United
States
Environmental
Protection
Agency
EPA­
910­
D­
01­
004
May
2001
Issue
Paper
4
Temperature
Interaction
Prepared
as
Part
of
EPA
Region
10
Temperature
Water
Quality
Criteria
Guidance
Development
Project
Elizabeth
Materna,
U.
S.
Fish
and
Wildlife
Service
Temperature
Interaction
Contents
Abstract
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1
Introduction
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1
What
is
stress
and
how
are
fish
affected
by
it?
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2
Why
are
these
interactions
important
to
consider
in
developing
a
temperature
criterion?
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3
How
do
these
interactions
affect
salmonids?
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3
Can
you
describe
a
situation
in
which
a
fish
is
facing
multiple
stressors?
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3
What
physical
aspects
of
aquatic
ecosystems
are
influenced
by
temperature
or
influence
temperature?
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3
Density
and
viscosity
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4
Depth
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4
Stream
flow
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4
Suspended
sediment
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4
How
are
chemical
constituents
affected
by
temperature?
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5
Dissolved
oxygen
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5
pH
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7
Hardness
and
alkalinity
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7
Chemical
toxicity
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7
Ammonia
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8
Organics
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9
Metals
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9
Cyanide
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11
Chlorine
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11
Nitrogen
supersaturation
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11
What
aspects
of
salmonid
biology
are
influenced
by
temperature?
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11
Competition
and
predation
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11
Disease
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11
What
factors
are
involved
in
infection
by
disease?
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12
Are
warm­
water
vectors
of
disease
present
in
rivers
of
the
Pacific
Northwest?
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12
Is
just
a
single
life
stage
susceptible
to
disease?
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13
Wouldn't
disease
be
obvious
in
salmon
if
it
were
present?
Wouldn't
dead
fish
be
noticeable
if
this
were
a
problem?
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13
What
are
some
modes
of
infection?
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14
Has
infection
with
warm­
water
diseases
been
documented
historically
in
streams
of
the
region?
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14
Are
warm­
water
disease
outbreaks
in
salmonids
a
thing
of
the
past?
Has
infection
with
warm­
water
diseases
been
documented
recently
in
streams
of
the
region?
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15
What
is
the
relationship
between
increasing
temperature
and
columnaris
disease?
Are
there
any
apparent
critical
temperature
thresholds?
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16
Rate
of
infection
increases
with
temperature
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16
Migration
effects
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16
Holding
effects
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17
Temperature
Interaction
Juvenile
survival
rate
decreases
with
increasing
temperature
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17
Time
to
death
decreases
with
increasing
temperature
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17
Are
other
salmon
diseases
of
warm
water
similar
to
columnaris
in
their
temperature­
survival
relationships?
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18
What
is
the
relationship
between
disease
and
stress?
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18
How
does
temperature
affect
immune
response?
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23
Does
temperature
influence
the
impact
of
angling
pressure?
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23
Is
growth
affected
by
temperature
changes?
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23
What
is
the
importance
of
temperature
to
salmonid
food
resources?
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24
How
does
temperature
affect
photobiology?
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25
How
well
are
these
interactive
relationships
understood?
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25
What
is
the
likelihood
of
exposure
of
salmonids
to
multiple
stressors?
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25
What
other
complexities
of
multiple
stressors
need
to
be
considered?
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26
Have
any
States
addressed
these
temperature
relationships
within
their
water
quality
criteria?
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27
What
tools
are
available
to
help
evaluate
these
multiple
stressors
and
the
effects
to
salmonid
populations?
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27
Conclusions
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27
Literature
Cited
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28
1
Temperature
Interaction
Issue
Paper
4
Temperature
Interaction
Prepared
as
Part
of
Region
10
Temperature
Water
Quality
Criteria
Guidance
Development
Project
Elizabeth
Materna
Abstract
Pacific
Northwest
salmon
rely
on
many
interwoven
factors
to
maintain
their
health,
wellbeing
population,
and
distribution.
Abnormal
conditions
in
a
fish's
environment
may
elicit
a
stress
response.
If
a
fish
is
already
responding
to
one
stressor,
it
is
less
likely
to
withstand
another.
Temperature
can
be
a
biological,
physical,
or
chemical
stressor.
Biologically,
temperature
affects
the
metabolism
of
fish
and
their
ability
to
resist
disease.
Physically,
temperature
affects
properties
of
water
and
fishes'
tolerance
to
suspended
sediment.
Chemically,
temperature
can
change
the
concentration
of
substances
in
water
and
reduce
a
fish's
ability
to
withstand
chemical
exposure.
Not
all
these
relationships
are
well
understood,
but
they
need
to
be
considered
when
developing
a
temperature
standard.
This
issue
paper
reviews
biological,
physical,
and
chemical
properties
related
to
temperature
within
salmonid
ecosystems.

Introduction
An
ecological
system
is
a
complex
relation
of
numerous
interconnected
physical,
chemical,
and
biological
processes
occurring
simultaneously.
These
processes,
which
profoundly
influence
the
structure
and
function
of
an
ecosystem,
are
strongly
affected
by
temperature.
Animals
within
an
ecosystem
are
exposed
to
these
processes,
some
of
which
may
be
stressful.
A
stressor
can
generally
be
described
as
any
physical,
chemical,
or
biological
entity
that
can
produce
an
adverse
response.
This
paper
focuses
on
multiple
interactions
that
can
create
stress
for
fish.

Temperature
has
a
vital
role
in
various
processes
that
help
determine
whether
a
watershed
is
suitable
for
fish.
These
include
aquatic
plant
photosynthesis
and
respiration,
chemical
reaction
rates,
gas
solubilities,
and
microbially
mediated
processes.
Temperature
also
is
important
in
controlling
almost
all
processes
in
fish
(
Jensen
et
al.
1993),
both
physiological
and
behavioral
(
see
Behavior
and
Physiology
issue
papers).

Because
temperature
has
such
far­
reaching
influence,
interrelated
parameters
must
be
considered
in
developing
a
water
quality
criterion
for
temperature.
These
temperature
interactions
are
discussed
below
in
the
following
questions
and
answers.
2
Temperature
Interaction
What
is
stress
and
how
are
fish
affected
by
it?

Wedemeyer
and
McLeay
(
1981)
define
a
stressor
as
an
environmental
change
severe
enough
to
require
a
physiological
response
on
the
part
of
a
fish,
population,
or
ecosystem.
Adaptation
will
occur
if
the
stress
response
can
reestablish
a
satisfactory
relationship
between
the
changed
environment
and
the
ecosystem.
Acclimation
can
be
said
to
have
occurred
if
the
compensatory
stress
response
enables
a
restoration
of
physiological
variables
to
within
limits
that
do
not
compromise
survival
(
Jobling
1994).

A
wide
range
of
biological,
chemical,
and
physical
factors
can
challenge
the
physiological
systems
of
fish.
Various
stressors
such
as
handling,
fright,
forced
swimming,
anesthesia,
rapid
temperature
changes,
and
scale
loss
all
elicit
a
stress
response
characterized
by
physiological
changes,
which
tend
to
be
similar
for
all
stressors
(
Wedemeyer
and
McLeay
1981).
The
stress
response
proceeds
as
follows:
the
central
nervous
system
triggers
the
release
of
stress
hormones
(
i.
e.,
corticosteroids),
changes
occur
in
blood
chemistry
and
hematology
(
i.
e.,
reduced
blood
clotting
time),
and
metabolism
may
be
altered,
which
in
turn
can
result
in
tissue
changes
(
nitrogen
balance
and
oxygen
debt)
followed
by
loss
of
electrolytes
(
Wedemeyer
and
McLeay
1981).
These
responses
are
expressed
through
changes
in
predator
avoidance,
growth,
parr­
smolt
transformation,
spawning
success,
migratory
behavior,
and
incidence
of
disease.
There
also
is
a
reduction
in
tolerance
to
subsequent
stressors
(
Wedemeyer
and
McLeay
1981).
At
the
population
level,
stress
response
may
reduce
recruitment
and
species
abundance
and
diversity.

Chronic
exposure
to
these
sublethal
stressors
can
result
in
reduced
reproductive
success
or
decreased
survival
of
individuals,
which
may
endanger
the
survival
of
entire
populations
(
Jobling
1994).
Thus,
the
success
of
fish
and
fish
populations
in
acclimating
to
environmental
changes
depends
on
the
compensatory
abilities
of
individual
organisms.

A
fish's
tolerance
to
environmental
alterations
depends
on
its
ability
to
regulate
stabilizing
processes
either
physiologically
or
behaviorally
(
see
Physiology
and
Behavior
issue
papers).
Single
or
multiple
stressors
requiring
adjustments
that
are
beyond
the
fish's
ability
will
eventually
be
lethal,
either
directly
or
indirectly,
through
secondary
processes
such
as
disease.

The
stress
response
is
usually
considered
in
terms
of
primary,
secondary,
and
tertiary
changes,
starting
at
the
endocrine
system
and
concluding
at
the
organismal
level.
Jobling
(
1994)
describes
a
characteristic
series
of
responses
divided
into
three
stages:
(
1)
alarm,
which
is
the
onset
of
compensation
through
initiation
of
physiological
changes
and
homeostatic
control
systems;
(
2)
resistance,
the
successful
restoration
of
physiological
balance,
albeit
with
reduced
performance
capacity;
and
(
3)
exhaustion,
or
biological
tolerance
limits
being
exceeded
as
a
result
of
exposure
to
the
stressors.

To
persist
and
ultimately
reproduce,
fish
need
to
perform
such
necessary
activities
as
obtaining
oxygen,
swimming,
metabolizing,
and
resisting
pathogens.
The
fish's
potential
capacity
to
carry
out
these
activities
is
determined
by
genes
and
developmental
changes
(
Schreck
1981).
Stress
places
a
physiological
load
on
the
fish,
thereby
reducing
its
capacity
to
cope
with
subsequent
stresses
(
Schreck
1981).
The
appropriate
recovery
time
depends
on
the
severity
and
duration
of
the
initial
stress
and
on
habitat
conditions.
3
Temperature
Interaction
Why
are
these
interactions
important
to
consider
in
developing
a
temperature
criterion?

To
produce
a
temperature
criterion
that
ensures
protection
and
management
of
aquatic
ecosystems,
we
must
understand
the
way
in
which
different
variables
affect
interactions
among
organisms
and
their
aquatic
environment.
Interactions
are
influenced
by
variables
that
can
alter
the
organism's
physiological
condition
or
the
physicochemical
characteristics
of
the
system.
Temperature
may
have
the
most
far­
reaching
influence
of
the
many
water­
quality
variables.

How
do
these
interactions
affect
salmonids?

For
each
natural
characteristic
of
water,
such
as
temperature,
there
is
an
optimal
zone
for
a
given
species
where
the
species
functions
most
efficiently.
If
the
characteristic
becomes
less
favorable,
the
organism
usually
has
physiological
processes
that
allow
it
to
partially
compensate,
but
at
some
metabolic
cost.
The
change
may
be
semipermanent,
in
which
case
the
animal
has
acclimated
to
the
new
condition.
For
example,
fish
held
at
higher
than
normal
temperature
show
an
increase
in
upper
lethal
temperature
and
may,
for
a
while,
prefer
a
temperature
above
the
one
they
normally
select.
Near
the
outer
limits
of
the
fish's
range,
the
metabolic
load
on
the
organism
becomes
greater,
reducing
its
capacity
to
carry
out
normal
activities
such
as
feeding
and
reproduction.
The
implications
of
these
environmental
conditions
are
quite
predictable.
If
an
organism
is
already
under
stress
or
metabolic
loading
from
increased
water
temperature,
when
faced
with
an
added
stressor
(
e.
g.,
toxic
pollutant,
disease),
it
would
probably
be
less
capable
of
dealing
with
it
and
show
greatly
increased
susceptibility.
Under
these
conditions,
temperature
may
be
a
factor
modifying
the
response
of
the
fish
(
Rand
and
Petrocelli
1984).

Synergistic
interactions
occur
among
the
many
factors
that
make
up
the
environment
of
a
fish.
The
physiological
and
behavioral
condition
of
a
fish
are
very
important
to
its
ability
to
withstand
temperature
extremes
(
Paladino
et
al.
1980).
A
fish
that
is
stressed
by
sublethal
levels
of
a
toxicant
or
by
a
disease
may
have
a
much
lower
temperature
tolerance
than
a
healthy
fish
of
the
same
age,
sex,
and
species.

Can
you
describe
a
situation
in
which
a
fish
is
facing
multiple
stressors?

A
fish
population
that
has
recently
been
exposed
to
a
prolonged
series
of
high­
temperature
days
is
an
example
of
a
situation
involving
multiple
stressors.
After
a
long
period
of
inadequate
food
intake,
high
metabolic
costs,
and
lack
of
growth,
which
could
result
from
exposure
to
high
temperatures,
the
population
may
be
weakened
from
energy
depletion.
Subsequently,
fish
may
be
more
susceptible
to
disease,
because
many
diseases
attack
fish
that
are
already
weakened
from
some
other
stress.

What
physical
aspects
of
aquatic
ecosystems
are
influenced
by
temperature
or
influence
temperature?

Physical
aspects
of
aquatic
ecosystems
that
are
influenced
by
temperature
or
influence
temperature
include
density
and
viscosity,
current,
depth,
stream
flow,
and
suspended
sediment.
These
are
discussed
below.
4
Temperature
Interaction
Density
and
viscosity.
The
density,
or
mass
per
unit
volume,
of
liquid
water
is
affected
by
temperature
(
Gordon
et
al.
1992).
Water
reaches
maximum
density
at
39.2
°
F
(
4
°
C)
under
normal
atmospheric
pressure.
As
water
temperature
increases
above
39.2
°
F
(
4
°
C),
water
density
decreases.
Water
density
also
decreases
as
temperature
decreases
below
39.2
°
F
(
4
°
C),
until
the
freezing
point
is
reached.
Upon
freezing
it
becomes
considerably
less
dense
as
a
solid
than
as
a
liquid.

Viscosity
is
the
property
of
a
fluid
that
describes
how
rapidly
it
can
be
deformed,
or
the
relative
rate
with
which
a
fluid
can
pour
out
of
a
jar.
Water
viscosity
is
strongly
temperature
dependent,
and
as
temperature
increases
viscosity
decreases
(
Gordon
et
al.
1992).

How
would
a
change
in
water
density
and
viscosity
translate
as
an
expression
in
the
aquatic
ecosystem
and
salmonid
populations?
A
temperature
increase
would
lead
to
decrease
in
water
density
and
viscosity,
and
possibly
a
more
rapid
settling
of
the
suspended
sediment
particles
within
a
stream.
Decreases
in
density
and
viscosity
cause
an
increase
in
the
settling
speed
of
suspended
particles
(
Hodges
1977).

The
distribution
of
sediment
sizes
along
a
stream
is
one
of
the
physical
habitat
factors
influencing
the
distribution
of
organisms
(
Gordon
et
al.
1992).
Species
differ
in
their
substrate
preferences
and
requirements.
When
gravel­
bed
streams
fill
with
silt,
for
example,
they
may
show
a
shift
in
insect
species
composition
that,
in
turn,
can
affect
fish
species
composition.
Infilling
of
gravels
with
finer
sediments
can
reduce
intergravel
flow
rates,
suffocate
eggs,
limit
burrowing
activity,
and
trap
emerging
young.

Even
so,
density
and
viscosity
changes
associated
with
altered
temperature
regimes
are
generally
not
considered
to
have
a
major
impact
on
salmonids
or
their
habitats.

Depth.
Water
depth
has
an
influence
on
water
temperature,
because
shallow
water
tends
to
heat
up
and
cool
down
more
rapidly
(
Gordon
et
al.
1992).

Stream
flow.
Because
streamflows
normally
decrease
during
the
summer
months
in
most
portions
of
the
Pacific
Northwest,
temperature
and
salinity
levels
may
rise
and
plant
growth
within
the
channel
can
increase
(
Gordon
et
al.
1992).
Some
species
may
rely
on
low­
flow
periods
for
a
part
of
their
life
history,
but
others
experience
stress
during
this
time.
During
times
of
low
flow
when
the
stream
may
be
confined
to
limited
areas,
increasing
predation
and
competition
for
nutrients
and
space
occur
within
the
remaining
waters.
Generally,
the
concentration
of
dissolved
ions
in
water
(
salinity)
is
inversely
related
to
discharge
levels,
with
the
highest
salinities
during
low
flows
and
higher
flows
having
a
diluting
effect.
As
with
other
factors,
tolerance
of
saline
conditions
can
influence
the
distribution
and
abundance
of
stream
inhabitants.

Suspended
sediment.
In
coho
salmon,
temperature
is
an
influencing
factor
for
level
of
tolerance
to
suspended
sediments.
To
study
this,
scientists
look
at
median
lethal
concentration
(
or
LC50),
which
is
the
concentration
in
water
to
which
test
organisms
are
exposed
that
is
estimated
to
be
lethal
to
50%
of
the
test
organisms.
The
96­
hr
LC50
of
yearling
coho
exposed
to
suspended
fine
sediment
from
the
Fraser
River
(
75
µ
m
median
diameter)
decreased
when
5
Temperature
Interaction
temperature
was
increased
(
Servizi
and
Martens
1991).
Fish
at
44.6
°
F
(
7
°
C)
had
the
greatest
resistance
(
i.
e.,
tolerance
decreased)
to
suspended
sediment
concentrations,
with
a
96­
hr
LC50
of
23
mg/
L.
The
temperature
increase
resulted
in
tolerance
of
suspended
sediment
being
33%
less
at
64.4
°
F
(
18
°
C)
than
at
44.6
°
F
(
7
°
C).
Very
low
temperature
was
also
found
to
decrease
the
fish's
tolerance.
Reduced
tolerance
to
suspended
sediments
at
low
temperatures
may
be
primarily
related
to
the
capacity
of
the
fish
to
maintain
the
cough
reflex
and
ventilation
rates
that
are
adequate
to
clear
the
gills
of
particles.

How
are
chemical
constituents
affected
by
temperature?

Temperature
affects
the
following
constituents
of
water:
dissolved
oxygen,
pH,
hardness
and
alkalinity,
chemical
toxicity,
ammonia,
organics,
metals,
cyanide,
chlorine,
and
nitrogen.
Each
constituent
is
discussed
below.

Dissolved
oxygen.
The
solubility
of
oxygen
in
water
is
directly
proportional
to
the
temperature
(
Hutchinson
1957).
Solubility
of
oxygen
decreases
in
a
nonlinear
manner
with
increasing
temperature
(
Figure
1).

There
is
an
important
relationship
between
temperature
and
the
dissolved
oxygen
(
DO)
needs
of
fish.
As
temperature
increases,
metabolic
rates
increase,
increasing
the
demand
for
oxygen
by
an
organism.
At
the
same
time,
the
DO
available
to
the
organism
decreases.
Therefore,
at
times
of
the
year
when
fish
may
experience
temperature
stress
they
also
may
experience
stress
from
low
DO
levels.

Aquatic
organisms
are
more
likely
to
experience
respiratory
distress
in
warm
water
than
in
cool
water.
Active
fish
who
live
in
cold
water,
such
as
trout,
experience
a
sharp
rise
in
respiratory
rate
at
temperatures
above
59
°
F
(
15
°
C).
This
is
the
principal
reason
their
growth
rate
Figure
1.
Oxygen
saturation
concentrations
(
mg/
L)
at
various
temperatures
(
°
C).
Derived
from
Hodges
(
1977).
6
Temperature
Interaction
declines
at
higher
temperatures
even
when
they
are
fed
to
excess
(
Elliott
1978,
as
cited
in
Allen
1995).
The
need
to
live
in
cold
water
of
such
species
can
be
attributed
as
much
to
the
effects
of
oxygen
availability
at
higher
temperatures
as
to
temperature
itself
(
Hynes
1970,
as
cited
in
Allen
1995).

Chinook
salmon
require
certain
conditions
of
temperature
and
DO
for
migration.
When
these
conditions
are
not
met,
adult
migration
is
prevented
(
McCullough
1999).
In
the
Willamette
River,
a
combination
of
average
daily
minimum
DO
of
3.3
mg/
L
and
an
average
daily
maximum
water
temperature
of
72.3
°
F
(
22.4
°
C)
resulted
in
cessation
of
upstream
migration
of
spring
chinook
past
Willamette
Falls
(
Alabaster
1988).
Data
from
Hallock
et
al.
(
1970)
collected
in
the
San
Joaquin
Delta
showed
that
the
average
minimum
DO
at
which
chinook
migrate
while
avoiding
temperatures
>
66
°
F
(
18.9
°
C)
was
about
4.2
mg/
L.
Although
combinations
of
temperature
and
DO
that
result
in
no
adult
migration
do
not
indicate
that
adults
died,
these
conditions
at
least
cause
stress
and
probable
deterioration
in
condition,
and
also
reduce
spawning
success.

If
higher
DO
levels
or
colder
temperatures
are
available
to
fish,
negative
effects
of
other
variables
could
be
tempered.
A
study
conducted
in
Montana
(
Feldmeth
and
Eriksen
1978)
found
that
where
grayling
distribution
in
Odell
Lake
extended
to
deep
portions
of
the
lake
in
which
water
temperatures
were
very
cold
(
39.2­
41
°
F
[
4­
5
°
C]),
the
fish
did
not
experience
equilibrium
loss
until
DO
concentrations
dropped
to
very
low
levels
(
1.6
mg/
L).
More
evidence
that
DO
mitigates
negative
thermal
effects
is
suggested
by
Erman
and
Leidy
(
1975),
who
documented
that
trout
fry
can
exist
in
isolated
pools
with
temperatures
as
high
as
72.3
°
F
(
22.4
°
C).
They
attribute
this
to
the
presence
of
DO
in
groundwater
seeping
into
the
pool,
producing
oxygen
concentrations
of
3.5
mg/
L.
These
fish
also
swam
near
the
surface
to
maximize
oxygen
uptake.

EPA
(
1986),
in
its
Ambient
Water
Quality
Criteria
for
DO
guidance,
described
a
study
by
Warren
et
al.
(
1973)
that
indicates
growth
of
salmonids
is
most
susceptible
to
the
effects
of
low
DO
concentrations
when
the
metabolic
demands
or
opportunities
are
greatest.
This
is
demonstrated
by
greater
sensitivity
of
growth
to
low
DO
concentrations
when
temperatures
are
high,
even
with
plentiful
food.
The
greatest
effects
and
highest
thresholds
of
effect
within
the
growth
data
occurred
at
high
temperatures
(
64­
71.1
°
F
[
17.8­
21.7
°
C]).
Growth
data
from
chinook
salmon
tests
indicate
that
growth
tests
conducted
at
50­
59
°
F
(
10­
15
°
C)
would
underestimate
the
effects
of
low
DO
concentrations
at
higher
temperatures
by
a
significant
margin.
For
example,
at
5
mg/
L
DO,
growth
was
not
affected
at
55.4
°
F
(
13
°
C),
but
at
temperatures
of
68
°
F
(
20
°
C)
growth
was
reduced
by
34%.
Results
from
coho
tests
also
support
the
idea
that
effects
of
low
DO
become
severe
at
higher
temperatures.

Fish
may
be
able
to
adjust
their
behavior
to
compensate
for
low
DO
levels.
Fish
confronted
with
hypoxia
(
deficiency
of
oxygen
reaching
body
tissue)
are
able
to
change
activity
level
or
location
in
a
thermal
gradient
as
a
means
of
adjusting
metabolic
rate.
The
final
temperature
preference
for
rainbow
trout
under
lowered
oxygen
conditions
was
significantly
lower
than
under
normal
oxygen
(
Schurmann
et
al.
1991).
It
is
to
the
fish's
physiological
advantage
to
select
a
lower
temperature
in
a
hypoxic
environment,
as
the
decrease
in
temperature
leads
to
a
reduced
metabolic
rate
and
a
higher
blood
oxygen
affinity
(
see
Behavior
issue
paper).
7
Temperature
Interaction
pH.
The
modulating
effect
of
temperature
on
pH
primarily
occurs
under
both
acidic
and
alkaline
conditions.
Under
acidic
conditions,
Robinson
et
al.
(
1976)
found
that
the
higher
the
temperature
(
39.2,
57.2,
and
69.8
°
F
[
4,
14,
and
21
°
C]),
the
shorter
the
survival
time
for
brook
trout
in
a
lethal
pH
environment.
The
authors
ascribe
this
to
the
elevation
of
metabolic
functions
in
cold­
blooded
organisms
held
in
a
warm
environment.
Such
an
increase
in
metabolic
demands
would
multiply
the
burden
of
physiological
stress
from
low
pH
conditions.
Temperature
also
is
significant
in
the
tolerance
of
rainbow
trout
to
acidic
conditions.
Kwain
(
1975)
tested
rainbow
trout
embryos
and
found
that
at
a
given
pH
level
the
lowest
mortality
occurred
at
50
°
F
(
10
°
C),
higher
mortality
at
41
°
F
(
5
°
C)
and
the
greatest
mortality
at
59
°
F
(
15
°
C).
However,
rainbow
trout
fingerlings
showed
greater
tolerance
to
acidic
conditions
when
acclimated
at
68
°
F
(
20
°
C)
than
when
acclimated
at
50
°
F
(
10
°
C).

Other
instances
of
synergistic
pH­
temperature
relations
are
noted
in
the
literature.
Dockray
et
al.
(
1998)
demonstrated
that
in
juvenile
rainbow
trout
that
have
either
an
unlimited
or
a
limited
food
ration,
the
combination
of
warmer
temperature
(+
3.6
°
F
[+
2
°
C])
and
sublethal
low
pH
appeared
to
have
a
slightly
higher
metabolic
cost
than
either
stressor
alone.

For
alkaline
conditions,
the
combination
of
high
pH
(

9)
and
elevated
temperature
(
71.6
°
F
[
22
°
C])
has
been
shown
to
have
an
independent,
additive
effect
on
mortality
in
rainbow
trout
(
Wagner
et
al.
1997).
Of
four
treatments,
two
consisted
of
the
following
pH
and
temperature
combinations:
control
pH
7.7­
7.8
with
temperature
61.3­
61.9
°
F
(
16.3­
16.6
°
C),
treatment
pH
9
(
±
0.05)
with
temperature
71.1
°
F
(
±
0.5
°
F)
(
21.7
°
C
[
±
0.3
°
C]).
Mortality
was
significantly
higher
with
the
high
temperature
and
high
pH
treatment
(
100%)
than
for
fish
exposed
to
high
pH
only
(
72%).
High
temperature
alone
caused
no
mortality
after
96
hours
and
all
fish
in
the
control
treatment
survived.

Hardness
and
alkalinity.
Water
hardness
(
sum
of
calcium
and
magnesium
concentrations)
has
been
shown
to
interact
with
thermal
stress.
In
experiments
with
rainbow
trout
reared
in
hard
water
and
soft
water,
median
resistance
times
to
thermal
stress
were
lower
in
juveniles
reared
in
hard
water
than
in
soft
water
(
Craigie
1963).

As
alkalinity
(
acid­
neutralizing
capacity)
of
water
increases,
a
lowered
resistance
to
temperature
may
occur
in
some
salmonids.
Vigg
and
Koch
(
1980)
tested
two
strains
of
Lahontan
cutthroat
trout
in
waters
with
alkalinity
of
1,
487,
357,
and
69
mg/
L
and
reported
upper
lethal
temperature
ranges
of
65.5­
68.4
°
F
(
18.6­
20.2
°
C),
68.4­
70
°
F
(
20.2­
21.1
°
C),
and
71.2­
73.4
°
F
(
21.8­
23
°
C),
respectively.
Different
tolerances
to
high
temperatures
also
were
detected
between
the
two
strains.

Chemical
toxicity.
Despite
voluminous
data
on
temperature
interactions
with
toxicity
of
various
chemicals,
generalizations
are
not
possible.
No
single
pattern
explains
the
effects
of
temperature
on
the
toxicity
of
pollutants
to
aquatic
organisms.
Increased
water
temperature
can
increase
the
solubility
of
many
substances
in
water
or
alter
their
chemical
form
(
Sprague
1985).
Temperature
change
in
a
given
direction
may
increase,
decrease,
or
cause
no
change
in
toxicity,
depending
on
the
toxicant,
the
species,
and
the
experimental
design
(
Sprague
1985).
Although
limited
evidence
suggests
that
temperature
may
not
have
much
effect
on
the
chronic
"
no­
effect"
8
Temperature
Interaction
thresholds
of
pollutants
(
Sprague
1985),
temperature
may
alter
the
rate
of
toxification
in
chronic
exposures
(
Mayer
et
al.
1994).

Because
the
physiology
of
fish
is
strongly
related
to
temperature,
their
response
to
chemical
exposures
is
also
influenced
by
temperature.
Salmonids
are
cold­
blooded,
thus
their
body
temperature
tracks
their
environmental
temperature
rather
precisely,
with
little
lag,
even
when
the
environmental
temperature
changes
rapidly
(
Stauffer
et
al.
1975).
Consequently,
metabolic
processes
will
exhibit
increases
and
decreases
with
temperature.
As
metabolic
demands
and
oxygen
consumption
increase,
gill
ventilation
must
also
rise
proportionately
(
Heath
and
Hughes
1973).
A
rise
in
water
flow
over
the
gills
results
in
more
rapid
uptake
of
toxic
chemicals
through
the
gills
(
Black
et
al.
1991).

Tolerable
temperature
ranges
vary
among
species,
and
to
a
lesser
degree
with
age,
physiological
condition,
and
temperature
to
which
the
fish
has
been
acclimated
(
Cairns
et
al.
1975).
Sublethal
exposure
to
toxic
chemicals
may
reduce
the
upper
lethal
temperatures
of
fish,
thereby
constricting
the
tolerance
zone
(
Paladino
et
al.
1980).
Fish
that
are
already
weakened
by
other
causes
are
expected
to
be
much
more
sensitive
to
toxicants
than
are
healthy
individuals
(
Jobling
1994).

When
fish
are
exposed
to
potential
toxicants,
the
chemicals
may
enter
the
body
over
the
gill
membranes
and
cause
damage.
The
toxicants
may
then
affect
the
physiological
functions
of
the
fish
in
a
variety
of
ways.
Toxicants
may
also
be
consumed
along
with
food
and
subsequently
absorbed
from
the
gastrointestinal
tract.
Certain
chemicals
may
then
be
deposited
and
stored
in
various
tissues
of
the
body,
causing
tissue
concentrations
to
rise
with
prolonged
exposure
to
the
chemical.
A
major
determinant
of
the
bioaccumulation
of
a
toxicant
under
a
given
set
of
exposure
conditions
is
the
rate
at
which
the
chemical
is
metabolized,
detoxified,
and
excreted
from
the
body,
processes
that
are
controlled
by
temperature.

Ammonia.
The
concentration
of
ammonia
(
NH3)
in
water
depends
on
a
number
of
factors
in
addition
to
total
ammonia
concentration;
most
important
among
these
are
pH
and
temperature.
The
concentration
of
NH3
increases
with
increasing
temperature
(
EPA
1985).

Based
on
this
relationship
of
pH
and
temperature
with
ammonia,
EPA's
national
ambient
water
quality
criteria
for
ammonia
are
determined
using
ambient
temperature
and
pH.
Many
States
have
adopted
the
national
criteria
for
ammonia,
which
incorporate
ambient
temperature
and
pH.

EPA
(
1985)
reported
an
effect
of
temperature
on
the
toxicity
of
the
un­
ionized
ammonia
species,
independent
of
the
effect
of
temperature
on
the
aqueous
ammonia
equilibrium.
Rainbow
trout
were
more
sensitive
to
un­
ionized
ammonia
at
low
temperatures
when
tested
at
37.4
and
57.2
°
F
(
3
and
14
°
C),
at
41
and
64.4
°
F
(
5
and
18
°
C),
and
at
53.6
and
66.2
°
F
(
12
and
19
°
C).
This
trend
also
is
reported
for
several
warm­
water
species.

To
determine
metabolic
costs
and
physiological
consequences
associated
with
growth
in
a
warmer
environment
polluted
with
an
environmentally
realistic
level
of
ammonia,
Linton
et
al.
9
Temperature
Interaction
(
1997)
took
quantitative
bioenergetic
and
physiological
measurements
on
juvenile
rainbow
trout
exposed
over
summer
to
a
simulated
warming
scenario
of
+
3.6
°
F
(+
2
°
C)
in
the
presence
and
absence
of
70
µ
mol
total
ammonia/
L.
They
concluded
that
juvenile
rainbow
trout
fed
to
satiation
and
exposed
over
summer
(
approaching
78.8
°
F
[
26
°
C]
at
hottest
time)
can
make
the
metabolic
adjustments
necessary
to
maintain
growth.
However,
in
the
presence
of
a
sublethal
ammonia
concentration,
the
cost
of
growth
will
increase
and
growth
may
be
compromised.
The
authors
found
that
in
the
+
3.6
°
F
(+
2
°
C)
ammonia
treatment,
the
stimulating
effect
observed
in
the
low­
level
ammonia
treatment
alone
was
lost
in
the
greater
energy
demands
when
fish
had
to
cope
with
the
additional
stress
of
a
small
further
increase
in
temperature.

Organics.
Acute
toxicity
tests
were
conducted
on
rainbow
trout
with
four
chemicals
(
terbufos,
trichlorfon,
4­
nitrophenol,
and
2,4
dinitrophenol)
to
determine
interactive
effects
with
water
temperature
(
Howe
et
al.
1994).
Temperature
was
found
to
significantly
increase
the
toxicity
of
all
chemicals
except
nitrophenol.
Chemical
bioconcentration
was
also
significantly
affected
by
temperature
and
was
directly
related
to
toxicity
in
most
tests.

A
linear
relationship
between
uptake
of
a
toxicant
and
consumption
of
oxygen
was
confirmed
by
a
temperature­
induced
change
in
the
gill
membrane
of
rainbow
trout
and
oxygen
demand
(
Black
et
al.
1991).
When
temperatures
were
reduced
from
62.6
to
46.4
°
F
(
17
to
8
°
C),
both
oxygen
and
toxicant
uptake
were
reduced
by
50%.
Changes
in
oxygen
consumption
were
correlated
with
changes
in
toxicant
uptake
for
three
compounds
tested
(
benzo[
a]
pyrene,
2,2',
5,5'­
tetrachlorobiphenyl,
and
naphthalene).
Acute
temperature
change
had
a
proportional
effect
on
the
uptake
of
oxygen
and
the
three
toxicants
by
fish
gills.

Other
organic
chemicals
show
varied
reactions
to
temperature.
Polychlorinated
biphenyl
(
PCB)
accumulation
rates
are
enhanced
by
increased
temperature
in
brown
trout
(
Spigarelli
et
al.
1983,
as
cited
in
Rattner
and
Heath
1995).
Higher
temperatures
provide
protection
to
rainbow
trout
exposed
to
permithrin,
an
insecticide
(
Kumaraguru
and
Beamish
1981):
the
96
hr
LC50
for
1
g
trout
increased
an
order
of
magnitude
from
0.62
to
6.43
µ
g/
L
between
41
and
68
°
F
(
5
and
20
°
C).
Rattner
and
Heath
(
1995)
also
report
that
some
organochlorine
compounds
exhibit
greater
toxicity
at
cold
temperatures
in
fish,
whereas
certain
organophosphorus
compounds
elicit
the
opposite
response.

Metals.
Water
temperature
is
important
in
the
accumulation
of
metals
in
fish.
In
an
oligotrophic
lake,
Kock
et
al.
(
1996)
found
that
Arctic
char
experienced
enhanced
uptake
of
cadmium
and
lead
as
a
consequence
of
increasing
metabolic
rates
during
the
summer.
Although
peak
metals
concentrations
in
the
water
occurred
in
the
spring
with
low
pH
and
snowmelt
runoff,
the
highest
concentrations
in
the
fish
occurred
during
the
summer
(
46.4­
50
°
F
[
8­
10
°
C]).

Temperature
greatly
influences
mercury
accumulation,
elimination,
and
toxicity
in
fish.
Mercury
toxicity
in
rainbow
trout
fingerlings
is
shown
to
be
related
to
temperature
(
MacLeod
and
Pessah
1973).
Mercury
toxicity
was
found
to
increase
with
temperature
(
41,
50,
and
68
°
F
[
5,
10,
and
20
°
C]),
probably
because
of
factors
such
as
rate
of
chemical
reaction,
diffusion,
active
transport
of
toxic
materials
across
membranes,
and
metabolic
rate.
Increased
accumulation
rate
of
mercury
also
was
observed
at
higher
temperatures,
which
can
be
attributed
to
effects
on
metabolic
rate
and
uptake.
Elimination
of
mercury
from
the
fish
flesh
also
10
Temperature
Interaction
depended
on
temperature,
with
warmer
temperature
(
68
°
F
[
20
°
C])
increasing
the
elimination
rate.
Time
to
death
was
found
to
be
linearly
related
to
temperature.

Sublethal
exposure
to
a
potentially
lethal
chemical
agent
can
reduce
the
resistance
of
aquatic
organisms
to
elevated
temperatures.
Exposure
to
as
little
as
1.5
mg/
L
nickel
(
Ni)
for
7
to
21
days
significantly
suppressed
resistance
of
rainbow
trout
to
elevated
temperatures,
but
28­
day
exposure
to
0.9
mg/
L
Ni
did
not.
In
a
critical
thermal
maximum
(
CTM)
test
(
10.8
°
F/
h
[
6
°
C/
h]
rate
of
increase),
equilibrium
loss
in
fingerling
rainbow
trout
occurred
at
68
°
F
(
20
°
C)
with
prior
exposure
to
3
mg/
L
Ni
after
7
of
days
exposure,
and
at
79.9
°
F
(
26.6
°
C)
with
prior
exposure
to
0.8
mg/
L
Ni
in
a
30­
day
exposure
(
Becker
and
Wolford
1980).
Although
a
great
reduction
in
CTM
occurred
after
prior
exposure
to
3
mg/
L
Ni,
even
5
mg/
L
Ni
did
not
cause
a
reduction
in
migratory
behavior
or
capacity
for
seawater
survival
in
coho
(
Lorz
et
al.
1978,
as
cited
in
Wedemeyer
1980).

Copper
can
inhibit
or
inactivate
gill
ATPase
function
during
coho
smoltification
at
chronic
exposure
concentrations
of
20
to
30
µ
g/
L
(
Lorz
and
McPherson
1976).
If
sublethal
cadmium
or
zinc
concentrations
are
simultaneously
present,
concentrations
as
low
as
10
µ
g/
L
copper
can
suppress
gill
ATPase,
thereby
reducing
downstream
migration
(
Lorz
et
al.
1978,
as
cited
in
Wedemeyer
et
al.
1980).
If
coho
are
subjected
to
thermal
stress
and
chronic
copper
exposure
during
emigration,
it
is
likely
that
ATPase
activity
and
readiness
to
tolerate
saltwater
would
be
impaired.
Lydy
and
Wissing
(
1988)
found
that
sublethal
copper
exposure
for
3
days
significantly
lowered
the
thermal
tolerance
(
measured
by
critical
thermal
maximum)
for
two
species
of
darter.

Temperature
influences
on
zinc
toxicity
vary
depending
on
acclimation
temperature
and
exposure
duration.
Hodson
and
Sprague
(
1975),
using
Atlantic
salmon
in
bioassay
tests,
found
that
salmon
acclimated
and
exposed
at
a
water
temperature
of
66.2
°
F
(
19
°
C)
were
more
tolerant
of
zinc
than
were
those
acclimated
and
exposed
at
37.4
°
F
(
3
°
C)
and
51.8
°
F
(
11
°
C).
The
difference
was
approximately
50%
from
66.2
°
F
(
19
°
C)
compared
with
37.4
°
F
(
3
°
C).
As
acclimation
temperatures
became
lower,
however,
salmon
were
less
tolerant
(
lower
LC50
values).
Zinc
toxicity
appears
to
be
enhanced
by
temperature
as
a
stressor.
Moderate
(
14.4
°
F
[
8
°
C]
change
in
temperature)
and
severe
(
28.8
°
F
[
16
°
C]
change
in
temperature)
heat
stresses
shortened
time
to
mortality
and
increased
tolerance
only
under
moderate
heat
stress.
Severe
heat
stress
also
changed
the
pattern
of
response
by
altering
the
slope
of
the
toxicity
curves.
Moderate
and
severe
cold
stresses
also
lengthened
time
to
mortality,
but
decreased
tolerance.
Cold
stresses
decreased
the
slopes
of
the
toxicity
curves.
Lower
acclimation
temperatures
were
associated
with
longer
survival
but
less
tolerance,
i.
e.,
lower
LC50
values.
Salmon
acclimated
to
37.4
°
F
(
3
°
C)
had
shorter
survival
when
exposed
to
heat
stress
(
test
temperatures
higher
than
acclimation
temperatures),
and
heat
stress
caused
a
slight
decrease
in
the
slope
of
the
toxicity
curve.
Temperature
may
have
produced
this
effect
through
transient
changes
in
metabolic
rate
and
the
amount
of
water
passing
over
the
gills.
Slowing
of
metabolism
due
to
cold
may
have
induced
longer
survival
by
reducing
ventilation
rate
and
consequently
zinc
uptake.
In
contrast,
heat
may
have
accelerated
metabolic
rate
and
zinc
accumulation
and
shortened
survival
time.
Reduction
in
thresholds
with
cold
stress
and
increase
with
heat
stress
may
result
from
biochemical
processes
that
vary
with
temperatures,
such
as
isoenzymes.
Isoenzymes
that
are
active
during
heat
exposure
might
have
different
sensitivity
to
zinc
than
do
those
active
during
cold
exposure.
11
Temperature
Interaction
Temperature
has
a
marked
effect
on
toxicity
of
cadmium
to
rainbow
trout,
making
them
more
vulnerable
at
higher
temperatures.
Fish
acclimated
and
exposed
at
42.8
°
F
(
6
°
C)
survived
significantly
longer
than
those
acclimated
and
exposed
at
53.6
°
F
(
12
°
C),
which
in
turn
survived
significantly
longer
than
fish
exposed
at
64.4
°
F
(
18
°
C)
(
Roch
and
Maly
1979).
In
addition,
lethal
thresholds
increased
with
decreasing
temperature.
Cold­
acclimated
(
42.8
°
F
[
6
°
C])
fish
showed
a
greater
10­
day
lethal
threshold
concentration
and
survived
approximately
twice
as
long
as
warmacclimated
(
64.4
°
F
[
18
°
C])
fish
exposed
to
the
same
concentrations.
Roch
and
Maly
(
1979)
suggest
that
the
rate
at
which
cadmium
affects
fish
is
governed
by
temperature
in
a
way
that
resembles
the
effect
of
temperature
on
metabolic
rate
following
rapid
temperature
change.

Cyanide.
An
increase
in
temperature
has
been
found
to
reduce
resistance
and
survival
time
in
salmon
smolts
and
trout
exposed
to
acutely
lethal
concentrations
of
cyanide
(
Cairns
et
al.
1975).
Conversely,
a
higher
96­
hr
LC50
(
less
toxic)
was
found
for
juvenile
rainbow
trout
at
elevated
temperatures
(
Kovacs
and
Leduc
1982).
Rattner
and
Heath
(
1995)
hypothesize
that
fish
are
better
able
to
tolerate
cyanide
at
higher
temperatures
because
of
detoxifying
enzyme
activity,
which
is
highly
temperature
dependent.
At
acutely
toxic
concentrations,
death
occurs
more
rapidly
at
high
than
low
temperatures
because
uptake
is
rapid
and
metabolic
demand
accelerates
as
aerobic
metabolism
is
blocked
by
cyanide.

Chlorine.
In
general,
chlorine
is
more
toxic
at
higher
temperatures
during
continuous
exposure.
However,
in
an
experiment
where
fish
were
exposed
to
a
pulsed
dose
of
chlorine,
temperature
had
little
effect
on
toxicity
for
a
variety
of
cold­
water
fish
species
(
Rattner
and
Heath
1995).

Nitrogen
supersaturation.
The
Oregon
Department
of
Environmental
Quality
(
ODEQ)
Issue
Paper
(
1995)
states
that
lethal
and
sublethal
effects
of
nitrogen
gas
supersaturation
on
adult
salmonids
may
be
exacerbated
by
high
temperatures
and
prolonged
exposures
(
Beiningen
and
Ebel
1970).
High
temperatures
can
also
aggravate
the
adverse
effects
of
nitrogen
supersaturation
(
Beiningen
and
Ebel
1970,
Ebel
1969).

What
aspects
of
salmonid
biology
are
influenced
by
temperature?

Competition
and
predation.
Temperature
is
a
key
determinant
of
the
outcome
of
competitive
interactions
in
a
fish
community.
Predation
is
also
keenly
influenced
by
temperature.
The
Behavioral
issue
paper
contains
discussion
on
multiple
interactions
related
to
these
topics.

Disease.
The
influence
of
water
temperature
on
salmonid
susceptibility
to
diseases
and
its
control
on
resistance
of
fish
exposed
to
disease
pathogens
are
well
documented
in
fish
pathology
literature.
Fish
diseases
involve
presence
of
the
disease
organism,
infection
of
the
host,
and
resistance
to
or
progression
of
the
disease,
resulting
in
recovery
or
death.
Infection
rate
and
disease
outcome
depend
on
a
variety
of
factors,
foremost
among
them
being
water
temperature,
disease
virulence,
and
genetics
of
the
stock.
During
periods
of
warm
water
temperature,
disease
outbreaks
are
frequently
severe.
12
Temperature
Interaction
What
factors
are
involved
in
infection
by
disease?

Most
fish
diseases
are
favored
by
increased
water
temperatures
(
Ordal
and
Pacha
1963).
The
temperature
regime,
condition
of
the
fish,
genetic
susceptibility
to
the
disease,
virulence
of
the
disease
organism,
and
other
stressors
determine
the
infection
rate,
the
percentage
survival,
and
the
mean
time
to
death.
Condition
of
the
fish
can
be
described
in
terms
of
overall
health
(
presence
of
other
diseases),
condition
factor
(
a
function
of
fat
reserves,
food
availability,
and
growth
rates),
and
presence
of
various
points
of
entry
of
the
disease.
Cuts
or
abrasion
of
the
skin
or
gills
often
provide
routes
for
infection.
Some
diseases
are
either
present
or
absent
in
a
watershed
(
e.
g.,
Ceratomyxa),
but
others
appear
to
be
ubiquitous
and
merely
await
temperature
stimuli
to
become
active.

Are
warm­
water
vectors
of
disease
present
in
rivers
of
the
Pacific
Northwest?

The
bacterial
infection
columnaris
has
been
observed
throughout
the
mainstem
Columbia
River
and
in
numerous
tributaries:
the
Okanogan,
Wenatchee,
John
Day,
Umatilla,
Yakima,
Snake,
and
Similkameen
Rivers.
It
is
carried
by
all
species
of
Pacific
salmon
and
also
by
carp,
sucker,
chub,
bass,
northern
pikeminnow,
chiselmouth,
and
catfish
(
Colgrove
and
Wood
1966).
Ordal
and
Pacha
(
1963)
considered
temperature­
induced
columnaris
a
major
factor
responsible
for
declines
of
Columbia
River
chinook.
The
system
of
reservoirs
has
been
credited
with
the
biggest
increase
in
columnaris
disease
in
the
Columbia
River
(
Snieszko
1964).

Although
dramatic
fish
kills
from
columnaris
infection
have
been
documented,
other
diseases
associated
with
warm
water
can
also
produce
significant
mortalities.
Aeromonas
salmonicida,
A.
punctata,
and
A.
hydrophila
(
also
known
as
liquefaciens)
are
common
bacterial
pathogens
linked
to
organic
pollution
(
Snieszko
1974)
and
high
water
temperatures
(
Groberg
et
al.
1978).
These
organisms
are
the
infective
agent
for
furunculosis,
a
pathogen
affecting
all
Pacific
salmon.
Aeromonas
salmonicida
and
A.
hydrophila
have
been
shown
in
laboratory
studies
to
cause
mortality
in
less
than
3
days
at
71.6­
73.4
°
F
(
22­
23
°
C)
after
infection
and
to
produce
survivals
of
2%
to
30%
with
constant
temperature
exposure
in
the
range
69.1­
73.9
°
F
(
20.6­
23.3
°
C)
(
Fryer
et
al.
1976).
Resistance
to
this
disease
varies
greatly
with
fish
strain,
as
revealed
in
studies
on
steelhead
stocks
(
Wade
1986),
but
expression
of
the
disease
is
also
related
to
water
temperature.

Likewise,
there
are
stock
variations
in
resistance
to
Ceratomyxa
shasta
but
regardless
of
stock
the
effects
are
enhanced
by
warm
water.
The
occurrence
of
infective
units
of
C.
shasta
and
rate
of
infection
have
also
been
linked
to
presence
of
slack
flows
(
Ratliff
1981,
Margolis
et
al.
1992).
High
infection
frequency
is
associated
with
reduced
time
to
death
(
Ratliff
1983).

Presence
of
the
infective
stage
of
C.
shasta
was
demonstrated
in
many
locations
in
the
Columbia
and
Snake
Rivers
by
holding
disease­
susceptible
rainbow
trout
in
liveboxes
for
7
or
14
days
at
various
locations
(
Hoffmaster
et
al.
1988).
C.
shasta
is
also
a
serious
disease
problem
on
the
Sandy
and
Willamette
Rivers,
where
92%
and
62%,
respectively,
of
fish
that
died
before
spawning
were
infected
with
the
disease.
The
disease
appears
to
be
controlled
by
water
temperatures
<
50
°
F
(
10
°
C)
(
Sanders
et
al.
1970).
Fryer
and
Pilcher
(
1974)
found
that
C.
shasta
mortality
in
rainbow
trout
was
96%
to
100%
at

69.1
°
F
(
20.6
°
C);
92%
and
96%
at
59
and
54
°
F
13
Temperature
Interaction
(
15
and
12.2
°
C);
84%
to
75%
at
48.9­
44.1
°
F
(
9.4­
6.7
°
C);
and
0%
at
39
°
F
(
3.9
°
C).
In
juvenile
coho
salmon,
mortality
was
92%
to
100%
at

69.1
°
F
(
20.6
°
C);
57%
to
59%
at
64
°
F
(
17.8
°
C);
13%
to
31%
at
59­
54
°
F
(
15­
12.2
°
C);
and
0%
to
4%
at

48.9
°
F
(
9.4
°
C).

Is
just
a
single
life
stage
susceptible
to
disease?

Infection
of
salmon
with
warm­
water
diseases
can
occur
at
any
life
stage.
That
is,
infections
and
mortality
from
disease
can
occur
at
the
egg,
alevin,
fry,
parr,
smolt,
or
adult
life
stages.
The
alevin
and
fry
stages
are
probably
less
likely
to
be
significantly
affected
in
the
field
because
temperatures
are
generally
below
critical
thresholds
during
these
phases.

Juvenile
salmon
do
show
greater
sensitivity
to
some
diseases
at
higher
temperatures.
Uninjured
fingerlings
exposed
for
30
minutes
to
Bacillus
columnaris
and
then
held
in
water
at
70
°
F
(
21.1
°
C)
all
died
within
3
days,
whereas
only
24%
of
fish
similarly
exposed
for
38
days
died
at
64.9
°
F
(
18.3
°
C)
for
38
days
and
60%
of
fish
at
60.1
°
F
(
15.6
°
C)
(
Fish
and
Rucker
1943).
No
mortality
occurred
at
50
°
F
(
10
°
C)
over
the
38
days.
Susceptibility
to
disease
is
a
function
of
concentration
of
columnaris
organisms,
length
of
exposure,
and
temperature
(
Fujihara
et
al.,
as
cited
in
Parker
and
Krenkel
1969)
as
well
as
age
of
individual
(
increased
age,
increased
resistance)
(
Olson
and
Fujihara
1963,
as
cited
by
Parker
and
Krenkel
1969).
Table
1
also
illustrates
that
young
chinook
salmon
exposed
to
C.
columnaris
exhibited
increased
mortality
on
exposure
to
increasing
temperatures
(
Rucker
and
Ordal
1944,
cited
by
Ordal
and
Pacha
1963).

Wouldn't
disease
be
obvious
in
salmon
if
it
were
present?
Wouldn't
dead
fish
be
noticeable
if
this
were
a
problem?

Rather
large
kills
of
juvenile
fall
chinook
were
reported
at
McNary
Dam
on
the
Columbia
River
in
July
1994
and
July
1998
during
periods
of
high
water
temperature
(
Tiffan
et
al.
1996).
These
observations
represented
a
small
subsample
of
the
entire
migrating
population
that
passed
the
dam.
In
the
mainstem,
however,
dead
juvenile
fish
may
not
rise
to
the
surface
and
they
decompose
rapidly.
Infected
fish
become
easy
prey
to
predators
and
may
be
included
in
predation
rate
rather
than
disease
mortality
rate.
In
addition
to
increased
predation,
diseased
fish
probably
are
less
able
to
perform
essential
functions,
such
as
feeding,
swimming,
and
defending
territories,
and
may
not
migrate
or
grow
effectively
or
achieve
critical
size
prior
to
ocean
entry.

Mortality
from
disease
generally
requires
several
days.
Juveniles
that
become
infected
prior
to
emigrating
from
natal
habitat
to
the
ocean
may
die
unnoticed
in
mainstem
reservoirs
or
in
the
ocean
(
Ratliff
1981,
1983).
When
individual
adult
fish
are
radiotracked,
it
is
rare
to
find
a
carcass
even
when
it
is
washed
ashore
(
Schreck
et
al.
1994).
Mammals
or
other
scavengers
are
generally
efficient
at
removing
carcasses.
In
some
rivers,
such
as
the
Fraser
in
Canada,
that
have
very
large
adult
salmon
migrations,
warm
water
has
frequently
produced
dramatic
fish
kills
that
are
very
noticeable.
However,
run
sizes
in
rivers
of
Oregon,
Washington,
and
Idaho
today
are
typically
small
enough
that
mortality
of
juveniles
or
adults
from
any
source
could
go
unnoticed.
14
Temperature
Interaction
Table
1.
Increased
mortality
observed
in
chinook
salmon
exposed
to
C.
columnaris
on
exposure
to
increased
temperatures
Temperature
(
°
C)
Time
of
exposure
(
days)
Mortality
(%)

22
3
100
20
7
90
17.8
7
45
16
7
30
What
are
some
modes
of
infection?

For
columnaris
infection,
the
infection
rate
and
time
to
death
are
related
to
the
virulence
of
the
disease
organism,
the
condition
of
the
fish,
and
the
method
of
infection.
With
highly
virulent
log­
phase
cells,
contact
is
the
most
effective
method
of
infection,
but
is
least
effective
in
lowvirulence
strains
(
Pacha
1961).
However,
Fish
and
Rucker
(
1943)
showed
that
uninjured
sockeye
fingerlings
exposed
to
columnaris
became
infected
and
died
within
only
48
h.
Injured
fish
required
72
h
to
die.
Temperatures
<
60.1
°
F
(<
15.6
°
C)
prevented
infection,
but
higher
temperatures
led
to
rapid
death.
Temperatures
of
69.8
°
F
(
21
°
C)
allowed
the
bacteria
to
easily
penetrate
the
mucus
coating
of
skin
and
gills,
and
between
60.1
°
F
(
15.6
°
C)
and
69.8
°
F
(
21
°
C)
bacteria
invaded
the
body
through
cuts
and
abrasions
(
Fish
1948).
The
perils
of
adult
migration
through
fish
ladders
and
over
sharp
rocks,
and
descaling
and
abrasion
of
juveniles
on
fish
screens,
are
but
a
few
means
for
opening
routes
of
infection.
Prespawning
mortality
can
be
minimized
by
holding
adults
in
water
temperatures

50
°
F
(

10
°
C)
to
allow
abrasions
to
heal
(
Fish
1944).

Contagion
of
columnaris
has
been
suspected
during
passage
of
salmon
through
fish
ladders
(
Pacha
1961),
and
increased
incidence
may
be
a
result
of
the
creation
of
slow­
moving
reservoirs
(
Snieszko
1964).
Warm
sloughs
may
also
harbor
a
disease
organism
in
coarsefish
that
can
then
infect
salmonids
migrating
in
warmed
reservoirs
(
Fujihara
et
al.
1971).
Likewise,
ceratomyxa
infection
has
been
most
severe
in
locations
and
under
conditions
having
low
or
slack
flows,
such
as
reservoirs
or
side
arms
of
channels
(
Ratliff
1981,
Margolis
et
al.
1992).

Has
infection
with
warm­
water
diseases
been
documented
historically
in
streams
of
the
region?

Problems
with
columnaris
disease
in
the
Columbia
River
were
heavily
documented
in
numerous
studies
conducted
from
the
1940s
to
the
early
1970s.
In
the
Fraser
River,
columnaris
is
of
continued
concern
because
of
the
noticeable
impacts
to
adult
sockeye
on
spawning
grounds.
As
determined
by
surveys
of
antibody
titers
in
1964­
65
and
1969­
70,
peak
yearly
columnaris
infection
rates
in
the
Columbia
River
can
be
at
least
70%
to
80%
in
adults
(
Fujihara
and
Hungate
1970).
15
Temperature
Interaction
Surveys
of
infection
frequency
of
sockeye
and
chinook
in
the
Snake
River
in
July
and
early
August
of
1955­
1957
revealed
28%
to
75%
of
fish
infected
when
water
temperature
was
>
70
°
F
(>
21.1
°
C)
(
Ordal
and
Pacha
1963).
During
this
same
period
the
disease
was
widespread
in
the
Yakima
and
Okanogan
Rivers.
In
1958,
high
percentages
of
salmon
were
infected
judging
by
samples
taken
at
several
mainstem
Columbia
River
dams
from
Rock
Island
to
Bonneville,
as
well
as
on
the
Yakima,
Wenatchee,
and
Okanogan
Rivers.
In
1958,
water
temperatures
in
the
Okanogan
were
so
warm
that
the
run
was
vastly
damaged
by
columnaris.
Thousands
of
adults
left
the
Okanogan
to
seek
the
cooler
temperatures
of
a
tributary
(
the
Similkameen
River),
only
to
die
there
from
columnaris
infection
(
Pacha
and
Ordal
1970).
Over
the
years
1955
to
1959,
the
sockeye
run
to
Redfish
Lake,
Idaho,
declined
by
an
order
of
magnitude,
coincident
with
a
large
increase
in
Columbia
River
water
temperatures.
In
1955
and
1956,
the
frequency
of
infected
sockeye
was
34%
and
50%,
respectively,
in
samples
taken
at
Clarkston,
Washington
(
Pacha
1961).
Even
though
these
infection
frequencies
were
high,
it
is
likely
that
they
became
higher
as
the
fish
migrated
toward
their
spawning
grounds.
Pacha
(
1961)
reported
that
Anacker
(
1956)
sequentially
sampled
the
sockeye
run
into
the
Okanogan
River,
finding
that
columnaris
frequency
rose
from
6.3%
in
August
at
Rock
Island
to
23.8%
and
then
38%
in
9
and
15
days,
respectively,
further
along
in
the
migration.
At
the
termination
of
the
run
the
disease
incidence
was
55%
(
Pacha
and
Ordal
1970).

Chondrococcus
columnaris
infection
was
implicated
in
high
sockeye
mortalities
in
the
Columbia
River
(
Fish
1948).
Columnaris
becomes
increasingly
active
above
60.1
°
F
(
15.6
°
C)
(
Colgrove
and
Wood
1966).
The
near
obliteration
of
the
run
of
1941
at
Bonneville
Dam
occurred
when
temperatures
reached
a
high
of
74.5
°
F
(
23.6
°
C)
and
an
average
of
68.5
°
F
(
20.3
°
C)
(
Fish
1948).
For
adult
sockeye
on
Fraser
River
spawning
grounds,
mortality
of
females
ranged
from
5%
to
86%
from
bacterial
gill
infections
at
temperatures
of
71.6
°
F
(
22
°
C)
(
International
Pacific
Salmon
Fisheries
Commission
1962,
as
cited
by
Parker
and
Krenkel
1969).
In
1970,
there
was
a
columnaris
epidemic
in
the
Hanford
Reach
and
in
the
Wenatchee
portion
of
the
mainstem
Columbia
River,
in
which
it
appeared
that
coarsefish
passed
the
disease
to
adult
sockeye
during
their
migration
(
Fujihara
et
al.
1971).

In
1967
and
1968,
coho
placed
in
liveboxes
in
the
Columbia
River
at
Bonneville
Dam
had
ceratomyxa
infection
rates
of
53%
and
60%,
respectively.
At
the
Dalles
Dam
in
1967,
rainbow
trout
in
liveboxes
exhibited
a
13%
infection
rate
(
Sanders
et
al.
1970).

Are
warm­
water
disease
outbreaks
in
salmonids
a
thing
of
the
past?
Has
infection
with
warm­
water
diseases
been
documented
recently
in
streams
of
the
region?

Although
warm­
water
fish
diseases
were
studied
intensively
in
the
past,
insufficient
attention
has
been
given
to
them
recently.
This
is
probably
because
far
fewer
numbers
of
fish
are
present
today
and
many
other
problems
demand
redress.
Columnaris
infection
frequencies
have
been
documented
in
fall
chinook
in
small­
scale
surveys
conducted
in
recent
years
on
the
Columbia
River.
After
the
large
fish
kill
at
McNary
Dam
on
July
16,
1994,
125
juvenile
fall
chinook
were
collected
at
John
Day
Dam
and
held
at
the
Lower
Columbia
River
Fish
Health
Laboratory
at
the
USFWS
facility
in
Cook,
Washington.
In
a
4­
day
period,
94%
of
these
fish
died
from
a
columnaris
infection
considered
to
be
a
low­
virulence
strain
(
Tiffan
et
al.
1996).
In
mid­
July
1998,
three
consecutive
days
of
high
fall
chinook
mortality
were
detected
at
McNary
16
Temperature
Interaction
Dam
because
of
high
water
temperatures.
Of
25
fish
sampled
from
the
Juvenile
Fish
Facility
at
McNary
Dam
that
were
distressed
(
swimming
on
their
sides),
88%
had
columnaris
infection.
Although
the
fish
were
near
death,
there
were
no
visible
external
signs
of
disease
(
Tiffan,
USFWS,
Cook,
WA).

In
the
Rogue
River,
prespawning
mortality
from
furunculosis
and
columnaris
averaged
12%
for
wild
and
36%
for
hatchery
spring
chinook
from
1977
through
1981
(
Cramer
et
al.
1985,
as
cited
by
Lindsay
et
al.
1989).

Infection
frequency
of
rainbow
trout
by
ceratomyxa
was
generally
<
20%
in
reservoirs
near
many
of
the
mainstem
Columbia
and
Snake
River
dams.
However,
in
June
1984
infection
frequency
was
52%
at
the
Dalles
Dam,
and
in
July
1986
at
Hells
Canyon
and
Oxbow
Dams
was
96%
and
95%,
respectively
(
Hoffmaster
et
al.
1988).

What
is
the
relationship
between
increasing
temperature
and
columnaris
disease?
Are
there
any
apparent
critical
temperature
thresholds?

Rate
of
infection
increases
with
temperature.
Laboratory
studies
are
very
good
at
identifying
the
influence
of
temperature
on
infection
rate.
Juvenile
spring
chinook
infection
with
C.
columnaris
at
temperatures
of

54
°
F
(

12.2
°
C)
was
negligible,
but
between
59
°
F
(
15
°
C)
and
73.9
°
F
(
23.3
°
C)
the
percentage
of
infected
fish
rose
steadily
with
temperature
from
27%
to
80%
(
Fryer
and
Pilcher
1974).

Coho
salmon
and
rainbow
trout
exposed
to
C.
columnaris
had
a
rapidly
increasing
rate
of
infection
with
increase
in
temperatures
above
54
°
F
(
12.2
°
C)
(
Fryer
and
Pilcher
1974).
For
coho
and
rainbow,
infection
frequency
of
the
experimental
group
was
low
at
54
°
F
(
12.2
°
C)
(
3%
to
8%)
but
was
49%
and
40%,
respectively,
at
59
°
F
(
15
°
C),
and
rapidly
jumped
to
100%
at
temperatures

69.1
°
F
(

20.6
°
C).

Migration
effects.
Prespawning
survival
rates
among
adult
sockeye
in
the
Fraser
River
spawning
areas
were
as
low
as
10%
(
as
found
in
the
Chilko
stock)
in
the
early
1960s.
Given
that
river
temperatures
enroute
to
spawning
grounds
for
the
Chilko
and
Stuart
Lake
runs
averaged
62.1
°
F
(
16.7
°
C)
during
1956
(
Idler
and
Clemens
1959),
it
appears
that
if
fish
can
survive
migration
through
these
adverse
temperatures,
it
would
be
essential
to
find
suitable
temperatures
on
spawning
grounds.
Unfortunately,
during
other
years,
temperatures
at
Hell's
Gate
during
the
Horsefly
sockeye
migration
can
be
even
higher
(
up
to
66.7
°
F
[
19.3
°
C])
(
Williams
et
al.
1977).
Bouck
et
al.
(
1970)
(
as
cited
by
EPA
and
NMFS
1971)
did
not
observe
sockeye
mortalities
from
columnaris
at
62.1
°
F
(
16.7
°
C)
but
did
note
frequent
lesions
and
death
at
68
°
F
(
20
°
C).
Temperatures
of
68
°
F
(
20
°
C)
were
reported
to
result
in
100%
mortality
of
chinook
during
columnaris
outbreaks
(
Ordal
and
Pacha
1963).

The
evidence
from
the
laboratory
and
field
indicates
that
temperatures
between
62.1
°
F
(
16.7
°
C)
and
68
°
F
(
20
°
C)
and
greater
lead
to
infection
of
adult
salmon
with
columnaris
under
exposure
to
low­
virulence
strains,
but
infection
can
occur
at
even
lower
temperatures
when
highvirulence
strains
are
present.
Relatively
short
river
reaches
with
heightened
temperatures
may
17
Temperature
Interaction
lead
to
infection
that
then
runs
its
course
during
the
prespawning
period.
Temperatures
between
68
and
75.2
°
F
(
20­
24
°
C)
have
been
linked
to
extreme
sockeye
mortality
in
the
Columbia
River.

Holding
effects.
Columnaris
becomes
increasingly
active
above
60.1
°
F
(
15.6
°
C),
as
revealed
in
studies
on
Horsefly
Creek,
British
Columbia
(
Colgrove
and
Wood
1966).
It
was
found
that
adult
sockeye
held
at
a
mean
temperature
of
60.1
°
F
(
15.6
°
C)
on
spawning
grounds
had
survival
rates
of
only
19%
to
37%.
However,
when
held
at
mean
temperatures
of
55
°
F
(
12.8
°
C)
and
a
maximum
<
57
°
F
(<
13.9
°
C),
the
sockeye
did
not
die
and
gill
lesions
from
columnaris
infection
began
to
heal
(
Colgrove
and
Wood
1966).
A
mean
of
55
°
F
(
12.8
°
C)
and
a
maximum
of
<
57
°
F
(<
13.9
°
C)
is
a
recommended
holding
temperature
on
spawning
grounds.

This
evidence
indicates
that
temperatures
between
57
and
60.1
°
F
(
13.9­
15.6
°
C)
constitute
a
transitional
temperature
region
below
which
recovery
from
columnaris
after
infection
could
occur,
or
above
which
infection
and
mortality
continue
to
increase.

Juvenile
survival
rate
decreases
with
increasing
temperature.
Rates
of
survival
from
columnaris
infection
in
spring
chinook
were
found
to
decrease
between
temperatures
of
39
and
73.9
°
F
(
3.9­
23.3
°
C)
(
Fryer
and
Pilcher
1974)
(
see
McCullough
1999,
Table
7).
Survival
was

30%
for
temperatures
of
69.1
°
F
(
20.6
°
C)
or
greater.
Time
to
death
from
the
point
of
infection
was
reduced
from
7
to
2.5
days
as
temperatures
increased
from
59
to
73.9
°
F
(
15­
23.3
°
C)
(
see
McCullough
1999,
Table
8).

A
temperature
of
54
°
F
(
12.2
°
C)
appears
to
be
the
threshold
for
initiating
significant
mortalities
in
coho.
Below
this
temperature
survival
was
near
100%
(
see
McCullough
1999,
Table
9).
In
rainbow
trout
survival
was

8%
for
temperatures
above
64
°
F
(
17.8
°
C).
As
with
coho,
the
threshold
for
initiating
significant
mortality
in
rainbow
occurred
at

54
°
F
(

12.2
°
C).
Experiments
with
steelhead
infected
with
Flexibacter
columnaris,
a
columnaris
strain
of
intermediate
virulence,
showed
that
percentage
survival
was
very
high
in
the
temperature
range
39­
54
°
F
(
3.9­
12.2
°
C)
but
decreased
from
44%
to
0%
as
temperatures
rose
from
59
to
73.9
°
F
(
15­
23.3
°
C)
(
Holt
et
al.
1975).

In
summary,
on
the
basis
of
laboratory
and
field
studies
on
chinook,
coho,
sockeye,
rainbow
trout,
and
steelhead
by
numerous
investigators,
infection
and
mortality
by
columnaris
disease
were
negligible
at
temperatures

55
°
F
(

12.8
°
C),
but
temperatures

59
°
F
(

15
°
C)
produced
significantly
increased
mortalities.

Time
to
death
decreases
with
increasing
temperature.
Mean
time
to
death
after
infection
with
columnaris
varied
from
4.2
to
7
days
with
exposure
to
59
°
F
(
15
°
C)
in
juvenile
chinook,
coho,
and
steelhead.
Steelhead
were
the
most
sensitive
(
Fryer
and
Pilcher
1974).
18
Temperature
Interaction
Are
other
salmon
diseases
of
warm
water
similar
to
columnaris
in
their
temperaturesurvival
relationships?

Rates
of
infection,
percentage
survival,
and
time
to
death
after
infection
that
were
reported
for
columnaris
infection
in
a
cross­
section
of
salmonids
are
very
similar
to
those
reported
for
A.
salmonicida,
A.
hydrophila,
and
Vibrio
(
see
McCullough
1999).

What
is
the
relationship
between
disease
and
stress?

In
most
cases,
an
equilibrium
exists
in
the
interactions
among
fish,
their
pathogens,
and
the
aquatic
environment,
and
this
equilibrium
must
be
altered
for
disease
to
occur
(
Wedemeyer
et
al,
1976,
Esch
and
Hazen
1980,
Walters
and
Plumb
1980,
cited
in
Wedemeyer
and
Goodyear
1984).
When
the
relation
among
host­
pathogen­
environment
is
favorable
for
the
host,
fish
populations
normally
exhibit
good
health,
growth,
and
survival.
When
this
relation
is
impaired,
the
incidence
of
diseases
will
begin
to
increase.
When
the
relation
is
poor,
health
problems
accompanied
by
reduced
growth
and
survival
may
become
chronic
(
Roberts
1978
and
Schaperclaus
1979,
as
cited
in
Wedemeyer
and
Goodyear
1984).
A
number
of
environmental
alterations
have
been
associated
with
poor
fish
health,
including
unfavorable
or
fluctuating
temperatures
(
Wedemeyer
et
al.
1976,
Knittel
1981,
Malins
et
al.
1980
and
1982,
cited
in
Wedemeyer
and
Goodyear
1984).

Fish
disease
incidence
is
potentially
a
very
sensitive
index
of
stress
(
Wedemeyer
and
McLeay
1981).
Fish
diseases
do
not
necessarily
have
one
cause
but
are
the
end
result
of
the
relationship
among
the
pathogen,
fish,
and
environment.
Good
examples
of
stress­
mediated
diseases
are
those
resulting
from
bacterial
pathogens
that
are
continuously
present
in
most
natural
waters.
The
presence
of
many
of
these
pathogens
will
result
in
widespread
disease
only
if
unfavorable
environmental
conditions
also
exist
and
the
host
defense
system
has
been
compromised.
Table
2
describes
diseases
that
can
infect
salmonids
and
the
conditions
that
predispose
salmonids
to
such
disease.

As
warming
temperatures
increase
the
abundance
or
virulence
of
disease
organisms
to
salmonids,
they
also
decrease
a
fish's
ability
to
withstand
the
stress
of
disease.
When
environmental
conditions
are
optimal
for
a
disease,
it
grows
more
rapidly
and
may
be
more
virulent.
If
environmental
conditions
are
more
optimal
for
the
disease
than
they
are
for
the
fish,
there
is
a
greater
likelihood
that
the
disease
will
overcome
the
host's
defense
systems
and
create
serious
illness
(
Wedemeyer
and
Goodyear
1984).
This
concept
is
illustrated
with
Ceratomyxa
shasta,
the
myxosporean
responsible
for
causing
the
disease
of
ceratomyxosis
in
salmonid
fishes.
Fish
can
become
infected
in
low
water
temperatures,
although
the
progress
of
the
disease
is
temperature
dependent
and
most
infections
are
detected
in
warmer
waters
(
Bartholomew
et
al.
1989).
Juvenile
rainbow
trout
exposed
to
the
infective
stage
of
C.
shasta
and
held
at
water
temperatures
of
44.1­
73.9
°
F
(
6.7­
23.3
°
C)
had
little
or
no
ability
to
overcome
the
infection,
with
mean
time
from
exposure
to
death
directly
correlated
to
temperature
(
Udey
et
al.
1975).
As
with
rainbow
trout,
juvenile
coho
salmon
also
showed
a
temperature
dependence
with
mean
time
from
exposure
to
death.
However,
results
of
coho
salmon
experiments
that
showed
progressive
and
significant
increase
in
mortality
with
increased
water
temperature
from
48.9
to
68.9
°
F
(
9.4­
20.5
°
C)
differed
from
results
of
rainbow
trout
experiments
in
which
observed
mortality
appeared
to
be
independent
of
temperature.
Table
2.
Fish
diseases
and
conditions
that
predispose
fish
to
the
disease
Temperature
Interaction
19
Disease
Type
Disease
Etiological
Agent
Optimal
Growth/

Prevalent
Tempsa
Susceptible
Species
Conditions
of
Predisposition
Citations
Bacterial
Furunculosis
Aeromonas
salmonicida
20­
22
°
C/

>
12
°
C
young
salmonids
low
DO,
crowding,
handling
Post
1987,

Piper
et
al.
1982
Motile
Aeromonad
Disease
A.
hydrophila
A.
puctata
20­
22
°
C/

>
12­
14
°
C
all
freshwater
fish
nutritional
deficiencies,
stress,

physical
damage,
low
DO,

overcrowding
Post
1987
Vibriosis
Vibrio
anguillarum
18­
20
°
C/

>
14
°
C
marine
and
estuarine
fish
stress
or
trauma,
handling,
low
DO,

high
salinity
or
organic
loads,

elevated
temperature
Post
1987,
Inglis
et
al.
1993,

Piper
et
al.
1982
Pseudomonad
Septicemia
Pseudomonas
fluourescens
20­
25
°
C/
all
fish
species
stress,
increased
water
temperature,

pH
extremes,
toxic
substance
exposure,
reduced
DO,
poor
nutrition
Post
1987,
Wedemeyer
and
McLeay
1981
Enteric
Redmouth
Disease
(
Yersiniosis)
Yersinia
ruckeri
22
°
C/

11­
18
°
C
rainbow,
steelhead,

cutthroat
trout
coho
and
chinook
salmon
handling,
overcrowding,
reduced
DO,
other
stresses
Post
1987
Columnaris
Disease
Flexibacter
columnaris
28­
30
°
C/

>
15
°
C
freshwater
fish
crowding,
physical
injuries
and
nutritional
deficiencies,
high
water
temperatures,
low
DO,
handling
Post
1987,
Piper
et
al.
1982
Fin
Rot
Cytophaga
spp
4­
10
°
C/

4­
10
°
C
coldwater
and
coolwater
fishes
malnutrition,
toxic
substances
present,
high
pH,
physiological
imbalance
Post
1987
Bacterial
Gill
Disease
various
species
of
flexibacteria,
flavobacteria,
pseudomonads
or
aeromonads
all
fish
species
crowding,
low
DO,
elevated
ammonia,
particulates
in
water,
gill
irritants
Post
1987,
Wedemeyer
and
McLeay
1981
Mycobacteriosis
Mycobacterium
marinum
M.
fortuitum
25­
35
°
C/
all
fish
species
Post
1987
Table
2.
Fish
diseases
and
conditions
that
predispose
fish
to
the
disease
(
continued)

Temperature
Interaction
20
Disease
Type
Disease
Etiological
Agent
Optimal
Growth/

Prevalent
Tempsa
Susceptible
Species
Conditions
of
Predisposition
Citations
Nocardiosis
Nocardia
asteroides
37
°
C
rainbow
and
brook
trout
Post
1987
Ulcer
Disease
Haemophilus
piscium
20­
25
°
C
brook
trout
Post
1987
Flavo­
bacteriosis
Flavobacterium
spp
all
fish
species
injuries,
poor
physiological
condition,
malnutrition,
other
conditions
that
reduce
defenses
Post
1987
Streptococcus
Septicemia
Streptococcus
spp
37
°
C
rainbow
trout
Post
1987
Pasteurellosis
Pasteurella
piscicida
17­
31
°
C
growth
temp
range,
not
necessarily
optimal
brown
trout
(
mainly
eastern
US)
high
temperature,
pollution,
low
DO,

overpopulation
Post
1987
Bacterial
Kidney
Disease
Renibacterium
salmoninarum
15
°
C/
all
salmonid
species
soft
water
(
hardness
<
100
mg/
l)
Post
1987,
Wedemeyer
and
McLeay
1981
Mycotic
(
fungal)
Saprolegniasis
Saprolegnia
parasitica,
Achlya
hoferi
and
Dictyuchus
spp
15­
30
°
C
freshwater
and
brackish
water
fish
malnutrition,
presence
of
toxic
substances,
skin,
fin
or
gill
damage,

temperature,
high
or
low
pH,
high
salinity
Post
1987
Branchiomycosis
Branchiomyces
sanguinis
B.
demigrans
25­
32
°
C/

>
20
°
C
all
fish
species
(
central
U.
S.)
presence
of
organic
contaminants,

algal
blooms
and
water
temperature
>
20
°
C,
low
DO,
low
pH
Post
1987
Parasitic
Ichtyobodiasis
(
Costiasis)
Ichtyobodo
necatrix
and
I.
pyriformis
10­
25
°
C
all
fish
species
crowding,
malnutrition
Post
1987,
Piper
et
al.
1982
Ichthyophthirius
(
Ich)
Ichthyophthirius
multifiliis
24­
26
°
C/

>
12­
15
°
C
freshwater
fish
Post
1987,
Piper
et
al.
1982
Hexamitiasis
Hexamita
spp
most
trout
and
salmon
species
Post
1987
Table
2.
Fish
diseases
and
conditions
that
predispose
fish
to
the
disease
(
continued)

aOptimal
growth
indicates
the
optimal
temperature
for
growth
of
the
etiological
agent.
Prevalent
temperature
indicates
temperatures
at
which
outbreak
of
the
disease
commonly
occurs.

Temperature
Interaction
21
Disease
Type
Disease
Etiological
Agent
Optimal
Growth/

Prevalent
Tempsa
Susceptible
Species
Conditions
of
Predisposition
Citations
Whirling
Disease
Myxosoma
cerebralis
all
salmonid
species
Post
1987
Ceratomyxiasis
Shasta
Ceratomyxa
shasta
rainbow,
cutthroat
and
brook
trout
coho,
chinook,

chum,
and
sockeye
salmon
Post
1987
Proliferative
Kidney
Disease
classification
unsettled
16
°
C
full
disease
development
rainbow
trout
Post
1987
Viral
Infectious
Pancreatic
necrosis
unclassified
virus
20­
23
°
C
young
salmonids
Post
1987
Infectious
Hematopoietic
Necrosis
(
Sockeye
salmon
virus)
Infectious
Hematopoietic
Necrosis
Virus
13­
18
°
C/

<
15
°
C
(
min.
temp
4
°
C)
young
chinook
and
sockeye
salmon
and
rainbow
and
steelhead
trout
Post
1987
Herpesvirus
Herpesvirus
salmonis
rainbow
trout
Post
1987,

Piper
et
al.
1982
22
Temperature
Interaction
Groberg
et
al.
(
1983)
experimented
with
the
effects
of
temperature
on
coho
infected
with
Vibrio
anguillarum.
Where
mortality
occurred,
shorter
mean
time
to
death
with
increasing
temperature
was
observed
among
groups
at
all
temperatures.
Regression
analysis
revealed
linear
relationship
between
water
temperature
and
log10
of
the
mean
time
to
death.
The
authors
assert
that
with
infections
of
Pacific
salmon,
in
vivo
growth
of
the
bacterium
at
water
temperatures
>
59
°
F
(>
15
°
C)
is
often
rapid
enough
to
overcome
host
responses.
However,
when
water
temperatures
are
<
53.6
°
F
(<
12
°
C),
the
in
vivo
growth
rate
of
the
microorganism
is
suppressed
so
that
host
responses
more
often
prevail.
Between
53.6
and
59
°
F
(
12
and
15
°
C),
the
result
may
depend
on
more
subtle
factors
related
to
the
fitness
of
the
host,
such
as
nutritional
condition,
immunological
status,
and
stress
factors.

Infections
are
often
attributed
to
a
compromised
defense
system
of
the
host
fish,
which
can
result
from
a
variety
of
stresses,
including
temperature.
Prespawning
mortalities
of
chinook
and
sockeye
salmon
examined
in
association
with
the
Grand
Coulee
fish
salvage
project
were
affected
by
water
temperature.
Higher
temperatures
tend
to
favor
the
growth
of
invading
pathogenic
microorganisms
and
reduce
the
natural
defenses
of
the
fish
(
Fish
1944).
Development
of
columnaris
disease
in
susceptible
fish
is
temperature
related
and
occurs
primarily
in
fish
that
have
been
injured
or
that
experience
physical
and
nutritional
deficiencies
(
Post
1987).
A
combination
of
conditions
such
as
high
water
temperature,
high
pollution
levels,
low
DO,
high
population
density,
and
presence
of
an
opportunistic
pathogen
caused
pasteurellosis
in
millions
of
white
perch
and
striped
bass
(
Post
1987).
Post
(
1987)
also
indicates
that
saprolegniasis
is
a
secondary
infection
caused
by
toxic
substances
or
damage
from
external
parasites,
stress
from
reduced
water
temperature,
high
or
low
pH,
or
high
salinity.
Similarly,
branchiomycosis
is
a
fungal
disease
of
gill
tissue
that
is
usually
environmentally
induced
by
organic
contaminants,
algal
blooms,
and
water
temperatures
above
68
°
F
(
20
°
C).
Low
DO
and
low
pH
also
have
a
role
in
outbreaks
of
the
disease
(
Post
1987).
Although
Pseudomonad
septicemia
(
caused
by
a
Pseudomonas
bacterium)
usually
occurs
among
cultured
and
aquarium
fishes,
it
can
occasionally
appear
among
wild­
ranging
fishes
during
extremes
of
temperature,
pH,
pollution,
or
other
environmental
stressors.
Reduced
DO,
increased
water
temperature,
and
poor
nutrition
are
factors
that
predispose
the
fish
to
this
disease
(
Post
1987).
Hemorrhagic
septicemias
(
Aeromonas,
Pseudomonas)
may
occur
because
of
low
oxygen,
chronic
exposure
to
trace
contaminants,
elevated
water
temperatures,
or
overwintering
at
low
temperatures
(
Wedemeyer
and
Goodyear
1984).
Maule
et
al.
(
1996)
note
that
the
observed
differences
in
the
prevalence
and
severity
of
Renibacterium
salmoninarum
(
which
causes
bacterial
kidney
disease)
infections
between
Snake
and
Columbia
River
fish
may
have
been
the
result
of
differences
in
water
temperature
and
migration
times,
although
these
factors
were
not
directly
tested.
The
authors
observed
that
fish
sampled
at
dams
from
the
Snake
River
that
had
a
longer
migration
in
warmer
water,
had
higher
prevalence
of
infection
than
those
from
the
Columbia
River
or
fish
hatchery.

Several
diseases
are
not
directly
attributed
to
temperature,
but
are
attributed
to
compromises
caused
by
other
environmental
stressors.
Fin
rot
or
coldwater
disease,
which
is
a
chronic
disease
caused
by
Cytophaga
species
or
subspecies,
is
usually
associated
with
conditions
such
as
malnutrition,
presence
of
toxic
substances,
high
pH,
or
physiological
imbalance
(
Post
1987).
Bacterial
gill
disease
(
Myxobacteria
species)
can
be
caused
by
chronic
low
oxygen
or
elevated
ammonia
and
excessive
particulate
matter
(
Wedemeyer
and
Goodyear
1984).
Flavobacteria
are
23
Temperature
Interaction
usually
opportunistic
pathogens
that
attack
when
fish
are
injured,
in
poor
physiological
condition,
in
a
state
of
malnutrition,
or
in
other
conditions
that
reduce
defenses
(
Post
1987).
All
freshwater
fish
are
susceptible
to
columnaris
disease
(
causative
agent
Flexibacter
columnaris),
but
the
disease
most
commonly
occurs
in
response
to
physical
injuries
and
nutritional
deficiencies
(
Post
1987).

Fish
infected
with
disease
are
also
more
vulnerable
to
other
stressors,
such
as
impacts
from
dissolved
gas
or
suspended
sediments.
Fish
with
moderate
to
high
levels
of
Renibacterium
salmoninarum
are
more
vulnerable
to
the
effects
of
dissolved
gas
supersaturation
and
die
sooner
than
fish
with
lower
levels
of
infection
(
Weiland
et
al.
1999).
The
authors
suggest
that
such
fish
have
a
reduced
metabolic
scope
for
activity
and
have
less
energy
available
to
deal
with
other
stressors.
Servizi
and
Martens
(
1991)
also
noted
that
disease
may
lower
the
tolerance
of
fish
to
suspended
sediments.
In
their
study,
the
combined
stresses
caused
by
suspended
sediments
and
infection
evidently
compounded
to
lower
tolerance
in
the
test
fish.
Tolerance
to
suspended
sediments
may
be
a
combination
of
physical
and
physiological
factors
related
to
oxygen
availability
and
uptake
by
fish
which
are
related
to
temperature.

How
does
temperature
affect
immune
response?

The
species
of
fish
and
its
optimum
environmental
temperature
affect
the
magnitude
and
rapidity
of
immunizing
response.
Immune
response
time
for
antibody
production
is
related
to
environmental
temperature.
In
cold­
water
fish,
immune
response
is
relatively
slow,
whereas
in
warm­
water
fish
immune
response
seems
to
be
more
rapid,
especially
in
the
higher
ranges
of
temperature
acceptability
(
Post
1987).

Does
temperature
influence
the
impact
of
angling
pressure?

Findings
of
Wilkie
et
al.
(
1996)
show
that
Atlantic
salmon
are
more
susceptible
to
delayed
postangling
mortality
under
midsummer
(~
68
°
F
[~
20
°
C])
conditions
than
in
fall
conditions
(~
42.8
°
F
[~
6
°
C]).
The
authors
postulate
that
elevated
water
temperature
has
a
key
role
in
determining
the
different
physiological
responses
of
summer­
angled
and
fall­
angled
salmon.

In
a
related
study,
Wydoski
et
al.
(
1976)
examined
physiological
response
of
rainbow
trout
to
hooking
stress,
including
effects
of
water
temperatures
on
extent
and
severity
of
delayed
physiological
changes.
They
found
a
somewhat
more
severe
blood
chemistry
disturbance
caused
by
hooking
stress
at
higher
water
temperatures.

Is
growth
affected
by
temperature
changes?

Temperature
changes
have
striking
effects
on
food
intake,
maintenance
requirements,
metabolic
rates,
enzyme
processes,
diffusion
of
small
molecules,
membrane
functions,
and
protein
synthesis
rates
(
Houlihan
et
al.
1993).
Water
temperature
has
a
major
influence
on
the
amount
of
food
consumed
by
a
fish
(
Jobling
1994).
Feeding
and
growth
also
are
affected
by
oxygen
levels.
Rates
of
oxygen
consumption
increase
as
the
feeding
conditions
of
fish
are
improved
because
well­
fed
fish
have
higher
metabolic
rates
(
Jobling
1994).
Hence,
when
the
DO
concentration
in
water
is
low,
food
intake
may
be
suppressed
because
there
is
not
enough
24
Temperature
Interaction
oxygen
to
support
the
high
energy
demands
of
a
well­
fed
fish.
A
reduction
in
food
intake
at
low
DO
levels
would
undoubtedly
have
consequences
for
growth.
When
rainbow
trout
were
reared
at
59
°
F
(
15
°
C)
under
differing
levels
of
DO,
food
intake
was
reduced
when
oxygen
saturation
fell
below
60%,
and
growth
and
food
conversion
efficiency
appeared
to
be
affected
when
saturation
fell
below
70%
(
Jobling
1994).
DO
levels
are
closely
tied
to
water
temperatures,
with
increasing
temperature
leading
to
decreased
solubility
of
oxygen.
In
elevated
temperature
regimes,
growth
could
be
compromised
through
synergistic
effects
of
low
DO
and
elevated
temperature.

What
is
the
importance
of
temperature
to
salmonid
food
resources?

An
environmental
stressor
that
is
not
directly
lethal
still
can
act
indirectly
by
reducing
the
availability
of
food
during
a
critical
life
stage
(
Johnson
1968,
as
cited
in
Wedemeyer
and
Goodyear
1984).
The
reduced
ration
would
decrease
growth
and
possibly
increase
predation,
malnutrition,
and
disease.
Temperature
vastly
influences
the
aquatic
insect
community
on
which
salmonids
rely
for
much
of
their
food
source.

Temperature
is
extremely
significant
to
aquatic
insect
life
history,
affecting
growth,
metabolism,
reproduction,
emergence,
and
distribution
(
Vannote
and
Sweeney
1980).
Aquatic
insects
respond
to
the
entire
temperature
regime,
including
overall
levels,
seasonal
and
daily
ranges,
rate
functions,
and
the
timing
and
duration
of
thermal
events.
Latitudinal
distributions
of
some
aquatic
insects
appear
to
be
determined
in
large
part
by
temperature
(
Ward
1992).
Because
aquatic
insects
generally
lack
well­
developed
temperature
compensation
mechanisms
(
Vannote
and
Sweeney
1980),
the
temperature
of
the
habitat
is
of
greater
importance
than
for
animals
able
to
maintain
a
relatively
constant
metabolic
rate
over
a
wide
range
of
temperatures.
According
to
Vannote
and
Sweeney
(
1980),
adult
body
size,
metabolic
efficiency,
fecundity,
and
abundance
will
be
greatest
near
the
center
of
a
species'
range
where
the
temperatures
are
optimal.
Conversely,
populations
living
where
thermal
conditions
are
less
optimal
will
be
smaller
and
less
fecund,
with
correspondingly
reduced
competitive
ability.
Decreased
body
size
and
fecundity
in
overly
warm
habitats
result
from
the
increased
cost
of
maintenance,
whereas
decreased
body
size
and
fecundity
in
overly
cool
habitats
result
from
reduced
assimilation
rates,
with
more
energy
allocated
to
adult
tissue
maturation
and
less
to
larval
growth.
Ward
(
1992)
explains
that
other
factors
in
addition
to
temperature
are
involved
in
the
translation
of
high
fecundity
into
population
density.

The
thermal
environment
is
important
within
the
various
life
stages
of
aquatic
insects.
Temperature
affects
fecundity,
and
the
responses
of
eggs
to
temperature
changes
influence
distribution
of
aquatic
insects
and
the
competitiveness
of
a
species
at
a
given
locale
(
Ward
1992).
Temperature
may
influence
the
egg
incubation
period,
hatching
success,
duration
of
hatching,
and
induction
and
termination
of
diapause.
Temperature
helps
to
regulate
seasonal
changes
in
growth
rates
of
aquatic
insects
and
operates,
at
least
to
some
extent,
independently
of
nutritional
factors.
Temperatures
that
are
optimal
for
high
growth
rates
may
not
be
optimal
for
growth
efficiency,
emergence
success,
or
adult
longevity.
Intra­
and
interspecies
variability
in
the
number
of
generations
per
year
is
normally
attributed
to
thermal
differences
between
habitats
at
different
latitudes
or
altitudes.
Timing
and
duration
of
emergence
of
aquatic
insects
involves
responses
to
temperature,
often
interacting
with
length
of
daylight.
25
Temperature
Interaction
Temperature
influences
the
growth
of
aquatic
insects
directly
through
its
effects
on
feeding
and
assimilation
rates,
and
indirectly
by
determining
the
composition,
quantity,
and
quality
of
food
available
(
Ward
1992).
Growth
of
some
aquatic
insects
is
regulated
by
the
interaction
of
temperature
and
food
quality;
seasonal
changes
in
food
quality,
partly
caused
by
temperature,
may
determine
the
effect
of
a
given
temperature
on
growth
(
Ward
1992).

The
complexity
of
temperature
and
its
relation
to
salmonid
food
supplies
is
illustrated
in
a
study
by
Li
et
al.
(
1994)
on
the
cumulative
effects
of
stream­
bank
disturbance
on
the
food
chain
of
high­
desert
trout
streams.
The
authors
found
that
watersheds
with
greater
canopy
along
steam
banks
had
higher
numbers
of
rainbow
trout,
lower
daily
maximum
temperatures,
and
perennial
flow.
Significant
correlations
were
found
between
exposure
to
the
sun
and
algae
amounts,
algae
amounts
and
total
number
of
invertebrates,
algae
amounts
and
number
of
plant­
eating
invertebrates,
and
number
of
total
invertebrates
and
herbivorous
invertebrates.
However,
there
was
no
significant
correlation
between
number
of
trouts
and
number
of
either
total
invertebrates
or
plant­
eating
invertebrates.
As
temperature
increased,
trout
numbers
decreased
in
relation
to
the
decrease
in
invertebrates.
The
authors
attribute
this
to
metabolic
expenditures
being
greater
than
could
be
offset
by
increases
in
food
supply,
and
to
shifts
in
the
food
chain
that
make
the
food
supplies
more
limited
(
less
palatable
trout
prey
dominate
the
food
base
in
warm­
water
reaches).

How
does
temperature
affect
photobiology?

Indirectly,
temperature
can
affect
the
amount
of
light
entering
a
waterbody.
Algal
species
prefer
certain
temperature
ranges
(
Hodges
1977),
and
their
productivity
is
limited
by
environmental
factors
such
as
light,
temperature,
and
nutrients.
If
these
factors
are
improved,
productivity
can
increase
substantially.
Increased
productivity
can
lead
to
accumulation
of
silt,
leading
to
shallower
and
warmer
water
and
encroachment
of
vegetation
along
the
edges
of
lake
or
stream
systems,
ultimately
creating
a
eutrophic
condition
(
Rost
et
al.
1979).
Eutrophication
reduces
water
clarity
by
creating
more
turbidity
and
less
light
penetration.
Thus,
elevated
water
temperatures
could
ultimately
lead
to
lower
light
penetration
which
may
coincide
with
a
decrease
in
salmonid
vision.

How
well
are
these
interactive
relationships
understood?

Most
laboratory
experiments
address
single
stressors
while
providing
optimal
conditions
for
all
the
other
processes.
Even
controlled
experiments
investigating
multiple
stressors
usually
provide
optimum
conditions
for
any
processes
outside
the
test
variables.
It
is
extremely
difficult
to
conduct
experiments
that
allow
a
detailed
analysis
of
several
environmental
factors.
Extending
the
results
of
such
experiments
to
a
population
living
in
a
natural,
complex
setting
is
a
challenge,
because
the
impact
of
a
stressor
could
be
either
more
or
less
pronounced
in
a
natural
setting
than
in
the
laboratory.

What
is
the
likelihood
of
exposure
of
salmonids
to
multiple
stressors?

The
issue
of
multiple
stressors
facing
salmonids
is
very
real
in
the
Pacific
Northwest.
As
an
example,
Oregon's
1998
303(
d)
List
of
Water
Quality
Limited
Waterbodies
reports
that
the
26
Temperature
Interaction
Columbia
River
reach
from
the
mouth
to
Tenasillahe
Island
now
has
limited
quality
because
of
bacteria,
temperature,
DO,
total
dissolved
gas,
and
toxics
(
tissue
and
water).
The
reach
from
Tenasillahe
Island
to
the
Willamette
River
is
water
quality
limited
for
the
same
reasons
and
for
pH.
In
addition,
analysis
of
water
samples
collected
for
the
Lower
Columbia
River
Bi­
State
Water
Quality
Program
detected
metals
with
an
average
frequency
of
30%,
and
64%
of
these
detections
exceeded
the
State
or
Federal
chronic
criterion
(
Tetra
Tech
1993).
The
metals
exceeding
the
criterion
were
aluminum,
cadmium,
copper,
iron,
lead,
selenium,
and
zinc.

Often,
situations
that
cause
stress
for
fish
are
related
to
a
combination
of
impacts.
An
example
is
the
major
effects
of
livestock
grazing
on
stream
and
riparian
ecosystems
in
the
arid
Western
United
States.
Belsky
et
al.
(
1999)
found
that
in
addition
to
increases
in
water
temperature
resulting
from
reduced
shade,
increased
solar
exposure,
widening
of
stream
channels,
and
lower
summer
flows,
many
other
impacts
are
associated
with
grazing.

Increases
in
nutrient
concentrations
can
stimulate
algal
and
aquatic
plant
growth.
In
excess,
nutrients
stimulate
algal
blooms,
and
subsequent
decomposition
reduces
the
DO
in
the
stream.
Soil
compaction
can
lead
to
a
reduction
in
water
storage
capacity
resulting
in
decreases
in
the
amount
of
aquatic
habitat
with
summer
and
late­
season
low
flows.
Competitive
behavior
and
predation
pressure
will
escalate
as
aquatic
habitat
decreases.
Increases
in
erosion
due
to
removal
of
vegetational
cover
can
increase
sediment
load
to
streams
and
result
in
loss
of
pools
and
pool
volume,
reduced
foraging
success
by
aquatic
organisms,
and
reduced
DO
in
substrates.
Ultimately,
these
combined
stresses
of
increased
water
temperature,
greater
turbidity
and
siltation,
low
DO,
damage
to
spawning
beds,
fewer
insects
and
other
food
items,
decreased
hiding
cover,
and
reduced
resistance
to
waterborne
diseases
can
decrease
fish
species
diversity,
abundance,
and
productivity.

Cattle
grazing
is
not
the
only
factor
damaging
stream
and
riparian
habitats
in
the
Pacific
Northwest.
Urban
development,
mining,
damming,
road
construction,
logging,
and
agricultural
activities
have
also
exacted
heavy
tolls
on
riparian
and
aquatic
ecosystems.
These
factors
have
caused
cumulative
impacts
on
Western
streams
and
created
stress
for
salmonid
populations.

What
other
complexities
of
multiple
stressors
need
to
be
considered?

Numerous
elements
are
not
directly
affected
by
temperature
yet
are
relevant
to
the
discussion.
For
example,
young
fish
need
to
extend
more
energy
to
swim
through
slack
water
created
by
dams
as
compared
with
moving
downstream
with
a
current.
At
elevated
temperatures,
the
energy
cost
would
be
even
greater
given
the
increased
metabolic
demands
of
fish.
Another
consideration
is
that
fish
often
live
in
simplified
environments,
devoid
of
habitat
diversity
they
can
use
to
behaviorally
thermoregulate.
This
impairs
the
salmon's
natural
survival
strategies.
The
physical
changes
in
habitat
(
e.
g.,
reservoirs,
channelization)
and
hydrology
(
e.
g.,
flow
timing,
volume)
that
have
occurred
throughout
the
majority
of
waters
in
the
Pacific
Northwest
are
additional
stressors.
27
Temperature
Interaction
Have
any
States
addressed
these
temperature
relationships
within
their
water
quality
criteria?

Certain
temperature
relationships
are
much
better
understood
than
others.
For
example,
the
relationship
of
temperature
and
dissolved
oxygen
has
been
well
studied
and
documented,
as
has
the
temperature­
ammonia
relationship.
In
the
case
of
ammonia,
EPA's
national
criteria
(
adopted
by
many
States)
are
based
on
ambient
pH
and
temperature.
Other
temperature
relationships,
as
exhibited
with
some
organic
chemicals,
are
not
as
invariable
or
well
understood,
and
temperature
has
not
been
incorporated
into
any
national
or
State
criteria.

Oregon's
review
of
temperature
(
ODEQ
1995)
recognizes
that
in
considering
interacting
variables
and
stressors,
whether
to
control
temperature
or
some
other
variable
depends
on
which
factor
is
controllable.
The
ODEQ
Temperature
Issue
Paper
(
1995)
realizes
that
in
lower
mainstem
reaches
with
point
sources,
biochemical
oxygen
demand
(
BOD)
is
likely
to
be
the
more
controllable
factor.
Less
can
be
done
in
these
reaches
to
reduce
temperature.
Upper
basin
reaches
are
at
higher
altitudes,
often
above
point
sources,
and
are
often
spawning
and
rearing
locations
for
migrating
and
resident
salmonids.
In
these
reaches
it
is
more
likely
that
temperature,
rather
than
BOD,
is
being
increased
by
human
activity.
With
the
technical
literature
showing
that
aquatic
organisms
exposed
to
low
DO
are
under
significant
stress
and
that
these
organisms
undergo
additional
stress
when
water
temperature
increases,
the
ODEQ
addressed
this
interactive
effect
in
its
last
revision
to
the
State
water
quality
standards.
The
provision
is
in
the
form
of
a
narrative
criterion
stating
that
there
will
be
no
increase
in
temperature
from
human
sources
when
DO
levels
are
within
0.5
mg/
L
of
the
DO
criterion.

What
tools
are
available
to
help
evaluate
these
multiple
stressors
and
the
effects
to
salmonid
populations?

The
presence,
abundance,
diversity,
and
distribution
of
fish
communities
depend
on
their
ability
to
respond
to
a
variety
of
physical
and
chemical
factors,
yet
typically
risk
assessment
is
limited
to
a
single
stressor.
Methods
for
analyzing
and
assessing
the
interaction
of
multiple
stressors
need
to
be
further
developed
or
refined.
Some
models
have
attempted
to
evaluate
for
multiple
stressors,
but
these
models
have
limitations
and
may
not
have
extended
utility
in
the
Pacific
Northwest.

Conclusions
When
fish
are
stressed
for
any
reason,
they
are
less
able
to
deal
with
other
stressors.
Alternatively,
if
fish
are
living
under
optimal
conditions,
they
are
better
able
to
handle
any
single
or
multiple
stressors
that
develop.
If
a
temperature
standard
can
make
temperatures
more
suitable
for
salmonid
populations
in
the
Pacific
Northwest,
it
is
expected
that
other
interrelated
stressors
would
not
be
as
detrimental.

When
setting
a
standard,
we
probably
cannot
control
for
the
numerous
stressors
that
interact
with
temperature.
A
safety
factor
is
often
included
when
developing
water
quality
criteria
in
28
Temperature
Interaction
order
to
accommodate
combinations
of
stressors.
Such
a
factor
does
not
control
for
all
effects
to
salmonids,
but
controls
for
known
and
unknown
variation
within
the
multitude
of
natural
stressors.

For
many
of
the
chemical
variables
that
can
be
influenced
by
temperature,
information
is
scant
or
shows
no
pattern
to
consistently
explain
temperature
effects.
However,
much
more
information
exists
regarding
oxygen's
relationship
with
temperature.

The
ammonia
criteria
adopted
by
Oregon,
Washington,
and
Idaho,
and
recommended
in
national
guidance,
already
incorporate
ambient
temperature.
Thus,
there
is
no
further
need
to
address
ammonia
in
regional
temperature
criteria.
Several
other
interrelated
chemical
stressors
have
criteria
in
place,
although
temperature
is
not
embodied
within
them.
As
with
ammonia,
it
is
not
necessary
to
address
these
chemicals
further.

Most
fish
diseases
are
favored
by
increased
water
temperatures.
Warming
temperatures
often
increase
the
abundance
or
virulence
of
disease
organisms.
In
addition,
warming
temperatures
also
may
lessen
the
ability
of
a
fish
to
withstand
the
stress
of
disease.

In
many
Pacific
Northwest
streams,
salmonids
are
faced
with
multiple
stressors
as
a
result
of
human
activities.
A
temperature
criterion
alone
cannot
control
for
this
myriad
of
stressors.
For
example,
the
effects
of
predation
from
warm­
water
exotic
species
may
not
be
controllable
within
the
natural
temperature
potential
or
temperature
standard.
The
temperature
criteria
cannot
be
used
to
remediate
for
these
species
or
to
create
artificial
temperatures.

Addressing
temperature
alterations
is
just
one
aspect
of
protecting
native
salmon
stocks.
To
fully
safeguard
survival
and
recovery
of
these
fish,
other
stressors
also
need
to
be
controlled
to
some
degree.
Even
if
the
recommended
temperature
standard
provides
for
optimal
thermal
regimes,
the
standard
alone
cannot
completely
safeguard
salmonid
persistence.

Literature
Cited
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.

Allen
JD.
1995.
Stream
ecology:
Structure
and
function
of
running
waters.
Dordrecht,
the
Netherlands:
Kluwer
Academic
Publishers.
388
pp.

Bartholomew
JL,
Rohovec
JS,
Fryer
JL.
1989.
Ceratomyxa
shasta,
a
myxosporean
parasite
of
salmonids.
US
Fish
Wildlf
Serv,
Fish
Disease
Leaflet
#
80.
10
pp.

Becker
CD,
Wolford
MG.
1980.
Thermal
resistance
of
juvenile
salmonids
sublethally
exposed
to
nickel,
determined
by
the
critical
thermal
maximum
method.
Environ
Pollut
(
Ser
A)
21:
181­
189.

Beiningen
KT,
Ebel
WJ.
1970.
Effect
of
John
Day
Dam
on
dissolved
nitrogen
concentration
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