ARTICLE

Optimum and maximum temperatures of sockeye salmon(Oncorhynchus nerka) populations hatched at different temperaturesZ. Chen, K. Anttila, J. Wu, C.K. Whitney, S.G. Hinch, and A.P. Farrell

Abstract: Temperature tolerance and heart rates were compared among nine sockeye salmon (Oncorhynchus nerka (Walbaum inArtedi, 1792)) populations, whose eggs were incubated at 10, 14, and 16 °C before rearing all hatchlings at a common temperature.Critical thermal maximum (CTmax) significantly differed among populations and temperature treatments. Populations withshortermigration distance and a lowermigration and spawning temperature tended to have higher CTmax at 90 days posthatch.However, the relationship was reversed when fish of similar size were compared at 135–214 days posthatch. CTmax at 90 daysposthatch was also positively related to body mass, which differed appreciably among populations at this development stage.With growth, the population differences in CTmax diminished from 3.1 to 1 °C. Elevated incubation temperature also decreasedCTmax. Arrhenius breakpoint temperature (ABT) for maximum heart rate differed among populations incubated at 14 °C. TheChilko Lake population, which rear at 1.2 km above sea level, had the highest heart rate across all temperatures when incubatedat 14 °C, but the lowest ABT among populations. This study provides clear evidence for the local adaptation among sockeyesalmon populations with respect to temperature tolerance and cardiac capacity, information that adds to the debate onwhetherintraspecific variance is adaptive, or a constraint, or both.

Key words: sockeye salmon, Oncorhynchus nerka, critical thermal maximum, Arrhenius breakpoint, maximum heart rate, incuba-tion, developmental plasticity, population differences, adaptation, optimum temperature.

Résumé : Une comparaison de la tolérance a la température et des fréquences cardiaques a été réalisée pour neuf populationsde saumon rouge (Oncorhynchus nerka (Walbaum in Artedi, 1792)) dont les œufs ont été incubés a 10, 14 et 16 °C préalablement al’élevage de tous les alevins vésiculés a une même température. La température maximale critique (CTmax) variait de manièresignificative selon la population et le traitement thermique. Les populations caractérisées par de plus courtes distances demigration et des températures de migration et de frai plus faibles présentaient généralement des CTmax plus élevées 90 joursaprès l’éclosion. Toutefois, a de 135 a 214 jours après l’éclosion, cette relation était inversée pour des poissons de taille semblable.La CTmax a 90 jours après l’éclosion était également positivement corrélée a la masse corporelle, qui variait considérablementselon la population a ce stade du développement. Au fil de la croissance, les variations de CTmax entre populations ont diminuéde 3,1 a 1 °C. Une température d’incubation élevée se traduisait également par une diminution de la CTmax. La températured’inflexion du diagramme d’Arrhenius (ABT) pour la fréquence cardiaque maximum variait entre les populations incubées a14 °C. La population du lac Chilko, dont l’élevage a lieu a 1,2 km au-dessus du niveau de lamer, présentait la fréquence cardiaquela plus élevée a toutes les températures pour une incubation a 14 °C, mais la plus faible ABT de toutes les populations. L’étudedémontre clairement une adaptation locale chez les populations de saumons rouges en ce qui concerne la tolérance a latempérature et la capacité cardiaque. Ces résultats éclairent le débat a savoir si la variance intraspécifique est une adaptation,une contrainte ou les deux. [Traduit par la Rédaction]

Mots-clés : saumon rouge, Oncorhynchus nerka, température maximale critique, point d’inflexion du diagramme d’Arrhenius,fréquence cardiaque maximum, incubation, plasticité du développement, différences entre populations, adaptation, tempéra-ture optimale.

IntroductionLocal adaptation has fundamental importance in evolution, bio-

diversity, and conservation. In the Pacific northwest of NorthAmerica, sockeye salmon (Oncorhynchus nerka (Walbaum in Artedi,1792)) is an excellent model to study local adaptations (Taylor1991). This is because more than 100 populations have been iden-tified in the Fraser River watershed alone (Beacham et al. 2004).These populations have genetically adapted and phenotypicallyadjusted to their natal watershed (Slaney et al. 1996), with geneticdiversity among them being maintained by high natal spawningsite fidelity and precise spawning timing. However, in recent

years, elevated river temperatures during adult spawning migra-tions have been associated with migration mortality (Farrell et al.2008; Hinch and Martins 2011; Hinch et al. 2012), disease (Milleret al. 2011), and phenological shifts (Taylor 2008). Given that themean summer temperature of the Fraser River has warmed by�2 °C compared with 60 years ago (Hinch and Martins 2011) and afurther 2 °C increase is predicted before the end of 21st century(Ferrari et al. 2007), the need to understand the capacity of sock-eye salmon populations to cope with warm temperature has someurgency.

Although thermal acclimation can benefit the temperature tol-erance of adult fish, this is not always the case during early devel-

Received 15 November 2012. Accepted 11 March 2013.

Z. Chen, K. Anttila, and J. Wu. Department of Zoology, The University of British Columbia, 6270 University Boulevard, Vancouver, BC V6T 1Z4, Canada.C.K. Whitney and S.G. Hinch. Department of Forest Sciences, The University of British Columbia, 2424 Main Mall, Vancouver, BC V6T 1Z4, Canada.A.P. Farrell. Department of Zoology, The University of British Columbia, 6270 University Boulevard, Vancouver, BC V6T 1Z4, Canada; Department of Zoology, TheUniversity of British Columbia, 6270 University Boulevard, Vancouver, BC V6T 1Z4, Canada; Faculty of Land and Food Systems, The University of British Columbia,2357 Main Mall, Vancouver, BC V6T 1Z4, Canada.

Corresponding author: Z. Chen (e-mail: czq2007hlj@gmail.com).

265

Can. J. Zool. 91: 265–274 (2013) dx.doi.org/10.1139/cjz-2012-0300 Published at www.nrcresearchpress.com/cjz on 12 March 2013.

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opmental stages (Angilletta 2009). Sockeye salmon reproductionis greatly influenced and indeed regulated by temperature, bothdirectly and indirectly. Adult fish generally spawn in autumn, assummer river temperatures are cooling. Hatching depends on thewinter temperature and normally takes about 90 days, with emer-gence occurring in early spring as the water temperature in-creases (Burgner 1991), and the surface ice melts and theavailability of food increases (Hinch et al. 2006). Abnormal rearingtemperature has been proven to be one of the most importantfactors causing early life mortality in fish (Murray and McPhail1988; Beacham andMurray 1989; Lahnsteiner et al. 2012). Elevatedtemperature during egg incubation can also cause skeletal abnor-mality (Dionísio et al. 2012), pericardial edema (Kurokawa et al.2008), irregular myofibrillar growth (Albokhadaim et al. 2007),and poor swimming performance (Burgess et al. 2006). Moreover,increased incubation temperature leads to small hatchlings(Ojanguren and Braña 2003; Finstad and Jonsson 2012), possiblybecause routine metabolic rate and energy consumption increaseexponentially with temperature, thus, leading to reduced capac-ity for growth and development at temperature beyond theoptimum (Pörtner 2010). Although the effects of incubation tem-perature on fish embryogenesis are well studied (Murray andMcPhail 1988; Damme et al. 1992; Mueter et al. 2002; Burt et al.2012; Lahnsteiner et al. 2012), little is known in terms of howincubation temperature affects the posthatch temperature toler-ance of fish andwhether or not population differences exist. How-ever, more broadly, Chinese Pond Turtles (Mauremys reevesii (Gray,1831)) incubated at high incubation temperature increased theircritical thermal minimum (Du et al. 2006), while elevated incuba-tion temperature decreased preference temperature of the Com-mon Snapping Turtle (Chelydra serpentine (L., 1758)) (O’Steen 1998).

Here, the focus is intraspecific differences in temperature tol-erance of British Columbia sockeye salmon fry and the influenceof egg incubation temperature on this tolerance. The focus on theearly life stage is because the normally high mortality rates (onlyabout 7% of sockeye salmon eggs survive to the fry stage; Bradford1995) might set the first choke point for thermal selection. Locallyadapted sockeye salmon populations have evolved to have manydistinct traits, so that spawning and incubation temperatures arerelated to egg size and migration distance and temperature, forexample. Yet, Pacific salmon are regarded as having limited plas-ticity in terms of maximum temperature tolerance, whichchanges by just 2–3 °C over an acclimation temperature range of10 °C (Brett 1952). In contrast, in a more eurythermal fish, e.g., themummichog (Fundulus heteroclitus (L., 1766)), the increase could be�6 °C over the same acclimation range (Fangue et al. 2006). Apriori, we expected to discover intraspecific and developmentaldifferences in critical thermal maxima (CTmax) among the ninesockeye salmon populations when eggs were incubated at threedifferent temperatures. Furthermore, we used the Arrheniusbreakpoint temperature (ABT) for maximum heart rate (fH) as asurrogate to estimate optimum temperature (Topt) (Casselmanet al. 2012) for selected populations. Here, we present findings on(i) intraspecific differences of CTmax and maximum fH amongnine different sockeye salmon populations, and (ii) the effect ofincubation temperature on CTmax and maximum fH.

Materials and methods

AnimalsAll procedures involving animals were carried out according to

protocols A10-0335 and A08-0338, which were approved by TheUniversity of British Columbia Committee on Animal Care in ac-cordance with the Canadian Council on Animal Care. Gameteswere obtained from nine geographically distinct spawning areasfor sockeye salmon (Harrison River, Weaver Creek, Gates Creek,Scotch Creek, Adams River, Chilko River, Horsefly River, StellakoRiver, and Columbia River – Okanagan; Fig. 1). The eggs were

fertilized and incubated at The University of British Columbia at10, 14, and 16 °C (for details seeWhitney et al. 2013), which yielded27 temperature treatment groups that were maintained sepa-rately at these temperatures until hatch. Survival at hatch variedamong populations and temperatures, ranging between 45% and94.2% at 10 °C, between 46.1% and 85.4% at 14 °C, and between14.2% and 55.8% at 16 °C (Table 1). After hatch, each temperaturetreatment group was maintained separately, but reared at a com-mon garden temperature (5–7 °C) under simulated natural photo-period that varied with seasons. Fish were fed with powderedcommercial salmon diets (EWOS Canada Ltd., Surrey, British Co-lumbia, Canada) to satiation two times per day, except 24 h priorto testing. The first set of CTmax determinations was performedwhen fish had attained a similar age of 90 days posthatch (n =20–24 per population, except Harrison at 16 °C = 13). However,population and egg rearing temperature differences resulted in avariable body mass among the treatment groups (0.17 ± 0.01 to0.60 ± 0.03 g; Fig. 2). Since incubation temperature affects fish sizeat hatch (Ojanguren and Braña 2003) and body size can affecttemperature tolerance (Underwood et al. 2012), a second set ofCTmax determinations was performedwhen each population hadattained a common mean body mass of �1 g (0.89 ± 0.03 to 1.23 ±0.04 g; n = 19–20 per population), which was achieved with agevarying from 135 to 214 days posthatch depending on populationand incubation temperature. High mortality occurred withinmost populations for egg incubation at 16 °C, therefore CTmaxwas determined for only four populations at 90 days posthatchand none were measured at �1 g (Table 1).

CTmax measurementUpper thermal tolerance for each treatment group was deter-

mined using critical thermal methodology described previouslyby Fangue et al. (2006). A batch of 19–24 fish from each group wasmeasured at a time. Briefly, fish were placed in a 40 L test con-tainer with temperature-controlled and aerated circulating water(3016D heater/chiller; Fisher Scientific, Ottawa, Ontario, Canada).Fish were given 1 h at a temperature of 7 °C to recover from thetransfer stress. Water temperature was then increased at 0.3 °Cper min to 20 °C and subsequently at 0.1 °C per min thereafter.CTmax represents the temperature when fish first lose equilib-rium continuously for 10 s. Fish were immediately removed,weighed, and returned to their acclimation condition to recover.Almost every fish was recovered from its CTmax determination.Fish used to determine CTmax at 90 days posthatch were allowedto have at least 1.5 month recovery period before the CTmax wasretested when the mean body mass was similar (�1 g).

Maximum fH measurementABT analysis of maximum fH during warming is a faster proto-

col to estimate Topt when compared with the protocol used tomeasure Topt from aerobic scope (Casselman et al. 2012). Thisthen allows for a higher throughput when measuring Topt forpopulation differences. To measure maximum fH, fish (n = 9–14per population; different fish than used in the CTmax determina-tions) were first anaesthetized (75 mg�L−1 MS-222 buffered with75 mg�L−1 NaHCO3; Sigma-Aldrich, St. Louis, Missouri, USA) andimmersed upside down in a sling (0.5 L), where the gills werecontinuously supplied with aerated, temperature-controlled wa-ter containing a maintenance dose of anaesthetic (65 mg�L−1 ofMS222 and NaHCO3). Two fish were measured at a time. For eachfish, two silver electrodes (5 cm in length, 30 gauge) were attachedto the ventral side of the body (positive one on the middle of thepectoral fins, and the negative one 1 cm away from positive elec-trode towards the pelvic fins), where the electrocardiogram (ECG)signal was captured. The electrodes were connected to a Grass P55AC amplifier (Astro-Med Inc., Brossard, Quebec, Canada) that am-plified (1000×) and filtered (60 Hz line filter; low-pass: 30–50 Hz;high-pass 0.1–0.3 kHz) the ECG signal. The conditioned ECG signal

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was digitalized using a BioPac MP-150 data acquisition system andanalyzed using Acqknowledge version 3.8 software (BIOPAC Sys-tems, Goleta, California, USA). Anaesthetized fish were initiallystabilized at 7 °C for 1 h prior to intraperitoneal injection of atro-pine sulfate (1.2 mg�kg−1; Sigma-Aldrich) to block inhibitory vagaltonus to the heart and produce amaximumheart rate. Casselmanet al. (2012) using coho salmon (Oncorhynchus kisutch (Walbaum,1792)) had previously shown minimal stimulatory effects on iso-proterenol on fH, and so an injection of isoproterenol was omittedhere to preclude potential adverse effects of multiple injectionsinto very small fish. fH had stabilized 15 min after the atropineinjection, when the water was incrementally heated by 1 °C per 6min until a temperature was reached that initiated cardiac ar-rhythmia (Tar). This protocol established relationship betweenmaximum fH and temperature for each fish from which the indi-vidual ABT could be determined (see below). All the fish wererecovered in fresh water at 10 °C until autonomous opercularmovements were observed, allowing fish to be returned to theholding aquaria.

Data analysisAll data in figures and tables are presented as mean values and

standard errors of the mean (SE). A two-way ANOVA and post hocHolm–Šidák test for pairwise comparisons were used to analyzefixed effects of incubation temperature (10, 14, and 16 °C) andpopulation on CTmax, ABT, Tar, maximum fH, and fH at ABT. Thepossible interaction of incubation temperature and populationwas also analyzed. All statistical analyses were conducted withSigmaPlot version 11.0 (Systat Software Inc., San Jose, California,

USA). In all cases, the level of statistical significance was based onP < 0.05. For the ABT analysis, the exponential increase in heartrate against temperature (°C) was transformed to Arrhenius plot,from which the discontinuous increase of heart rate as a functionof temperature is regard as the ABT. The ABT analysis was per-formed for each individual fish according to Yeager and Gordon(1989), and a mean value (Table 3) was calculated for each temper-ature treatment group. Migration temperatures, spawning tem-peratures, and migration distances that were used for thecorrelation analyses with CTmax were obtained from Whitneyet al. (2013). Spawning temperatures were calculated from themean historical temperature of peak spawning period. Migrationdistances of populations represent the length of spawning migra-tion route from river entrance to natal streams. Migration tem-peratures were reported for historical mean values from varioussources, as cited inWhitney et al. (2013). Graphs and linear regres-sion calculations were conducted in Origin version 8.0 (OriginLabCorporation, Northampton, Massachusetts, USA).

Results

CTmax determinations at 90 days posthatchAt 90 days posthatch, mean CTmax varied by 3.1 °C, from 22.8 ±

0.25 to 25.9 ± 0.05 °C among all temperature treatment groups(Table 2). Significant population differences were discovered atincubation temperature of 10 and 14 °C. CTmaxwas also positivelycorrelated with body mass among populations with both 10 and14 °C egg incubation temperatures (Fig. 2). Although egg massinfluenced CTmax at 90 days posthatch (Fig. 3), it was unrelated to

Fig. 1. Map of the spawning locations in British Columbia where the gametes of sockeye salmon (Oncorhynchus nerka) were collected in 2010(modified from Whitney et al. 2013). Migration distance (D) and altitude (A) are also provided for each population.

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the survival at any stage (hatch, emergence, and 90 days post-hatch) at any incubation temperatures (R2 range from 0.03 to 0.32,P > 0.07, data not shown).

At 14 °C, the variation in CTmax was negatively associated withthe historic temperature of migration and spawning, as well asthe river migration distance between the natal spawning areaand the river entrance (P values between 0.01 and 0.03; Fig. 4). Anegative correlation between CTmax and spawning temperaturewas also observed for the 16 °C incubation group (P = 0.02).

Increasing incubation temperature significantly and consis-tently decreased the CTmax in all nine populations (Fig. 2,Table 2). This effect was evident even when the range for CTmaxwas considered at each incubation temperature because they didnot overlap. CTmax values were 24.9 ± 0.2 °C at 10 °C, 23.6 ± 0.2 °Cat 14 °C, and 23.1 ± 0.2 °C at 16 °C. The Weaver Creek population,for example, had the highest CTmax of 25.9 ± 0.05 °C at 10 °C,which was reduced to 24.1 ± 0.10 °C at 14 °C and to 23.1 ± 0.21 °C at16 °C. Curiously, as well as reducing CTmax, elevating incubationtemperature also introduced greater individual variance inCTmax independent of the developmental stages. Significant in-teraction also existed between population and incubation temper-ature (P < 0.01).

CTmax determinations at similar body massCTmax was re-measured for all treatment groups when the

mean fishmass was �1 g. Mean CTmaxwas generally elevated andthe population difference was reduced to <1 °C (Table 2). Thus,smaller fish generally exhibited a greater increase in CTmax dur-ing early development even with a common rearing temperature.Thus, temperature tolerance differed with life stage and in anintraspecific manner. Furthermore, egg incubation at 14 °C re-

Table 1. The percent survival from fertilization to 90 days posthatch (first critical thermal maximum (CTmax)) fornine sockeye salmon (Oncorhynchus nerka) populations incubated at three different temperatures (10, 14, and 16 °C) tohatch and reared at 5–7 °C thereafter.

Survival (%)

Stocks Egg (n)Egg mass(mg; mean ± SE)

Incubationtemperature (°C) Hatch Emergence 1st CTmax

Mean growth rate(mg�day−1) between1st and 2nd CTmax

Harrison 1751 72.8±1.0 10 57.7 51.8 46.5 11.91797 14 47.5 21.4 13.3 5.81752 16 21.9 4.3 1.2

Weaver 2178 52.2±0.6 10 94.2 89.3 81.1 10.02209 14 85.4 12.7 4.2 10.42195 16 50.8 22.0 3.8

Gates 2362 42.7±0.4 10 69.9 48.3 41.0 7.32332 14 63.8 48.2 21.9 5.62338 16 26.6 6.7 0

Scotch 2979 35.2±0.4 10 74.4 54.4 42.7 8.43061 14 72.3 65.3 5.2 7.63023 16 55.8 27.2 0

Adams 2848 41.3±1.4 10 69.0 64.9 58.7 8.02770 14 61.3 28.6 9.3 9.62914 16 48.9 16.7 2.6

Chilko 1520 41.6±0.4 10 45.0 41.2 33.0 10.31492 14 46.1 40.6 20.4 7.51510 16 14.2 5.6 0

Horsefly 2232 36.1±0.5 10 70.1 66.4 54.4 8.22091 14 73.7 67.9 31.7 7.72274 16 51.4 24.1 0.5

Stellako 2247 34.5±0.5 10 83.5 80.0 55.5 9.62333 14 68.7 58.1 10.8 9.62209 16 42.6 22.8 0

Okanagan 2992 38.1±0.6 10 70.0 64.7 55.0 10.33042 14 68.8 22.9 7.9 8.53070 16 41.5 15.9 1.5

Note: Populations are ordered from shortest to longest spawning location distance from the ocean (for location refer Fig. 1). Data(except survival at 1st CTmax and mean growth rates) were abstracted from Whitney et al. (2013), where further details are found.

Fig. 2. Critical thermal maximum (CTmax) determinations for ninesockeye salmon (Oncorhynchus nerka) populations in relation to bodymass: Harrison (squares), Weaver (circles), Gates (up-facingtriangles), Scotch (down-facing triangles), Adams (diamonds), Chilko(left-facing triangles), Horsefly (right-facing triangles), Stellako(stars), and Okanagan (pentagons). CTmax was measured twice foreach population, first at 90 days posthatch when differences existedfor body mass and second time at 135–214 days posthatch whenbody mass was similar among populations (those data are boundedby the broken box). Egg incubation temperatures were 10 °C (opensymbols), 14 °C (solid symbols), or 16 °C (half-solid symbols).Regression lines were fitted to the first set of data for incubationtemperatures of 10 °C (broken line) and 14 °C (solid line).

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sulted in a CTmax that was positively associated with the migra-tion distance, migration temperature, and spawning temperature(P values of 0.02–0.03), the opposite relationship obtained at 90days posthatch (Fig. 4).

Although growth rate remained lower for most populationsincubated at 14 °C when compared with 10 °C (Table 1), hatchlinggrowth clearly compensated for the depressive action of elevatedincubation temperature on CTmax (Fig. 2). For example, whenincubated at 10 °C, Scotch Creek hatchlings weighed 0.3 ± 0.01 gand had the lowest CTmax at 90 day posthatch (24.2 ± 0.04 °C), butCTmax increased to 26.1 ± 0.03 °C when fish had reached 1.2 ±0.05 g. In contrast, Weaver Creek hatchlings that already weighed0.50 ± 0.02 g at 90 days had a similar CTmax when it was re-measured at 1.1 ± 0.05 g about 62 days later. The body mass effectson CTmax were exacerbated for the 14 °C egg incubation temper-ature because of the interaction between incubation temperatureand hatchling body size (Fig. 2). There was also interaction be-tween population and incubation temperature (P < 0.01), because,e.g., the Gates population CTmax was higher at 14 °C incubation

temperature than at 10 °C, while the opposite was true for theother populations.

Maximum fH and ABTMaximum fH measurements were limited to four populations

(Gates, Weaver, Chilko, and Okanagan) from 10 and 14 °C incuba-tion temperatures and when they weighed 1.47 ± 0.09 to 2.03 ±0.11 g. Each of the eight treatment groups presented a clear ABT inmaximum fH (Table 3, Figs. 5A, 5B). However, ABT, Tar, and fH atABT for eggs incubated at 10 °C (Table 3) were similar amongpopulations. Instead, the peak fH attained was highest for Weaverand lowest for Okanagan despite a considerable period of rearingat a common temperature (Fig. 5A). In contrast, for eggs incubatedat 14 °C, significant population differences existed for ABT and thepeak fH, but not for Tar and fH at ABT. Chilko had the lowest ABT,but the highest mean fH at the temperature from 7 to 19 °C(Fig. 5B). Gates had the highest ABT andOkanagan had the highestpeak fH. Compared with the egg incubation temperature of 10 °C,14 °C significantly decreased ABT in Chilko by 1.9 °C, whileincreased ABT in Gates by 1.5 °C. Tar was also significantly in-creased by 1.5 °C in Okanagan when incubated at 14 °C. For peakfH, Okanagan at 14 °C was 21 beats�min−1 higher than the fish at10 °C (Table 3). There were significant interactions between incu-bation temperature and population in Topt (P < 0.01), peak fH(P < 0.01), and Tar (P < 0.01).

DiscussionIn general, broadly distributed species are often exposed to

various thermal environmental temperatures. Consequently,unique thermal regime of habitats could lead to local adaptationsassociated with genetic isolation. Embodied in these adaptations(such as timing of spawning migration, habitat selection, temper-ature tolerance, etc.) is the intraspecific capacity to survive cli-mate change. Our study in British Columbia sockeye salmon frydemonstrated that locally adapted populations indeed have po-tential to be selected and adapt to warming. However, the initialdifferences between populations seem to disappear as fish growand are reared at common garden environment. Thus, the degreeof local adaptation might be rather limited in this respect and forthis life stage. The ability of the populations to adapt to warmingalso will be discussed below.

Here, the intraspecific differences in CTmaxwere shown for thefirst time to be closely related to egg mass, fry mass, spawningmigration distance, and spawning temperature. For the FraserRiver sockeye salmon, these traits are known to be interrelatedbecause longer migrations tend to occur in warm interior lakesand rivers, and longer migrations are associated with a smalleregg size, which results in a smaller fry at hatch (Crossin et al.

Table 2. Critical thermal maximum (CTmax; mean ± SE) of nine sockeye salmon (Oncorhynchus nerka) populations,whose eggs had been incubated at 10, 14, and 16 °C, and reared at 5–7 °C thereafter.

CTmax (°C) to 90 days posthatch CTmax (°C) to common body mass

Population 10 °C 14 °C 16 °C 10 °C 14 °C

Harrison 25.6±0.04a 24.8±0.08a* 23.8±0.36*,† 25.7±0.04b 25.4±0.06ab*Weaver 25.9±0.05a 24.1±0.10b* 23.1±0.21*,† 25.6±0.05bc 25.1±0.13c*Gates 24.3±0.08b 23.0±0.17e* NA 25.3±0.15c 25.6±0.08a*Scotch 24.2±0.04b 23.5±0.16cd* NA 26.1±0.03a 25.5±0.1ab*Adams 25.4±0.04a 23.9±0.17bc* 22.8±0.29*,† 25.7±0.03b 25.4±0.05ab*Chilko 24.4±0.06b 23.5±0.09cd* NA 25.7±0.05ab 25.6±0.05aHorsefly 24.5±0.07b 23.2±0.14d* NA 25.8±0.04ab 25.5±0.08ab*Stellako 24.6±0.06b 23.2±0.14d* NA 25.8±0.04ab 25.4±0.1abc*Okanagan 25.6±0.05a 23.4±0.11d* 22.8±0.25*,† 25.7±0.05b 25.2±0.11bc*

Note: Different letters indicate significant differences (P < 0.05) among populations under the same incubation temperature withineach trail. Asterisks indicate significant differences (P< 0.05) in CTmax between 10 °C and either 14 or 16 °C. Crosses indicate significantdifferences (P < 0.05) between 14 and 16 °C. NA, no fish were analyzed. The number of fish (n) for each CTmax determination at 90 daysposthatchwas 20–24, except for Harrison at 16 °C (n = 13). The number of fish for each CTmax determination at common bodymass was19–20.

Fig. 3. Critical thermal maximum (CTmax) measured at 90 daysposthatch in relation to dry egg mass for nine sockeye salmon(Oncorhynchus nerka) populations reared at different egg incubationtemperatures: Harrison (squares), Weaver (circles), Gates (up-facingtriangles), Scotch (down-facing triangles), Adams (diamonds), Chilko(left-facing triangles), Horsefly (right-facing triangles), Stellako(stars), and Okanagan (pentagons). Regression lines were fitted tothe data for the three egg incubation temperatures: 10 °C (opensymbols), 14 °C (Solid symbols), and 16 °C (half-solid symbols).

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2004). Although the intraspecific variation in CTmax and effect ofincubation temperature on CTmax are novel discoveries and pro-vide hints at what factors might contribute to the populationvariability in temperature tolerance, they will make generaliza-tions on the effects of elevated temperature all the more difficultat the level of a watershed. For example, the relatively low uppertemperature tolerance of adult Weaver Creek sockeye salmoncompared with other populations has resulted in significant mor-tality during spawning migration (Lee et al. 2003; Farrell et al.2008). Yet here, Weaver Creek hatchlings were among the mosttemperature tolerant of the nine populations at 90 days posthatch(Table 2), driven largely by having one of the largest body masses

after hatch (Fig. 2) in association with a short migration distanceand large egg mass (Figs. 1, 2). Weaver Creek was also one of thepopulations least affected by adverse egg incubation temperaturein survival (Table 1). Thus, enhanced temperature tolerance ofyoung may compensate for reduced temperature tolerance of theparents in this particular population.

The difficulty in generalizing about temperature toleranceprobably derives from the heterozygous environment and multi-ple ecotypes that salmon experience throughout their life history,especially for those that undergo long-distance migrations. Weprovide clear evidence here that temperature tolerance of sockeyesalmon is very finely tuned at different life stages for each popu-

Fig. 4. Critical thermal maximum (CTmax) in relation to adult river migration temperature, spawning temperature, and migration distancefor nine sockeye salmon (Oncorhynchus nerka) populations incubated at 10, 14, and 16 °C: Harrison (squares), Weaver (circles), Gates (up-facingtriangles), Scotch (down-facing triangles), Adams (diamonds), Chilko (left-facing triangles), Horsefly (right-facing triangles), Stellako (stars), andOkanagan (pentagons). Solid symbols and regression lines represent the CTmax at 90 days posthatch, while open symbols and regression linesrepresent the CTmax for fish at a similar body mass.

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lation. At 90 days posthatch, coastal populations of sockeyesalmon had higher CTmax than the interior populations. Thehigher temperature tolerance during early life stages could bene-fit egg and hatchling development in coastal sockeye salmon inBritish Columbia because they inhabit warmer creek water dur-ing winter and spring. Their short migration distance enables

them to have energy to conceive bigger eggs (Crossin et al. 2004),which can then compensate for higher incubation temperature.Indeed, others have previously shown that a large yolk mass canbuffer against untoward effects of elevated incubation tempera-ture on survival and growth of hatchlings (Beacham and Murray1985; Ojanguren and Braña 2003; Finstad and Jonsson 2012). Wesuggest a similar buffering effect on CTmax, a proposition thatneeds to be experimentally tested but one certainly supported bythe significant correlation between egg mass and CTmax demon-strated here, which was independent of incubation temperature.Such benefits, however, could be short lived because by 1 g, dif-ferences in CTmax had largely disappeared and we surprisinglyfound that interior fish became more temperature tolerant thanthe costal populations. A cautionary note here is that populationswith the larger eggs and fry were younger (minimally 135 daysposthatch), whereas the smallest eggs and fry had required up to4.5 months to reach this body mass. The key implication here isthat both development stage and overall massmust be consideredin future comparisons of temperature tolerance among juvenilesalmon. It is still, however, unclear whether the plasticity is theresult of a body mass constraint or an adaptation to differentialontogenetic selection pressures.

The optimum incubation temperature for sockeye salmon isregarded between 4 and 12.5 °C (McCullough et al. 2001), whichencompasses 10 °C used here. Brett (1952) reported CTmax mea-surements for 4.7 month posthatch sockeye salmon at a similarbody mass (0.87 g) as our common mass determination. TheirCTmax of 24.4 °C lies at the lower end of the range (24.2–25.9 °C)in our first determination, but is lower than the second determi-nation in this study when our fish had a slightly larger bodymass.

As in previous studies, incubation temperature had strongpopulation-specific effects on offspring survival (Table 1). For ex-ample, survival at emergence with a 14 °C incubation ranged from67.9% for Horsefly to 12.7% for Weaver, and survival decreased to31.7% and 4.2% at 90 days posthatch, respectively. Survival beyond90 days posthatch and through to �1 g body mass was stableamong populations with incubation temperatures of 10 °C (87%–97%) and 14 °C (90%–94%), but not at 16 °C (32%–52%) (data notshown). Thus, despite a common incubation temperature post-hatch, elevated egg incubation temperature had considerablepopulation-specific survival consequences until long after hatch-ing. The question then arises as to what effect this population-specific mortality has on CTmax. The common prediction of theeffect is that the least tolerant individuals would be the ones thatdied. Thus, mean tolerance of a population should increase. How-ever, we did not find the relationships between survival rate andCTmax in and between any of the incubation temperatures. More-over, on the surface it seems that the deleterious effect of elevatedincubation temperature not only caused higher mortality, but

Table 3. Body mass, Arrhenius breakpoint temperature (ABT), temperature when cardiac arrhythmia first started(Tar), heart rate (fH) at ABT, and the peak fH attained for four selected populations of sockeye salmon (Oncorhynchusnerka), whose eggs had been incubated at 10 and 14 °C, and reared at 5–7 °C thereafter.

Temperature (°C) fH (beats�min−1)

Incubationtemperature (°C) Population (n) Mass (g) ABT Tar ABT Peak Q10

10 Weaver (11) 1.72±0.11ab 16.0±0.4 24.1±0.4 102.73±2.7 142.79±2.8a 2.1/1.6Gates (12) 2.03±0.11a 15.6±0.5 24.0±0.3 101.07±3.8 138.94±3.4ab 2.1/1.6Chilko (11) 1.48±0.11b 16.3±0.4 24.2±0.2 102.94±3.2 136.51±5.0ab 2.2/1.5Okanagan (12) 1.89±0.11a 16.8±0.6 23.0±0.7 95.80±5.8 124.60±6.3b 2.2/1.6

14 Weaver (14) 1.65±0.10 15.4±0.4ab 23.2±0.4 95.79±2.8 127.30±4.7b* 2.1/1.5Gates (11) 1.60±0.11* 17.1±0.5a* 24.4±0.5 107.55±3.9 142.60±5.0ab 2.1/1.6Chilko (9) 1.47±0.09 14.4±0.3b* 23.1±0.6 101.80±4.6 133.21±5.2ab 2.3/1.3Okanagan (11) 1.78±0.11 16.7±0.6a 24.5±0.4* 105.36±3.1 145.66±3.5a* 2.1/1.6

Note: Different letters indicate significant differences (P < 0.05) between populations under the same incubation temperature.Asterisks indicate significant differences (P < 0.05) between incubation temperatures for each population. The thermal sensitivity ofheart rate (Q10) before and after ABT is also presented.

Fig. 5. Arrhenius plots of maximum heart rate (fH) for four selectedsockeye salmon (Oncorhynchus nerka) populations whose eggs wereincubated at 10 °C (A) and 14 °C (B). The Arrhenius breakpointtemperature (ABT) for the mean data are the intersection of the twolinear regression lines for each data set, which is for illustrativepurposes because the actual ABT was based on an analysis of ABTfor individual fish rather than that for the mean data as shown here.Data points represent mean values of ln(fH) with SE bars. Whenconnected by a line in each population, all data points have thesame sample size as shown in Table 3. Solitary points are mean datafor at least nine fish because the remainder of the fish had becomearrhythmic at a lower temperature and were excluded from thelarger data set.

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also reduced CTmax of the surviving juvenile offspring, as evi-denced, for example, by the coexistence of low survival and CT-max for Chilko incubated at 10 °C, and the dramatic decrease insurvival and CTmax for Weaver eggs incubated at 14 °C. The del-eterious effect of adverse incubation temperature could be a pos-sible explanation of the reduced CTmax, which needs to beexamined. But also it may be misleading because of the inverserelationship between incubation temperature and bodymass andthe direct relationship between body mass and CTmax in thecurrent study (Fig. 1).

The effect of fry size posthatch on CTmax is a novel discoverythat could have important implications in a global warming sce-nario. Besides the intraspecific differences of hatchling size, in-creasing incubation temperature reduces fry mass (here andpreviously, e.g., Beacham and Murray 1985; Ojanguren and Braña2003; Finstad and Jonsson 2012), likely because of a reduced aero-bic scope and capacity for growth (Pörtner 2010). Reduced fry size,however, correlated negatively with CTmax, explaining some ofthe population variation in CTmax. Thus, a lower CTmax can nowbe added to a growing list of deleterious effects associated withhigh egg incubation temperature, which includemortality, devel-opmental abnormalities (Zummo et al. 1996; Albokhadaim et al.2007; Kurokawa et al. 2008; Dionísio et al. 2012), behavior (Burger1990), temperature selection (O’Steen 1998), and swimming per-formance (Carey and Franklin 2009). Therefore, small salmonhatchlings can be more susceptible to extremely warm tempera-tures until they gain bodymass, an ontogenetic shift that could berelated to the progressive switch from cutaneous- to gill-mediatedoxygen uptake (Wells and Pinder 1996; Rombough 1997;Schönweger et al. 2000) particularly if temperature tolerance isrelated to the capacity to supply oxygen to tissues at higher tem-peratures (Pörtner and Knust 2007). Even so, egg mass, growthrate, and fry size did not explain all the variation of temperaturetolerance among locally adapted populations and incubation tem-perature treatments, which means that other underlying factors(such as the deleterious effect we referred before and trade-offs ofhigh temperature survival) explaining differences in thermal tol-erance await future research. Besides the constraint of bodymass on CTmax, the temperature–size rule (hotter is smaller;Kingsolver and Huey 2008) suggests the possibility of an adaptivebenefit if a process of sustained adaptation to high temperatureselect for thermally tolerant individuals. For example, a potentialcapacity for populations to adapt to increased incubation temper-ature could accrue from a shortened development time limitingthe adverse effect of high temperature on embryo development.Parental thermal history is an additional factor that could havepotential importance in shaping the CTmax of offspring via trans-generational effect (Donelson et al. 2012), an effect that is verylikely to be more pronounced under harsh environments (Einumand Fleming 1999). We have demonstrated that the thermal expe-rience of parent during the spawning migration was significantlycorrelated to temperature tolerance (Fig. 4), although the mecha-nisms are unclear.

CTmax is an index of short-term temperature tolerance. There-fore, physiological temperature optimamay havemore ecologicalrelevance in terms of long-term survival. Indeed, the conceptualmodel of oxygen- and capacity-limited thermal tolerance, which isgaining prominence, emphasizes the importance of the optimumtemperature for aerobic scope (Farrell 2002; Pörtner and Knust2007; Pörtner and Farrell 2008). Within this concept, it has beenproposed for adult salmon that the heart, and specifically maxi-mum fH, may trigger the limitation in oxygen delivery associatedwith Topt of aerobic scope (Steinhausen et al. 2008; Farrell 2009;Eliason et al. 2011). Furthermore, Casselman et al. (2012) recentlyshowed that Topt for aerobic scope and the ABT for maximum fHwere coincident in juvenile coho salmon. Thus, the measure-ments of ABT and maximum fH made here for four populationsmay have ecological relevance. Indeed, cardiac arrhythmias devel-

oped at a temperature 1.3–2.7 °C lower than the CTmax, suggest-ing that cardiac failure is already underway before fish lose theirrighting reflex. This result is consistent with the previous findingsthat the cardiac life support system not only has failed to keep upwith the increasing oxygen demand of warming, but is also show-ing signals of failing to function properly (Braby and Somero2006). A cautionary note for this comparison is the rate of heatingwhich differed between CTmax and fH tests. Methodology andwarming rates are known to affect measurements of thermal lim-its (Santos et al. 2011).

ABT of sockeye salmon averaged about 16.1 °C for the 10 °Cincubation temperature and 15.9 °C for the 14 °C incubation tem-perature. Both values are close to the preferred physiological andoptimal temperatures of different populations of sockeye salmon(14–18 °C) (Brett et al. 1969; Brett 1971; Eliason et al. 2011). WhereasABT did not differ among the four populations when incubated at10 °C, Chilko sockeye salmon had significantly lower ABT whenincubated at 14 °C and a higher maximum fH across all tempera-tures. Although incubation temperature is known to altercardiac differentiation during development (Zummo et al. 1996;Kurokawa et al. 2008), this is the first evidence for incubationtemperature having a functional effect in fish, influencing ABT formaximum fH. Furthermore, the higher maximum fH may indicatethat Chilko juveniles have a high cardiac capacity compared withother sockeye populations, a conclusion also reached for adultChilko sockeye salmon (Eliason et al. 2011). However, further stud-ies are needed to detail the associations between cardiac capacityand temperature tolerance. Biochemical changes, such as en-zyme, hormone (O’Steen and Janzen 1999), protein (Krone et al.1997), and nucleic acid (Høie et al. 1999) content are related toincubation temperature. Studying whether and how these factorscontribute to the alterations of the temperature tolerance will beimportant. Similarly, further study is needed to discover why ahigher incubation temperature increased variance of CTmaxacross populations. Consistent with the previous discoveries ofother traits (Beacham and Murray 1985; Burt et al. 2012; Whitneyet al. 2013), the increased variance of phenotypic traits at indi-vidual and population levels was the reflection of the inequal-ity in coping with adverse environments, thus, it has adaptivesignificance.

In summary, temperature tolerance and growth at the earlydevelopment period of fry were closely related to and affected bythe egg incubation temperature. Clear evidence for the local ad-aptation among sockeye salmon populations and developmentalplasticity in terms of temperature tolerance was revealed fromthe significant population differences discovered in this study. Atthe same time, at least from the perspective of CTmax, the capac-ity for thermal adaptation seems to be limited, which then couldbe viewed as a constraint. There arewider debates around thermaladaptation under a climate change scenario. Therefore, our sug-gestion must be tempered by the caveat that not all sockeye pop-ulations have been studied and the full extent of individualvariability has not been assessed. A few temperature tolerant in-dividuals could easily act as founders for a new population, andthese individuals are unlikely to be represented in mean values.Furthermore, low genetic variance in temperature tolerance (if itis the case for species in the wild) does not have to be a geneticconstraint for adaptation (Walters et al 2012). For sockeye salmon,the adaptive relations between temperature tolerance, egg size,growth, and transgenerational effects remain complex and war-rants further study.

AcknowledgementsWe thank J. Mann from EWOS Canada Ltd.; M. Casselman and

all members of the A.P. Farrell laboratory; and N. Sopinka, A.Lotto, and all members of the S.G. Hinch laboratory for the assis-tance with this study. Funding for this project was provided by agrant from the China Scholarship Council to Z.C., a grant from the

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Academy of Finland to K.A., a postgraduate scholarship from theNatural Sciences and Engineering Research Council of Canada(NSERC) to C.K.W., and NSERC Discovery Grant to S.G.H. andA.P.F. A.P.F. holds a Canada Research Chair.

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