Document ID: EPA-HQ-OW-2003-0068-0033
Agency: epa
Document Type: Supporting & Related Material
Title: 
Posted Date: 2003-09-22T04:00Z

57
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
Smoltification
How
is
smoltification
measured?

The
rate
of
silvering
during
smoltification
is
related
to
temperature,
presmolt
size,
migration
timing,
and
photoperiod
(
McMahon
and
Hartman
1988).
Silvering
generally
increases
with
increased
temperatures
(
Hoar
1988).
During
the
smolt
transformation,
body
lipids
decrease
in
quality
and
quantity
and
the
smolt
assumes
a
lower
condition
factor
(
weight
per
unit
length)
(
Hoar
1988).
Survival
of
smolts
in
the
marine
environment
depends
heavily
on
the
degree
of
smoltification,
which
can
be
measured
in
terms
of
ability
to
regulate
plasma
sodium
concentrations
and
grow
in
seawater
(
Mahnken
and
Waknitz
1979,
Clarke
and
Shelbourn
1985).

What
is
physiological
stress
and
at
what
temperatures
does
it
occur
in
salmonids?

Many
stressors
can
induce
physiological
stress
in
salmonids.
These
include
temperature
(
high,
low,
or
thermal
shock),
hyperosmotic
stress
(
when
juveniles
enter
the
saline
waters
of
the
estuary
or
ocean),
migration
(
physical
exertion),
crowding,
and
other
factors.
Stress
can
be
detected
via
changes
in
the
endocrine
system.
A
promising
indicator
of
smoltification
is
the
sharp
increase
in
thyroxine
(
T4)
in
blood
plasma
(
Wedemeyer
et
al.
1980).
Numerous
other
physiological
tests
are
available
to
index
the
degree
of
stress
on
fish
health
(
Wedemeyer
1980,
Iwama
et
al.
1998,
Beckman
et
al.
2000).
Among
these
are
measures
of
plasma
glucose
and
cortisol
as
indices
of
acute
or
chronic
stress
(
Wedemeyer
1980),
changes
in
gill
ATPase
activity
(
Zaugg
1981),
and
heat
shock
protein
production
(
Iwama
et
al.
1998).

Not
all
stress
or
associated
endocrine
changes
are
bad.
Migration
upstream
in
adults
and
downstream
in
juveniles
or
the
smoltification
process
are
stressful
but
essential
aspects
of
salmon
life
history.
These
processes
involve
instantaneous
to
seasonal
shifts
in
endocrine
balance
that
reflect
physiological
processes
over
time.
During
smoltification
there
is
a
predictable
pattern
of
gill
ATPase
activity
throughout
the
downstream
migration
(
Beckman
et
al.
2000).
However,
any
physiological
process
can
be
disrupted.
In
terms
of
thermal
influence,
this
can
alter
developmental
rates
(
shift
t
he
timing
of
life
history
events),
or
impair
or
inhibit
functions.
Impairment
caused
by
thermal
stress
can
be
increased
when
it
is
combined
with
other
stressors
(
e.
g.,
low
dissolved
oxygen).
Habitat
destruction
and
water
pollution
can
act
together,
leading
to
a
cumulative
stress.
The
magnitude
of
the
stress
can
be
detected
using
endocrine
(
ATPase,
cortisol),
biochemical
(
e.
g.,
lipid),
morphological
(
e.
g.,
body
shape,
condition
factor,
degree
of
silvering),
or
developmental
(
stage
of
egg
development)
indicators
to
detect
deviation
from
normal
range
or
rate
of
change.

Thermal
stress
is
any
temperature
change
that
significantly
alters
biological
functions
of
an
organism
and
lowers
probability
of
survival
(
Elliott
1981).
Stress
was
categorized
by
Fry
(
1947
as
cited
by
Elliott
1981)
and
Bret
t
(
1958)
as
lethal
(
leading
to
death
within
the
resistance
time),
limiting
(
restricting
essential
metabolites
or
interfering
with
energy
metabolism
or
respiration),
inhibiting
(
interfering
with
normal
functions
such
as
reproduction,
endocrine
and
ionic
balance,
and
feeding
functions),
and
loading
(
increased
burden
on
metabolism
that
controls
growth
and
activity).
The
latter
three
stresses
can
be
lethal
when
continued
over
a
long
period
(
Elliott
1981).
58
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
Loading
stress
increases
with
temperature
above
the
positive
growth
zone,
but
it
also
increases
with
reduction
in
food
availability
because
this
shrinks
the
growth
zone.
Thermal
stress
can
have
a
cumulative
effect
between
the
feeding
limit
(
temperature
at
which
feeding
ceases,
slightly
beyond
the
chinook
growth
limit
of
66.4
°
F
[
19.1
°
C])
and
the
UILT
(
Elliott
1981).
Within
this
zone
the
combined
effects
of
foo
d
limitation,
low
oxygen
concentrat
ion,
high
t
urbidity,
competition
for
space,
and
temperature
can
result
in
death
(
Elliott
1981,
Wedemeyer
and
McLeay
1981).
This
is
the
so­
called
tolerance
zone,
identified
by
Elliott
as
the
exposure/
acclimation
temperature
bounded
by
the
UILT
for
7­
d
exposure.
Reduced
oxygen
concentration
and
other
factors
can
accentuate
thermal
stress
(
Wedemeyer
and
McLeay
1981)
even
within
the
growth
zone
and
can
lower
the
optimum
growth
temperature.

What
are
the
seasons
for
passage
of
smolts
of
common
anadromous
species
and
how
would
this
information
be
used?

The
timing
of
smolt
passage
relative
to
the
water
temperature
regime
of
migration
habitat
is
vital
to
surviving
the
passage,
feeding,
avoiding
predators,
avoiding
disease,
and
improving
the
level
of
smolt
ification
during
emigrat
ion.
Some
general
dates
of
smolt
passage
past
selected
dams
on
the
Columbia
and
Snake
Rivers
are
given
in
Table
6
as
a
representation
of
the
issues
that
need
to
be
considered.
For
example,
passage
of
any
species
or
life
history
type
can
occupy
an
extensive
time
period.
To
allow
full
protect
ion
of
the
run,
the
total
duration
of
the
run
must
be
known.
However,
t
here
is
considerable
year­
to­
year
variation
in
timing.
In
addition,
the
downstream
passage
of
smolts
and
adults
of
the
same
stock
may
be
different.
That
is,
protection
of
a
stock
involves
providing
suitable
water
temperatures
for
all
life
stages.

What
are
heat
shock
proteins
and
what
do
they
indicate?

Heat
shock
proteins
(
HSPs)
are
expressed
in
response
to
biotic
and
abiotic
stressors
(
e.
g.,
heat
or
cold
shock,
anoxia,
diseases,
chemical
contaminants
including
heavy
metals).
These
unique
proteins
are
produced
in
cells
and
tissues
of
many
organisms,
including
fish
(
Dietz
1994,
Iwama
et
al.
1998)
under
environmental
stress.
They
have
many
biochemical
roles,
including
proper
folding
of
cellular
proteins
and
restoring
thermally
denatured
proteins
to
their
native
state.
Temperatures
at
which
HSPs
are
induced
can
be
mediated
by
acclimation
temperature
(
Dietz
1994).
Although
HSPs
can
be
related
to
thermal
tolerance,
their
presence
also
indicates
environmental
stress.
Although
they
help
repair
cellular
protein
damage
caused
by
stressors
such
as
high
temperature,
they
are
a
useful
indicator
of
thermal
stress
t
hat
requires
tissue
repair
(
Currie
and
Tufts
1997)
and
leads
to
irreparable
cell
damage.

What
temperature
range
is
recomm
ended
for
reducing
physiological
stress?

The
optimum
temperature
range
provides
for
feeding
activity,
normal
physiological
response,
and
normal
behavior
(
i.
e.,
without
thermal
stress
symptoms)
and
is
slightly
wider
than
the
growth
range.
Deviation
from
this
range
implies
greater
stress,
leading
to
greater
impairment
in
physiological
functions
and
greater
mortality.
Stresses
of
migration
and
acclimation
to
saltwater
activate
many
low­
grade
infections
by
freshwater
disease
organisms
(
Wedemeyer
et
al.
1980)
and
the
mortalities
produced
by
these
diseases
go
largely
unnoticed.
Optimum
temperatures
likewise
minimize
physiological
stress.
Growth
temperatures
that
are
optimum
or
59
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
lower
tend
to
be
minimally
subject
to
warm­
water
diseases.

Table
6.
Historical
dates
of
smolt
migration
past
selected
dams
on
the
Columbia
and
Snake
Rivers.
Data
from
Fish
Passage
Center
(
1993)

Monitoring
Sites
(
dams)
Species
Historical
Passage
Dates1
10%
50%
90%

Lower
Granite
Chinook
1'
s
4/
17
4/
27
5/
24
Chinook
0'
s
na
na
na
Steelhead
4/
28
5/
12
6/
01
Sockeye
na
na
na
Rock
Island
Chinook
1'
s
4/
22
5/
07
5/
22
Chinook
0'
s
6/
06
7/
04
8/
02
Steelhead
5/
06
5/
15
5/
31
Coho
5/
13
5/
21
5/
29
Sockeye
4/
19
5/
02
5/
26
McNary
Chinook
1'
s
4/
23
5/
10
5/
23
Chinook
0'
s
6/
15
7/
03
7/
20
Steelhead
4/
29
5/
18
6/
02
Coho
5/
16
5/
21
5/
31
Sockeye
5/
01
5/
16
6/
03
John
Day
Chinook
1'
s
4/
28
5/
15
5/
30
Chinook
0'
s
6/
08
7/
21
9/
01
Steelhead
4/
26
5/
15
5/
31
Coho
5/
06
5/
13
5/
31
Sockeye
5/
10
5/
22
6/
04
Bonneville
Chinook
1'
s
4/
19
5/
02
5/
21
Chinook
0'
s
na
na
na
Brights2
6/
07
6/
27
7/
29
Steelhead
4/
26
5/
14
5/
31
Coho
4/
27
5/
10
6/
01
Sockeye
5/
11
5/
23
6/
04
1
Historical
percentiles
are
based
on
passage
data
for
7
years
(
1984­
90)
at
Lower
Granite
and
McNary
dams;
6
years
(
1985­
90)
at
Rock
Island
Dam;
4
years
(
1986­
89)
at
John
Day
Dam;
and
4
years
(
1987­
90)
at
Bonneville
Dam
for
spring
migrants
and
3
years
(
1988­
90)
for
summer
migrants.

2
"
Brights"
at
Bonneville
Dam
refers
to
subyearling
chinook
arriving
after
June
1;
this
excludes
most
"
tule"
fall
chinook
originating
from
Spring
Creek
hatch
ery.

Why
might
it
be
adv
isable
to
use
naturally
re
ared
vs.
h
atchery­
reared
salm
onids
to
measure
physiological
status?

Significant
differences
between
conditions
in
the
field
and
in
the
hatchery
can
lead
to
different
physiological
responses
in
these
environments.
For
example,
these
environments
may
have
different
seasonal
temperature
profiles,
photoperiod,
nutrition,
and
social
interactions,
which
could
produce
variations
in
developmental
timing,
growth
rate,
size
at
age,
and
body
composition
(
Beckman
et
al.
2000).
Consequently,
the
physiological
status
of
hatchery­
reared
fish
may
not
60
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
relect
that
of
naturally
reared
fish.

Differences
in
physiological
indicators
between
hatchery
and
wild
salmonids
were
reported
for
Columbia
River
chinook
(
Congleton
et
al.
2000).
Co
rtisol
concentrations
were
higher
in
wild
than
hatchery
chinook
in
early,
mid­,
and
late
season.
In
this
study,
cortisol
was
used
as
an
indicator
of
stress
in
barge
transportation.
However,
for
both
wild
and
hatchery
fish,
cortisol
declined
during
the
barging
in
early
and
late
season,
but
not
mid­
season.
This
effect
was
produced
by
social
interaction
with
the
high
densities
of
steelhead
that
were
loaded
on
barges
in
mid­
season,
causing
stress
in
chinook.
In
addition,
ATPase
activity
was
significantly
lower
in
migrating
hatchery
steelhead
and
chinook
in
the
Columbia
River
than
in
the
wild
fish
of
these
species.
These
differences
were
greatest
in
late
April
to
early
May.
Hatchery
rearing
can
result
in
suppression
of
gill
ATPase
activity
for
at
least
7
wk
after
release
(
Congleton
et
al.
2000).

How
does
physiological
status
of
smolting
salmon
change
seasonally?

Few
studies
on
smolting
salmonids
monitor
a
broad
range
of
physiological
indicators,
much
less
study
salmon
in
the
wild
throughout
the
year.
Beckman
et
al.
(
2000)
reported
endocrine
and
physiological
status
of
naturally
reared
spring
chinook
juveniles
in
the
Yakima
River,
Washington.
Status
was
measured
in
terms
of
condition
factor,
weight,
stomach
fullness,
body
appearance,
liver
glycogen,
body
lipid,
gill
Na+­
K+
ATPase,
plasma
thyroxine
(
T4),
and
plasma
insulin­
like
growth
fact
or­
I
(
IGF­
I).
The
smolting
period
(
April­
May)
was
characterized
by
an
increase
in
ATPase
activity,
plasma
T4,
and
IGF­
I.
At
the
same
time
there
was
a
decrease
in
condition
factor,
body
lipid,
and
liver
glycogen.
Body
lipid
reached
a
high
in
late
summer
(
5%­
8%)
and
a
low
during
winter
of
2%­
3.5%,
and
then
increased
to
4%
by
March.
Body
lipid
again
declined
during
April­
May,
when
smolting
occurred.
Condition
followed
the
same
pattern
as
whole­
body
lipid
content.
Body
weight
of
juveniles
increased
dramatically
from
February
to
May.
A
similar
decline
in
body
lipid
content
was
reported
for
chinook
and
steelhead
from
the
American
River,
California
(
Castleberry
et
al.
1991).
High
lipid
content
in
juveniles
is
associated
with
high
adult
return
rates.
For
example,
fall
chinook
smolts
with
7.9%
whole
body
lipid
had
an
adult
return
rate
nearly
1.9
times
greater
than
those
having
only
4.1%
(
Burrows
1969
as
cited
by
Castleberry
et
al.
1991).

In
springtime,
plasma
T4,
IGF­
I,
and
gill
ATPase
increased
as
fish
migrated
downstream
in
the
Yakima
River
(
Beckman
et
al.
2000).
These
indicators
of
smolt
ification
have
been
reported
in
other
studies.
Other
reported
changes
include
increased
growth
rate,
increases
in
plasma
growth
hormone
(
GH),
and
metabolic
rates
(
Hoar
1988,
as
reported
by
Beckman
et
al.
2000).
During
smoltification
there
are
two
distinct
phases
 
first
anabolic,
then
catabolic.
The
anabolic
phase
in
Yakima
River
spring
chinook
occurs
from
January
through
March
and
is
characterized
by
an
increase
in
condition
factor,
IGF­
I,
weight,
and
lipid.
The
catabolic
phase
which
follows
from
April
through
May
is
characterized
by
an
increase
in
co
ndition
factor
and
IGF­
I,
but
a
decline
in
weight
and
lipid
content.
A
high
plasma
GH
causes
depletion
of
glycogen
and
lipid.

How
does
photoperiod
influence
growth
rate
and
subsequent
saltwater
readiness
of
smolts?

Juveniles
migrating
downstream
from
freshwater
t
o
saltwater
exhibit
saltwater
readiness
in
61
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
their
ability
to
regulate
plasma
sodium
concentrations.
If
high
water
temperatures
impair
smoltification
processes,
including
the
ability
to
regulate
plasma
sodium,
survival
in
saltwater
would
be
reduced.
The
ability
of
a
juvenile
to
regulate
plasma
sodium
depends
on
its
growth
rate
and
consequent
size.
Growth
rate
is
a
function
of
temperature
and
food
availability.
A
study
of
spring
chinook
growth
rate
under
satiation
feeding
found
that
photoperiod
experience
at
first
feeding
(
i.
e.,
after
emergence)
helps
to
set
the
potential
growth
rate.
Juveniles
exposed
to
a
short­
day
photoperiod
from
February
to
mid­
April
followed
by
a
long­
day
photoperiod
had
a
significantly
greater
growth
rate
and
final
body
weight
by
midsummer
than
juveniles
that
experienced
only
a
long­
day
photoperiod
(
Clarke
et
al.
1992).
A
long­
day
photoperiod
after
emergence
is
apparently
a
developmental
cue
that
produces
a
slower
growth
rate
than
in
fish
exposed
to
a
short­
then
long­
day
photoperiod
at
the
same
temperature.
This
cue
causes
juveniles
to
overwinter
at
least
1
year
before
emigration.
In
saltwater
challenge
tests,
the
ability
of
juveniles
to
regulate
plasma
sodium
by
midsummer
depended
on
their
experiencing
the
natural
sequence
of
photoperiods.
It
is
questionable
whether
juveniles
that
experienced
a
long­
day
photoperiod
at
emergence
would
actually
attempt
to
emigrate
in
the
first
summer.
Growth
rate
and
body
size
are
vital
in
determining
tendency
to
emigrate
and
subsequent
survival
(
Bilton
et
al.
1982).
The
study
by
Clarke
et
al.
(
1992)
does
highlight
the
need
to
consider
photoperiod
history
from
emergence
through
rearing
as
well
as
food
availability
and
temperature
in
comparisons
of
growth
rates
between
stocks.

Salmon
parr
feed
throughout
the
summer
in
streams,
gaining
weight
,
length,
and
lipid
content
(
see
Beckman
et
al.
2000).
As
autumn
approaches,
Atlantic
salmon
parr
may
become
segregated
into
two
size
groups,
indicating
their
ability
to
smolt
the
following
spring
(
upper
modal
group)
or
the
need
to
spend
another
year
growing
in
freshwater
(
lower
modal
group)
(
Metcalfe
and
Thorpe
1992).
Overwintering
salmon
undergo
a
period
of
anorexia
(
loss
of
body
fat)
coinciding
with
a
loss
of
appetite
and
cessation
of
growth,
even
when
food
is
present
.
The
onset
of
anorexia
is
controlled
by
photoperiod
(
Thorpe
1986,
as
cited
by
Metcalfe
and
Thorpe
1992).
However,
the
loss
in
body
fat
is
controlled
by
variable
"
defended"
energy
levels.
That
is,
fish
that
will
smolt
in
the
spring
maintain
a
higher
appetite
and
feeding
rate.
This
balances
energy
costs
of
maintaining
a
feeding
station
and
capturing
food
against
the
gain
in
growth
rate
and
ability
to
smolt
early,
thereby
avoiding
mortality
in
a
second
overwintering
period.

Are
smolts
affected
by
high
temperatures
during
migration?

Migration
during
the
smolt
phase
can
be
lethal.
For
example,
in
the
lower
Sacramento
River,
a
50%
mortality
was
estimated
over
a
48­
km
migration
distance,
based
on
smolt
releases
during
the
May­
June
period,
1983­
1990.
These
mortalities
were
associated
with
temperatures
of
73.4
±
1.9
°
F
(
23
±
1.1
°
C)
(
Baker
et
al.
1995).

In
addition
to
thermally
induced
mortality
during
migration,
smolting
juveniles
can
be
indirectly
affected
by
high
temperatures.
For
example,
subyearling
chinook
rearing
in
nearshore
areas
of
the
Columbia
River
can
be
forced
into
the
main
current
to
avoid
increasing
temperatures
along
river
margins.
This
becomes
significant
above
62.6
°
F
(
17
°
C)
(
Connor
et
al.
1999).
Reduced
food
in
marginal
areas
of
the
river
coupled
with
high
wat
er
temperatures
reduces
the
capability
of
the
river
to
rear
fish
to
proper
smolt
condition
(
Coutant
1999).
62
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
Gill
ATPase
is
a
useful
indicator
of
smolt
ification.
In
the
Columbia
River,
high
levels
of
gill
ATPase
activity
are
frequently
associated
with
longest
travel
time
downstream
through
the
dams.
However,
subyearling
fall
chinook
have
occasionally
exhibited
slowest
travel
times
with
highest
ATPase
levels
(
Tiffan
et
al.
2000).
Rapid
juvenile
growth
in
premigrants
typically
accompanies
increasing
ATPase
levels,
leading
to
increased
ability
to
osmoregulate
in
seawater.
Migration
in
an
impounded
river
may
alter
the
relationship
between
ATPase
and
time
of
ocean
entry.
Tiffan
et
al.
(
2000)
determined
that
ATPase
activity
increased
for
Hanford
Reach
fall
chinook
from
Hanford
Reach
to
McNary
Dam
and
decreased
afterward.
Even
though
saltwater
mortality
declined
over
this
migration
path,
the
decline
in
ATPase
activity
in
1994
appeared
to
be
greater
than
in
1995.
The
greater
1994
loss
may
account
for
that
year's
higher
mortality
rate
in
saltwater
challenges.
Chinook
smolts
often
migrate
during
reduced
streamflows
and
elevated
water
temperatures.
Mainstem
dams
cause
significant
delays
in
migration
rates,
and
smolts
in
reservoir
forebays
undergo
prolonged
exposure
to
surface
temperatures
as
high
as
77
°
F
(
25
°
C)
or
more
(
Venditti
et
al.
2000).
Such
high
temperatures
limit
fall
chinook
production
by
impairing
the
ability
of
juveniles
to
grow,
smolt,
and
maintain
appropriate
migration
timing.
Late
emigration
results
in
the
lowest
survival
rates
(
Connor
et
al.
1999).

Are
smolts
subject
to
cumulative
stresses
from
thermal
exposure?

Temperatures
of
64.9­
70
°
F
(
18.3­
21.1
°
C)
place
smolts
under
either
lethal
or
loading
stresses
that
can
impair
metabolic
activity
(
Brett
1958).
For
example,
in
subyearling
fall
chinook
in
the
Columbia
River,
temperatures
of
64.4­
68
°
F
(
18­
20
°
C)
inhibit
feeding.
Heat
shock
proteins
are
produced
after
exposure
to
68
°
F
(
20
°
C)
for
several
hours
(
Sauter
and
Maule
1997).

What
temperatures
are
required
to
inhibit
smoltification
in
steelhead
and
salmon?

Smolt
transformation
in
steelhead
rearing
in
water
>
52.3
°
F
(
11.3
°
C)
was
inhibited
(
Adams
et
al.
1973);
rearing
temperatures
>
55.4
°
F
(
13
°
C)
prevent
increases
in
ATPase
activity
(
Hoar
1988).
This
effect
is
stronger
in
steelhead
than
in
coho,
chinook,
o
r
Atlantic
salmon
(
Adams
et
al.
1973,
Adams
et
al.
1975
as
cited
by
Johnston
and
Saunders
1981).
Temperatures
>
56.5
°
F
(
13.6
°
C)
do
not
permit
smoltification
in
summer
steelhead
(
Zaugg
et
al.
1972,
as
cited
by
Zaugg
and
Wagner
1973).
In
winter
steelhead,
a
temperature
of
54.1
°
F
(
12.3
°
C)
is
nearly
the
upper
limit
for
smolting
(
Zaugg
and
Wagner
1973).
Zaugg
(
1981)
found
that
a
temperature
of
53.6
°
F
(
12
°
C)
could
inhibit
successful
migration
to
the
ocean
in
wint
er
steelhead.
Because
ocean
entry
in
the
Columbia
River
normally
occurs
in
mid
and
late
May
and
river
temperatures
typically
reach
53.6
°
F
(
12
°
C)
by
mid­
May,
failure
of
steelhead
smolts
to
enter
the
ocean
may
be
attributed
to
low
water
flow
and
associated
high
water
temperatures
(
Zaugg
1981).
Dawley
et
al.
(
1979
as
cited
by
Zaugg
1981)
observed
that
peak
steelhead
migration
to
the
ocean,
as
determined
by
capture
at
Jones
Beach,
coincided
with
river
temperatures
above
53.6
°
F
(
12
°
C).

In
the
American
River,
California
juvenile
steelhead
(
young­
of­
the­
year)
were
captured
during
their
downstream
migration
for
measurement
of
Na+
­
K+
ATPase
(
Castleberry
et
al.
1991).
The
authors
reported
that
ATPase
act
ivity
increased
from
capture
temperatures
of
60.8
°
F
(
16
°
C)
to
68
°
F
(
20
°
C),
and
that
increased
river
temperatures
did
not
suppress
smoltification,
but
may
have
enhanced
it.
However,
they
also
noted
that
ATPase
activity
was
uniform
for
fish
of
standard
lengths
from
60
to
100
mm.
The
authors
interpreted
this
evidence
to
mean
that
63
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
steelhead
did
not
develop
into
smolts
at
sizes
below
100
mm
SL.
Furthermore,
they
did
not
sample
steelhead
longer
than
100
mm
but
indicated
they
were
not
common.
In
the
American
River,
steelhead
emerged
from
early
April
through
early
May
and
were
abundant
in
the
middle­
lower
river
site
from
early
May
to
early
June.
At
t
his
period,
temperatures
cycled
daily
from
61.7
to
66.2
°
F
(
16.5­
19
°
C).
In
addition,
capture
temperatures
up
to
mid­
May
were
often
as
much
as
3.6
°
F
(
2
°
C)
greater
than
the
average
temperature
for
the
2­
wk
period
prior
to
capture,
meaning
that
the
correlation
of
ATPase
with
temperature
may
not
be
as
meaningful
as
believed.
This
study
did
not
deal
with
yearling
steelhead
and
did
not
describe
successful
smolt
migration.
Steelhead
usually
do
not
migrate
to
sea
until
reaching
age
1
to
3
years
(
Moyle
1976,
as
cited
by
Castleberry
et
al.
1991),
so
it
is
not
clear
what
relevance
ATPase
activity
in
age­
0
juveniles
has
to
smolt
saltwater
readiness,
but
it
does
indicate
temperature
ranges
that
juveniles
experience
in
their
pre­
smolt
migrations.
These
data
do
not
appear
to
challenge
the
large
body
of
literature
detailing
the
sensitivity
of
steelhead
smolts
to
migration
temperatures
>
53.6­
55.4
°
F
(
12­
13
°
C).

Some
smoltification
processes
are
greatly
retarded
by
water
temperatures
>
55.4
°
F
(
13
°
C),
and
in
some
Pacific
salmonids
smolt
stage
cannot
be
attained
at
60.8
°
F
(
16
°
C)
(
see
references
cited
by
Johnston
and
Saunders
1981).
An
apparent
exception
is
that
temperatures
as
high
as
59
°
F
(
15
°
C)
have
been
used
to
increase
growth
rate
and
onset
of
smolting
in
coho.
However,
desmoltification
is
also
high
at
this
temperature.
Laboratory
tests
clearly
showed
that
a
high
constant
temperature
regime
of
68
°
F
(
20
°
C)
during
coho
emigration
caused
a
very
restricted
peak
in
gill
ATPase
activity
compared
with
a
normal
50
°
F
(
10
°
C)
temperature
regime.
Under
the
elevated
temperature
regime,
ATPase
activity
plummeted
prior
to
ocean
entry
(
Zaugg
and
McLain
1976).
Fall
chinook
undergo
an
even
greater
desmoltification
rate
at
temperatures
of
59
°
F
(
15
°
C)
(
Wedemeyer
et
al.
1980).
In
work
on
Central
Valley
chinook
stocks
from
California,
Marine
(
1997)
found
that
normal
smolt
development
patterns
can
be
altered
or
inhibited
with
prolonged
rearing
in
a
temperature
range
of
62.6­
75.2
°
F
(
17­
24
°
C)
compared
with
rearing
in
a
range
of
55.4­
60.8
°
F
(
13­
16
°
C).
Evidence
for
the
effects
of
temperatures
exceeding
62.6
°
F
(
17
°
C)
came
from
changes
in
gill
ATPase
activity,
reduced
survival
in
acute
seawater
exposure,
and
a
reduced
hypo­
osmoregulatory
capability.
In
addition,
juvenile
chinook
exposed
for
2.5
months
to
62.6­
75.2
°
F
(
17­
24
°
C)
incurred
increased
loss
to
predation
compared
with
juveniles
exposed
in
the
range
55.4­
60.8
°
F
(
13­
16
°
C),
although
the
causal
mechanism
was
not
identified.
Sockeye
terminate
their
downstream
migration
if
water
temperature
exceeds
53.6­
57.2
°
F
(
12­
14
°
C)
(
Brett
et
al.
1958),
although
coho
can
withstand
some
further
increases.
The
influence
on
the
smoltification
process,
though,
may
be
common
to
both
species.

What
temperatures
are
required
to
reverse
smoltification
in
steelhead?

Yearling
steelhead
held
at
43.7
°
F
(
6.5
°
C)
and
transferred
to
59
°
F
(
15
°
C)
had
a
marked
reduction
in
gill
ATPase
activity,
indicating
a
reversal
of
some
smolting
changes
(
Wedemeyer
et
al.
1980).
When
temperatures
exceeded
55.4
°
F
(
13
°
C),
gill
Na­
K­
ATPase
activity
declined
in
fish
that
had
already
begun
smoltification,
and
there
was
a
decreased
ability
to
migrate
(
Zaugg
and
Wagner
1973).
Zaugg
and
Wagner
(
1973)
considered
this
effect,
operating
well
below
lethal
limits,
to
have
serious
implications
for
survival
o
f
steelhead
because
it
inhibited
migrat
ory
ability.

Can
incubation
temperature
affect
smolt
emigration
timing?
64
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
Temperature
regime
can
influence
time
of
smolt
emigration.
Research
on
Carnation
Creek,
British
Columbia,
revealed
that
most
variation
in
chum
and
coho
emigration
dates
was
attributed
to
mean
stream
temperatures
between
peak
spawning
and
emergence
(
Holtby
et
al.
1989).
Shifts
in
this
portion
of
the
annual
temperature
regime
were
linked
to
land­
use
practices
(
Hartman
et
al.
1984).
Alteration
in
the
emigration
date
in
turn
can
affect
survival
in
the
marine
environment
(
Thedinga
and
Koski
1984,
Holtby
et
al.
1989).
From
laboratory
studies,
it
would
appear
that
an
accelerated
temperature
regime
during
springtime
would
result
in
either
earlier
emigration
(
caused
by
more
rapid
development
to
the
smolt
stage)
or
less
success
in
smoltification
(
caused
by
high
temperature
desmoltification
or
inhibitory
effects)
(
see
Zaugg
and
Wagner
1973).

What
river
temperatures
are
associated
with
peaks
in
migration?

Most
steelhead
emigration
occurs
before
river
temperatures
rise
above
53.6
°
F
(
12
°
C).
Emigration
can
extend
into
temperatures
as
high
as
61.7
°
F
(
16.5
°
C).
The
53.6
°
F
(
12
°
C)
limiting
temperature
normally
does
not
occur
until
mid­
May,
but
in
low­
flow
years
can
occur
in
late
April;
this
shift
in
thermal
regime
may
cause
a
reduction
in
steelhead
survival
(
Zaugg
1981).
The
South
Umpqua
River,
a
so
uthern
Oregon
coast
al
river
subject
to
thermal
extremes,
has
a
wild
spring
chinook
run.
This
stock
begins
emigration
when
stream
temperatures
exceed
50
°
F
(
10
°
C).
Approximately
50%
of
the
emigration
takes
place
at
54.5­
59
°
F
(
12.5­
15
°
C)
and
the
upper
tail
of
the
run
is
generally
complete
befo
re
68
°
F
(
20
°
C)
is
exceeded.
Large
fish
that
are
presumably
most
ready
to
enter
the
ocean
delay
entry
until
temperatures
warm
beyond
50
°
F
(
10
°
C)
(
Roper
and
Scarnecchia
1999).
In
spring
chinook
from
the
American
River,
California,
juvenile
levels
of
gill
Na+­
K+
ATPase
increased
with
increasing
standard
length
between
30
and
80
mm
and
capture
temperature
from
53.6
to
64.4
°
F
(
12­
18
°
C)
(
Castleberry
et
al.
1991).
However,
juveniles
were
no
longer
found
in
the
lower
river
in
early
May.
Maximum
daily
temperatures
ranged
from
64.4
to
69.8
°
F
(
18­
21
°
C)
and
minimum
daily
temperatures
were
as
low
as
59
°
F
(
15
°
C).
Juveniles
were
found
in
the
middle
upper
site
in
late
June
when
diel
temperatures
fluctuated
regularly
between
approximately
59
and
64.4
°
F
(
15
and
18
°
C).
These
chinook
typically
enter
the
ocean
2­
4
months
after
emergence
at
a
size
o
f
40­
80
mm
(
sizes
of
juveniles
captured
at
monitoring
sites).
These
data
indicate
that
temperatures
as
high
as
64.4
°
F
(
18
°
C)
do
not
prevent
ATPase
levels
from
increasing,
but
temperatures
beyond
this
appear
to
eliminate
juveniles
from
affected
river
reaches.

How
do
freshwater
and
ocean
temperatures
affect
time
of
ocean
entry?

The
relation
of
the
temperature
of
the
lower
reach
of
a
river
entering
the
ocean
and
the
temperature
of
the
ocean
itself
is
important
in
determining
growth
rates
in
the
early
ocean
phase
and
survival.
Two
of
the
most
important
factors
regulating
seawater
adaptability,
such
as
ability
to
regulate
plasma
sodium,
are
freshwater
rearing
temperature
and
time
of
transfer
to
seawater.
The
relative
growth
rate
of
fall
chinook
in
seawater
was
greatest
after
rearing
in
freshwater
in
temperatures
of
46.4­
57.2
°
F
(
8­
14
°
C),
followed
by
transfer
to
55.4­
58.1
°
F
(
13­
14.5
°
C)
in
early
May
to
early
June.
Freshwater
rearing
at
60.8
°
F
(
16
°
C)
resulted
in
growth
rates
that
were
70%
of
those
at
50
°
F
(
10
°
C)
(
i.
e.,
a
temperature
within
the
preferred
range).

Smolts
must
be
able
to
regulate
plasma
sodium,
maintain
their
silver
color
(
indicative
of
their
degree
of
smoltification),
and
maintain
a
high
growth
rate.
The
temperatures
present
in
the
65
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
freshwater
environment
and
ocean
during
the
smolt's
emigration
and
ocean
entry,
as
well
as
its
timing
of
ocean
entry,
are
critical
in
determining
initial
growth
rates.
Freshwater
temperatures
must
be
low
enough
during
emigration
so
that
complete
smoltification
can
take
place
prior
to
ocean
entry.
If
all
these
conditions
are
met
(
and
also
the
size
of
migrants
leaving
the
natal
tributaries
is
optimum),
a
smolt
will
likely
be
able
to
maintain
critical
size
before
ocean
entry.
Otherwise,
desmoltification
can
take
place,
smolts
fail
to
maintain
a
critical
size,
and
they
become
parr­
revertants
(
Mahnken
and
Waknitz
1979,
Folmar
et
al.
1982).
By
losing
their
smolt
status,
juveniles
fail
to
enter
the
ocean,
die,
o
r
at
tempt
to
rear
in
the
lower
river
to
await
smolt
ification
in
a
subsequent
year,
which
is
unlikely.

Hatchery
releases
should
be
timed
to
avoid
extreme
temperatures
during
smoltification
to
ensure
maximum
passage
survival.
Releases
should
coincide
with
historic
migration
times,
however
(
Wedemeyer
et
al.
1980).
If
historic
migration
timing
now
coincides
with
adverse
temperatures,
naturally
produced
salmon
and
steelhead
are
likely
to
be
affected.
Altered
(
e.
g.,
earlier)
times
of
release
of
hatchery
fish
to
avoid
human­
caused
thermal
stress
may
result
in
inappropriate
ocean
entry
timing
and
lower
overall
survival.

What
is
the
role
of
temperature
in
migratory
response
and
seawater
adaptation?

A
maximum
temperature
of
approximately
53.6
°
F
(
12
°
C)
is
recommended
for
chinook
and
coho
to
maintain
migratory
response
and
seawater
adaptation
in
juveniles
(
Wedemeyer
et
al.
1980,
CDWR
1988,
p.
4).

Wedemeyer
et
al.
(
1980)
recommended
that
winter
and
spring
hatchery
water
temperatures
below
53.6
°
F
(
12
°
C)
would
protect
the
smoltification
process
for
chinook,
coho,
and
steelhead.
Their
recommendations
apply
to
proper
physiological
development
during
the
smoltification
process,
timing
of
saltwater
entry,
and
high
marine
survival.

How
can
multiple
stresses
during
the
smolting
phase
be
reduced?

Infection
of
fish
with
freshwater
diseases
should
be
minimized
because
the
stresses
of
migration
and
acclimatio
n
to
saltwater
can
increase
mortality
from
disease
(
Wedemeyer
et
al.
1980).
Warm­
water
diseases
can
be
transmitted
through
hatchery
practices,
by
contagion
in
migration
through
dam
passageways,
and
in
barging.

Human­
caused
increases
in
estuary
temperature
must
be
restricted.
In
addition,
numerous
chemical
contaminants,
such
as
herbicides,
that
can
become
concentrated
in
the
estuary
have
been
shown
to
inhibit
smolt
function
and
migratory
behavior
(
Wedemeyer
et
al.
1980).
The
smoltification
process
is
physiologically
stressful
to
fish.
Additional
stresses
associated
with
elevated
temperature
or
other
pollutants
should
be
avoided.
(
See
Multiple
Effects
issue
paper
for
a
detailed
discussion
of
these
effects.)

Swimming
Speed
How
is
swimming
speed
measured?
66
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
Sustained
swimming
performance
is
a
swimming
speed
that
can
be
maintained
for
long
periods
(>
200
min)
without
fatigue.
This
activity
is
totally
aerobic,
so
no
oxygen
debt
builds
up.
Sustained
swimming
during
migration
tends
to
occur
at
15%­
20%
of
maximum
swimming
speed
(
Bell
1991).
Some
tests
have
documented
swimming
for
periods
of
2
wk
without
fatigue
for
a
variety
of
species.
Prolonged
swimming
speeds
define
a
performance
of
shorter
duration
(
20
s­
200
min)
that
involves
both
aerobic
and
anaerobic
metabolism.
Exhaustion
of
glycogen
stores
can
result
in
fatigue.
Within
the
range
of
speeds
that
define
prolonged
swimming
at
a
particular
temperature,
the
faster
the
speed,
the
more
anaerobic
metabolism
is
responsible.
Critical
swimming
speed
is
a
special
case
of
prolonged
swimming.
It
may
be
measured
in
fish
swimming
at
a
particular
temperature
(
either
a
temperature
to
which
they
are
fully
acclimated
or
as
an
acute
performance
at
a
test
temperature)
or
by
increasing
swimming
velocity
in
increments
(
such
as
10
cm/
s)
to
determine
the
maximum
speed
at
which
swimming
can
be
maintained
for
a
fixed
period
(
e.
g.,
60
min).
If
a
fish
can
swim
60
min
continuously
at
50
cm/
s
but
only
a
fraction
of
t
hat
time
at
60
cm/
s,
the
crit
ical
speed
is
interpolat
ed.
A
median
performance
for
a
test
group
of
fish
is
taken
as
the
critical
swimming
speed.
Comparisons
among
sizes
within
a
species
can
be
made
in
terms
of
body
length/
s
rather
than
cm/
s.
Burst
swimming
is
the
maximum
swimming
rate
that
can
be
achieved
for
periods
up
to
20
s
and
is
largely
independent
of
temperature.
This
is
essential
for
prey
capture,
predator
avoidance,
and
rapid
migration
through
swift
water.
During
burst
swimming,
fish
consume
some
oxygen
but
are
powered
mostly
by
anaerobic
metabolism.
Burst
swimming
can
reach
approximately
22
ft/
s
in
chinook,
coho,
and
sockeye
and
up
to
27
ft/
s
in
steelhead
(
Bell
1991).

It
is
interesting
to
compare
swim
speeds
determined
from
laboratory
studies
with
those
from
field
studies.
Hinch
and
Rand
(
1998)
used
electromyogram
radiotelemetry
on
Fraser
River
sockeye
to
measure
tail
beat
frequency
(
TBF).
TBF
was
then
converted
to
swim
speeds
using
laboratory
regressions
of
TBF
against
swim
speed.
Swim
speeds
varied
by
reach
within
study
sections
in
accordance
with
constrictions,
channel
form,
and
probably
associated
flow
patterns.
In
a
7.6­
km
study
section
in
t
he
lower
Fraser
River,
including
the
Fraser
River
canyon,
average
swim
speeds
varied
from
approximately
75
to
125
cm/
s
in
the
10
consecutive
study
reaches.
In
this
river
section,
water
temperatures
ranged
from
60.8
to
66.2
°
F
(
16­
19
°
C)
during
tracking.
Speeds
varied
by
river
reach
depending
on
constrictions
and
channel
bank
form.
Male
sockeye
swam
at
mean
speeds
of
118
cm/
s
and
females
at
90
cm/
s.
In
another
study
year,
male
average
swim
speed
was
only
about
half
as
fast
(
i.
e.,
62
cm/
s).
Near
the
spawning
grounds
approximately
900
km
furt
her
upstream,
water
temperatures
ranged
from
68
to
71.6
°
F
(
20­
22
°
C)
and
average
swim
speeds
declined
to
50­
60
cm/
s
(
Hinch
and
Rand
1998).
This
decline
in
swim
speed
may
be
asso
ciated
with
the
warm
river
temperatures.
Other
explanations
might
be
that
those
individuals
that
migrate
at
very
high
swim
speeds
when
encountering
complex
flow
patt
erns
(
see
Hinch
and
Bratty
2000)
were
already
eliminated
from
the
population
by
exhaustion,
or
the
population
in
general
might
have
suffered
energy
depletion
t
hat
impaired
swimming
capacit
y.

Combinations
of
swimming
speeds
and
time
periods
exceeding
critical
time
limits
may
build
up
lactic
acid
in
tissues
and
require
resting
periods
of
up
to
3
hours
before
further
swimming
can
occur
(
Paulik
et
al.
1957).
Rate
of
recovery
from
anaerobic
metabolism
is
a
function
of
water
temperature
and
oxygen
concentration.

At
what
swimming
speeds
do
metabolic
transitions
occur?
67
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
Data
from
Bainbridge
(
1960,
1962)
for
rainbow
trout
and
Brett
(
1964)
for
sockeye,
as
summarized
in
a
single
figure
by
Beamish
(
1978),
illustrate
the
sharp
differentiation
among
sustained,
prolonged,
and
burst
swimming
performances
at
a
fixed
temperature.
As
swimming
speed
is
reduced
in
the
prolonged
swimming
zone
(
i.
e.,
performance
time
of
20
s­
200
min),
swimming
can
eventually
be
performed
without
fatigue;
this
point
denotes
the
transition
to
sustained
swimming
(
i.
e.,
the
temperature­
swimming
time
period
combination
that
allows
continuous
swimming
for
long
periods).
At
higher
swimming
speeds
in
the
prolonged
swimming
zone,
a
transition
occurs
in
the
plot
of
log
(
time
to
fatigue)
versus
velocity
that
denotes
a
transition
from
prolonged
to
burst
swimming
(
Beamish
1978).
This
transition
(
i.
e.,
of
the
critical
swimming
speed)
occurs
at
approximately
3
and
5
body
lengths/
s
in
rainbow
and
sockeye,
respectively.
At
these
velocities,
fatigue
occurs
in
approximately
20
s.
Burst
swimming
speed
increases
only
as
time
to
fatigue
decreases.
Because
of
evidence
such
as
this
for
many
fish
species,
20
s
is
generally
taken
as
the
period
producing
this
metabolic
transition.

Critical
swimming
speed
is
a
physiological
performance
measure
that
can
indicate
the
ability
of
a
fish
to
function
in
a
natural
flowing­
water
environment.
It
indicates
ability
to
capture
prey
and
avoid
predators
(
Castleberry
et
al.
1991).
Sharp
reductions
in
critical
swimming
speed
at
high
temperatures
indicate
environmental
risk
for
a
given
life
stage
and
fish
size
(
see
Griffiths
and
Alderdice
1972,
Brett
and
Glass
1973).

Why
is
swimming
speed
vital
to
adults
during
migration?

During
adult
migration,
swimming
speed
is
important
in
maintaining
progress
toward
holding
or
spawning
areas
upstream.
At
falls,
rapids,
or
fish
ladders,
adult
migratory
fish
must
often
be
able
to
swim
in
the
sustained
speed
range,
and
for
challenges
at
significant
falls
or
under
high
water
velocities,
instantaneous
burst
swimming
must
be
available.
The
swimming
velocity
needed
to
leap
a
falls
depends
on
the
height
of
the
falls;
the
higher
the
falls,
the
greater
the
speed
that
must
be
attained
when
thrusting
through
the
water
surface.

Water
temperature
and
oxygen
concentrations
are
significant
controls
on
swimming
speed.
However,
progress
upstream
also
depends
on
other
factors,
such
as
water
velocities
along
the
migratory
path
and
barriers
to
migration
(
e.
g.,
falls,
debris
jams,
or
dams).
In
moderate
water
velocities,
as
found
in
reservoirs,
migration
rates
of
chinook
can
match
or
exceed
those
in
freeflowing
reaches
(
Bjornn
1998c,
as
cited
by
NMFS
1999).
Very
high
flows
can
impede
migration.
Under
normal
river
flow
rates
the
tradeoffs
between
difficult
passage
at
dams
and
easier
swimming
in
reservoirs
make
it
difficult
to
estimate
the
net
effect
(
NPPC
1999).
It
is
possible
that
to
t
he
degree
that
adults
would
be
stressed
by
repeated
dam
passage
enroute
to
spawning
grounds.
Maintenance
of
migratory
ability
remains
dependent
on
proper
flow
direction
and
olfactory
cues
and
cool
temperatures
(
NPPC
1999).
If
water
temperature
is
high
and/
or
oxygen
concentrations
are
low,
swimming
speed
and
migration
rates
can
be
impaired;
fish
may
refuse
to
migrate,
migrate
back
downstream,
or
seek
shelter
in
tributaries
or
other
cold­
water
refuges
if
such
are
available
(
NMFS
1999,
draft
white
paper).
Under
these
conditions,
net
upstream
movement
may
be
reduced
or
extremely
delayed.
Holding
in
warmed
pools
can
result
in
spread
of
warm­
water
diseases.
68
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
Swimming
speeds
can
be
substantially
impaired
at
temperatures
above
the
swimming
optimum.
Fraser
River
sockeye
have
an
optimum
temperature
of
62.6
°
F
(
17
°
C)
for
swimming
endurance,
but
this
is
reduced
20%
at
69.8
°
F
(
21
°
C)
(
Macdonald
et
al.
in
press).
This
takes
on
ecological
significance
given
the
varying
temperatures
in
the
river.
At
Hell's
Gate
on
the
Fraser
River,
temperatures
were
>
64.4
°
F
(
18
°
C)
for
a
60­
d
period
during
summer;
upstream
temperatures
reached
a
maximum
of
>
71.6
°
F
(
22
°
C).
Zones
of
elevated
temperature
create
stressful
conditions
that
impair
swimming
capability
in
demanding
passage
conditions
(
Macdonald
et
al.
in
press).
The
tendency
for
some
sockeye
migrants
at
Hell's
Gate
to
become
hyperactive
and
exhibit
a
"
burst­
then­
sustained
speed"
pattern
under
high
flows
at
passage
const
rictions
would
make
them
even
more
susceptible
to
combined
effects
of
high
temperature
and
hypoxia
if
these
conditions
coincided
with
high
flows
(
Hinch
and
Bratty
2000).

Why
is
swimming
speed
vital
to
smolts
during
migration?

Smolts
migrating
downstream
have
different
problems
with
current
velocities
than
do
adults.
For
adults,
high
current
velocity
can
impede
upstream
migration,
but
with
moderate
temperatures
and
oxygen
concentrations,
their
upstream
movement
tends
to
be
easier
because
they
can
seek
conditions
in
which
sustained
or
prolonged
swimming
speed
exceeds
current
velocity,
thus
allowing
net
upstream
travel.
Smolts,
on
the
other
hand,
benefit
from
rapid
current
flow
because
their
downstream
progress
depends
on
water
velocity
rather
than
swimming
speed.
Downstream
migrants,
such
as
subyearling
fall
chinook,
are
capable
of
controlling
their
downstream
rate
of
travel
by
swimming
toward
shore,
where
they
feed
in
shallows.
If
marginal
areas
are
too
warm
and
if
the
warm
water,
fine
sediment
substrate
conditions,
and
slow
water
do
not
produce
abundant
macroinvertebrates
that
can
serve
as
prey
(
see
Coutant
1999),
growth
rates
and
survival
may
be
low.

With
downstream
smolt
migration,
swimming
speeds
must
not
be
impaired
because
swimming
is
vital
to
controlling
rate
of
descent
and
avoiding
obstacles.
Temperature
must
not
be
so
high
that
swimming
is
inhibited.
In
addition,
for
juveniles
(
including
smolts),
nonimpairment
of
swimming
capability
is
important
because
of
the
increased
vulnerability
to
predation
that
accompanies
the
effect
of
high
water
temperature
on
swimming
performance
(
Bams
1967,
Schreck
1990,
Kruzynski
and
Birtwell
1994,
all
as
cited
by
Marine
1997).
However,
some
reduction
in
swimming
capacity
is
expect
ed
during
smoltification
(
Smith
1982,
as
cited
by
Castleberry
et
al.
1991),
resulting
in
reduced
ability
to
maintain
position
in
current
and
the
tendency
to
be
swept
downstream
more
rapidly.

How
does
temperature
affect
juvenile
swimming
speed?

Brett
(
1958)
provided
a
useful
graph
of
the
relationship
between
cruising
speed
(
ft/
s)
and
acclimation
temperature
for
underyearling
sockeye
and
coho.
Sockeye
acclimated
to
59
°
F
(
15
°
C)
achieved
their
maximum
cruising
speed
(
approx.
1.12
ft/
s).
Coho
acclimated
to
68
°
F
(
20
°
C)
attained
their
maximum
cruising
speed
(
approx.
1.02
ft/
s).
Sockeye
swimming
speed
was
reduced
to
approximately
58%
of
maximum
as
water
temperature
was
increased
to
upper
incipient
lethal
levels.
Coho
swimming
speeds
were
reduced
to
approximately
91%
of
maximum
at
these
temperatures.
This
information
reveals
a
decline
in
performance
when
acclimation
temperature
increases
above
optimal
levels.
The
percentage
decline
in
swimming
performance
appeared
to
be
69
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
greater
in
sockeye
than
in
coho.
However,
upper
incipient
lethal
levels
would
no
t
permit
indefinite
swimming
because
lethal
effects
would
emerge.
In
addition,
sublethal
effects
such
as
energy
depletion
and
exhaustion
would
likely
occur.
Although
swimming
performances
of
adults
would
be
expected
to
follow
a
similar
pattern
(
i.
e.,
optimum
at
an
intermediate
temperature
with
decline
at
higher
and
lower
temperatures),
adults
are
much
more
sensitive
to
thermal
stress
than
are
juveniles
(
Becker
1973).

How
do
temperature
and
oxygen
jointly
affect
juvenile
swimming
speed?

Davis
et
al.
(
1963)
found
that
as
oxygen
concentrations
declined
below
9.0
mg/
L,
maximum
swimming
speed
of
coho
was
reduced.
Swimming
performance
increased
from
59
°
F
to
68
°
F
(
10­
20
°
C),
as
noted
in
the
previously
cited
studies
by
Brett
(
1958).
Dahlberg
et
al.
(
1968)
studied
coho
final
swimming
speed
at
68
°
F
(
20
°
C)
under
various
oxygen
concentrations
and
found
a
dramatic
reduction
in
swimming
speed
below
a
dissolved
concentration
of
7­
8
mg/
L.
With
a
DO
of
5
mg/
L
(
53%
saturation)
swimming
speed
was
reduced
10%
below
maximum.
Further
reductions
in
DO
caused
a
precipitous
reduction
in
final
speed
(
See
Temperature
Interactions
issue
paper
for
additional
detail
on
effects.)

How
are
physiological
optimum,
growth
optimum,
preferred
temperature,
swimming
maximum,
and
metabolic
scope
derived?

The
physiological
optimum
is
derived
by
averaging
the
growth
optimum
and
preferred
temperature
(
Brett
1971).
Preferred
temperature
also
is
correlated
with
the
temperature
providing
the
maximum
metabolic
scope.
This,
in
turn,
is
related
t
o
the
temperature
providing
the
maximum
critical
swimming
speed
(
Kelsch
and
Neill
1990).
Swimming
speed
is
highest
at
the
preferred
temperature
(
Kelsh
1996).

How
can
allocation
of
energy
to
metabolism
an
d
swimming
be
used
to
interpret
fitness
and
resistance
to
disease?

The
standard
metabolic
rate
(
SMR)
is
calculated
in
terms
of
oxygen
consumption
extrapolated
to
zero
activity
and
indicates
the
resting
metabolic
rate
of
unfed
fish
(
Priede
1985).
The
scope
for
activity
defines
the
performance
capacity
of
the
organism.
The
rate
of
oxygen
consumption
at
the
maximum
aerobic
swimming
rate
defines
the
active
metabolic
rate
(
Priede
1985,
Evans
1990),
which
is
that
found
for
a
fasted
fish
swimming
at
critical
speed
(
Beamish
1978,
Kelsh
and
Neill
1990).
The
specific
dynamic
action
(
SDA)
is
the
metabolic
rate
attributable
to
digestion
of
a
meal.
In
fish,
feeding
and
peak
digestion
tend
to
be
cyclic
and
are
correlated
with
water
temperature
and
photoperiod.
In
addition,
power
(
i.
e.,
the
short­
term
allocation
of
metabolic
resources,
see
Priede
1985)
devoted
to
SDA
is
related
to
the
size
and
quality
(
e.
g.,
protein
content)
of
the
meal
consumed.
Therefore,
the
power
demand
for
SDA
varies
and
consumes
variable
portions
of
the
available
energy
defined
by
the
scope
for
activity.
In
ecological
terms,
the
greater
the
available
power
at
any
given
temperature
in
excess
of
the
basic
demands
of
SMR
and
SDA,
the
greater
the
fitness
(
Evans
1990).
Fish
operating
under
a
temperature
that
allows
only
a
small
power
output
in
excess
of
SMR
and
SDA
needs
have
little
ability
to
deal
with
additional
power
demands
caused
by
disease,
the
need
to
apply
burst
swimming
to
escape
predators
or
swim
against
currents,
and
so
on.
The
seriousness
of
this
situation
is
reflected
in
the
70
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
danger
of
feeding
cultured
fish
at
high
temperatures,
despite
the
fact
that
more
energy
is
required.
With
the
heightened
power
demand
for
SDA
at
high
temperatures,
any
unnecessary
stress
can
lead
to
metabolic
power
overload
and
mortality
(
Priede
1985).

In
addition
to
the
correlation
between
the
maximum
scope
for
activity
and
preferred
temperatures,
median
survival
has
ot
her
ecological
importance.
Survival
of
an
individual
fish
is
probably
maximized
by
temperatures
in
the
mid­
range
of
its
scope
for
activity.
The
temperature
range
that
maximizes
scope
for
activity
tends
to
be
correlated
with
t
he
center
of
distribution
of
the
species
and
maximum
production.
The
ability
of
the
organism
to
adapt
to
its
thermal
environment
is
related
to
its
ability
to
maximize
available
power
(
Evans
1990).

How
do
temperature,
light
intensity,
and
photoperiod
influence
swimming
speed?

A
plot
of
prolonged
swimming
performances
for
a
variety
of
species
relative
to
temperature,
as
summarized
by
Beamish
(
1978),
indicates
that
sockeye
attain
maximum
speed
at
59
°
F
(
15
°
C),
whereas
coho
and
lake
trout
reach
maximum
prolonged
swimming
speeds
at
approximately
62.6­
64.4
°
F
(
17­
18
°
C).

Diel
changes
in
swimming
speed
by
factors
of
approximately
2­
3
have
been
observed
in
sockeye
in
coastal
waters
(
Madison
et
al.
1972)
and
chinook
in
the
Columbia
River
(
Johnson
1960);
speeds
were
lower
at
night
than
during
the
day.
Quinn
(
1988
as
cited
by
Quinn
et
al.
1997)
also
reported
t
hat
sockeye
swimming
speeds
were
lower
in
coastal
waters
at
night.
Light
intensity
or
photoperiod
apparently
provides
a
behavioral
regulation
of
swimming
speed.
However,
Hatch
et
al.
(
1993),
using
video
time­
lapse
recording,
det
ect
ed
significant
adult
sockeye
movement
past
Zosel
Dam
on
the
Okanogan
River
between
2000
and
0600
h.
In
fact,
most
passage
occurred
during
nighttime.
Such
was
not
the
case
at
Tumwater
Dam
on
the
Wenatchee
River,
where
daytime
passage
was
predominant.
Sockeye
on
the
Okanogan
can
apparently
take
advantage
of
nighttime
passage.
Provided
that
nighttime
water
temperature
is
lower
than
daytime
temperature,
sockeye
might
escape
significant
thermal
stress.
High
net
migration
rates
(
up
to
3.4
km/
h)
were
observed
in
these
sockeye
populations
(
Quinn
et
al.
1997),
which
could
either
decrease
exposure
time
to
thermal
stress
or
produce
dangerous
levels
of
fatigue
under
warm
river
conditions.

How
do
fish
size
and
acclimation
temperature
affect
swimming?

Small­
size
sockeye
held
a
swimming
advantage
relative
to
larger
size
sockeye
over
the
length
range
8­
60
cm
(
Brett
and
Glass
1973).
That
is,
critical
swimming
speed
(
60­
min
sustained
speed)
was
6.7
body
lengths/
s
at
the
smallest
size
and
decreased
to
2.1
body
lengths/
s
at
the
maximum
size
when
measured
at
68
°
F
(
20
°
C).

Swimming
performance
also
depends
on
prior
acclimation
temperature
in
relation
to
exposure
temperature.
This
effect
can
be
measured
in
acute
temperature
exposure
tests.
Griffiths
and
Alderdice
(
1972)
found
that
for
juvenile
coho
over
a
temperature
range
of
approximately
35.6­
77
°
F
(
2­
25
°
C),
a
low
acclimation
temperature
of
35.6
°
F
(
2
°
C)
produced
maximum
critical
speed
(
5
lengths/
s)
at
a
test
temperature
of
57.2
°
F
(
14
°
C).
As
acclimation
temperature
was
increased,
so
did
the
test
temperature
producing
the
maximum
critical
speed.
At
an
acclimation
71
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
temperature
of
68
°
F
(
20
°
C),
a
test
temperature
of
68
°
F
(
20
°
C)
produced
a
critical
speed
of
6.0
lengths/
s.
Critical
swimming
speed
declined
dramatically
as
test
temperature
was
increased
above
68
°
F
(
20
°
C).
An
acclimation
and
test
temperature
of
68
°
F
(
20
°
C)
provided
the
highest
critical
swimming
performance
(
Griffiths
and
Alderdice
1972).
For
juvenile
coho
salmon
a
temperature
of
68
°
F
(
20
°
C)
appeared
to
provide
maximum
metabolic
scope
and
swimming
speed,
given
unlimited
food.

Can
disease
affect
swimming
speed?

Tests
of
critical
swimming
performance
on
Fraser
River
adult
sockeye
at
66.2­
69.8
°
F
(
19­
21
°
C)
indicated
that
diseases,
including
fungal
infections,
reduced
swimming
speed
35%
from
control
conditions
(
Jain
et
al.
1998,
as
cited
by
Macdonald
et
al.
in
press).

What
is
known
about
swimming
speed
for
three
species
of
char?

Beamish
(
1980)
measured
critical
swimming
speed
for
three
species
of
char:
arctic
char,
Salvelinus
alpinus;
brook
trout,
S.
fontinalis;
and
lake
char,
S.
namaycush,
at
41,
50,
and
59
°
F
(
5,
10,
and
15
°
C).
Median
critical
swimming
speed
for
each
species
increased
with
temperature
over
the
range
of
41
to
59
°
F
(
5­
15
°
C).
Swimming
performance
and
oxygen
uptake
decreased
as
temperatures
exceeded
59
°
F
(
15
°
C).

Can
swimming
act
as
an
indicator
of
sublethal
stress?

Swimming
performances
have
been
suggested
for
assessing
sublethal
effects
of
water
quality
(
temperature
and
other
combined
pollutants)
on
fish
(
Brett
1967,
as
cited
by
Beamish
1978).
Upstream
migration
requires
a
combination
of
all
three
modes
of
swimming
(
sustained,
prolonged,
and
burst).
Swimming
to
exhaustion
in
coho
requires
up
to
18­
24
h
for
complete
recovery
(
Paulik
et
al.
1957).
After
3
h
of
rest,
recovery
is
only
67%
complete.
Exhaustion
may
be
produced
by
repeated
attempts
to
negotiate
falls
or
fish
ladders,
escape
predators,
or
struggle
against
the
line
of
a
sport
angler.
But
lower
energy
reserves,
decreased
scope
for
activity,
or
unacceptable
delays
in
reaching
holding
or
spawning
areas
because
of
need
for
metabolic
recovery
mean
that
the
cumulative
effect
of
swimming
stress
may
result
in
prespawning
mortality
or
reduced
reproductive
success.

How
are
adult
swimming
speeds
and
migration
rate
related?

Brett
(
1965
as
cited
by
Brett
1983)
plotted
the
swimming
efficiency
of
2.3­
kg
sockeye
as
the
energy
cost
(
kcal/
kg/
km)
vs.
swimming
speed
(
km/
h).
Low
speeds
(<
1
km/
h)
required
too
much
energy
expenditure
because
of
the
large
metabolism
requirement
in
a
prolonged
migration
period.
Intermediate
speeds
(
1.0­
2.6
km/
h)
had
the
least
energy
expenditure.
Optimum
efficiency
was
achieved
at
1.8
km/
h.
Interestingly,
the
mean
current
velocity
of
the
Columbia
River
is
7
km/
h,
whereas
maximum
sustainable
swimming
speed
is
5
km/
h.
The
energy
expendit
ure
observed
in
sockeye
was
equated
to
a
swimming
speed
of
4.3
km/
h
by
Brett
(
1965
as
cited
by
Brett
1983).
This
implies
that
sockeye
must
be
able
to
t
ravel
largely
in
low­
velocity
currents
to
conserve
energy.
Fastest
migrat
ion
speeds,
determined
by
radio
tracking
in
mid­
run
spring
chinnok
in
the
Willamette
River
(
late
May­
early
June)
were
1.8
km/
h,
although
most
of
the
migration
occurred
at
72
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
speeds
of
1.3­
1.7
km/
h
at
55.4­
66.2
°
F
(
13­
19
°
C)
(
Schreck
et
al.
1994).
Further
investigation
of
energy
and
swimming
speeds
is
needed
because
the
total
distances
traveled
are
uncert
ain.
Adult
salmonid
migration
can
involve
considerable
downstream
and
upstream
exploration
for
a
given
net
distance
traveled
upstream
(
Schreck
et
al.
1994).
If
frequent
fall­
back
through
dams
occurs,
total
travel
distances
and
energy
expendit
ure
could
become
great,
placing
t
he
individuals
in
considerable
bioenergetic
stress.

Recent
studies
using
EMG
radiotelemetry
on
volitionally
swimming
adult
sockeye
in
the
Fraser
and
Nechako
Rivers
in
British
Columbia
revealed
the
average
swim
and
migration
speeds
in
different
river
reaches
that
presented
various
migration
challenges
attributable
to
channel
constriction.
Average
swim
speeds
in
these
reaches
varied
from
1.8
to
4.5
km/
h.
Migration
speeds
in
these
same
reaches
ranged
from
0.2
to
2.2
km/
h
(
Hinch
and
Rand
1998).
Swim
speeds
were
much
more
constant
than
migration
speeds,
indicating
that
sockeye
have
a
preferred
or
optimum
swim
speed
(
Hinch
and
Rand
1998).
However,
application
of
EMG
telemetry
at
Hell's
Gate,
a
major
constriction
in
the
Fraser
River,
showed
that
adult
sockeye
that
were
unsuccessful
at
passing
this
impediment
swam
for
prolonged
periods
at
speeds
exceeding
critical
velocity,
depleted
energy
reserves,
and
required
prolonged
recovery
periods
(
Hinch
and
Bratty
2000).
Although
complex
flow
conditions
associated
with
channel
constrictions
and
fish
ladders
can
lead
to
fatigue
in
unsuccessful
upstream
migrants,
low
oxygen
concentration
and
high
temperature
can
reduce
the
success
rate
even
further
(
Hinch
and
Bratty
2000).
By
modeling
bioenergetics
of
sockeye
swimming
up
the
Fraser
River
and
accounting
for
the
temperature
variations
as
experienced
over
a
44­
year
period
in
which
maximum
temperatures
of
69.8
°
F
(
21
°
C)
occurred
periodically,
it
was
determined
that
8%
of
the
sockeye
run
over
this
time
period
was
subject
to
energy
depletion
and
prespawning
mortality
(
Rand
and
Hinch
1998).
Because
as
much
as
20%
of
initial
energy
must
be
conserved
to
complete
spawning,
factors
that
contribute
to
energy
depletion
(
high
temperature,
high
velocity
flows,
passage
barriers
and
constrictions,
confusing
flow
patterns)
need
to
be
reduced.

Adult
Migration
to
R
eproduction
What
temperatures
are
associated
with
migration?

Migration
is
generally
considered
to
occur
or
be
feasible
to
some
extent
for
summer
and
fall
chinook
at
57­
68
°
F
(
13.9­
20.0
°
C)
and
51­
66.9
°
F
(
10.6­
19.4
°
C),
respectively
(
Bell
1991).
However,
a
migration
threshold
at
a
temperature
of
69.8­
71.6
°
F
(
21­
22
°
C)
is
documented
by
numerous
studies
across
major
migratory
salmonid
species
in
the
Columbia
River
(
Table
3).

Summer
water
temperatures
in
many
streams
of
the
Pacific
Northwest
can
be
high
enough
to
cause
migration
difficulties.
The
Snake
River
provides
an
example.
In
each
of
the
Snake
River
reservoirs
there
is
an
approximately
2­
month
period
during
which
water
temperatures
exceed
69.8
°
F
(
21
°
C)
(
Dauble
and
Mueller
1993,
p.
39).
At
Lower
Granite
reservoir
this
period
extends
from
mid­
July
to
mid­
September.
This
period
in
which
water
temperature
exceeds
adult
migration
thresholds
overlaps
the
adult
migration
periods
of
summer
chinook,
fall
chinook,
sockeye,
and
summer
steelhead
(
Dauble
and
Mueller
1993,
Fish
Passage
Center
data
sheet)
(
also
see
Table
7)
and
the
smolt
outmigration
of
fall
chinook
and
sockeye
at
Lower
Granite
Dam
(
Fish
Passage
Center
1998).
Even
spring
chinook
migration
to
spawning
grounds
can
be
inhibited
for
73
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
continuous
periods
of
more
than
2
months
by
temperatures
in
major
tributaries
of
the
Snake
(
i.
e.,
Tucannon
River)
(
Bumgarner
et
al.
1997).
Chinook,
sockeye,
and
steelhead
of
the
Snake
River
Table
7.
Adult
migration
period
for
chinook
and
steelhead
Reservoir
Spring
chinook
Summer
chinook
Fall
chinook
Steelhead
Ice
Harbor
4/
1­
6/
8
6/
12­
8/
11
8/
12­
10/
31
4/
1­
10/
31
Lower
Monumental
4/
1­
6/
13
6/
14­
8/
13
8/
14­
10/
31
4/
1­
10/
31
Little
Goose
4/
14­
6/
15
6/
16­
8/
15
8/
16­
11/
15
4/
1­
10/
31
Lower
Granite
3/
1­
6/
17
6/
18­
8/
17
8/
18­
12/
15
4/
1­
10/
31
Note:
Adult
sockeye
passage
at
Lower
Granite
Dam
extends
from
June
15
to
August
20
(
Dauble
and
Mueller
1993).
Steelhead
migration
includes
the
group
A
run
from
April
1
to
August
25
and
the
B
run
from
August
26
to
October
31.

are
all
listed
under
the
ESA
as
either
t
hreatened
or
endangered,
migrate
during
periods
affected
by
warm
water,
and
require
consideration
for
their
migration
success
and
survival.

Fall
chinook
hist
orically
entered
the
Snake
River
from
late
August
through
November
with
a
peak
in
September
(
Snake
River
Subbasin
Plan
1990).
At
Ice
Harbor
Reservoir
during
1990,
water
temperatures
were
73.4
°
F
(
23
°
C)
on
August
15
(
i.
e.,
the
initiation
of
the
migration
period)
but
declined
to
only
71.6
°
F
(
22
°
C)
by
September
16
(
Karr
et
al.
1992).
As
an
example
of
the
problem
posed
for
fall
chinook
migration,
1990
water
temperatures
in
Lower
Granite
Reservoir
peaked
on
approximately
August
13
at
77
°
F
(
25
°
C)
and
gradually
declined
to
about
69.8
°
F
(
21
°
C)
by
September
16
(
Karr
et
al.
1992).
Temperature
histories
for
Snake
reservoirs
such
as
these
indicate
that
migration
blockages
of
4
wk
can
occur.
Since
September
1990,
attempts
have
been
made
to
reduce
Snake
River
reservoir
temperatures
by
releasing
water
from
Dworshak
Dam.
Releases
of
co
ld
water
of
up
to
14
kcfs
have
been
made
to
improve
fish
migration
and
survival.

Periodic
inability
to
migrate
because
of
high
water
temperatures
was
almost
certainly
one
of
a
number
of
environmental
challenges
presented
to
salmon
under
historic
conditions.
However,
unimpounded
rivers
have
thermal
regimes
that
are
different
from
those
of
impounded
rivers.
Even
if
a
free­
flowing
river
experienced
a
maximum
daily
temperature
that
impeded
upstream
migration,
it
would
no
t
have
continuous
temperatures
beyond
the
migration
threshold,
nor
would
they
be
present
for
many
consecutive
days.
A
healthy
stream
system
would
provide
abundant
cold­
water
refuges
along
the
entire
migration
route.
Large
reservoirs
on
mainstem
rivers,
channel
alterations
(
loss
of
pools
via
removal
of
large
woody
debris
or
sedimentation,
channelization),
and
altered
cold­
water
input
sources
(
e.
g.,
wetland
loss,
interception
of
shallow
groundwater
flow
by
the
road
system)
lengthen
exposure
to
temperatures
that
could
block
migration,
shift
maximum
temperatures
to
later
in
the
year,
eliminate
cold­
water
refuges,
result
in
more
constant
daily
temperatures,
and
heat
river
margin
habitats
(
Coutant
1999).
These
habitats
would
be
best
for
74
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
juvenile
rearing
(
especially
fall
chinook
migrating
slowly
to
the
ocean),
if
not
for
the
high
temperatures
present
during
summer
and
early
autumn
months.

If
adults
or
smolts
were
able
to
seek
colder
water
at
depth,
they
could
avoid
the
migration
barriers.
However,
there
is
very
little
temperature
stratification
in
t
he
reservoirs
(
Bennett
et
al.
1997,
Karr
et
al.
1998).
Adult
salmon
in
the
vicinity
of
the
Snake
River
mouth
are
known
to
hold
in
the
much
cooler
Columbia
River
to
avoid
adverse
temperatures.
However,
they
have
a
limited
opportunity
to
then
migrate
through
the
Snake
River,
find
a
mate,
and
spawn.
This
window
is
predetermined
by
their
stored
body
energy,
their
maturation
during
holding,
and
their
need
to
deposit
eggs
in
sufficient
time
for
development
and
emergence.
Although
salmon
have
some
inherent
flexibility
in
their
life
cycle,
this
can
easily
be
overwhelmed
by
stresses
imposed
in
river
management.
In
addition,
salmon's
range
of
tolerance
to
high
temperatures
in
their
environment
can
easily
be
exceeded,
lowering
their
survival.

The
year
1998
set
record
high
temperatures
throughout
the
Fraser
River
Watershed
in
British
Columbia,
Canada.
It
also
set
records
for
high
losses
to
the
river's
sockeye
salmon
run.
Macdonald
et
al.
(
in
press)
evaluated
the
effects
of
temperature,
flows,
disease,
and
other
stressors
to
determine
the
likely
cause
of
the
estimated
in­
river
loss
of
3,394,000
adult
fish
and
increased
prespawning
mortality
in
some
early­
run
stocks.
Temperature
was
the
main
cause
of
both
en
route
and
prespawning
losses
to
the
1998
Fraser
River
sockeye
runs.
Mean
daily
water
temperatures
at
Hell's
Gate
(
a
lower
mainstem
site)
were
the
highest
recorded
for
most
days
during
the
summer
of
1998,
frequently
exceeding
68
°
F
(
20
°
C)
in
late
July
and
early
August
(
warmest
mean
summer
temperatures
in
the
51
years
of
record).
From
their
review
of
the
historical
database,
the
authors
suspected
that
losses
in
spawning
runs
occur
when
mean
river
temperatures
exceed
62.6­
64.4
°
F
(
17­
18
°
C)
for
prolonged
periods.
They
noted
that
chinook
salmon
also
appear
susceptible
to
high
temperatures
in
the
Fraser
River
system.
In
1998
unusually
large
losses
(
25%
of
population)
occurred
in
the
South
Thompson
River,
where
summer
mean
temperatures
were
frequently
above
68
°
F
(
20
°
C)
and
reached
a
high
of
approximately
73.4
°
F
(
23
°
C).
The
only
other
year
with
reports
of
large
chinook
losses
was
1994,
also
an
unusually
warm
year.

Migration
stress
and
reproductive
impairment
in
salmon
populations
may
result
from
the
cumulative
effects
of
exposure
to
less
than
optimum
environmental
conditions.
Macdonald
et
al.
(
in
press)
suggested
that
migration
blockages,
susceptibility
to
disease,
impaired
maturation,
increases
to
stress
parameters,
reduced
efficiency
of
energy
use,
and
reduced
swimming
performance
are
all
more
common
as
daily
mean
temperatures
exceed
62.6
°
F
(
17
°
C).
The
authors
found
that
measuring
physiological
indicators
of
stress
and
reproductive
condition
is
useful
in
evaluating
the
effects
of
temperature
on
migratory
sockeye
salmon.

How
can
stress
during
migration
affect
later
reproductive
success
in
salmonids?

Macdonald
et
al.
(
in
press)
monitored
stress
and
reproductive
state
in
both
prespawning
and
postspawning
sockeye
from
the
Horsefly
River
stock
(
midsummer
run).
The
Horsefly
River
stock
entered
the
Fraser
River
during
the
warmest
period
of
the
year.
During
migration
to
the
spawning
grounds,
temperatures
were
well
over
68
°
F
(
20
°
C).
Four
stress
parameters
and
three
reproductive
parameters
were
examined.
In
addition,
some
of
the
fish
collected
were
art
ificially
75
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
spawned
and
their
eggs
placed
in
capsules
in
the
gravel
of
their
natal
stream
and
examined
to
determine
both
fertilization
and
hatching
success.

In
1998,
Horsefly
sockeye
(
midrun
stock)
females
had
plasma
cortisol
levels
(
a
primary
indicator
of
stress)
that
reflected
exposure
to
acute
stress
and
that
were
generally
higher
than
those
in
other
migrating
Fraser
River
sockeye
stocks
in
previous
years.
The
levels
of
lactate
(
a
secondary
indicator
of
stress)
in
Horsefly
salmon
at
all
reproductive
stages
examined
showed
that
these
fish
had
engaged
in
stressful
exercise
even
though
the
flow
rates
in
1998
were
substantially
lower
than
in
1997,
when
water
flows
created
very
challenging
migration
conditions.
There
were
several
indications
that
the
early
portion
of
the
1998
Horsefly
run
was
suffering
from
impaired
maturation.
Many
of
the
females,
particularly
those
in
poor
co
ndition,
had
low
estradiol
and
progesterone
levels,
possibly
from
high­
temperature
stress
that
caused
suppression
of
estrogen
synthesis
and
an
inability
to
switch
to
the
synt
hesis
of
17,20P
(
an
indicator
of
final
maturat
ion
in
males
and
females).
These
processes
are
known
to
be
linked.
Testosterone
(
an
indicator
of
maturation
in
males
and
females)
also
was
depressed
in
females
in
poor
condition,
further
evidence
that
these
fish
would
probably
not
reach
maturity
or
spawn
viable
eggs.
Elevated
but
sublethal
temperatures
are
known
to
negatively
affect
secretion
of
the
hormones
cont
rolling
sexual
maturation
in
sockeye
salmon
in
the
Fraser
River.
The
likely
physiological
consequences
of
these
reduced
hormone
levels
are
poor
spawning
success,
poor
egg
quality
and
viability,
and
senescent
death
prior
to
spawning.
All
three
of
these
reproductive
impairment
problems
were
evident
in
1998
in
each
of
the
stock
groups.

What
temperatures
are
recommended
for
holding?

Hatchery
managers
have
long
known
that
highest
survival
of
chinook
adults
occurs
when
water
temperatures
do
not
exceed
57.2
°
F
(
14
°
C)
(
Leitritz
and
Lewis
1976,
Piper
et
al.
1982).
Fish
(
1944)
reported
very
high
holding
survival
of
sockeye
when
temperatures
were
<
60
°
F
(
15.6
°
C),
but
survival
was
only
51%
under
a
fluctuating
regime
of
48.9­
73.9
°
F
(
9.4­
23.3
°
C).

Can
temperature
affect
viability
of
gametes
developing
in
adults?

Temperature
can
influence
the
reproductive
success
of
fish
well
before
spawning.
Prespawning
effects
can
be
separated
into
at
least
two
time
periods:
before
ovulation
and
after
ovulation.
Before
o
vulat
ion,
reproductive
success
can
be
hampered
by
mortality
t
o
the
adult
spawner
(
Andrew
and
Geen
1960,
Bouck
et
al.
1975,
Schreck
et
al.
1994,
Cooper
and
Henry
1962,
as
cited
in
Gilhousen
1980)
and
interference
with
ovulation
and
spermatogenesis.
After
ovulation,
reproductive
success
can
be
harmed
through
decreased
egg
and
sperm
fitness
and
reduced
embryonic
survival
rates.
Here
we
discuss
only
the
impact
of
temperature
on
ovulation
and
subsequent
egg
survival.

Hatchery
managers
have
long
known
that
highest
survival
of
chinook
adults
occurs
at
water
temperatures
less
than
57.2
°
F
(
14
°
C)
(
Leitritz
and
Lewis
1976,
Piper
et
al.
1982).
When
adults
hold
in
higher
water
temperatures,
egg
survival
increasingly
declines
(
Hinze
1959,
Hinze
et
al.
1956,
as
cited
by
Marine
1992).

After
ovulation
in
females
and
sperm
maturation
in
males,
the
effect
of
elevated
water
76
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
temperature
on
rainbow
trout
egg
and
sperm
viability
becomes
important
(
Billard
1985).
Holding
females
at
68
°
F
(
20
°
C)
for
70
h
reduced
viability
of
eggs
held
in
the
body
cavity,
compared
with
holding
females
at
50
°
F
(
10
°
C)
(
Billard
and
Breton
1977,
as
cited
by
Billard
1985).
To
promote
female
maturation
and
egg
development,
holding
at
temperatures
from
42
to
55.9
°
F
(
5.6­
13.3
°
C)
is
essential
(
Leitritz
and
Lewis
1976).

Smith
et
al.
(
1983)
and
Piper
et
al.
(
1982)
cited
work
demonstrating
that
rainbow
trout
adult
broodfish
should
be
held
at
temperatures
below
53.9­
55.9
°
F
(
12.2­
13.3
°
C)
before
spawning
to
produce
good­
quality
eggs,
whereas
holding
temperatures
above
55.4
°
F
(
13
°
C)
have
been
found
to
reduce
in
vivo
posto
vulat
ory
egg
survival
(
Flett
et
al.
1996,
Billard
and
Gillet
1981,
as
cited
in
Billard
1985).
Temperatures
of
64.4
°
F
(
18
°
C)
or
higher
were
found
to
reduce
the
volume
of
male
sperm,
and
a
temperature
of
68
°
F
(
20
°
C)
was
found
to
cause
a
drop
in
egg
fertility
in
vivo
to
5%
after
4.5
d
(
Billard
and
Breton
1977).
At
50
°
F
(
10
°
C),
fertility
of
the
eggs
held
in
the
hen
trout
remained
high.
Saki
et
al.
(
1975,
as
cited
in
de
Gaudemar
and
Beal
1998)
found
that
embryonic
and
posthatching
survival
in
O.
mykiss
decreased
significantly
if
eggs
remained
ripe
in
the
body
cavity
for
more
than
5­
7
d
after
ovulation,
and
fertility
could
approach
zero
after
2
wk
(
Stein
and
Hochs
1979,
as
cited
in
de
Gaudemar
and
Beal
1998).

When
ripe
adult
chinook
females
were
exposed
to
temperatures
beyond
the
range
55.9­
60
°
F
(
13.3­
15.6
°
C),
prespawning
adult
mortality
became
pronounced
and
survival
of
eggs
to
the
eyed
stage
decreased.
Prespawning
adults
exposed
to
prolonged
temperatures
of
60­
62
°
F
(
15.6­
16.7
°
C)
had
survival
of
eggs
t
o
the
eyed
stage
of
70%
when
incubated
at
54.8­
55.9
°
F
(
12.7­
13.3
°
C)
and
survival
of
50%
when
incubated
at
60­
62
°
F
(
15.6­
16.7
°
C).
Adults
exposed
to
55­
59
°
F
(
2.8­
15
°
C)
water
temperature
had
egg
survival
of
80%
to
the
eyed
stage
when
then
incubated
at
the
same
temperatures
(
Hinze
1959,
as
cited
by
CDWR
1988).
The
highest
survival
of
eggs
(
95%)
to
the
eyed
stage
was
in
those
taken
from
adults
held
at
53­
53.9
°
F
(
11.7­
12.2
°
C)
(
Hinze
et
al.
1956
as
cited
by
CDWR
1988).
Eggs
t
aken
from
chinook
held
at
co
nstant
temperatures
>
55.4­
59
°
F
(
13­
15
°
C)
have
poor
viability
(
Hinze
et
al.
1956,
as
cited
by
Marine
1992,
Rice
1960,
Leitritz
and
Lewis
1976).

Berman
(
1990)
held
adults
at
63.5­
66.2
°
F
(
17.5­
19
°
C)
for
a
2­
wk
period
before
spawning.
Control
fish
were
held
at
57.2­
59.9
°
F
(
14­
15.5
°
C).
Progeny
of
the
elevated
treatment
group
had
higher
prehatch
mortality
and
a
much
greater
rate
of
developmental
abnormalities
than
the
control
group.
In
addition,
alevin
weight
and
length
were
less
in
the
elevated
group.
The
smaller
alevin
size
could
be
attributable
to
the
smaller
size
of
eggs
in
the
elevated
group.
It
is
interesting
that
even
though
no
differences
were
observed
in
fertilization
rates
of
eggs
between
the
elevated
and
control
groups,
numerous
delayed
effects
occurred.

Two
coho
stocks
migrating
to
spawning
grounds
in
eastern
Lake
Erie
had
very
different
survival
of
embryos
to
hatch,
attributable
to
the
water
temperatures
on
the
migration
route.
The
stock
that
migrated
in
waters
>
59
°
F
(
20
°
C)
in
mid­
August
to
early
September
had
deformed
eggs
with
mean
survival
rates
to
hatching
of
low
to
0%,
depending
on
the
year.
The
neighboring
stock
had
very
little
warm
shoal
water
to
traverse
during
migration,
were
exposed
to
temperatures
3.6­
7.2
°
F
(
2­
4
°
C)
lower,
and
had
normal
eggs
with
high
viability
(
84%
embryo
survival)
(
Flett
et
al.
1996).
77
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
Hokanson
et
al.
(
1973)
measured
a
significant
effect
of
prespawning
temperature
exposure
on
brook
trout
broodstock.
When
brook
trout
were
spawned
at
50.7
°
F
(
10.4
°
C)
or
at
55.7
°
F
(
13.2
°
C)
and
subsequently
reared
at
50
°
F
(
10
°
C),
percentage
of
normal
hatching
was
65%
and
38%,
respectively.
When
brook
trout
were
spawned
at
50.7
°
F
(
10.4
°
C)
or
55.7
°
F
(
13.2
°
C)
and
subsequently
reared
at
60.8
°
F
(
16
°
C),
percentage
of
normal
hatching
was
0%
in
each
case.
Percentage
of
normal
hatching
was
>
90%
at
constant
incubation
temperatures
of
40.8­
46.4
°
F
(
6­
8
°
C)
and
declined
steadily
to
0%
at
60.8
°
F
(
16
°
C).
The
highest
percentage
of
viable
eggs
per
female
was
found
at
46.4
°
F
(
8
°
C).
An
increase
in
spawning
temperature
from
50
to
60.8
°
F
(
10­
16
°
C)
resulted
in
a
steady
decline
to
near
zero
in
spawnings
per
female,
viable
eggs
per
female,
and
total
eggs
per
female.
The
temperature
range
42.8­
60.8
°
F
(
6­
16
°
C)
may
represent
the
right
portion
of
a
bell­
shaped
survival
curve.
This
study
provides
import
ant
evidence
that
adult
holding
water
temperatures
and
temperature
at
fert
ilization
are
as
important
as
incubat
ion
temperature
in
determining
egg
viability.
In
female
brook
trout
the
maximum
temperature
for
maturation
and
ovulation
is
60.8­
66.2
°
F
(
16­
19
°
C).
Males
can
achieve
functional
maturity
at
temperatures
as
high
as
62.2
°
F
(
19
°
C).
However,
at
66.2
°
F
(
19
°
C)
development
of
ova
becomes
inhibited
and
ova
can
be
resorbed.
Hokanson
et
al.
recommended
that
for
brook
trout
in
the
month
prior
to
spawning,
maximum
water
temperature
should
be
<
66.2
°
F
(
19
°
C)
and
mean
temperature
should
be
<
60.8
°
F
(
16
°
C).
During
the
breeding
season
maximum
water
temperature
should
be
<
53.6
°
F
(
12
°
C).
Optimal
spawning
activity,
gamete
viability,
and
embryo
survival
would
take
place
at
mean
spawning
temperatures
<
48.2
°
F
(
9
°
C).

Egg
survival
during
egg
development
has
also
been
studied
in
rainbow
trout.
Postovulation
survival
of
eggs
in
the
body
cavity
of
rainbow
trout
females
held
at
>
55.4
°
F
(
13
°
C)
was
much
lower
than
at
lower
holding
temperatures
(
Billard
and
Gillet
1981,
as
cited
by
Billard
1985).

Forced
delays
in
spawning,
such
as
are
frequently
caused
by
difficulties
in
passing
dams,
can
cause
decreases
in
reproductive
success.
In
Atlantic
salmon
a
delay
in
spawning
from
any
source
causes
overripening
in
females.
Prolonged
holding
of
eggs
after
ovulation
reduces
egg
viability
and
increases
retention
and
malformation.
As
little
as
a
1­
wk
delay
in
spawning
after
full
maturation
causes
a
marked
reduction
in
egg
quality
(
de
Gaudemar
and
Beall
1998).

In
addition
to
the
effects
on
egg
viability
caused
by
holding
adult
female
salmon
at
elevated
water
temperature
(>
59­
60.8
°
F
[
15­
16
°
C]),
warm
water
can
also
lower
viability
of
eggs
of
nonanadromous
salmonid
adults
by
influencing
their
nutrition
during
their
feeding
period
(
see
Hokanson
1977).
A
lowered
food
intake
leading
up
to
egg
deposition,
when
growth
is
normally
rapid,
may
accompany
elevated
water
temperature.
Poor
growing
conditions
for
salmonids
that
achieve
maturit
y
in
freshwater
can
result
in
poor
reproductive
success
(
Coutant
1977).
A
rapid
decline
in
quality
of
rainbow
trout
eggs
within
the
body
cavity
after
ovulation
has
been
reported
at
holding
temperatures
of
55.4­
59
°
F
(
13­
15
°
C)
by
numerous
authors
(
see
citations
in
Flett
et
al.
1996,
Billard
1985,
Smith
et
al.
1983).
Cutthroat
females
held
at
temperatures
fluctuating
from
35.6
to
50
°
F
(
2­
10
°
C)
produced
eggs
of
significantly
higher
quality
than
females
held
at
50
°
F
(
10
°
C)
(
Smith
et
al.
1983).

Bouck
et
al.
(
1975)
studied
survival
of
sockeye
acclimated
to
55.4
°
F
(
13
°
C)
and
adjusted
to
test
temperatures
at
a
rate
of
3.6
°
F
(
2
°
C)/
d.
Adults
holding
at
a
t
est
temperature
of
71.6
°
F
(
22
°
C)
died
after
3.2
d
from
thermal
effects.
Holding
for
11.7
d
at
68
°
F
(
20
°
C)
resulted
in
100%
78
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
mortality
from
indirect
thermal
effects
(
infection
by
columnaris).
Fish
held
at
61.7
°
F
(
16.5
°
C)
had
lower
health
and
reproductive
indices
than
fish
held
at
50
°
F
(
10
°
C).
Among
these
indices
were
the
absence
of
fat
reserves
at
61.7
°
F
(
16.5
°
C)
vs.
abundant
reserves
at
50
°
F
(
10
°
C),
the
doubling
of
weight
loss,
enlarged
liver,
and
reduced
egg
size
at
the
higher
temperature.
The
noninfectious
pathology
at
61.7
°
F
(
16.5
°
C)
occurs
precisely
during
the
major
period
of
reproductive
development
in
the
Columbia
River.
For
these
reasons,
Bouck
et
al.
concluded
that
50
°
F
(
10
°
C)
was
more
favorable
for
maturing
sockeye
than
61.7
°
F
(
16.5
°
C),
and
in
addition,
did
not
subject
these
fish
to
the
greater
risk
of
thermal
death
and
disease
associated
with
60.8
and
68
°
F
(
16
and
20
°
C)
holding.

Water
temperatures
can
speed
up,
slow
down,
or
st
op
entirely
the
ripening
of
gonads
and
ovulation
in
fish
(
Flett
et
al.
1996,
Gilhousen
1990,
Gillet
1991
as
cited
in
Baroudy
and
Elliott
1994,
and
Reingold
1968
as
cited
in
Bailey
and
Evans
1971).
Billard
and
Breton
(
1977)
found
that
temperatures
as
high
as
64.4
°
F
(
18
°
C)
had
no
adverse
effect
on
male
rainbow
trout
spermatogenesis,
but
sperm
volume
and
gonadotrope
secretion
were
both
higher
at
50
°
F
(
10
°
C)
than
at
64.4
°
F
(
18
°
C).
At
temperatures
above
55.4
°
F
(
13
°
C),
ovulation
may
still
occur
in
rainbow
trout,
but
postovulatory
egg
survival
in
the
body
cavity
is
much
shorter.
Taranger
and
Hansen
(
1993)
used
Atlantic
salmon
(
Salmo
salar)
to
test
the
timing
of
ovulation
under
different
temperature
regimes.
Water
temperature
was
either
increased
from
50
°
F
(
10
°
C)
to
55.4­
57.2
°
F
(
13­
14
°
C)
(
warm
water),
decreased
abruptly
from
50
°
F
(
10
°
C)
to
41­
44
°
F
(
5­
7
°
C)
(
cold
water)
or
gradually
decreased
from
50
to
46.4
°
F
(
10­
8
°
C)
(
ambient
control)
from
November
1
onward.
Median
ovulation
time
was
delayed
by
5
wk
in
the
warm­
water
group
compared
with
ambient
controls,
with
43%
of
the
females
remaining
nonovulated
at
the
end
of
the
study.
Only
minor
effects
were
observed
on
timing
of
ovulation
in
the
cold­
water
group
compared
with
the
ambient
controls.
Survival
of
eggs
to
the
eyed
stage
was
significantly
higher
in
the
cold­
water
group
(
92.1%)
than
in
both
the
ambient
control
group
(
84.5%)
and
the
warm­
water
group
(
76.6%).
The
results
indicate
that
high
water
temperature
during
the
spawning
season
may
inhibit
ovulation
and
have
a
detrimental
effect
on
gamete
quality.
Morrison
and
Smith
(
1986,
as
cited
in
Taranger
and
Hansen
1993)
found
that
low
water
temperature
delayed
ovulation
in
winter
spawning
rainbow
trout
and
that
an
increase
in
water
temperature
could
accelerate
ovulation.

Although
eggs
in
the
body
cavity
of
the
female
are
less
sensitive
than
they
are
out
side
the
female
(
roughly
several
weeks
compared
with
a
few
days)
(
Billard
and
Gillet
1981,
Billard
and
Breton
1977),
once
ovulation
has
occurred
the
quality
of
the
eggs
will
begin
to
decline
as
they
overripen
(
Gillet
1991
as
cited
in
Baroudy
and
Elliott
1994,
Bouck
and
Chapman
1975,
Flett
et
al.
1996,
Sakai
et
al.
1987
as
cited
in
Flett
et
al.
1996,
de
Gaudemar
and
Beal
1998).
Bry
(
1981),
as
cited
in
Flett
et
al.
(
1996),
found
that
eggs
retained
in
the
body
cavity
after
ovulation
show
a
high,
significant
decline
in
quality
by
9­
12
d
after
ovulation
at
54
º
F
(
13
º
C).
Escaffre
et
al.
(
1977),
as
cited
in
Flett
et
al.
(
1996),
reported
a
rapid
decline
in
egg
quality
when
water
temperature
exceeded
57.2­
59
º
F
(
14­
15
º
C).
De
Gaudemar
and
Beal
(
1998)
found
that
8
d
after
o
vulat
ion
in
Atlantic
salmon,
egg
survival
already
seemed
affected.
In
rainbow
trout,
Sakai
et
al.
(
1975),
as
cited
in
de
Gaudemar
and
Beal
(
1998),
showed
a
decrease
in
embryonic
and
posthatching
survival
if
ova
were
kept
more
than
5­
7
d
in
the
abdominal
cavity
after
ovulation.
They
also
found
that
after
15
d
ova
underwent
a
decrease
in
fertility,
which
could
even
be
close
to
zero
after
2
wk
according
to
Stein
and
Hochs
(
1979),
as
cited
in
de
Gaudemar
and
Beal
(
1998).
79
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
Bouck
and
Chapman
(
1975)
found
that
50
°
F
(
10
°
C)
would
be
more
favorable
fo
r
sexually
maturing
adult
sockeye
salmon
than
61.7
°
F
(
16.5
°
C).
Body
weight
losses
for
females
averaged
8.5%
at
50
°
F
(
10
°
C)
and
13.2%
at
61.7
°
F
(
16.5
°
C).
Although
fat
reserves
were
abundant
in
the
50
°
F
(
10
°
C)
group,
they
were
absent
at
61.7
°
F
(
16.5
°
C).
Higher
temperatures,
61.7
°
F
versus
50
°
F
(
16.5
vs.
10
°
C),
were
associated
with
advanced
development
of
secondary
sexual
characteristics
(
snout
and
dark
skin)
and
diminished
development
of
gonads.
Females
bore
similar
numbers
of
eggs
at
50
and
61.7
°
F
(
10
and
16.5
°
C),
but
eggs
were
11%
less
in
weight
in
the
61.7
°
F
(
16.5
°
C)
group,
which
was
correlated
with
percentage
body
weight
loss.
Bouck
(
1977)
found
results
very
similar
to
those
reported
in
Bouck
and
Chapman
(
1975).

Exposure
o
f
ripe
adults
and
eggs
to
water
temperatures
above
55.9
°
F
(
13.3
°
C)
is
commonly
assumed
to
result
in
greater
than
normal
losses
and
abnormalities
of
young
fish
(
Morat
and
Richardson
1983,
Weidlein
1971,
Dunham
1968,
as
cited
in
CDWR
1988).
Rice
(
1960)
tested
hatchery
holding
facilities
to
determine
the
best
conditions
for
holding,
spawning,
and
incubating
chinook
salmon
stocks
from
the
American
River
in
California.
He
determined
that
a
facility
with
temperatures
below
44.96
°
F
(
7.2
°
C)
was
too
cold
for
successful
incubation,
but
one
with
temperatures
ranging
between
46.94
and
60
°
F
(
8.3
and
15.6
°
C)
was
satisfactory
for
egg
development.

Billard
and
Breton
(
1977)
found
that
temperatures
above
55.4
°
F
(
13
°
C)
allowed
ovulation
to
occur
in
rainbow
trout,
but
postovulatory
egg
survival
time
in
the
body
cavity
was
much
shorter
than
at
lower
temperatures.
The
authors
noted
that
in
vivo
survival
of
ovulated
eggs
(
4
d)
in
rainbow
trout
was
high
(
approximately
95%)
for
70
h
at
68
°
F
(
20
°
C),
but
beyond
this
point
survival
dropped
rapidly
and
dramatically
(
to
approximately
5%
at
110
h).
This
demonstrated
that
rainbow
trout
broodfish
must
be
held
at
water
temperatures
not
exceeding
55.9
°
F
(
13.3
°
C)
(
preferably
not
above
53.9
°
F
[
12.2
°
C])
for
a
period
of
2­
6
months
before
spawning
to
produce
eggs
of
good
quality
(
Smith
et
al.
1983
as
cited
by
Bruin
and
Waldsdorf
1975,
Leitritz
and
Lewis
1976).

Temperatures
shown
to
affect
salmonid
egg
quality
vary.
Flett
et
al.
(
1996)
suspected
that
the
low
survival
to
hatching
observed
in
adult
coho
salmon
migrants
was
caused
by
traveling
through
waters
warmer
than
68
°
F
(
20
°
C).
Temperatures
greater
than
60
°
F
(
15.6
º
C)
were
noted
to
decrease
egg
survival
and
co
ntribut
e
to
coagulated
yolk
in
sac­
fry
(
Hinze
et
al.
1956
as
cited
by
CDWR
1988,
Olson
and
Foster
1957).
Greatest
survival
occurred
in
eggs
taken
from
fish
when
water
temperature
was
in
the
53.1­
54
º
F
(
11.7­
12.2
º
C)
range.
Furthermore,
it
was
noted
that
early
embryonic
damage
may
be
manifested
during
the
latter
part
of
the
fry
stage
and
just
after
feeding
has
begun
in
the
fingerling
stage,
so
rates
of
survival
to
hatching
may
underestimate
the
detriment
al
effect
of
prespawning
temperatures.
Rice
(
1960)
found
that
holding
broodsto
ck
in
hatchery
waters
that
were
consistently
above
60
°
F
(
15.6
°
C)
reduced
survival
of
eggs
to
the
eyed
stage
by
12.7%
compared
with
holding
the
broodstock
between
46.9
and
60
°
F
(
8.3­
15.6
°
C).
Bouck
et
al.
(
1970,
as
cited
in
EPA
and
NMFS
1971),
however,
found
no
apparent
adverse
effects
on
coho
salmon
eggs
in
utero
after
prolonged
exposure
of
adult
fish
to
62
°
F
(
16.7
°
C).
When
females
hold
in
warm
water,
eggs
tend
to
be
smaller
with
less
stored
energy,
which
means
less
energy
for
alevin
development
and
the
necessity
for
earlier
feeding
to
sustain
life.
Berman
and
Quinn
(
1989)
cited
a
personal
communication
with
B.
Ready,
the
manager
o
f
the
Kalama
State
Fish
Hatchery,
showing
egg
mortalities
of
50%
or
more
from
adults
held
in
river
waters
80
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
fluctuating
from
57.9
to
66.9
°
F
(
14.4­
19.4
°
C).
The
current
supervisor
of
the
Kalama
Falls
Hatchery,
Ron
Castaneda,
acknowledges
that
they
incur
some
increased
losses
at
holding
temperatures
around
60­
64
°
F
(
15.6­
17.8
°
C),
but
they
have
not
had
mortality
as
high
as
50%.
It
is
perhaps
useful
to
note
that
this
hatchery
incubates
in
the
natural
river
water
as
well.

In
an
unpublished
1995
study,
Dr.
Craig
Clarke
(
cited
in
Macdonald
et
al.
in
press)
exposed
early
Stuart
sockeye
salmon
captured
at
Hell's
Gate
to
two
temperature
treatments
(
59
and
66.2
°
F
[
15
and
19
°
C])
for
2
wk.
Two
weeks
of
exposure
to
66.2
°
F
(
19
°
C)
in
the
laboratory
reduced
plasma
testosterone
levels
significantly
in
both
sexes
compared
with
59
°
F
(
15
°
C)
exposure.
Levels
of
11­
ketotestost
erone
and
estradiol
were
low
and
below
the
detection
limit
in
many
fish
at
66.2
°
F
(
19
°
C).
Furthermore,
circulating
levels
of
the
major
hormones
cont
rolling
sexual
maturation
were
also
depressed
at
62.2
°
F
(
19
°
C).
Similarly,
Manning
and
Kime
(
1985
as
cited
in
Macdonald
et
al.
in
press)
found
that
steroid
biosynthesis
was
suppressed
in
rainbow
trout
testes
at
62.6
°
F
(
17
°
C).
Clearly,
the
potential
for
suppression
of
sexual
development
and
intergenerational
impairment
existed
in
1998
when
migration
temperatures
exceeded
62.2
°
F
(
19
°
C)
at
many
locations
and
times.
This
possibility
was
supported
further
by
an
experimental
assessment
of
the
spawning
success
of
t
he
early
Stuart
and
Horsefly
stocks.
Macdonald
et
al.
(
in
press)
monitored
stress
and
reproductive
state
in
bo
th
prespawning
and
postspawning
sockeye
from
the
Horsefly
River
Stock
(
midsummer
run).
The
Horsefly
River
stock
entered
the
Fraser
River
of
British
Columbia
during
the
warmest
period
of
the
year.
During
migration
to
the
spawning
grounds,
temperatures
were
well
in
excess
of
68
°
F
(
20
°
C).
Four
stress
parameters
and
three
reproductive
parameters
were
examined.
In
addition,
a
portion
of
the
fish
collected
were
artificially
spawned
and
their
eggs
placed
in
capsules
in
the
gravel
of
their
natal
stream
and
examined
to
determine
both
fertilization
and
hatching
success.
Fertilization
success
was
found
to
be
lower
in
1998
than
in
1997.
Horsefly
fish
that
arrived
on
the
spawning
grounds
in
early
1998
suffered
even
lower
fertilization
success
rates
than
the
Stuart
fish,
and
only
10%
of
their
eggs
hatched.
Egg
hatching
success
(
but
not
fertilization
success)
was
influenced
by
the
condition
of
the
spawning
female
as
estimated
by
stress
and
reproductive
parameters.
Females
that
arrived
late
tended
to
have
lower
levels
of
testosterone
and
spawned
eggs
that
hatched
more
successfully.
These
late
arrivals
likely
experienced
less
severe
water
temperatures
during
their
entire
migration
than
did
early
fish.
The
likely
difference
at
Hell's
Gate
was
that
mean
daily
temperatures
were
64.4­
66.2
°
F
(
18­
19
°
C)
versus
69.8­
71.6
°
F
(
21­
22
°
C).
These
observations
suggested
that
the
upper
threshold
temperature
for
successful
migration
lies
between
64.4
and
71.6
°
F
(
18
and
22
°
C).

Based
on
the
information
reviewed
above,
it
can
be
concluded
that
holding
migratory
fish
at
constant
temperatures
above
55.4­
60.1
º
F
(
13­
15.6
º
C)
may
impede
spawning
success.
Maximum
constant
temperatures
of
50­
54.5
º
F
(
10­
12.5
º
C)
may
provide
better
reproductive
co
nditions
in
most
salmon
and
trout.

How
is
survival
of
prespawning
adults
affected
by
water
temperature?

Leitritz
and
Lewis
(
1976)
and
Piper
et
al.
(
1982)
recommended
chinook
broodstock
holding
temperatures
of
42.8­
57.2
°
F
(
6­
14
°
C).
Conventional
hatchery
practice
is
to
consider
chinook
broodstock
thermally
stressed
at
temperatures
>
59
°
F
(
15
°
C);
survival
declines
dramatically
when
temperatures
exceed
62.6
°
F
(
17
°
C)
(
Marine
1992).
Raleigh
et
al.
(
1986)
described
adult
chinook
prespawning
temperatures
as
maximal
in
the
range
46.4­
54.5
°
F
(
8­
12.5
°
C)
but
declining
to
zero
81
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
at
75.2
°
F
(
24
°
C).
A
study
by
Fish
(
1944)
revealed
that
adult
chinook
survival
under
fluctuat
ing
temperature
regimes
of
48.9­
73.9
°
F
(
9.4­
23.3
°
C)
(
mean
=
10.8
°
F
[
16
°
C])
was
only
36%,
but
at
52­
60
°
F
(
11.1­
15.6
°
C)
(
mean
=
53
°
F
[
11.9
°
C])
survival
was
75%
after
holding
in
ponds
for
approximately
2
months.
This
study
highlights
the
benefit
of
holding
adults
under
cold
water
temperatures
to
promote
survival.
However,
in
this
Grand
Coulee
Fish
Salvage
Program,
disease
outbreaks
(
especially
columnaris)
in
the
holding
pond
environments
made
cold­
water
holding
particularly
necessary
to
inhibit
pathogens.

Prespawning
mortality
of
wild
spring
chinook
in
the
Warm
Springs
River
varied
from
34%
to
75%
during
the
period
1977­
1986.
In
1980
and
1981
prespawning
mortality
averaged
74%.
BKD
was
implicated
in
this
high
mortality
because
it
was
responsible
for
mortality
in
the
hatchery.
Even
though
all
adults
released
to
the
Warm
Springs
River
above
the
hatchery
were
inoculated
for
BKD
in
1982­
1986,
mortality
was
still
high
(
24%­
59%).
In
the
Rogue
River,
Oregon,
furunculosis
and
columnaris
were
the
primary
cause
of
mortality
of
wild
and
hatchery
adults
from
1977
to
1981.
Prespawning
mortality
in
wild
and
hatchery
fish
was
12%
and
36%,
respect
ively,
during
this
period
(
Cramer
et
al.
1985
as
cited
by
Lindsay
et
al.
1989).
Wild
spring
chinook
in
the
lower
Rogue
River
exhibited
high
prespawning
mortality
in
May­
July
1992
as
water
temperature
ranged
from
64.4
to
69.8
°
F
(
18­
21
°
C)
(
M.
Everson,
ODFW,
pers.
comm.,
as
cited
by
Marine
1992).
The
foregoing
studies
point
out
the
variability
of
prespawning
salmonid
mortality
in
the
wild
and
the
magnitude
of
disease
effects
observed
under
thermal
stress.

What
temperature
ranges
are
associated
with
the
adult
spawning
period?

There
is
conflict
between
the
fish's
inherent
temperature
preferences
and
its
need
to
spawn
within
a
limited
time
frame.
That
is,
given
a
prolonged
high­
temperature
period
during
adult
holding,
adults
may
be
forced
to
spawn
during
adverse
conditions,
leading
to
poor
egg
and
sperm,
embryo,
alevin,
or
fry
survival.
For
this
reason,
fish
habitat
managers
must
use
discret
ion
in
selecting
suitable
spawning
temperatures.
Even
though
fish
may
have
been
observed
spawning
under
warm
temperatures,
as
during
the
initial
days
of
the
spawning
period,
there
is
no
guarantee
that
embryo
survival
is
high
for
the
early­
spawning
fish.
There
is
some
plasticity
in
timing
of
life
stage
events
relative
to
annual
climatic
patterns
(
i.
e.,
if
sufficient
energy
remains
in
the
adult
body
in
the
prespawning
stage,
some
delay
in
spawning
is
feasible),
and
adjustments
can
be
made
throughout
the
life
cycle,
but
inability
to
compensate
fully
tends
to
be
expressed
as
population
mortality,
poor
growth,
reduced
fecundity,
and
reduced
fitness.

Spawning
of
chinook
in
a
wide
variety
of
locations
has
been
reported
for
a
composite
temperature
range
of
35.9­
66
°
F
(
2.2­
18.9
°
C)
(
Mattson
1948,
Burner
1951,
both
as
cited
by
Raleigh
et
al.
1986,
Crawford
et
al.
1976
as
cited
by
Vigg
and
Watkins
1991,
Olson
and
Foster
1955,
Chambers
1956
as
cited
by
Andrew
and
Geen
1960,
Snyder
et
al.
1966
as
cited
by
Parker
and
Krenkel
1969,
Wilson
et
al.
1987).
Recommended
spawning
temperatures
for
spring,
summer,
and
fall
chinook
given
by
Reiser
and
Bjornn
(
1979)
and
Bjornn
and
Reiser
(
1991)
in
their
literature
review
were
42­
57
°
F
(
5.6­
13.9
°
C).
These
limits
were
extracted
from
Bell
(
1986).
EPA
and
NMFS
(
1971)
recommended
a
maximum
temperature
of
55
°
F
(
12.8
°
C).
Bell
(
1991)
gave
a
range
of
42­
57.5
°
F
(
5.6­
14.2
°
C)
as
the
preferred
spawning
zone,
with
51.8
°
F
(
11
°
C)
as
a
preferred
temperature
based
on
an
extensive
summary
of
literature.
82
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
What
temperatures
or
thermal
regimes
are
required
to
initiate
spawning?

In
autumn­
spawning
species
such
as
the
Pacific
salmon,
it
can
be
assumed
that
the
highest
temperatures
associated
with
the
spawning
period
are
temperatures
that
allow
spawning
to
be
initiated.
For
chinook,
the
extreme
high
temperature
at
spawning
was
66
°
F
(
18.9
°
C).
However,
egg
survival
at
these
temperatures
cannot
be
assumed.
In
general,
60.4
°
F
(
16
°
C)
is
the
maximum
associated
with
initiation
of
fall
chinook
spawning
(
Groves
and
Chandler
1999).

It
has
been
reported
that
spawning
is
initiated
when
temperatures
decline.
Chambers
(
1956
as
cited
by
Raleigh
et
al.
1986)
found
that
spring
chinook
normally
spawn
as
water
temperature
declines
from
55
to
40.1
°
F
(
12.8­
4.5
°
C)
and
fall
chinook
spawn
under
a
56.1­
41
°
F
(
13.4­
5
°
C)
decline.
The
critical
temperature
threshold
of
approximately
55
°
F
(
12.8
°
C)
and
declining
temperature
are
apparently
associated
with
ability
to
complete
the
spawning
act,
maximum
long­
term
viability
of
eggs
and
alevins,
and
bett
er
resistance
to
death
by
disease
in
adults
and
eggs.
Although
prespawning
mortality
attributed
to
bioenergetic
stress
may
be
a
significant
factor
in
overall
adult
mort
ality
up
to
spawning
time,
it
is
uncertain
how
to
separate
disease
and
bioenergetic
stress
effects.

Spawning
can
be
initiated
only
under
a
limited
temperature
range.
In
the
Hanford
Reach
of
the
Columbia
River,
the
median
date
for
peak
spawning
was
November
11,
based
on
surveys
from
1948
to
1992.
On
this
date
the
mean
weekly
temperature
was
54.5
°
F
(
12.5
°
C)
and
the
maximum
weekly
temperature
was
57.2
°
F
(
14
°
C)
(
Dauble
and
Watson
1997).
However,
in
both
the
Hanford
Reach
and
Snake
River
spawning
zones,
spawning
activity
begins
as
weekly
mean
water
temperatures
decline
below
60.8
°
F
(
16
°
C)
and
continues
up
to
41
°
F
(
5
°
C)
(
Groves
and
Chandler
1999).
Because
studies
of
egg
survival
and
development
after
fertilization
for
chinook
and
other
salmon
species
indicate
reduced
survival
under
temperatures
of
53.6­
60.8
°
F
(
12­
16
°
C),
preferred
spawning
temperatures
of
55
°
F
(
12.8
°
C)
(
maximum)
have
typically
been
recommended
(
see
EPA
and
NMFS
1971,
review
of
McCullough
1999).
These
data
indicate
that
it
is
essential
for
mainstem
temperatures
to
decline
rapidly
below
60.8
°
F
(
16
°
C)
so
that
spawning
activities
can
commence
and
also
so
that
egg
survival
continues
to
improve
during
the
spawning
period.

Fall
chinook,
sockeye,
and
coho
were
all
reported
to
spawn
on
falling
temperatures
starting
at
peaks
of
51­
55
°
F
(
10.6­
12.8
°
C)
(
Chambers
1956
as
cited
by
Andrew
and
Geen
1960).
Sockeye
spawning
success
was
only
45%
when
mean
daily
temperatures
during
spawning
were
57.9­
61
°
F
(
14.4­
16.1
°
C).
On
the
Fraser
River,
spawning
temperatures
>
55
°
F
(
12.8
°
C)
were
associated
with
an
increasing
number
of
females
that
died
without
spawning
(
Andrew
and
Geen
1960).
Temperatures
>
53.6
°
F
(
12
°
C)
can
inhibit
or
delay
spawning
by
Atlantic
salmon
(
Beall
and
Marty
1983,
as
cited
by
de
Gaudemar
and
Beall
1998).
In
the
laboratory,
brook
trout
spawning
was
typically
initiated
at
50
°
F
(
10
°
C)
but
occurred
under
temperatures
as
high
as
60.8
°
F
(
16
°
C)
(
Hokanson
et
al.
1973).
Spawning
of
brook
trout
begins
to
occur
after
the
weekly
mean
temperature
falls
below
55.4
°
F
(
13
°
C)
(
approximately
early
October).
During
the
spawning
period,
water
temperatures
steadily
decline
from
approximately
55
to
44.8
°
F
(
12.8­
7.1
°
C)
(
Hokanson
et
al.
1973).
Based
on
a
survey
of
temperature
effects
o
n
all
aspects
o
f
spawning
in
fall­
spawning
salmonids,
it
appears
that
spawning
temperatures
in
the
spring
and
fall
chinook
spawning
habitats
having
a
55
°
F
(
12.8
°
C)
peak
and
that
a
declining
trend
would
satisfy
biological
requirements.
Keying
the
spawning
period
to
rapidly
falling
temperatures
is
common
among
83
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
fall­
spawning
salmonids
and
has
been
documented
for
chinook
of
the
Pacific
Northwest
(
Groves
and
Chandler
1999,
Lindsay
et
al.
1986).

Although
spawning
for
bull
trout
may
begin
as
early
as
mid­
August,
spawning
activity
is
reported
to
be
initiated
when
water
temperatures
begin
to
fall
to
48.2
°
F
(
9
°
C)
or
lower
(
McPhail
and
Murray
1979,
Shepard
et
al.
1982,
Kraemer
1994,
Brenkemen
1998).
Both
the
coastal
rainbow
and
the
redband
trout
spawn
in
the
spring,
stimulated
by
rising
water
temperatures.
Behnke
(
1992)
suggested
that
along
the
Pacific
coast
a
water
temperature
of
about
37.4­
42.8
°
F
(
3­
6
°
C)
may
initiate
some
spawning
activity,
but
spawning
does
not
usually
occur
until
temperatures
reach
42.8­
48.2
°
F
(
6­
9
°
C).
Although
this
spawning
activity
would
typically
occur
from
late
December
through
April,
in
some
very
cold
headwater
streams
local
temperatures
may
delay
spawning
until
July
or
August
for
some
stocks.
Beschta
et
al.
(
1987)
suggested
that
rainbow
trout
spawn
between
35.9
and
68
°
F
(
2.2
and
20
°
C),
Bell
(
1986)
set
the
range
at
35.9­
66
°
F
(
2.2­
18.9
°
C),
and
Piper
et
al.
(
1982)
concluded
the
range
was
50­
55
°
F
(
10­
12.8
°
C).

Conclusions
for
spawning.
Egg
mortality,
alevin
development
linked
to
thermal
exposure
of
eggs
in
ripe
females
or
newly
deposited
in
gravel,
and
egg
maturation
are
negatively
affected
by
exposure
to
temperatures
above
approximately
54.5­
57.2
°
F
(
12.5­
14
°
C).
Therefore,
a
spawning
temperature
range
of
42­
55
°
F
(
5.6­
12.8
°
C)
(
maximum)
appears
to
be
a
reasonable
recommendation
for
Pacific
salmon,
unless
colder
thermal
regimes
are
natural
in
any
tributary.

SUPPORTING
DISCUSSION
AND
LITERATURE
 
LETHAL
EFFECTS
What
is
the
utility
of
UILT
data
and
how
has
it
been
applied?

Upper
incipient
lethal
temperature
data
were
tabulated
in
NAS
(
1972)
for
juveniles
and
adults
of
many
fish
species.
UILT
values
for
many
salmonid
species
have
since
been
added
to
the
literature;
a
cross­
section
is
summarized
in
Table
4,
extracted
from
McCullough
(
1999).
The
UILT
values
correspond
to
the
highest
acclimation
temperatures,
and
consequently,
are
very
similar
to
UUILT
values.
Given
prior
acclimation
to
temperatures
lower
than
listed
in
the
table,
however,
the
UILT
values
would
likely
be
lower.
This
means
that
in
the
field,
mortality
can
be
induced
at
temperatures
significantly
lower
than
UUILT
levels.

Studies
of
the
effect
of
elevated
water
temperature
on
survival
of
a
wide
variety
of
salmonids
using
transfer
to
high
constant
temperature
(
UILT
experiments)
show
much
consistency
among
species.
In
those
tests
in
which
acclimation
temperature
was
68
°
F
(
20
°
C)
and
the
UILT
was
approximately
equal
to
the
UUILT,
UILT
values
found
ranged
from
73.4
to
80.6
°
F
(
23­
27
°
C).
Redband
trout
tend
to
be
the
most
heat
resistant
of
the
salmonids;
UILT
values
for
all
other
species
ranged
from
73.4
to
78.8
°
F
(
23­
26
°
C).

NAS
(
1972)
recommended
that
for
any
acclimation
temperature,
short
­
term
exposure
be
limited
to
UILT
(
factor
of
safety,
3.6
°
F
[
2
°
C]).
This
assumes
that
at
the
UILT
temperature,
50%
of
the
population
would
die
within
the
test
period
(
at
least
1,000
min),
but
if
the
temperature
is
reduced
by
3.6
°
F
(
2
°
C),
no
mortalities
would
occur
in
this
time
period.
Although
this
assumption
may
generally
be
valid,
it
also
relies
on
no
incidence
of
disease
or
other
sublethal
effects.
When