30
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
SUPPORTING
DISCUSSION
AND
LITERATURE
 
SUBLETHAL
EFFECTS
Incubation
and
Early
Fry
Development
Which
temperatures
provide
optimum
conditions
for
incubation
and
early
fry
development
in
the
following
species?

Chinook
salmon.
Once
spawning
has
taken
place,
the
eggs
of
chinook
salmon
hatch
in
about
2
months
and
the
young
remain
in
the
gravel
for
2­
3
wk
before
emerging.
Many
researchers
have
tested
incubation
survival
at
constant
exposure
to
various
test
temperatures.
Complete
mortality
(
100%)
has
been
noted
at
incubation
temperatures
from
57
to
66.9
°
F
(
13.9­
19.4
°
C)
(
Donaldson
1955,
Garling
and
Masterson
1985,
Seymour
1956,
Eddy
1972,
as
cited
in
Raleigh
et
al.
1986).
Significant
mortality
(
over
50%)
has
been
noted
at
constant
incubation
temperatures
from
49.8
to
62
°
F
(
9.9­
16.7
°
C)
(
Donaldson
1955,
Seymour
1956,
Burrows
1963,
Bailey
and
Evans
1971,
as
cited
in
Alderdice
and
Velsen
1978;
Hinze
1959,
as
cited
in
Healy
1979).
A
constant
incubation
temperat
ure
of
46.4
°
F
(
8
°
C)
produced
more
robust
alevin
and
fry
Figure
1.
Critical
swimming
velocity
as
a
function
of
water
temperature.
Data
source
was
tabulated
in
Myrick
and
Cech
(
2000).
31
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
survival
than
constant
exposure
to
either
39.2
or
53.6
°
F
(
4
or
12
°
C)
in
a
study
by
Murray
and
Beacham
(
1986),
and
Velsen
(
1987)
compiled
data
showing
that
the
best
survival
(>
92.9%)
occurred
between
44.9
and
49.2
°
F
(
7.2
and
9.6
°
C).
Heming
(
1982),
however,
found
good
survival
at
bo
th
50
and
53.6
°
F
(
10
and
12
°
C).
Heming
tested
survival
in
bot
h
incubation
t
rays
and
artificial
redds.
Survival
rates
declined
as
the
temperatures
increased
from
42.8
to
46.4,
50,
and
53.6
°
F
(
6­
8,
10,
and
12
°
C).
The
greatest
survival
(
91.7%­
98%)
occurred
at
42.8
and
46.4
°
F
(
6
and
8
°
C),
but
it
was
still
very
good
(
90.2%­
95.9%)
at
50
°
F
(
10
°
C).
Incubation
at
53.6
°
F
(
12
°
C)
consistently
had
the
lowest
survival
(
84.6%­
89.3%).
Heming
also
tested
survival
rates
from
incubation
to
hatching
against
survival
rat
es
from
hatching
through
complete
yolk
absorption.
His
work
suggests
higher
incubation
temperatures
may
create
a
metabolic
energy
deficit
for
pre­
emergent
salmon
that
increases
mortality.
Once
alevin
have
hatched
and
absorbed
their
yolk
sacs
they
will
need
to
make
a
transition
to
active
feeding.
Heming
and
McInery
(
1982)
found
that
temperatures
of
42.8,
46.4,
and
50
°
F
(
6,
8,
and
10
°
C)
resulted
in
an
average
survival
of
98.4%
during
this
transitional
period,
while
53.6
°
F
(
12
°
C)
was
asso
ciated
with
a
decrease
in
survival
to
89.2%.
The
maximum
conversion
of
yolk
t
o
tissue
weight
was
reported
by
Heming
(
1982)
(
as
cited
by
Beacham
and
Murray
1986)
to
occur
at
42.8
°
F
(
6
°
C)
or
below.
Seymour
(
1956)
noted
a
ninefold
increase
in
abnormalities
in
fry
incubated
at
60
°
F
(
15.6
°
C)
and
higher
when
compared
with
those
incubated
between
39.9
and
55
°
F
(
4.4­
12.8
°
C).
Seymour
also
noted
that
fry
incubated
at
39.9
°
F
(
4.4
°
C)
emerged
at
a
larger
size
than
those
reared
at
higher
temperatures;
however,
subsequent
fry
growth
was
maximized
at
55
°
F
(
12.8
°
C).

Considered
together,
the
work
of
the
authors
cited
above
most
strongly
suggests
that
constant
temperatures
above
48.2­
50
°
F
(
9­
10
°
C)
and
below
41
°
F
(
5
°
C)
may
reduce
the
survival
of
chinook
salmon
embryos
and
alevins.
Although
constant
temperatures
of
51.8­
53.6
°
F
(
11­
12
°
C)
can
still
result
in
good
success,
the
results
are
consistently
less
than
what
is
produced
at
lower
temperatures.
As
discussed
previously
in
this
paper,
constant
laboratory
test
temperatures
of
48.2­
50
°
F
(
9­
10
°
C)
should
be
considered
roughly
equivalent
to
naturally
fluctuating
stream
temperatures
with
daily
maximums
of
51.8­
53.6
°
F
(
11­
12
°
C).

Some
researchers
have
tried
to
mimic
the
naturally
fluctuating
and
falling
temperatures
actually
experienced
by
incubating
eggs,
or
have
stepwise
reduced
the
incubation
temperatures
as
incubation
progressed.
Initial
incubation
temperatures
from
60
to
62
°
F
(
15.6­
16.7
°
C)
have
been
associated
with
significant
to
total
losses
of
young
fish
through
the
incubation
to
early
fry
development
phase
(
Healy
1979,
Johnson
and
Brice
1953,
California
Department
of
Water
Resources
[
CDWR]
1988,
and
Jewett
1970
as
cited
in
CDWR
1988).
Rice
(
1960)
found
that
source
waters
declining
from
60
to
46.9
°
F
(
15.6­
8.3
°
C)
resulted
in
satisfactory
egg
development,
although
he
did
not
provide
survival
rates
or
clearly
consider
survival
through
to
the
fry
stage.
Johnson
and
Brice
(
1953)
found
survival
often
exceeded
90%
where
initial
water
temperatures
(
as
a
daily
mean)
were
below
53.9
°
F
(
12.2
°
C).
Healy
(
1979)
found
that
highest
survival
(
97%)
occurred
in
creek
water
where
the
daily
maximum
reached
55
°
F
(
12.8
°
C)
only
a
few
times
during
the
first
2
wk
of
development,
but
also
noted
that
survival
was
still
very
good
(
90%­
94%)
where
the
initial
temperatures
were
between
55
and
57.5
°
F
(
12.8
and
14.2
°
C).
Olson
and
Nakatani
(
1969)
found
53.7%­
88%
survival
in
egg
lots
started
at
54.5
°
F
(
12.5
°
C),
experiencing
a
brief
increase
to
58.4
°
F
(
14.7
°
C)
in
the
first
wk,
and
then
quickly
dropping
back
to
53.6­
54.5
°
F
(
12­
12.5
°
C)
and
assuming
a
seasonal
downward
trend
in
temperature
(
test
water
paralleled
both
diel
and
seasonal
fluctuations).
Olson
and
Foster
(
1955)
found
the
greatest
survival
at
an
initial
test
32
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
temperature
of
52.8
°
F
(
11.6
°
C)
(
92.2%),
but
reported
no
appreciable
differences
in
survival
rates
at
initial
test
temperatures
of
56.8,
59,
and
60.8
°
F
(
13.8,
15,
and
16
°
C)
(
89.9%­
83.9%)
(
test
water
paralleled
seasonal
daily
average
temperatures).
Seymour
(
1956)
t
ested
four
geographically
distinct
stocks
of
chinook.
Taking
into
co
nsideration
both
mortality
and
growth
rate,
the
optimum
temperature
was
estimated
as
52
°
F
(
11.1
°
C)
for
eggs
and
fry.
The
mortality
rate
was
considered
low
at
all
stages
of
development
for
lots
reared
between
39.9
and
55
°
F
(
4.4­
12.8
°
C).
Lots
with
initial
temperatures
of
64.9
°
F
(
18.3
°
C)
had
t
he
highest
mortality
(
11%,
24%,
40%,
and
100%).
In
the
cyclic
and
fluctuat
ing
temperature
tests
reviewed
here,
temperatures
at
the
beginning
of
incubation
that
are
below
51.8­
55
°
F
(
11­
12.8
°
C)
are
typically
associated
with
optimal
survival
rates.
This
compares
well
with
the
adjusted
optimal
range
o
f
52.7­
54.5
°
F
(
11.5­
12.5
°
C)
suggested
above
based
on
examining
the
constant
temperature
exposure
studies.
This
range
also
compares
well
with
the
optimal
temperature
range
of
46.4­
53.6
°
F
(
8­
12
°
C)
recommended
by
the
Independent
Scientific
Group
(
1996)
study.

Donaldson
(
1955)
transferred
eggs
to
more
optimal
50­
55
°
F
(
10­
12.8
°
C)
incubation
temperatures
after
various
periods
of
exposure
to
higher
temperatures.
He
found
that
tolerance
to
temperature
exposure
varies
with
the
stage
of
development.
He
also
found
20%
mortality
could
be
induced
by
exposing
eggs
to
66.9
°
F
(
19.4
°
C)
for
1
d,
64.9
°
F
(
18.3
°
C)
for
3
d,
and
62.9
°
F
(
17.2
°
C)
for
less
than
10
d.
Donaldson's
work
lends
further
support
to
the
observations
made
by
other
authors
such
as
Jewett
(
1970,
as
cited
in
CDWR
1988)
that
the
latent
effects
of
holding
eggs
at
higher
than
optimal
temperatures
continues
through
the
period
of
absorption
of
the
yolk
sac;
thus,
using
mortality
estimates
at
the
time
of
hatching
underestimates
the
total
temperature­
induced
mortality.
Donaldson
found
the
developmental
stages
associated
with
the
greatest
percentages
of
temperature
induced
mortality
were:
(
1)
the
time
up
until
the
closure
of
the
blastopore
(
200
T.
U.);
(
2)
the
period
just
previous
to
and
during
hatching;
and
(
3)
when
fry
are
adapting
themselves
to
feeding.
He
also
found
that
when
eggs
were
exposed
to
test
temperatures
62.9,
64.9,
and
66.9
°
F
(
17.2,
18.3,
and
19.4
°
C)
past
the
eye
pigmentation
stage
(
350
T.
U.),
the
time
necessary
for
complete
hatching
doubled,
and
the
frequency
of
common
abnormalities
increased
with
both
the
higher
temperatures
and
longer
exposures.
Murray
and
Beacham
(
1986)
found
that
initial
incubation
at
39.2
°
F
(
4
°
C)
reduced
survival
even
with
later
transfer
(
at
completion
of
epiboly)
to
warmer
waters
46.4
and
53.6
°
F
(
8
and
12
°
C).
Transfers
after
epiboly
or
completion
of
eye
pigmentation
from
39.2
to
53.6
°
F
(
4­
12
°
C)
and
from
53.6
to
39.2
°
F
(
12­
4
°
C)
also
caused
an
increase
in
alevin
mortality.
The
authors
also
found
that
decreasing
temperature
produced
longer
and
heavier
alevins
and
fry.
Combs
(
1965)
found
that
eggs
developed
to
the
128­
cell
stage
at
42.4
°
F
(
5.8
°
C)
could
then
t
olerat
e
35
°
F
(
1.7
°
C)
for
the
remainder
of
the
incubation
period
with
only
moderate
losses.
Mortality
of
14.5%
was
observed
with
a
transfer
time
of
72
h,
whereas
only
3.3%
mortality
occurred
with
a
transfer
at
144
h.
These
three
works
together
suggest
that
the
effects
of
suboptimal
initial
incubation
temperatures
may
not
be
nullified
by
later
changes
in
the
temperature
regime
to
more
optimal
levels;
that
sudden
changes
in
temperature
at
either
early
or
lat
er
stages
of
development,
regardless
o
f
the
direction
of
that
change,
can
be
harmful
to
pre­
emergent
life
stages;
and
that
initial
incubation
at
optimal
temperatures
may
condition
eggs
and
embryos
such
that
they
can
withstand
very
low
winter
temperature
regimes.

In
addition
to
Donaldson
(
1955),
Neitzel
and
Becker
(
1985)
conducted
work
on
the
effects
of
short­
term
increases
in
temperature
that
can
be
used
to
support
daily
maximum
temperature
33
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
criteria.
Neitzel
and
Becker
used
chinook
salmon
to
determine
the
effects
of
short­
term
dewatering
of
redds
by
hydropower
facilities.
Neitzel
and
Becker
found
that
sudden
increases
in
temperatures
from
50
°
F
to
above
71.6
°
F
(
10­
22
°
C
)
for
1­
8
h
significantly
reduced
survival
of
cleavage
eggs
in
chinook
salmon.
Controls
held
at
50
°
F
(
10
°
C)
had
very
low
mortalities
(
less
than
2%).
Mortality
in
treatment
groups
was
8%­
10%
at
71.6
°
F
(
22
°
C)
after
2­
h
exposure,
and
was
22%
after
a
1­
h
exposure
at
74.3
°
F
(
23.5
°
C).
They
further
found
that
decreasing
the
temperature
from
50
°
F
(
10
°
C)
to
near
freezing
32
°
F
(
0
°
C)
for
up
to
24­
h
did
not
increase
mortality
in
eggs,
embryos,
or
alevin.
Considering
the
work
o
f
Neitzel
and
Becker,
it
would
appear
that
chinook
salmon
eggs
and
embryos
are
relatively
tolerant
of
short­
term
increases
in
temperature
up
to
71.6
°
F
(
22
°
C).
However,
because
Donaldson
(
1955)
found
that
66.9
°
F
(
19.4
°
C)
produced
20%
mortality
in
1
d
and
64.9
°
F
(
18.3
°
C)
produced
20%
in
3
d,
setting
a
more
restrictive
single
daily
maximum
temperature
limit
is
certainly
warranted.
Furthermore,
as
described
above,
incubation
conditions
where
daily
maximum
temperatures
were
in
the
range
of
57.9­
60.8
°
F
(
14.4­
15.6
°
C)
produced
reduced
survival
rates,
so
further
caution
may
be
warranted
in
allowing
daily
maximum
temperatures
to
exceed
56.3­
58.1
°
F
(
13.5­
14.5
°
C)
during
incubation.

Although
there
is
some
disagreement,
the
literature
is
consistent
overall
regarding
optimal
incubation
requirements
for
chinook
salmon.
Providing
for
optimal
protection
from
fertilization
through
initial
fry
development
requires
that
constant
or
acclimation
temperatures
be
maintained
below
48.2­
50
°
F
(
9­
10
°
C)
and
that
individual
daily
maximum
temperatures
generally
not
exceed
56.3­
58.1
°
F
(
13.5­
14.5
°
C).

Coho
salmon.
Embryo
survival
is
consistently
maximized
in
tests
at
constant
temperature
exposures
between
36.5
and
43.7
°
F
(
2.5­
6.5
°
C)
and
is
only
slightly
less
successful
between
34.4
and
51.6
°
F
(
1.3­
10.9
°
C)
(
Dong
1981,
Tang
et
al.
1987,
Murray
et
al.
1988,
Velsen
1987).
Davidson
and
Hutchinson
(
1938,
as
cited
in
Sandercock
1991)
suggested
that
optimum
temperature
for
egg
incubation
is
39.2­
51.8
°
F
(
4­
11
°
C).
Mortalities
tend
to
become
moderate
(
74%­
79%)
at
51.8­
54.5
°
F
(
11­
12.5
°
C),
and
at
54.5­
56.3
°
F
(
12.5­
13.5
°
C),
mortalities
of
50%
can
be
expected.
Above
57.2­
57.9
°
F
(
14­
14.4
°
C),
tests
commonly
report
100%
mortality
or
close
to
it.
Alevin
survival
may
be
excellent
(
97%)
at
34.3­
51.6
°
F
(
1.3­
10.9
°
C)
(
Dong
1981,
Tang
et
al.
1987),
and
the
most
robust
fry
are
at
incubation
temperatures
of
39.2­
46.4
°
F
(
4­
8
°
C)
(
Dong
1981,
Murray
et
al.
1988).
Alevin
mortalities
of
51%­
59%
occur
at
54.5
°
F
(
12.5
°
C)
(
Dong
1981),
and
100%
mortality
occurs
at
57.2­
57.9
°
F
(
14­
14.4
°
C)
(
Dong
1981,
Murray
et
al.
1988).

From
the
studies
discussed
above,
we
are
relatively
confident
that
egg
survival
is
consistently
best
at
exposure
to
constant
temperatures
of
36.5­
43.7
°
F
(
2.5­
6.5
°
C),
but
may
still
be
excellent
for
many
stocks
at
temperatures
of
34.4­
51.5
°
F
(
1.3­
10.9
°
C).
Alevin
and
fry
survival
and
health
may
be
best
at
exposure
to
constant
temperatures
of
39.2­
46.4
°
F
(
4­
8
°
C),
but
survival
may
remain
excellent
up
to
51.6
°
F
(
10.9
°
C).
This
review
of
the
available
literature
suggests
that
a
constant
44.6­
50
°
F
(
7­
10
°
C)
may
form
the
upper
threshold
for
optimal
development
of
coho
salmon
eggs
and
alevin.
Adjusting
this
laboratory­
based
naturally
fluctuating
stream
environment
(
as
discussed
previously)
results
in
the
recommendation
that
to
fully
support
the
pre­
emergent
stages
of
coho
development,
the
7­
d
average
of
daily
maximum
temperatures
should
not
exceed
48.2­
53.6
°
F
(
9­
12
°
C).
34
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
No
information
is
available
that
suggests
coho
salmon
embryos
and
alevins
are
more
sensitive
to
short­
term
(
daily
peak)
increases
in
temperature
than
any
other
Pacific
salmon.
The
one
study
reviewed
that
looks
at
short­
term
temperature
changes
for
coho
was
by
Tang
et
al.
(
1987).
In
that
study,
incubation
temperatures
were
increased
from
50.3
to
62.6
°
F
(
10.2­
17
°
C)
and
lowered
from
50.3
to
39.2
°
F
(
10.2­
4
°
C)
for
8
h.
In
neither
test
did
these
modest
changes
result
in
any
statistically
significant
increase
in
mortality.
Additionally,
one
field
study
reported
coho
alevins
capable
of
at
least
partial
survival
(
substantial
change
in
later
numbers
of
juveniles)
when
daily
peak
temperatures
rose
from
14
to
20
°
C
during
the
month
of
May
while
some
were
still
in
the
gravels.
The
control
stream
had
no
change
in
later
abundance
of
juveniles
and
had
temperatures
of
51.8­
54.5
°
F
(
11­
12.5
°
C)
(
visually
interpolated
from
graph)
during
May.
In
the
impacted
stream,
summer
maximum
temperatures
in
two
successive
years
were
75.2
and
86
°
F
(
24
and
30
°
C),
and
in
the
unimpacted
stream,
summer
temperatures
remained
below
59
°
F
(
15
°
C)
(
Hall
and
Lantz
1969).
In
the
review
of
the
literature,
no
clear
basis
was
found
for
setting
a
daily
peak
temperature
specific
to
coho
incubation.

Chum
salmon.
Incubat
ion
survival
fro
m
fertilization
to
emergence
is
variable,
but
can
be
excellent
anywhere
from
39.2
to
53.5
°
F
(
4­
12
°
C)
(
Murray
and
Beacham
1986,
Beacham
and
Murray
1985).
In
the
initial
period
of
embryo
development,
temperatures
of
46.4­
53.6
°
F
(
8­
12
°
C)
produce
the
highest
survival.
However,
in
later
stages
of
incubation,
temperatures
of
41­
46.4
°
F
(
5­
8
°
C)
produce
the
best
survival
as
well
as
the
largest
and
heaviest
alevin
and
fry
(
Beacham
and
Murray
1986).
Temperatures
of
53.6
°
F
(
12
°
C)
in
the
later
developmental
stages
can
result
in
heavy
losses
in
some
stocks
(
Beacham
and
Murray
1985,
Beacham
and
Murray
1986).
The
optimal
temperature
range
for
conversion
of
yolk
to
tissue
weight
was
estimated
to
be
42.8­
50
°
F
(
6­
10
°
C)
(
Beacham
and
Murray
1986),
and
optimal
respiration
efficiency
has
been
estimated
to
range
from
51.8
to
54.5
°
F
(
11­
12.5
°
C)
for
pro
larvae
and
larvae
(
Zinichev
and
Zot
in
1988).
Constant
incubation
at
temperatures
of
57.7
and
60.8
°
F
(
14
and
16
°
C)
as
well
as
at
36.5
°
F
(
2.5
°
C)
have
been
associated
with
embryonic
mortalities
of
50%
(
Beacham
and
Murray
1990).
The
alevin
stages
of
development
(
late),
however,
were
shown
to
have
very
high
survival
rates
when
exposed
to
temperatures
as
low
as
35.6
°
F
(
2
°
C).

Based
on
the
literature
reviewed,
constant
incubation
temperatures
from
39.2
to
53.6
°
F
(
4­
12
°
C)
commonly
produce
excellent
incubation
results;
however,
some
researchers
have
noted
less
than
optimal
survival
occurring
at
the
edges
of
this
range.
It
appears
that
constant
initial
incubation
temperatures
of
46.4­
50
°
F
(
8­
10
°
C)
would
be
most
consistently
optimal
for
chum
salmon.
In
reviewing
the
literature,
no
specific
basis
was
found
for
setting
a
daily
peak
temperature
for
incubating
chum.

Pink
salmon.
The
range
for
successful
incubation
has
been
suggested
to
be
from
39.9
to
55.9
°
F
(
4.4
to
13.3
°
C)
(
Beschta
et
al.
1987,
Bonar
et
al.
1989).
Murray
and
Beacham
(
1986)
reported
excellent
survival
(
91%­
97%)
with
initial
fertilization
occurring
at
57.2
°
F
(
14
°
C)
and
a
0.9
°
F
(
0.5
°
C)
drop
in
temperature
every
3
d
down
to
41
°
F
(
5
°
C).
When
they
allowed
temperatures
to
drop
further
to
39.2
and
35.6
°
F
(
4
and
2
°
C),
survival
was
reduced.
Murray
and
McPhail
found
survival
of
94%
from
fertilization
to
emergence
at
41
°
F
(
5
°
C),
and
Beacham
and
Murray
(
1986)
found
the
greatest
survival
for
5
stocks
and
21
families
of
pink
salmon
tested
at
46.4
°
F
(
8
°
C).
Velsen
(
1987)
compiled
data
showing
that
the
best,
although
highly
variable,
survival
(
generally
>
89.5%)
occurred
between
46.4
and
55.4
°
F
(
8
and
13
°
C).
Survival
decreased
35
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
at
an
incubation
temperature
of
51.8
°
F
(
11
°
C)
in
a
test
by
Murray
and
McPhail
(
1988),
and
was
50%
at
59­
60
°
F
(
15­
15.5
°
C)
(
Beacham
and
Murray
1990).
Temperatures
of
41­
46.4
°
F
(
5­
8
°
C)
produced
the
largest
alevins
in
a
study
by
Murray
and
McPhail
(
1988),
and
46.4
°
F
(
8
°
C)
produced
the
longest
(
Beacham
and
Murray
1986)
and
heaviest
(
Murray
and
McPhail
1988)
fry.

Survival
of
the
alevin
life
stage
was
found
to
be
generally
excellent
(>
97%)
for
21
families
of
pink
salmon
tested
at
temperatures
ranging
from
39.2
to
35.6
°
F
(
4­
2
°
C)
(
Beacham
and
Murray
1986).
Survival
to
emergence
was
reportedly
low,
at
57.2
°
F
(
14
°
C)
(
Murray
and
McPhail
1988).

Examining
low
incubation
temperatures,
Beacham
and
Murray
(
1986)
found
that
temperatures
of
39.2
°
F
(
4
°
C)
consistently
resulted
in
the
lowest
survival
for
5
stocks
and
21
families
of
pink
salmon,
and
in
a
1990
study
found
50%
mortality
at
41
°
F
(
5
°
C).
Murray
and
McPhail
(
1988),
Beacham
and
Murray
(
1990),
and
Bailey
and
Evans
(
1971)
found
100%
mortality
at
incubation
temperatures
of
35.6
°
F
(
2
°
C).
Murray
and
Beacham
(
1986)
transferred
embryos
in
a
late
stage
of
development
from
46.4
°
F
to
33.8
°
F
(
1­
8
°
C)
and
found
that
while
northern
stocks
had
100%
survival,
southern
stocks
had
mortalities
ranging
from
38%
to
60%.

Based
on
the
research
cited
above,
constant
temperatures
of
40.1­
53.6
°
F
(
4.5­
12
°
C)
and
a
constantly
declining
temperature
regime
beginning
at
57.2
°
F
(
14
°
C)
can
produce
excellent
and
perhaps
optimal
survival
rates
of
incubating
pink
salmon.
However,
a
constant
temperature
of
46.4
°
F
(
8
°
C)
appears
to
produce
the
most
consistently
optimal
results;
and
although
tests
up
to
53.6­
55.9
°
F
(
12­
13.3
°
C)
were
found
to
produce
optimal
results,
several
tests
found
temperatures
of
51.8­
53.6
°
F
(
11­
12
°
C)
(
as
well
as
ones
conducted
at
40.1­
41
°
F
[
4.5­
5
°
C])
to
produce
less
survival
and
smaller
fry.
Furthermore,
in
natural
streams
the
temperatures
do
not
decline
at
a
steady
rate,
and
temperatures
of
59­
60.8
°
F
(
15­
16
°
C)
have
resulted
in
high
mortality.
In
considerat
ion
of
all
of
these
issues,
we
should
assume
that
constant
or
acclimatio
n
temperatures
in
the
range
of
46.4­
50
°
F
(
8­
10
°
C)
represent
optimal
conditions
for
embryonic
development.
No
specific
information
was
reviewed
that
examined
the
effect
of
short­
term
and
infrequent
peaks
of
temperature
on
developing
pink
salmon.

Sockeye
salmon.
Murray
and
McPhail
(
1988)
and
Combs
(
1965)
reported
that
sockeye
salmon
are
more
tolerant
of
low
incubation
temperatures
and
less
tolerant
of
high
incubation
temperatures
than
the
other
Pacific
salmon.
At
constant
exposure,
Combs
(
1965)
reported
that
temperatures
of
39.9­
54.8
°
F
(
4.4­
12.7
°
C)
produced
similarly
high
survival
rates
(
85.8%­
90.9%),
with
the
highest
occurring
at
42.4
°
F
(
5.8
°
C).
Combs
found
that
incremental
increases
in
mortality
of
53%­
67%
occurred
when
the
temperature
was
lowered
from
42.4
to
39.9
°
F
(
5.8
to
4.4
°
C)
or
raised
from
54.8
to
57.5
°
F
(
12.7­
14.2
°
C).
Velsen
(
1987)
found
that
while
survival
rates
were
highly
inconsistent
between
34
and
59
°
F
(
1.1­
15
°
C),
the
best
survival
generally
occurred
between
35.8
and
42.4
°
F
(
3.1
and
5.8)
(
generally
>
90%),
with
fair
survival
(>
70%)
occurring
in
the
range
35.8­
54.9
°
F
(
2.1­
12.7
°
C),
and
survival
rates
consistently
poor
(
17%­
76%)
above
57.2
°
F
(
14
°
C).
Murray
and
McPhail
(
1988)
found
that
survival
was
highest
at
46.4
°
F
(
8
°
C)
(
79%)
but
only
40%
at
both
51.8
and
41
°
F
(
11
and
5
°
C).
Andrew
and
Geen
(
1960)
reported
that
in
the
first
2
years
of
a
4­
year
field
study,
the
Salmon
Commission
found
that
eggs
initially
incubated
at
temperatures
of
45
°
F
(
7.2
°
C)
had
lower
survival
than
tho
se
initially
incubated
at
50,
55,
and
60
°
F
(
10,
12.8,
and
15.6
°
C).
In
a
followup
experiment
the
following
2
years,
they
found
that
eggs
exposed
to
temperatures
of
60­
62
°
F
(
15.6­
16.7
°
C)
for
short
periods
suffered
severe
losses
during
the
36
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
exposure,
and
that
temperatures
of
62­
64.9
°
F
(
16.7­
18.3
°
C)
caused
extensive
losses
both
during
and
following
exposure.
In
a
study
by
Craig
et
al.
(
1996),
the
temperature
range
of
46.4­
50
°
F
(
8­
10
°
C)
resulted
in
the
optimum
1:
1
male­
to­
female
sex
ratio
in
offspring,
although
the
study
design
really
only
allows
the
conclusion
that
temperature
in
the
early
stage
of
development
affects
sex
determination.

The
data
on
sockeye
incubation
survival
are
highly
variable.
Overall,
however,
it
can
be
said
that
constant
o
r
acclimation
temperatures
in
the
range
of
39.2­
54.5
°
F
(
4­
12.5
°
C)
produce
variable
but
often
excellent
survival
rates
in
sockeye
salmon,
but
that
the
range
46.4­
50
°
F
(
8­
10
°
C)
appears
most
consistently
optimum.
No
specific
studies
were
found
to
suggest
a
basis
for
a
single
daily
maximum
temperature
limit
during
the
incubation
period
for
sockeye
salmon.

Steelhead.
In
establishing
a
State
standard
to
protect
spawning,
we
should
consider
temperature
recommendations
established
to
protect
embryo
development.
Fuss
(
1998)
considered
the
range
42­
52
°
F
(
5.6­
11.1
°
C)
to
be
optimal
for
steelhead
egg
survival
in
the
Washington
State
hatchery
program,
and
Bell
(
1986)
suggested
that
50
°
F
(
10
°
C)
is
the
preferred
hatching
temperature
for
steelhead
eggs.
Rombough
(
1988)
found
less
than
4%
embryonic
mortality
at
42.8,
48.2,
and
53.6
°
F
(
6,
9,
and
12
°
C),
but
noted
an
increase
to
15%
mortality
at
59
°
F
(
15
°
C).
Alevin
mortality
was
less
than
5%
at
all
temperatures
tested,
but
alevins
hatching
at
59
°
F
(
15
°
C)
were
considerably
smaller
and
appeared
less
well
developed
than
those
incubated
at
the
lower
test
temperatures.
Redding
and
Schreck
(
1979)
similarly
found
that
emergent
fry
were
larger
at
53.6
°
F
(
12
°
C)
than
at
60.8
°
F
(
16
°
C).
Based
on
the
works
reviewed
above,
it
appears
that
an
optimal
constant
incubation
temperature
occurs
below
51.8­
53.6
°
F
(
11­
12
°
C).
No
specific
research
results
were
found
that
could
be
used
to
suggest
a
single
daily
maximum
temperature
limit
for
waters
containing
incubating
steelhead.

Nonanadromous
rainbow
trout.
Kamler
and
Kato
(
1983)
tested
incubation
survival
at
48.2,
50,
53.6,
57.2,
and
60.8
°
F
(
9,
10,
12,
14,
and
16
°
C).
They
found
the
highest
survival
of
eggs
at
50
and
53.6
°
F
(
10
and
12
°
C),
slightly
lower
survival
at
57.2F
(
14
°
C),
and
abrupt
dro
ps
in
survival
at
both
48.2
°
F
(
9
°
C)
and
60.8
°
F
(
16
°
C).
Velsen
(
1987)
compiled
data
on
the
incubation
survival
of
both
rainbow
trout
and
steelhead
trout
that
showed
survival
was
consistently
high
(>
92%)
between
39.2
and
48.2
°
F
(
4
and
9
°
C),
and
fair
(>
78%)
between
37.4
and
59
°
F
(
3
and
15
°
C),
but
very
poor
(
7%)
above
60.8
°
F
(
16
°
C).
Survival
to
the
swim­
up
stage
in
two
strains
of
rainbow
trout
had
94%­
98%
survival
at
44.6
°
F
(
7
°
C),
72%­
95%
at
39.2
°
F
(
4
°
C),
and
<
12%­
41%
survival
at
35.6
°
F
(
2
°
C)
(
Stonecypher
and
Hubert
1994).
Kwain
(
1975)
found
that
the
lowest
mortalities
occurred
at
44.6
and
50
°
F
(
7
and
10
°
C),
Billard
and
Breton
(
1977)
found
a
drop
in
fertility
at
temperatures
higher
than
50
°
F
(
10
°
C),
and
Kashiwagi
et
al.
(
1987,
as
cited
in
Taylor
and
Barton
1992)
found
optimal
hatching
occurred
at
50
°
F
(
10
°
C).
Humpesh
(
1985)
found
that
optimal
hatching
(>
90%)
occurred
between
44.6
and
51.8
°
F
(
7
and
11
°
C),
and
Alekseeva
(
1987,
as
cited
in
Taylor
and
Barton
1992)
suggested
that
optimal
incubation
occurs
with
temperatures
rising
from
41.5
°
F
to
50.9
°
F
(
5.3­
10.5
°
C).
Rombough
(
1988,
as
cited
in
Taylor
and
Barton
1992)
found
that
at
temperatures
less
than
53.6
°
F
(
12
°
C)
there
was
less
than
4%
mortality.
Constant
temperatures
above
53.6
°
F
(
12
°
C)
have
produced
variable,
but
generally
lower
survival
during
incubation
temperatures,
with
often
severe
losses
occurring
at
temperatures
of
59­
60.8
°
F
(
15­
16
°
C)
(
Velsen
1987,
Billard
and
Breton
1977,
Kwain
1975,
Kamler
and
Kato
1983,
and
Rombough
1988,
as
cited
in
Taylor
and
Barton).
37
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
On
the
basis
of
the
literature
cited
above,
we
can
generally
conclude
that
constant
or
acclimation
temperatures
in
the
range
of
44.6­
50
°
F
(
7­
10
°
C)
are
opt
imal
for
incubation
and
embryonic
development
of
rainbow
trout.
No
specific
studies
were
found
that
test
the
ability
of
O.
mykiss
eggs
or
alevin
to
survive
high
single
daily
maximum
temperatures.

Cutthroat
trout.
Eggs
o
f
sea­
run
cutthroat
incubate
6­
7
wk
before
they
hatch,
and
the
alevin
remain
in
the
gravel
fo
r
about
another
2
wk
before
they
emerge
(
Trotter
1989,
Pauley
et
al.
1989).
Fry
may
emerge
from
March
through
June,
depending
on
the
location
and
time
of
spawning,
but
peak
emergence
occurs
in
mid­
April
(
Trotter
1989,
Wydoski
and
Whitney
1979).
Pauley
et
al.
(
1989)
cite
studies
demonstrating
that
the
optimum
temperature
for
incubation
is
50­
60.8
°
F
(
10­
11
°
C).
Bell
(
1986)
has
suggested
that
the
range
for
hatching
of
cutthroat
trout
eggs
is
from
39.9
to
55
°
F
(
4.4­
2.8
°
C).
Smith
et
al.
(
1983)
found
that
west
­
slope
cutthroat
trout
eggs
held
in
creek
water
with
a
fluctuating
temperature
of
35.6­
50
°
F
(
2­
10
°
C)
had
significantly
better
survival
than
eggs
held
at
a
constant
50
°
F
(
10
°
C).

Hubert
and
Gern
(
1995)
found
68.6%
survival
in
a
control
population
held
at
44.6
°
F
(
7
°
C)
when
testing
the
effects
of
lowering
incubation
temperatures
in
the
early
stage
of
development.
Mortality
rates
were
no
different
from
controls
when
temperatures
were
lowered
to
37.4
°
F
(
3
°
C)
at
least
13­
15
d
after
fertilization
but
were
higher
if
the
cooling
took
place
sooner.
Stonecypher
and
Hubert
(
1994)
found
that
survival
to
swim­
up
stage
in
Snake
River
cutthroat
trout
was
95%
at
44.6
°
F
(
7
°
C),
approximately
87%
at
39.2
°
F
(
4
°
C),
and
less
than
16%
at
35.6
°
F
(
2
°
C).

It
is
somewhat
problematic
to
set
standards
to
protect
the
incubation
of
cutthroat
trout
t
hat
can
be
reasonably
applied
statewide.
Cutthroat
are
a
spring
spawning
species
that
often
spawns
high
in
the
watershed
and
has
a
very
broad
period
of
spawning
when
examined
statewide.
Stocks
that
exist
in
lower
or
warmer
watersheds
spawn
as
early
as
February
when
temperatures
rise
above
42.8
°
F
(
6
°
C),
whereas
stocks
that
exist
in
high­
elevation
snow­
melt
streams
may
need
to
wait
until
late
June
or
July
for
waters
to
be
sufficiently
warm
(
42.8­
51.8
°
F
[
6­
11
°
C])
for
successful
spawning.
If
there
were
no
risk
o
f
egg
loss
from
sudden
late
winter
and
spring
freshets,
we
could
suggest
that
the
spring
spawning
strategy
is
relatively
unencumbered
by
changes
in
the
temperature
regime.
Although
earlier
spawning
exposes
cutthroat
eggs
to
higher
risks
of
physical
damage,
the
earlier
hatch
also
places
surviving
resident
fry
in
a
good
position
to
maximize
summer
growth
and
thus
increase
their
survival
opportunities
over
the
following
winter.
It
may
well
be
that
the
superior
growth
of
anadromous
salmonids
in
the
ocean
phase
makes
increases
in
weight
gain
from
earlier
emergence
of
less
value,
but
this
relat
ionship
remains
to
be
tested.
In
general,
specific
stocks
will
have
adapted
their
spawning
and
emergence
periods
to
optimize
both
incubation
survival
and
early
fry
growth.
Significant
changes
in
the
temperature
regime,
such
as
earlier
spring
warming,
will
bring
unknown
risks
to
individual
populations.
Therefore,
although
an
optimal
temperature
regime
is
recommended
in
this
paper
for
cutthroat
trout,
it
would
be
best
to
tailor
it
to
the
historic
spawning
patterns
found
in
specific
stocks.
To
initiate
spawning
in
most
stocks,
the
water
temperatures
must
at
least
warm
up
to
daily
maximums
of
42.8­
44.6
°
F
(
6­
7
°
C),
although
some
stocks
may
not
begin
spawning
until
temperatures
reach
51.8
°
F
(
11
°
C).
Specific
studies
on
incubation
survival
suggest
that
incubation
may
be
optimized
with
constant
or
acclimation
temperatures
in
the
range
of
44.6­
50
°
F
(
7­
10
°
C).
No
specific
basis
was
found
in
the
literature
for
setting
single
daily
maximum
criteria
for
the
incubation
of
cutthroat
trout.
38
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
What
are
the
conclusions
for
incubation
requirements?

Spawning
signals
the
beginning
of
the
life­
cycle
stage
(
egg
deposition
and
initial
egg
incubation)
that
is
most
sensitive
to
warm
waters.
Critical
spawning
temperatures
for
a
variety
of
salmonids
are
summarized
in
Table
5.
Because
the
spawning
period,
egg
fertilization,
and
initial
incubation
are
sensitive
life
stages
dependent
on
thermal
regimes,
special
consideration
must
be
given
to
ensure
that
criteria
to
protect
incubation
are
applied
at
the
proper
time
of
year.

Table
5.
Upper
optimal
temperature
regimes
based
on
constant
or
acclimation
temperatures
necessary
to
achieve
full
spawning
protection
of
the
nine
key
cold­
water
fish
species
indigenous
to
the
Pacific
Northwest
Fish
species
Critical
spawn
temperatures
Upper
optimal
temperature
range
°
F
(
°
C)
Single
daily
maximum
temperature
°
F
(
°
C)

Chinook
48.2­
50
(
9­
10)
56.3­
58.1
(
13.5­
14.5)

Pink
50­
53.6
(
10­
12)

Chum
46.4­
50
(
8­
10)

Char
35.6­
42.8
(
2­
6)
42.8
(
6)

Sockeye
46.4­
50
(
8­
10)

Coho
44.6­
50
(
7­
10)

Cutthroat
44.6­
50
(
7­
10)

Rainbow
44.6­
50
(
7­
10)

Steelhead
51.8­
53.6
(
11­
12)

Growth
For
growth,
what
are
the
demands
for
energy
and
how
is
the
balance
determined
by
temperature?

In
terms
of
energy
budgets,
fish
production
energy
(
P)
equals
the
sum
of
growth
(
G),
reproduction
(
Rp),
shed
scales
(
Ex),
and
secretions
(
S),
as
shown
in
the
following
equation:

P
=
G
+
Rp
+
Ex
+
S.

Energy
assimilated
from
food
equals
the
difference
between
energy
ingested
and
defecated,
or
A
=
I
!
F.

Energy
assimilated
is
distributed
into
production
(
P),
respiration
(
R),
and
excretion
(
U),
as
