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Population Origin and Water Temperature AffectDevelopment Timing in Embryonic Sockeye SalmonC. K. Whitneya, S. G. Hincha & D. A. Pattersonb

a Pacific Salmon Ecology and Conservation Laboratory, Department of Forest andConservation Sciences, University of British Columbia, 2424 Main Mall, Vancouver, BritishColumbia V6T 1Z4, Canadab Fisheries and Oceans Canada, Science Branch, Cooperative Resource ManagementInstitute, School of Resource and Environmental Management, Simon Fraser University,Burnaby, British Columbia V5A 1S6, CanadaPublished online: 11 Sep 2014.

To cite this article: C. K. Whitney, S. G. Hinch & D. A. Patterson (2014) Population Origin and Water Temperature AffectDevelopment Timing in Embryonic Sockeye Salmon, Transactions of the American Fisheries Society, 143:5, 1316-1329, DOI:10.1080/00028487.2014.935481

To link to this article: http://dx.doi.org/10.1080/00028487.2014.935481

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ARTICLE

Population Origin and Water Temperature AffectDevelopment Timing in Embryonic Sockeye Salmon

C. K. Whitney and S. G. Hinch*Pacific Salmon Ecology and Conservation Laboratory, Department of Forest and Conservation

Sciences, University of British Columbia, 2424 Main Mall, Vancouver, British Columbia V6T 1Z4,

Canada

D. A. PattersonFisheries and Oceans Canada, Science Branch, Cooperative Resource Management Institute,

School of Resource and Environmental Management, Simon Fraser University, Burnaby,

British Columbia V5A 1S6, Canada

AbstractPredicting the future impact of changing thermal regimes on life history stages for wild fish requires a better

understanding of the relative importance of population origin and offspring size on embryonic development. Weassessed hatch timing and offspring size of Sockeye Salmon Oncorhynchus nerka in relation to egg size (variationfrom full-sibling families), population origin, and temperature (three treatments of 10, 14, and 16�C). Both hatchtiming and hatch duration varied by the interacting effects of population origin and thermal treatment, shown incrossing reaction norms. Hatching was faster, yet more variable, at higher temperatures across many groups, sowhile fish generally hatched faster, developmental asynchrony also increased among families. On average, fishincubated at 16�C were shorter but not lighter at hatch, showing developmental tradeoffs between basal metabolicrequirements and growth. Egg size decreased among populations as migratory distance increased, but developmentrates were not related to egg size. In this case, embryonic development rates were linked to temperature andpopulation-specific cues for hatch timing more than to the maternal influence of egg size.

Within species, genetically distinct populations are likely to

differ in parentally mediated developmental qualities, such as

offspring size and reproductive strategies related to local adap-

tation (in fish: Brannon 1987; Jensen et al. 2008; Hutchings

2011; in birds: Charmantier et al. 2008). In fish, offspring sur-

vival during early development is a critical indicator of popu-

lation viability over time (Bradford 1995; Jensen et al. 2008).

Temperature is a regulatory factor that affects most biological

processes in ectotherms; elevated temperature can increase

basal metabolism and speed development rates, affecting

embryogenesis, offspring size, growth, and survival (Velsen

1987; Pankhurst and Munday 2011). Salmonids are

particularly susceptible to temperature changes during their

sessile embryonic stage and mobility-limited posthatch stages

(Brannon 1987) when significant shifts in temperature can

result in sublethal or lethal effects on developing eggs and lar-

vae (e.g., Velsen 1987; Blaxter 1992). With small tolerance

limits around thermal optima (Rombough 1997), adaptation to

thermal conditions during embryonic stages is of critical

importance (Janhunen et al. 2010).

Within the different species of Pacific salmon Oncorhyn-

chus spp., genetically distinct populations display measureable

physiological and behavioral differences linked to their unique

life histories and the adaptive strategies employed to maximize

*Corresponding author: scott.hinch@ubc.caReceived March 10, 2014; accepted June 3, 2014

1316

Transactions of the American Fisheries Society 143:1316–1329, 2014

� American Fisheries Society 2014

ISSN: 0002-8487 print / 1548-8659 online

DOI: 10.1080/00028487.2014.935481

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fitness (Taylor 1991; Hodgson and Quinn 2002; Fraser et al.

2011). Adaptive differences to environmental conditions

among populations have been observed in the spawning period

(Hodgson and Quinn 2002; Eliason et al. 2011), prompting the

question of whether this adaptive diversity persists to the

embryo and early-development stages. In the Fraser River of

British Columbia, migration effort, elevation change, and

migration distance vary among coastal-spawning populations,

with short migrations of »20 km and long migrations for inte-

rior-spawning populations, some of which travel over

1,200 km to reach their natal spawning streams (Groot and

Margolis 1991). Fraser River Sockeye Salmon Oncorhynchus

nerka provide a good model for examining the interaction of

incubation temperature, population origin, and egg size on

early development (see Whitney et al. 2013 for thermal toler-

ance in terms of survival on these same populations).

Offspring size and viability are influenced by the maternal

traits of egg size, thermal history, and population adaptation

to environmental conditions (Jonsson et al. 1996; Jonsson

and Jonsson 2011). Egg size plays an important role in the

development of fish, affecting offspring size, morphology,

and competitiveness (Bagenal 1969; Brooks et al. 1997).

Developmental timing cues control annual movement pat-

terns in highly migratory species, such as salmonid fish, and

these cues are mediated by environmental and genetic influ-

ences, such as temperature and population origin. Experimen-

tally, incubation temperature is likely to affect thermally

adapted populations differentially depending on their histori-

cal thermal regime. Previous research suggests that at a com-

mon temperature embryos from populations with cooler

incubation environments (cool-experienced populations)

develop faster than embryos from populations with warmer

incubation environments (warm-experienced populations), an

adaptive response that may reduce thermally mediated hatch-

ing and emergence asynchrony among groups (e.g., Brannon

1987; Beacham and Murray 1990). Beacham and Murray

(1989) observed that under the same incubation treatment, a

cool-experienced population produced longer and heavier off-

spring than a warm-experienced population relative to egg

size, a response attributed to differences in yolk conversion

efficiency (Beacham and Murray 1987, 1989). The postemer-

gent competitive benefits of large eggs (e.g., larger alevin

and fry, improved offspring condition, lower immediate

exogenous energy requirements, and improved competitive-

ness) may be more important than egg number when consid-

ering the additive negative consequences of elevated

incubation temperature on offspring viability (Kinnison et al.

2001; Braun et al. 2013).

The evolution of developmental phenology affects a species

response to climate change and drives adaptation to shifting

environmental conditions (Hodgson and Quinn 2002;

Bradshaw and Holzapfel 2008; Jensen et al. 2008). Hatch and

emergence timing varies among populations to reflect local

spawning conditions and thermal patterns (Beacham and

Murray 1987, 1989; Brannon 1987; Berg and Moen 1999) and

is related to migration timing to the ocean (Beacham 1988).

Over time, environmental conditions at hatch and emergence

have resulted in a well-timed development sequence to maxi-

mize fitness and population-wide survival; a sequence that is

likely to be affected by temperature shifts (Tallman 1986;

Blaxter 1992; Pankhurst and Munday 2011).

For juvenile fish, accumulated thermal units (ATUs), or

degree-days, represent the sum of temperature exposure since

fertilization and can be used as a means to predict develop-

mental events in early life history (Burt et al. 2012b). While

less commonly evaluated in an experimental context (but see

Springate et al. 1984; Beacham and Murray 1988; Murray

et al. 1990; Berg and Moen 1999), hatch timing is closely

associated with emergence timing (Crisp 1988). Hatch timing

has consequences for the survival of developing embryos

within gravel redds related to environmental variables, includ-

ing dewatering, oxygen availability, and gravel ice in spring

(Cope and Macdonald 1998). Measuring hatch duration can

describe developmental synchrony within a population and

habitat adaptation across populations. Hatch synchrony tends

to decrease under suboptimal conditions, which has implica-

tions for population viability, but little is known about this

relationship as this aspect of development timing is rarely

explored in salmonids (Kamler 2002; Burt et al. 2012b).

The objective of this study was to explore the influence of

population, incubation temperature, and egg size on develop-

ment timing and offspring size at hatch in Sockeye Salmon. A

previous study looked at survival (Whitney et al. 2013), an

important metric to estimate fitness but one that provides an

incomplete picture; development timing and offspring size are

both key parameters for determining early life competitive

advantage among populations. In this study, we assessed popu-

lation-level differences in offspring development rates and ale-

vin size at hatch using three incubation temperature treatments

(10, 14, and 16�C). Temperatures were chosen to span ther-

mally optimal, elevated, and climate-change-associated high

incubation temperatures for the species during early embry-

onic development (McCullough et al. 2001). We predicted

that (1) within a common temperature, development timing

would vary by population, and specifically that embryos from

populations that spawn at cooler temperatures would develop

faster than populations that spawn at warmer temperatures.

Thus, while warmer incubation temperature should result in

faster development overall, population differences in hatch

timing will emerge, especially at the more “stressful” high

temperatures. Additionally, we predicted that (2) alevin size

(i.e., length and mass) would be negatively related to time to

hatch, as yolk conversion efficiency would be reduced at high

temperatures, so that those fish that developed faster in ele-

vated temperatures would hatch as smaller alevin. In addition,

we discuss some of the potential ecological consequences of

changes in hatch timing and alevin size relevant to the differ-

ent populations.

HATCH TIMING AMONG SOCKEYE SALMON POPULATIONS 1317

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METHODSOffspring collection.—This study used nine populations of

Sockeye Salmon from the Fraser (n D 8) and Columbia (n D1) rivers. The Fraser River populations are all abundant, geo-

graphically distinct populations within the watershed, which

has a variety of migration distances and spawning conditions,

and they display a range of life history characteristics (See

Whitney et al. 2013 for details; Figure 1). The populations

vary in thermal history during spawning and incubation, which

is related to both spawn timing and the environmental charac-

teristics of the natal streams (i.e., warmwater inlet versus gla-

cial runoff) (Table 1).

Gametes were collected from 12 to 20 pairs of repro-

ductively mature male and female Sockeye Salmon that

were collected from the spawning grounds of each

population. Adults were sacrificed by cerebral concussion

and measured for size parameters (fork length, postorbital

hypural length, postorbital fork length, total mass), and

eggs and milt were hand expelled and collected in clean,

dry plastic containers. All containers were immediately

oxygenated and chilled to 0–4�C for immediate transporta-

tion to the laboratory facilities at the University of British

Columbia. As some populations were geographically iso-

lated and transport to the laboratory took much longer than

for others, all groups were fertilized at a standardized 24 h

after collection. Previous work has shown that transporting

unfertilized gametes results in higher survival than trans-

porting activated, developing eggs (Jensen and Alderice

1983) and that salmonid eggs and sperm will remain viable

with a 95–100% fertilization potential for up to 5 d as

long as temperature is low and sufficient oxygen levels are

maintained within the containers (Jensen and Alderice

1984).

Fertilization protocol and incubation methods.—Gametes

were crossed by a randomized mating design in which

each male was paired once with each female (n D 12–20

families/population) using a dry fertilization method

(details in Patterson et al. 2004). Individual family baskets

were then randomly distributed in vertical-stack Heath

incubators, with single replicates of each family at 10, 14,

or 16�C.Fertilized eggs were monitored and maintained according

to the methods used in Whitney et al. (2013). Mortality

between fertilization and hatching was significantly higher for

all populations at the 16�C treatment (45 § 27% [mean §SD], across all groups), versus 15 § 15% at 14�C, and only 7

§ 16% at 10�C (for details and survival analysis, see Whitney

et al. 2013).

Once hatching was observed for any family in a popula-

tion at a given temperature, newly hatched alevin were

recorded daily and hatching rate and duration were moni-

tored. Within 1 d of each population’s 90–95% hatch point,

five alevin (when available) from each family were mea-

sured for length and weight at hatch. Alevin were eutha-

nized in dilute MS-222 (tricaine methanesulfonate), blotted

to remove excess moisture, weighed (§0.01 mg), and mea-

sured for length (length from nose to visible end of body

tissue [LS]; §0.5 mm). In cases of low survivorship within

a family, as many alevin as were available were measured

(<5) as among family means were used for population val-

ues, and those families with no remaining alevin were

excluded from the analyses.

Data analysis.—All statistical analyses were based on

population means (i.e., averages of family values for the off-

spring of each mating pair). Daily counts of egg hatching

were used to describe ATUs prior to first hatch (H0), 5%

hatch (H5), median hatch date (H50), and hatching duration

(HD; number of days between 5% and 95% hatch per family).

These metrics were chosen because they represent early

FIGURE 1. Map of the study populations in the Fraser River watershed and

the upper Columbia River within British Columbia. Embryos and adult sam-

ples from each group were transported back to laboratory facilities at the Uni-

versity of British Columbia in Vancouver, British Columbia, for fertilization,

incubation, and husbandry throughout early development. Map courtesy of

Whitney et al. 2013.

1318 WHITNEY ET AL.

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TABLE1.

EnvironmentalcharacteristicsandecologyforeightpopulationsofSockeyeSalmonfrom

theFraserRiver

watershed

andonepopulationfrom

theColumbia

River

watershed

(Okanagan

River).Peakspaw

ningdateandmean,maxim

um,andminim

um

spaw

ningtemperaturesforFraserRiver

populationsarereported

from

a10-d

periodencompassingtheestimated

meanpeakspaw

ning

dateduringtheyears1990–2010.Peakriver

entrydates

inparentheses

reflectrecentshiftsin

runtimingto

earlierriver

entry.

Populationa

Characteristics

Gates

Creek

Scotch

Creek

Chilko

River

Horsefly

River

Stellako

River

Okanagan

River

Adam

s

River

Weaver

Creek

Harrison

River

Run-tim

inggroup

Early

summer

Early

summer

Summer

Summer

Summer

ColumbiaRiver

Late

Late

Late

Peakriver

entry

Jul31

Jul31

Aug11

Aug11

Aug11

Jun15

Sep

27

(Sep

12)

Sept27

(Aug27)

Sept27

(Aug27)

Historicalpeakspaw

ndate

Sep

3Sep

10

Sep

28

Sep

10

Sep

28

Oct17

Oct11

Oct19

Nov12

Collectiondate(2010)

Aug31

Sep

8Sep

21

Sep

27

Oct1

Oct14

Oct18

Oct25

Nov10

Dry

eggmass(m

g;mean§

SD)

42.7§

2.6

35.1§

3.0

41.6§

2.4

35.9§

3.6

34.5§

3.2

38.4§

4.5

41.3§

6.1

52.2§

4.4

72.8§

6.8

Mean§

SDspaw

ning

temperature

(�C)

9.59§

0.76

10.84§

2.75

9.95§

1.3912.72§

1.9210.95§

2.33

12.9

11.81§

1.9610.43§

1.418.50§

1.13

Maxim

um

§SDspaw

ning

temperature

(�C)

10.22§

0.90

11.92§

2.79

10.83§

1.1614.06§

1.9811.97§

2.44

Nodata

13.07§

2.0111.57§

1.489.09§

1.29

Minim

um

§SDspaw

ning

temperature

(�C)

8.90§

0.70

9.46§

3.02

8.45§

2.7511.21§

1.91

9.81§

2.27

Nodata

9.95§

2.66

9.42§

1.527.73§

1.40

aSourcefortheFraserRiver

populations:PacificSalmonFoundation–FisheriesandOceansCanada.Sources

fortheOkanagan

River

population:HodgsonandQuinn(2002);Hyattet

al.(2003);S.Folks,

Okanagan

NationAlliance,personalcommunication.

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development (H0, H5), average population incubation

requirements (H50), and the incubation requirements for the

majority of offspring within a population to successfully

hatch (a measure of developmental synchrony, HD). Dry egg

mass, alevin mass (MH), and alevin length (LH) at hatch were

also analyzed.

Alevin size response was assessed using a linear mixed

model with population and temperature treatment as the fixed

effects and family as the random effect. Temperature and pop-

ulation differences were tested using mixed-effect three-way

ANOVAs (Type III sum of squares), using population, tem-

perature, and family to determine the statistical significance of

the fixed effects of population and temperature, and subse-

quent Tukey’s honestly significant difference (HSD) post hoc

multiple comparisons tests for alevin size and hatch timing

analysis. All analyses were conducted using R (R Foundation:

www.r-project.org).

Population variation was assessed using a full model with

the following form:

yjk DmC Tj � PCF.Pk/CEk C ejk;

where y is the response variable (H0, H5, H50, HD, MH, or

LH), T represents the temperature treatment (j), P is the

population, E represents egg mass, and F is the individual

family identity (full-sib families; k) nested within popula-

tions. For all analyses, temperature and population were

considered fixed effects, varying by the random effect of

family. Egg size was found to be nonsignificant and was

subsequently removed. The effect of Heath stacks within

the incubation design was evaluated but was also found to

be nonsignificant and was thus also removed. Differences

among fixed effects (temperature treatments and popula-

tion) were tested using Tukey’s HSD tests.

Additionally, Pearson’s correlations were calculated to

assess the relationship between egg mass, alevin size, and

hatch timing. Regression analyses were used to compare egg

size with migration distance and offspring size (MH, LH) with

adult female fork length. The significance level for all tests

was set at a D 0.05.

RESULTS

Hatch Timing

Temperature, population, and the interaction of temperature

£ population, but not egg mass, significantly affected all

hatching characteristics (Table 2). All populations developed

faster as incubation temperature increased, but the magnitude

of this difference varied by population (Tukey’s HSD among

incubation temperatures: development at both 14�C and 16�Cwas faster than at 10�C, at 16�C it was faster than at 14�C; P< 0.0001). Alevin from the cool-spawning Chilko River had

the longest incubation time to reach hatch at 10�C (P < 0.01),

longer than the Adams, Horsefly, and Scotch populations,

which spawn at warmer temperatures (P < 0.01), and longer

than cool-spawning Harrison and Weaver populations at 14�C(P < 0.05). At 16�C, Okanagan alevin incubated the longest

to hatch (44 § 2.03 d [mean § SD]) among all populations

(P < 0.001), while Harrison fish hatched the fastest (38.1 §1.8 d; not significant) (Table 3). Considering ATUs rather

than days, all populations required more ATUs to reach hatch-

ing at higher temperatures, except for Harrison River embryos,

which hatched with lower ATUs at 16�C than at 10�C (P D0.0506; Figure 2). In general, the among-population differen-

ces reflected the same pattern as for the metric of days to 5%

hatch, whereby Chilko alevin required the longest incubation

to hatch at both 10�C and 14�C, but Okanagan populations

were the slowest to hatch at 16�C (Table 3).

Development time to median hatch (H50) was affected by

incubation temperature (ANOVA: F2, 399 D 52.1, P < 0.0001)

in the same way, with hatching occurring earlier with higher

temperatures (Figure 3). Both population and the interaction

of population £ temperature also significantly affected time to

median hatch (P < 0.0001; Table 4). Alevin from the Chilko

population required significantly more ATUs (672 § 24.85

ATUs [mean § SD]) to reach median hatch at 10�C than those

from all other populations (P < 0.001), while those from

the Adams population required less (605.5 § 19.32 ATUs)

than most other cool-experienced groups (Chilko, Gates,

Harrison, Okanagan; P < 0.001) but the same as other warm-

experienced populations (P > 0.10) (Table 3). At 14�C, most

populations required more ATUs to reach 50% hatch (661.5 §37.7 ATUs [mean § SD of all populations]; P < 0.001) than

TABLE 2. Summary statistics for mixed-model ANOVAs with family as a random effect and temperature and population as fixed effects. Egg mass was signif-

icantly different among populations (P < 0.01). The results are presented for six early life history traits: time to first hatch (H0; in both days and ATUs), hatch

duration (HD; days, 5–95% hatch), time to 50% hatch (H50; days), alevin length, and alevin mass. The F-values are shown with degrees of freedom in parenthe-

ses; asterisks represent significance (* D P< 0.01, ** D P < 0.001, n.s. D not significant).

Effect H0, days H0, ATUs HD H50 Alevin length Alevin mass

Temperature 639.16 (2)** 5.10 (2)* 37.84 (2)** 52.10 (2)** 13.49 (2)** 1.53 (2) n.s.

Population 17.29 (8)** 8.99 (8)** 15.86 (8)** 7.49 (8)** 12.95 (8)** 56.17 (8)**

Temperature £ population 6.57(16)** 5.05 (16)** 8.58 (16)** 3.39 (16)** 6.25 (16)** 1.11 (16) n.s.

1320 WHITNEY ET AL.

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TABLE3.

Summarydataofhatch

timingcharacteristicsacross

populationsandincubationtemperatures.Thecollectiondateisshownas

isthenumber

offamiliesin

each

populationto

surviveto

hatch

byincubationtemperature.Abbreviationsareas

follows:H0representsthefirsthatch

within

apopulation,H5isthe5%

hatch

within

apopulation,HDisthehatch

durationbetween5%

and95%

hatch,

H50isthemedianhatch

point,andCRindicates

ColumbiaRiver.Populationsareranked

inorder

ofcollectiondate.

Population

Measurement

Gates

Creek

Scotch

Creek

Chilko

River

Horsefly

River

Stellako

River

Okanagan

River

(CR)

Adam

s

River

Weaver

Creek

Harrison

River

Collectiondate(2010)

Aug31

Sept8

Sept21

Sept27

Oct1

Oct14

Oct18

Oct25

Nov10

Fam

ilies/population

(10� C

;14� C

;16� C

)

18;18;15

20;20;20

10;11;7

14;14;14

15;15;15

20;20;20

20;20;20

20;19;19

16;16;9

H0;days

10� C

56.7§

2.7

59.9§

2.15

63.5§

1.51

59.0§

2.94

59.7§

1.4

62.6§

1.8

59.6§

1.5

59.9§

1.35

61.4§

1.15

14� C

44.9§

2.1

43.7§

1.13

47.8§

1.84

42.1§

2.13

42.2§

1.7

45.2§

1.7

43.5§

0.9

44.1§

1.4

44§

1.2

16� C

39.3§

2.8

37.7§

2.6

41.7§

1.8

36.8§

1.7

37.8§

2.5

41.7§

3.5

38.9§

0.9

38.9§

1.85

36.7§

2.6

H5;days

10� C

58.8§

3.1

60.3§

1.4

65.5§

2.95

60.6§

2.1

60.2§

1.08

62.6§

1.2

60.1§

1.1

60.3§

1.3

62.8§

1.0

14� C

45.4§

1.85

44.2§

1.05

47.5§

1.2

44.2§

1.25

45.1§

5.34

45.9§

1.65

44.3§

1.25

44.8§

1.08

44.8§

1.2

16� C

40.5§

2.3

39.9§

1.25

42.9§

1.95

39.5§

1.0

39.9§

1.8

44.2§

2.0

40.1§

1.3

40.1§

1.6

38.1§

1.8

HD;days

10� C

9.2§

2.8

4.2§

1.5

5.2§

2.6

3.6§

1.0

2.9§

1.0

7.6§

3.5

2.8§

0.9

5.3§

2.7

5.8§

3.3

14� C

6.0§

2.6

5.35§

2.4

6.1§

1.6

4.1§

1.3

8.9§

4.8

8.0§

2.6

8.3§

2.9

6.4§

1.8

6.1§

1.9

16� C

8.1§

1.9

7.0§

1.8

7.1§

1.7

6.4§

1.7

7.8§

2.4

6.6§

1.9

8.2§

1.6

6.6§

1.6

6.9§

1.7

H50;days

10� C

63.3§

1.6

61.9§

1.2

67.2§

2.5

62.1§

1.65

60.9§

0.9

54.3§

2.6

60.6§

1.9

61.75§

1.2

64.4§

1.5

14� C

47.1§

2.2

45.75§

1.48

50.4§

3.0

45.2§

1.3

46.5§

2.6

49.5§

2.8

47.0§

2.9

47.8§

2.1

46.5§

2.0

16� C

43.7§

2.2

42.4§

1.7

45.6§

2.6

41.9§

1.5

42.4§

2.0

46.4§

2.5

43.6§

2.4

43.0§

1.9

41.2§

1.3

H50;ATUs

10� C

633.3§

16

619§

11

672§

25

621§

16

608.6§

9642.5§

25

605.5§

19

617.5§

12

644§

15

14� C

658.7§

31

640.5§

21

705§

42

633§

18

650.5§

36

692§

39

658.7§

41

670§

29

651§

28

16� C

698.6§

35

678.4§

28

729§

41

669.7§

24

678.4§

31.8

741.6§

41

696.8§

38

688§

31

659§

21

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at 10�C. In the high-temperature treatment (16�C), Adams

River alevin still required more thermal units to hatch than all

the other populations (696.8 § 37.6 ATUs; P < 0.001), and in

general the “heat sum” requirement for all populations was

greater than at cooler-temperature treatments (694.2 § 40.38

ATUs [mean § SD of all populations]; P < 0.0001).

Hatch duration (5–95% hatch within families) varied signif-

icantly by population, temperature, and the interaction of tem-

perature £ population (Figure 4; Table 3). Post hoc analysis

of temperature treatment showed hatching duration at the

10�C treatment (5.24 § 3.1 d [mean § SD]) took significantly

less time than at the 16�C treatment (7.2 § 1.9 d) across all

populations (P < 0.0001). Among populations, Gates Creek

alevin took significantly longer to reach 95% hatch (9.2 § 2.8

d) than those from most other river systems (P < 0.001; 5.24

§ 3.12 d [mean § SD of all populations]). At 14�C and 16�C,Horsefly River alevin exhibited greater hatch synchrony

among families than other groups (than Adams, Okanagan,

and Stellako; P < 0.001 at 14�C).

Egg size Across Populations

Egg mass (dry) differed among populations, and for most

populations this was inversely related to migration distance

such that longer-migrating adults produced smaller eggs (over-

all relationship; R2 D 0.39, P < 0.0001). Female fork length

described very little of the variation in egg mass across all

populations (R2 D 0.13, P < 0.0001).

The effect of egg mass was included in the original model

for each hatch-timing characteristic but was found to be non-

significant and was thus removed from the final analyses.

Days to median hatch were not correlated with egg weight at

either 14�C (P D 0.907) or 16�C (P D 0.178) but were slightly

related at 10�C (Pearson’s correlations: r D 0.168, n D 152,

P D 0.0369). Egg mass was not correlated with either days

(r D ¡0.039, P D 0.41) or ATUs to first hatch (r D ¡0.07,

P D 0.1375) across temperatures. At 10�C, egg size was only

moderately related to H5, in that larger eggs took longer to

hatch (r D 0.187, P D 0.02), while at 16�C the inverse was

true (r D ¡0.26, P D 0.0017), so that larger eggs hatched

faster.

Offspring Size

The interaction of temperature £ population was signifi-

cantly related to differences in alevin length (ANOVA: F16,

400 D 7.92, P < 0.0001) but not mass (ANOVA: F16, 399 D0.76, P D 0.7282). Across all populations, alevin were shorter

at hatch when incubated at higher temperatures than when

incubated at 10�C (P < 0.0001), while alevin mass did not

vary across incubation temperatures (Figure 5; Table 4). Egg

mass explained a great deal of the variation in alevin mass at

hatch, irrespective of thermal treatment (R2 D 0.59,

P < 0.0001), but not in alevin length (R2 D 0.05, P < 0.0001),

for which incubation temperature and population played more

of a role.

DISCUSSION

Exposure of Sockeye Salmon to high temperatures (14�Cand 16�C compared with 10�C) during incubation caused sub-

stantial differences both within and among populations in

hatch timing, hatch duration, and offspring size. Egg mass var-

ied among populations, but this trait only affected alevin mass

at hatch, not developmental timing or offspring length. Con-

sidering the fitness implications of hatch timing and offspring

size, these results suggest that Sockeye Salmon development

and offspring competitiveness may be affected by temperature

regime and that this effect will vary by population but that egg

mass is not a main driver of among-population differences in

hatching characteristics.

Hatch Timing: Populations Matter More than Egg Size

Hatch and emergence timing have ecological implications

for salmonids within natural aquatic communities, whereby

development timing cues relate to life stage survival and sub-

sequent life history transitions (Crozier et al. 2008). In gen-

eral, incubation studies suggest that development rates reflect

adaptation to local conditions (Taylor 1991; Hendry et al.

1998; Jensen et al. 2008) and changes to those thermal

FIGURE 2. Required heat sum, as measured by accumulated thermal units

(ATUs), to reach 5% hatching across all populations at three incubation tem-

peratures (10, 14, and 16�C). All populations except the cool-experienced Har-rison population required more ATUs to reach hatch at higher temperatures;

OK D Okanagan.

1322 WHITNEY ET AL.

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regimes are likely to have both biological and ecological

effects on species and ecosystems (Steel et al. 2012).

Incubation requirements did vary by population, but there

was no relationship between the development rate of embryos

and the average spawning temperature for each of the popula-

tions. Similarly, development time to median hatch was not

related to spawn date or parental migration experience

(Figure 3 versus Table 1). In theory, developmental synchrony

should be evident from early development to later life stages,

from fry emergence to smolt migration to ocean systems, and

from adult movement at sea (Godin 1982; Tallman 1986; Bea-

cham and Murray 1987, 1988; Brannon 1987). While most

research on development timing has focused on emergence

rather than hatch as discussed here, alevin hatch timing has

been linked to emergence timing (Godin 1982; Crisp 1988).

However, in this study it is not clear why some populations

hatch considerably earlier than others under the same thermal

experience (e.g., fish from the Adams River hatched 6 d earlier

FIGURE 3. The influence of incubation temperature among populations on time to median hatching from fertilization (d.p.f. D days postfertilization) at three

incubation temperatures: (a) 10�C, (b) 14�C, and (c) 16�C. Responses for all treatments are ranked by the order of populations in the 10�C treatment. The black

lines show the median response for a population, the boxes contain the data between the 25th and 75th quartiles, whiskers show the 10th and 90th percentiles,

and open circles show extreme data; OK D Okanagan

HATCH TIMING AMONG SOCKEYE SALMON POPULATIONS 1323

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TABLE4.

Measurements(m

ean§

SD)foralevin

mass(M

H)andlength

(LH)at

hatch

across

populationsunder

theinfluence

ofthreeincubationtemperatures(10,14,and16� C

).Allpopulationsare

from

theFraserRiver

exceptfortheOkanagan

River

population,whichisfrom

theColumbiaRiver.

Population

Metric

Tem

perature

(�C)

Gates

Creek

Scotch

Creek

Chilko

River

Horsefly

River

Stellako

River

Okanagan

River

Adam

s

River

Weaver

Creek

Harrison

River

MH(m

g)

10

115.3§

12.5

91.6§

7.9

110.6§

7.7

96.4§

16.0

91.1§

8.1

99.5§

11.7

105.4§

75.0

128.8§

12.9

176.1§

16.3

14

104.6§

7.9

97.0§

64.9

111.1§

8.9

93.6§

9.2

91.6§

16.4

99.4§

15.2

99.1§

10.8

123.4§

13.8

170.7§

17.2

16

107.8§

17.9

90.2§

11.6

109.0§

8.8

94.9§

10.5

90.9§

7.9

98.8§

17.4

97.9§

8.9

127.4§

13.0

166.5§

15.5

LH(m

m)

10

19.9§

1.6

19.4§

0.9

21.9§

1.0

19.7§

1.4

19.0§

0.7

20.3§

0.8

18.9§

0.7

20.2§

0.8

21.1§

1.1

14

16.9§

1.4

17.9§

1.0

20.1§

0.9

18.6§

0.9

19.5§

1.3

18.4§

1.1

19.2§

1.3

18.4§

0.8

19.4§

1.4

16

17.4§

1.1

17.7§

1.1

19.7§

1.1

18.3§

1.1

17.6§

1.3

17.9§

1.0

17.8§

0.9

18.6§

1.0

19.1§

0.8

1324

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than those from the Chilko River, both at 10�C). Hatching ear-

lier would allow alevin to avoid intergravel ice conditions

sooner (Cope and Macdonald 1998) and avoid dewatering

events and localized low-oxygen environments, thus increas-

ing competitiveness for those fish. However, there is likely an

increase energetic activity cost associated with hatching early

into colder winter thermal regimes, especially as alevin, a very

vulnerable life stage (Blaxter 1992). Future work should seek

to better understand such trade-offs and their ecological rele-

vance to the populations described herein.

Consistent with earlier work on Sockeye Salmon, egg size

differed significantly among populations and this variation in

size occurred along a gradient of migration distance from river

entry, for which longer migrations were associated with

smaller eggs (Crossin et al. 2004). While previous work has

shown that egg size can be negatively (Beacham and Murray

1985) or positively (Heath et al. 1999) related to offspring sur-

vival, it is often unrelated to embryo viability (Hutchings

1991; Nadeau et al. 2009; Burt et al. 2012a). In our study, ele-

vated temperature increased development rates, resulting in

earlier hatching than for those embryos incubated at cool tem-

peratures, but egg size did not significantly affect developmen-

tal timing characteristics among populations.

While incubation duration is often inversely related to egg

size in Pacific salmon (so that smaller eggs hatch faster)

(Bagenal 1969), we show that among the populations in our

study incubation duration depends more on population origin

and water temperature than on egg size, a pattern observed

previously for fry emergence (Brannon 1987). Indeed, the pop-

ulation that hatched the fastest at high temperatures (Harrison

River) had the largest eggs (Tables 1, 3), although the signifi-

cant mortality observed for this population (Whitney et al.

2013) may have resulted in a selection bias towards faster-

growing families. Moreover, the effect of egg size was not sig-

nificantly related to time to first hatch, 5% hatch, or 50%

(median) hatch. As there was some evidence for faster

FIGURE 4. Hatch duration reaction norms by population under incubation

temperatures of 10, 14, and 16�C. Overall hatch synchrony across populations

increased with temperature, while hatch synchrony within populations

decreased. Hatch duration was measured between 5% and 95% hatch for each

family and is shown as averages per population; OK D Okanagan.

10 14 16

16

18

20

22

Incubation temperature

Ale

vin

leng

th (

mm

)

10 14 16

0.10

0.15

0.20

Incubation temperature

Ale

vin

mas

s (g

)

FIGURE 5. The effect of temperature on (left panel) alevin length and (right panel) alevin mass across all populations under three incubation temperatures.

The black lines show median values, the boxes contain all data within the 25th and 75th quartiles, whiskers show the 10th and 90th percentiles, and open circles

show extreme data. Only length varied significantly among temperatures (P < 0.0001).

HATCH TIMING AMONG SOCKEYE SALMON POPULATIONS 1325

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hatching of larger eggs at high temperatures, future research is

needed to examine the effects of warming thermal regimes

with climate change as an interaction with egg size.

Environmental temperature regimes are a selective force

driving development rates, and research on Rainbow Trout O.

mykiss suggests that parallel adaptation for rapid early devel-

opment may be linked to similar thermal regimes among geo-

graphically distinct populations (Miller et al. 2012). In that

study, populations adapted to cool temperatures in early life

had very rapid development rates, whereas in our study only

some of the cold-spawning populations, such as the Harrison

River Sockeye Salmon, exhibited rapid embryonic develop-

ment to hatch. In particular, further work on Harrison River

Sockeye Salmon is needed as this population is likely

affected by warm lake inflow, which may mediate the usual

late-season temperature, suggesting that this late-spawning

population is perhaps not as cold adapted as would otherwise

be expected.

Thermal Requirements: Compensation and HatchDuration

Thermally elevated basal metabolic rates require a greater

proportion of endogenous energy reserves, leaving less for

growth and development (Beacham and Murray 1985; Kamler

2008; Jonsson and Jonsson 2011). Blaxter (1992) also sug-

gested that larval length and weight decrease with increased

incubation temperature due to the disproportionate increase in

development rate versus growth rate so that cell differentiation

occurs before sufficient tissue develops to allow for normal

weight or length. In poikilotherms, development rates are

directly related to temperature (Brett 1971) but exposure to

supraoptimal temperature can result in a compensatory

response in incubation rate, in which the amount of ATUs

required to reach a certain development stage, such as hatch-

ing, increases at temperatures beyond a certain threshold

(Brannon 1987). Elevated development rates can result in pre-

mature hatching if these rates increase proportionately to ris-

ing temperature. This disassociation between metabolic and

growth rates is generally seen as temperature exceeds an upper

thermal limit (Rombough 1994). This relationship between

metabolic and growth rates is thought to vary by population

and to be linked with historical emergence date (Konecki et al.

1995). Evidence of a thermally driven compensatory response

at hatch (Brannon 1987) was observed in our study, in which

most populations required more ATUs to reach hatching at the

14�C and 16�C treatments than at the cold treatment (10�C;Chilko). That this was especially evident at both the moderate

(14�C) and high (16�C) incubation temperatures suggests that

parallels between hatch timing and hatching success should be

investigated further.

Hatch duration varied by temperature treatment, with

higher temperatures being related to protracted hatching

(decreased hatch synchrony) within a population. This has

rarely been investigated but was also observed in a separate

study on one of our Sockeye Salmon populations (Weaver

Creek; Burt et al. 2012b). Kamler (2005) also noted increased

hatching asynchrony at elevated incubation temperature. Syn-

chrony in hatch and thus emergence timing should allow popu-

lations to “swamp” predators (Godin 1982). Asynchrony in

development timing within populations may also be an adap-

tive response to resource competition, especially in years of

high abundance as a means of lowering competition for scarce

resources (Godin 1982). While the direct fitness implications

of hatch timing are thus less than clear, the association

between hatch and emergence timing is strong enough to link

the consequences of environmental effects on changing timing

sequences for population-specific adaptations.

Offspring Size and Growth

Across all populations, alevin hatched from the high-tem-

perature treatment were shorter and lighter than those from the

same population raised under the cool-temperature treatment

(10�C). This pattern has been shown previously (but mostly

for emergent fish) in Sockeye Salmon (Hendry et al. 1998)

and other salmonids (Pink Salmon O. gorbuscha, Murray and

Beacham 1986; Brown Trout Salmo trutta, Ojanguren and

Brana 2003; Arctic Char Salvelinus alpinus, Janhunen et al.

2010). Alevin length, but not mass, was significantly affected

by temperature treatment, consistent with the suggestion that

under higher temperature alevin utilize their yolk sac less for

growth and more for routine basal metabolism (Beacham and

Murray 1989; Rombough 1994; Kamler 2008). As shown

here, if temperature is high enough during incubation to affect

the efficiency of yolk conversion to body tissue, alevin length

may be affected more than alevin mass (Beacham and Murray

1985). Indeed, this reduction in growth efficiency was shown

in subsequent work to persist through to the emergent stage in

these same populations (Whitney 2012), confirming that tem-

perature did not merely result in premature hatching but did

affect offspring growth.

Conclusions

Suboptimal temperature during incubation is likely to have

deleterious consequences for developing embryos beyond a

reduction in survival. This research suggests that temperature

patterns and population differentiation may affect offspring

competitiveness and development timing more than egg size,

especially when comparing widely disparate temperatures and

geographically isolated populations. The implications of varia-

tion in hatch timing are wide ranging, and differences among

populations may directly affect survival and thus population

viability. Further investigation into how populations vary in

early life history traits, and how these genetic differences

interact with environmental conditions such as temperature,

will be necessary in order to allow us to predict the

1326 WHITNEY ET AL.

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evolutionary response of Sockeye Salmon to climate change

and peak temperature events. This work highlights the impor-

tance of population variation in thermal adaptation and is a

reminder of the relevance of maintaining genetic diversity for

species conservation.

ACKNOWLEDGMENTS

All research was conducted with the approval of the Animal

Ethics Committee of the University of British Columbia,

according to the principles of the Canadian Council on Animal

Care (#A08-0388). C.K.W. was supported by a Natural Scien-

ces and Engineering Research Council of Canada, Canada

Graduate Scholarship and a VanDusen Graduate Fellowship

from the University of British Columbia Faculty of Forestry,

with project funding deriving from Natural Sciences and Engi-

neering Research Council of Canada Strategic and Discovery

Grants to S.G.H. and support from Fisheries and Oceans

Canada’s Environmental Watch group. The authors thank

members of the Okanagan Nation Alliance, in particular R.

Bussanich and S. Folks, for field support and assistance. Many

thanks to all the members of the Pacific Salmon Ecology and

Conservation Laboratory, especially A. Lotto, J. Burt, E.

Vogt, A. Haas, K. Robinson, N. Sopinka, and E. Martins.

REFERENCESBagenal, T. B. 1969. Relationship between egg size and fry survival

in Brown Trout Salmo trutta L. Journal of Fish Biology 1:

349–353.

Beacham, T. D. 1988. A genetic analysis of early development in

Pink (Oncorhynchus gorbuscha) and Chum salmon (Oncorhyn-

chus keta) at three different temperatures. Genome 30:89–96.

Beacham, T. D., and C. B. Murray. 1985. Effect of female size, egg

size, and water temperature on developmental biology of Chum

Salmon (Oncorhynchus keta) from the Nitinat River, British

Columbia. Canadian Journal of Fisheries and Aquatic Sciences

42:1755–1765.

Beacham, T. D., and C. B. Murray. 1987. Effects of transferring Pink

(Oncorhynchus gorbuscha) and Chum (Oncorhynchus keta)

salmon embryos at different developmental stages to a low incu-

bation temperature. Canadian Journal of Zoology 65:96–105.

Beacham, T. D., and C. B. Murray. 1988. Variation in developmental

biology of Pink Salmon (Oncorhynchus gorbuscha) in British

Columbia. Canadian Journal of Zoology 66:2634–2648.

Beacham, T. D., and C. B. Murray. 1989. Variation in developmental

biology of Sockeye Salmon (Oncorhynchus nerka) and Chinook

Salmon (O. tshawytscha) in British Columbia. Canadian Journal

of Zoology 67:2081–2089.

Beacham, T. D., and C. B. Murray. 1990. Temperature, egg size, and

development of embryos and alevins of five species of Pacific

salmon: a comparative analysis. Transactions of the American

Fisheries Society 119:927–945.

Berg, O. K., and V. Moen 1999. Inter–and intrapopulation variation in

temperature sum requirements in Norwegian Atlantic Salmon.

Journal of Fish Biology 54:636–647.

Blaxter, J. H. S. 1992. The effect of temperature on larval fishes.

Netherlands Journal of Zoology 42:336–357.

Bradford, M. J. 1995. Comparative review of Pacific salmon survival

rates. Canadian Journal of Fisheries and Aquatic Sciences

52:1327–1338.

Bradshaw, W. E., and C. M. Holzapfel. 2008. Genetic response to

rapid climate change: it’s seasonal timing that matters. Molecular

Ecology 17:157–166.

Brannon, E. L. 1987. Mechanisms stabilizing salmonid fry emergence

timing. Canadian Special Publication of Fisheries and Aquatic

Sciences 96:120–124.

Braun, D. C., D. A. Patterson, and J. D. Reynolds. 2013. Maternal

and environmental influences on egg size and juvenile life-his-

tory traits in Pacific salmon. Ecology and Evolution 3:

1727–1740.

Brett, J. R. 1971. Energetic responses of salmon to temperature: a

study of some thermal relations in the physiology and freshwater

ecology of Sockeye Salmon (Oncorhynchus nerka). American

Zoologist 11:99–113.

Brooks, S., C. R. Tyler, and J. P. Sumpter. 1997. Egg quality in fish:

what makes a good egg? Reviews in Fish Biology and Fisheries

7:387–416.

Burt, J. M., S. G. Hinch, and D. A. Patterson. 2012a. Developmental

temperature stress and parental identity shape offspring burst

swimming performance in Sockeye Salmon (Oncorhynchus

nerka). Ecology of Freshwater Fish 21:176–188.

Burt, J. M., S. G. Hinch, and D. A. Patterson. 2012b. Parental identity

influences progeny responses to incubation thermal stress in

Sockeye Salmon Oncorhynchus nerka. Journal of Fish Biology

80:444–462.Charmantier, A., R. H. Mccleery, L. R. Cole, C. Perrins, L. E. B.

Kruuk, and B. C. Sheldon. 2008. Adaptive phenotypic plasticity

in response to climate change in a wild bird population. Science

320:800–803.Cope, R. S., and J. S. Macdonald. 1998. Responses of Sockeye

Salmon (Oncorhynchus nerka) embyros to intragravel incubation

environments in selected streams within the Stuart-Takla water-

shed. Canadian Forest Service Information Report NOR-X-

356:283–294.

Crisp, D. T. 1988. Prediction, from temperature, of eyeing, hatching

and ‘swim-up’ times for salmonid embryos. Freshwater Biology

19:41–48.Crossin, G. T., S. G. Hinch, A. P. Farrell, D. A. Higgs, A. G. Lotto, J.

D. Oakes, and M. C. Healey. 2004. Energetics and morphology

of Sockeye Salmon: effects of upriver migratory distance and ele-

vation. Journal of Fish Biology 65:788–810.

Crozier, L. G., A. P. Hendry, P. W. Lawson, T. P. Quinn, N. J. Man-

tua, J. Battin, R. G. Shaw, and R. B. Huey. 2008. Potential

responses to climate change in organisms with complex life histo-

ries: evolution and plasticity in Pacific salmon. Evolutionary

Applications 1:252–270.

Eliason, E. J., T. D. Clark, M. J. Hague, L. M. Hanson, Z. S. Gal-

lagher, K. M. Jeffries, M. K. Gale, et al. 2011. Differences in

thermal tolerance among sockeye salmon populations. Science

332:109–112. doi:10.1126/science.1199158

Fraser, D. J., L. K. Weir, L. Bernatchez, M. M. Hansen, and E. B.

Taylor. 2011. Extent and scale of local adaptation in

salmonid fishes: review and meta-analysis. Heredity 106:

404–420.

HATCH TIMING AMONG SOCKEYE SALMON POPULATIONS 1327

Dow

nloa

ded

by [

The

Uni

vers

ity o

f B

ritis

h C

olum

bia]

at 1

0:54

30

Sept

embe

r 20

14

Godin, J.-G. J. 1982. Migrations of salmonid fishes during early life

history phases: daily and annual timing. Pages 22–50 in E. L.

Brannon and E. O. Salo, editors. Proceedings of the salmon and

trout migratory behaviour symposium. University of Washington,

Seattle.

Groot, C., and L. Margolis. 1991. Pacific salmon life histories. Uni-

versity of British Columbia Press, Vancouver.

Heath, D. D., C. W. Fox, and J. W. Heath. 1999. Maternal effects on

offspring size: variation through early development of Chinook

Salmon. Evolution 53:1605–1611.

Hendry, A. P., J. E. Hensleigh, and R. R. Reisenbichler. 1998.

Incubation temperature, developmental biology, and the diver-

gence of Sockeye Salmon (Oncorhynchus nerka) within Lake

Washington. Journal of Fisheries and Aquatic Sciences

55:1387–1394.

Hodgson, S., and T. P. Quinn. 2002. The timing of adult Sockeye

Salmon migration into freshwater: adaptations by populations to

prevailing thermal regimes. Canadian Journal of Zoology

80:542–555.

Hutchings, J. A. 1991. Fitness consequences of variation in egg size

and food abundance in Brook Trout Salvelinus fontinalis. Evolu-

tion 45:1162–1168.

Hutchings, J. A. 2011. Old wine in new bottles: reaction norms in sal-

monid fishes. Heredity 106:421–437.

Hyatt, K. D., M. M. Stockwell, and D. P. Rankin. 2003. Impact

and adaptation responses of Okanagan River Sockeye Salmon

(Oncorhynchus nerka) to climate variation and change effects

during freshwater migration: stock restoration and fisheries

management implications. Canadian Water Resources Journal

28:689–714.

Janhunen, M., J. Piironen, and N. Peuhkuri. 2010. Parental effects on

embryonic viability and growth in Arctic Charr Salvelinus alpi-

nus at two incubation temperatures. Journal of Fish Biology

76:2558–2570.

Jensen, J. O. T., and D. F. Alderice. 1983. Changes in mechanical

shock sensitivity of Coho Salmon (Oncorhynchus kisutch) eggs

during incubation. Aquaculture 32:303–312.

Jensen, J. O. T., and D. F. Alderice. 1984. Effect of temperature on

short-term storage of eggs and sperm of Chum Salmon (Onco-

rhynchus keta). Aquaculture 37:251–265.

Jensen, L. F., M. M. Hansen, C. Pertoldi, G. Holdensgaard, K.-L.

D. Mensberg, and V. Loeschcke. 2008. Local adaptation in

Brown Trout early life-history traits: implications for climate

change adaptability. Proceedings of the Royal Society B

275:2859–2868.

Jonsson, B., and N. Jonsson. 2011. Development and growth. Fish

and Fisheries Series 33:1–21

Jonsson, N., B. Jonsson, and I. A. Fleming. 1996. Does early growth

cause a phenotypically plastic response in egg production of

Atlantic Salmon? Functional Ecology 10:89–96.

Kamler, E. 2002. Ontogeny of yolk-feeding fish: an ecological

perspective. Reviews in Fish Biology and Fisheries 12:

79–103.

Kamler, E. 2005. Parent–egg–progeny relationships in teleost fishes:

an energetics perspective. Reviews in Fish Biology and Fisheries

15:399–421.

Kamler, E. 2008. Resource allocation in yolk-feeding fish. Reviews in

Fish Biology and Fisheries 18:143–200.

Kinnison, M. T., M. J. Unwin, A. P. Hendry, and T. P. Quinn. 2001.

Migratory costs and the evolution of egg size and number in

introduced and indigenous salmon populations. Evolution

55:1656–1667.

Konecki, J. T., C. A. Woody, and T. P. Quinn. 1995. Influence of tem-

perature on incubation rates of Coho Salmon (Oncorhynchus

kisutch) from ten Washington populations. Northwest Science

69:126–132.

McCullough, D., S. Spalding, D. Sturdevant, and M. Hicks. 2001.

Summary of technical literature examining the physiological

effects of temperature on salmonids. U.S. Environmental Protec-

tion Agency, Issue Paper 5, EPA-910-D-01-005, Washington,

D.C.

Miller, M. R., J. P. Brunelli, P. A. Wheeler, S. Liu, C. E. Rex-

road III, Y. Palti, C. Q. Doe, and G. H. Thorgaard. 2012. A

conserved haplotype controls parallel adaptation in geographi-

cally distant salmonid populations. Molecular Ecology

21:237–249.

Murray, C. B., and T. D. Beacham. 1986. Effect of varying tempera-

ture regimes on the development of Pink Salmon (Oncorhynchus

gorbuscha) eggs and alevins. Canadian Journal of Zoology

64:670–676.

Murray, C. B., T. D. Beacham, and J. D. McPhail. 1990. Influ-

ence of parental stock and incubation temperature on the

early development of Coho Salmon (Oncorhynchus kisutch)

in British Columbia. Canadian Journal of Zoology 68:

347–358.

Nadeau, P. S., S. G. Hinch, L. B. Pon, and D. A. Patterson. 2009. Per-

sistent parental effects on the survival and size, but not burst

swimming performance of juvenile Sockeye Salmon Oncorhyn-

chus nerka. Journal of Fish Biology 75:538–551.

Ojanguren, A. F., and F. Brana. 2003. Thermal dependence of embry-

onic growth and development in Brown Trout. Journal of Fish

Biology 62:580–590.

Pankhurst, N. W., and P. L. Munday. 2011. Effects of climate change

on fish reproduction and early life history stages. Marine and

Freshwater Research 62:1015–1026.

Patterson, D. A., H. Guderley, P. Bouchard, J. S. Macdonald,

and A. P. Farrell. 2004. Maternal influence and population

differences in activities of mitochondrial and glycolytic

enzymes in emergent Sockeye Salmon (Oncorhynchus

nerka) fry. Canadian Journal of Fisheries and Aquatic Scien-

ces 61:1225–1234.

Rombough, P. J. 1994. Energy partitioning during fish development:

additive or compensatory allocation of energy to support growth?

Functional Ecology 8:178–186.

Rombough, P. J. 1997. The effects of temperature on embryonic and

larval development. Pages 351–376 in C. M. Wood and D. G.

McDonald, editors. Global warming: implications for freshwater

and marine fish. Cambridge University Press, Society for Experi-

mental Biology Seminar Series 61, Cambridge, UK.

Rugh, R. 1952. Experimental embryology. Burgess Publishing, Min-

neapolis, Minnesota.

Springate, J. R. C., N. R. Bromage, J. A. K. Elliott, and D. L. Hudson.

1984. The timing of ovulation and stripping and their effects on

the rates of fertilization and survival to eying, hatch and swim-up

in the Rainbow Trout (Salmo gairdneri R.) Aquaculture 43:

313–322.

1328 WHITNEY ET AL.

Dow

nloa

ded

by [

The

Uni

vers

ity o

f B

ritis

h C

olum

bia]

at 1

0:54

30

Sept

embe

r 20

14

Steel, E. A., A. Tillotson, D. A. Larson, A. H. Fullerton, K. P. Denton,

and B. R. Beckman. 2012. Beyond the mean: the role of variabil-

ity in predicting ecological effects of stream temperature on

salmon. Ecosphere 3(11):104.

Tallman, R. F. 1986. Genetic differentiation among seasonally dis-

tinct spawning populations of Chum Salmon Oncorhynchus keta.

Aquaculture 57:211–217.

Taylor, E. 1991. A review of local adaptation in Salmonidae, with

particular reference to Pacific and Atlantic salmon. Aquaculture

98:185–207.

Velsen, F. P. J. 1987. Temperature and incubation in Pacific

salmon and Rainbow Trout: compilation of data on

median hatching time, mortality and embryonic staging.

Canadian Data Report of Fisheries and Aquatic Sciences

626.

Whitney, C. K. 2012. Variation in embryonic thermal tolerance

among populations of Sockeye Salmon: offspring survival,

growth, and hatch timing in response to elevated incubation tem-

perature. Master’s thesis. The University of British Columbia,

Vancouver.

Whitney, C. K., S. G. Hinch, and D. A. Patterson. 2013. Provenance

matters: thermal reaction norms for embryo survival among

Sockeye Salmon Onchorhynchus nerka populations. Journal of

Fish Biology 82:1159–1176.

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