmon had low marine survival; however, the formerhad slow δ15N turnover, since the regression crossed at30 days, whereas the latter had rapid turnover because theregression crossed before day 20. May AFK pink salmon, a

low marine survival cohort, were categorized as having slowδ15N turnover because their values were relatively high(+11.0 to 11.5) at 50 days from release, especially whencompared with May WHN pink salmon at 50 days.

Discussion

Isotopic shifts concomitant with salmon fry growthGiven a difference between the isotopic composition of

salmon diet in PWS and that of their natal or hatchery foodsource, rapidly growing fry were expected to shift their iso-topic composition in proportion to their increase in bodymass (Hesslein et al. 1993). This was the case for δ

15N; the

high 15N content natal-hatchery signature was replaced3–4 weeks after release (more quickly for earlier releases),suggesting that after ranging free for a month, their bodiesconsisted principally of protein acquired from feeding in the

natural environment. Our observations were similar to thosefor sockeye salmon fry feeding in a lake, which shifted froma parental-derived natal isotopic signature until they were~40–45 mm in length (Kline et al. 1993). In contrast to δ

15N,salmon fry from the WHN and MB hatcheries did notchange appreciably in 13C content because δ13C signaturesderived from the natal-hatchery period and those resultingfrom consuming potential food sources in PWS appear notto have differed appreciably.

The salmon fry δ15N shift of ~2.5‰ reflected incorpora-tion of 15N-depleted (relative to their natal-hatchery signa-ture) N mass during growth. A δ15N change model basedsolely upon dilution by N mass increase and given assumed

© 2002 NRC Canada


Fig. 3. (a) Coded wire tagged (CWT) salmon fry δ15N in relation to time, in days since release from hatcheries, for three W.H.

Norenberg (WHN) hatchery pink salmon (Oncorhynchus gorbuscha) release dates (25 April, 7 May, and 11 June 1994; indicated by

Apr WHN Pink, May WHN Pink, and June WHN Pink, respectively), WHN hatchery chum salmon (Oncorhynchus keta) released from

30 May to 3 June (indicated by WHN Chum in the legend), Main Bay (MB) hatchery sockeye salmon (Oncorhynchus nerka) released

from 28 to 31 May 1994 (indicated by MB Sockeye), A.F. Koernig (AFK) hatchery pink salmon releases of 10 and 17 May 1994,

which are indicated in the legend as May AFK Pink, and the AFK pink salmon hatchery release of 13 June, which is indicated in the

legend as June AFK Pink. The reference line is at δ15N = 11.5, which was used as the criterion to differentiate rapid and slow nitrogen

isotopic turnover. (b) Only a slight change of WHN and MB CWT salmon fry δ

13

C′ in relation to time, in days since release fromhatcheries, for the same cohorts as shown in a. AFK cohorts, however, were significantly 13C depleted, suggesting that the Gulf of

Alaska was the carbon source.



initial and assumed final isotopic values produced resultsthat were in the range of our observations when N mass wassmall (<~50 mg). Observed variability in the 15N dataamong the cohorts could thus, in part, be explained by dif-ferences in initial mass. Because the 15N content of PWSbiota is proportional to trophic level (e.g., Kline and Pauly1998), shifts to increased trophic level with size could ex-plain how larger salmon fry had elevated δ

15N values. Her-bivorous zooplankton species like the copepod Neocalanushad δ

15N values of ~+8.0‰ (Kline 1999). Omnivorous andcarnivorous zooplankton had correspondingly higher δ15Nvalues (Kline and Pauly 1998; Kline 1999). Based on trophic15N enrichment, salmon fry consuming only herbivores wereexpected to have δ

15N values of ~+11.4‰. This estimate,however, must be examined the context of the isotopic vari-ability of herbivores. For example, the Neocalanus δ

15N SDvalue from PWS is ~1.0 (Kline 2001b). Furthermore, PWSzooplankton δ15N values increased during early May of 1994

when phytoplankton exhausted the nutrient supply (Kline1999). The slower decrease in δ

15N of fry released in Aprilmay thus have reflected feeding on this more positive foodsource, i.e., a food source less different from their na-tal-hatchery signature than those released in May, sincethese latter fry fed when the δ15N values of production hadrebounded to less positive values. Nevertheless, May WHNfry attained their least positive δ15N values of +10.4‰ at~125 mg N on approximately day (of the year) 180 whenApril releases were larger, but slightly more positive(>200 mg and δ15N = +10.8‰).

Larger fry had δ15N values up to +12.5‰, suggesting ashift to a diet averaging approximately one third of a trophiclevel higher than that reflected by a δ15N value of +11.4‰(trophic level estimated using formula in Kline and Pauly1998). Salmon with >150 mg N may therefore have con-sumed a greater proportion of higher (than herbivore)trophic level prey than smaller fry. This conjecture is sup-

© 2002 NRC Canada


Fig. 4. (a) The relationship of coded wire tagged (CWT) salmon fry δ15N with N mass for three W.H. Norenberg (WHN) hatchery

pink salmon (Oncorhynchus gorbuscha) release dates (25 April, 7 May, and 11 June 1994; indicated by Apr WHN Pink, May WHN

Pink, and June WHN Pink, respectively), WHN hatchery chum salmon (Oncorhynchus keta) released from 30 May to 3 June (indicated

by WHN Chum in the legend), and Main Bay (MB) hatchery sockeye salmon ( Oncorhynchus nerka) released from 28 to 31 May 1994

(indicated by MB Sockeye). The thin lines indicate change in δ15N predicted by isotopic dilution model for initial N masses ranging

from 5 to 20 mg indicated by inset legend. (b) Linear (abscissa reversed so that data are approximately chronological, from left to

right, along each line) relationship of CWT salmon fry δ15N released from indicated PWS hatcheries in 1994 in relation to C/N, with

the addition of data for the A.F. Koernig (AFK) hatchery pink salmon releases of 10 and 17 May 1994, which are indicated in thelegend as May AFK Pink, and the AFK pink salmon hatchery release of 13 June, which is indicated as June AFK Pink.



ported by stomach content analyses made by M. Sturdevant

(given in appendix 4 of Oakey and Pauly 1998) of pink andchum salmon fry (size range not specified) during 1994 thatsuggest a diet consisting, in part, of a combination of carniv-orous and herbivorous zooplankton. Stomach contents forboth species also included fish, presumably larvae, in ap-proximately the same proportion as carnivorous and herbiv-orous zooplankton combined, when averaged over time. InMay, large calanoids and euphausiids (life stages not speci-fied) were the dominant constituents in pink salmon diets,whereas fish and large calanoids were the dominant constit-uents in chum salmon diets. Large calanoids were less im-portant in June and July for pink salmon, while smallcalanoids were more important. Gastropods (presumably thecommon pteropod Limacina) became the second most im-

portant diet component, after fish, for both pink and chumsalmon fry during July. Because zooplankton taxa other thanthe large calanoid copepod Neocalanus had higher δ15N, andtherefore had a higher trophic level compared to Neocalanus(Kline and Pauly 1998; Kline 1999), the reduced proportionof large calanoids in the stomach content analysis could ex-plain the δ15N increases measured in salmon during July.

Carbon isotopic compositionIt was possible to assess dietary information from salmon

fry 13C content for those fry with C derived from the open(nonnatal nonhatchery) environment because of C and Nmass increases, direct evidence of turnover from δ15N data,and the C/N decline from ~6 to ~4.0–4.5, which took placeduring early marine feeding. Furthermore, the C/N declinesuggested that the natal-hatchery C pool was lost more rap-idly than N. The declining C/N of hatchery-produced salmonfrom time of release also suggested a concomitant decreasein lipid content and therefore whole-body energetic content(McConnaughey and McRoy 1979). This conjecture, whichdepends upon the relationship between C/N and fishwhole-body energetic content (Paul et al. 2001), was sup-ported by the observation of Paul and Willette (1997) thatwhole-body energetic content of hatchery pink salmon sam-pled near the WHN hatchery was lower at the end of Maycompared to early May, while body length increased.

The distinctive δ13C′ values of AFK salmon compared with

those from the more northern hatcheries in PWS reflectedfeeding on a separate, 13C-depleted food source. Such a dif-ference in food source can be taxonomically independent be-cause a single copepod species, Neocalanus cristatus, in thestudy area exhibited the same δ13C′ range as observed herefor salmon fry (Kline 1999). The species composition of dietcan thus be invariant, e.g., 100% Neocalanus, when at thesame time the isotopic composition of diet can be highlyvariable. Therefore, isotopically based diets must be referredto in nontaxonomic terms like food sources. Organic carbon(food sources) originating in the GOA in 1994–1995 wascharacterized as 13C depleted compared to food sources orig-inating within PWS (Kline 1999). The proximity (~15 km)of the AFK hatchery to the GOA (Fig. 1), and the direct

connection to it via one passage is consistent with the notionthat AFK hatchery fry primarily consumed Gulf carbon. Incontrast, the other hatcheries are >50 km from the Gulf andconnect to it via several passages.

Isotopic patterns versus survivalA far greater proportion of the pink salmon released in

June 1994 from both the AFK and WHN hatcheries survivedto maturity than did earlier 1994 releases. Did early marinefeeding history differences detected with stable isotopes con-fer any survival advantage? Large differences in food sourcewere apparent from δ13C′ values that, however, appeared tohave a hatchery-derived geographic dependency that was notrelated to survival, since salmon from the AFK and WHNhatcheries consisted of releases with both high and low sur-vival. The dependency on PWS vs. GOA carbon during earlymarine feeding appeared to confer no survival advantage to1994 salmon fry because such a dependency difference wasnot observed within a hatchery where survival differencesoccurred.

Salmon that were released from hatcheries from the endof May (~day 150) and later were larger, either from fastergrowth (in terms of change in either C or N mass) or frombeing released at a larger size, than those released earlier.The fry released at a large size in June exhibited muchhigher survival rates. These differences could have resulted

© 2002 NRC Canada


Days since release from hatchery

Release cohort

(day of year,

species) 1–10 11–20 21–30 31–40 41–50 51–60 61–82

Day 115, pink salmonmg N 27.8 18.7 (11.2) 4 77.9 (18.0) 14 236.5 (102.5) 8

δ15N 12.5 12.5 (0.4) 22 11.1 (0.4) 14 10.8 (0.3) 11

Day 127, pink salmon

mg N 6.0 (2.5) 6 15.6 (4.0) 8 29.6 (2.8) 5 127.8 (33.2) 18 175.8

δ15N 12.8 (0.6) 5 11.5 (0.2) 5 11.0 (0.2) 5 10.4 (0.2) 19 10.6

Days 150 and 154, chum salmon

mg N 20.1 (6.8) 47 39.8 227.5 (45.6) 3 321.7 (54.1) 8

δ15N 12.5 (0.3) 47 11.8 10.8 (0.3) 3 11.2 (0.3) 8

Day 162, pink salmon

mg N 96.5 (38.0) 26 166.8 (63.1) 11 227.0 (63.0) 5

δ15N 10.9 (0.2) 27 10.9 (0.2) 11 10.9 (0.2) 5

Table 2. Mean N mass and isotopic ratio for 1994 salmon fry in relation to release date (cohort) and time since release with standard

deviation (in parentheses) and N (when N > 1).



because (i) the larger fry were less vulnerable to predationdue to their size, or (ii) the large fry group was being held innet pens while the earlier release groups were subjected to aperiod of high predation losses. Willette et al. (1999b) foundno significant differences in the mean wet weight, length,and condition factor between the early and large late releasegroups when they were mixed together in late June. There-fore, the second alternative was more likely the cause of thedifferent survival rates between the two groups.

The effects of temperature and prey density on growth werepossible factors determining salmon fry mortality (Willetteet al. 1999b). Water temperature may have been an impor-tant factor affecting material turnover, since seasonal warm-ing of the water column (Cooney et al. 2001) acceleratedgrowth and protein turnover rates in later-released fry.Warming water temperatures may also explain the acceler-ated C/N change of late May and June releases. The morerapid C/N ratio decline of later releases suggested an accel-erated consumption of initial lipid stores (assuming C/N as alipid proxy; McConnaughey and McRoy 1979) that wasprobably due to greater metabolic demand from seasonalwarming and that should have been an additional factor af-

fecting these fish. From their N mass change, protein turn-over was also suggested to be very rapid. These observationsimply that foraging rates for the later releases were greaterthan for earlier releases, but this is is a contraindication of ahypothetical inverse relationship between foraging stress andsurvival rate (Cooney 1993).

Year-to-year differences in zooplankton density, particu-larly if they are due to variation in the GOA carbon subsidylike those evidenced here for AFK fry, could be suggestedby isotopic analysis of fishes such as salmon fry or theirpredators (Kline 2001a). Willette et al. (1999b) described re-

sults from a statistical model that predicted survival to adultfrom size, number, and timing of hatchery salmon releasesand subsequent duration of the macrozooplankton bloom.Recent modeling studies indicate that year-to-year variabilityin PWS pelagic productivity patterns may reflect weatherconditions occurring during the spring phytoplankton bloomperiod (Eslinger et al. 2001). Productivity-affected salmongrowth rates would, in turn, affect vulnerability to predation,because slower-growing fish are susceptible to predation fora longer time (Parker 1971; West and Larkin 1987).

It may be possible to elucidate pelagic productivity pat-terns, including long-term change, from stable isotope data.For example, Schell (2001) conjectured from systematic de-crease in both δ13C and δ15N content of bowhead whale ba-leen that primary productivity in the Bering Sea has declinedover multidecadal time periods. It is thus tempting to specu-late that the carbon isotope differences ascribed to GOA andPWS carbon observed in juvenile salmon may also reflectdifferences in primary productivity within the region. Thisspeculation is supported by productivity modeling that sug-gested greater zooplankton productivity during cold andstormy spring conditions than warm and calm springs(Eslinger et al. 2001). Eslinger et al. (2001) suggested thatthe latter pattern leads to a rapid but short-lived PWS phyto-plankton blooms, increasing contributions to the benthosbecause the phytoplankton cannot be fully utilized by the zoo-

© 2002 NRC Canada


Fig. 5. δ13C′ in relation to C/N ratio for three W.H. Norenberg (WHN) hatchery pink salmon ( Oncorhynchus gorbuscha) release dates

(25 April, 7 May, and 11 June 1994; indicated by Apr WHN Pink, May WHN Pink, and June WHN Pink, respectively), WHN hatch-

ery chum salmon (Oncorhynchus keta) released from 30 May to 3 June (indicated by WHN Chum), Main Bay (MB) hatchery sockeye

salmon (Oncorhynchus nerka) released from 28 to 31 May 1994 (indicated by MB Sockeye), A.F. Koernig (AFK) hatchery pink

salmon releases of 10 and 17 May 1994, which are indicated in the legend as May AFK Pink, and the AFK pink salmon hatchery re-

lease of 13 June, which is indicated in the legend as June AFK Pink.

Cohort code

from Table 1

Relative N

isotope turnover

Relative C isotope

signature

High survival

C Rapid High

E Rapid Low

F Slow High

Low survival

A Slow High

B Rapid HighD Slow Low

Table 3. Qualitative assessment of high- and low-mortality co-

horts to isotopic pattern.



plankton. Fast algal growth rate and concomitant [CO2]aq andnutrient depletion occurring during warm springs is a nonex-clusive cause for increased phytoplankton δ13C values (e.g.,Cullen et al. 2001). These higher δ13C values when propa-gated up the food chain may thus be an indicator of this typeof phytoplankton bloom. The higher δ

13C values found inPWS may therefore reflect the greater water stability charac-

teristic of this type of bloom and of PWS relative to GOA(Vaughan et al. 2001). Consequently, the WHN salmon mayhave been more dependent on zooplankton that had fed onphytoplankton that had undergone more rapid growth thanthose from AFK, thus reflecting a bottom-up effect (i.e., aphysics–nutrient–phytoplankton interaction effect propagatedto the fish). Nonetheless, this difference between the hatcher-ies was not manifested by a parallel difference in survival.

Simulation models suggested that survival rate patternscould be explained by differences in effects of predationamong release cohorts (Willette et al. 2001). If predation onsalmon fry was the principal factor controlling marine sur-vival, isotopically evidenced differences in food source andtrophic shifts occurring in 1994 appeared not to predispose

fry to this loss. Alternative hypotheses therefore need to beconsidered. For example, the later releases may have beenless vulnerable to predation because of predator behavior(e.g., prey-switching; Willette et al. 1999a). Such differencesin vulnerability would not be reflected by fry isotopic signa-ture. Thus, the highly variable survival rates of 1994 PWShatchery salmon were more likely due to causes other thanthose that can be inferred from differences in observed iso-tope abundance.

Other applicationsThe turnover of a natal or hatchery isotopic signature is

important for interpretation of field data (Kline et al. 1993).For example, Perry et al. (1996) conjectured that the ob-

served variability in stable isotope abundance among frysampled near Vancouver Island reflected isotopic differencesin diet of hatchery and wild (nonhatchery) salmon. Thisstudy suggested protocols for selecting fry so that a data setwill reflect only postnatal or posthatchery feeding based onN mass gain or C/N decline. The empirical criteria foundhere may be useful in another setting until local criteria canbe established. In this study, fry with C/N < 4.5 and N mass> ~50 mg reflected postnatal or hatchery feeding. Salmonfry selected on these criteria exhibited a range in pelagic or-ganic carbon source dependency based on 13C content. Al-though these criteria could be applied to other studies,caution should be used because temperature appeared to bean important factor in regulating turnover in PWS. The vari-ability in turnover rate in PWS suggested that time per se(e.g., a specified period since release) may not be an effec-tive criterion for selecting fish not containing significantproportions of previously acquired material.

Elucidation of material turnover from initial (isotopic andmass) values, which was aided by knowing capture and re-lease dates of individual hatchery salmon that were sampledafter free-ranging for up to three months, would not havebeen possible without CWTs and a large sampling effort.CWTs are being supplanted by otolith thermal marking(OTM) technology. OTM technology makes it possible todetermine very effectively which salmon in a sample from

PWS (and other locations where the technology is applied)are from hatcheries, and from an absence of markings, whichare from natural propagation. Whereas OTM technology en-ables the mass marking of virtually all of a hatchery’s pro-duction (all PWS hatchery salmon are presently being OTMmarked), there will be a trade-off, since OTM fish may notbe marked specifically for a date of release.

In summary, we have shown that salmon fry exhibited avariety of early marine feeding histories based on their hav-ing a large range in both carbon and nitrogen stable isotopeabundance. These patterns of isotopic variability could notbe related directly to marine survival rates. Additionally, ourdata provided direct evidence for rapid turnover of materialin early stage juvenile fishes through a noncaptive feeding ex-periment complementing previous captive studies (Hesslein etal. 1993).

Acknowledgments

The research described in this paper was funded by the

Exxon Valdez Oil Spill Trustee Council. The findings pre-sented by the authors are their own and not necessarily theTrustee Council’s position. We were assisted by a large crewfrom the Alaska Department of Fish and Game that collectedfish specimens. M. Powell and K. Antonucci facilitated theretrieval of archived salmon samples. K. Antonucci preparedsamples for mass spectrometry. Bruce Barnett at the Univer-sity of Alaska Fairbanks Stable Isotope Facility performedthe stable isotope analysis. V. Patrick provided suggestionsfor the data analysis. Tim Joyce of the Alaska Department of Fish and Game provided hatchery data. S. Baumann pre-pared the map shown in Fig. 1. This paper benefitted fromsuggestions made by Ole A. Mathisen, three anonymous re-viewers, and an anonymous associate editor.

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Appendix A

© 2002 NRC Canada


Hatchery Salmon species Release date Capture date Days since release N total N pilot study

WHN Pink 25 April 8 May 13 22 5

WHN Pink 25 April 9 May 14 1WHN Pink 25 April 8 June 44 1

WHN Pink 25 April 9 June 45 2








WHN Pink 25 April 1 July 67 1

WHN Pink 25 April 10 Jul 76 1



WHN Pink 7 May 8 May 1 4 1

WHN Pink 7 May 11 May 4 2 2

WHN Pink 7 May 25 May 18 8

WHN Pink 7 May 2 June 26 5




WHN Pink 7 May 10 July 64 1

AFK Pink 10 May 7 July 58 1 1




MB Sockeye 28 May 24 June 27 1

MB Sockeye 28 May 25 June 28 1MB Sockeye 28 May 26 June 29 3

MB Sockeye 28 May 1 July 34 1





WHN Chum 30 May 4 June 5 4



WHN Chum 30 May 14 July 45 1




MB Sockeye 30 May 12 July 43 1MB Sockeye 31 May 4 June 4 1


WHN Chum 3 June 4 June 1 23

WHN Chum 3 June 5 June 2 16

WHN Chum 3 June 11 July 38 1





WHN Pink 11 June 25 June 14 1


Table A1. Sample inventory, ordered by hatchery release date, indicating total number ( N ) of samples from each release–capture date

combination for each species and hatchery; same information from pilot study in right-most column.




Hatchery Salmon species Release date Capture date Days since release N total N pilot study





WHN Pink 11 June 1 July 20 1WHN Pink 11 June 10 July 29 6

WHN Pink 11 June 11 July 30 5

WHN Pink 11 June 12 July 31 5

AFK Pink 13 June 7 July 24 21 21

AFK Pink 13 June 8 July 25 20 20

Note: Hatchery abbreviations are as follows: WHN, W.H. Norenberg; MB, Main Bay; AFK, A.F. Koernig. Dates are from 1994.

Table A1 (concluded ).

Fig.

No. Cohort Model

Independent

variable A B C R2 T2 CI ratio

2a April WHN pink N (mg) = AeB(d ) d 10.76 0.043 0.83 16.3 1.6

2a May WHN pink N (mg) = AeB(d ) d 10.50 0.048 0.86 14.5 1.6

2a June WHN pink N (mg) = AeB(d ) d 37.18 0.054 0.47 12.8 2.12a WHN chum N (mg) = AeB(d ) d 19.74 0.063 0.96 11.0 1.2

2a MB sockeye N (mg) = AeB(d ) d 318 0.014 0.20 49.6 undefined

2b April WHN pink C (mg) = AeB(d ) d 42.85 0.041 0.81 17.1 1.6

2b May WHN pink C (mg) = AeB(d ) d 42.89 0.044 0.85 15.7 1.6

2b June WHN pink C (mg) = AeB(d ) d 127.8 0.054 0.46 12.9 2.1

2b WHN chum C (mg) = AeB(d ) d 74.54 0.060 0.96 11.5 1.2

2b MB sockeye C (mg) = AeB(d ) d 1126 0.014 0.18 51.3 undefined

2c April WHN pink C/N (atom ratio) = AeB(d ) + 4 d 2.27 0.057 0.88 12.2 1.9

2c May WHN pink C/N (atom ratio) = AeB(d ) + 4 d 1.26 0.029 0.25 23.7 9.8

2c June WHN pink C/N (atom ratio) = AeB(d ) + 4 d 6.31E+31 5.438 0.06 0.1 1.1

2c Chum WHN C/N (a tom r atio) = AeB(d ) + 4 d 0.80 0.083 0.40 3.9 26.6

2c S oc keye MB C/N (a tom r atio) = AeB(d ) + 4 d 1.76 0.353 0.79 4.2 undefined

3a April WHN pink δ15N = AeB(d ) + C d 3.348 0.473 10.7 0.79 14.7 73.6

3a May WHN pink δ15N = AeB(d ) + C d 2.99 0.040 10.1 0.86 17.2 2.7

3a June WHN pink δ15N = AeB(d ) + C d –72.05 6.10E-06 82.9 0.00 113561 undefined3a WHN chum δ

15N = AeB(d ) + C d 1.669 0.069 11.1 0.76 10.0 6.3

3a MB sockeye δ15N = AeB(d ) + C d 2.195 0.055 11.4 0.55 12.6 undefined

3b April WHN pink δ13C′ = –A(d ) – B d 0.009 19.38 0.18

3b May WHN pink δ13C′ = –A(d ) – B d 0.027 19.28 0.48

3b June WHN pink δ13C′ = –A(d ) – B d 0.038 21.2 0.43

3b WHN chum δ13C′ = –A(d ) – B d 0.016 19.31 0.12

3b MB sockeye δ13C′ = –A(d ) – B d 0.025 18.66 0.31

4a April WHN pink δ15N = A × M/(B + M) M 0.1412 0.095 0.20

4a May WHN pink δ15N = A × M/(B + M) M 0.05961 0.066 0.90

4a June WHN pink δ15N = A × M/(B + M) M 0.07961 0.702 0.03

4a WHN chum δ15N = A × M/(B + M) M 0.1223 0.183 0.39

4a MB sockeye δ15N = A × M/(B + M) M 0.1947 5.127 0.35

4b April WHN pink δ15N = A + B(C/N) C/N 5.50 1.350 0.71

4b May WHN pink δ15N = A + B(C/N) C/N 6.49 0.998 0.63

4b June WHN pink δ15N = A + B(C/N) C/N 9.84 0.263 0.014b WHN chum δ

15N = A + B(C/N) C/N 9.10 0.703 0.23

4b MB sockeye δ15N = A + B(C/N) C/N 6.76 1.259 0.40

5 April WHN pink δ13C′ = –A + B(C/N) C/N 21.08 0.301 0.11

5 May WHN pink δ13C′ = –A + B(C/N) C/N 23.77 0.7748 0.49

5 June WHN pink δ13C′ = –A + B(C/N) C/N 16.41 –0.9927 0.02

5 WHN chum δ13C′ = –A + B(C/N) C/N 18.24 –0.2738 0.70

5 MB sockeye δ13C′ = –A + B(C/N) C/N 24.96 1.352 0.32

Note: Relative goodness-of-fit for nonlinear models is indicated by bold for high correlation coefficient while having a half-time (T2) confidenceinterval ratio (CI ratio) <7. Significant (P < 0.05) linear models indicated by bold. Hatchery abbreviations: WHN, W.H. Norenberg; MB, Main Bay; AFK,A.F. Koernig. d , days since release; M, mass of nitrogen in milligrams; C/N, atom ratio. The models come out of the data—via computer fit, they werenot a priori.

Table A2. Regression parameters for Figs. 2 to 5.

Pacific salmon (Oncorhynchus spp.) early marine feeding patterns based on 15N/14N and 13C/12C in...

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