Document ID: EPA-HQ-OW-2003-0068-0034
Agency: epa
Document Type: Supporting & Related Material
Title: 
Posted Date: 2003-09-22T04:00Z

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
84
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
this
method
was
proposed,
cumulative
effects
of
repeat
exposure
to
high
temperatures
were
not
well
known
(
see
DeHart
1975,
Golden
1975,
Golden
1976,
Golden
and
Schreck
1978).

Although
temperatures
of
73.4­
78.8
°
F
(
23­
26
°
C)
are
generally
considered
the
UUILT
for
most
salmonids,
UILT
values
are
typically
1.8­
3.6
°
F
(
1­
2
°
C)
less
than
UUILT.
The
UILT
values
are
incipient
lethal
temperatures
that
correspond
to
acclimation
temperatures
lower
than
the
UUILT.
Because
we
can
never
assume
that
fish
in
the
field
will
be
acclimated
to
the
highest
acclimation
temperature,
the
more
appropriate
lethal
temperature
in
the
field
may
be
up
t
o
3.6
°
F
(
2
°
C)
less
than
UUILT.
The
factor
of
safety
would
then
have
to
be
applied
t
o
this
value,
and
even
then
the
additional
sublethal
or
cumulative
lethal
concerns
remain.

The
73.4­
78.8
°
F
(
23­
26
°
C)
UUILT
range
for
salmonids
applies
to
the
juvenile
life
stage.
Although
information
on
salmon
adults
is
much
more
limited,
it
indicates
that
adults
are
far
more
sensitive
than
juveniles
to
high
temperatures.
Becker
(
1973)
identified
the
thermal
tolerance
of
chinook
jacks
to
be
69.8­
71.6
°
F
(
21
°
­
22
°
C)
on
the
basis
of
a
168
h
TLM
test.
Coutant
(
1970)
identified
the
incipient
lethal
temperature
for
chinook
jacks
as
71.6
°
F
(
22
°
C)
with
prior
acclimation
to
66.2
°
F
(
19
°
C)
(
estimated
from
ambient
river
temperatures).
Columbia
River
steelhead,
acclimated
to
a
river
temperature
of
66.2
°
F
(
19
°
C)
had
a
lethal
threshold
of
69.8
°
F
(
21
°
C)
(
Coutant
1970).
These
lethal
limits
are
9.9
°
F
(
5.5
°
C)
lower
than
for
juvenile
rainbow
acclimated
to
64.4
°
F
(
18
°
C)
(
Alabaster
and
Welcomme
1962,
as
cited
by
Coutant
1972).

Servizi
and
Jensen
(
1977)
found
that
the
geometric
mean
survival
times
(
GMST)
for
adult
sockeye
were
less
than
for
juveniles.
They
also
reported
that
the
median
survival
times
(
MST)
for
adult
coho
found
by
Coutant
(
1969)
were
similar
to
those
of
sockeye
over
the
exposure
range
80.6­
86
°
F
(
27­
30
°
C).
The
GMST
for
adult
sockeye
was
1,000
min
at
75.2
°
F
(
24
°
C)
with
acclimation
at
60.4­
64.9
°
F
(
15.8­
18.3
°
C).
Survival
time
at
78.8
°
F
(
26
°
C)
was
only
100
min.
Time
to
loss
of
equilibrium
and
survival
time
of
adults
were
plotted
vs.
exposure
temperature
on
the
same
graph.
The
curve
for
loss
of
equilibrium
was
considerably
lower
than
the
time­
to­
death
curve.
For
this
reason,
Servizi
and
Jensen
(
1977)
considered
the
loss
of
equilibrium
temperature
more
ecologically
significant.
Furthermore,
because
sockeye
exposed
to
temperatures
of
approximately
64.4­
69.8
°
F
(
18­
21
°
C)
become
highly
susceptible
to
Flexibacter
columnaris,
researchers
took
this
temperature
range
as
a
greater
thermal
threat
to
continued
sto
ck
survival.

Although
UUILT
or
UILT
temperatures
are
well
known
and
consistent
for
the
various
salmonids,
they
are
probably
not
useful
in
setting
temperature
standards.
Certainly
they
represent
the
upper
limits
to
tolerance,
but
salmonids
in
a
stream
system
tend
to
be
restricted
to
maximum
temperatures
that
are
3.6­
7.2
°
F
(
2­
4
°
C)
lower
than
UILT
values.
In
general,
a
maximum
temperature
of
71.6­
75.2
°
F
(
22­
24
°
C)
represents
the
normal
upper
temperature
limit
in
the
field
(
see
McCullough
1999).
As
this
limit
is
approached,
juvenile
density
declines
t
o
zero.
Using
the
presence/
absence
threshold
as
a
temperature
standard
for
salmon
habitat
can
only
be
done
when
density
is
at
or
near
zero.

Although
the
UILT
has
limited
value
in
establishing
the
temperature
standard
itself,
the
a
and
b
coefficients
for
a
given
acclimation
temperature
are
useful
in
estimating
exposure
times
that
will
result
in
50%
mortality.
In
addition,
NAS
(
1972)
recommended
(
MWAT)
as
an
index
to
tolerable
prolonged
exposures.
This
index
was
estimated
as
either:
85
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
[(
opt.
temp.
+
zng
temp.)/
2],

where
the
zng
or
zero
net
growth
temperature
is
that
temperature
which
results
in
zero
net
growth
of
a
population
(
i.
e.,
subt
racting
tissue
lost
as
population
mortality
from
that
added
in
growth)

or
opt.
temp.
+
(
UILT
!
opt.
temp)/
3.

Each
formula
is
based
o
n
the
assumption
that
adequate
growth
rates
can
be
maintained
if
the
weekly
average
maximum
temperature
falls
between
the
optimum
and
the
UILT
or
the
zero
net
growth
temperature.
However,
the
decline
in
growth
rate
can
be
very
steep
if
temperature
is
above
the
optimum.
Consequently,
limiting
reductions
in
growth
rates
to,
for
example,
80%
of
maximum
levels
can
lead
to
much
greater
reductions
in
growth,
given
errors
estimating
the
relationship
or
managing
temperature
in
a
watershed.

Are
there
potential
weaknesses
in
reliance
on
MWAT?

Hokanson
et
al.
(
1977)
advised
caution
in
using
short­
term
exposure
experiments
to
calculate
long­
term
exposures,
such
as
with
MWAT.
They
reported
for
O.
mykiss
that,
given
a
physiological
optimum
of
60.8­
64.4
°
F
(
16­
18
°
C)
and
a
UILT
of
78
°
F
(
25.6
°
C)
(
at
60.8
°
F
[
16
°
C]
acclimation),
one
would
calculate
an
MWAT
of
66.2
°
F
(
19
°
C)
and
a
maximum
temperature
(
applying
the
2
°
C
safety
factor
of
Coutant
1972)
of
75.2
°
F
(
24
°
C)
for
short­
term
exposure.
Measurement
of
rainbow
trout
growth
showed
that
at
a
fluct
uating
temperature
of
71.6
±
6.8
°
F
(
22
±
3.8
°
C)
specific
growth
rate
was
zero.
Under
this
temperature
regime
mortality
rate
was
42.8%/
d
during
the
first
7
d.
For
experiments
within
the
optimum
range
(
59.9­
63.1
°
F
[
15.5
°
C­
17.3
°
C]
for
a
fluct
uating
regime),
average
specific
mort
ality
was
0.36%/
d.
Combining
data
on
specific
growth
and
mortality
rates,
the
authors
were
able
to
predict
yield
for
a
hypothetical
population
under
t
he
temperature
regimes.
A
rainbow
trout
population
would
exhibit
zero
increase
over
a
40­
d
period
(
maintenance)
at
a
constant
temperature
of
73.4
°
F
(
23
°
C)
and
a
fluctuating
temperature
with
a
mean
of
69.8
±
6.8
°
F
(
21
±
3.8
°
C)
because
growth
balances
mortality.
Several
sources
report
temperatures
of
69.8­
73.4
°
(
21­
23
°
C)
as
the
upper
limit
of
rainbow
trout
distribution
in
the
field
(
Hokanson
et
al.
1977).
Numerous
authors
have
reported
upper
limits
to
salmonid
distribution
as
approximately
71.6­
75.2
°
F
(
22­
24
°
C).

With
this
laboratory
information
and
corroborating
field
information,
Hokanson
et
al.
(
1977)
recommended
a
mean
weekly
temperature
of
62.6
±
3.6
°
F
(
17
±
2
°
C)
for
rainbow
trout
so
that
maximum
yield
is
not
reduced
more
than
27%
under
normal
fluctuating
temperature
regimes.
Production
has
been
shown
to
be
substantially
reduced
even
just
above
the
physiological
optimum.
This
paper
has
great
significance.
It
was
published
5
years
after
the
National
Academy
of
Sciences
recommended
the
use
of
MWAT
to
establish
prolonged
exposure
temperatures.
The
NAS
acknowledged
that
growth
rate
should
be
expressed
as
net
biomass
gain
or
net
growth.
Yield
is
that
portion
o
f
the
population
available
to
humans;
t
he
remainder
is
lost
as
mortality,
which
can
be
substantial
if
temperatures
are
high.
Also,
if
temperatures
are
high,
much
of
the
energy
assimilated
from
food
is
lost
as
excessive
metabolism.
If
the
MWAT
is
66.2
°
F
(
19
°
C),
86
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
and
yield
is
reduced
27%
from
maximum,
even
at
a
mean
weekly
temperature
of
62.6
±
3.6
°
F
(
17
±
2
°
C)
it
is
obvious
that
MWAT
is
not
protective.

In
addition
to
concern
for
the
inadequacy
of
the
MWAT,
this
criterion
also
covered
reproduction
and
development
needs
of
salmonids.
A
quo
te
from
NAS
(
1972)
is
useful:

Uniform
elevations
of
temperature
by
a
few
degrees
during
the
spawning
period,
while
maintaining
short­
term
temperature
cycles
and
seasonal
thermal
patterns,
appear
to
have
little
overall
effect
on
the
reproductive
cycle
of
resident
aquatic
species,
other
than
to
advance
the
timing
for
spring
spawners
or
delay
it
for
fall
spawners.
Such
shifts
are
often
seen
in
nature,
although
no
quantitative
measurements
of
reproductive
success
have
been
made
in
this
connection.

However,
significant
recent
research
has
shown
that
calculated
MWAT
temperatures
(
e.
g.,
66.2
°
F
(
19
°
C)
for
rainbow
trout)
result
in
damage
to
gametes
during
reproductive
stages.
On
the
basis
of
these
technical
findings,
any
temperature
criterion
that
can
result
in
a
27%
reduction
in
biomass
and
affect
gamete
viability
must
be
questioned.

How
can
UILT
data
be
evaluated
against
UUILT
data?

Temperatures
as
low
as
73.4
°
F
(
23
°
C)
have
been
found
to
produce
50%
mortality
(
LT50)
over
the
course
of
a
week
in
rainbow
trout
acclimated
to
very
cold
(
39.2
°
F
[
4
°
C])
waters
(
Sonski
1982,
Threader
and
Houston
1983
as
cited
in
Taylor
and
Barton
1992),
with
the
lethal
temperature
rising
to
75.2
°
F
(
24
°
C)
in
moderately
cold­
water­
acclimated
42.8­
51.8
°
F
(
6­
11
°
C)
fish
(
Black
1953,
Stauffer
et
al.
1984,
Bidgood
1980
as
cited
in
Taylor
and
Barton
1992).
However,
at
most
acclimatio
n
temperatures
likely
to
be
encountered
during
the
spring
through
fall
seasons
(
53.6­
68
°
F
[
12­
20
°
C]),
lethal
levels
are
consistently
in
the
range
of
77­
78.8
°
F
(
25­
26
°
C)
(
Bidgood
and
Berst
1969,
Hokanson
et
al.
1977).
With
cautious
acclimation
to
temperatures
in
the
range
of
73.4­
75.2
°
F
(
23­
24
°
C),
rainbow
trout
may
not
experience
LT50
effects
until
a
week
at
78.8
°
F
(
26
°
C)
(
Charlon
et
al.
1970
as
cited
in
Grande
and
Anderson
1991).
Even
with
careful
acclimatio
n,
77
°
F
(
27
°
C)
results
in
high
or
complete
mortality
in
less
than
24
hours
(
Charlon
et
al.
1970),
and
temperatures
of
84.2­
86
°
F
(
29­
30
°
C)
result
in
50%
mortality
in
1­
2
hours
(
Kaya
1978,
Craigie
1963,
Alabaster
and
Welcomme
1962
as
cited
in
Taylor
and
Barton
1992).

How
can
prolonged
exposure
to
cyclic
temperatures
be
evaluated?

Under
fluctuating
temperature
test
conditions,
rainbow
trout
have
experienced
50%
mortality
in
a
week
of
daily
cycles
from
69.8
to
77
°
F
(
21­
27
°
C)
(
Lee
1980).
Sonski
(
1983),
however,
was
able
to
culture
rainbow
trout
in
ponds
that
reached
84
°
F
(
28.9
°
C),
and
Chandrasekaran
and
Subb
Rao
(
1979)
reported
that
rainbow
trout
were
largely
able
to
survive
in
rearing
ponds
with
months
of
daily
maximum
temperatures
of
78.8­
84.2
°
F
(
26­
29
°
C).

It
seems
important,
given
the
low
lethal
levels
reported
in
the
literature,
to
evaluate
whether
individual
research
results
would
unduly
influence
the
temperature
recommendations.
In
Figures
3
and
4,
lethality
data
for
salmon
and
char
species
(
extracted
from
the
summary
by
Hicks
2000)
are
combined
and
examined
in
two
different
ways
to
develop
a
stronger
basis
for
regional
daily
87
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
maximum
criteria.

In
Figure
3,
all
of
the
available
7­
d
LT50
data
(
50%
of
test
organisms
die
over
a
7­
d
constant
exposure
test)
for
char
and
salmonids
are
presented
by
acclimation
temperature.
This
distribution
is
then
used
to
make
criteria
recommendations
for
acclimation
temperatures.
At
low
acclimation
temperatures,
constant
exposure
to
just
above
72.5
°
F
(
22.5
°
C)
would
be
expected
to
result
in
50%
mortality
over
a
week.
Reducing
this
value
to
a
level
where
no
lethality
would
be
expected
to
any
adults
or
juveniles
would
result
in
a
daily
maximum
not
to
exceed
68.9
°
F
(
20.5
°
C).

Figure
4
considers
resistance
against
short
exposures
to
high
temperatures,
as
might
occur
in
a
natural
fluctuating
stream
environment.
Resistance
time
is
very
important
to
estimating
potential
lethality;
it
is
the
time
spent
above
a
lethal
threshold
that
determines
whether
short­
term
lethal
effects
will
occur.
Different
peak
temperatures
(
e.
g.,
71.6,
75.2,
80.6,
and
86
°
F
[
22,
24,
27,
and
30
°
C]),
may
be
lethal
to
an
organism,
but
the
organism
can
likely
withstand
these
temperatures
for
variable
lengths
of
time.
A
populat
ion
of
fish
may
be
able
to
withstand
69.8
°
F
(
21
°
C)
for
7
d
of
constant
exposure
without
any
mortality,
but
have
50%
of
the
population
die
after
2
d
at
75.2
°
F
(
24
°
C).
At
80.6
°
F
(
27
°
C),
50%
mortality
may
occur
after
less
than
2
h
of
exposure,
and
at
86
°
F
(
30
°
C)
complete
mortality
may
occur
in
just
a
few
minutes.

In
considering
the
effect
o
f
repeat
ed
hot
days,
it
is
important
to
incorporate
cumulative
effects.
DeHart
(
1975)
found
that
lethal
effects
depend
on
the
area
of
the
temperature
time
curve
that
is
above
a
fish's
UILT.
Thermal
effects
accumulate
over
several
days
when
the
daily
temperature
cycle
fluctuates
above
the
UILT,
and
the
time
above
the
UILT
influences
the
thermal
resistance
time
regardless
of
any
lower
test
temperatures.
In
other
words,
the
ability
of
a
fish
to
resist
a
single
day's
exposure
to
a
lethal
temperature
may
not
be
sufficient,
and
15
minutes
spent
at
7.2
°
F
(
4
°
C)
over
the
UILT
is
of
more
consequence
than
the
same
time
spent
at
3.6
°
F
(
2
°
C)
over
the
UILT.

In
Figure
3,
LT50
results
are
plotted
for
durations
of
1
hour
or
less.
At
acclimation
levels
less
than
53.6
°
F
(
12
°
C),
50%
mortality
can
be
expected
at
77
°
F
(
25
°
C)
with
a
1­
h
exposure,
or
at
75.5
°
F
(
24.2
°
C)
with
a
2­
h
exposure.
Reducing
these
values
to
levels
where
no
lethality
would
be
expected
would
result
in
temperatures
not
exceeding
73.4
or
71.6
°
F
(
23
or
22
°
C),
respectively.
Because
adults
are
considered
more
sensitive
than
juveniles
(
all
of
the
1­
h
or
less
data
were
for
juvenile
fish),
and
the
effects
of
lethal
exposures
are
cumulative,
we
can
assume
that
death
may
occur
with
repeated
exposure
to
daily
maximum
temperatures
greater
than
69.8­
71.6
°
F
(
21­
22
°
C).
This
estimate
is
very
similar
to
the
results
(
68.9­
70
°
F
[
20.5­
21.1
°
C])
at
low
acclimation
temperatures
in
the
approach
shown
in
Figure
2.

Acclimation
Temperature
°
F
(
°
C)
Combined
LT50
for
all
Salmonids
Esti
mated
LT1
with
NAS
Adjustment
41
(
5)
72.46
(
22.48)
68.9
(
20.5)

50
(
10)
73.56
(
23.09)
70
(
21.1)

39
(
15)
74.66
(
23.7)
71.06
(
21.7)
88
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
68
(
20)
75.75
(
24.31)
72.14
(
22.3)

Figure
3.
Combined
lethality
data
for
all
salmonid
species
(
based
on
7­
d
LT50
constant
temperature
exposure
test
results).

SUPPORTING
DISCUSSION
AND
LITERATURE
 
SUBLETHAL
AND
LETHAL
EFFECTS
FOR
NATIVE
CHAR,
REDBAND
TROUT,
AND
CUTTHROAT
TROUT
SPECIES
What
are
the
thermal
requirements
of
bull
trout
and
Dolly
Varden?

Incubation.
For
bull
trout,
McPhail
and
Murray
(
1979)
compared
egg
survival
and
water
temperature
and
reported
the
highest
egg
survival
to
hatching
(
80­
95%)
in
water
temperatures
of
35.6­
39.2
°
F
(
2­
4
°
C).
Shortest
hatch,
largest
alevins,
and
largest
hatching
fry
were
also
associated
with
these
low
temperatures
35.6­
39.2
°
F
(
2­
4
°
C).

Research
suggesting
that
spawning
does
not
peak
until
temperatures
fall
to
below
44.6
°
F
(
7
°
C)
is
consistent
with
the
results
o
f
studies
determining
temperatures
necessary
for
the
89
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
successful
incubation
of
char
eggs.
These
studies
show
that
char
require
temperatures
below
42.8
°
F
(
6
°
C)
to
achieve
optimal
egg
survival
(
Buchanan
and
Gregory
1997).
It
is
generally
agreed
that
poor
survival
occurs
at
temperatures
above
44.6­
46.4
°
F
(
7­
8
°
C).
Under
t
est
conditions
where
temperatures
were
held
constant,
46.4­
50
°
F
(
8­
10
°
C)
resulted
in
very
poor
survival
of
eggs
(
0%­
20%)
in
tests
by
McPhail
and
Murray
(
1979),
and
test
temperatures
in
the
range
of
44.6­
51.8
°
F
(
7­
11
°
C)
were
reported
Time
to
LT50
Temperature
(
C)
1
sec
34.32
30
sec
30.42
1
min
29.62
60
min
24.99
120
min
24.2
Figure
4.
Instantaneous
mortality
for
char
and
salmon
combined
(
based
on
LT50
data
for
exposures
of
less
than
1
hour
and
acclimation
to
<
12C).

to
result
in
poor
survival
in
hatchery
culture
by
Brown
(
1985).
McPhail
and
Murray
(
1979)
found
a
temperature
of
42.8
°
F
(
6
°
C)
to
produce
variable
survival
rates
(
60%­
90%),
and
the
range
of
90
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
35.6­
39.2
°
F
(
2­
4
°
C)
produced
the
best
survival
(
80%­
95%).
In
studies
on
the
related
species
of
Arctic
char,
Humpesch
(
1985)
reported
optimal
incubation
to
occur
at
41
°
F
(
5
°
C).

In
conclusion,
for
bull
trout,
temperatures
falling
to
48.2
°
F
(
9
°
C)
and
below
may
initiate
spawning,
but
colder
temperatures
during
incubation
and
yolk
absorption
produce
the
largest
size
and
greatest
number
of
fry
(
McPhail
and
Murray
1979).
Although
spawning
tends
to
peak
at
44.6
°
F
(
7
°
C),
water
temperatures
continue
to
decline
as
the
spawning
season
progresses
and
drop
toward
the
optimum
incubation
temperatures
of
35.6­
42.8
°
F
(
2­
6
°
C).
Bull
trout
tend
to
select
redds
directly
adjacent
to
or
below
areas
of
groundwater
upwelling,
resulting
in
relatively
constant
cold
water
temperatures
for
egg
incubation
with
little
diel
fluctuation
(
Baxter
and
Hauer
2000).

Growth.
In
a
laboratory
study
by
McMahon
et
al.
(
1999),
limited
rations
lowered
the
optimal
temperature
for
growth.
For
satiation­
fed
and
66%
of
satiation­
fed
juvenile
bull
trout,
optimum
growth
occurred
at
a
temperature
range
of
53.6­
60.8
°
F
(
12­
16
°
C).
When
energy
availability
was
low
(
one­
third
satiation­
fed
fish),
maximum
growth
occurred
at
lower
temperatures
(
46.4­
53.6
°
F
[
8­
12
°
C]).
In
a
related
species,
Arctic
char,
the
upper
thermal
limits
to
both
feeding
and
growth
were
70.7­
71.2
°
F
(
21.5­
21.8
°
C)
(
Thyrel
et
al.
1999).

In
a
study
analyzing
the
temperature
effects
on
bull
trout
distribution
in
581
sites,
Rieman
and
Chandler
(
1999)
found
that
juvenile/
small
bull
trout
appeared
most
likely
to
occur
at
summer­
mean
temperatures
of
42.8­
48.2
°
F
(
6­
9
°
C)
or
single
maximums
of
51.8­
57.2
°
F
(
11­
14
°
C).
When
given
a
choice
of
temperatures
from
46.4
to
59
°
F
(
8­
15
°
C)
in
a
large
plunge
pool,
juvenile
bull
trout
showed
a
clear
preference
for
the
coldest
water
available
(
6.4­
48.2
°
F
[
8­
9
°
C])
(
Bonneau
and
Scarnecchia
1996).

Migration.
Upstream
spring
migration
of
adult
bull
trout
may
be
related
to
water
temperatures
and
flows.
In
Rapid
River,
Idaho,
a
review
of
trap
counts
and
temperature
for
1985
through
1992
reported
a
general
trend
of
increasing
upstream
bull
trout
counts
as
water
temperatures
reached
50
°
F
(
10
°
C)
(
Elle
et
al.
1994).
McPhail
and
Murray
(
1979)
found
peak
upstream
movement
coincided
with
water
temperatures
of
50­
53.6
°
F
(
10­
12
°
C).

Spawning.
Bull
trout
spawning
areas
are
often
associated
with
cold­
water
springs,
groundwater
infiltration,
and
the
co
ldest
st
reams
in
a
given
watershed
(
Pratt
1992,
Rieman
and
McIntyre
1993,
Rieman
et
al.
1997).
Bull
trout
spawning
is
initiated
as
temperatures
drop
to
48.2
°
F
(
9
°
C)
or
lower,
and
egg
mortality
is
lowest
and
alevin
development
is
strongest
at
colder
temperatures
(
McPhail
and
Murray
1979).
In
Indian
Creek,
tributary
to
the
Yakima
River,
bull
trout
spawning
activity
peaked
when
stream
temperatures
were
42.8­
46.4
°
F
(
6­
8
°
C)
(
James
and
Sexauer
1994).
In
the
North
Fork
Skokomish
River,
bull
trout
spawned
in
October
after
water
temperatures
dropped
below
43.7
°
F
(
6.5
°
C)
(
Brenkman
1998).
Mean
daily
river
temperatures
ranged
from
38.3
to
45.5
°
F
(
3.5­
7.5
°
C)
during
the
remainder
of
the
spawning
period.
This
does
not
differ
significantly
from
descriptions
of
temperatures
initiat
ing
bull
trout
spawning
in
Montana
(
Shepard
et
al.
1982),
Oregon
(
Ratliffe
1992),
or
Washington
(
Kraemer
1994).

Although
spawning
for
bull
trout
may
begin
as
early
as
mid­
August,
spawning
activity
is
reported
to
be
initiated
when
water
temperatures
begin
to
decrease
and
fall
to
48.2
°
F
(
9
°
C)
or
91
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
lower
and
does
not
peak
until
temperatures
fall
below
44.6
°
F
(
7
°
C)
(
McPhail
and
Murray
1979,
Shepard
et
al.
1982,
Kraemer
1994,
Brenkemen
1998).
Kraemer
(
1994)
noted
that
when
stream
temperatures
rise
to
above
46.4
°
F
(
8
°
C)
once
spawning
has
been
initiated,
spawning
usually
stops
or
slows.

Bull
trout
require
a
narrow
range
of
cold
temperatures
to
rear
and
reproduce
and
may
thrive
in
waters
too
cold
for
other
salmonid
species
(
Balon
1980).
McPhail
and
Murray
(
1979)
reported
that
0%­
20%,
60%­
90%,
and
80%­
95%
of
bull
trout
eggs
from
a
British
Columbia
river
survived
to
hatching
at
water
temperatures
of
46.4­
50,
42.8,
and
35.6­
39.2
°
F
(
8­
10,
6,
and
2­
4
°
C),
respectively.
In
Montana,
Weaver
and
White
(
1985)
found
that
39.2­
42.8
°
F
(
4­
6
°
C)
was
needed
for
bull
trout
egg
development.
Buchanan
and
Gregory
(
1997)
defined
a
range
o
f
33.8­
42.8
°
F
(
1­
6
°
C)
that
would
meet
bull
trout
egg
incubation
requirements
in
Oregon.

Although
data
are
not
shown
directly
for
char
species,
other
salmonids
are
known
to
undergo
some
conditioning
in
the
early
stage
of
incubation
that
allows
excellent
survival
at
very
low
temperatures.
Where
conditioning
does
not
occur,
and
t
he
eggs
are
incubated
at
an
early
stage
at
very
low
temperatures,
significant
reductions
in
survival
have
been
noted
(
Murray
and
Beacham
1986,
Seymour
1956).
Thus
even
if
35.6
°
F
(
2
°
C)
is
suboptimal
at
a
constant
incubation
temperature,
natural
seasonal
declines
in
temperature
to
35.6
°
F
(
2
°
C)
in
the
incubation
period
may
not
decrease
survival.
This
assumption
is
supported
by
work
showing
that
newly
hatched
Arctic
char
(
Salvelinus
alpinus)
alevins
are
tolerant
of
temperatures
near
32
°
F
(
0
°
C)
(
Baroudy
and
Elliott
1994)
and
that
the
lower
limit
for
hatching
in
Arctic
char
is
less
than
33.8
°
F
(
1
°
C).

On
the
basis
of
the
information
examined,
the
initiation
of
spawning
behavior
and
in
vivo
egg
development
will
be
fully
supported
by
keeping
maximum
temperatures
in
the
spawning
areas
below
44.6­
46.4
°
F
(
7­
8
°
C)
during
the
spawning
season.
Given
that
excellent
survival
has
been
noted
in
test
s
at
42.8
and
43.7
°
F
(
6
and
6.5
°
C),
that
some
increased
problems
with
disease
may
be
initiated
at
the
higher
end
of
this
range,
and
that
a
variety
of
impacts
to
spawning
have
been
noted
above
44.6
°
F
(
7
°
C),
it
appears
that
constant
or
acclimation
temperatures
in
the
range
of
37.4­
42.8
°
F
(
3­
6
°
C)
are
optimal
for
the
incubation
of
char.
Because
char
are
highly
resistant
to
low
temperatures
and
low
temperatures
discourage
disease
organisms,
water
temperatures
that
swiftly
decline
to
35.6­
39.2
°
F
(
2­
4
°
C)
as
the
incubation
season
progresses
appear
highly
favorable.

What
are
the
therm
al
requirem
ents
for
Lahontan
cutthroat
tro
ut?

Growth.
Laboratory
studies
of
growth
conducted
at
constant
temperatures
showed
that
growth
remained
the
same
at
temperatures
of
55.4,
68,
and
71.6
°
F
(
13,
20,
and
22
°
C)
(
Dickerson
et
al.
1999,
as
cited
in
Dunham
1999).
Growth
was
significantly
reduced
at
75.2
°
F
(
24
°
C).
Tests
done
under
a
fluctuating
temperature
regime
of
68­
78.8
°
F
(
20­
26
°
C)
with
a
daily
mean
of
73.4
°
F
(
23
°
C)
for
1
wk
showed
growth
rates
were
lower
under
this
temperature
regime
than
for
fish
exposed
to
constant
temperatures
of
55
and
68
°
F
(
13
and
20
°
C).
The
growth
rates
under
the
fluctuating
regime
were
similar
to
growth
rates
of
fish
held
at
a
constant
73.4
°
F
(
23
°
C).

Thermal
stress
 
heat
shock
proteins.
Lahontan
cutthroat
trout
begin
to
produce
heat
shock
proteins
immediately
when
exposed
to
78.8
°
F
(
26
°
C)
water
temperature.
Fish
exposed
to
75.2
°
F
(
24
°
C)
water
temperature
began
to
produce
heat
shock
proteins
within
24
h.
Fish
exposed
92
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
to
71.6
°
F
(
22
°
C)
water
temperature
did
not
produce
heat
shock
proteins,
even
after
5
d
of
exposure.

Occurrence.
Dunham
(
1999)
found
that
the
distribution
limit
of
most
Lahontan
populations
corresponded
closely
to
a
maximum
summer
water
temperature
of
78.8
°
F
(
26
°
C).
The
Willow
Creek
population
in
Oregon
occurred
in
water
with
daily
maximum
temperatures
up
to
83
°
F
(
28.4
°
C).

Lethal
effects.
It
has
often
been
assumed
that
Lahontan
cutthroat
trout
have
a
greater
tolerance
for
warm
water
than
other
salmonids
because
of
their
geographic
distribution
in
warm
climates.
Although
there
are
not
abundant
studies
of
Lahontan
cutthroat
thermal
requirements,
good
evidence
indicates
that
this
species
is
comparable
to
other
salmon
and
trout
in
its
response
to
warm
water.

Critical
thermal
maximum
(
CTM)
tests
of
thermal
resistance
were
conducted
on
two
strains
of
Lahontan
cutthroat
t
rout
by
Vigg
and
Koch
(
1980).
The
two
strains
tested
were
Marble
Bluff
and
the
Summit
Lake
strain
found
in
Pyramid
Lake.
The
test
was
designed
to
determine
the
effect
of
alkalinity
on
CTM
values.
In
both
strains
it
was
found
that
as
alkalinity
increased
from
69
to
1,487
mg/
L,
the
CTM
decreased.
Average
CTM
values
determined
for
the
death
(
D)
temperature
endpoint
were
approximately
72.3­
67.2
°
F
(
22.4­
19.6
°
C)
over
this
alkalinity
range
(
average
values
for
the
two
strains).
This
CTM
study
employed
a
stepped
temperature
increase
equal
to
1.8
°
F
(
1
°
C)/
d
up
to
an
exposure
temperature
of
68
°
F
(
20
°
C),
starting
from
an
acclimation
temperature
of
60.8
°
F
(
16
°
C).
After
68
°
F
(
20
°
C)
was
reached,
the
increments
were
1.8
°
F
(
1
°
C)/
4d.
Because
of
the
stepped
increases
and
the
two
different
rates
of
heating,
the
study
methodology
is
not
completely
analogous
to
conventional
CTM
technique.
The
initial
period
of
increase
to
68
°
F
(
20
°
C),
however,
could
be
considered
to
provide
nearly
full
acclimation
(
given
a
4­
d
acclimation
at
each
step)
before
the
subsequent
heating
schedule.
The
temperature
increase
rates
for
the
two
exposure
periods
averaged
approximately
0.04
°
C/
h
and
0.01
°
C/
h,
respectively
(
averaging
the
thermal
increase
over
the
step
time
interval).
CTM
test
s
provide
results
that
have
a
different
meaning
from
UILT
test
results.
Comparison
of
CTM
values
for
other
salmonids
that
have
corresponding
UILT
values
is
useful
to
understand
the
relative
thermal
tolerance
of
Lahontan
cutt
hroat
.
For
example,
appropriate
comparisons
of
CTM
values
among
species
can
be
made
by
contrasting
the
Lahontan
results
with
CTM
values
for
salmonids
whose
temperature
increase
rates
are
0.018­
0.14
°
F
(
0.01­
0.08
°
C)/
h
and
starting
from
acclimation
temperatures
of
60.8­
68
°
F
(
16­
20
°
C)
(
McCullough
1999).
Grande
and
Anderson
(
1991)
measured
a
CTM
of
79.3
°
F
(
26.3
°
C)
for
2­
to
3­
month­
old
rainbow
trout,
81
°
F
(
27.2
°
C)
for
3­
to
4­
month­
old
brook
trout,
and
78.6
°
F
(
25.9
°
C)
for
2­
t
o
4­
month­
old
lake
trout.
Elliott
and
Elliott
(
1995)
reported
CTM
of
81.9
°
F
(
27.74
°
C)
for
Atlantic
salmon
and
76.6
°
F
(
24.8
°
C)
for
brown
trout.
The
Lahontan
cutthroat
studies
reported
CTM
for
a
death
endpoint;
the
Grande
and
Anderson
studies
also
used
a
death
endpoint.
If
a
loss
of
equilibrium
(
LE)
endpoint
is
used
to
record
CTM,
the
crit
ical
temperature
is
generally
slightly
lower
than
if
a
death
endpoint
is
used.
For
example,
at
a
heating
rate
of
1.8
°
F
(
1
°
C)/
h,
Becker
and
Genoway
(
1979)
measured
a
CTM
for
coho
salmon
as
81.8
and
81.7
°
F
(
27.7
and
27.6
°
C)
for
the
LE­
and
death­
temperature
endpoints,
respectively.
However,
at
a
64.4
°
F
(
18
°
C)/
h
heating
rate,
these
values
were
83.6
and
85.4
°
F
(
28.7
and
29.7
°
C),
respectively.
In
conclusion,
the
CTM
values
for
Lahontan
cutthroat
trout,
compared
with
other
salmonids
tested
in
a
similar
manner
(
i.
e.,
rainbow
trout,
brook
trout,
lake
trout,
Atlantic
salmon,
brown
trout),
are
93
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
much
lower.
UILT
values
determined
in
other
studies
(
see
Table
4)
for
all
the
species
that
were
contrasted
above
with
Lahontan
ranged
from
73.4
to
79.5
°
F
(
23­
26.4
°
C).
Using
CTM
data
as
a
guide,
these
results
appear
t
o
indicate
that
Lahontan
cutthroat
would
likely
have
lower
UILT
values
than
these
other
salmonids.

Dickerson
and
coworkers
(
1999,
and
unpublished
data,
in
Dunham
1999)
found
in
laboratory
tests
at
constant
temperatures
that
survival
was
100%
at
75.2
°
F
(
24
°
C)
but
dropped
to
35%
at
78.8
°
F
(
26
°
C).
Tests
done
under
a
fluctuating
temperature
regime
of
68­
78.8
°
F
(
20­
26
°
C)
with
a
daily
mean
of
73.4
°
F
(
23
°
C)
for
1
wk
showed
no
mortality
even
though
this
regime
provided
1­
h/
d
exposure
to
78.8
°
F
(
26
°
C)
for
7
consecutive
days,
a
temperature
that
produced
mortality
during
longer
exposures
(
Dickerson
and
Vinyard
1999).
These
data
indicate
that
the
UILT
is
probably
between
77
and
78.8
°
F
(
25
and
26
°
C).
However,
temperature
adjustment
rates,
starting
from
an
initial
temperature
of
55.4
°
F
(
13
°
C),
were
7.2
°
F/
d
(
4
°
C/
d)
up
to
the
test
temperature.
That
is,
a
conventional
time
period
for
acclimation
was
not
allowed
prior
to
the
final
exposure
temperature.
This
could
result
in
a
slight
underprediction
of
UUILT.

What
are
the
therm
al
requirem
ents
for
w
estslope
cu
tthroat
trout?

Incubation
and
egg
survival.
In
a
study
by
Shepard
et
al.
(
1982),
westslope
cutthroat
trout
in
the
Flathead
River
basin,
Montana,
emerged
in
July
and
August
following
incubation
temperatures
ranging
from
35.6
to
50
°
F
(
2­
10
°
C).
Fry
were
approximately
20
mm
long
at
emergence.
Adult
westslope
cutthroat
trout
held
in
cool
35.6­
39.2
°
F
(
2­
4
°
C)
water
temperatures
produced
more
viable
eggs
than
those
held
in
constant
water
temperatures
of
50
°
F
(
10
°
C)
(
Smith
et
al.
1983,
in
Shepard
et
al.
1982).

Growth.
Westslope
cutthroat
streams
are
typically
cold,
nutrient­
poor
waters
in
which
conditions
for
growth
tend
to
be
less
than
optimal
(
Liknes
and
Graham
1988).

Spawning.
Initiation
and
timing
of
spawning
activity
is
related
to
water
temperatures.
Adults
move
into
tributaries
during
high
streamflows
and
spawn
in
the
spring
when
water
temperatures
are
near
50
°
F
(
10
°
C)
(
Scott
and
Crossman
1973).

Occurrence.
Westslope
cutthroat
trout
and
bull
trout
have
similar
life
history
patterns,
often
occupy
the
same
headwater
streams,
and
restrict
themselves
to
the
coldest
sections
of
streams
(
Jakober
et
al.
1998,
Behnke
1992).
Westslope
trout
prefer
cooler
water
temperatures
than
do
both
brook
trout
and
Yellowstone
cutthroat
trout
(
B.
Shepard,
personal
communication).

Westslope
cutthroat
trout
and
redband
trout
may
occur
in
the
same
system.
They
can
be
allopatric
or
sympatric,
but
the
redband
generally
inhabit
lower
reaches
and
cutthroat
trout
(
often
with
bull
trout)
dominate
the
upper,
higher
gradient
sections
where
annual
temperature
units
are
considerably
less
(
Mullan
et
al.
1992).

What
are
the
therm
al
requirem
ents
for
redband
trou
t?

Growth
and
feeding.
Dwyer
et
al.
(
1986)
conducted
temperature
experiments
at
39.2,
44.6,
50,
60.8,
and
66.2
°
F
(
4,
7,
10,
13,
16,
and
19
°
C)
on
rainbow
trout
and
redband
trout
94
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
collected
from
Threemile
Creek,
Catlow
Basin.
Redband
trout
from
Threemile
Creek
showed
the
best
growth
at
66.2
°
(
19
°
C)
(
no
higher
temperatures
were
tested),
whereas
rainbow
trout
exhibited
the
best
growth
at
59­
60.8
°
F
(
15­
16
°
C).

In
a
study
by
Sonski
(
1982,
as
cited
by
Sonski
1983b),
redband
trout
reached
their
maximum
growth
rate
at
68
°
F
(
20
°
C).
Growth
rates
were
less
at
both
59
°
F
(
15
°
C)
and
73
°
F
(
22.8
°
C).

Redband
trout
are
thought
to
exhibit
the
upper
limit
for
feeding
response
for
all
salmonids
of
the
Pacific
Northwest.
No
feeding
was
observed
by
Sonski
(
1982
as
cited
by
Sonski
1984)
for
juvenile
redband
at
temperatures
above
77.9­
80.6
°
F
(
25.5­
27
°
C).
In
a
comparison
of
thermal
tolerance
by
three
rainbow
trout
species,
Sonski
(
1984)
found
that
no
redband
trout
or
Wytheville
rainbow
fed
at
temperatures
higher
than
78.8
°
F
(
26
°
C),
and
the
Firehole
River
rainbow
would
not
feed
beyond
80
°
F
(
26.7
°
C).

Metabolic
activity
and
swimming
speed.
Gamperl
(
in
litt.)
conducted
temperature
studies
in
Bridge
Creek
("
warm"
stream)
and
Little
Blitzen
River
("
cold"
stream)
in
the
Harney
basin.
Gamperl's
studies
found
that
despite
the
two
streams'
different
thermal
histories,
redband
trout
from
each
stream
exhibited
a
similar
preferred
temperature
of
55
°
F
(
12.8
°
C).
Bridge
Creek
trout
had
greater
metabolic
power
and
improved
swimming
efficiency
at
75.2
°
F
(
24
°
C)
than
at
53.6­
57.2
°
F
(
12­
14
°
C)
compared
with
the
Little
Blitzen
River
redband,
which
had
similar
values
for
metabolic
power
and
swimming
performance
at
53.6­
57.2
°
F
(
12­
14
°
C)
and
75.2
°
F
(
24
°
C).
Gamperl
concluded
that
some
populations
of
redband
trout
can
tolerate,
and
may
have
adapted
to,
warm
environmental
temperatures.
However,
these
studies
should
be
taken
as
preliminary
because
they
were
not
replicated.

Occurrence.
There
are
observations
of
redband
trout
feeding
and
surviving
at
relatively
high
temperatures
for
a
salmonid
(
82.4
°
F
[
28
°
C],
Behnke
1992;
81.3
°
F
[
27.4
°
C]
Sonski
1986;
80.6
°
F
[
27
°
C]
Bowers
et
al.
1979),
although
it
is
unclear
whether
temperatures
were
measured
in
the
vicinity
of
the
stream
that
the
fish
actually
inhabited.
These
trout
may
rely
on
microhabitats
or
thermal
refuges
to
maintain
populations
in
desert
environments
(
see
Ebersole
et
al.
in
press).

Lethal
effects.
In
a
comparison
of
thermal
resistance
among
redband
trout,
Firehole
River
rainbow,
and
Wytheville
rainbow,
Sonski
(
1984)
found
very
little
difference.
He
measured
UILT
values
for
subyearling
trout
acclimated
at
73.4
°
F
(
23
°
C)
of
79.1,
79.3,
and
80.6
°
F
(
26.2,
26.3,
and
27.0
°
C),
respectively.
These
values
are
probably
equivalent
to
UUILT
values
because
it
appears
that
resistance
was
not
improved
by
acclimation
beyond
59
°
F
(
15
°
C).
It
is
interesting
that
redband
trout
were
not
significantly
different
in
their
thermal
tolerance
from
other
rainbow
stocks,
despite
their
reputation
as
being
tolerant
of
higher
water
temperatures.
95
Summary
of
Technical
Literature
Examining
the
Physiological
Effects
of
Temperature
LITERATURE
CITED
Adams
BL,
Zaugg
WS,
McLain
LR.
1975.
Inhibition
of
salt
water
survival
and
Na­
K­
ATPase
elevation
in
steelhead
trout
(
Salmo
gairdneri)
by
moderate
water
temperatures.
Trans
Am
Fish
Soc
104(
4):
766­
769.

Adams
BL,
Zaugg
WS,
McLain
LR.
1973.
Temperature
effect
on
parr­
smolt
transformation
in
steelhead
trout
(
Salmo
gairdneri)
as
measur
ed
by
gill
sodium­
pota
ssium
stim
ulated
adenosine
tr
iphosphatase.
Comp
Biochem
Physiol
44A:
1333­
1339.

Alabaster
JS.
1988.
The
dissolved
oxygen
requirements
of
upstream
migrant
chinook
salmon,
Oncorhynchus
tshawytscha,
in
the
lower
Willamette
River,
Oregon.
J.
Fish
Biol
32:
635­
636.

Alcorn
SR.
1976.
Temperature
tolerances
and
upper
lethal
lim
its
of
Salmo
apache.
Trans
Am
Fish
Soc
105(
2):
294­
295.

Alderdice
DF,
Velsen
FPJ.
1978.
Relation
between
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