consumption of juvenile brown trout in a Norwegian stream\ and the energy budgets of early migrants .... "Francis 0889#[ This procedure may overestimate the.
Journal of Animal Ecology 0888\ 57\ 672Ð682
Juvenile migration in brown trout] a consequence of energetic state TORBJO RN FORSETH\ TOR F[ N $SJE\ BROR JONSSON and KARSTEIN HA ý RSAKER Norwegian Institute of Nature Research\ Tungasletta 1\ N!6374 Trondheim\ Norway^ and Norwegian Institute of Nature Research\ Dronningensgt[ 02\ PO Box 625 Sentrum\ N!9094 Oslo\ Norway
Summary 0[ We explored the mechanisms determining age and size at juvenile migration in brown trout Salmo trutta L[ A 022Cs tracer methodology was used to estimate food consumption of juvenile brown trout in a Norwegian stream\ and the energy budgets of early migrants and stream residents were compared[ 1[ Fast!growing brown trout migrated to the lake earlier and at a smaller body size than slower!growing individuals[ The 1¦ migrants were signi_cantly larger than those that remained 0 or more years longer in the stream[ The 2¦ migrants were signi_cantly larger than the 1¦ migrants[ Some fast!growing males matured in the stream\ whereas all females left the stream before maturing sexually[ 2[ The food consumption and the energy budgets for 1¦ migrants were more than four times higher than those of the resident 1¦ _sh[ Total energy allocated to growth was also higher among migrants\ and the total metabolic costs were _ve times higher among migrants than among resident _sh[ 3[ The proportional energy allocation to growth among the 1¦ migrants was much lower "about half# than that of those remaining longer in the stream[ The reduction in the proportion of energy available for growth from age 0¦ to 1¦ was larger among migrants "77)# than among resident _sh "57)#[ Reduction in the proportion of energy available for growth is a probable explanation for why migrations are initiated at age 1[ 4[ Our study supports the hypothesis that fast!growing individuals shift their niche earlier and at a smaller body size than slower!growing individuals because they maintain higher metabolic rates and are energetically constrained at a younger age by limited food resources than slow growers[ Key!words] energy budget\ food consumption\ growth\ life history\ metabolic rate[ Journal of Animal Ecology "0888# 57\ 672Ð682
Introduction Many animals perform extensive niche shifts because their ability to utilize resources and avoid predation changes through their ontogeny "Werner + Gilliam 0873^ L|Abee!Lund et al[ 0882#[ While the ultimate causes of niche shifts are obvious\ the maximization of _tness\ the proximate mechanisms controlling the
Þ 0888 British Ecological Society
Correspondence] Dr Torbjo rn Forseth\ Norwegian Insti! tute of Nature Research\ Tungasletta 1\ N!6374 Trondheim\ Norway[ Tel[ ¦ 36 62790386^ Fax] ¦ 36 62790390^ E!mail] torbjorn[forsethÝninatrd[ninaniku[no
shifts are under debate[ The timing of niche shifts has been related to body size "e[g[ Werner 0868^ Grossman 0879^ Persson 0872^ Werner + Gilliam 0873^ Sand! lund\ N%sje + Jonsson 0881^ Bohlin\ Dellefors + Far! emo 0885#\ growth rate "e[g[ Werner + Gilliam 0873^ Thorpe\ Metcalfe + Huntingford 0881^ O kland et al[ 0882^ Forseth\ Ugedal + Jonsson 0883#\ the ratio between growth rate and mortality "Werner + Gilliam 0873# and metabolic rate "e[g[ Metcalfe\ Wright + Thorpe 0881^ Forseth et al[ 0883^ Metcalfe\ Taylor + Thorpe 0884#[ These studies show that although body size is an important aspect of niche shifts\ the timing of the shifts is probably related both to developmental 672
673 Juvenile migrations and energetics
Þ 0888 British Ecological Society Journal of Animal Ecology\ 57\ 672Ð682
rates and to the physiological state of the animals[ Environmental cues inducing the niche shifts may be changes in food availability "e[g[ Langeland et al[ 0880^ N%sje et al[ 0880^ Sandlund et al[ 0881# or other environmental factors like a change in water tem! perature "e[g[ Forsythe 0857^ Jonsson + Ruud! Hansen 0874^ Hvidsten et al[ 0884#[ Among _shes\ ontogenetic changes in resource use are nearly universal "Werner + Gilliam 0873#[ One classic example is the salmonids that migrate as juv! eniles from nursery streams to lakes or the ocean where they feed until they mature and return to spawn in their stream of origin[ Gross "0876# developed a migration model for understanding the evolution of such strategies[ According to this model\ _shes migrate if the growth and survivorship advantages of utilizing a second habitat\ plus the cost of moving between the habitats\ exceed the advantages of staying in only one habitat for the same period of time[ However\ all individuals in a population do not always migrate "Jonsson + Jonsson 0882#\ and migrations may occur at di}erent age and size "Jonsson\ Jonsson + Hansen 0889#\ probably because growth and sur! vivorship in di}erent habitats may vary with body size "e[g[ size!dependent feeding opportunities\ growth rates and mortality risk#[ During the last decade\ _eld and experimental studies have provided important knowledge of the mechanisms determining age and size at migration\ particularly for anadromous sal! monids[ One general pattern is that fast!growing indi! viduals smolt "i[e[ the physiological\ morphological and behavioural transformation of juvenile salmonids in preparation for life at sea# younger "Jonsson 0874^ Thorpe 0876a\b^ Metcalfe et al[ 0878# and at a smaller body size "Jonsson 0874^ O kland et al[ 0882# than more slow!growing individuals[ Smolt size is pheno! typically plastic and related to individual growth rates as a norm of reaction "sensu Stearns 0881#[ O kland et al[ "0882# hypothesized that fast!growing indi! viduals smolt earlier because they maintain higher metabolic rates and are energetically constrained earl! ier than slow growers by limited food resources[ A recent experimental study may support this hypoth! esis[ Metcalfe et al[ "0884# demonstrated a strong relationship between social status and standard meta! bolic rate in juvenile Atlantic salmon "the higher the standard metabolic rate\ the more dominant the _sh#\ and they suggested an indirect link between intra! speci_c variation in metabolic rates and life!history strategies[ Moreover\ from experimental dominance studies\ Huntingford et al[ "0889# suggested that the larger size of dominant _sh\ reported for a number of salmonids\ might be a consequence and not a cause of high status[ A possible conclusion from these studies is that some individuals are born with a higher standard metabolic rate\ or attain a higher rate shortly after hatching\ than other individuals from the same popu! lation[ This may in~uence their future growth and life history\ including niche shifts[ This also accords with
the predictions from a new model\ developed by Thorpe et al[ "0887#\ that life!history events in sal! monids are triggered by a combination of physio! logical state "e[g[ lipid content or body mass# and the rate of change of state[ In the present study\ we explored the hypothesis that fast!growing individuals shift their niche earlier and at a smaller body size than slower!growing indi! viduals because they maintain higher metabolic rates and are energetically constrained earlier than slow growers by limited food resources[ Energy budgets of juvenile brown trout "Salmo trutta L[# that migrated from a small study stream to a lake were compared with individuals that remained in the stream[ Our prediction was that at the year of migration\ the rela! tive proportion of the available energy for growth should be lower for migratory than for resident indi! viduals\ as the migrants have higher metabolic rates[ The life history of brown trout in this watercourse is similar to the life history of many anadromous salmonids[
Methods STUDY AREA AND SAMPLING
Juvenile brown trout were sampled in Litjaa\ a small spawning and nursery stream of large piscivorous brown trout in the Lake Femund "51 >N 01 >E\ 551 m a[s[l[#\ the second largest "193 km1# natural lake in Norway[ The average summer water discharge in Litjaa is 9=4 m2 sÐ0 "lower parts# and average maximum discharge during spring ~ood is ¼ 4 m2 sÐ0[ Brown trout is the only _sh species that spawn in the stream\ but during summer minnows "Phoxinus phoxinus L[# occasionally enter the river to feed for shorter periods[ In addition\ the Lake Femund supports populations of white_sh "Coregonus lavaretus L[#\ pike "Esox lucius L[#\ perch "Perca ~uviatilis L[#\ grayling "Thymallus thymallus L[# and burbot "Lota lota L[#[ Pike\ perch\ burbot and adult brown trout are predators on juv! enile brown trout[ In Litjaa a _sh!trap 49 m upstream from the outlet into the lake caught all ascending and descending _sh "including 9¦#[ A second trap\ ¼ 1=4 km upstream\ caught only descending _sh and ensured no immi! gration into the study area[ The traps were operational from early June\ shortly after the spring ~ood\ until late September and were monitored twice a day[ All descending _sh were sampled for further analysis\ whereas ascending _sh were measured "total length in cm#\ marked "by _n clipping# and released above the trap[ Migrations may also occur during the spring ~ood before the trap was operational[ Migration dur! ing spring ~ood is common among salmonids\ but is not obligatory "review in Jonsson 0880#[ In this work only summer migration is addressed[ About one!third of the study section is slow!~owing and meandering\
674 T[ Forseth et al[
whereas the remaining two!thirds are more rapid! ~owing[ Temperatures were recorded every 3 h by temperature loggers in the lower parts of the stream[ Water discharge was recorded twice a day in the same area[ Brown trout were sampled by electro_shing in four periods "12 June\ 01 July\ 00 August and 4 September 0884#[ The whole area was sampled on 12 June\ whereas only the rapid!~owing parts and smaller sub! sections of the slow!~owing meandering parts were _shed at the other samplings[ Very few _shes\ and mainly older and larger adults\ were caught in the slow!~owing meandering parts[ At each sampling\ the aim was to collect a minimum of 19 individuals from each of _ve year classes "9¦ \ 0¦ \ 1¦ \ 2¦ and 3¦#[ This was accomplished on most occasions\ with the main exception of 3¦ which occurred in low densities in the stream[ In addition\ some older _sh were caught "4 and 5¦#[ Each _sh was weighed "nearest 9=90 g#\ total length "mm# measured\ and aged by use of sacculus otoliths[ The stomachs were removed and deep frozen[ To com! pare growth of individuals caught by electro_shing and the descending migrants caught in the lower trap\ length at earlier ages was back!calculated by use of otoliths "Jonsson + Stenseth 0866#[ Back!calculation was done by direct proportion\ i[e[ DahlÐLea method "Francis 0889#[ This procedure may overestimate the lengths at age Ð 0\ but the relationship between the groups should not be altered[
FOOD CONSUMPTION ESTIMATES
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Food consumption was estimated by a tracer method "Forseth et al[ 0881#\ using stable caesium "022Cs#[ Cae! sium is naturally occurring in very low concentrations\ not feasible for ordinary quantitative analyses[ Although radioactive caesium has been globally dis! persed through fallout from nuclear bomb tests and accidents "Chernobyl#\ the concentration is often too low for quanti_cation[ We thus added a total of 5 kg of stable caesium chloride to the stream[ Five kg of caesium salt were dissolved in 399 L of stream water and slowly released 49 m above the upper trap during a 49!h period from 12 to 14 June 0884[ Another kg of caesium\ dissolved in 099 L water\ was released in the lower one!third of the stream "just below the meander! ing section# during the following day[ The estimation of food consumption is based upon estimating the intake of caesium from an observed change in caesium body burden with time[ The rates of assimilation and elimination are known "Forseth et al[ 0881^ Ugedal et al[ 0881#\ and the food con! sumption is obtained by dividing the caesium intake by the caesium concentration in the food[ Daily food rations "Di mg dry mass "dw## were estimated by the tracer method according to Forseth et al[ "0881# with a two!component caesium elimination]
Ii 9[84 =
Qi¦0−Qi = e−kli 0−e−kli
= k0i
¦9=94 =
Qi¦0−Qi = e−k1i 0−e−k1i
= k1i
eqn 0
and Di
Ii Sbij = Ci = fij
eqn 1
where Ii is daily caesium intake "mg#\ Qi and Qi¦0 are caesium body burdens "mg kgÐ0# in _sh at times i and i ¦ 0\ respectively\ given by Q C_Wi where C_ is caesium concentration "mg kgÐ0# and Wi is _sh mass "g#\ k0i and k1i are the rate constants for slow and fast elimination "dayÐ0#\ respectively\ bij is the assimilation of caesium from the jth prey item\ Ci is the caesium concentration in the prey items "mg kgÐ0# and fij is the proportion of the jth prey item in the diet of trout[ Fish that receive an acute oral caesium dose generally show two!component elimination curves "Kevern 0855^ Gallegos + Whicker 0860#[ According to exper! imental data on brown trout "Ugedal et al[ 0881#\ ¼ 19) of the caesium body burden is eliminated fast and 79) slowly when the _sh is given a single dose of caesium[ Under conditions of a continuous intake of caesium\ the importance of the short!lived component gradually decreases "Kolehmainen 0863^ Forseth et al[ 0881#[ The food consumption estimates in the present study were done from 2 to 00 weeks after caesium was added to the stream[ We thus predicted "Ugedal et al[ 0881# that 84) of the caesium body burden was elim! inated slowly and 4) fast\ and used elimination rates estimated by the equations for brown trout given by Ugedal et al[ "0881#[ Calculations were made step! wise\ with separate variable values for each successive day\ because eqn 0 is valid only if elimination "k# and intake "I# are constant during the period under con! sideration[ Elimination is a function of both _sh mass and ambient temperature "Ugedal et al[ 0881#\ and intake varies seasonally[ However\ both k and I were assumed to be constant within a day[ At present\ it is not possible to calculate the statistical precision of food consumption estimates by the Cs tracer method when the estimates are based on average input!values from groups of _sh rather than individuals[ The proportion of each of the prey categories "sur! face insects\ Eurycercus lamellatus\ chironomid zoo! benthos and other zoobenthos# was determined through analysis of stomach contents[ Assimilation data from laboratory brown trout were available "Forseth et al[ 0881#[ The caesium concentration was measured in individual _sh and pooled samples of stomach content from each age class and sampling date[ This was done by instrumental neutron acti! vation analysis "INAA#\ i[e[ by irridation of the samples\ activation of 022Cs to radioactive 023Cs and gamma spectrometry[ Daily values for _sh mass and caesium con!
675 Juvenile migrations and energetics
centrations in _sh and stomach contents were cal! culated from linear interpolations between the geo! metric mean values determined for subsequent sampling dates[ Daily temperatures were calculated from a Gaussian curve _tted to observations "Forseth et al[ 0881#[ The curve _t smooths the day!to!day vari! ation in temperature[ Food consumption was estimated for the age classes 9¦ to 3¦ from 01 July to 4 September 0884[ In addition\ consumption was estimated for descending 1¦ brown trout caught in the lower trap between 18 August and 03 September\ during a peak in the 1¦ migration[ Because we were not able to di}erentiate between migrating brown trout and those that remained in the stream before the _sh actually started to move downstream\ body mass and caesium con! centration in July were not available for these _sh[ Thus\ body mass at the start of the growth season "set at 0 June when temperatures exceeded 3 >C# was back! calculated from otoliths\ and mass on 01 July was estimated from forward linear extrapolation[ Two methods were used to estimate the caesium level for 1¦ migrants on 01 July[ First\ we used the average of nine _sh with the highest caesium concentration "upper one!third# of 17 _sh sampled during elec! tro_shing on 01 July[ Second\ we used a linear regression of the caesium concentration in 1¦ brown trout caught in the trap and the day number on which they were caught[ This analysis also included 1¦ _sh that migrated before the peak migration in September[ The latter method gave concentrations twice as high as the _rst\ and we compared the estimated food con! sumption using these two values to evaluate the sen! sitivity of the estimates to variation in caesium con! centration at the start date[
ENERGY BUDGETS
The balanced energy budget of _shes is given by] C P¦R¦F¦U
Þ 0888 British Ecological Society Journal of Animal Ecology\ 57\ 672Ð682
eqn 2
where C is the total energy in the food consumed\ P is the energy in production "somatic and gonadal growth#\ R is the total energy of metabolism\ F is the energy of the faeces and U is the energy of the excret! ory products[ The total metabolism "R# is usually div! ided into three components] the metabolic cost of "i# maintaining the physiological state "maintenance metabolism\ Rs#\ "ii# swimming "activity metabolism\ Ra#\ and "iii# digesting and assimilating food "speci_c dynamic action\ Rf#[ The energy in the food consumed "C# was calculated as the product of the mass of food consumed from 01 July to 4 September and the energy in the prey animals "stomach content#[ Similarly\ the energy of production "P# was calculated as the product of the mass gain during the period and the energy of _sh body mass[ The energy in the stomach content and _sh body mass was estimated by determining the proportions of dry
matter\ ash\ fat and protein\ and multiplying the fat and protein proportions by energy conversion factors "Bra_eld + Llewellyn 0871^ Jobling 0872#[ Individual _shes within each age class and sampling date were pooled in these analyses[ The stomach contents were analysed for each age class but stomachs from di}er! ent samplings were pooled because the variation was larger among age classes than among samplings[ Ascending _sh caught in the trap were analysed sep! arately[ The proportion of energy intake lost in faeces "F# and excretory products "U# was estimated from the equations given for brown trout by Elliott "0865# with data on _sh mass\ ambient temperature and food con! sumption for brown trout from Litjaa[ Finally\ meta! bolic costs "R# were estimated from R C Ð "F ¦ U# Ð P[
Results A diverse pattern of downward movements of juvenile brown trout was observed "Fig[ 0#[ Shortly after emergence from the gravel some 9¦ brown trout were caught in the lower trap[ These were among the smal! lest individuals from that cohort "trap 08 mm\ stream 14 mm#\ presumably displaced by high water dis! charge or unable to establish territories in the stream[ A few 0¦ brown trout were also caught in the trap during the season[ These individuals were smaller\ albeit not signi_cantly "t Ð 0=07\ P × 9=94#\ than those that remained in the stream "2=1 and 2=8 g\ respectively#[ The 1! and 2!year!old trout dominated in catches in the lower trap[ Descending 1¦ brown trout caught in the trap between 18 August and 03 September\ during a peak in the migration\ were sig! ni_cantly larger "t 2=01\ P ³ 9=90# than those caught in the stream during electo_shing on 4 Sep! tember "09=8 and 7=9 g\ respectively#[ Back cal! culations of lengths showed that descending 1¦ trout had always been larger than those that remained in the stream\ and that the di}erence was signi_cant from the beginning of their second summer "F 3=08\ P ³ 9=94#[ Among 2!year!olds no such size di}erence was found "t 9=18\ P × 9=94#[ Descending 2¦ indi! viduals were signi_cantly "t Ð 1=85\ P ³ 9=90# larger than descending 1¦ "06=1 and 09=8 g\ respectively#[ We also compared the size of di}erent aged brown trout with those in the Lake Femund "T[F[ N%sje\ unpublished data#[ Asymptotic lengths "2 SE#\ esti! mated by curve _tting to a von Bertalan}y "0827# growth model\ were 040=7 "02=3# and 445=5 "20=2# mm\ respectively[ Thus\ the average maximum size in the lake is 2=6 times that in the stream[ Some of the _sh caught in the Lake Femund may belong to other populations as there are at least two other tributaries near Litjaa where brown trout spawn[ The majority of the adults that returned for spawning in Litjaa during 0884 "caught in the trap# were between 159 and 399 mm long\ with a maximum at 379 mm[
676 T[ Forseth et al[
Fig[ 0[ Juvenile migration pattern in Litjaa] A ~ow diagram indicating the proportion of individuals at di}erent ages "0Ð4¦# that migrate from the stream to Lake Femund[ Small and Large indicate that migrating individuals are smaller or larger than those that remain in the stream[ Shading denotes sexually mature males[
No sexually mature females were caught during electro_shing in the stream[ Thus\ all females appeared to leave the stream to feed in the lake[ A few 2 \ 39) of the 3¦ and all 4¦ males caught in the stream were sexually mature[ The two mature males caught during electro_shing in September were the largest individuals at that sampling[ Back!calculations showed that mature 2¦ males "four individuals# were signi_cantly larger "MÐW] Z Ð 0=84\ P 9=94^ t Ð 1=70 P ³ 9=90# than immatures "n 15# at the start of the growth season[ No such size di}erence was found among 3! and 4!year!old males[ The estimated daily food rations varied between periods and among age classes of brown trout "Table 0#[ The daily rations were generally higher dur!
ing the _rst period from 01 July to 00 August than the second from 00 August to 4 September[ Mass speci_c daily rations were highest for 9¦[ The daily rations for 0¦ were less than one!third of the rations for 9¦[ Thereafter\ the estimated daily rations in the _rst period declined gradually with age[ During the second period daily rations _rst increased from age 0¦ to 1¦ and then declined from age 2¦ to 3¦ [ As expected from the weight increment the absolute rations increased by age[ The estimated daily food rations were generally similar to maximum food rations for brown trout predicted from the average _sh mass and ambient temperatures by the model of Elliott "0864a\b#\ with an average ratio "all age classes and both periods# between observed and maximum
Table 0[ Mean body mass "M g\2 84) C[L[#\ ambient temperature "T>C#\ speci_c growth rate "Gw percentage\ 2 84) C[L[#\ mass speci_c "D mg dw g fw# and absolute daily rations "Dabs mg dw# estimated for di}erent age classes of brown trout from Litjaa during two periods in 0883[ The ratios between observed and maximum growth rate "2 84) C[L[\ estimated under the assumption that the maximum growth are estimated without error#\ and between estimated and maximum weight speci_c daily rations are also tabulated[ Maximum growth of brown trout was calculated from the equations in Elliott et al[ "0884# and maximum daily rations from the equations in Elliott "0864a\b# Age
0¦ 1¦ 2¦ 3¦ 00 AugÐ4 Sep 9¦ 0¦ 1¦ 2¦ Þ 0888 British Ecological Society Journal of Animal Ecology\ 57\ 672Ð682
3¦
09=1
9=70 9=84 9=88 0=09
9=56 9=81 0=12 9=83
677 Juvenile migrations and energetics
rations of 0=01[ However\ for 9¦ brown trout the estimated daily rations were much higher than the predicted maximum rations\ particularly during the second period "ratio 1=05#[ The growth rates were\ in accordance with the daily rations\ generally higher during the _rst than the second period "Table 0#[ The growth rate declined with age and size[ The estimated growth rates were similar or slightly lower than the estimated maximum growth rate for brown trout predicted from the growth model of Elliott\ Hurley + Fryer "0884#\ with an average ratio "all age classes and both periods# between observed and maximum growth at 9=53[ On three occasions only\ the upper 84) C[L[ of this ratio were lower than 0\ indicating observed growth rates sig! ni_cantly lower than predictions[ Comparisons between daily food rations of resident and migratory 1¦ brown trout revealed large di}er! ences "Table 1#[ The estimated absolute daily ration "mg dw# for 1¦ brown trout caught in the trap during downward migration between 18 August and 03 Sep! tember "migrants# was more than four times higher than that of _sh caught during electro_shing on 4 September "resident#[ The di}erence was somewhat smaller "ratio 2=5# when comparisons were made on the basis of weight speci_c food rations "mg dw g fwÐ0#[ The estimated daily rations for migrants do not appear to be sensitive to variation in initial caesium concentration as a 099) increase in concentration caused only a 3) reduction in the estimated food ration "Table 1#[ Migratory 1¦ brown trout had only slightly higher growth rates than resident 1¦ "Table 1#\ and the di}erence was not signi_cant "overlapping 84) C[L[#[ The resident individuals grew at a maximum rate\ whereas the migratory indi! viduals had growth rates below the estimated maximum "Table 1#[ Food consumption was not estimated for migratory 2¦ brown trout and comparisons between resident and migratory individuals could not be made for this age class[ However\ major di}erences in consumption
are unlikely as they had similar body size and caesium concentrations[ The energy budgets were higher during the _rst than the second period\ and increased with age "Fig[ 1a#[ The allocation pattern di}ered among age classes but was similar in both periods[ The proportional allo! cation of energy to growth was approximately twice as high for 0¦ than for 9¦ brown trout\ and 0¦ brown trout allocated ¼ 39) of the available energy to growth "Fig[ 1b#[ The allocation to growth was much lower for 1¦ "05) during the _rst period# and for older _sh[ Migratory 1¦ brown trout had an energy budget 3=4 times higher than resident 1¦ "Fig[ 2a#\ and migrants had more energy available for growth[ How! ever\ the proportional allocation to growth was low among migrants "3=5)# compared to resident brown trout "01)# "Fig[ 2b#[ The proportion of energy lost through faeces and excretory products was similar "¼ 29)# for the two groups of _sh\ but migrants allocated a higher proportion of energy to metabolism "53)# than those that remained in the stream "46)#[ The total metabolic costs were _ve times higher among migrating than among resident 1¦[
Discussion EVALUATION OF METHODS
The use of stable caesium "022Cs# as a tracer for esti! mating brown trout food consumption appeared to be very successful[ With the exception of age!group 9¦\ the estimated daily food rations were similar to predictions from a laboratory!based model for maximum consumption "Elliott 0864a\b#[ For the smallest _sh "9¦#\ the food rations were much higher than the maximum rations[ This may be expected as Elliott "0864a\b# never used _sh this small and extrapolations from larger _sh may be invalid[ The estimated daily rations matched the general expec!
Table 1[ Mean body mass "M g\ 284) C[L#\ ambient temperature "T>C#\ mass increase "DM#\ speci_c growth rate "Gw percentage\ 284) C[L#\ mass speci_c "D mg dv = g fw# and absolute daily rations "Dabs mg dv# estimated for 1 ¦ brown trout caught during electro_shing in Litjaa 4 September 0883 "resident# and brown trout caught in a trap during downwards migration between 18 August and 03 September[ All values are given for the period between 01 July and 4 September[ Two estimates for relative daily rations are presented for migrants[ The latter value is based on initial caesium concentration in _sh twice as high as the _rst "confer method section for details#[ The ratios between observed and maximum growth rate "284) C[L\ estimated under the assumption that the maximum growth are estimated without error#\ and between estimated and maximum weight speci_c daily rations are also tabulated[ Maximum growth of brown trout was calculated from the equations in Elliott et al[ "0884# and maximum daily rations from the equations in Elliott "0864a\b#
Þ 0888 British Ecological Society Journal of Animal Ecology\ 57\ 672Ð682
M
T
DM
Gw
D
Dabs
Gw:Gwmax
D:Dmax
Migratory
8=96 "6=67Ð09=24# 5=55 "4=85Ð6=27#
00=53
3=30
43=1:41=9
332=9
00=53
1=85
9=78 "9=73Ð9=83# 9=71 "9=68Ð9=74#
03=8
099=8
9=64 "9=69Ð9=68# 9=87 "9=83Ð0=90#
Resident
678 T[ Forseth et al[
Fig[ 1[ The energy budgets from 01 July to 00 August "left panel# and 00 August to 4 September "right panel# 0884 for the age classes 9¦ to 3¦ of brown trout in Litjaa[ Total energy allocation "a# and proportional allocation "b# of energy to growth "P# and metabolism "R# and energy lost through faeces and urine "F ¦ U#[
Þ 0888 British Ecological Society Journal of Animal Ecology\ 57\ 672Ð682
tation for the e}ect of temperature\ body size and season[ Daily rations were higher during the _rst sam! pling period "JulyÐAugust# than during the second period "AugustÐSeptember#\ when temperature was 1=6 >C lower and food abundance was probably lower as\ e[g[ large insect larvae have hatched[ In accordance with expectations\ daily mass speci_c rations declined by age and body size "e[g[ Wootton 0889#[ To our knowledge\ stable caesium as a tracer element has been used to estimate food consumption in _sh on one occasion only "Hakonson\ Gallegos + Whicker 0864#[ Forseth et al[ "0881# compared estimates for brown trout food consumption based on the turnover of radioactive caesium "026Cs# from the Chernobyl fall! out\ with estimates from a well established method based on the amount of food in the stomach and the rate of gastric evacuation "Elliott 0861^ Eggers 0866#[ The estimates were very similar\ and Forseth et al[ "0881# concluded that the use of caesium as a tracer is a reliable method for estimating food consumption[ In principle\ there is no di}erence between using stable and radioactive caesium as a trace element[ The high food consumption among 1¦ migrants
and the large di}erence in consumption rate between migrants and the stream dwellers is essential to our conclusions[ As we were unable to di}erentiate between migrating brown trout and those that remained in the stream before the _sh actually started to move downstream\ we had to estimate the initial caesium concentration "on 01 July# of the migratory individuals[ However\ the estimated daily ration was essentially insensitive to variation in initial caesium concentration[ A 099) increase in concentration 0 month before the downstream migration started caused only a 3) reduction in the estimated food ration[ The main reason for the much higher food consumption among migrants than those that remained in the stream is that migrants had 0=4 times higher caesium concentration when they were caught in the trap[ The estimated food consumption for migrants was nearly four times higher than maximum consumption predicted from laboratory studies "Elli! ott 0864a\b#[ This is very high and indicates that _sh leaving the river at an age of 1 years are feeding at an exceptionally high rate\ making them energy!wise the best performing _sh in the population[
689 Juvenile migrations and energetics
Fig[ 2[ The energy budgets for migratory and stream resident 1¦ brown trout in Litjaa from 01 July to 4 September 0884[ Total energy allocation "a# and proportional allocation "b# of energy to growth "P# and metabolism "R# and energy lost through faeces and urine "F ¦ U# for 1¦ brown trout caught in a trap during downward migration between 18 August and 03 September "migrants# and _sh caught in the stream on 4 September "resident#[
EVALUATION OF HYPOTHESIS
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In accordance with our hypothesis\ fast!growing brown trout migrated earlier and at smaller body size than slower!growing individuals[ 1¦ migrants were signi_cantly larger than those that remained in the stream\ and 2¦ migrants were signi_cantly larger than 1¦ migrants[ Comparisons across cohort "i[e[ 1 and 2¦ migrants# may be questionable because cohorts may experience di}erent growth rates "for example due to variable year!class strength and den! sity!dependent growth#\ but judging from the mag! nitude of the size di}erence "2¦ being nearly twice as heavy as 1¦#\ it is obvious that the young migrants were smaller than those that migrated 0 year older[ This result appears general among migratory sal! monids as it accords with _ndings from studies on brown trout "Bohlin\ Dellefors + Faremo 0882^ Jons! son + Gravem 0874^ Jonsson 0874^ Bohlin et al[ 0885#\ Atlantic salmon "Jonsson et al[ 0889^ O kland et al[ 0882#\ sockeye salmon "Oncorhynchus nerka# "Burgner
0880# and Arctic charr "Salvelinus alpinus# "Forseth et al[ 0883#[ The food consumption and energy budgets were much higher for migratory than stream resident trout[ The absolute daily ration for 1¦ migrants was more than four times higher and the energy budget "i[e[ the energy of consumed food# 3=4 times higher than for resident 1¦ _sh[ Despite this large di}erence in food consumption\ the speci_c growth rate did not di}er signi_cantly between resident and migratory indi! viduals[ However\ the total energy allocated to growth\ and thus their mass increase\ was higher among migrants[ Moreover\ the total metabolic costs were _ve times higher among migrants than among resident _sh[ In the present study\ it was impossible to di}erentiate between the di}erent components of metabolic costs[ A large proportion of the estimated di}erence can probably be explained by the higher costs of digesting and assimilating "speci_c dynamic action\ Rf in eqn 2# a much larger amount of food for migratory than resident _sh[ However\ as the di}er! ences in metabolic costs between the two groups were larger than the di}erences in energy accumulated through food\ the hypothesis of higher standard meta! bolic rates among early migrants of Atlantic salmon "O kland et al[ 0882^ Metcalfe et al[ 0884# is given some support[ An alternative explanation is that migrants have higher activity costs than those that remained in the stream[ The distribution of metabolic cost among the components is\ however\ not essential to the con! clusions in the present study[ Although the total energy allocated to growth and the mass increase was higher among migrants\ their proportional allocation to growth was much lower than that of resident _sh "about half#[ All 1¦ brown trout had lower proportional allocation to growth than 0¦ _sh\ but the reduction was larger among migrants "77)# than among resident _sh "57)#[ A reduction in the proportional energy available for growth is a likely explanation for why migration is initiated at age 1[ Moreover\ it may explain why some individuals\ those with higher metabolic rates\ migrate earlier than others[ They experience a larger drop in their proportional energy available for growth and seek alternative actions\ such as migrating to an alter! native feeding niche\ to maintain their status as fast growers[ Slower!growing individuals experience a smaller drop in proportional energy available for growth and remain in the stream for one more year[ Most 2¦ individuals migrate to the lake\ but some of the largest males mature sexually and remain in the stream[ Migratory costs for juveniles in Litjaa can probably be neglected as the migrations are short and no change in salinity occurs[ Thus\ the optimal time for migration is the one that maximizes the ratio between the growth bene_t of changing habitat and the costs of increased mortality after migration[ Post!migration mortality of salmonids is often assumed to be nega!
680 T[ Forseth et al[
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tively size!dependent because predation is size!depen! dent^ small migrants are susceptible to a higher num! ber of predatory species and a wider size range of predators than larger ones "Bohlin et al[ 0882\ 0885#[ As young migrants are smaller than older migrants\ early migration is more risky than late migration[ Brown trout cannot\ prior to migration\ measure the growth they will attain in a new habitat[ To opti! mize the time of migration\ individuals thus have to respond to some change in conditions in their present habitat[ The underlying mechanism which supports the {decision| to migrate is assumed to be related to growth rate\ or a physiological process like metabolic rate which is correlated with growth rate "Jonsson + Jonsson 0882#[ Brown trout from Litjaa experienced a relatively large drop in growth rate from age 0¦ to 1¦ \ but migrants maintained as high growth rates in the summer of migration as resident _sh[ Thus\ the growth rate per se cannot explain why some indi! viduals migrate earlier than others[ However\ their relative allocation to growth declined signi_cantly "from age 0¦ to 1¦#\ and young migrants experi! enced a larger drop than older ones[ Thus\ it appears that the _sh are able to measure\ by some physio! logical mechanism\ changes in their amount of surplus energy available for growth\ as postulated by Thorpe "0875#[ Juvenile brown trout thus appear to migrate from one habitat to another as a phenotypically plastic response to declining growth performance as they reach an environmental threshold in their present habitat[ This accords with the general assumption that migration is a biological response to adversity "Taylor + Taylor 0866#[ Individuals may reach this threshold at di}erent ages and sizes depending on their meta! bolic status[ Fast!growing individuals migrate earlier and at a smaller body size than slower!growing indi! viduals\ because their metabolic rates are higher\ and consequently experience a larger drop in their allo! cation of energy to growth[ By migrating\ the _sh are probably able to retain a higher growth rate than possible under the feeding opportunities in the orig! inal habitat[ For fast!growing individuals\ an alternative to migration is to mature sexually in the stream[ The size advantage attained in the stream\ relative to slower! growing individuals\ may then be converted into a _tness advantage by earlier reproduction and the pos! sibly of participating in more spawning events during life[ Among brown trout in Litjaa\ this tactic was followed by a small proportion of the males only[ These males were among the largest within their cohorts[ Among females\ the _tness gained by migrat! ing to the lake and returning as large spawners with high fecundity appears to be more than balanced by the higher risk of mortality by postponing maturation[ Among males\ alternative mating strategies such as sneaking\ may promote early maturation among fast! growing individuals\ as _tness may be high for both
small and large individuals "Jonsson 0874#[ For fast! growing males it thus appears to be alternative stra! tegies of migration or early maturation[ Most follow the _rst route\ but some use the alternative[ All in all\ the present study supports the hypothesis that fast!growing individuals shift niche earlier and at a smaller body size than slower!growing individuals\ because they maintain higher metabolic rates and are energetically constrained younger than slow growers by limited food resources "Jonsson + Jonsson 0882#[ The sources of the variation in metabolic rates among individuals are unknown\ but maternal and devel! opmental e}ects and genetic diversity may all cause such variation in metabolic rates[ Egg size\ time of hatching and emergence from the gravel "Metcalfe + Thorpe 0881#\ early developmental e}ects and even random e}ects "e[g[ spatial and temporal variation in the quality and availability of food items at _rst exogenous feeding# giving some individuals a head! start in life\ may cause di}erentiated metabolic rates within one cohort[ Genotypic di}erences in metabolic rates may also be maintained within a population due to variable selection pressures[ A high metabolic rate is advantageous only if an additional energy intake can be attained through food consumption "Forseth et al[ 0883#[ An individual|s possibility to attain such an additional intake may depend upon cohort or population size "density dependency# and environ! mental factors in~uencing prey availability[ It is important to understand the sources of variation in metabolic rates\ because the consequences may be many[ Recent studies indicate that in salmonids early metabolic rates represent an important premise for several of the life!history decisions the _sh has to make later in life "Metcalfe et al[ 0878^ Metcalfe 0880^ Titus + Mosegaard 0880^ Metcalfe et al[ 0881^ Forseth et al[ 0883^ Metcalfe et al[ 0884#\ and the present study shows that the metabolic status is also important for the timing of juvenile migrations in salmonids[
Acknowledgements We thank Randi Saksgard\ Karl Ove So ndmo r\ Sturla Bro rs\ Barbro Klo ven and Jens Gisle Haukdal for assistance in the _eldwork[ We also thank Engerdal Fjellstyre for allowing us to work undisturbed in Litjaa[ Finally\ we are grateful for the comments and corrections made by Malcolm Elliott and John Thorpe[ Financial support was provided by the Direc! torate for Nature Management\ Norway\ by the Norwegian Institute for Nature Research and by the European Commission "FAIR Programme\ contract CT84Ð9998#[
References Bohlin\ T[\ Dellefors\ C[ + Faremo\ U[ "0882# Optimal time and size for smolt migration in wild sea trout "Salmo
681 Juvenile migrations and energetics
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Jonsson\ N[ "0880# In~uence of water ~ow\ water tem! perature and light on _sh migration in rivers[ Nordic Jour! nal of Freshwater Research\ 55\ 19Ð24[ Jonsson\ B[ + Gravem\ F[R[ "0874# Use of space and food by resident and migrant brown trout\ Salmo trutta[ Environmental Biology of Fishes\ 03\ 170Ð182[ Jonsson\ B[ + Jonsson\ N[ "0882# Partial migration] niche shift versus sexual maturation in _shes[ Reviews in Fish Biology\ 2\ 237Ð254[ Jonsson\ N[\ Jonsson\ B[ + Hansen\ L[P[ "0889# Partial seg! regation in the timing of migration of Atlantic salmon of di}erent ages[ Animal Behaviour\ 39\ 202Ð210[ Jonsson\ B[ + Ruud!Hansen\ J[ "0874# Water temperature as the primary in~uence on timing of seaward migrations of Atlantic salmon "Salmo salar# smolts[ Canadian Journal of Fisheries and Aquatic Sciences\ 31\ 482Ð484[ Jonsson\ B[ + Stenseth\ N[C[ "0866# A method for estimating _sh length from otolith size[ Report from the Institute of Freshwater Research\ Drottningholm\ 45\ 70Ð75[ Kevern\ N[R[ "0855# Feeding rate of carp estimated by a radioisotopic method[ Transactions of the American Fish! eries Society\ 84\ 252Ð260[ Kolehmainen\ S[E[ "0863# Daily feeding rates of bluegill "Lepomis macrochirus# determined by a re_ned radio! isotope method[ Journal of Fisheries Reseach Board of Canada\ 20\ 56Ð63[ L|Abee!Lund\ J[H[\ Langeland\ A[L[ + Jonsson\ B["0882# Spatial segregation by age and size in brown trout and Arctic charr] a trade!o} between feeding possibilities and risk of predation[ Journal of Animal Ecology\ 51\ 059Ð057[ Langeland\ A[L[\ L|Abee!Lund\ J[H[\ Jonsson\ B[ + Jonsson\ N[ "0880# Resource partitioning and niche shift in Arctic charr\ Salvelinus alpinus and brown trout\ Salmo trutta[ Journal of Animal Ecology\ 59\ 784Ð801[ Metcalfe\ N[B[ "0880# Competitive ability in~uences seaward migration age in Atlantic salmon[ Canadian Journal of Zoology\ 58\ 704Ð706[ Metcalfe\ N[B[\ Huntingford\ F[A[\ Graham\ W[D[ + Thorpe\ J[E[ "0878# Early social status and the devel! opment of life!history strategies in Atlantic salmon[ Pro! ceedings of the Royal Society of London B\ 125\ 6Ð08[ Metcalfe\ N[B[\ Taylor\ A[C[ + Thorpe\ J[E[ "0884# Meta! bolic rate\ social status and life!history strategies in Atlan! tic salmon[ Animal Behaviour\ 38\ 320Ð325[ Metcalfe\ N[B[ + Thorpe\ J[E[ "0881# Early predictors of life!history events] the links between _rst feeding date\ dominance and seaward migration in Atlantic salmon\ Salmo salar L[ Journal of Fish Biology\ 30 "Suppl[ B#\ 82Ð 88[ Metcalfe\ N[B[\ Wright\ P[J[ + Thorpe\ J[E[ "0881# Relation! ship between social status\ otolith size at _rst feeding and subsequent growth in Atlantic salmon "Salmo salar L[#[ Journal of Animal Ecology\ 50\ 474Ð478[ N%sje\ T[F[\ Jonsson\ B[\ Sandlund\ O[T[ + Kjellberg\ G[ "0880# Habitat switch and niche overlap in coregonid _shes] e}ects of zooplankton abundance[ Canadian Jour! nal of Fisheries and Aquatic Sciences\ 37\ 1296Ð1204[ O kland\ F[\ Jonsson\ B[\ Jensen\ A[ + Hansen\ L[P[ "0882# Is there a threshold size regulating smolt size in brown trout and Atlantic salmon < Journal of Fish Biology\ 31\ 430Ð449[ Persson\ L[ "0872# Food consumption and competition between age classes in a perch "Perca ~uviatilis# population in a shallow eutrophic lake[ Oikos\ 39\ 086Ð196[ Sandlund\ O[T[\ N%sje\ T[F[ + Jonsson\ B[ "0881# Onto! genetic changes in habitat use by white_sh\ Coregonus lavaretus[ Environmental Biology of Fishes\ 22\ 230Ð238[ Stearns\ S[C[ "0881# The Evolution of Life Histories[ Oxford University Press\ Oxford[Taylor\ L[R[ + Taylor\ R[A[J[ "0866# Aggregation\ migration and population mech! anisms[ Nature\ 154\ 304Ð310[
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potential among migratory brown trout "Salmo trutta# fry competing for territories] evidence from otoliths[ Canadian Journal of Fisheries and Aquatic Sciences\ 37\ 08Ð16[ Ugedal\ O[\ Jonsson\ B[\ NjDstad\ O[ + NFumann\ R[ "0881# E}ects of temperature and body size on radiocaesium retention in brown trout "Salmo trutta L[#[ Freshwater Biology\ 17\ 054Ð060[ von Bertalan}y\ L[ "0827# A quantitative theory of organic growth[ Human Biology\ 09\ 070Ð102[ Werner\ E[E[ "0868# Niche partitioning by food size in _sh communities[ PredatorÐPrey Systems in Fisheries Man! agement "eds R[H[ Stroud + H[ Clepper#\ pp[ 200Ð211[ Sport Fishing Institute\ Washington D[C[ Werner\ E[E[ + Gilliam\ J[F[ "0873# The ontogenetic niche and species interaction in size!structured populations[ Annual Review of Ecology and Systematics\ 04\ 282Ð314[ Wootton\ R[J[ "0889# Ecology of Teleost Fishes[ Chapman + Hall\ London[ Received 05 April 0887^ revision received 3 November 0887
