The effect of thermal acclimation on aerobic scope and critical swimming speed in Atlantic salmon

27 Pages·2017·0.9 MB·English

©2017.PublishedbyTheCompanyofBiologistsLtd|JournalofExperimentalBiology(2017)220,2757-2764doi:10.1242/jeb.154021
RESEARCHARTICLE
The effect of thermal acclimation on aerobic scope and critical
swimming speed in Atlantic salmon, Salmo salar
MaltheHvas1,*,OleFolkedal1,AlbertImsland2,3andFrodeOppedal1
ABSTRACT factors, acclimation involves a range of biochemical changes in
enzyme functioning, alterations in the composition of membrane
The Atlantic salmon is extensively studied owing to conservation
lipidsandadjustmentsofhaematologicalparameters(Roots,1968;
concerns and its economic importance in aquaculture. However, a
HoustonandDeWilde,1968,1969;SomeroandHochachka,1971).
thorough report of their aerobic capacity throughout their entire
Atlantic salmon (Salmo salar Linnaeus 1758) naturally reside
thermalnichehasnotbeendescribed.Inthisstudy,Atlanticsalmon
(∼450g)wereacclimatedfor4weeksat3,8,13,18or23°C,andthen intheAtlantic Oceanandadjacentriversystems fromSvalbardat
78°N to Northern Spain at 42–43°N (Jensen et al., 2014; Horreo
testedinalargeBrett-typeswimmingrespirometeringroupsof10per
et al., 2011). Within this geographical area, Atlantic salmon
trial.Bothstandardmetabolicrateandactivemetabolicratecontinued
encounter seawater temperatures down to 0–3°C in the far north
toincreasewithtemperature,whichresultedinanaerobicscopethat
(Reddin, 1985; Lacroix, 2013) and above 20°C during river
alsoincreasedwithtemperature,butwasstatisticallysimilarbetween
migration in the south (Valiente et al., 2004). Local populations
13, 18 and 23°C. The critical swimming speed peaked at 18°C
(93.1±1.2cms−1), and decreased significantly at the extreme havedistinctgeneticidentities,whichmayaidintheiradaptationto
temperatures to 74.8±0.5 and 84.8±1.6cms−1 at 3 and 23°C, thewide range of habitats in which theyare found (Bourret et al.,
2013; Jensen et al., 2014). However, genotypic differences
respectively.At23°C,theaccumulatedmortalityreached20%over
appear negligible when evaluating cardiac function at different
4weeks,whilenofishdiedduringacclimationatcoldertemperatures.
temperatures, where Atlantic salmon show a remarkable ability to
Furthermore,fishat23°Chadpoorappetiteandlowerconditionfactor
improvecardiacperformancethroughthermalacclimationregardless
despite still having a high aerobic scope, suggesting that oxygen
ofgeneticorigin(Anttilaetal.,2014).ThissuggeststhatanAtlantic
uptake was not the limiting factor in the upper thermal niche
salmonprimarilyreliesonphenotypicplasticitywhenitencounters
boundary. In conclusion, Atlantic salmon were able to maintain a
differentthermalenvironmentsthroughoutitsnaturaldistribution.
highaerobiccapacityandgoodswimmingcapabilitiesthroughoutthe
A widely used concept for the assessment of whole-animal
entire thermal interval tested, thus demonstrating a high level of
performanceisthescopeforactivity,coined byFry(1947)asthe
flexibility in respiratory capacity towards different temperature
aerobic scope (AS), which is the difference between the standard
exposures.
metabolic rate (SMR) and the activemetabolic rate (AMR). SMR
KEYWORDS:U ,Respirometry,Scopeforactivity,Temperature representstheminimumrestingmetabolicstate,whileAMRisthe
crit
maximum rate of aerobic metabolism. The AS thereby provides a
INTRODUCTION quantification of oxygen available for fitness related traits such
Nearlyallspeciesoffisharepoikilothermicanimalsandtherefore as growth, foraging, locomotion and fecundity (Priede, 1985;
mustcopewithenvironmentallyinducedfluctuationsintemperature ClaireauxandLefrancois,2007).
ofvariousmagnitudes(Nelson,2016).Becausetemperatureaffects Metabolism is greatly influenced by temperature, where SMR
the rate of physiological processes, fish have a preferred thermal increasesinexorablyfromaccelerationofallbiochemicalprocesses,
window in which they can function optimally, which is highly whilst AMR tends to either reach a plateau or decrease at higher
dependentonspecies-specificadaptations(Scholanderetal.,1953; temperatures dictated by the maximal capacity of the cardio-
Fry, 1958; Beamish, 1981). Species from environments in which respiratorysystem. Consequently, the scope foractivityexhibits a
temperatureisnearlyconstantallyear,suchasinarcticregionsand thermal optimum (Fry and Hart, 1948; Brett, 1971; Eliason and
y
tropical coral reefs, may only tolerate a very narrow range of Farrell, 2016). The temperature at which AS is maximized is g
o
temperatures (Somero and DeVries, 1967; Nilsson et al., 2009), associated with optimum growth (Brett, 1971; Claireaux et al.,
l
whereas fish from more variable environments have broader and 2000; Mallekh and Lagarder̀e, 2002; Khan et al., 2014) and the io
B
more flexible thermal windows (Fry and Hart, 1948; Claireaux highestcriticalswimmingspeed(U )inincrementalswimspeed
crit l
etal.,2006;Norinetal.,2014).Flexibilityinthermaltoleranceis protocols, which also coincides with maximum cardiac function a
t
partly due to the capacity for acclimation, which typically occurs (Brett, 1965; Farrell, 2002). Furthermore, fish populations are n
e
within days or weeks (Hazel and Prosser, 1974). Among other expected to occupy habitats where AS is high (Pörtner and Peck, m
2010;AsburyandAngilletta,2010). i
r
ASmaytherebyprovide anindication ofhowwellaspeciesof e
p
1InstituteofMarineResearch,Matredal5984,Norway.2DepartmentofBiology, fishiscopinginagivenenvironment.However,somestudieshave x
UniversityofBergen,Bergen5007,Norway.3Akvaplan-niva,IcelandOffice, E
founddiscrepanciesinthisassumptionwheregrowthoptimadidnot
Akralind4,Kopavogur201,Iceland. f
correlate with the highest AS (Gräns et al., 2014), and where AS o
*Authorforcorrespondence([email protected]) continued to increase up to near-lethal temperatures, while the al
fish behaviourally preferred colder waters (Norin et al., 2014). n
M.H.,0000-0002-2967-5525 r
Furthermore,arecentreviewfoundthatfishspeciesdonotalways u
o
Received25November2016;Accepted10May2017 haveaclearthermaloptimuminAS(Lefevre,2016). J
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RESEARCHARTICLE JournalofExperimentalBiology(2017)220,2757-2764doi:10.1242/jeb.154021
Norge AS, Nesttun, Norway), and the propeller speed (rpm) was
Listofsymbolsandabbreviations controlledwithafrequencyconverter(ITTMonitoringandControl,
AMR activemetabolicrate Norway). To determine the relationship between propeller speed
AS aerobicscope and the water current velocity, an acoustic Doppler velocimeter
COT costoftransport (Vectrino Lab Velocimeter, Nortek AS, Rud, Norway) was
FAS factorialaerobicscope
mountedattherearoftheswimsection.Waterwasaddedintothe
Ṁ oxygenconsumptionrate
O2 tunneloppositeoftheswimsectionthroughanadjustableinletthat
Q temperaturecoefficient
10
drew from the same reservoir used for the holding tanks, where
SMR standardmetabolicrate
U criticalswimmingspeed temperaturewastightlyregulated.Themaximumflowcapacityinto
crit
thetunnelwas∼280litresmin−1,whichwasmorethanenoughfor
rapidflushingofthesetup,torestoreoxygenlevelsandtomaintain
constant temperatures during swim trials. A camerawas placed at
Atlantic salmon are an extensively studied species because of therearoftheswimsectiontomonitorthefishwithoutdisturbing
their economic importance in aquaculture and for conservation them. An oxygen sensor was deployed adjacent to the camera
concerns from declining natural populations (e.g. Horreo et al., (RINKO ARO-FT, JFE Advanced Co., Japan), which was
2011; Bourret et al., 2013). To complete their anadromous life connected to a computer where measurements were logged every
cycle, Atlantic salmon undoubtedly need to function at a wide 2 s (MiniSoft SD200W, SAIV A/S Environmental Sensors &
range of temperatures, and appear to possess an impressive Systems, Norway). Fatigued fish were easily removed from the
phenotypic plasticity in response to thermal acclimation (Anttila tunnelattherearwherethetopopeningcouldbepartiallyremoved.
et al., 2014). However, a thorough description of the aerobic The main advantage of using a relatively large swim tunnel
capacity and swimming performance throughout their thermal setup is that underestimations of U are avoided, since fish are
crit
nicheislacking. freely able to change between steady and burst and glide
Theaimofthepresentstudywasthereforetoquantifythescope swimming gaits (e.g. Tudorache et al., 2007; Deslauriers and
foractivitybymeasuringAMRandSMR,whilealsoobtainingU Kieffer, 2011; Remen et al., 2016). However, to obtain reliable
crit ̇
andmonitoringswimmingbehaviour,atfivedifferentacclimation oxygenconsumptionrate(M )measurementswithinareasonable
O2
temperatures from 3 to 23°C. This was achieved by performing timeinthissetup,groupsoffishhadtobetestedsimultaneouslyto
swim tunnel respirometry, where oxygen uptake provides an reduce the ratio between biomass and volume, which meansthat
indirect measure of aerobic metabolism. It was hypothesized that measurements represent a group average. Because the mass-
̇
Atlanticsalmonwouldbeabletomaintainahighscopeforactivity specificM decreaseswithsize,itisimperativetousefishwithin
O2
andthereforealsoahighU inawidethermalinterval,whereinthe thesamesizeclass.
crit
optimumtemperaturefortheseparametersshouldcorrespondwith The fish used in the experiments had a cross-sectional area of
theoptimumgrowthofpost-smoltsat13°C(Handelandetal.,2003, ∼30cm2,meaningthatmorethanthreefishwouldhavetooverlap
2008). toexceed10%ofthecross-sectionalareaoftheswimtunnel,which
was 1017cm2. Generally, the fish were evenly spread out in the
MATERIALSANDMETHODS swim section during swim trials and would not overlap for long
Animalsandenvironmentalmonitoring periods. Exceptions were at the lowest speed initially, and
Atlantic salmon post-smolts (Aquagen, Norway) were held in infrequently when individuals fatigued simultaneously at the
the Tank Environmental Laboratory at the Institute of Marine highest speeds. Therefore, the effect of solid blocking was not
Research, Matre, Norway, in indoor large circular tanks (3m correctedforhere(BellandTerhune,1970;Plaut,2001).Because
diameter, 5.3m3) with a water flow of 120litresmin−1 in full- groupsoffishweretestedsimultaneously inthissetup,itislikely
strength seawater (34‰) under a natural photoperiod. The fish thatindividualsexperiencedeitherslightlyhigherorlowercurrent
were fed standard commercial feed (Nutra, 3mm pellet size, velocities depending on their relative position in the swim tunnel,
Skretting, Norway) in excess through automatic feeding devices owing to hydrodynamic interaction with other fish and the tunnel
from 10:00 to 14:00 h each day. The temperature in the holding itself.However,thesetcurrentspeedshouldstillberepresentative
tanks was continuously monitored and kept within ±0.1°C by fortheactualcurrentspeedsexperiencedbythefishandtherefore
custom software at the research facility. Dissolved oxygen was sufficientforthepurposeofthisstudy.
y
alsomonitored,andwasnotallowedtofallbelow85%saturation. g
o
To achieve this at the highest acclimation temperatures during Experimentalprotocols l
o
daytime,itwas necessarytoaddaninletofhyperoxicwater.All Acclimation procedures and swim tunnel respirometry were i
B
experiments were performed in accordance with the Norwegian conducted between June and September 2016. Prior to swim
l
a
laws and regulations for procedures and experiments on live trials,thefishhadbeenacclimatedforaminimumof4weeksto3,
t
animalsunderpermitnumber9776. 8, 13, 18 or 23°C. When targeting 3 and 23°C, the fish had n
e
previouslybeenexposedto8and18°C,respectively,for4weeks m
Swimtunnelsetup to better accommodate the transition to these more extreme ri
e
A thorough description of the large Brett-type swim tunnel temperatures.Groupsof10fishwereusedineachswimtrial,and
p
respirometer used for the experiments is provided in Remen et al. sixreplicatetrialswereconductedforeachofthefivetemperature x
E
(2016).Themainspecificationsoftheswimrespirometerarebriefly groups.
f
summarized as follows. The swim section of the tunnel had an Intheafternoon,randomfishweregentlynettedandtransferred o
internaldiameterof36cmandwas248cmlong,whichprovideda to the swim tunnel. Because the swim tunnel was situated in the al
n
volumeof252litres.Thevolumeoftheentireswimtunnelsystem same room as the holding tanks, movement only took a few
r
was 1905litres. Water currents were generated by a motor-driven seconds, which presumably minimised handling stress. The fish u
o
propeller(Flygt4630,11°propellerblade,XylemWaterSolutions were left to acclimate in the tunnel overnight at 15cms−1 J
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RESEARCHARTICLE JournalofExperimentalBiology(2017)220,2757-2764doi:10.1242/jeb.154021
(∼0.45 body lengths s−1) with moderate flushing to maintain withhighanaerobiccapacities(Leeetal.,2003).AMRwasdefined
̇
temperatureandoxygenlevels. as the highest M measured which coincided with the current
O2
Swimtrialscommencedthefollowingday.Currentvelocitywas velocity where the majority of the fish reached fatigue. Because
increased incrementally by 15cms−1 every 30min until all fish Ṁ was not measured in the few fish that required one more
O2
reached fatigue. Fatiguewas defined as when fish no longer were velocity increment to fatigue than the majority, AMR may have
able to remove themselves from the rear grid, even with human been slightly underestimated for the best swimmers. However, a
̇
tactilestimulation.Thetimewasnoted,andthenfatiguedfishwere plateau in M was observed between the highest speeds where
O2
quicklyremovedfromthetunnelandeuthanizedwithablowtothe somefishhadbeenremovedinbetween,indicatingthatthereported
head.Forklength(L )andmassweremeasuredforeveryindividual AMRisrepresentativeforallthefish.
f
afterremovalfromthetunnel. U wascalculatedaccordingtoBrett (1964):
crit
To measure oxygen uptake, the swim tunnel system was kept
t U
closed for the first 20min of each increment interval and U ¼U þ f i; ð2Þ
crit f t
subsequently flushed for the remaining 10min, to re-establish i
oxygenlevelsforthefollowingincrementspeed.Oxygenwasnot whereU isthelastcompletedcurrentvelocity,t isthetimespent
f f
allowed to fall below 85% saturation during closed periods. To at the current velocity where fatigue was reached, t is the time
i
accomplish this at 23°C during high current velocities, the closed spent at each velocity and U is the magnitude of the velocity
i
period was occasionally reduced to 15min. Furthermore, because increment.
10 fish were tested simultaneously, the period of oxygen Toassessswimmingefficiency,thegrossandnetcostoftransport
measurement was sometimes shortened when the first fish started (COT) was calculated for each swimming speed as the energy
̇
tofatigueandthushadtoberemovedfromthetunnel.Becausethis required to travel 1 km. M was converted to joules using an
onlyoccurredatthehighestvelocities,itwasstillpossibletoobtain oxycalorific coefficient ofO214.2 J mg−1 O (Videler, 1993;
2
agoodtraceofoxygenconsumptioninthesereducedmeasurement Ohlbergeretal.,2006),andthendividedbytheswimmingspeed.
intervals. If six or more fish remained at the onset of the next Only swimming intensities that were considered primarily
incrementspeed,oxygenmeasurementswerecontinued.Withfewer aerobically fuelled were included in these calculations. The
fish it became increasingly more difficult to obtain a proper trace minimumCOTwasestimatedastheminimumofaparabolafitted
within reasonable time because of the large volume of the to the gross COT as a function of swimming speed for each
experimental setup relative to fish biomass. However, the fish acclimationtemperature.
generally reached fatigue within one increment interval, so final
̇
M measurements represented the majority of the fish, while the Statisticalanalyses
O2 ̇
bestswimmersineachtrialwerealreadynearfatiguewhenreliable Differences in M between groups were tested with a one-way
O2
oxygen measurements were no longer possible. No noteworthy ANOVA(Sigmaplot12.3,SystatSoftware),whileanestedtwo-way
background oxygen consumption from bacterial respiration was ANOVA (Statistica 13.0, Quest Software) was used when
detectedafterswimprotocols. measurements for individual fish were available (U and size
crit
Tail-beatfrequencywasmeasuredinthreerandomlyselectedfish parameters).ATukey’sposthoctestwasusedtodeterminewhich
ateachcurrentvelocitybycounting100tailbeatswithastopwatch, groupsdiffered,whiletheShapiro–WilktestandLevene’smeantest
andchangesfromsteadytoburstandglideswimmingasthecurrent were used to confirm normality and equal variance in the data,
speedincreasedwererecorded. respectively.P-valuesbelow0.05wereconsideredsignificant.All
dataarepresentedasmeans±s.e.m.
Calculations
For each closed period in the swim trials, a linear regression was RESULTS
fittedtothedecreaseinoxygenconcentrationasafunctionoftime. The fish used in the swim trials were within a similar size range
̇
Theslopewasthen usedtocalculatethemass-specificM ofthe between acclimation groups (Table 1). However, the fish at 3 and
O2
fishatthegivenswimmingspeed: 8°Cweresignificantlyheaviercomparedwith13and18°Cbecause
these trials were carried out 1month later. Even though trials at
DO 23°Cwereconductedbetweenthetrialsat3and8°C,thesefishhad
2ðV (cid:2)V Þ
M_ ¼ Dt sys b ; ð1Þ asignificantlylowermass,butsimilarforklengthwhichresultedin y
O2 M a poor condition factor for this group (Table 1). During the g
b o
acclimationat23°C,thefishfednormallyinthefirstweek,butin l
o
whereΔO2/Δtisthechangeinoxygenovertime,Vsysisthevolume the latter period appetite declined. This coincided with increased Bi
ofthesystem,andV andM arethevolumeandmassofthefish, mortalitywhere20%hadperishedafterfourweeksofacclimation
b b l
respectively, where a density of 1kgl−1 is assumed. SMR was a
t
calculatedbyexponentiallyfittingṀ asafunctionofswimming n
O2 e
speedandextrapolatingbacktozeroswimmingspeed(Brett,1964; Table1.Mass,forklengthandconditionfactorforAtlanticsalmonused m
Beamish, 1978). Theoretically, oxygen consumption should intheswimtrialsatdifferentacclimationtemperatures(N=60) ri
e
increase exponentially with swimming speed (Beamish, 1978).
Temperature(°C) Mass(g) Forklength(cm) Conditionfactor p
However, because the anaerobic component becomes more x
3 479±18a 35.8±0.5a,b 1.02±0.01a E
substantial at high current velocities when the fish approaches its
8 491±19a 36.9±0.5a 0.95±0.01b f
maximumoxygenuptake,thecurvetendedtoreachaplateauinthe 13 437±16a,b 35.1±0.4b,c 0.98±0.01a,b o
present study. The final one or two measurements were therefore 18 408±16b 34.0±0.4c 1.01±0.01a al
n
omitted from the SMRcalculation because theyskewed the curve 23 413±13b 36.0±0.4ab 0.87±0.01c r
and caused a substantial reduction to the R2 of the fit. A similar u
̇ Statisticaldifferencesbetweengroupsareindicatedbysuperscriptletters o
plateauinginMO2priortoUcrithasalsobeenseeninothersalmonids (Tukeyposthoctest,P<0.05).Dataaremeans±s.e.m. J
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RESEARCHARTICLE JournalofExperimentalBiology(2017)220,2757-2764doi:10.1242/jeb.154021
Oxygenconsumptionandaerobicscope
SMRincreasedsteadilywithtemperaturefrom44±5mgO kg−1h−1at
2
30 3°Cto231±5mgO kg−1h−1at23°C,correspondingtoaQ of2.2.
%) Themagnitudeofth2eQ effectwasgreatestatthelowertemp1e0ratures,
ortality ( 20 fei.vge.3te.1mfpreormatu3rteos1w3e°rCesci1og0mnifpiacraendtlwyidthiff1e.r6enfrtofmrom13etaoch23o°tChe.rS(MFiRg.a2tAa)ll.
m AMRcontinuedtoincreasecontinuallyto23°C,withthemagnitudeof
ed changebeinggreatestfrom3to13°C(Fig.2A).
ulat The highest AS (AMR–SMR) was measured at 23°C, where
um 10 it was 421±12 compared with only 212±7mgO2 kg−1 h−1 at
cc 3°C. However, AS was not significantly different between 13, 18
A
and 23°C (Fig. 2C). The factorial AS (AMR/SMR) decreased
throughout the entire temperature interval from 5.74±0.33 at 3°C
0 down to 2.95±0.12 at 23°C, where a significant difference was
0 5 10 15 20 25 found from 3 to 8°C and at every two temperature increments
Time (days) thereafter(Fig.2C).
Anoverviewoftheoxygenuptakerateasafunctionofswimming
Fig.1.AccumulatedmortalityofAtlanticsalmonintheholdingtanks speedatdifferenttemperatures,includingtotalremainingfishatthe
duringacclimationto23°C.
highest velocities, is shown in Fig. 3A. Each temperature has a
distinct curve owing to differences in SMR and AMR. Oxygen
(Fig. 1). At the other temperatures, no fish died except for a consumption increased with swimming speed until a certain
small number initially due to side wounds obtained during the temperature-dependent point where the curve flattens out. When
transportation from the rearing facilities to the acclimation tanks thisoccurs,continuedswimmingisnotsustainableforlongowingto
severalweeksbeforeacclimationprotocolswereinitiated. an increasingly greater reliance on anaerobic metabolism to meet
A B
e 100
d c
600 c
1) c 90
–
–1 kg h2 400 b –1m s) 80 b d
(mg OO2 a d e U (ccrit 70 a
.M 200
c
b
a 60
0
C D
1) 500 a
–1– h c c c pe 6 y
g 400 o g
scope (mg O k2 320000 a b orial aerobic sc 4 b b,c c,d d ntalBiolo
obic Fact 2 me
Aer 100 eri
p
x
0 6 E
0 5 10 15 20 25 0 5 10 15 20 25
f
Temperature (°C) o
l
a
Fig.2.Metabolicrate,swimmingspeedandaerobicscopeofAtlanticsalmonatdifferentacclimationtemperatures.(A)Standardmetabolicrate(SMR) n
(filledcircles)andactivemetabolicrate(AMR)(opencircles),(B)criticalswimmingspeed(U ),(C)aerobicscope(AMR–SMR)and(D)factorial r
crit u
aerobicscope(AMR/SMR).N=6forA,CandD;N=60forB.Differentlettersindicatessignificantdifferencesbetweenthetemperaturegroups(Tukeyposthoc o
test,P<0.05).Dataaremeans±s.e.m. J
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RESEARCHARTICLE JournalofExperimentalBiology(2017)220,2757-2764doi:10.1242/jeb.154021
A B
700
23°C 53 (17) 4
18°C
600
1) 13°C 59 43 (6)
–
–1O kg h2 540000 83°°CC 58 42 (1) –1)s (s 3
mg 60 (17) eat 2
(O2 300 ail b
.M T
200 59 38 (0)
1
100
0 0
C D
2500
10,000
–1m) –1) 2000
k 8000 m
–1 1 k
g –
OT (J k 6000 T (J kg 1500
O
Gross C 4000 Net C 1000
2000 500
0 0
0 20 40 60 80 100 0 20 40 60 80 100
Swimming speed (cm s–1)
Fig.3.SwimmingperformanceofAtlanticsalmonasafunctionofswimmingspeedatdifferentacclimationtemperatures.(A)Oxygenconsumptionrate
(Ṁ ),(B)tail-beatfrequency,(C)grosscostoftransport(COT)and(D)netCOT.N=6forA,CandD;N=18forB.NumbersinAaretotalremainingfish
O2
inthebeginningofthecorrespondingswimspeed,whilethenumberinbracketsistotalfishremainingatthesubsequentvelocityincrementwhereoxygenuptake
wasnotmeasured.TheisolatedpointsinArepresentthecalculatedSMRfrombackextrapolationtozeroswimspeed.Dataaremeans±s.e.m.
̇
energyrequirements.Furthermore,theplateauinginM wasreached distinctcurveforeachacclimationtemperature,wherethecalculated
whennearlyallthefishstillremainedinthesetup,suggOe2stingthatthe minimumCOTwas40,45,58,61and59cms−1at3,8,13,18and
derivedAMRisarepresentativeaveragefortheentiregroup. 23°C,respectively (Fig. 3C).At intermediateand high swimming
speeds, net COTwas similar between the 8, 13 and 18°C groups,
Swimmingperformance whilethe23°CgrouphadahighernetCOTfrom45to75cms−1,
U increased significantly from 74.8±0.6cms−1 at 3°C to and the 3°C group had a lower net COT from 30 to 60cms−1
crit
statisticallysimilarpeakvaluesof91.3±0.4and 93.1±1.2cms−1at comparedwiththeothergroups(Fig.3D).
13and18°C,respectively.At23°C,U haddecreasedsignificantly
crit
to a similar value as found at 8°C (84.9±1.6 and 84.7±0.4cms−1, DISCUSSION
y
respectively)(Fig.2B).U expressedasbodylengthss−1showeda Highaerobiccapacitythroughouttheentirethermalniche g
crit o
similarpattern(datanotshown). Although the pattern of oxygen consumption in Atlantic salmon l
o
The tail-beat frequency appeared to be independent of changed dramatically with temperature, the resulting scope for i
B
temperature at low and moderate swimming speeds (Fig. 3B). activity generally remained fairly conserved with statistical
l
a
However,atthecoldertemperatures,thehighestattainabletail-beat similarities from 13 to 23°C, and a reduction by 32% at 8°C
t
frequency was impaired, which was most apparent at 3°C, with a comparedwiththepeakat23°C(Fig.2C).Similarly,theswimming n
e
peakof2.78±0.04 tail beatss−1 whenswimming at75cms−1. In performance expressed as U also remained high throughout the m
crit
comparison,at18°C,thefishreachedatail-beatfrequencyof3.24± exposedtemperatures. ri
0.07 tail beats s−1 when swimming at the same speed. Generally, A drastic impairment in swimming capability and AMR was e
p
burst and glide swimming was first observed sporadically at only measured at 3°C, where an earlier gait transition to burst x
E
60cms−1,andbecamegraduallymorepronouncedandfrequentat and glide swimming suggested that the salmon became
f
higherspeeds.Gaittransitiontookplaceearlierat3°C(45cms−1), anaerobic at lower swimming speeds. In support of this, colder o
which in conjunction with the curves for tail-beat frequency and temperatures reduce the maximum velocity of shortening of red al
̇ n
M fromthisgroup(Fig.3BandA,respectively)indicatesthatthey muscle fibres and their power production in fish, and as a
beOc2ameaerobicallychallengedatlowerspeedscomparedwiththe consequence, white muscles are recruited earlier (Rome, 1990; ur
o
othergroups,andhencethelowerU (Fig.2B).GrossCOThada Romeetal.,1992). J
crit
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RESEARCHARTICLE JournalofExperimentalBiology(2017)220,2757-2764doi:10.1242/jeb.154021
Cold acclimation also increases red muscle mass in temperate impaired if these are not compensated for by an increased feed
fish,whichimprovesstridelength,andtherebyreducestherequired intake, as seen in rainbow trout (Morgan et al., 2001). If the
tail-beatfrequencycomparedwithwarm-acclimatedfishswimming availableASisreducedathighertemperatures,therelativeenergetic
at similar speeds (Sisson and Sidell, 1987; Sidell and Moerland, cost of feeding and growing may be too high. Reduced appetite
1989; Taylor et al., 1996). It is possible that relatively higher could therefore also be behaviourally driven to avoid anaerobic
tail-beat amplitudes compensated for the observed lower tail-beat metabolism,assuggestedbythereducedfeedintakeinAtlanticcod
frequenciesat3°CinAtlanticsalmon.However,amplitudewasnot (Gadus morhua) under conditions with low AS (Claireaux et al.,
measured in this study. The observed reduction in maximum tail- 2000). However, in the present study, the AS was not reduced at
beatfrequencyat3°Ccouldthereforeindicatethatcoldacclimation 23°CinAtlanticsalmon;onthecontrary,itwashigherherethanat
alsoincreasesredmusclemassinAtlanticsalmon.Thus,whilethe anyothertemperatureinvestigated,althoughstatisticallysimilarto
maximumswimmingcapacityisreduced,theenergeticsofslowor values at both 13 and 18°C. The inevitable increase in SMR was
moderate swimming is improved, as illustrated by a reduced net accompanied by a similar increase in AMR, which demonstrates
COTcomparedwiththeotheracclimationgroups.Furthermore,the that Atlantic salmon are well equipped to meet their oxygen
loweredSMRimprovesthecumulativeCOT,whichmaybeanother requirementswellabovetemperaturesatwhichgrowthandappetite
importantadvantageincolderwaters(HoarandRandall,1978). decline. This suggests that Atlantic salmon have evolved to cope
Reverse seasonal acclimation has been found to reduce U in withextremelyhightemperaturesrelativetotheirpreferredthermal
crit
browntrout (Salmo trutta) (Dayand Butler, 2005). This indicates niche for periods of time (days), which should be adequate to
that U may have been underestimated at 3 and 8°C in Atlantic spatiallydealwiththeproblembysearchingforlowertemperatures
crit
salmonbecausethisexperimentwasperformedduringthesummer or withstanding the duration of exposure, e.g. during river
monthsinasimulatednaturalphotoperiod.Theseasonalvariation migrationsinthesummer.
inswimmingcapacityforAtlanticsalmoncouldthereforebeeven U inAtlanticsalmonwaslowerat23°Ccomparedwith13and
crit
smallerthansuggestedbythepresentstudy. 18°C, despite similar AS. Assuming an increased tendency for
Regardless, the aerobic capacity appears to remain adequate in hyperactivityaspreviouslydiscussed,fishat23°Cwereperhapsina
the entire thermal niche, illustrating a high flexibility to changing state of metabolic recovery during the swim trials, which may
environmentalconditionsforthiseurythermalspecies. have reduced their swimming efficiency and peak performance,
considering that AMR was not compromised. This was further
Physiologicallimitationsathightemperatures supportedbyahighernetCOT,indicatingthatswimmingat23°C
When Atlantic salmon were kept at 23°C, theirappetite gradually wasrelativelymorecostly.Similarly,inwarm-acclimatedrainbow
becamemorereduced,whichresultedinapoorconditionfactorfor trout,therepeatedswimmingperformancewasfoundtobereduced
fish tested in the swim trials. More importantly, a cumulative because exercise recovery was slower compared with colder
mortalityof20%intheholdingtanksoccurred,primarilyoverthe acclimated fish (Jain and Farrell, 2003). Therefore, this may
last 2 weeks of the 4-week acclimation period. If they were partiallyexplainalowerU at23°C.However,thepoorcondition
crit
strugglingwithmeetingtheiroxygenrequirementsat23°C,anovert factorand apparent lackof appetite during the acclimation period
increase in gill ventilation or even the onset of ram ventilation arealsolikelytohaveimpairedtheswimmingperformance.
should be apparent, as seen in triploid Atlantic salmon during The physiological barrier at high temperatures in fish has
moderatehypoxiaat19°C(Hansenetal.,2015).However,thiswas widely been ascribed to limitations in sufficient oxygen uptake
notobservedhere,andoxygensaturationintheholdingtankswas andsupplytothetissues(Brett,1971;Farrell,2002;Pörtnerand
always kept above 85%. Furthermore, the high AS found in the Knust,2007).InPacificsalmonids,ASandcardiacperformance
swim tunnel trials strongly suggests that their routine oxygen decline when the fish approach their upper incipient lethal
requirementsweresatisfied. temperature, which is linked to an insufficient myocardial
Apossibleexplanationforthehighmortalityratecouldinstead oxygen supply as returning venous blood to the heart becomes
be hyperactivity initiated as a form of escape behaviour after more depleted during exercise (Farrell, 2002, 2007). In warm-
prolongedexposureinasuboptimalthermalenvironment.Delayed acclimatedAtlanticsalmon,theupperincipientlethaltemperature
deathfromstrenuousactivitiesisawell-documentedphenomenon was found to be 27.8°C (Elliott, 1991), which corresponds with
in fish that is associated with high lactate levels and a high cardiac collapse at 27.5°C (Anttila et al., 2014). In theory, AS
intracellular acidosis (Black, 1958; Wood et al., 1983). shouldthereforealsocollapseat∼27°C,yetwasstillpreservedat
y
Furthermore, cortisol was likely elevated during these stressful 23°Cinthepresentstudy. g
o
conditions, and lactate recovery is slower in the presence of Inbarramundi(Latescalcarifer),ASwasfoundtoincreaseupto l
o
cortisol(Pagnottaetal.,1994). near lethal temperatures (Norin et al., 2014), and likewise in i
B
Reducedgrowthandlowerconditionfactorathightemperatures seasonal-acclimated European sea bass (Dicentrarchus labrax)
l
a
haspreviouslybeendocumentedinAtlanticsalmon(Kullgrenetal., whereAScontinuedtoincreasefrom7°Cto30°C(Claireauxetal.,
t
2013; Hevrøy et al., 2015). In particular, decreased food intake 2006),andapproacheditsacutecriticaltemperatureat35°C(Wang n
e
andloweredfeedconversionefficiencyinfishacclimatedto18°C et al., 2014). These patterns in thermal performance also describe m
compared with 12°C was found to be associated with elevated thermallyacclimatedAtlanticsalmon. ri
e
plasma levels of growth hormone and leptin, while several Thus, in ecologically relevant settings, oxygen limitation does
p
metabolitesinenergymetabolismwerereducedat18°C(Kullgren not seem to be the proximal factor in defining the upper thermal x
E
et al., 2013). These authors therefore concluded that impaired niche boundary in this species. To thrive and remain competitive
f
growth and appetite at higher temperatures was caused by the in environments with chronically elevated temperatures, other o
anorexigenic function of leptin in conjunction with changes in factors concerning hormone balance, stress, behaviour and nerve al
n
growthhormoneendocrinology(Kullgrenetal.,2013). functioning to ensure proper growth, appetite and fecundity
r
Higher temperatures increases metabolic rates and the overall therefore appear to be more important in Atlantic salmon and u
o
maintenance costs of preserving homeostasis, and growth is otherspeciesoffishthatareabletomaintainhighAS. J
2762
RESEARCHARTICLE JournalofExperimentalBiology(2017)220,2757-2764doi:10.1242/jeb.154021
ThermaloptimainAtlanticsalmon Competinginterests
Growth in Atlantic salmon post-smolts is maximized at 13°C Theauthorsdeclarenocompetingorfinancialinterests.
(Handelandetal.,2003,2008),andU asameasureofswimming
crit Authorcontributions
capabilities peaks at 18°C while the AS still is conserved at 23°C
Conceptualization:M.H.,O.F.,A.I.,F.O.;Methodology:M.H.,O.F.,A.I.,F.O.;
(presentstudy).Forthemajorityoftheirlifecyclepostsmoltification,
Software:A.I.;Formalanalysis:M.H.,A.I.;Investigation:M.H.;Resources:O.F.,
Atlantic salmon will experience temperatures below 8°C (Reddin, F.O.;Datacuration:M.H.;Writing-originaldraft:M.H.;Writing-review&editing:
1985; Lacroix, 2013; Jensen et al., 2014), and may even M.H.,O.F.,A.I.,F.O.;Supervision:O.F.,A.I.,F.O.;Projectadministration:O.F.,F.O.;
behaviourally avoid temperatures above 15°C (Johansson et al., Fundingacquisition:O.F.,F.O.
2009; Lacroix, 2013). Therefore, Atlantic salmon fit the idea of
Funding
multipleoptimumtemperaturesfordifferentphysiologicalprocesses
ThisstudywasfundedbytheNorgesForskningsråd(ResearchCouncilofNorway)
andlifehistorytraits,whereitisacknowledgedthatanyfactor,inno throughtheCentreforResearch-basedInnovationinAquacultureTechnology,
hierarchicalorder,maybelimitingineitheracuteorchronicthermal EXPOSED(237790).
challenges (Clark et al., 2013). Similar multiple optimum
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