Food restriction prior to release reducesprecocious maturity and improves migrationtendency of Atlantic salmon (Salmo salar) smolts

Anssi Vainikka, Riina Huusko, Pekka Hyvärinen, Pekka K. Korhonen,Tapio Laaksonen, Juha Koskela, Jouni Vielma, Heikki Hirvonen,and Matti Salminen

Abstract: Since food availability is known to affect both the precocious maturation and start of feeding migration in wildjuvenile salmonids, we examined if a reduction in otherwise plentiful feeding in hatcheries could improve migrationtendency and the subsequent survival of released Atlantic salmon (Salmo salar) smolts. A reduction in diet lipid contentand feed ration (FR) the previous spring and in FR in the winter prior to release proved efficient; spring-diet treatmenthalved the proportion of mature males in the autumn prior to release, and a reduction in FR in the winter prior to releasedecreased latency before leaving the stocking site. In addition, a reduction in FR in winter affected the onset of migration,improved migration speed, and defined the direction of migration downstream in controlled experiments. However, dietmanipulations neither affected the swimming endurance nor improved the generally poor tag recapture rates. We concludethat reduced FR at specific times could be used to reduce both precocious male maturity and improve the migrationtendency of released salmon.

Résumé : Il est établi que la disponibilité alimentaire a une incidence tant sur la maturation précoce que sur le début de lamigration trophique des salmonidés juvéniles sauvages. Nous avons donc tenté de déterminer si une réduction del’alimentation, normalement abondante, dans les alevinières pouvait améliorer la tendance a la migration et la surviesubséquente de saumoneaux de saumon atlantique (Salmo salar) libérés. Une réduction du contenu lipidique du régimeainsi que de la ration (FR) au printemps précédant la libération et une réduction de la FR a l’hiver précédant la libérationse sont avérées efficaces; le traitement printanier a réduit de moitié la proportion de mâles matures a l’automne précédantla libération et la réduction de la FR a l’hiver précédant la libération a réduit le temps de latence avant le départ du sited’empoissonnement. En outre, une réduction de la FR en hiver a influencé le début de la migration, amélioré la vitesse demigration et défini la direction de migration vers l’aval dans le cadre d’essais contrôlés. La manipulation du régimealimentaire n’a toutefois pas eu d’effet sur l’endurance a la nage, ni n’a amélioré les taux généralement faibles de recaptured’individus étiquetés. Nous en concluons que la réduction de la FR a des moments précis pourrait être utilisée pour réduirela maturité précoce des mâles et améliorer la tendance a migrer de saumons libérés.

[Traduit par la Rédaction]

Introduction

Diadromous migration characterizes many salmonids: theystart life in freshwater, migrate to the sea to feed and grow, andreturn to fresh water to spawn (reviewed by McCormick et al.1998; Klemetsen et al. 2003). Fish migration patterns areevolutionarily driven by the differential risk of predation andthe availability of food in alternative, seasonally or ontogenet-ically changing, often oceanic or lacustrine and riverine hab-

itats (Gross et al. 1988; Brönmark et al. 2008). Apart frommost Pacific salmon, salmonids such as Atlantic salmon(Salmo salar) and brown trout (Salmo trutta) can mature inrivers (e.g., Jonsson and Jonsson 1993; Marschall et al. 1998)and adopt an alternative or partial resident life-history strategydepending on food availability and conspecific density(Thorpe et al. 1998; Olsson et al. 2006). In Atlantic salmon,environmental variation is discernible in large individual- andpopulation-level variation in the timing of the downstream

Received 20 January 2012. Accepted 12 September 2012. Published at www.nrcresearchpress.com/cjfas on 19 November 2012.J2012-0025

Paper handled by Associate Editor James Grant.

A. Vainikka, P. Hyvärinen, P.K. Korhonen, and T. Laaksonen. Finnish Game and Fisheries Research Institute, Manamasalontie 90,FI-88300, Paltamo, Finland.R. Huusko. Finnish Game and Fisheries Research Institute, University of Oulu, P.O. Box 413, FI-90014, Oulu, Finland.J. Koskela and J. Vielma. Finnish Game and Fisheries Research Institute, Survontie 9, FI-40500 Jyväskylä, Technopolis, Finland.H. Hirvonen. Department of Biosciences, P.O. Box 65, FI-00014 University of Helsinki, Finland.M. Salminen. Finnish Game and Fisheries Research Institute, P.O. Box 2, FI-00791 Helsinki, Finland.

Corresponding author: Anssi Vainikka (e-mail: anssi.vainikka@uef.fi).

1981

Can. J. Fish. Aquat. Sci. 69: 1981–1993 (2012) Published by NRC Research Pressdoi:10.1139/f2012-119

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migration and in fish age and size at first spawning (Metcalfeand Thorpe 1990).

Both the onset of smoltification and precocious maturationin males can be influenced by the availability of food atspecific times during parr development (e.g., Rowe et al. 1991;Wysujack et al. 2009; Lans et al. 2011). For example, bimodalsize distribution typical to both wild and aquaculture environ-ments at the end of the first year of the salmon life cyclemanifests as distinct smoltification ages (Thorpe et al. 1980).Fast growth also promotes precocious maturity in severalsalmonids, but the timing of the onset of maturation andsmoltification differs (e.g., Thorpe 1994a, 1994b; Forseth etal. 1999). While the exact onset time of smolt developmentappears unclear, hormonal changes leading to smoltificationcan typically be observed in early February (Dickhoff et al.1997). It is also known that the hormonal onset of maturationin the spring inhibits simultaneous but not subsequent smolti-fication in Atlantic salmon (Shrimpton and McCormick 2002).Therefore, the manipulation of food availability at specifictimes could be used to control the occurrence of smoltificationand precocious maturation.

Since the damming of natal salmon rivers for the production ofelectricity, power companies have been required to compensatefor the loss of natural reproduction by annually releasing largenumbers of hatchery-reared smolts (currently about 5 million) tobe ranched in the Baltic Sea. However, sea-ranching of hatchery-reared fish is increasingly challenged by poor and decliningsmolt-to-adult return rates (e.g., McKinnell and Karlström 1999;Kallio-Nyberg et al. 2011a, 2011b). Poor stocking results alsothreaten the success of currently implemented reintroductionprograms in rivers that are being opened for spawning migra-tion by the construction of fish ladders. In particular, hatchery-reared smolts might be slower to start feeding migration andconsequently (Kekäläinen et al. 2008; Johnson et al. 2010)suffer from higher mortality than wild smolts (Chittenden et al.2008; Lacroix 2008; Romakkaniemi 2008). The decliningreturn rates of stocked smolts oppose trends in the size, con-dition, and lipid content of stocked smolts (Vainikka et al.2010; Larsson et al. 2012) but are collinear with abundancetrends of Atlantic salmon throughout the whole northern At-lantic (Parrish et al. 1998; Klemetsen et al. 2003; Huusko andHyvärinen 2012).

Because the adoption of a migratory life-history strategycan depend on individual condition and growth rate in fish(e.g., Berglund 1995; Hutchings and Jones 1998; Brodersen etal. 2008), there is a reason to suspect that continuously devel-oping hatchery rearing methods aiming to produce largesmolts in minimal time could have negative impacts on themigration tendency of released smolts (Lans et al. 2011;Larsson et al. 2012). In particular, changes in fish feeds couldcontribute to the large-scale decline observed in stockingsuccess, since hatcheries around the Baltic Sea are likely to usethe same or similar commercial fish feeds. The development ofcommercial fish feeds for the aquaculture industry has beendriven by the needs of fish production for human consumption,and separate fish feeds rarely exist for smolts produced spe-cifically for stocking purposes (e.g., Bjerkeng et al. 1997;Tacon and Metian 2008).

Our aim in this study was to examine at a realistic produc-tion scale whether a reduction in feed ration and diet lipidcontent (collectively called feed restriction) in spring (1 year

before release), reduction in feed ration in the winter prior tostocking, or both treatments together would (i) reduce preco-cious male maturity and (ii) improve smolt migration ten-dency, assessed both experimentally (a) in artificial circularstreams and (b) in a realistic release situation, and finally(iii) improve the survival of stocked Atlantic salmon in com-parison with standard hatchery raising. To understand mech-anisms of potential changes in migration behaviour andmaturation, we monitored the mortality, growth, condition, fatcontent, visual smoltification status, and condition of pectoraland dorsal fins of fish during hatchery rearing. According toprevious research, we predicted that springtime feed restrictionwould reduce precocious male maturity in the autumn beforestocking (Thorpe 1994a; Berglund 1995; Rowe et al. 1991)and that a reduction in feed ration in winter would improve thesmoltification process and migration tendency of the salmonsmolts (Lans et al. 2011; Larsson et al. 2012). The combinedtreatment was predicted to induce both of the desired effects.Feed restriction was predicted to induce an earlier start ofmigration both in the migration experiments and in the actualrelease situation, as well as higher migration speed in themigration experiments compared with control fish with lowmigration tendency.

Materials and methods

FishThe fish used in this study were the artificially bred off-

spring of River Oulujoki salmon brood stock, maintained bythe Taivalkoski unit of the Finnish Game and Fisheries Re-search Institute (FGFRI). The eyed eggs (N � 72 000) weretransported to the Kainuu Fisheries Research unit of FGFRI(64°29=N, 27°30=E) on 22 March 2007. After �30% initialmortality, the fingerlings (N � 20 320) were raised usingstandard methods (Det Norske Veritas Quality system certif-icate No. 2000-HEL-AQ-833, SFS-EN ISO 9001) and com-mercially available fish feeds (Nutra ST and Nutra PARR 1.5by Skretting, Norway) in four 3.2 m2 glass fibre tanks (4400–5737 individuals·tank–1) until 24 April 2008. At the beginningof the experiment (Table 1), the fish were randomly dividedinto 16 indoor glass fibre tanks (3.2 m2) so that in each tankthere were 1020 nonmarked fish and 250 fish marked bypassive integrated transponder (PIT; Allflex 11 mm full duplexpit tag, TX705-FDX-B; density in total: 397 fish·m–2). Thetagged fish were randomly chosen, but only fish of 65 mmin total length or longer could be tagged (a maximum 5% offish were smaller than 65 mm). At the event of marking(7 May – 14 May 2008), the fish were anaesthetized usingMS-222 (tricaine methanesulfonate). After marking, thefish were bathed in chloramine (7.3 g·m–3) for 20 min toprevent infection.

The fish were raised in four replicates per diet group inindoor tanks until 30 June 2008, the date of the termination ofthe spring diet treatments, when the fish were transferred to 16uncovered outdoor concrete ponds of 50.0 m2 (water flow�3–5 L·s–1) in their original groups (still four replicates pertreatment) and held in a density 25 fish·m–2 until release. Allthe animal experimentation in this study was performed ac-cording to Finnish legislation and under licence ESLH-2008-04178/Ym-23.

1982 Can. J. Fish. Aquat. Sci. Vol. 69, 2012

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Diet groupsFour different diets were used. The applied diets were

combinations of changes in feed lipid content and feedration. Manipulation of feed lipid content was made possi-ble by obtaining identical feeds (Raisio Feed Ltd., Finland,according to the license holder Skretting) without post-extrusion fish oil and with normal postextrusion fish oil.Lipid-reduced feed was prepared by performing the post-extrusion of crude, fish-oil-free feed with a specific amountof fish oil at Laukaa unit of FGFRI. Several pellet sizes andfeed names (Nutra PARR, Royal Response) were usedduring the experiment in accordance with regular farmingpractices.

The control (standard) diet (CD) consisted of a regular commer-cial diet fed at the standard feed ration used by FGFRI (see above).The spring diet (SD) involved feed composition and feed rationmanipulation during 16 May 2008 – 30 June 2008 (45 days). Duringthis period, the crude lipid content of the air-dried 1.7 mm feedscrumble was reduced to 14.5% (crude protein 54.4%) in compari-son with 27.7% of the commercial feed (crude protein 46.7%). Thefeed ration was reduced to 50% and the realized total feed deliveryby 53.3% of the CD by feeding the fish every other day. The SD didnot differ from the CD from 30 June 2008. The winter diet (WD)was applied during 30 October 2008 – 31 May 2009 (7 months).During this period, the fish were only fed once a week, reducing totalfood availability by 85% and realized total feed delivery by 59.1%.The feed itself was unaltered commercial fish feed with a crude fatcontent of 24%. In the combined spring and winter diet (SWD)group, both of the abovementioned diets were used. Therefore,standard feeding in this group only occurred during the period 1 July2008 – 29 October 2008.

The feed ration reduction was implemented by decreasingthe frequency of feeding days, as this was assumed to ensurea more equal feed division among individuals than a daily

reduction in feeding rate (Pirhonen and Forsman 1998). Dur-ing the feeding days, the feed was delivered in multiple shortpulses by automatic feeders according to a computer-drivensystem taking into account the day length, water temperature,oxygen level, and the biomass of fish in individual ponds. Thesize heterogeneity of individual fish was taken into accountusing a mixture of several pellet sizes for all treatments: a1:2:1 mixture of pellet sizes 1.2, 1.5, and 1.7 mm was usedduring 9 July – 18 August 2008; and a 1:2:1 mixture of pelletsizes 1.5, 1.7, and 2.5 mm was used during 19 August 2008 –25 May 2009. In all diet groups, and throughout the experi-ments, a small amount of excess feed was observed on the tankand pond bottoms, indicating that the fish were feeding ac-cording to appetite on feeding days.

Monitoring growth, condition, body fat content,maturity, fin erosion, and mortality

The PIT-tagged fish in each replicate tank or pond weremeasured for total length and body mass under anaesthetic(MS-222 or clove oil) four times during the raising period(Table 1). One measurement occasion lasted several days, butchanges in individual parameters during this time were as-sumed to be trivial with regard to diet manipulation. Individualstandardized mass-specific growth rates (�%; Ostrovsky1995) were calculated for the three growth periods and themigration experiment period (Table 1) using the followingformula:

(1) � �Mt

β � M0β

β � t� 100

where M0 is the fish body mass (g) at the beginning of theperiod, Mt is the body mass (g) at the end of the period, t is the

Table 1. Timetable of the experiment and the applied treatments.

Event Period M Fat Date N/T

Rearing started in four tanks — 22 Mar. 2007 4400–5737Random division of fish to 16 3.2 m2 tanks — 24 Apr. 2008 1270

PIT-marking and size measurements I I I 14 May 2008 250Spring diet manipulation starts 16 May 2008 1260Spring diet ends 30 June 2008 1260

Size measurements II II II 10 July 2008 1250All fish transferred to 16 outdoor 50 m2 ponds 11 July 2008 1250Size measurements, maturity checks III III 16 Oct. 2008 1230

Winter diet manipulation starts III 30 Oct. 2008 1230Migration experiments start in circular streams 10 Nov. 2008 200 � 200Swimming performance test I for 493 fish 30 Apr. 2009 1230Size measurements IV IV 20 May 2009 1210

Winter diet manipulation ends — 30 May 2009 1210Release of smolts to Merikoski (1000 fish per treatment) — 1 June 2009 250Swimming performance test II for 77 fish — 3 June 2009 0Migration experiments end in circular streams — 21 July 2009 0

Note: “M” refers to measurement occasion, “Fat” indicates the body fat content sampling occasions when 10 nonmarked fish were randomly removedfrom each tank, “Period” identifies the start of the corresponding growth period, “Date” is the finishing date for the event, and “N/T” is the target number ofindividuals per tank after the event, except for migration experiments, for which the N/T stands for the N per treatment group.

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length of the growth period (days), and � is an allometric massexponent describing the relationship between growth rate andbody mass. The value of � � 0.31 was obtained from Elliottand Hurley (1997).

The adjusted Fulton’s condition factor (K) was calculated foreach individual using the following equation: K � 100 g·cm–b

total body mass (g) � (total body length (cm))–b, where b (2.95)was obtained as the slope of a regression of ln(mass) on ln(totallength) using all the data pooled from the measurements (linearregression, R2 � 0.981, P � 0.001; Bolger and Connolly 1989).Because of the poor fit of the regression for the pooled datafrom the migration experiment, the condition factors werecalculated separately for the initial measurements (b � 2.99)and the final measurements (b � 3.02) in the migration ex-periment (see below).

The total lipid (mass percentage) content of the fish wasdetermined from freeze-dried fish after each diet manipu-lation period using hydrochloric acid hydrolysis andSoxhlet extraction in petroleum– ether. The analysis wasperformed from a pooled sample of 10 nonmarked fish pertank (four replicates), except after the fourth size measure-ments, when PIT-tagged fish were analyzed individually. Inaddition, lipid content was determined for 11 smoltsstocked in River Varisjoki (six at age 1� and five at age0�), nearby the research station. The semiwild fish werecaptured by smolt trap during their downstream migrationas 2-year-old smolts and were used as a reference for wildsmolts.

Mortality was observed daily, but since not all the fish wereindividually marked, only treatment-specific counts of deadfish were used in the statistical tests. The maturity of PIT-marked male fish was determined in October 2008 at the timeof the third size measurements (Table 1), before theWD ma-nipulation could have influenced maturation; a fish was calleda mature male if it released milt when gently pressed; other-wise, it was called an immature male or female. The compar-ison of maturation rates between the treatments is based on theassumption that the sex ratio is equal between the diet groups.No fish were sacrificed for the analysis of maturity status, andnoninvasive maturity determination was not possible at thetime of release in spring 2009 (Table 1).

Simultaneously with the last size measurements (Table 1),the condition of the pectoral fins and the dorsal fin wasclassified visually on a scale of A to E (Latremouille 2003):A, pristine; B, erosion �20% or fractures; C, erosion 20%–50%; D, erosion � 50; E, full erosion. Smoltification statuswas based on a scale of 1 to 4: 1, parr — clear parr marks,brownish overall, no silver colour; 2, signs of smoltification,but brownish colour and parr marks clearly visible; 3, 50%silver colouration, parr marks weakly visible; 4, visually clas-sified as smolt — fully silvered.

The respective total numbers of individuals and PIT-taggedindividuals per treatment at the end of the raising period wereas follows: CD: 4587 and 737; SD: 4719 and 719; WD: 4674and 724; SWD: 4452 and 652.

Swimming endurance testsTo test whether migration and survival variation among diet

groups could result from differences in swimming capacity, a

total of 493 randomly chosen PIT-tagged fish were tested forswimming endurance between 23 March and 3 April 2009. Intotal, 77 of these fish were randomly excluded from the groupof released fish and tested again on 2–3 June 2009, i.e., shortlyafter the fish were released at the Merikoski fish ladder (seebelow). The fish were kept in separate tanks for 4 days withoutfood prior to the swimming tests and measured for length andmass after the tests. In the swimming endurance test, a fish wasplaced into a flow-through transparent tube (1200 mm long,inner diameter 100 mm, 5 mm grids in both ends) and allowedto acclimatize for 90 s before the water current was increasedevery 5 s as described by a polynomial equation, where trefers to time (s) (entered without unit): water current speed(m·s–1) � 1.59 � 10�8·t4 – 6.40 � 10�8·t3 � 6.90 � 10�3·t2 –0.00298·t � 0.0321 (quadratic regression: R2 � 0.999). Thetest was terminated the moment the fish lost its ability to swimagainst the current and drifted against the grid at the end of thetube. The total time (s) from the moment of the first incrementof the current until the finishing moment was used as themeasure of swimming endurance.

Migration experiments in circular streamsTo study whether the timing and parameters of smolt mi-

gration differed between CD and SWD groups, 400 parr (totallength: 169.0 19.9 mm; body mass: 44.5 15.3 g; mean standard deviation) were randomly chosen from the SD ponds(4 � 50 fish) and CD ponds (4 � 50 fish) and divided intoeight circular channels in their original group composition(four control � four treatment channels; outer circumference30.9 m, inner circumference 26.0 m, one round � 28.45 m,channel width 1.5 m, water depth on average 333 mm, N � 50fish per channel) with directional water flow (water flow0.11 m·s–1 or 55 L·s–1; Table 1). Prior to the migration exper-iments, the fish were weighed and measured for total lengthand surgically tagged with half duplex PIT-tag (Texas Instru-ments Inc., http://www.ti.com) in anaesthesia on 21–22 Octo-ber 2008. The PIT tag (23 mm � 4 mm) was ventrallyimplanted into the body cavity of the fish. Each channel wasequipped with four PIT-reading antennas (at equal distances)that recorded individual movements nine times per second(Supplemental Table S11; Janhunen et al. 2011).

The experiment continued until 20–21 July 2009. The fishin the four CD streams were fed a standard amount of feedeach day by automatic feeders (as during raising — seeabove), whereas the fish in the four WD streams were only fedevery seventh day (85% reduction in feed ration and 75.4%reduction in the realized total feed delivery). The movementdata were analyzed for the period between January and July(zero hour corresponds to 1400, 5 January 2009, and the finalhour 4341 corresponds to 0700 on 5 July 2009), because nosigns of migration were observed during the late autumn.Furthermore, since some fish increased swimming activity asearly as in January, 672 h (4 weeks) were excluded from thebeginning. To explain such early activity, we analyzed theproportion of active (exceeding the threshold, see below) andstationary fish during this period with respect to the treatmentand channel.

The automatically collected movement data were used tocalculate the individual number of antenna bypasses and the

1Supplementary data are available with the article through the journal Web site at http://nrcresearchpress.com/doi/suppl/10.1139/f2012-119.

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direction of bypasses per hour during the whole experimentusing the PIT-Data (N. Vuokko, 2007–2010) software pack-age. The hourly data were then used to determine eightindividual-level parameters: (1) time until average migrationactivity threshold (two rounds per hour) during a 72 h timeslot; (2) time until maximal average moving activity during a72 h slot; (3) time until the maximal increase in movingactivity during a 72 h slot. The rate of increase was defined asthe slope of the regression between activity and observationhour; (4) the maximal rate of activity increase during a 72 hslot (see above); (5) specificity of movement during maximalactivity in a 72 h slot; (6) specificity of movement duringmaximal migration activity increase in a 72 h slot; (7) averageswimming speed during maximal migration activity in a 72 hslot; (8) average swimming speed during maximal migrationactivity increase in a 72 h slot.

For the calculation of migration specificity, the average dis-tance moved (i) in total, (ii) downstream, and (iii) upstreamduring the 72 h slot was calculated. The specificity index (rangefrom –1 to �1) of migration was defined as the net distancemoved downstream divided by the total distance moved. There-fore, negative specificity values indicate upstream migration (–1indicates only upstream migration and �1 only downstreammigration). If a fish did not show activity above the thresholdvalue, the maximal length of the experiment (4341 h) was as-signed for each of the latency measures (1–3). After the experi-ments, the test fish were killed.

Release experiment and the tag recoveries from fishedand returning fish

To examine if the latency times before leaving the stockingsite depend on diet treatments, �700 (153–202 fish per treat-ment) PIT-tagged fish and �1937 Floy-tagged fish (taggingbetween 4 March and 7 April 2009, yellow T-bar anchor,Hallprint Pty Ltd., http://www.hallprint.com) were releaseddaily onto the Merikoski fish ladder between 29 May and1 June 2009 (cf. Greenstreet 1992). One tank of fish pertreatment per day was released in mixed order onto the thirduppermost step (N � 2100 PIT-tagged fish and 5812 Floy-tagged fish in total). The daily mean water temperature was11.6–13.9 °C.

The fish ladder used for release was 200 m long in total and had16 steps (mean depth 2.0 m, step length 6–14.8 m, step width5.3–9.8 m, water flow 1.2 m3·s–1). The ladder was located�2000 m upstream from the opening of River Oulujoki tothe Bothnian Bay of the Baltic Sea. The ladder wasequipped with three PIT-reading antennas (SupplementalTable S11) in the doorways between the steps (two down-stream and one upstream from the stocking site). PIT-readersfunction reliably when the fish pass the antenna one at a time(Greenberg and Giller 2000), but may miss tags if several fishpass the antenna simultaneously. During the first days afterrelease, a large number of fish left the stocking site, and only426 of 2100 fish were detected by the antennas. Therefore, twoanalysis options were chosen: (1) all released fish were anal-ysed with the assumption that all the undetected fish left within2 days, and (2) only the directly observed (and thus mostlylate-leaving) fish were used in the analyses. Neither alternativewas likely completely correct, but together they were assumedto reveal factors that influenced latency before leaving thestocking site.

After the release, fish movements were followed until theend of September 2009. No signals from stocked fish wereobtained from 15 July 2009 onwards, indicating that no fishstayed on or returned to the fish ladder after that date. Thelast signal of a given fish from any of the antennas was usedto calculate the latency time before leaving the stockingsite.

Tag recovery data from a multinational commercialsalmon fishery combined with detections of returning fishby PIT-antennas in Merikoski by 28 October 2011 includedonly 19 fish, and no statistical differences among the treat-ments were detected.

Statistical analysesTo attribute the observed response variable values to diet

treatments, tanks, and individual characteristics includingbody length and mass, condition, and growth rate, we usednested univariate and multivariate generalized linear models(GLZ) with repeated effects when necessary (Ruohonen1998). When individual data were not available, tank-specificmeans were used. Bonferroni-type multiple comparisons wereused to study the pairwise differences among treatments.In addition, cross-tabulations and corresponding Pearson’s�2 tests were used to examine the effect of diet treatments onthe frequency of different smoltification and maturity classes.Mortality was compared among groups by bootstrapping theobserved frequencies with original sample size by 100 000times and examining the 95% confidence intervals derivedusing the first percentile technique, i.e., picking the 2500th and97 500th values from the sorted table of 100 000 bootstrapfrequency estimates. The selection of model in logistic regres-sion analyses was based on the principle of parsimony, bio-logical feasibility of the candidate models, and comparisons ofAkaike information criterion (AIC). Classification precision wasused as another criterion for the model fit. To confirm the resultsof the multivariate analysis of covariance (MANCOVA) in themigration experiments (because of violations of homoscedastic-ity), nonparametric Mann–Whitney U tests were used to com-pare the behavioral variables of all tanks and without theimpact of covariates.

To explain the desired short latency prior to leaving thestocking site by logistic regression, the fish were classified intotwo classes assumed to have potential implications for thesurvival of smolts in general: (1) fish that left within 2 days ofstocking and (2) fish that stayed in the ladder for longer than2 days (see also Fängstam et al. 1993). This somewhat arbi-trary choice of division was based on the observation (com-bined with the assumption of PIT-reader failure during the firstdays) that the majority of fish left (1793 fish vs. 303 fish)within the first 2 days.

To fulfill the normality assumption, addressed by visual in-spection of frequency histograms in relation to normal curves andassociated Kolmogorov–Smirnov tests, body mass, condition fac-tors, and all behavioural variables (latency prior to starting mi-gration after release and all the behavioural response variables inthe migration experiments) were ln-transformed (ln(X � 1) whennecessary) prior to analyses. Prior to the analyses of covariance,we tested for covariate � factor interactions. The linearity ofcovariate-dependent variable relationships was visually ad-dressed by running separate linear regression analyses (notshown). All the statistical analyses were performed using

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SPSS 16.0 (SPSS Inc., Chicago, Illinois) and R (R Develop-ment Core Team, http://www.r-project.org) except for boot-strap analyses performed using AV Bio-Statistics 4.9 (built bythe corresponding author). For a detailed description of thestatistical analyses, see Supplementary Table S21.

Results

Development of body length, mass, condition and fatcontent

The combined SWD decreased the length-at-release by10.1%, mass-at-release by 11.9%, and condition-at-release by12.9% in comparison with CD (repeated measures analysis ofvariance (RM-ANOVA), for standard group: total length196.4 mm, body mass 66.7 g, and condition factor 1.01;Supplemental Table S31). The effect of WD was the secondstrongest with 4.0%, 7.1%, and 10.9% decreases, respectively.The effect of SD, especially on body mass and condition,almost disappeared by the time of release (length: 4.8%, mass:4.8%, and condition: 1.0%; Supplemental Table S11).

Body lipid content increased throughout the raising period (RM-ANOVA, Wilks’ � � 0.032, F[3,10] � 99.26, P � 0.001) butdepended on the treatment (RM-ANOVA, Wilks’ � � 0.037,F[9,10] � 24.49, P � 0.001; Fig. 1). Individual ANOVAs foreach measurement occasion revealed that the SD and SWDmanipulation groups had lower body lipid content than the CDand WD groups (P � 0.001; Fig. 1) at the second measure-ment after the SD period. At the third measurement, however,the SD and SWD fish had compensated for their previouslylower body lipid content, and thus no significant differencesamong the diet groups were found (P � 0.060). At the timeof release, the body lipid content in the SWD and WD groupswas well below the lipid content of fish in other groups(P � 0.001; Fig. 1), whereas the SD group had reached thesame level as the CD group.

The food treatment and rearing tank affected the finalbody lipid content (ANCOVA, treatment: F[3,137] � 20.16,P � 0.001), but fish total length had no effect (tank withintreatment: F[18,137] � 4.05, P � 0.001; total length:F[1,137] � 0.89, P � 0.348). Based on raw averages, theaverage body lipid content was highest in the SDgroup (8.3%), second highest in the CD group (8.1%), thirdhighest in the WD group (5.3%), and lowest in the SWDgroup (5.2%). However, the body lipid content of the re-

leased fish was significantly higher in all diet manipulationgroups compared with River Varisjoki smolts stocked 1 or2 years before sampling (ANOVA, F[5,165] � 122.27, P � 0.001;Fig. 1). At the time of release, CD and SD did not differsignificantly, nor did WD and SWD (Bonferroni pairwisecomparison, P � 0.05; Fig. 1).

Effects of diet manipulation on total mortality in thehatchery

Total mortality during the experimental period was4.58%. According to bootstrapped confidence intervals,mortality was unequally divided between the among (Sup-plemental Fig. S11). Among the dead fish, individuals fromthe CD group were underrepresented and individuals from theSWD group overrepresented. The SD and WD groups did notdiffer from each other in total mortality. However, the absolutedifferences in mortality were small (CD: 3.62%, WD: 4.62%,SD 4.66%, SWD: 5.42%).

Fin erosionDorsal fin condition was influenced by diet manipulation, as

fin damage was clearly least common in the CD group (�2 �555.82, df � 15, P � 0.001). The dorsal fin was in pristinecondition in 18.4% of the CD fish, in 9.4% of the SD fish, in5.2% of the WD fish, and in 3.8% in SWD fish. In general,10.5% of the fish in total suffered from severe dorsal finerosion (class E). Fin damage was more rare in pelvic fins, butthe same pattern among the diet groups was also observed inthis case (�2 � 100.52, df � 15, P � 0.001). The pelvic finswere in pristine condition in 47.4% of the CD fish, 42.6% ofthe SD fish, 36.3% of the WD fish, and 30.0% in SWD fish.Only 2.3% of the fish were classified as C–E; i.e., clearlydamaged pelvic fins.

SmoltificationVisual characteristics of smoltification were influenced by

diet (�2 � 54.46, df � 9, P � 0.001; Fig. 2). Completesmoltification (class 4) was the most frequent in the SD group(72.4%), followed by CD (65.8%), WD (62.0%), and SWD(56.5%). Precocious maturity the previous autumn decreasedthe likelihood of complete smoltification (�2 � 40.71, df � 3,P � 0.001), as it was observed in 65.1% of immature fish butin only 39.7% of fish that had matured previously.

Candidate GLZs indicated that the parabolic growth rate duringthe second or third growth period did not affect the likelihood ofcomplete smoltification (class 4 vs. classes 1–3). However, dietmanipulation (Wald �2 � 80.5, df � 3, P � 0.001), tank withintreatment (Wald �2 � 155.5, df � 12, P � 0.001), final total bodylength (Wald �2 � 441.2, df � 1, P � 0.001), and finalcondition (Wald �2 � 12.3, df � 1, P � 0.001) all affectedthe likelihood of full smoltification. The final logistic re-gression model predicted the correct smoltification categoryfor 68.4% of nonsmolted fish and for 76.8% of smolted fish.In comparison with the combined SWD group, the CDgroup significantly retarded smoltification (B � – 0.95,P � 0.001), but no other differences were observed am-ong diet treatments. Both the total length (B � 0.067,P � 0.001) and condition factor (B � 3.77, P � 0.001) hada positive effect on smoltification. However, since dietmanipulation affected both the length and condition of thefish, the negative main effect of CD on smoltification arose

Fig. 1. Development of fresh body lipid content of Atlantic salmonsmolts in the four different diet treatments over the course ofrearing (N � 64 pooled samples of 10 fish and 11 semiwildindividuals). Measurement occasion four corresponds to the time ofrelease of fish.

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likely because of high nonindependent covariate values inthis group.

Precocious maturationPrecocious maturity prior to WD was generally rare among

the raised fish, but was more common in the CD groups(CD�WD) than in the SD groups (SD�SWD) (3.28% vs.1.65%, respectively; �2 � 9.94, P � 0.002). The final modelfor predicting precocious maturation included the diet group(for CD vs. SD groups: B � –1.56, P � 0.101), tank withintreatment (0.09 � P � 0.858), and the constant (B � –40.49,P �0.001). Length at the second measurement (B � 0.047,P � 0.001), condition factor at the end of the second growthperiod (B � 39.60, P � 0.001), and the parabolic growth rateduring the first growth period (B � 0.65, P � 0.062) contrib-uted positively or nearly significantly to the likelihood ofprecocious maturation. The parabolic growth rate during thesecond growth period, i.e., after SD, decreased the likelihoodof precocious maturation (B � –3.36, P � 0.001). The finalmodel predicted the correct maturity class for 99.6% of theimmature fish and for 70.9% of the mature fish.

Swimming capacityDiet manipulation did not influence the swimming endur-

ance measured in April 2009 (ANCOVA, F[3,406] � 1.84,P � 0.140; the effect of tank: F[12,406] � 1.03, P � 0.418).All the covariate effects were either significant or close tosignificant (ANCOVA, total length: B � 0.001, F[1,406] �11.90, P � 0.001; condition factor: B � 0.131, F[1,406] �3.35, P � 0.068; growth rate: B � – 0.067, F[1,406] � 4.42,P � 0.036), indicating that long fish in good condition hadimproved swimming endurance, while a high growth ratehad the opposite effect. The variation in swimming endur-ance in the second swimming capacity tests could not beexplained by any of the factors or covariates (P � 0.105).

Growth, precocious maturity, and smoltification inexperimental streams

The decrease in feed ration affected the mean length, bodymass, and condition factor in the migration experiments sim-ilarly to the main experiment (MANOVA, all multivariate

results except the nested effect of tank, P � 0.001, tank effect:Wilks’ � � 0.955, F[18,1075.29] � 0.970, P � 0.492; forbetween-subject effects see Supplemental Table S41). Therespective predicted final body length, mass, and conditionfactors were 176.9 mm, 34.7 g, and 0.587 for the SWD fishand 197.2 mm, 50.9 g, and 0.620 for the CD fish. The de-creased feed ration did not affect precocious male maturity, as23 fish were found to be sexually mature at the end of theexperiment in the SWD group compared with 32 in the CDgroup (�2 � 1.759, P � 0.185). The final logistic regressionmodel explaining precocious maturity included, in addition tothe constant (B � –11.93, P � 0.001), treatment (for SWD vs.CD: B � 2.00, exp(B) � 7.41, P � 0.124), tank withintreatment (0.211 � P � 0.949), length at the beginning of theexperiment (B � 0.11, exp(B) � 1.12, P � 0.001), andln-transformed condition factor at the end of the experiment(B � 30.07, exp(B) � 1.15 � 1013, P � 0.001). This modelpredicted the correct maturity class for 97.6% of immature and85.5% of mature fish.

There was no difference in the proportion of fullysmolted individuals between the diet groups (�2 � 2.62,df � 1, P � 0.106). After the experiment, 81.2% of the CDfish and 87.2% of diet restriction group fish were visuallyclassified as fully smolted.

Migration in experimental streamsThe ln-transformed final condition factor at the end of the

experiment, precocious maturity, treatment, and tank nestedwithin treatment all explained significant variation in the ln-transformed behavioural response variables (MANCOVA,multivariate results, P � 0.001). Of these variables, the treat-ment (2 � 0.626) and tank within treatment (2 � 0.391) hadthe strongest multivariate effects. The between-subject effectsaligned with the multivariate effects (Supplemental Table S51)and showed that feed restriction affected all of the responsevariables (Figs. 3 and 4). A high condition factor had anegative impact on all variables except the time until thresholdactivity (Supplemental Table S51).

Based on raw averages, the fish in the feed restricted groupexceeded threshold migration activity 2 weeks (14.4 days) before

Fig. 2. Frequencies of visual smoltification classes among treatments at the time of release. The corresponding percentages of mature malesin the previous autumn were 2.5% (standard diet), 1.1% (spring diet), 4.0% (winter diet), and 2.2% (combined diet) (N � 3589).

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the standard fish, but displayed maximal migration activity14.7 days later than the standard fish. Further, based on rawaverages, the fish in the feed restricted group showed maximalmigration activity of 281.9 m·h–1, whereas the CD group mi-grated at a much slower speed of 82.4 m·h–1 (cf. Fig. 4).

Nonparametric Mann–Whitney U tests confirmed the results ofthe MANCOVA (suffering from violations of the assumption ofhomoscedastic variances among groups), with the exception thatthe standard-raised fish did not differ from the feed-restricted fishin the time until maximal migration activity (U � 6514.00,N � 390, P � 0.316; for all other behavioural variables:P � 0.001). Cross-tabulation revealed that wintertime migrationactivity was more common among the feed restricted fish(31.6%) than among the CD group (9.1%) (�2 � 30.5, df � 1,

P � 0.001). However, wintertime migration activity did not occurin three of the replicate tanks and as such was very tank-specific(�2 � 99.0, df � 7, P � 0.001).

Latency before leaving the release siteMost of the fish left the release site within 2 days (Fig. 5).

Nested candidate ANCOVA models indicated that none of thecovariates, i.e., body length-at-release, condition factor-at-release, and parabolic growth rate during period III, signifi-cantly explained variance in the ln-transformed time spentbefore leaving the release site. The final ANOVA modelrevealed differences among the diet groups but not betweenmature and immature individuals (Table 2; Fig. 6). Two-sample Kolmogorov–Smirnov tests indicated that the residual

Fig. 3. Predicted marginal mean (a) times (ln(days)) to the start of smolt migration in experimental streams with three different criteriasince 5 January 2009 and (b) maximal rate of activity increase and specificity of migration at the time of maximal activity and maximalactivity increase period according to nested multivariate analysis of covariance (MANCOVA) (N � 393).

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distributions of latency times were different (P � 0.017)among all other diet group pairs except for SD vs. SWD andCD vs. SWD pairs (see Fig. 5). This suggests that in additionto differences in average premigration latency times, therewere fine-scale differences in leaving times among the dietgroups.

The final binomial GLZ model on data including onlydirectly observed fish correctly predicted 87.2% of caseswhere the fish did not leave the fish ladder within 2 days fromrelease. The precision to predict a rapid start to migration waspoor (38.8% correct), which might be explained by the highrate of missed bypasses (86.1% of all fish). The regressioncoefficients for diet groups were not significant (P � 0.313),nor were condition factor-at-release (B � 5.22, P � 0.071) andgrowth rate during growth period III (B � 1.48, P � 0.216).The final GLZ model on data including all released PIT-taggedfish, i.e., the model with only significant explanatory variablesand factors, completely failed to predict the likelihood ofstaying in the stocking site for more than 2 days, as all the fishwere predicted to leave. However, the model indicated thatcompared with SWD, SD (B � –0.963, P � 0.001) and CD(B � –0.846, P � 0.002) decreased the likelihood of earlymigration. In contrast, compared with maturity, immaturity(B � 0.829, P � 0.012) and high condition factor-at-release(B � 3.536, P � 0.015) increased the likelihood of an earlystart to migration.

Fig. 4. Predicted marginal mean swimming speeds at the time ofmaximal swimming activity (open bars) and the time of maximalactivity increase (shaded bars) according to nested multivariateanalysis of covariance (MANCOVA) in the migration experimentsin circular streams (N � 393). The circumference of the tank is77.34 m, which translates to absolute maximum swimming activityvalues of 232.2 and 79.3 m·h–1 between the reduced ration andstandard ration groups, respectively.

Fig. 5. Observed latencies (in days) prior to leaving the stockingsite in the different diet groups: (a) standard diet; (b) spring diet;(c) winter diet; and (d) combined spring and winter diet (N �426). Fish that left within 2 days were classified as fast to leaveand the fish that spent more than 2 days in the stocking site aspotential nonmigratory fish.

Table 2. The effects of diet manipulation on the ln-transformedlatency prior to leaving the stocking site according to a nestedanalysis of variance (ANOVA).

SourceTypeIV SS df F Sig. Partial 2

Intercept 141 1 80.8 �0.001 0.166Diet manipulation 28.4 3 5.43 0.001 0.039Tank nested within

treatment51.5 8 3.69 �0.001 0.068

Immaturity vs.maturity

2.69 1 1.54 0.215 0.004

Corrected model 85.5 12 4.08Error 706 405Total 1580 418

Note: For the model predictions see Fig. 5.

Fig. 6. Predicted latencies prior to leaving the release site(Merikoski fish ladder) according to nested analysis of variance(ANOVA, N � 426). The letters above the main effects (a, b)indicate groups that do not differ from each other according topairwise Bonferroni comparisons.

Vainikka et al. 1989

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DiscussionBased on our results, we suggest that spring and winter feed

restriction periods may be useful in reducing precocious malematurity and improving the overall migratory tendency amonghatchery-reared smolts of Atlantic salmon. In particular, therelatively short SD period reduced the proportion of preco-ciously mature males by almost 50%, more than observed byBerglund (1995). Winter feed reduction appeared effective inincreasing both the migration speed and the precision of mi-gration downwards in experimental conditions and as suchsupported earlier findings both in salmon (Lans et al. 2011)and brown trout (Wysujack et al. 2009; Larsson et al. 2012).The positive effect of winter feed reduction was also seen inthe release data; fish exposed to winter or the combined springand winter feed ration reduction left the stocking site earlierthan the fish from the SD group. The SWD did not improve themigration start in comparison with WD only, although the SDreduced previous male maturity that was otherwise found todelay migration start.

The reduction in feed ration in our study was implementedby decreasing the frequency of feeding. This is an efficientmethod to minimize between-individual variation in growthand development (Pirhonen and Forsman 1998). Feed restric-tion treatments were effective in reducing the body size andcondition of salmon smolts at release, but fish in the SD groupshowed compensatory growth after the diet manipulation pe-riod and matched or almost matched the control fish in size,body condition, and body lipid content by the time of therelease. However, compensatory growth can be beneficial ifthe fasting period still induces desired effects, such as reducedprecocious maturation (Morgan and Metcalfe 2001; Jokikokkoet al. 2006). Despite the promising results in the start ofmigration, feed restriction did not significantly increase thefishery tag return rates or the numbers of returning spawners.The tag return rate remained equally low in all groups (onaverage 0.2%), indicating that the Baltic Sea environment iscurrently very challenging for released salmon and (or) thatthe released smolts suffer from domestication or other factorsnot considered in our study (see also Jokikokko et al. 2006;Araki et al. 2007; Kallio-Nyberg et al. 2009). Swimmingcapacity measured experimentally against water current didnot vary among the treatments. However, the negative effectof a fast growth on swimming capacity suggests that the fastgrowth rates in hatcheries may have negative effects on theswimming performance of released fish. Feed restriction alsohad clearly negative effects on fin erosion and mortality in thehatchery. Even though fin erosion did not affect latency priorto leaving the stocking site (ANOVA not shown), the negativeeffects of feed restriction might have contributed to the lack ofdifference in return rates of fish with respect to the diet groups.

The migration experiment in artificial streams suggestedthat wintertime food availability could influence the start offeeding migration in a variety of ways. First, feed restrictioninduced movement in the middle of the winter before theexpected smolt migration, although the effect was stronglystream-specific. The increased movement of some individualsafter the excluded period but before the expected smolt mi-gration explained why feed-restricted fish, on average, ex-ceeded threshold migration activity 2 weeks before the controlfish. This suggested that low food availability in the juvenile

environment may force the parr to search for areas with betterfeeding opportunities. Second, the reduced feed ration delayedthe timing of maximal downward migration activity for2 weeks in comparison with the control ration. However, oncethe feed-restricted fish had started migrating, their migrationwas much faster and more clearly oriented downstream thanthat of the control fish. Surprisingly, feed restriction in streamchannels had no effect on smoltification, and over 81% of allfish were fully smolted by the end of the experiment.

The results of the migration experiment in the seminaturalstreams supported those observed in the actual stocking situ-ation in the Merikoski fish ladder. Both results suggested thatfeed restriction in the winter prior to stocking is the key factorinvolved in accelerating the start of migration. Despite theunfortunate fact that a large proportion of fish left the stockingsite undetected, we were able to compare the individual qual-ities of the fish that left within 2 days with those that delayedtheir migration start by more than 2 days after stocking. Thepositive effect of the high condition factor on migratory be-haviour contrasts with the results in brown trout (Wysujack etal. 2009). Our analyses suggested that feed restriction prior torelease generally had a positive effect on the start of migrationby slowing down growth rate, whereas a high condition factorat the onset of smoltification had a positive effect on migrationtendency (cf. Pirhonen and Forsman 1999). This suggests thatthe optimal feed restriction period prior to release could beshorter and started later than in our study. Still, the effects offeed restriction on the migratory behaviour of salmon mayvary from year to year (Beckman et al. 1999; Lans et al. 2011).

Both smoltification and maturation depend on growth rate,and a certain threshold size must be exceeded at a specific timefor a development route to be adopted (e.g., Elson 1957;Myers et al. 1986; Thorpe 1994a). Fast-growing salmonidjuveniles have been found to start smoltification earlier thanslow-growing individuals both in natural and aquaculture con-ditions (Thorpe et al. 1980; Thériault and Dodson 2003). Thesame pattern has also been observed among different Atlanticsalmon populations, so that the mean smolt age is lower inrivers with better growth opportunities (Metcalfe and Thorpe1990). On the other hand, high food availability and lowconspecific density in the natural environment may completelyprevent feeding migration in partially migrating brown trout(Olsson et al. 2006). Since high food availability at differenttimes can both improve and hinder the smoltification processand migration tendency, the optimal regulation of feed rationand diet composition represents a challenge for the aquacul-ture of smolts for release. For example, prolonged feed restric-tion during May–November did not improve the smoltificationprocess or migration activity of brown trout parr in the studiesof Pirhonen and Forsman (1998, 1999), whereas winter feedrestriction improved the migratory behaviour of brown trout inanalogous studies of Wysujack et al. (2009) and Larsson et al.(2012). In our study, the observed patterns were apparentlycontradictory; while the winter diet improved migration ten-dency both in the experimental streams and in the authenticstocking situation (also see Lans et al. 2011), it decreased theproportion of fully visually smolted individuals in comparisonwith the CD or SD groups. Similarly, while a high growth rateprior to release explained a long latency prior to leaving therelease site, large size and good condition were positively relatedto visual smoltification. However, smoltification score did not

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explain variance in latency prior to starting migration. Our resultsare in line with the physiological observations of an insulinconcentration peak and correlated fast growth period starting inFebruary in successfully smolting parr (Dickhoff et al. 1997) andwould suggest that feed restriction during the critical smoltingperiod somewhat hinders rather than enhances the smoltifica-tion process in salmon.

Our analyses revealed that male maturity in the autumnprior to their release in the spring decreased the likelihood ofboth visual smoltification and fast migration start and as suchsupported earlier studies (Fängstam et al. 1993 and referencestherein). Precocious maturity at the time of release is known toinfluence the migration and survival of released salmonsmolts, but the effects of precocity vary among years and maydepend on body size (Lundqvist et al. 1988; Kallio-Nyberg etal. 2009, 2011b). According to our results, feed restriction atthe onset time of both maturation and smoltification does notprovide additional benefits over efficient feed restriction at thetime of smoltification (cf. Rowe and Thorpe 1990). However,the lack of response to combined spring and winter feedrestriction in our study may well be explained by the low ratesof precocious maturity. If springtime feed restriction reducesprecocious maturation by 50% as observed in this study, thiswould be likely to have strong effects on the migration of fishshowing typically much higher frequencies of precocious ma-turity (Kallio-Nyberg et al. 2009).

Body lipid content was unnaturally high among all thereleased fish in this study (5%–8%) compared with smoltsrecaptured in a natural river (2%). As such, our results werecomparable to the lipid content reduction obtained in the feedrestriction experiment by Lans et al. (2011). Since the deter-mination of body lipid content was not possible without sac-rificing the fish, we could not link individual body lipidcontent directly with individual migratory behaviour. How-ever, correlative evidence from our study and comparativeevidence from brown trout (Larsson et al. 2012) suggest thatbody lipid content can play a major role in influencing migra-tion decisions, although salmon and brown trout may alsodiffer in how they respond to the size of lipid reserves(Larsson et al. 2012).

Strong heritable components in smolting and maturation age(Gjerde 1984; Duston et al. 2005) can pose challenges for theuniform production of smolts that are both immature and readyto start feeding migration at the time of release. In this respect,the maximally effective manipulation of released phenotypesby food restriction or any other means could potentially im-prove the success of stocking by maximizing the numbers offish that are physiologically ready to start feeding migration.Our results as well as other similar studies (Lans et al. 2011;Larsson et al. 2012) are encouraging, showing that male pre-cocious maturation can be reduced and the overall migrationtendency of smolts improved by spring and winter food re-striction periods, respectively. However, further research isneeded to optimally schedule the fasting periods to producethe desired effects but to avoid undesired side effects onmortality and fin erosion.

AcknowledgementsThe staff of the Kainuu Fisheries Research Unit is grate-

fully acknowledged for their efforts in this study. The staffof the Laukaa Fisheries Research Unit and Finnish Food

Safety Authorities is acknowledged for the lipid contentanalyses. The staff of Oulu Game and Fisheries ResearchUnit is acknowledged for implementing the PIT-tag datamonitoring at the Merikoski fish ladder. Oulun Energia Oyis acknowledged for the use the Merikoski fish ladder forresearch. We thank the Maj and Tor Nessling Foundationfor funding (project 2011392). Neil Metcalfe, associateeditor James Grant, and an anonymous reviewer are grate-fully acknowledged for their constructive comments andsuggestions on the earlier versions of the draft of this paper.Tmi Kielipalvelu Enticknap-Seppänen revised the languageof the manuscript.

ReferencesAraki, H., Cooper, B., and Blouin, M.S. 2007. Genetic effects of

captive breeding cause a rapid, cumulative fitness decline in thewild. Science, 318(5847): 100–103. doi:10.1126/science.1145621.PMID:17916734.

Beckman, B.R., Dickhoff, W.W., Zaugg, W.S., Sharpe, C., Hirtzel,S., Schrock, R., Larsen, D.A., Ewing, R.D., Palmisano, A.,Schreck, C.B., and Mahnken, C.V.W. 1999. Growth, smoltifica-tion, and smolt-to-adult return of spring chinook salmon fromhatcheries on the Deschutes River, Oregon. Trans. Am. Fish.Soc. 128(6): 1125–1150. doi:10.1577/1548-8659(1999)128�1125:GSASTA�2.0.CO;2.

Berglund, I. 1995. Effects of size and spring growth on sexualmaturation in 1� Atlantic salmon (Salmo salar) male parr: inter-actions with smoltification. Can. J. Fish. Aquat. Sci. 52(12): 2682–2694. doi:10.1139/f95-857.

Bjerkeng, B., Refstie, S., Fjalestad, K.T., Storebakken, T., Rødbotten,M., and Roem, A.J. 1997. Quality parameters of the flesh ofAtlantic salmon (Salmo salar) as affected by dietary fat contentand full-fat soybean meal as a partial substitute for fish meal in thediet. Aquaculture, 157(3–4): 297–309. doi:10.1016/S0044-8486(97)00162-2.

Bolger, T., and Connolly, P.L. 1989. The selection of suitable indicesfor the measurement and analysis of fish condition. J. Fish Biol.34(2): 171–182. doi:10.1111/j.1095-8649.1989.tb03300.x.

Brodersen, J., Nilsson, P.A., Hansson, L.-A., Skov, C., and Brönmark, C.2008. Condition-dependent individual decision-making determinescyprinid partial migration. Ecology, 89(5): 1195–1200. doi:10.1890/07-1318.1. PMID:18543613.

Brönmark, C., Skov, C., Brodersen, J., Nilsson, P.A., and Hansson,L.-A. 2008. Seasonal migration determined by a trade-off betweenpredator avoidance and growth. PLoS ONE, 3(4): e1957. doi:10.1371/journal.pone.0001957. PMID:18414660.

Chittenden, C.M., Sura, S., Butterworth, K.G., Cubitt, K.F., PlantalechManel-la, N., Balfry, S., Økland, F., and McKinley, R.S. 2008.Riverine, estuarine and marine migratory behaviour and physiologyof wild and hatchery-reared coho salmon Oncorhynchus kisutch(Walbaum) smolts descending the Campbell River, BC, Can-ada. J. Fish Biol. 72(3): 614 – 628. doi:10.1111/j.1095-8649.2007.01729.x.

Dickhoff, W.W., Beckman, B.R., Larsen, D.A., Duan, C., andMoriyama, S. 1997. The role of growth in endocrine regulation ofsalmon smoltification. Fish Physiol. Biochem. 17(1/6): 231–236.doi:10.1023/A:1007710308765.

Duston, J., Astatkie, T., and MacIsaac, P.F. 2005. Genetic influenceof parr versus anadromous sires on the life histories of Atlanticsalmon (Salmo salar). Can. J. Fish. Aquat. Sci. 62(9): 2067–2075.doi:10.1139/f05-120.

Vainikka et al. 1991

Published by NRC Research Press

Can

. J. F

ish.

Aqu

at. S

ci. D

ownl

oade

d fr

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.nrc

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of

Eas

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on

04/2

4/13

For

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use

onl

y.

Elliott, J.M., and Hurley, M.A. 1997. A functional model for maxi-mum growth of Atlantic Salmon parr, Salmo salar, from twopopulations in northwest England. Funct. Ecol. 11(5): 592–603.doi:10.1046/j.1365-2435.1997.00130.x.

Elson, P.F. 1957. The importance of size in the change from parr tosmolt in Atlantic salmon. Can. J. Fish Cult. 21: 1–6.

Fängstam, H., Berglund, I., Sjöberg, M., and Lundqvist, H. 1993.Effect of size and early sexual maturity on downstream migrationduring smolting in Baltic salmon (Salmo salar). J. Fish Biol. 43:517–529.

Forseth, T., Nesje, T.F., Jonsson, B., and Hårsaker, K. 1999. Juvenilemigration in brown trout: a consequence of energetic state.J. Anim. Ecol. 68(4): 783–793. doi:10.1046/j.1365-2656.1999.00329.x.

Gjerde, B. 1984. Response to individual selection for age at sexualmaturity in Atlantic salmon. Aquaculture, 38(3): 229–240. doi:10.1016/0044-8486(84)90147-9.

Greenberg, L.A., and Giller, P.S. 2000. The potential of flat-bedpassive integrated transponder antennae for studying habitat use bystream fishes. Ecol. Freshw. Fish, 9(1–2): 74–80. doi:10.1034/j.1600-0633.2000.90108.x.

Greenstreet, S.P.R. 1992. Migration of hatchery reared juvenile At-lantic salmon, Salmo salar L., smolts down a release ladder.1. Environmental effects on migratory activity. J. Fish Biol. 40(5):655–666. doi:10.1111/j.1095-8649.1992.tb02614.x.

Gross, M.R., Coleman, R.M., and McDowall, R.M. 1988. Aquaticproductivity and the evolution of diadromous fish migration. Sci-ence, 239(4845): 1291–1293. doi:10.1126/science.239.4845.1291.PMID:17833216.

Hutchings, J.A., and Jones, M.E.B. 1998. Life history variation andgrowth rate thresholds for maturity in Atlantic salmon, Salmosalar. Can. J. Fish. Aquat. Sci. 55(S1): 22–47. doi:10.1139/d98-004.

Huusko, A., and Hyvärinen, P. 2012. Atlantic salmon abundance andsize track climate regimes in the Baltic Sea. Boreal Environ. Res.17: 139–149.

Janhunen, M., Kekäläinen, J., Kortet, R., Hyvärinen, P., and Piironen,J. 2011. No evidence for an indirect benefit from female matepreference in Arctic charr Salvelinus alpinus, but female ornamen-tation decreases offspring viability. Biol. J. Linn. Soc. 103(3):602–611. doi:10.1111/j.1095-8312.2011.01659.x.

Johnson, S.L., Power, J.H., Wilson, D.R., and Ray, J. 2010. Acomparison of the survival and migratory behavior of hatchery-reared and naturally reared steelhead smolts in the Alsea River andestuary, Oregon, using acoustic telemetry. N. Am. J. Fish. Manage.30(1): 55–71. doi:10.1577/M08-224.1.

Jokikokko, E., Kallio-Nyberg, I., Saloniemi, I., and Jutila, E. 2006.The survival of semi-wild, wild and hatchery-reared Atlanticsalmon smolts of the Simojoki River in the Baltic Sea. J. Fish Biol.68(2): 430–442. doi:10.1111/j.0022-1112.2006.00892.x.

Jonsson, B., and Jonsson, N. 1993. Partial migration: niche shiftversus sexual maturation in fishes. Rev. Fish Biol. Fish. 3(4):348–365. doi:10.1007/BF00043384.

Kallio-Nyberg, I., Salminen, M., Saloniemi, I., and Kannala-Fisk, L.2009. Marine survival of reared Atlantic salmon in the Baltic Sea:the effect of smolt traits and annual factors. Fish. Res. 96(2–3):289–295. doi:10.1016/j.fishres.2008.12.009.

Kallio-Nyberg, I., Salminen, M., Saloniemi, I., and Lindroos, M.2011a. Effects of marine survival, precocity and other life historytraits on the cost–benefit of stocking salmon in the Baltic Sea.Fish. Res. 110(1): 111–119. doi:10.1016/j.fishres.2011.03.019.

Kallio-Nyberg, I., Saloniemi, I., Jutila, E., and Jokikokko, E. 2011b.Effect of hatchery rearing and environmental factors on thesurvival, growth and migration of Atlantic salmon in the BalticSea. Fish. Res. 109(2–3): 285–294. doi:10.1016/j.fishres.2011.02.015.

Kekäläinen, J., Niva, T., and Huuskonen, H. 2008. Pike predation onhatchery-reared Atlantic salmon smolts in a northern Baltic river.Ecol. Freshw. Fish, 17(1): 100–109. doi:10.1111/j.1600-0633.2007.00263.x.

Klemetsen, A., Amundsen, P.-A., Dempson, J.B., Jonsson, B.,Jonsson, N., O’Connell, M.F., and Mortensen, E. 2003. Atlanticsalmon Salmo salar L., brown trout Salmo trutta L., and Arcticcharr Salvelinus alpinus (L.): a review of aspects of their lifehistories. Ecol. Freshw. Fish, 12(1): 1–59. doi:10.1034/j.1600-0633.2003.00010.x.

Lacroix, G.L. 2008. Influence of origin on migration and survival ofAtlantic salmon (Salmo salar) in the Bay of Fundy, Canada. Can.J. Fish. Aquat. Sci. 65(9): 2063–2079. doi:10.1139/F08-119.

Lans, L., Greenberg, L.A., Karlsson, J., Calles, O., Schmitz, M., andBergman, E. 2011. The effects of ration size on migration byhatchery-raised Atlantic salmon (Salmo salar) and brown trout(Salmo trutta). Ecol. Freshw. Fish, 20(4): 548–557. doi:10.1111/j.1600-0633.2011.00503.x.

Larsson, S., Serrano, I., Eriksson, L.-O., and Fleming, I. 2012. Effectsof muscle lipid concentration on wild and hatchery brown trout(Salmo trutta) smolt migration. Can. J. Fish. Aquat. Sci. 69(1):1–12. doi:10.1139/f2011-128.

Latremouille, D.N. 2003. Fin erosion in aquaculture and naturalenvironments. Rev. Fish. Sci. 11(4): 315–335. doi:10.1080/10641260390255745.

Lundqvist, H., Clarke, W.C., and Johansson, H. 1988. The influenceof precocious sexual maturation on survival to adulthood of riverstocked Baltic salmon, Salmo salar, smolts. Ecography, 11(1):60–69. doi:10.1111/j.1600-0587.1988.tb00781.x.

Marschall, E.A., Quinn, T.P., Roff, D.A., Hutchings, J.A., Metcalfe,N.B., Bakke, T.A., Saunders, R.L., and Poff, N.L. 1998. A frame-work for understanding Atlantic salmon (Salmo salar) life history.Can. J. Fish. Aquat. Sci. 55(S1): 48–58. doi:10.1139/d98-007.

McCormick, S.D., Hansen, L.P., Quinn, T.P., and Saunders, R.L.1998. Movement, migration, and smolting of Atlantic salmon(Salmo salar). Can. J. Fish. Aquat. Sci. 55(S1): 77–92. doi:10.1139/d98-011.

McKinnell, S.M., and Karlström, Ö. 1999. Spatial and temporalcovariation in the recruitment and abundance of Atlantic salmonpopulations in the Baltic Sea. ICES J. Mar. Sci. 56(4): 433–443.doi:10.1006/jmsc.1999.0456.

Metcalfe, N.B., and Thorpe, J.E. 1990. Determinants of geographicalvariation in the age of seaward-migrating salmon, Salmo salar.J. Anim. Ecol. 59(1): 135–145. doi:10.2307/5163.

Morgan, I.J., and Metcalfe, N.B. 2001. Deferred costs of compensa-tory growth after autumnal food shortage in juvenile salmon. Proc.R. Soc. London B Biol. Sci. 268(1464): 295–301. doi:10.1098/rspb.2000.1365. PMID:11217901.

Myers, R.A., Hutchings, J.A., and Gibson, R.J. 1986. Variation inmale parr maturation within and among populations of Atlanticsalmon, Salmo salar. Can. J. Fish. Aquat. Sci. 43(6): 1242–1248.doi:10.1139/f86-154.

Olsson, I.C., Greenberg, L.A., Bergman, E., and Wysujack, K. 2006.Environmentally induced migration: the importance of food.Ecol. Lett. 9(6): 645–651. doi:10.1111/j.1461-0248.2006.00909.x.PMID:16706909.

1992 Can. J. Fish. Aquat. Sci. Vol. 69, 2012

Published by NRC Research Press

Can

. J. F

ish.

Aqu

at. S

ci. D

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nive

rsity

of

Eas

tern

Fin

land

on

04/2

4/13

For

pers

onal

use

onl

y.

Ostrovsky, I. 1995. The parabolic pattern of animal growth: deter-mination of equation parameters and their temperature depen-dencies. Freshw. Biol. 33(3): 357–371. doi:10.1111/j.1365-2427.1995.tb00398.x.

Parrish, D.L., Behnke, R.J., Gephard, S.R., McCormick, S.D., and Reeves,G.H. 1998. Why aren’t there more Atlantic salmon (Salmo salar)?Can. J. Fish. Aquat. Sci. 55(S1): 281–287. doi:10.1139/d98-012.

Pirhonen, J., and Forsman, L. 1998. Effect of prolonged feed restric-tion on size variation, feed consumption, body composition,growth and smolting of brown trout, Salmo trutta. Aquaculture,162(3–4): 203–217. doi:10.1016/S0044-8486(98)00215-4.

Pirhonen, J., and Forsman, L. 1999. Can smolting and maturation ofhatchery-reared brown trout Salmo trutta L. be affected by fooddeprivation during the first and second years of rearing? Aquacult.Res. 30(8): 611–620. doi:10.1046/j.1365-2109.1999.00380.x.

Romakkaniemi, A. 2008. Conservation of Atlantic salmon by sup-plementary stocking of juvenile fish. Ph.D. thesis, University ofHelsinki, Helsinki, Finland.

Rowe, D.K., and Thorpe, J.E. 1990. Suppression of maturation inmale Atlantic salmon (Salmo salar L.) parr by manipulation offeeding and growth in spring months. Aquaculture, 86: 291–313.doi:10.1016/0044-8486(90)90121-3.

Rowe, D.K., Thorpe, J.E., and Shanks, A.M. 1991. Role of fat storesin the maturation of male Atlantic salmon (Salmo salar) parr. Can.J. Fish. Aquat. Sci. 48(3): 405–413. doi:10.1139/f91-052.

Ruohonen, K. 1998. Individual measurements and nested designs inaquaculture experiments: a simulation study. Aquaculture, 165(1–2): 149–157. doi:10.1016/S0044-8486(98)00252-X.

Shrimpton, J.M., and McCormick, S.D. 2002. Seasonal changes inandrogen levels in stream- and hatchery-reared Atlantic salmonparr and their relationship to smolting. J. Fish Biol. 61(5): 1294–1304. doi:10.1111/j.1095-8649.2002.tb02472.x.

Tacon, A.G.J., and Metian, M. 2008. Global overview on the use offish meal and fish oil in industrially compounded aquafeeds: trendsand future prospects. Aquaculture, 285(1–4): 146–158. doi:10.1016/j.aquaculture.2008.08.015.

Thériault, V., and Dodson, J.J. 2003. Body size and the adoption ofa migratory tactic in brook charr. J. Fish Biol. 63(5): 1144–1159.doi:10.1046/j.1095-8649.2003.00233.x.

Thorpe, J.E. 1994a. Reproductive strategies in Atlantic salmon,Salmo salar L. Aquacult. Fish. Manage. 25: 77–87.

Thorpe, J.E. 1994b. An alternative view of smolting in salmonids.Aquaculture, 121(1–3): 105–113. doi:10.1016/0044-8486(94)90012-4.

Thorpe, J.E., Morgan, R.I.G., Ottaway, E.M., and Miles, M.S. 1980.Time of divergence of growth groups between potential 1� and2� smolts among siblings Atlantic salmon. J. Fish Biol. 17(1):13–21. doi:10.1111/j.1095-8649.1980.tb02738.x.

Thorpe, J.E., Mangel, M., Metcalfe, N.B., and Huntingford, F.A.1998. Modelling the proximate basis of salmonid life-history vari-ation, with application to Atlantic salmon, Salmo salar L. Evol.Ecol. 12(5): 581–599. doi:10.1023/A:1022351814644.

Vainikka, A., Kallio-Nyberg, I., Heino, M., and Koljonen, M.-L.2010. Divergent trends in life-history traits between Atlanticsalmon, Salmo salar of wild and hatchery origin in the Baltic Sea.J. Fish Biol. 76(3): 622–640. doi:10.1111/j.1095-8649.2009.02520.x. PMID:20666901.

Wysujack, K., Greenberg, L.A., Bergman, E., and Olsson, I.C. 2009.The role of the environment in partial migration: food availabilityaffects the adoption of a migratory tactic in brown trout Salmotrutta. Ecol. Freshw. Fish, 18(1): 52–59. doi:10.1111/j.1600-0633.2008.00322.x.

Vainikka et al. 1993

Published by NRC Research Press

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