Appendix L

Maximum Temperature:

Upper Optimal Temperature Limits for Salmonids in the Willamette and
Lower Columbia Rivers

***Ann Richter*** ***and*** ***Steven Kolmes***

***Environmental Studies Program, University of Portland***

Introduction

The Willamette/Lower Columbia River Technical Recovery Team (WLC-TRT) is
responsible for recommending delisting criteria. As these criteria need
to address all the factors for species listing, they must make reference
to habitat.

Adequate water quality is important to all salmonids at all life-history
stages. The distributions of native salmonid fish in the Pacific
Northwest are strongly tied to temperature conditions in their habitats.
Because water temperature affects the health of individual fish, it also
affects entire populations and species assemblages. Temperature may
directly affect salmonids in obvious ways, or indirectly through
interaction with other important variables (Dunham et al. 2001). For
example:

-   Given sufficient magnitude and time, high temperatures can cause
    weight loss, disease, competitive displacement by species better
    adapted to the prevailing temperature, or death (Sullivan et al.
    2000).

-   When fish are stressed by any one process, they are less able to
    deal with other stressors. Salmonids already stressed by high water
    temperature will be less able to deal with a second stressor (e.g.,
    toxic pollutant, pathogen). Warmer temperatures often increase the
    infection rate or virulence of fish pathogens and lessen the ability
    of a fish to withstand disease (Materna 2001).

Human Influence on Thermal Regimes

In many streams that once were inhabited by large salmon runs,
temperature regimes are now inhospitable. An important factor in the
recovery of salmonid populations is the restoration of temperature
regimes (Poole et al. 2001a, b).

Human activities can affect thermal regimes by simplifying the physical
structure of aquatic systems, thereby eliminating natural thermal
buffers and insulators (Poole and Berman 2001). Clearing and developing
land, dredging or straightening streams, grazing and other land-use
activities influence temperature regimes by altering factors external to
the stream, structures within the stream, and the amount of water
flowing in the stream (Poole et al. 2001a, b). These activities often
directly or indirectly simplify the structure of stream channels or
riparian zones, as has occurred in the lower Willamette River (Sedell
and Froggatt 1984). This type of channel simplification can potentially
increase temporal variability and decrease fine-scale spatial
variability in stream temperature, both of which may have negative
consequences for salmonids (Poole et al. 2001b, Poole and Berman 2001).
Removing riparian vegetation in small streams, where shading is
important, can increase daily variation in stream temperature (Beschta
1997). For streams where groundwater buffers temperature, change in
groundwater temperature or flow dynamics can alter the seasonal
availability of cold water, including increased seasonal variation in
water temperature. Small-scale thermal refugia can provide important
habitat for salmonids during periods of warmer water temperatures
(Ebersol 2002), but even slight changes in temperature extremes, or mean
temperature, can result in refugium, and therefore salmonid, loss.
Changes in the timing of maximum and minimum temperatures can occur with
or without associated changes in the actual values of maximum, minimum,
or mean stream temperatures, and these too can threaten salmonids
because of their sensitivity to temperature at many life stages. Water
temperature is an indicator of habitat quality, which is an integrator
of what is happening in a watershed.

Thermal refugia are important in maintaining salmonid populations
because when daily variation in stream temperature is high, salmonids
may be exposed to stressful or lethal temperatures for part of the day.
Thermal refugia provide protection for salmonids when temperatures are
extreme (Ebersol 2002). At peak summertime temperatures, only a small
percentage of habitat in some streams may be cool enough. Loss of
riparian vegetation, the elimination of large beaver populations,
removal of large woody debris, channel simplification, reduced
groundwater discharge due to changes in upland vegetation, water
withdrawals, and other human activities cause the loss of the fine-scale
spatial distribution of appropriate thermal habitats upon which salmon
rely (Poole et al. 2001b). This can cause fish to migrate greater
distances to find appropriate habitats or not find them at all.

In the same way, seasonal variation in temperature can create thermal
barriers to salmonid immigration and emigration. Anthropogenic
activities can increase the coarse-scale temporal variation of streams,
exposing salmonids to extremes beyond the normal range of variation and
resulting in habitat fragmentation and elimination of the large,
well-connected tracts of high-quality thermal habitat. This habitat
fragmentation has been shown to degrade both population structure and
persistence (Poole et al. 2001b).

In a recent draft document entitled Draft EPA Region 10 Guidance for
State and Tribal Water Quality Standards,[^1] the U.S. Environmental
Protection Agency (EPA) recommended a four-part approach for state and
tribal temperature standards to support native salmonids. This approach
includes the adoption of:

1.  thermal, potential numeric criteria for bodies of water, which are
    estimations (generally on the subbasin scale) of the thermal
    potential of bodies of water based on an average meteorological
    year, with adjustments for other climatic conditions;

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2.  interim, species-life-stage numeric criteria as a bridge until a
    newer approach to temperature criteria is developed;

3.  temperature management plan provisions; and

4.  provisions to protect existing cold-water areas.

The EPA criteria are based on salmonid guilds. These guilds are
described by the EPA as groups of species sharing similar life
strategies, with similar temperature and habitat needs and limitations.
In the Pacific Northwest, the cold-water guild includes the five Pacific
salmon, anadromous steelhead trout, and coastal cutthroat and rainbow
trout. This document discusses the species-specific data that exist, and
then uses them as background criteria to support the EPA's recommended
guild approach. The EPA draft criteria are being considered for
application to potential salmonid habitat, as distinct from present or
historical salmonid habitat. Potential habitat has not been explicitly
identified by the EPA, but consists of those areas salmonids might
inhabit without the dismantling of major barriers to passage. Whether
the use of the potential habitat concept comes to closely match the
spatial distribution and population number requirements eventually
adopted by the National Marine Fisheries Service (NMFS) for delisting
threatened or endangered salmonids, the guild approach associated with
it can be evaluated separately in terms of maximum temperature criteria
for salmonid delisting.

This paper will summarize the large body of information about thermal
effects on salmonids, specific to life stage and species, and use that
information to propose draft water temperature criteria. Several groups
that recently produced white papers on the topic are the Pacific
Northwest Environmental Indicator Work Group (PNWEIWG), the Sustainable
Ecosystems Institute (SEI), the EPA Water Temperature Criteria Technical
Workgroup, the Columbia River Inter-Tribal Fish Commission, and the
Washington State Department of Ecology. The participating agencies in
the PNWEIWG are the British Columbia Ministry of Environment, Lands, and
Parks; the Alaska Department of Environmental Conservation; the Idaho
Division of Environmental Quality; the Washington State Department of
Ecology (WDOE); Environment Canada; and the U.S. EPA (Region 10). In
1997, directors of these agencies asked the PNWEIWG to pilot development
of regional indicators associated with risks to salmonid stocks.
Indicators were required to: (1) have data available, (2) be integral to
measuring the performance of salmon issues for PNWEIWG agencies, and (3)
be able to be reported cost-effectively in a monitoring program.

Martin Environmental, Parametrix Inc., and Weyerhaeuser Company
participated in the SEI, which was funded by the Oregon Forest
Industries Council, Washington Forest Protection Association, and
Weyerhaeuser Company. The SEI developed a risk-based approach to analyze
summer temperature effects on juvenile salmon species in their December
2000 publication, *An Analysis of the Effects of Temperature on
Salmonids of the Pacific Northwest with Implications for Selecting
Temperature Criteria* (Sullivan et al. 2000). This report reviewed the
aspects of temperature affecting the rearing of salmonid species in the
freshwater environment and discussed lethal (acute) as well as sublethal
(chronic) effects. The main focus of the report was on temperatures
affecting growth and mortality (Sullivan et al. 2000).

The EPA established the Water Temperature Criteria Technical Workgroup
to assist in developing temperature criteria guidance for EPA Region 10.
The purpose of the EPA guidance is to help Pacific Northwest states and
tribes adopt water temperature standards that (1) meet the biological
requirements of native salmonid species (Pacific salmon, trout, and
charr) for survival and recovery pursuant to the Endangered Species Act
(ESA); (2) provide for the protection and propagation of salmonids under
the Clean Water Act (CWA); and (3) meet the salmonid restoration goals
of federal trust responsibilities with treaty tribes. The technical
workgroup, a panel of experts on salmonid biology and stream
temperature, represented the following agencies: EPA, U.S. Forest
Service, WDOE, NMFS, U.S. Fish and Wildlife Service, Columbia River
Inter-Tribal Fisheries Commission, Idaho Department of Environmental
Quality, Oregon Department of Environmental Quality, U.S. Geological
Survey (USGS) Biological Resources Division, and USGS Water Resources
Division. In 2001, the technical workgroup submitted a final summary
report to the policy workgroup of the EPA Region 10 Water Temperature
Guidance Project entitled *Technical Synthesis: Scientific Issues
Relating to Temperature Criteria for Salmon, Trout, and Charr Native to
the Pacific Northwest.*[^2] Five technical summaries on the major
physical and biological considerations for developing water temperature
standards were developed to provide a scientific foundation for the
project:

1.  thermal effects on salmonid physiology (McCullough et al. 2001),

2.  thermal effects on salmonid behavior (Sauter et al. 2001),

3.  interactions between multiple stressors---thermal and
    other---affecting salmonids (Materna 2001),

4.  thermal influences on salmonid distribution (Dunham et al. 2001),
    and

5.  spatial and temporal variation in patterns of stream temperature
    (Poole et al. 2001a, b).

McCullough (1999) of the Columbia River Inter-Tribal Fish Commission,
prepared a summary report for EPA Region 10, in which he reported that
significant impacts to survival due to temperature regime can occur in
all life stages. Sublethal impacts to life processes such as growth,
survival, reproductive success, migration success, disease, feeding,
territoriality, aggressiveness, swimming, and bioenergetics can
cumulatively result in diminished survival and production of the
population.

In December 2000, the WDOE Water Quality Program released a draft
discussion paper and literature summary addressing temperature criteria
that included recommendations for chinook, coho, and chum salmon and
steelhead at critical life stages (WDOE 1999). The recommendations were
based on a thorough review of the literature and laboratory data
adjusted for application to natural waters.

The following sections discuss the scientific findings on the thermal
effects and requirements of salmonids, in general and by individual
species, and attempt to draw together materials from the documents
listed above.

##### 

General Salmonid Data

Smoltification

High temperatures during the smolt phase can result in outright
lethality, premature smolting, blockage of seaward migration,
desmoltification, shifts in emigration timing resulting in decreased
survival in the marine environment, and other stresses detrimental to
fitness. Temperatures that have been reported for impairing
smoltification are above a range from approximately 12º to 15ºC or more
(McCullough et al. 2001).

Adult Migration

Thermal blockages to adult salmon migration have also been identified.
Migration blockages occur consistently in the temperature range of 19º
to 23ºC (McCullough et al. 2001). For chinook and sockeye salmon and
steelhead in the Columbia River 21.7º to 23.9ºC has been cited as the
temperature range blocking migration (Fish and Hanavan 1948).

Spawning

Elevated temperatures can cause migration delays in salmonids that alter
timing of key processes, such as spawning, or can lead to stress,
disease, bioenergetic depletion, or death. If salmonids such as fall
chinook or coho are exposed to high temperatures just before or during
spawning, gametes held internally in adults can be severely affected,
resulting in a loss of viability that appears as poor fertilization rate
or embryo survival. McCullough et al. (2001) concluded that egg
mortality, alevin development, and egg maturation are negatively
affected by exposure to temperatures above approximately 12.5º to 14ºC.
A spawning temperature range of 5.6º to 12.8ºC (maximum) appears to be a
reasonable recommendation for Pacific salmon, unless colder thermal
regimes are natural in any tributary (McCullough et al. 2001).

Lethality

Analysis of lethal temperature suggested that a threshold of 26°C for
annual maximum temperature is a signal of imminent risk of direct
mortality (Sullivan et al. 2000). A site-specific analysis of duration
of exposure when annual maximum temperature is between 24°C and 26°C is
also recommended to ensure that duration/magnitude thresholds are not
exceeded. These annual maximum temperature values are intended to apply
to all salmon and trout species in natural rivers and streams in the
Pacific Northwest (Sullivan et al. 2000).

Distribution

After a review of field studies for chinook salmon, steelhead, and
rainbow trout, McCullough (1999) showed that the distributional limit of
these salmonids corresponds approximately to a mean daily water
temperature of 20°C and a maximum daily water temperature of 22º to
24°C. Hokanson et al. (1997) showed that water temperatures greater that
23ºC, even for short periods (hours), result in Pacific salmon and trout
moving into cold-water refugia. Eaton et al. (1995) proposed a higher
(95^th^ percentile) weekly mean temperature tolerance for chinook (24°C)
and coho (23.4°C) salmon, when the fish temperature database matching
system (FTDMS) approach was used to evaluate various distribution
records for 30 common North American fish species. However, when using
the FTDMS approach, the existence of thermal refugia provides a
potential source of error (Eaton 1995), and leads to recommendations
inconsistent with other studies. Many important salmon diseases become
virulent above 15.6°C, which makes the impact to population production
potentially more severe, because as temperatures rise toward the limits
to salmonid growth, the mortality rate increases. The balance may shift
to zero net growth, even at lower temperatures. In general, juvenile
salmonids appear to have final temperature preferences in the range
11.7° to 14.7°C (Ferguson 1958, Countant 1977, Jobling 1981, McCullough,
1999).

From a behavioral perspective, Sauter et al. (2001) suggest that water
temperature affects some aspects of juvenile life-history patterns,
including duration of freshwater rearing and outmigration timing.
Elevated water temperatures inhibit gill ATPase activity, an enzyme that
prepares juvenile salmonids for osmoregulation in seawater during
emigration. Decreased gill ATPase activity is associated with loss of
migratory behavior in anadromous juvenile salmonids. Spring water
temperatures must not exceed 12ºC for successful smoltification in
steelhead. For spring chinook and coho this value is 15ºC, and it may be
higher for summer migrating fall chinook subyearlings (Zaugg and Wagner
1973). In addition, higher water temperatures and longer exposure to
warm water increase the feeding rate of predatory species consuming
juvenile salmonids. Interspecific competition also appears to play a
role in the distribution and thermal preferences of juvenile salmonids
(Sauter et al. 2001).

Swimming Speed

If water temperature is too high, changes in swimming speed can impair
adult migration. Fish may refuse to migrate, migrate back downstream, or
seek shelter in tributaries or other available cold-water refugia.
Swimming speed is also vital to smolts' ability to maintain position in
the current, control rate of descent, and avoid obstacles. In addition,
high temperature can impair their ability to swim in quick bursts, which
is necessary to avoid predators (McCullough et al. 2001).

Chemical Constituents

Many chemical constituents are affected by temperature. Most notably,
dissolved oxygen (DO) decreases with increasing temperature. When fish
experience temperature stress, they may also experience stress from low
DO levels. McCullough (1999) showed that adult migration of chinook
salmon can be impeded when temperature and DO requirements are not met.
It is also well documented that the concentration of ammonia increases
with increasing temperature (EPA 1985). Although there is no single
pattern that explains the effects of temperature on the toxicity of
pollutants to aquatic organisms, some evidence shows that temperature
may change the rate of toxification under chronic exposures (Mayer et
al. 1994). Since rising temperatures result in an increase in metabolic
processes, gill ventilation must also rise proportionately (Heath and
Hughes 1973). Black et al. (1991) showed that an increase in water flow
over the gills, which may result from increased gill ventilation at
increased temperature, resulted in rapid uptake of toxicants via the
gills. Sublethal exposure to toxicants can reduce the upper lethal
temperatures of fish, constricting the thermal tolerance zone (Paladino
et al. 1980), and fish that are weakened by other causes may be much
more sensitive to toxic chemicals (Jobling 1994). Temperature has been
found to significantly increase the toxicity of some organic chemicals
such as terbufors, trichlorfon, and 2,4 dinitrophenol (Howe et al.
1994), as well as some metals such as mercury (MacLeod and Pessah 1973,
Materna 2001). There is evidence that higher temperatures can help fish
to withstand ammonia (cited in Sullivan et al. 2000).

Disease

Most fish diseases are exacerbated by higher water temperatures (Ordal
and Pacha 1963) and can infect salmon at many life stages. Diseases
associated with warm water in the Pacific Northwest are well documented.
They include the bacterial infections *columnaris,* caused by
*Flexibacter columnaris*; bacterial kidney disease (BKD), caused by
*Renibacterium salmoninarum*; the bacterial pathogens *Aeromonas
salmonicida*, *A. punctata*, *A. hydrophila*; and the protozoan parasite
*Ceratomyxa shasta*. Evidence from Idler and Clemens (1959), Williams et
al. (1977), Bouck et al. (1970) (as cited by EPA and NMFS 1971), and
Ordal and Pacha (1963) indicates that temperatures of 16.7º to 20ºC or
higher, lead to infection of adult salmon with *columnaris,* even with
exposure to low-virulence strains, and infection can occur at even lower
temperatures with high-virulence strains. Evidence from Colgrove and
Wood (1966) indicates that temperatures between 13.9º and 15.6ºC
constitute a transitional temperature region below which recovery from
*columnaris* after infection could occur, and above which infection and
mortality increase. Laboratory and field studies by numerous
investigators show that infection and morality by *columnaris* disease
were negligible at temperatures ≤ 12.8ºC, but temperatures ≥ 15ºC
produced significantly increased mortalities. Not only do juvenile
survival rates decrease with increasing temperature, but Fryer and
Pilcher (1974) also showed that time to death decreases with increasing
temperature for juvenile chinook salmon, coho salmon, and steelhead
(Materna 2001).

BKD is also a prevalent disease in which temperature has been shown to
have an effect on the mortality of infected salmonids. In an experiment
involving infected sockeye, coho, and steelhead over a range of
temperatures from 4° to 20.5°C, the highest mortalities due to BKD
occurred at 12.2°C, with declining mortalities at higher or lower
temperatures (Fryer and Sanders 1981, as cited in Chapman et al. 1991).
It is important to remember that elevated temperatures do not increase
mortality from all salmonid diseases; in fact, some diseases have higher
mortalities at temperatures well within an otherwise optimal range.

Groberg et al. (1978) studied the relationship of water temperature to
infections of coho salmon, chinook salmon, and steelhead with *A.
salmonicida* and *A. hydrophila*. Among the three salmonid species, at
3.9º and 6.7°C, mortality in fish infected with *A. salmonicida* varied
from 2 to 26%; at 20.5°C, 93 to 100% died within 2 or 3 days; at 6.7°C
or lower survival was 12 to 23 days. Results from experiments with *A.
hydrophila* gave similar results. At 20.5°C, mortality ranged from 64 to
100%; at 9.4°C or below, no deaths occurred.

General Recommendations for Salmonids

The Pacific Northwest Salmon Habitat Indicators Work Group (PNWSHIWG).
(1998) identified maximum water temperature as an influence on salmonid
migration patterns, development of eggs to alevins, fry emergence,
metabolism, behavior, susceptibility to parasites and disease, and
mortality. Water exceeding 20°C was categorized as causing "severe
impairment."

Chinook Salmon Data

Incubation and Early Fry Development

Based on the works of Donaldson (1955), Garling and Masterson (1985),
Seymour (1956), Eddy (1972, as cited in Raleigh et al. 1986), Burrows
(1963), Baily and Evans (1971), Heming (1982), Heming et al. (1982**)**,
the following temperatures are strongly suggested to provide optimum
conditions for incubation and early fry development for chinook salmon.
Constant temperatures above 9º to 10ºC may reduce the survival of
embryos and alevins. Temperatures of 11º to 12ºC can still result in
good survival, however the results are consistently less than what is
produced at lower temperatures (McCullough et al. 2001). Incubation
temperatures from 13.9º to 19.4ºC have been associated with complete
mortality while significant mortality (over 50%) has been noted at
constant incubation temperatures from 9.9º to 16.7°C (Hicks 2000).

Juvenile Rearing and Growth

Optimal rearing temperatures at natural feeding regimes are in the range
of 12.2º to 14.8°C for chinook salmon (Hicks 2000). Banks et al. (1971,
as cited by Garling and Masterson 1985), Clarke and Shelbourn (1985),
Brett et al. (1982), and Marine (1997) reported optimum growth
temperatures determined from feeding on full rations that range from
14.8º to 20ºC. Ration size in the laboratory and food supply in nature
can have significant effects on optimal temperatures for rearing, and
this complication is one that must be kept in mind when evaluating
temperature effects in eventual monitoring and evaluation efforts.
Feeding rates below the satiation level typical of field situations are
associated with reduced optimum growth temperatures (Elliott 1981).
Brett et al. (1982) reported an optimal growth temperature of 19°C for
chinook maintained in the laboratory at maximal daily ration, but that
growth rates in the field corresponded to a projected feeding level of
60% of maximal daily ration, which translated to an optimal growth
temperature of 14.8°C for the field population.

Smoltification

Although data on temperature impairment of smoltification is incomplete,
the existing literature suggests that temperatures should be generally
maintained below 12º to 13.8°C during outmigration of chinook salmon
smolts (Hicks 2000). The temperature threshold for impairment of
smoltification was found to be 12ºC by Zaugg (1981) in spring chinook
yearlings, while Marine (1997) found it to occur at 17º to 20ºC in fall
chinook subyearlings.

Adult migration

Immigrating spring chinook salmon in the Willamette River have
experienced thermal blockages at 21º to 22ºC (at oxygen 3.5 mg/l)
(Alabaster 1988). A temperature of 21ºC blocked migration of spring
chinook salmon in Clearwater, Idaho, (Stabler 1981) as well as summer
chinook salmon (Stuehrenberg et al. 1978, as cited by Dauble and Mueller
1993) of the Snake River. A temperature of 21.1ºC blocked spring chinook
in the Tucannon River (Bumgarner et al. 1997), and fall chinook in the
Sacramento River were blocked at 19º to 21ºC (oxygen \~ 5mg/l) (Hallock
et al. 1970).

Spawning

The following authors reported spawning temperature ranges in daily
average temperatures (DAT) for chinook salmon. For spring chinook
salmon, Olson and Foster (1955) reported 4.4º to 17.8ºC. For fall/summer
chinook, Raleigh et al. (1996, cited in ODEQ 1995) reported 5º to
13.4ºC. The majority of the temperature observations reviewed in Hicks
(2000) cited a maximum spawning temperature below 14.5°C for chinook
salmon.

Lethality

For chinook salmon, the upper incipient lethal temperature (UILT) has
been recorded at 25.1ºC (acclimation temperature 20º and 24ºC) by Brett
(1952), and 24.9ºC (acclimation temperature 21.1ºC) by Orsi (1971).

Behavior

For subyearling spring chinook salmon in the Dungeness River, Brett
(1952) found the acute preference temperature to be 12º to 13ºC at all
acclimation temperatures and the mean final preference temperature was
11.7ºC. Sauter (1996) found that spring chinook salmon smolts on
unlimited ration have a final temperature preference of 16.7ºC and
Spigarelli (1975) reported that adults prefer a field temperature of
17.3ºC. For fall chinook salmon, Sauter (1996) found parr to prefer a
mean 16.7ºC, while advanced smolts preferred 10.9ºC.

Recommendations for Chinook Salmon

Incubation and Early Fry Development

McCullough et al. (2001) recommended that temperatures be maintained
below 12ºC for incubation and fry development, and Hicks (2000)
recommended an adjusted 7-day average of the daily maximum temperatures
(7-DAM) of 11º to 12°C at the time of fertilization of chinook salmon
eggs. Both McCullough et al. (2001) and Hicks (2000) recommended and
that individual daily maximum temperatures (1-DM) of 13.5º to 14.5°C are
required to provide optimal protection from fertilization through early
fry development.

Growth

McCullough (1999) suggested using the growth optimum of 15.6°C for
spring chinook salmon as the temperature standard, because temperatures
lower than this cause no reduction in survival while temperatures higher
than this begin to reduce growth and lead to increasing mortality rates.
A synthesis of evidence from Bisson and Davis (1976) (as cited by
Garling and Masterson 1985), Brett et al. (1982), Marine and Cech
(1998**)**, Wilson et al. (1987), Reiser and Bjornn (1979), and Brett
(1952), lead McCullough et al. (2001) to recommend an optimum production
temperature zone of 10.0º to 15.6ºC. Adjusting laboratory temperatures
to naturally fluctuating stream temperatures, Hicks (2000) recommended
that a 7-DAM of 14.2º to 16.8°C during the peak of summer provides for
optimal growth conditions for chinook salmon.

Adult Migration

Hicks (2000) recommended that daily maximum temperatures should not
exceed 20º to 21°C in order to prevent migration blockage of adult
chinook salmon.

Lethality

Hicks (2000) recommended that to protect fish from acute lethality,
daily maximum temperatures not exceed 22°C. In addition, he recommended
that thermal plumes should not be allowed such that fish could become
even briefly exposed to water warmer than 30º to 32°C.

Coho Salmon Data

Incubation and Early Fry Development

From the studies of Dong (1981), Tang et al. (1987), Murray -and McPhail
(1988), Velsen (1987), and Davidson and Hutchinson (1938) (as cited in
Sandercock 1991), it is relatively clear that egg survival for coho
salmon is consistently best at constant temperatures of 2.5º to 6.5ºC,
but may still be acceptable for many stocks at temperatures of 1.3º to
10.9ºC. Alevin and fry survival and health may be best at constant
temperatures of 4º to 8ºC, but survival may remain acceptable up to
10.9ºC. A constant 12ºC may form the upper threshold for optimal
development of coho salmon eggs and alevin (McCullough et al. 2001,
Hicks 2000).

Flett et al. (1996) investigated the cause of low survival to hatch of
embryos (42%) of coho salmon from the Fairview, Pennsylvania, stock in
Lake Erie in 1988. It was proposed that the low survival was due to
delayed oocyte maturation, ovulation, and vent maturation. Flett et al.
(1996) suggested this was caused by exposure of the salmon to warm water
(above 20^o^C in his Fairview stock and 2º to 4^o^C higher than in the
Simcoe stock, which showed no such impairments) during late ovarian
maturation and migration.

Juvenile Rearing and Growth

Most literature shows that juvenile coho salmon are not particularly
sensitive to stream temperatures and generally suggests maximum
temperatures between 9.4º and 14.4°C as optimal. However, Everson (1973,
as cited by Sullivan et al. 2000) found that, depending on food
availability, growth optima occur at 15ºC. Average or constant
temperatures of 12º to 15°C probably best characterize optimal rearing
conditions (Hicks 2000). The Sustainable Ecosystems Institute review
(Sullivan et al. 2000) suggested 12º to 17°C as an acceptable
temperature range.

Smoltification

Both Zaugg and McLain (1976) and Adams et al. (1975) reported the
temperature threshold for impairment of smoltification of coho salmon to
be 15ºC.

Spawning

It has been reported that spawning activity in coho salmon may typically
occur in the range of 4.4º to 13.3°C (Hicks 2000), although Bell (1973)
suggested that temperatures should be within the range of 7.2º and
15.6°C for successful spawning of coho salmon. Bell (1991) reported a
DAT of 10º to 12.8ºC for spawning coho salmon.

Lethality

For coho fry, Brett (1952) reported UILT (the temperature at which 50%
of the population is dead after indefinite exposure) at 25.0ºC
(acclimation temperatures of 20º and 23ºC). Konecki et al. (1995) tested
juvenile coho salmon fry critical thermal maximum (CTM, the
species-specific temperature at which a fish loses equilibrium and dies,
which depends on acclimation temperature). Mean CTMs from three
populations captured in the field in Washington State were 28.2º, 29.1º,
and 29.2°C, which exceed published data from some laboratory tests for
juvenile coho (Beschta et al. 1987, DeHart 1975, McGeer et al. 1991).
The population from a relatively cool stream had a lower CTM than two
populations from warmer streams. After three months in the laboratory
under constant temperature regimes the CTMs no longer differed. This
indicated that the population-specific differences resulted from
different acclimation regimes rather than from genetic adaptation.
Constant exposure to temperatures of 22º to 23°C poses a risk of causing
direct lethality to juvenile coho salmon (Hicks 2000).

Behavior

For subyearling coho salmon, Brett (1952) reported a range of 12º to
14ºC for their temperature preference, which is affected by acclimation
temperature. Konecki et al. (1995) reported 11.6ºC (range 7º to 21ºC)
and 9.9ºC (range 6º to 16ºC) for the final temperature preference
(species-specific value that may be influenced by feeding level) for
subyearling coho salmon in two different creeks. Reutter and Herdendorf
(1974) reported that adult coho have a final preference temperature of
11.4ºC, while Spigarelli (1975) reported a preferred field temperature
of 17.3ºC.

Swimming Speed

Brett et al. (1958) investigated the effect of temperature on the
cruising speed of young coho salmon. Cruising speeds of subyearling and
yearling coho were determined for acclimation temperatures ranging from
1° to 24°C. Optimum cruising speed for juvenile coho occurred at 15°C.

Disease

Groberg et al. (1983) studied the effects of water temperature on
infection by the predominantly marine pathogen *Vibrio anguillarum* in
juvenile coho salmon at seven water temperatures range from 3º to 21°C.
More rapid death and higher mortality were observed at the elevated
water temperatures. Growth rates of *V. anguillarum* were directly
related to temperature.

Recommendations for Coho Salmon

Incubation and Early Fry Development

Adjusting laboratory temperatures to naturally fluctuating stream
environments resulted in a recommendation of a 7-DAM of 9º to 12°C to
fully support the pre-emergent states of coho salmon (McCullough et al.
2001, Hicks 2000).

Juvenile Rearing and Growth

Adjusting for a naturally fluctuating stream environment resulted in a
recommendation of 14º to 17°C for the 7-DAM to fully protect juvenile
coho salmon rearing (Hicks 2000).

Sullivan et al. (2000) developed and used a bioenergetics-based approach
to evaluate salmon growth in relation to environmental temperature, and
to suggest sublethal temperature thresholds for coho salmon. An upper
threshold for the 7-DAM temperature of 16.5°C was found to be
appropriate, assuming a 10% reduction in growth represents an
appropriate risk level (Sullivan et al. 2000).

Lethality

Subtracting a 2°C safety factor resulted in a recommendation of 20º to
21°C to avoid direct lethality to coho salmon (Hicks 2000).

Chum Salmon Data

Incubation and Early Fry Development

Based on the works of Murray and Beacham (1986), Beacham and Murray
(1985), and Zinichev and Zotin (1988), constant incubation temperatures
from 4º to 12ºC commonly produce excellent incubation results for chum
salmon; however, some researchers have noted that less-than-optimal
survival occurs at the edges of this range. Both McCullough et al.
(2001) and Hicks (2000) suggested that constant initial incubation
temperatures of 8º to 10ºC would be most consistently optimal for chum
salmon.

Juvenile Rearing

Optimal rearing occurs between about 13º to 14.5°C (Hicks 2000).

Spawning

The Independent Scientific Group (1996) reported an average range of 8º
to 13ºC for spawning, while Hicks (2000) reported that chum salmon most
consistently spawn within a range of 7º to 10.5°C.

Lethality

Brett (1952) reported the UILT for chum salmon fry at 23.7º and 23.8ºC
(acclimation temperature 20º and 23ºC, respectively). Hicks (2000)
stated that significant lethality to chum salmon can result from
constant exposure to 22º to 23°C.

Behavior

Brett (1952) reported that juvenile subyearling chum salmon have an
acute preference temperature of 12º to 14ºC at all acclimation
temperatures and final preference temperature of 14.1ºC. Groot and
Margolis (1991) reported adult migrant chum have an acute preference
temperature of 7º to 11ºC.

Recommendations for Chum Salmon

Incubation and Early Fry Emergence

Hicks (2000) recommended that the 7-DAM should not exceed 10º to 12°C
for fertilization through fry emergence.

Lethality

With the 2°C safety factor, it was recommended that daily maximum
temperatures should not exceed 20º to 21°C to prevent direct lethality
to chum salmon. In addition, fish should not be exposed even briefly to
temperatures greater than 33º to 34°C (Hicks 2000).

Steelhead Data

Incubation and early fry development

Considering the works of Fuss (1998), Bell (1986), Rombough (1988), and
Redding and Schreck (1979), it appears that an optimal constant
incubation temperature occurs below 11º to 12ºC for steelhead
(McCullough et al. 2001).

Juvenile Growth

Optimal growth for juvenile steelhead occurs in the range of 14º to 15°C
(Hicks 2000); although in a laboratory setting, Wurtsbaugh and Davis
(1977) found that steelhead growth could be enhanced by temperature
increases up to 16.5ºC.

Smoltification

For steelhead, Hoar (1988) reported temperatures higher than 13ºC, Adams
et al. (1975) reported higher than 12.7ºC, Zaugg et al. (1972, as cited
by Zaugg and Wagner 1973) reported higher than 13.6ºC and Zaugg (1981)
reported 12ºC as upper thresholds for impairment of smoltification.

Adult migration

Strickland (1967, as cited by Stabler 1981) reported 21ºC as the
temperature blocking adult steelhead migration in the Snake River.

Spawning

For steelhead, Bell (1991) reported a daily average temperature range of
10º to 12.8ºC for spawning.

Behavior

For subyearling steelhead in the South Umpqua River, with food
available, the preferred temperature was 15.0ºC and 17.8ºC for yearlings
(Roper and Scarnecchia, 1994).

Nielsen et al. (1994) studied steelhead use of thermally stratified
pools in Northern California streams. It was observed that 65% of the
juvenile steelhead in Rancheria Creek moved into thermal refugia---in
the form of adjacent stratified pools---during periods of high ambient
stream temperatures of 23º to 28°C. Just before moving into these pools,
fish showed a decline in foraging behavior and increased agonistic
activity. On the Middle Fork Eel River, summer-run steelhead adults were
found in deep stratified pools throughout the summer, when midday
ambient stream temperatures ranged from 26º to 29°C; these cold water
pockets were on average 3.5°C cooler than the stream. Where stream
temperatures reached upper incipient lethal levels, these thermally
stratified pools provided refuge habitat for significant numbers of
young-of-the-year, yearling, and adult steelhead.

Recommendations for Steelhead

Incubation and Early Fry Development

Based on the literature and adjusting for a naturally fluctuating river
environment, the recommendation of 13.5º to 14.5°C for the single daily
maximum temperature from fertilization through hatching was made by
Hicks (2000).

Juvenile Rearing and Growth

The adjusted value for recommendation to fully protect juvenile rearing
of steelhead was 16º to 17°C (Hicks 2000). Sullivan et al. (2000)
recommended the upper threshold for the 7-DAM temperature of 20.5°C for
steelhead, assuming that a 10% reduction in growth is an acceptable risk
level.

Smoltification

Hicks (2000) adjusted constant temperature ranges to the fluctuating
stream environment, and recommended a 7-DAM of 13.3º to 14.3ºC for
emigrating steelhead smolts.

Adult Migration

Based on the consistency of several studies, Hicks (2000) recommended
that temperatures remain lower than 21º to 22ºC (1-DAM) to prevent
thermal barriers to migrating steelhead, and that water in which
steelhead migrate or hold not exceed a 7-DAM of 16º to 17ºC.

Lethality

Hicks (2000) recommended that daily maximum temperatures remain below
19º to 20ºC to prevent directly lethal conditions to steelhead.

Draft Criteria

The EPA (2001) recommends that temperature-limit criteria be based upon
upper optimal physiological temperature preferences known to support
requisite biological processes of recognized salmonid life-history
stages. Moreover, the EPA (2001) recommends that the criteria be based
on guilds of salmonids, taking the spatio-temporal use of the landscape
by guild members into account. For the Lower Columbia and Willamette
Rivers, the guild present is the cold-water guild. Along with the
population growth and abundance criteria being developed by the WLC-TRT
and reported elsewhere, we suggest that temperature-based criteria for
the delisting of threatened and endangered salmonids under the
Endangered Species Act, written to be consistent with EPA upper optimal
temperature values, consist of two parts:

1.  A requirement that in order to delist salmonids in the Willamette
    and Lower Columbia River domain, the 7-DAM temperature maxima within
    the habitat of a given evolutionarily significant unit (ESU) must
    not be increasing over the course of 20 years. This requirement of
    thermal nondeterioration is intended to complement requirements for
    nondeterioration in population growth rates and abundance. Prior to
    delisting, data will need to be collected to show with high
    confidence that the slope of the observed temperature trend is less
    than or equal to zero. The 20-year period provides a long enough
    data set to avoid being confounded by temperature oscillations
    driven by the Pacific Decadal Oscillation (PDO) (Anderson 1998, Chao
    et al. 2000), which has considerable effects on climate in the
    Pacific Northwest.

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5.  Upper optimal temperature criteria be adopted, above which delisting
    cannot occur regardless of whether or not the direction of change is
    nondeteriorating. We suggest the following as temperature maxima
    above which delisting cannot occur for chinook, coho, chum salmon,
    and steelhead:

  ---------------------------------- ------------------ ------------------
                                     7-Day-Average\     Weekly Mean
                                     Maximum Daily      Temperatures
                                     Temperatures       

  Spawning and incubation            13ºC (55ºF)        10ºC (50ºF)

  Juvenile rearing                   16ºC (61ºF)        15ºC (59ºF)

  Adult migration                    18ºC (64ºF)        16ºC (61ºF)

  Smoltification except steelhead    16ºC (61ºF)        15ºC (59ºF)

  Steelhead smoltification at        14ºC (57ºF)        12ºC (54ºF)
  fourth-level HUC^a^ watershed                         
  ---------------------------------- ------------------ ------------------

^a^ HUC = hydrologic unit code

For all these criteria, the significant challenge of defining the
spatiotemporal range over which they should be applied remains. Those
spaces occupied by threatened and endangered salmonids need to be
regulated at the times of year that sensitive life stages are present,
and defining the bodies of water involved and the times to apply the
standards requires additional consideration and research. The concept of
assessing thermal potential being developed by the EPA involves modeling
the characteristics of bodies of water in order to determine whether a
distribution of temperatures sufficient to support salmonids (and other
beneficial uses) can be attained (see "Public Review Draft" at
<http://www.tboys.com/chalk2.htm>). Using this use-attainability
analysis, as prescribed by the existing Clean Water Act, there is no
obligation to provide unattainable conditions (in this case to apply the
temperature criteria). It may be that as the EPA develops concepts
related to use-attainability analysis (including appropriate model
selection, sensitivity analysis, and determination of an acceptable
level of anthropogenic degradation), it will begin to converge with the
efforts of the WLC-TRT and others involved in salmon recovery planning
to define spatio-temporal ranges over which maximum temperature criteria
will be applied. Some amelioration of the difficulties posed by this
challenge may be provided by the multiple runs and species that broaden
the times of concern beyond brief periods for many subbasins. Once the
spatio-temporal pattern to apply these standards has been defined for
any ESU, exemptions to the above temperature maxima for specific bodies
of water can still be proposed based on historical acclimation to higher
temperatures. Such an exemption would require physiological or
population-level evidence that higher temperature maxima would not harm
the fish native to that area, or that cold-water refugia are plentiful
and provide the circumstances required for salmonid survival. Evidence
required for an exemption would need to include the density, size, and
duration of thermal refugia; data indicating that the distribution of
refugia in space and time is adequate to be protective of the salmonids
(Ebersol 2002); and field and laboratory studies providing strong
evidence of physiological acclimation for the existing local population
whose habitat is under consideration.

The guild-based temperature criteria are supported by the data collected
for the salmonid species at the Willamette and Lower Columbia Rivers.
The relationships between individual species data and the guild-based
criteria are described briefly in the following paragraphs.

Spawning and Incubation

The 10^o^C weekly mean temperature criterion is consistent with the
upper temperature range for optimum survival of chinook salmon embryos
and alevins (Raleigh et al. 1986) and is within reported temperature
ranges for successful spawning (Olson and Foster 1955, Raleigh et al.
1986), although the majority of spawning observations reported by Hicks
(2000) recommended maximum temperature values for chinook salmon
consistent with the proposed criterion of 13^o^C.

For coho salmon, the weekly mean temperature criterion of 10^o^C is at
the upper end of their acceptable incubation temperature range
(McCullough et al. 2001, Hicks 2000). This criterion is within the
acceptable range of coho spawning temperatures (Hicks 2000, Bell 1973).

For chum salmon, the 10^o^C weekly mean temperature criterion is within
their safe temperature range for spawning (Hicks 2000) and incubation
(McCullough et al. 2001, Hicks 2000).

Steelhead spawning occurs at temperatures within the range protected by
the 10^o^C (weekly mean temperature criterion), as does their early fry
development (McCullough et al. 2001).

Juvenile Rearing

The 15^o^C weekly mean temperature criterion is at the upper edge of
optimal rearing temperatures for chinook with a natural feeding regime
(Hicks 2000).

The 15^o^C weekly mean temperature criterion is at the upper end of the
temperature range providing optimal rearing conditions for coho salmon
(Hicks 2000).

The 15^o^C weekly mean temperature criterion is slightly above the
optimal range for chum rearing reported by Hicks (2000).

Optimal growth temperatures for juvenile steelhead are in the range of
14º to 15^o^C (Hicks 2000), although in a laboratory setting slightly
higher temperatures were associated with a food supply in excess of that
characteristically available in nature (Wurtsbaugh and Davis 1977).

Smoltification

The extreme variability of habitat use by steelhead makes establishing a
temperature criterion for their smoltification challenging. The 12^o^C
proposed for a weekly mean temperature at the fourth-level hydrologic
unit (HUC) watershed is consistent with Zaugg and Wagner's (1973) gill
ATPase activity data. Weekly mean temperature values of 15^o^C proposed
as criteria for other salmonids are well above the values having
excessive physiological consequences for steelhead (Zaugg and Wagner
1973). The results of Adams et al. (1975) and Hoar (1988) support this
lower criterion for steelhead.

The weekly mean temperature criterion of 15^o^C may be more protective
of fall chinook salmon (Marine 1997) than spring chinook (Zaugg 1981).
Hicks (2000) found that temperatures above 13.8^o^C did produce
smoltification impairment in chinook.

For coho salmon the 15^o^C weekly mean temperature criterion is at the
threshold temperatures that cause smoltification impairment.

Adult Migration

The proposed maximum temperature criterion of 16^o^C is within the safe
range proposed for chinook temperature maxima by Hicks (2000) and seems
protective for coho and chum salmon survival during adult migration as
well (Hicks 2000). Adult migrant chum have a somewhat lower temperature
preference of 7º to ll^o^C (Groot and Margolis 1991). Adult steelhead
migration is not blocked until 21^o^C (Strickland 1967, as cited by
Stabler 1981). Steelhead have been reported to make use of deep
stratified pools as thermal refugia when midday ambient stream levels
ranged above their tolerance limits (Nielsen et al. 1994).

Framework for Temperature Criteria

Salmonid survival and recovery will require more than the attainment of
these temperature goals. A rich data set shows that in terms of thermal
tolerances, disease resistance and physiological adaptation in general
salmonid stocks native to specific bodies of water may be better adapted
to local conditions than are other members of their species. However, in
many populations the genetic modification due to hatchery operations may
significantly reduce the present levels of local adaptation. Definitive
criteria for salmonid recovery should eventually define ways to
incorporate spatio-temporal variability into them in a realistically
complex fashion and have as their eventual goal a process that realigns
the curves of current environmental variables so that they overlay
historic conditions rather than simply acting as a floor or ceiling. The
challenge of this task is exacerbated by the multiple salmonid life
stages that will need to be identified in their distribution over space
and time and monitored. It is crucial that along with the attainment of
habitat goals, historical salmonid populations be identified and
recovered in a way that maintains them in the milieu suitable for their
survival. Hatchery operations may need to be adjusted to serve this
goal. Salmonid harvest patterns and hydro operation management may both
need to take the significance of both environmental recovery and the
relationships of specific genetic stocks to their native rivers into
account (this study provides no information on hatcheries, hydro, or
harvest). The complexity of any solution to the problem of salmonid
survival will need to balance all of these considerations while
achieving temperature regimes suitable for the persistence of the salmon
ESUs.

**Literature Cited**

Adams, B. L., W. S. Zaugg, and L. R. Mclain. 1975. Inhibition of salt
water survival and Na-K-ATPase elevation in steelhead trout (*Salmo
gairdneri*) by moderate water temperatures. Trans. Am. Fish. Soc.
104(4): 766--769.

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

Anderson, J. 1998. Decadal climate cycles and declining Columbia River
salmon. Sustainable fisheries conference proceedings, 22 p.

Available at <http://www.cqs.washington.edu/papers/jim/victoria.html>.

Bailey, J. E., and D. R. Evans. 1971. The low-temperature threshold for
pink salmon eggs in relation to a proposed hydroelectric installation.
Fish. Bull. 69: 587--593.

Beacham, T. D., and C. B. Murray. 1985. Effect of female size, egg size,
and water temperature on development biology of chum salmon
(*Oncorhynchus keta*) from the Nitinat River, British Columbia. Can. J.
Fish. Aquat. Sci. 42(11): 1755--1765.

Bell, M. C. 1973. Fisheries handbook of engineering requirements and
biological criteria. U.S. Army Corps of Engineers. Fish Passage
Development and Evaluation Program, North Pacific Division, Portland,
Ore.

Bell, M. C. 1986. Fisheries handbook of engineering requirements and
biological criteria. U.S. Army Corps of Engineers, Fish Passage
Development and Evaluation Program, North Pacific Division, Portland,
Ore.

Bell, M. C. 1991. Fisheries handbook of engineering requirements and
biological criteria. U.S. Army Corps of Engineers. Fish Passage
Development and Evaluation Program, North Pacific Division, Portland,
Ore.

Beschta, R. L. 1997. Riparian shade and stream temperature: An
alternative perspective. Rangelands 19: 25--28.

Beschta, R. L., R. E. Bilby, G. W. Brown, L. B. Holtby, and T. D.
Hofstra. 1987. Stream temperature and aquatic habitat: Fisheries and
forestry interactions. *In* E. O. Salo and T. W. Cundy (eds.),
Streamside management: Forestry and fisheries interactions. College of
Forest Resources, University of Washington, Seattle. Contribution number
57. Proceedings of a Symposium held at the University of Washington,
12--14 February 1986. p. 191--231

Bisson, P. A. and G.E. Davis. 1976. Production of juvenile chinook
salmon. *Oncorhynchus tshawytscha*, in a heated model stream. NOAA Fish.
Bull. 74: 763-774.

Black, M. C., D. S. Millsap, and J. F. McCarthy. 1991. Effects of acute
temperature change on respiration and toxicant uptake by rainbow trout,
*Salmo gairdneri* (Richardson). Physiol. 64(1): 145--168.

Brett, J. R. 1952. Temperature tolerance in young Pacific Salmon, genus
*Oncorhynchus*. J. Fish. Res. Bd. Can. 9(6): 265--323.

Brett, J. R., M. Hollands, and D. F. Alderdice. 1958. The effect of
temperature on the cruising speed of young sockeye and coho salmon. J.
Fish. Res. Bd. Can. 15(4): 587--605.

Brett, J. R. 1971. Energetic responses of salmon to temperature. A study
of thermal relations in the physiology and freshwater ecology of sockeye
salmon (*Oncorhynchus nerka*). Am. Zool. 11(1): 99--113.

Brett, R. J., W. C. Clarke, and J. E. Shelbourn. 1982. Experiments on
thermal requirements for growth and food conversion efficiency of
juvenile chinook salmon *Oncorhynchus tshawytsha*. Can. Tech. Rep. Fish.
Aquat. Sci. No. 1127.

Bumgarner, J., G. Mendel, D. Milks, L. Ross, M. Varney, and J. Dedloff.
1997. Tucannon River spring chinook hatchery evaluation. 1996 Annual
report. Washington Department of Fish and Wildlife, Hatcheries Program
Assessment and Development Division. Report #H97-07. Produced for U.S.
Fish and Wildlife Service. Cooperative Agreement 14-48-000196539.

Burrows, R. 1963. Water temperature requirements for maximum
productivity of salmon. *In* Water temperature influences, effects, and
control. Proc. 12^th^ Northwest Symp. Water Pollution Research. U.S.
Department of Health, Education, and Welfare, Public Health Service,
Pacific Northwest Water Laboratory, Corvallis, Ore. p. 29--38.

Chao, Y., M. Ghil, and J. McWilliams. 2000. Pacific interdecadal
variability in this century's sea surface temperatures. Geophys. Res.
Ltrs. 27: 2261.

Chapman, D., A. Giorgi, M. Hill, A. Maule, S. McCutcheon, D. Park, W.
Platts, K. Pratt, J. Seeb, L. Seeb, and F. Utter. 1991. Status of Snake
River chinook salmon. Report to Pacific Northwest Utilities Conference
Committee, Portland, Ore. 531 p.

Clarke, W. C., and J. E. Shelbourn. 1985. Growth and development of
seawater adaptability by juvenile fall chinook salmon (*Oncorhynchus
tshawytscha*) in relation to temperature. Aquaculture 45: 21--31.

Colgrove, D. J., and J. W. Wood. 1966. Occurrence and control of
*Chondrococcus columnaris* as related to Fraser River sockeye salmon.
IPSFC Progress report no. 15. Int. Pac. Salmon Fish. Comm., Vancouver,
B.C., Canada. 51 p.

Countant, C. C. 1977. Compilation of temperature preference data. J.
Fish Res. Bd. Can. 34: 739--745.

DeHart, D.A. 1975. Resistance of three freshwater fishes to fluctuating
thermal environments. M.S. Thesis, Oregon State University, Corvallis.

Dauble, D. D., and R. P. Mueller. 1993. Factors affecting the survival
of upstream migrant adult salmonids in the Columbia River basin.
Recovery issues for threatened and endangered Snake River salmon.
Technical Report 9 of 11. Prepared for the U.S. Department of Energy,
Bonneville Power Administration, Div. Fish Wildl., Project No. 98-026,
Portland, Ore., June 1993.

Dong, J. N. 1981. Thermal tolerance and rate of development of coho
salmon embryos. M.S. thesis, University of Washington, Seattle.

Donaldson, J. R. 1955. Experimental studies on the survival of the early
stages of chinook salmon after varying exposures to upper lethal
temperatures. M.S. thesis, University of Washington, Seattle.

Dunham, J., J. Lockwood, and C. Mebane. 2001. Issue Paper 2. Salmonid
distributions and temperature. Prepared as Part of Region 10 Temperature
Water Quality Criteria Guidance Development Project. EPA-910-D-01-002.
Available at
http://yosemite.epa.gov/R10/WATER.NSF/1507773cf7ca99a7882569ed007349b5/ce95a3704aeb5715882568c400784499?OpenDocument

Eaton, J. G., J. H. McCormick, B. E. Goodno, D. G. O'Brian, H. G.
Stefany, M. Hondzo, and R. M. Scheller. 1995. A field information-based
system for estimating fish temperature tolerances. Fisheries 20(4):
10--18.

Ebersol, J. L. 2002. Heterogeneous thermal habitat for Northeast Oregon
stream fishes. Ph.D. Thesis, Oregon State University, Corvallis. 201 p.

Elliott, J. M., 1981. Some aspects of thermal stress on freshwater
teleosts. *In* A. D. Pickering (ed.), Stress and fish. Academic Press,
London. p. 209--245.

Environmental Protection Agency (EPA). 1985. Ambient Water Quality
Criteria for Ammonia, (EPA 440/5-85-001).

Environmental Protection Agency (EPA). 2001. Draft EPA Region 10
guidance for state and tribal temperature water quality standards. U.S.
EPA, Seattle, Wash. 33 p.

Environmental Protection Agency (EPA) and National Marine Fisheries
Service (NMFS). 1971. Columbia River Thermal Effects Study. Volume 1.
Biological Effects Study. U.S. Environmental Protection Agency and
National Marine Fisheries Service, Seattle, Wash. 102 p.

Everson, L. B. 1973. Growth and food consumption of juvenile coho salmon
exposed to natural and elevated fluctuating temperatures. M.S. Thesis,
Oregon State University, Corvallis. 68 p.

Ferguson, R. G. 1958. The preferred temperatures of fish and their
midsummer distribution in temperature lakes and streams. J. Fish. Res.
Bd. Can. 15: 607--624.

Fish, F. F., and M. G. Hanavan. 1948. A report upon the Grand Coulee
fish-maintenance project 1939--1947. Special Science Report 55, U.S.
Fish and Wildlife Service, Washington, D.C. 63 p.

Flett, P. A., K. R. Munkittrich, G. Van Der Kraak, and J. F.
Leatherland. 1996. Overripening as the cause of low survival to hatch in
Lake Erie coho salmon (*Oncorhynchus kisutch*) embryos. Can. J. Zool.
74: 851--857.

Fryer, J. L, and Pilcher K. S. 1974. Effects of temperature on diseases
of salmonid fishes. U.S. Environmental Protection Agency, Office of
Research and Development. Ecological Research Series. EPA-660/3-73-020.
114 p.

Garling, D. L., and Masterson M. 1985. Survival of Lake Michigan chinook
salmon eggs and fry incubated at three temperatures. Prog.
Fish-Culturalist. 47: 63--66.

Groberg, W. J. Jr., R. H. McCoy, K. S. Pilcher, and J. L. Fryer. 1978.
Relation of water temperature to infections of coho salmon
(*Oncorhynchus kisutch*), chinook salmon (*O. tshawytsch*), and
steelhead trout (*Salmo gairdneri*) with *Aeromonas salmonicida* and *A.
hydrophila*. J. Fish Res. Bd. Can. 35: 1--7.

Groberg, W. J. Jr., J. S. Rohavec, and J. L. Fryer. 1983. The effects of
water temperature on infection and antibody formation induced by *Vibrio
anquillarum* in juvenile coho salmon (*Oncorhynchus kisutch*). J. World
Maricul. Soc. 14: 240--248.

Groot, C., and L. Margolis, eds. 1991. Pacific salmon life histories.
University of British Columbia Press, Vancouver. 564 p.

Hallock, R. J., Elwell R. F., Fry D. H. 1970. Migrations of adult kind
salmon *Oncorhynchus tshawytsha* in the San Joaquin delta as
demonstrated by the use of sonic tags. Calif. Dept. Fish. Game. Fish.
Bull. 151. 92 p.

Heath, A. G., and G. M. Hughes. 1973. Cardiovascular and respiratory
changes during heat stress in rainbow trout (*Salmo gairdneri*). J. Exp.
Biol. 59: 323--338.

Heming, T. A. 1982. Effects of temperature on utilization of yolk by
chinook salmon (*Oncorhynchus tshawytscha*) eggs and alevins. Can. J.
Fish. Aquat. Sci. 39: 184--190.

Heming, T. A., J. E. McInernery, and D. F. Alderdice. 1982. Effect of
temperature on initial feeding in alevins of chinook salmon
(*Oncorhynchus tshawytscha*). Can. J. Fish. Aquat. Sci. 39(12):
1554--1562.

Hicks, M. 2000. Evaluating standards for protecting aquatic life in
Washington's surface water quality standards. Draft discussion paper and
literature summary. Washington State Department of Ecology, Olympia,
Wash.

Hoar, W. S. 1988. The physiology of smolting salmonids. *In* W. W. Hoar
and D. J. Randall (eds.), Fish physiology, Vol. XIB. Academic Press, New
York. p. 275--343.

Hokanson, K. E. F., C. F. Kleiner, and T. W. Thorslund. 1977. Effects of
constant temperatures and diel temperature fluctuations on specific
growth and mortality rates and yield of juvenile rainbow trout, *Salmo
gairdneri*. J. Fish. Res. Bd. Can. 34: 639--648.

Howe, G.E., L. L. Marking, T. D. Bills, J. J. Rach, and F. L. Mayer Jr.
1994. Effects of water temperature and pH on toxicity of terbufos,
trichlorfon, 4-nitrophenol, and 2,4-dinitrophenol to the amphipod
*Gammarus pseudolimnaeus* and rainbow trout (*Oncorhynchus mykiss*).
EPA/600/J-94/125. Environ. Toxicol. Chem. 13(1): 51--66.

Idler, D. R., and W. A. Clemens. 1959. The energy expenditures of Fraser
River sockeye salmon during the spawning migration to Chilko and Stuart
Lakes. IPSFC Prog. Rep., Int. Pac. Salmon Fish. Comm., Vancouver, B.C.,
Canada. 80 p**.**

Independent Science Group. 1996. Return to the River Report. Document
number 96-6, Northwest Power Planning Council Independent Scientific
Advisory Board, Portland, Ore.

Jobling, M. 1981. Temperature tolerance and the final
preferendum---rapid methods for the assessment of optimum growth
temperatures. J. Fish Biol. 19: 439--455.

Jobling, M. 1994. Fish bioenergetics. Chapman & Hall, London. 309 p.

Konecki, J. T., C. A. Woody, and T. P. Quinn. 1995. Critical thermal
maxima of coho salmon (*O. Kitsuch*) under field and lab acclimation
regimes. Can. J. Zool. 73: 993--996.

MacLeod, J. C., and E. Pessah. 1973. Temperature effects on mercury
accumulation, toxicity, and metabolic rate in rainbow trout (*Salmo
gairdneri*). J. Fish. Res. Bd. Can. 30: 485--492.

Marine, K. R. 1997. Effects of elevated water temperature on some
aspects of the physiological and ecological performance of juvenile
chinook salmon (*Oncorhynchus tshawytsha*): Implications for management
of California's Central Valley salmon stocks. M.S. thesis, University of
California, Davis. 71 p.

Marine, K. R., and J. J. Cech Jr. 1998. Effects of elevated water
temperature on some aspects of the physiological and ecological
performance of juvenile chinook salmon (*Oncorhynchus tshawytscha*):
Implications for management of California's chinook salmon stocks.
Stream temperature monitoring and assessment workshop. 12--14 January
1998. Sacramento, California. Forest Science Project, Humboldt State
University, Arcata, California.

Materna, E. 2001. Issue Paper 4. Temperature interaction. Prepared as
part of U.S. EPA Region 10 Temperature Water Quality Criteria Guidance
Development Project. EPA-910-D-01-004. Available at
http://yosemite.epa.gov/R10/WATER.NSF/1507773cf7ca99a7882569ed007349b5/
ce95a3704aeb5715882568c400784499?OpenDocument

Mayer, F. L. Jr., L. L. Marking, T. D. Bills, and G. E. Howe. 1994.
Physiochemical factors affecting toxicity in freshwater: Hardness, pH,
and temperature. *In* J. L. Hamelink, P. F. Landrum, H. L. Bergman, and
W. H. Benson (eds.), Bioavailability: Physical, chemical, and biological
interactions. CRC Press, Boca Raton, Fla. p. 5--22. EPA/600/A-94/199.

McCullough, D. A. 1999. A review and synthesis of effects of alterations
to the water temperature regime on freshwater life stages of salmonids,
with special reference to chinook salmon. Water Resource Assessment,
U.S. EPA 910-R-99-010, Columbia River Inter-Tribal Fish Commission,
Portland, Ore. 291 p.

McCullough, D., S. Spalding, D. Sturdevant, M. Hicks. 2001. Issue Paper
5. Summary of technical literature examining the physiological effects
of temperature on salmonids. Prepared as part of U.S. EPA Region 10
Temperature Water Quality Criteria Guidance Development Project.
EPA-910-D-01-005. Available at
<http://yosemite.epa.gov/R10/WATER.NSF/1507773cf7ca99a7882569ed007349b5/ce95a3704aeb5715882568c400784499?OpenDocument>

McGeer, J.C., L. Baranyi, and G.K. Iwama. 1991. Physiological responses
to challenge tests in six stocks of coho salmon (*Oncorhynchus
kisutch*). Can. J. Fish. Aquat. Sci. 48: 1761-1771.

Murray, C. B., and T. D. Beacham. 1986. Effect of varying temperature
regimes on the development of pink salmon (*Oncorhynchus gorbuscha*)
eggs and alevins. Can. J. Zool. 64: 670--676.

Murray, C. B., and J. D. McPhail. 1988. Effect of incubation temperature
on the development of five species of Pacific salmon (*Oncorhynchus*)
embryos and alevins. Can. J. Zool. 66(1): 266--273.

Nielsen, J. L., T. E. Lisle, and V. Ozaki. 1994. Thermally stratified
pools and their use by steelhead in Northern California streams. Trans.
Am. Fish. Soc. 123: 613--626.

Olson, P. A., and R. F. Foster. 1955. Temperature tolerance of eggs and
young of Columbia River chinook salmon. Trans. Am. Fish. Soc. 85:
203--207.

Ordal, E. J, and R. E. Pacha. 1963. The effects of temperature on
disease in fish. Proceedings of the Twelfth Pacific Northwest Symposium
on Water Pollution Research. U.S. Department of the Interior, Federal
Water Pollution Control Administration, Northwest Region, Corvallis,
Ore. p. 39--56.

Oregon Department of Environmental Quality (ODEQ). 1995. Water quality
standards review. Standards and Assessment Section, ODEQ, Portland, Ore.

Orsi, J. J. 1971. Thermal shock and upper lethal temperature tolerances
of young king salmon, *Oncorhynchus tshawytsha*, from the Sacramento-San
Joaquin River system. Anadromous Fisheries Branch Administrative Report
No. 71-11. California Department of Fish and Game, Sacramento, Calif. 16
p.

Paladino, F. V., J. R. Spotila, J. P. Schubauer, and K. T. Kowalski.
1980. The critical thermal maximum: A technique used to elucidate
physiological stress and adaptation in fishes. Rev. Can. Biol. 39(2):
115--122.

Pacific Northwest Salmon Habitat Indicators Work Group (PNWSHIWG). 1998.
Toward "A Small but Powerful" set of regional salmon habitat indicators
for the Pacific Northwest. Prepared for the PNWSHIWG by the Green
Mountain Institute for Environmental Democracy, Montpelier, Vermont.

Poole, G. C., and C. H. Berman. 2001. An ecological perspective on
in-stream temperature: Natural heat dynamics and mechanisms of
human-caused thermal degradation. Environ. Manage. 27(6): 787--802.

Poole, G., J. Dunham, M. Hicks, D. Keenan, J. Lockwood, E. Materna, D.
McCullough, C. Mebane, J. Risley, S. Sauter, S. Spalding, and S.
Sturdevant. 2001a. Scientific issues relating to temperature criteria
for salmon, trout, and char native to the Pacific Northwest. A summary
report submitted to the policy workgroup of the U.S. EPA Region 10 Water
Temperature Criteria Guidance Project. EPA 910-R-01-007. Available at
http://yosemite.epa.gov/R10/WATER.NSF/1507773cf7ca99a7882569ed007349b5/ce95a3704aeb5715882568c400784499?OpenDocument

Poole G., J. Risley, and M. Hicks. 2001b. Issue Paper 3. Spatial and
temporal patterns of stream temperature (revised). Prepared as part of
U.S. EPA Region 10 Temperature Water quality Criteria Guidance
Development Project. EPA-910-D-01-003. Available at
<http://yosemite.epa.gov/R10/WATER.NSF/1507773cf7ca99a7882569ed007349b5/>
ce95a3704aeb5715882568c400784499?OpenDocument

Raleigh R. F., W. F. Miller, and P. C. Nelson. 1986. Habitat suitability
index models and instream flow suitability curves: Chinook salmon. U.S.
Fish Wildlf. Serv. Biol. Rep. 82(10.122). 64 p.

Redding, J. M., and C. B. Schreck. 1979. Possible adaptive significance
of certain enzyme polymorphisms in steelhead trout (*Salmo gairdneri*).
J. Fish. Res. Bd. Can. 36: 544--551.

Reiser, D. W., and T. C. Bjorn. 1979. Habitat requirements of anadromous
salmonids. Gen. Tech. Rep. PNW-96. USDA Forest Service. Pacific
Northwest Forest and Range Experiment Station, Portland, Ore. 54 p.

Reutter, J. M., and C. E. Herdendorf. 1974. Laboratory estimates of the
seasonal final temperature preferenda of some Lake Erie fish. Proc.
17^th^ Conf. Great Lakes Res. 1974: 59--67.

Rombough, P. J. 1988. Growth, aerobic metabolism, and dissolved oxygen
requirements of embryos and alevins of steelhead, *Salmo gairdneri*.
Can. J. Zool. 66: 651--660.

Roper, B. B., D. L. Scarnecchia, T. J. L. Marr. 1994. Summer
distribution of and habitat use by chinook salmon and steelhead within a
major basin of the South Umpqua River, Oregon. Trans. Am. Fish. Soc.
123: 298--308.

Sandercock, F. K. 1991. Life history of coho salmon (*Oncorhynchus
kisutch*). *In* C. Groot and L. Margolis (eds.), Pacific salmon life
histories. University of British Columbia Press, Vancouver. p. 395--445.

Sauter, S. T. 1996. Thermal preference of spring and fall chinook salmon
during smoltification. M.S. thesis. Portland State University, Portland,
Ore.

Sauter, S. T., J. McMillan, and J. Dunham. 2001. Issue Paper 1. Salmonid
behavior and water temperature. Prepared as part of U.S. EPA Region 10
Temperature Water Quality Criteria Guidance Development Project.
EPA-910-D-01-001. Available at
http://yosemite.epa.gov/R10/WATER.NSF/1507773cf7ca99a7882569ed007349b5/ce95a3704aeb5715882568c400784499?OpenDocument

Sedell, J. R., and J. L. Froggatt. 1984. Importance of streamside
forests to large rivers: The isolation of the Willamette River, Oregon,
USA, from its floodplain by snagging and streamside forest removal. Int.
Ver. Theoret. Angew. Limnol. Verhandl 22: 1828--1834**.**

Seymour, A. H. 1956. Effects of temperature upon young chinook salmon.
Ph.D. thesis, University of Washington, Seattle. 127 p.

Spigarelli, S. A. 1975 Behavioral responses of Lake Michigan fishes to a
nuclear power plant discharge. *In* Environmental effects of cooling
systems in nuclear power plants. International Atomic Energy Agency
(IAEA), Vienna. p. 479--498.

Stabler, D. F. 1981. Effects of altered flow regimes, temperatures, and
river impoundment on adult steelhead trout and chinook salmon. M.S.
thesis, University of Idaho, Moscow. 84 p.

Sullivan, K., D. J. Martin, R. D. Carwell, J. E. Toll, and S. Duke.
2000. An analysis of the effects of temperature on salmonids of the
Pacific Northwest with implications for selecting temperature criteria.
Sustainable Ecosystems Institute, Portland, Ore.

Tang J., Bryant M.D., Brannon E. L. 1987. Effect of temperature extremes
on the mortality and development rates of coho salmon embryos and
alevins. Prog. Fish-Cult. 49(3): 167--174.

Velsen, F. P. J. 1987. Temperature and incubation of Pacific salmon and
rainbow trout. Compilation of data on median hatching time, mortality,
and embryonic staging. Canadian Data Report of Fisheries and Aquatic
Sciences 626.

Washington Department of Ecology (WDOE). 1999. Evaluating standards for
protecting aquatic life in Washington's surface water quality standards.
Temperature criteria. Preliminary review draft discussion paper. Draft
report and appendices. WDOE, Olympia, Wash.

Williams, I. V., U. H. M. Fagerlund, J. R. McBride, G. A. Strasdine, H.
Tsuyuki, and E. J. Ordal. 1977. Investigation of prespawning morality of
1973 Horsefly River sockeye salmon. IPSFC Progress report no. 37. Int.
Pac. Salmon Fish. Comm., Vancouver, B.C., Canada. 51 p.

Wilson, W. J., M. D. Kelley, and P. R. Meyer. 1987. Instream temperature
modeling and fish impact assessment for a proposed large-scale Alaska
hydro-electric project. *In* J. F. Craig and J. B. Kemper (eds.),
Regulated streams. Plenum Press, New York. p. 183--206.

Wurtsbaugh, W. A., and G. E. Davis. 1977. Effects of temperature and
ration level on the growth and food conversion efficiency of *Salmo
gairdneri*, Richardson. J. Fish. Biol. 11: 87--98.

Zaugg, W. S. 1981. Relationships between smolt indices and migration in
controlled and natural environments. *In* E. L. Brannon and E. O. Salo
(eds). Proceedings of the salmon and trout migratory behavior symposium.
School of Fisheries, University of Washington, Seattle. p. 173--183.

Zaugg, W. S., and L. R. McLain. 1976. Influence of water temperature on
gill sodium, potassium-stimulated ATPase activity in juvenile coho
salmon (*Oncorhynchus kisutch*). Comp. Biochem. Physiol. 54A: 419--421.

Zaugg, W. S., and H. H. Wagner. 1973. Gill ATPase activity related to
parr-smolt transformation and migration in steelhead trout (*Salmo
gairderi*): Influence of photoperiod and temperature. Comp. Biochem.
Physiol. 45B: 955--965.

Zinichev, V. V., and A. I. Zotin. 1987. Selected temperature and
optimums for development in prolarvae and larvae of chum salmon,
*Oncorhynchus keta*. J. Ichthyol. 27(6): 141--144.

[^1]: EPA. 2001. available at <http://yosemite.epa.gov/R10/WATER.NSF/>
    1507773cf7ca99a7882569ed007349b5/ce95a3704aeb5715882568c400784499?OpenDocument.

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