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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§
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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.
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