United States
Environmental Protection
Agency
EPA-910-D-01-004
May 2001
&EPA 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
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Contents
Abstract 1
Introduction 1
What is stress and how are fish affected by it? 2
Why are these interactions important to consider in developing a temperature criterion? 3
How do these interactions affect salmonids? 3
Can you describe a situation in which a fish is facing multiple stressors? 3
What physical aspects of aquatic ecosystems are influenced by temperature or influence
temperature? 3
Density and viscosity 4
Depth 4
Stream flow 4
Suspended sediment 4
How are chemical constituents affected by temperature? 5
Dissolved oxygen 5
pH 7
Hardness and alkalinity 7
Chemical toxicity 7
Ammonia 8
Organics ¦... .9
Metals 9
Cyanide 11
Chlorine 11
Nitrogen supersaturation 11
What aspects of salmonid biology are influenced by temperature? 11
Competition and predation 11
Disease 11
What factors are involved in infection by disease? 12
Are warm-water vectors of disease present in rivers of the Pacific Northwest? 12
Is just a single life stage susceptible to disease? 13
Wouldn't disease be obvious in salmon if it were present? Wouldn't dead fish be
noticeable if this were a problem? 13
What are some modes of infection? 14
Has infection with warm-water diseases been documented historically in streams of
the region? 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? 15
What is the relationship between increasing temperature and columnaris disease?
Are there any apparent critical temperature thresholds? 16
Rate of infection increases with temperature 16
Migration effects 16
Holding effects 17
Temperature Interaction
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Juvenile survival rate decreases with increasing temperature 17
Time to death decreases with increasing temperature 17
Are other salmon diseases of warm water similar to columnaris in their
temperature-survival relationships? 18
What is the relationship between disease and stress? 18
How does temperature affect immune response? 23
Does temperature influence the impact of angling pressure? 23
Is growth affected by temperature changes? 23
What is the importance of temperature to salmonid food resources? 24
How does temperature affect photobiology? 25
How well are these interactive relationships understood? 25
What is the likelihood of exposure of salmonids to multiple stressors? 25
What other complexities of multiple stressors need to be considered? 26
Have any States addressed these temperature relationships within their water
quality criteria? 27
What tools are available to help evaluate these multiple stressors and the effects
to salmonid populations? 27
Conclusions 27
Literature Cited 28
Temperature Interaction
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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, well-
being, 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.
Temperature Interaction
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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.
Temperature Interaction
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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.
Temperature Interaction
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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 ajar. 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 arc 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 |am median diameter) decreased when
Temperature Interaction
4
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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
at
O)
0
5
10
15 20 25 30 35 40
Temperature (C)
Figure 1. Oxygen saturation concentrations (mg/L) at various temperatures (°C). Derived from Hodges (1977).
Temperature Interaction
5
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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).
Temperature Interaction
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United States
Environmental Protection
Agency
EPA-910-D-01 -005
May 2001
<8EPA Issue Paper 5
Summary of Technical
Literature Examining the
Physiological Effects of
Temperature on Salmonids
Prepared as Part of EPA Region 10
Temperature Water Quality Criteria
Guidance Development Project
Dale A. McCullough, Colum bia River Inter-Tribal
Fish Commission
Shelley Spalding, U.S. Fish and Wildlife Service
Debra Sturdevant, Oregon Department of
Environmental Quality
Mark Hicks, Washington Department of Ecology
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Contents
Abstract 1
Introduction 2
SUMMARY OF THERMAL REQUIREMENTS 3
What arc the thermal requirements for incubation and early fry development? 3
What are the thermal requirements for growth? 3
What are the thermal requirements for smoltification? 6
What are the thermal requirements for swimming speed? 8
What are the thermal requirements for migration to spawning? 9
What are the thermal requirements for adult holding and spawning? 11
What are lethal temperature effects? 12
What conclusions can you draw for anadromous salmonids and coastal cutthroat and
rainbow trout? 13
What conclusions can you draw for bull trout and Dolly Varden? 17
What conclusions can you draw for other salmonids? 18
SUPPORTING DISCUSSION AND LITERATURE-GENERAL ISSUES 19
Laboratory and Field Studies 19
What are the advantages and disadvantages of laboratory and field data? 19
If our most precise understanding of thermal effects is from laboratory tests, what
methods can be used? 21
Potential for Variation Among Stocks or Species of Salmonids 23
Is there enough significant genetic variation among stocks or among species to warrant
geographically specific water temperature standards? 23
Are there evolutionary differences among salmonid species in the Pacific Northwest?
24
What arc the major differences in thermal tolerance among and within important families24
What is the variation in thermal response within a species? 26
Is there significant genetic flexibility within a stock that would allow for adaptation to
thermal regimes? 27
Besides survival, what other key biotic responses influenced by temperature vary among
stocks? 27
Growth 28
Swimming speed 29
SUPPORTING DISCUSSION AND LITERATURE-SUBLETHAL EFFECTS
30
Incubation and Early Fry Development 30
Which temperatures provide optimum conditions for incubation and early fry development
in the following species? 30
Chinook salmon 30
Coho salmon 33
Chum salmon 34
Pink salmon 34
Sockeye salmon 35
Steelhead 36
Nonanadromous rainbow trout 36
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
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Cutthroat trout 37
What are the conclusions for incubation requirements? 38
Growth 38
For growth, what are the demands for energy and how is the balance determined by
temperature? 38
Why is it important to be concerned with growth rate, production, and fish density? ... 39
What is the optimum range or optimum temperature for growth of various salmonids?
40
Chinook 40
Sockeye 41
Steelhead 42
What more is specifically known about growth rearing requirements of rainbow trout?
42
What is the relationship between growth temperatures and other physiological responses?
44
What are temperature feeding limits for salmonids? 45
How is feeding rate affected by acclimation temperature? 46
What are temperature growth limits for salmonids? 46
How docs food availability affect growth of salmonids at different temperature
exposures? 47
Is there evidence for food limitation in natural streams? 48
Can growth rates be predicted under field conditions using thermal history identified under
laboratory conditions? 49
Has acclimation to a temperature higher than the mean of a diel cycle been demonstrated?
51
Are there seasonal differences in growth rates not related to temperature? 51
What research seems to best describe the influence of fluctuating temperature on growth?
52
What is the range of laboratory growth rates under fluctuating temperature vs. constant
temperature? 54
Smoltification 57
How is smoltification measured? 57
What is physiological stress and at what temperatures does it occur in salmonids? .... 57
What are the seasons for passage of smolts of common anadromous species and how
would this information be used? 58
What are heat shock proteins and what do they indicate? 58
What temperature range is recommended for reducing physiological stress? 59
Why might it be advisable to use naturally reared vs. hatchery-reared salmonids to
measure physiological status? 60
How does physiological status of smolting salmon change seasonally? 60
How does photoperiod influence growth rate and subsequent saltwater readiness of
smolts? 61
Are smolts affected by high temperatures during migration? 62
Are smolts subject to cumulative stresses from thermal exposure? 62
What temperatures are required to inhibit smoltification in steelhead and salmon? 62
What temperatures are required to reverse smoltification in steelhead? 64
SummaryofTcchnical Literature Examining the Phjsiological Effects of Temperature
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Can incubation temperature affect smolt emigration timing? 64
What river temperatures are associated with peaks in migration? 64
How do freshwater and ocean temperatures affect time of ocean entry? 65
What is the role of temperature in migratory response and seawater adaptation? 65
How can multiple stresses during the smoking phase be reduced? 66
Swimming Speed 66
How is swimming speed measured? 66
At what swimming speeds do metabolic transitions occur? 67
Why is swimming speed vital to adults during migration? 67
Why is swimming speed vital to smolts during migration? 68
How does temperature affect juvenile swimming speed? 69
How do temperature and oxygen jointly affect juvenile swimming speed? 69
How are physiological optimum, growth optimum, preferred temperature, swimming
maximum, and metabolic scope derived? 69
How can allocation of energy to metabolism and swimming be used to interpret fitness and
resistance to disease? 70
How do temperature, light intensity, and photoperiod influence swimming speed? .... 70
How do fish size and acclimation temperature affect swimming? 71
Can disease affect swimming speed? 71
What is known about swimming speed for three species of char? 71
Can swimming act as an indicator of sublethal stress? 71
How are adult swimming speeds and migration rate related? 72
Adult Migration to Reproduction 73
What temperatures are associated with migration? 73
How can stress during migration affect later reproductive success in salmonids? 75
What temperatures are recommended for holding? 75
Can temperature affect viability of gametes developing in adults? 76
How is survival of prespawning adults affected by water temperature? 81
What temperature ranges are associated with the adult spawning period? 81
What temperatures or thermal regimes are required to initiate spawning? 82
Conclusions for spawning 83
SUPPORTING DISCUSSION AND LITERATURE-LETHAL EFFECTS 84
What is the utility of UILT data and how has it been applied? 84
Are there potential weaknesses in reliance onMWAT? 85
How can UILT data be evaluated against UUILT data? 86
How can prolonged exposure to cyclic temperatures be evaluated? 87
SUPPORTING DISCUSSION AND LITERATURE-SUBLETHAL AND LETHAL
EFFECTS FOR NATIVE CHAR, REDBAND TROUT, AND CUTTHROAT
TROUT SPECIES 89
What are the thermal requirements of bull trout and Dolly Varden? 89
Incubation 89
Growth 91
Migration 91
Spawning 91
What are the thermal requirements for Lahontan cutthroat trout? 92
Growth 92
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
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Thermal stress—heat shock proteins 92
Occurrence 93
Lethal effects 93
What are the thermal requirements for westslope cutthroat trout? 94
Incubation and egg survival 94
Growth 94
Spawning 94
Occurrence 94
What are the thermal requirements for redband trout? 94
Growth and feeding 94
Metabolic activity and swimming speed 95
Occurrence 95
Lethal effects 95
Literature Cited 96
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
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Issue Paper 5
Summary of Technical literature Examining the
Physiological Effects of Temperature
Region 10 Temperature Water Quality Criteria
Guidance Development Project
Dale A. McCullough, Shelley Spalding, Debra Sturdevant, and Mark Hicks
Abstract
The chief objective of this paper is to provide a literature review of the role temperature
exerts on the physiology of various salmonids. The fish are affected as species and within the
stages of their life history. The thermal environment, perhaps more than any other aquatic habitat
feature, influences the distribution, health and survival of our native salmonids. Temperature
tolerances for salmonid species typically refer to effects of temperature on an individual. Because
we are interested in sustainable populations of salmonids, this paper also reviews information on
the optimal or preferred ranges of temperatures that will be needed to promote long-term
survival, growth, and reproductive success.
Thermal stress occurs when a temperature or a change in temperature produces a significant
change to biological functions leading to decreased likelihood of survival. Thermal stress can lead
to lethal effects either immediately, in a period of days, or even weeks or months from the onset
of the elevated temperature. Thermal stress can also result in "sublethal" or indirect effects
resulting in death or reduced fitness that impairs processes such as growth, spawning,
smoltification, or swimming speed. Metabolic processes are directly related to temperature, and
the metabolic rate increases as a function of temperature. Fish are metabo lically efficient and
most likely to thrive within the preferred range of temperatures.
Different species of salmonids have evolved to utilize different thermal regimes, although
there is much overlap in their utilization of these regimes. Anadromous salmonids and coastal
cutthroat and rainbow trout tend to have similar temperature requirements; however, where
multiple species and life stages are present, temperature criteria need to protect the most sensitive
species and life history stage. For this guild, maximum growth and swimming speed occur at
55.4-68°F (13-20°C) under satiation feeding; reduced ATPase levels are experienced at
temperatures as low as 51.8-55.4°F (11-13°C), potentially resulting in delayed or ineffective
smoltification; adult migration maybe blocked at 69.8-73.4°F(21-23°Q; and temperatures of
42.8-50°F (6-10°C) or lower during incubation result in maxirmm survival and size at emergence.
Bull trout have lower temperature requirements than other salmonids with optimal incubation
occurring at 35.6-42.8°F (2-6°C), spawning being initiated as temperatures drop below 48.2°F
(9°C), and the maximum growth rate at satiation feeding occurring at 60.8°F (16°C). For other
salmonids such as redband trout, wests lope cutthroat trout, and mountain whitefish, little
information is available on the effects of temperature on their physiology.
SummaryofTechnical Literature Examining the Physiological Effects of Temperature
1
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Introduction
The distribution, health, and survival of our native fish species are inextricably linked to the
thermal environment. Temperature, perhaps more than any other environmental parameter,
greatly affects the status of fish and other aquatic life. With respect to thermal effects, lethal
temperatures do occur in the field and can be locally problematic in defining usable and unusable
habitat. Sublethal effects of temperature determine the overall well-being and patterns of
abundance of our native fish populations. Temperature exerts its control through its effect on the
physiology of the individual species and their Hfe stages. In addition, individuals within a species
population vary in their responses (e.g., lethal, growth) to temperature, generally according to a
bell-shaped distribution. As species individually or relative to one another experience
temperatures outside their physiological optimum range, the mix of species present in any given
waterbody may drastically change. Aside from direct mortality caused by very high temperatures,
temperature influences the abundance and well-being of organisms by controlling their metabolic
processes. Every species, including disease organisms, has optimal metabolic ranges. Community
composition is shaped by the level of numerous components of the habitat system, including
temperature, food, water, light, substrate, and so on, each of which can provide optimal or
suboptimal conditions. Temperature is one of the single most influential determinants of habitat
quality andean also act synergistically with other habitat elements.
Temperature through its effect on physiology influences the ability of fish to grow,
reproduce, compete for habitat, and escape predators. This issue paper examines the role of
temperature in the physiology of the salmonids native to the Pacific Northwest, and the
importance of lethal temperature effects compared with various types of sublethal effects in
controlling the survival and health of native fishes.
For further information on the effects of temperature on salmonids, we suggest you refer to
both the Behavior and Temperature Interaction issue papers in this series. This issue paper is
drawn heavily from existing extensive reviews of thermal effect literature (Berman 1998, EPA and
NMFS 1971, Hicks 1999, 2000, McCuDough 1999, ODEQ 1994) and is intended to extract from
this large body of literature the key documents illustrating various concepts and effects. For
additional guidance to the literature on thermal effects, we recommend starting from these
references.
The intention of this paper is to review physiological effects of temperature regimes for all
salmonids. However, the authors acknowledge the scarcity of relevant bull trout information and
have avoided including observations or case studies that are difficult to extrapolate, as is the case
with much of the bull trout temperature literature. In cases where there is information available
on a closely related charr species, that information may be included.
In the following questions and answers, we first summarize thermal requirements for
salmonid incubation and early fry development, growth, smoltification, swimming speed,
migration to spawning, and adult holding and spawning, and discuss lethal effects. Then we
present detailed documentation and references.
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
2
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SUMMARY OF THERMAL REQUIREMENTS
What are the thermal requirements for incubation and early fry development?
During incubation and early fry development, salmonid embryos and young fish have
different habitat requirements from those of spawning adults, even though the adult-selected
spawning site is the incubation environment for the progeny. During incubation, water
temperature affects the rate of embryo and alevin development, the amount of dissolved oxygen in
the water, and, to a significant extent, the survival of early fiy (Bjornn and Reiser 1991). Within
an acceptable range, the higher the temperature is the faster the rate of development will be and
the shorter the incubation period and time to emergence (Beacham and Murray 1990).
The effects of water temperature in regulating developmental rates of incubating eggs are
well documented (Hicks 2000, McCullough 1999). Temperatures from 39.2 to 53.6°F (4-12°C)
tend to produce relatively high survival to hatching and emergence, with approximately 42.8-50°F
(6- 10°C) being optimum for most salmonid species. However, although salmonids should avoid
temperatures that arc too cold or too warm during initial stages of incubation, the entire thermal
history (including accumulation of degree days) during incubation is of great importance to ensure
proper emergence timing. That is, a thermal regime that cools rapidly from 53,6°F (12°C) and
achieves low winter temperatures (according to natural cooling processes and rates) is essential
for acquiring the necessary thermal units to ensure proper emergence timing and high egg
survival. Unless water releases from dams alter winter thermal regimes in egg incubation habitat,
it is assumed that controlling summer rearing temperatures (maximum and diel fluctuation) will
also provide proper winter temperatures during incubation. Management "control" of summer
temperatures means taking those actions that would restore the thermal regimes consistent with
the system potential for the stream.
Char can be characterized as a stenothermal species because they require a narrow range of
cold temperatures to rear and reproduce and may thrive in waters too cold for other salmonid
species (Balon 1980). The literature suggests that the optimum water temperature range for bull
trout and Dolly Varden incubation occurs just below the optimal range for the other salmonids
native to the Pacific Northwest.
Native stocks of salmon, trout, and char are closely tied to their natal streams and have
evolved with natural fluctuations in stream temperatures and other environmental variables. Some
streams may have winter temperatures that are lower than the minimum recommended as optimal
for most salmonid species other than char; however, eggs are usually able to develop normally
because spawning and initial embryo development occur when temperatures are in the suitable
range. The presence of groundwater inflows close to spawning areas also helps ameliorate
seasonal temperature extremes that might be harmful to developing embryos.
What are the thermal requirements for growth?
Growth is one of the most sensitive indicators of overall fish health and is vulnerable to
changes in basic environmental conditions such as temperature. Unless a fish can grow it cannot
complete its life functions. For example, a fish must reach a sufficient size at hatching or
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
3
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emergence to have a high likelihood of survival. Size attained at the time of hatching or
emergence partially depends on egg size, which in turn is related to adult size and nutritional
status at spawning. Ifgrowth rates are too tow during the summer rearing period, body fat is not
sufficient to sustain a fish during the winter rearing period (Hokanson 1977). If the size during
overwintering is too small or the growth rate prior to emigration is too low, smolt size will be
insufficient to ensure successful transition to the marine environment (Folmar et al 1982).
Growth rates during egg incubation are affected by temperature in the graveL In streams with
low winter temperatures (e.g., <42.8°F [6°C]), feeding and total fish activity tend to be very low,
and consequently growth is minimal.
Growth rates of juvenile fish during summer are used as a convenient means of monitoring
the thermal impacts of most freshwater environments. Riparian canopy removal or channel
widening, which lead to increased maximum water temperatures during summer, are also
associated with lower minimum winter temperatures as well as increased diel fluctuations in both
seasons. Optimum growth temperatures for a variety of sahnonids, many of which are native to
the Pacific Northwest, are listed in Table 1. These optimum temperatures for feeding at full ration
range from 53.6 to 68°F (12-20°C). Because food availability in the field typically provides less
than satiation feeding, optimum growth temperatures in the field can be substantially reduced
(Elliott 1981).
Tabic 1. Selected growth optima for salmonids determined from feeding on full rations
Species
Optimum growth
temperature (°C)
Reference
Chinook (Oncorhynchus
tshawytscha)
15
Banks et al. (1971) (as cited byGarling
and Masterson 1985)
17
Clarke and Shelbourn (1985)
19
Brett et al. 1982
20
Marine (1997)
Sockeye (Oncorhynchus nerka)
15
Brett et al. 1969
Coho (Oncorhynchus kisutch)
15
Everson (1973, as cited by Sullivan et al.
2000)
Rainbow trout (Oncorhynchus
my kiss)
17.2-18.6
Hokanson et al. (1977)
16.5
Wurtsbaugh and Davis (1977)
15
Grabowski (1973)
15
Railsback and Rose (1999)
(redband trout)
20
Sonski (1983b)
Brook trout (Salvelinus
fontinalis)
12.4-15.4
McCormick et al. 1972
Lake trout (Salvelinus
namaycush
12.5
Edsall and Cleland (2000)
Brown trout (Salmo trutta)
13.9
Elliott and Hurley (1999)
13.1
Elliott et al. (1995)
Atlantic salmon (Salmo salar)
18
Siemicn and Carline (1991)
Arctic char (Salvelinus alpinus)
14
Jobling (1983)
15.1
Larsson and Berglund (1997)
European grayling (Thymallus
thymallus)
17.3
Mallet et al. (1999)
Summary of Technical Literature Examining the Physiological Effects of Temperature
4
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Bull trout (Salvelinus
12-16
McMahon et al. (1999)
confluentus)
Optimum growth temperature is that temperature which provides the most favorable
conditions for growth. Other biologcal performances such as feeding rate and conversion
efficiency may have other optimum temperatures. For example, feeding rate and conversion
efficiency both are influenced by temperature, but each can have a slightly different optimum
temperature. Because growth rate is more directly linked to energy assimilated (the result of the
combination of feeding rate and conversion efficiency), it seems most appropriate to emphasize
growth rate as a key biological performance indicator of the thermal environment quality rather
than the other two performances.
Growth rate is a function of temperature but also of food availability (Elliott 1981, Elliott
1994). Food availability in the field is normally thought to be substantially less than that needed
to provide satiation feeding. Consequently, if stream productivity restricts salmonid feeding to
levels less than satiation, then lower temperatures are required to ensure optimum growth rates.
Although laboratory-derived temperature growth optima are probably adequately defined for
various feeding levels, an absolute growth rate in the laboratory may not be matched in the field
given the differences in food quality. In hatchery culture situations, satiation feeding on hatchery
diets can produce excessive accumulation of lipid (Le., hatchery fish are often obese compared
with wild fish). This is not to say that optimum growth temperatures are not a useful biological
index to temperatures providing healthful conditions for salmonids residing in the center of their
distribution in the field. Instead it indicates that artificially increasing temperature in the field
above optimum produces a relative reduction in growth rate. Also, in order to provide the
greatest population production capacity (contributing to biomass, abundance, and fecundity—all
indicators of fitness and population long-term viability), it is important to provide thefuD range of
natural potential temperature longitudinally. This means very cold headwaters, cold midreaches,
and cold/cool lower reaches. This will produce, in general, lower than optimum growth in
headwaters, optimum growth in midreaches, and lower than optimum growth downstream.
Eliminating cold-water habitats upstream shrinks suitable habitat, converts more habitat to
suboptimal growth zones, and reduces potential production.
Optimum temperature can have another connotation. When we consider the effects of
temperature at any given life stage, multiple performances must often be achieved. For example,
if the highest growth rate were produced only under temperatures so high that a large portion of
the population would die from disease, the optimum temperature for satisfying overriding needs
(e.g., sustainability) of the population might be closer to the optimum for protection against
disease. If the disease resistance temperature optimum is so low that growth and reproduction are
low, the optimum would have to lie in a more intermediate position. However, as previously
described, most key biological performances are well correlated and have similar optima.
Preferred temperatures, optimum growth temperatures, and high disease resistance from common
warm-water diseases (e.g., furunculosis, columnaris) tend to be similar (Jobling 1981).
Consequently, we are able to survey the literature about optimum growth temperatures, compare
these temperatures with optima for other performances such as disease resistance or swimming
ability, and find a temperature range that would satisfy growth objectives but also meet other key
needs influencing survival.
Summary ofTcchnical Literature Examining the Physiological Effects of Temperature
5
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The physiological optimum is the temperature under which a number of physiological
functions, including growth, swimming, spawning and heart performance, are optimized.
Physiological optimum temperature can be estimated as the average of growth optimum and final
preferendum (Armour 1990, McCormick and Wegner 1981). Physiological optimum has been
used as the basis for estimates of suitable temperatures for fish survival (NAS 1972). Because
growth optima heavily influence the physiological optimum, optimum growth is intimately linked
with temperatures producing high survival. Optimum growth during the warm, maximum growth
season (generally summer) is then linked with high survival. Optimum growth depends on food
availability. As food availability declines, the temperature producing optimum growth also is
lowered. The growth optimum is also found near the temperature for maximum metabolic scope
(Brett 1952). The greater the scope, the greater the ability of fish to divert energy to either
somatic growth or gamete production. Obviously, maximizing growth is not desirable at all times.
For example, rapid egg development throughout incubation would result in improper emergence
timing, and rapid, early juvenile growth would result in early smolt emigration (Holtby et al.
1989). On the other hand, inadequate size attained bysmolts leads to poor ocean survival
(Metcalfe and Thorpe 1992). These contrasting demands imply that it is important to achieve
high growth rates during the growth season and to minimize the loss of energy during the
remainder of the year. At a stream system scale, this maximization of growth rates would occur
only in the center of the geographic distribution of the species according to the natural potential
of the system to produce the corresponding thermal regime. Exceeding the temperature
producing optimum growth (e.g., in the center of distribution) results in diminished growth rate,
increased disease incidence, and increased sublethal stress (see Elliott 1981).
Recommendation of temperatures for protection of fish species must emphasize high survival
by life stage (e.g., egg, juvenile, smolt, adult). High ability to perform all key life functions (e.g.,
feeding, growth, swimming, migration, reproduction, mate selection) is also an important link to
fitness and population viability.
The general form of the relationship between growth and temperature is a hump-shaped
(symmetrical or skewed) curve in which an intermediate temperature produces optimum growth,
and temperatures both higher and lower result in declines in growth rate to zero. Upper incipient
lethal temperatures (UILT) can obviously result in zero growth when mortality occurs. However,
growth rates at temperatures above the optimum can plummet rapidly to zero with increasing
temperature and reach zero at temperatures less than the UILT (Brett et aL 1982). Growth
responses can also be fairly broad in the vicinity of the optimum so that an optimum zone might
be described. Again, temperatures above the optimum zone can result in sharply declining growth
rates, so caution is warranted in setting criteria at the upper end of the optimum zone.
What are the thermal requirements for smoltification?
Smoltification occurs in juvenile fish as they prepare to move from a freshwater habitat to a
marine habitat. The parr to smolt transformation involves changes in activity, coloration, shape,
and physiological tolerance to seawater. The ultimate biological goal of smoltification is to
increase survival of smohs upon entering the marine environment.
Effects of temperature on the smolting process have been studied in terms of changes in
SummaryofTechnical Literature Examining the Physiological Effects of Temperature 6
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growth, condition factor, body silvering, body moisture and lipid content, salinity tolerance, and
gill Na-K-ATPasc activities (Johnston and Saunders 1981). 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, or other stresses detrimental to fitness.
Salmon and steelhead during the smolt phase have various degrees of sensitivity to elevated
water temperatures (e.g., Adams et al. 1973, Zaugg and McLain 1976, Hoar 1988).
Temperatures that have been reported in the literature as impairing smohification range from
approximately 53.6-59°F (12-15°C) or more (Table 2). Steelhead appear to be most sensitive
during this stage, as opposed to their greater resistance to high temperatures during other juvenile
stages. Although some bull trout do enter the nearshore marine environment, little is known
about their smoltification process and sensitivities. Smolt migration during periods of high water
temperatures can cause inhibition or reversal of the smoltification process or a termination of
migration (i.e., return to freshwater residency for an additional year). Qualitatively, this effect can
be linked to changes in visual or physiological indicators, such as gill Na+-K+ ATPase activity.
These qualitative indices, in turn, are linked to a towered survival of smolts when subjected to
seawater challenges. Lowered survival is associated with inability to osmoregulate due to altered
physiological status. Because sensitivity of smolts to elevated mainstem temperatures varies by
species and because species and stocks vary in migration timing, the significance of effects of
mainstem temperatures on smoltification and survival require consideration of thermal regime
during the migration period by species.
Table 2. Temperatures that have been linked to impairment of smoltification, ability of smolts to
migrate, or survival during smolt migration
Species
Temperature (°C) threshold for
impairment
Reference
Chinook
12
Wedemeyer et al. (1980)
17-20
Marine (1997)
12
Wedemeyer et al. (1980)
Coho
15
Zaugg and McLain (1976)
12
Wedemeyer et al. (1980)
15
Adams et al. (1975)
Steelhead
>13
Hoar (1988)
>12.7
Adams et al. (1975)
(summer steelhead)
>13.6
Zaugg et al. (1972, as cited by
Zaugg and Wagner 1973)
12
Zaugg (1981)
Sockeye
12-14
Brett et al. (1958)
Summary of Technical Literature Examining the Physiological Effects of Temperature 7
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To provide a thermal regime protective of smoltification, temperature should follow a
natural seasonal pattern (Wedemeyer et al. 1980). Varying temperatures are common in the
natural environment, and fluctuating temperatures are more stimulating to steelhead smoltification
than constant temperatures (Wagner 1974 as cited by Hoar 1988, Zaugg and Wagner 1973). An
extreme example of the interference of elevated and constant temperatures on smoltification can
be found in themainstem Columbia River reservoirs, where environmental conditions are of
considerable concern. The large thermal inertia due to the volume of stored water in the
reservoirs alters the seasonal, as well as diel, thermal regimes (Bennett et al. 1997, Karr et al.
1992, 1998).
What are the thermal requirements for swimming speed?
Beamish (1978) classified swimming performance of fish into three categories: sustained,
prolonged, and burst swimming. Sustained swimming performance is that swimming speed that
can be maintained for long periods (>200 min) without fatigue. Prolonged swimming speed
defines a performance of shorter duration (20 s to 200 min). Burst swimming speed is the speed a
fish can swim for a few seconds. Swimming speed for fish of a certain species and size can have
maximum swimming speeds defined by the number of body lengths traveled per second (Bjornn
and Reiser 1991) or in absolute terms of distanceAime.
According to Bell (1986), sustained speed is used for passage through difficult areas,
prolonged or cruising speed during migration, and dart or burst speed for escape, feeding, and
rapid movement through swift water. During adult migration, if water temperature is high or
oxygen concentrations are tow, swimming speed can be impaired and the fish may refuse to
migrate, migrate back downstream, or seek shelter in tributaries or other available cold-water
refuges (Fish 1948, Schreck et al. 1994). Under these conditions the migration maybe delayed or
restricted. Smolts, on the other hand, benefit from availability of rapid current flow because their
downstream progress depends on water velocity rather than their swimming speed. However,
swimming speeds of smolts must not be impaired because swimming is vital to maintaining
position in the current to control rate of descent and avoid obstacles.
Small fish generally have lower swimming speeds (ft/s) than large fish at any given
temperature. Large predators can easily overtake small fish, so that ability to avoid predators
with burst swimming is essential. Burst swimming used during avoidance behavior requires
recovery time, and excessive stress can lead to death. Burst swimming can be impaired under
high temperature or low oxygen conditions. Prcdaceous species more adapted to warm water
such as northern pikeminnow (native), walleye (exotic), and smallmouth bass (exotic), for
example, find their optimum swimming speeds at temperatures greater than those of salmon and
steelhead.
Water temperature and oxygen are significant controls on swimming speed. Swimming
performance also depends on prior acclimation temperature in relation to exposure temperature.
Disease has been shown to adversely affect the swimming performance of mature sockeye salmon
caught in Port Alberni Inlet and transferred to Simon Fraser University for swimming tests at
66.2-69.8°F (19-21°C) (as cited inMacdonald et al. in press). Critical swimming performance
Summary of Technical Literature Examining the Physiological Effects of Temperature 8
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was reduced to 65% of normal by diseases. Stress can also adversely affect swimming
performance. High plasma lactate levels are known to negatively affect swimming performance
(Farrell et al. 1998 as cited in Macdonald et al. in press). Telemetry studies at Hell's Gate suggest
that fish that failed to negotiate Hell's Gate exhibited one or more periods >10 min in which they
swam at speeds greater than their estimated critical swimming speed. Stress is believed to induce
such frantic behavior and cause the fish to be washed downstream.
Field studies with Fraser River sockeye (as cited in Macdonald et al. in press) reportedly
support the work of Brett (1971, 1995) (optimum swimming performance at 59-64.4°F
[15-18°C]) and found the temperature optimum to be 62.6°F (17°C) for swimming endurance,
with almost a 20% reduction in swimming speed at 69.8°F (21°C).
In 1997, researchers reportedly found that because of high water velocity some sockeye
salmon depleted their lipid stores more quickly than in previous years. Consequently, muscle
protein and gl>cogen reserves were utilized earlier in the migration than was expected under
normal conditions; many fish failed to reach the spawning grounds (Donaldson et al. 2000, Higgs
et al. 2000; as cited in Macdonald ct al. in press). Given that water temperature in 1998 exceeded
the average by 3.6-7.2°F (2-4°C), the authors expected that metabolic stores would have been
reduced at least 25% faster during river migration.
What are the thermal requirements for migration to spawning?
Salmonids often migrate great distances (intrabasin or upstream/downstream anadromous
migrations) in river systems during the warm season. The success of these migrations can depend
substantially on water temperatures. Most stocks of anadromous salmonids have evolved with
the temperature regime of the streams they use for spawning and migration, and alteration of the
normal temperature pattern can result in reduced fitness. Migration blockages occur consistently
among species in the temperature range 66.2-73.4°F (19-23°C) (Table 3).
Elevated temperatures in mainstem rivers that provide migration corridors (especially those
dominated by reservoirs) are harmful for survival and reproduction of bull trout, chinook,
steelhead, and sockeye (especially, because of their adult migration timing). These effects occur
via several mechanisms: (1) direct lethality to adults and smolts under high temperature
conditions, (2) delay in migration and spawning, (3) depletion of energy stores through
, heightened respiration, (4) deformation of eggs and decreased viability of gametes, and (5)
increased incidence of debilitating diseases. See the Behavior issue paper for a discussion of the
effects of temperature on the migratory behavior of salmonids.
Macdonald ct aL (in press) studiod the high mortality rates in sockeye and chinook salmon
that occurred in the Fraser River Watershed of British Columbia, Canada. They found
temperature to be the likely cause of both en route and prespawning losses. On the basis of their
review of the historical database, the authors suspected that losses in spawning runs occur when
mean daily river temperatures exceed 62.6-64.4°F (17-18°C) for prolonged periods. Migration
blockages, susceptibility to disease, impaired maturation process, increases to stress parameters,
reduced efficiency of energy use, and reduced swimming performance were all cited as potentially
serious hazards as daily mean temperatures exceed 62.6°F (17°C). In examining fertilization
Summary of Technical Literature Examining the Physiological Effects of Temperature 9
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success, the authors found significant impairment (only 10% success) in stocks that
Tabic 3. Studies that identify thermal blockages to adult salmon migration
Species
River
Temperature cited as
blocking migration
Reference
chinook, sockeye,
steelhcad
Columbia
71-75°F (21,7-23.9°C)
Fish and Hanavan (1948)
spri ng ch inook
Clearwater,
Idaho
69.8°F (21°C)
Stabler (1981)
spring chinook
Tucannon
69.9°F (21.1°C)
Bumgarner et al. (1997)
spring chinook
Willamette
69.8-71.6°F (21-22°C)
(at oxygen >3.5 mg/L)
Alabaster (1988)
summer chinook
Snake
69.8°F (21°C)
Stuehrcnberg et al. (1978) (as
cited by Dauble and Mueller
1993).
fall ch inook
Sacramento
66.2-69.8°F (19-21°Q
(oxygen ~5 mg/L)
Hallock et al. (1970)
steelhcad
Snake
69.8°F (21°C)
Strickland (1967, as cited by
Stabler 1981)
sockeye
Okanogan
69.8°F (21°C)
Major and Mighell (1967)
sockeye
Snake
71.9°F (22.2°C)
Quinn et al. (1997)
sockeye
Okanogan
73°F (22.8°C)
Hatch et al. (1993)
sockeye
Fraser
64.4-71.6°F (18-22°C)
Macdonanld et al. in press
migrated through the Fraser during 1998 (a record warm year) compared with success during
cooler years. Dr . Craig Garke (as cited in Macdonald et al in press) found that a 2-wk exposure
to 66.2°F (19°C) compared with 59°F (15°C) in the laboratory was sufficient to significantly
depress the hormones controlling sexual maturation in sockeye salmon. This was viewed as
consistent with the finding of Manning and Kime (1985, as cited in Macdonald et al. in press) that
steroid biosynthesis was suppressed in rainbow trout testes at 62.6°F (17°C).
Migration has been observed to occur under a wide range of conditions for each salmon
species (see Bjornn and Reiser 1991). This reflects a combination of characteristics about the
fish: the seasonality of their migration period, temperatures that were available to them during
their normal migration period, shifts in migration timing that may have occurred over time (e.g.,
effects of deliberate attempts by hatchery managers to create a run that does not overlap with a
wild run, the response by the stock itself to shifts in river temperature regimes during the
incubation, smolt migration, and/or adult migration periods), and in some species that migrate
during warm seasons their tolerance to elevated temperatures. Bioenergetic stresses (ability to
maintain long-term energy reserves), instantaneous power demands (ability to exhibit burst
swimming, jump falls, escape predators, recover from stress [exertion, disease]), and ability to
Summary of Technical Literature Examining the Phjsiological Effects of Temperature
10
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resist disease may all be of concern in the higher temperature range for migration. Just as
distribution ofjuveniles relates to temperature in a stream system (i.e., from optimum to
suboptimum to the distributional limits), migration temperatures can be assumed to have an
optimum that is less than the migration limit and migration can be impaired as the limit is
approached.
Fall and spring chinook are examples of different life history types of a single species having
differing migration and spawning timings. Given the similarity in ultimate upper incipient lethal
temperatures of these two races (NAS 1972) and the minor differences in ultimate upper incipient
lethal temperature (UUILT) among stocks of numerous species, it is reasonable to assume that
fall and spring chinook have similar UUILT values for juvenile and adult stages, respectively.
Because adult spring chinook migrate earlier in the year than fall chinook they encounter cooler
water temperatures in mainstem rivers. However, spring chinook also must hold in tributaries
until the autumn spawning season, so avoidance of high holding temperatures is their thermal
challenge. For fall chinook, the thermal challenge is avoidance of higher thermal stress both
during adult migration and during a more brief holding period. Temperature ranges for spring,
summer, and fall chinook migration have been summarized (see Bjornn and Reiser 1991), and
show that spring chinook tend to migrate under a range of temperatures having a tower
maximum. Given the similarity in lethal temperatures within this species, the temperatures linked
to successful migration for fall chinook might also adequately represent the capability of spring
chinook, which are not normally tested because temperatures do not tend to be as high during
their migration period. However, threshold temperatures linked to a complete inability to migrate
are very similar between spring and fall chinook, as well as among many anadromous species that
have been examined.
What are the thermal requirements for adult holding and spawning?
Full protection of salmonids during reproduction involves managing instream temperature
during several phases of the reproductive cycle (prespawning, spawning, and postspawning).
Successful reproduction can involve success (survival of adults and their gametes) during
migration, holding prior to spawning, mate selection, redd digging, egg deposition, and nest
guarding. For fall-spawning fish (e.g., bull trout, chinook, coho, chum), temperatures typically
reach their annual highs during migration and/or holding. Stocks that take advantage of the
predictability of the most generally favorable seasons time their migration and spawning to
complete life-cycle phases. Long-term alterations in temperature regimes can disrupt this timing.
Disruptions in timing include a reduction in time available to complete a subsequent life-cycle
process or a change in timing of this process.
Temperature can inhibit upstream migration of adult fish. This can result in seeking cold-
water refuges such as deep pools in the mainstem, cold tributary mouths, or downstream
mainstem areas. Inhibitory temperatures thus can cause migration delays that alter timing of key
processes such as spawning or can lead to stress, disease, bioenergetic depletion, or death. If
migration occurs at high temperatures just prior to spawning (such as in fall chinook or coho),
gametes held internally in adults can be severely affected, resulting in a loss of viability that
appears as poor fertilization or embryo survival. High temperatures during the holding or
prespawning stages can also occur in many locations, even if adults have managed to escape high
Summary ofTcchnical Literature Examining the Physiological Effects of Temperature
11
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mainstem migration temperatures. Then, if water temperatures have not begun to decline below
critical thresholds before spawning begins, fertilization and early incubation survival will be
affected. Early incubation is very sensitive to elevated temperatures. In addition, salmonid
diseases can affect the egg stage as readily as other life stages.
The above section on migration detailed the inhibition of adult migration that occurs with
elevated temperatures in migratory corridors. Spring chinook, summer chinook, and fall chinook
all migrate during different seasons, but high water temperatures can be assumed to have similar
effects on migration for all races. In addition, other species respond to the same thresholds.
Furthermore, it is of great concern that UILT values for chinook and coho are approximately the
same as the temperatures that inhibit migration. This implies that salmon will cease migrating at
temperatures just below those required to kill a portion of the population.
What are lethal temperature effects?
National Academy of Sciences (NAS) (1972) recommendations for water temperature
exposure for protection of aquatic life specify maximum acceptable temperatures for prolonged
exposures (> 1 wk), winter maximum temperatures, short-term exposure to extreme temperature,
and suitable reproduction and development temperatures. Lethal effects are thermal effects that
cause direct mortality within an exposure period of less than 1 wk. Prolonged exposure
temperatures and temperatures that interfere with normal reproduction and development can
result in mortality or reduction in population fitness or production, but the effects maybe delayed
or indirect, or result from impairment of function or reduction in suitable habitat or food quantity
and quality available.
Survival rates based on amount of time exposed and temperature of exposure are extremely
well described in the scientific literature. These time-temperature relationships have been
described using equations of the form log (time) = a + b (temp.), where time is expressed in
minutes, temperature is in degrees Celsius, and a and b are coefficients for intercept and slope of
the regression, respectively, described for individual acclimation temperatures (NAS 1972). The
regression describes the combinations of time and temperature that result in mortality (typically
recorded as the point of estimated 50% mortality) at various acclimation temperatures. The upper
incipient lethal temperature (UILT) is an exposure temperature, given a previous acclimation to a
constant acclimation temperature, that 50% of the fish can tolerate for 7 d (Elliott 1981).
Alternatively, UILT at a particular acclimation temperature has been determined as an exposure
temperature producing 50% survival within 1,000 min (Brett 1952, Elliott 1981) or 24 h
(Wedemeysr and McLeay 1981, Armour 1990). Within this variation in exposure times, we
expect a slightly lower UILT at a 7-d than a 24-h exposure. The UILT becomes greater with
increasing acclimation temperature until a point is reached at which further increase in acclimation
temperature results in no increase in temperature tolerated with the same survival level. This is
the ultimate upper incipient lethal temperature.
In addition to acclimating fish to a constant temperature prior to exposure to test
temperatures, fish maybe acclimated to a fluctuating temperature regime. It is possible to
determine for a cyclic acclimation temperature a corresponding constant temperature, that is, an
equivalent constant temperature. This is accomplished by experimentally determining the constant
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
12
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acclimation temperature within the range of the cyclic regime that produces the same response to
an exposure temperature as the cyclic regime.
Because UILT varies with increasing acclimation temperature until the UUILT is reached,
the UUILT is a good stable index for comparing thermal response among species. For salmonids,
a survey of the literature indicates that acclimation temperatures above approximately 68°F
(20°C) produce similar UILT values, although very small increases in UILT can occur at up to a
75.2°F (24°C) acclimation temperature. Consequently, it can be safely assumed that any UILT
study in which acclimation temperature was ^ 68°F (20°C) will produce a UILT nearly identical
to the UUILT. UILT values compiled from the literature (taken from McCullough 1999) for
various acclimation temperatures are presented in Table 4. Given the considerations above, these
values can be interpreted as estimates of UUILT.
What conclusions can you draw for anadromous salmonids and coastal cutthroat and
rainbow trout?
1. Five species of Pacific salmon—chum, Oncorhynchus keta\ coho, O. kisutch; sockeye, O.
nerka; chinook, O. tshawytscha; and pink, O. gorbuscha—and steelhead, O. mykiss, and
coastal cutthroat trout, O. clarki, are stenothermic and have similar physiological
requirements for cold water. Given their similarity in physiological requirements, a common
temperature criterion could be established to protect these seven species as a single group.
In those waterbodies where multiple species and life stages are present, temperature criteria
would need to be oriented to the most sensitive species and life history stage.
2. Measures of maximum growth and swimming speed are useful in defining the optimal
temperature range. However, these tests are typically conducted under controlled laboratory
conditions and may not accurately reflect the influence of temperature under the more
complex ecological context of natural stream systems. Laboratory results may need to be
adjusted downward to account for the influences of reduced food availability, competition,
predation, and other environmental variables. Also, laboratory results may not reveal
sublethal effects associated with an increased risk of warm-water disease and physiological
stresses of smoltification under elevated water temperatures.
a. Maximum growth and swimming speed generally occur within the range of 55.4-68°F
(13-20°C) for native salmon and trout under laboratory conditions in which fish are fed
to satiation. Maximum swimming speeds appear to be at temperatures greater than
those providing maximum growth rates. The ecological need for temperatures allowing
maximum growth is greater than for maximum swimming speed. That is, of the two
biological performances controlled by temperature, growth rates have a greater need to
be optimized on a basinwide scale (sec issue papers on Fish Distribution and
Spatio-Temporal Effects as well as the final synthesis paper for a complete description
of this concept). In addition, optimum growth temperatures provide nearly optimum
swimming speeds.
b. Streams with naturally low productivity or in which food availability is lower than
under natural conditions (e.g., caused by stream channel sedimentation and high
SummaryofTechnical Literature Examining the Physiological Effects of Temperature 13
-------
substrate embcddedness) can be expected to produce optimal growth at temperatures
that are lower by at least 3.6-7.2°F (2-4°C) and, under certain conditions, as much as
Table 4. Upper incipient lethal temperature of various juvenile salmonids
Species
Common
Name
Origin
(river/lake)
Author(s)
Accl.
Temp. ( C)
UILT (°C)
Oncorhynchus
tshawytscha
chinook
salmon
Dungeness
Hatchery, WA
Brett (1952)
20
24
25.1
25.1
Sacramento River
Orsi (1971, as
cited by CDWR
1988)
21.1
24.9
Oncorhynchus
kisutch
coho sal mon
Nile Cr. Hatchery,
British Columbia
Brett (1952)
20
23
25.0
25.0
Oncorhynchus
nerka
sock eye
salmon
Iss aquah Ha tch ery,
WA
McConnell and
Blahm (1970) (as
cited by Coutant
1972)
Brett (1952)
20
20
23
23.5
24.8
24.3
Oncorhynchus
keta
chum
salmon
Nile Cr. Hatchery,
British Columbia
Brett (1952)
20
23
23.7
23.8
Oncorhynchus
gorbuscha
pink
Dungeness
Hatchery, WA
Brett (1952)
20
24
23.9
23.9
Oncorhynchus
mykiss
rai nbow
trout
Lake Superior
Hokanson et al.
(1977)
16
25.6
France
Charlon et al.
(1970)
24
26.4
Lakes Erie, Ontario,
Huron, Superior
Bidgood and Berst
(1969)
15
25-26
Cherry et al.
(1977)
24
25
Stauffer et al.
(1984)
24?
26
Ontario
Threader and
Houston (1983)
20
25.9
Alabaster (1964)
(as ci ted by
Threader and
Houston 1983)
20
26.7
Summerland
Hatchery, British
Columbia
Firehole River, MT
Ennis Hatchery
Winthrop Hatchery
Black (1953)
Kaya (1978)
11
24.5
24.5
24.5
24
26.2
26.2
26.2
Summary of Technical Literature Examining the Ph>siological Effects of Temperature
14
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Table 4. Upper incipient lethal temperature of various juvenile salmonids (continued)
Species
Common
Name
Origin
(river/lake)
Author(s)
Accl.
Temp. (°C)
UILT (°C)
redband
trout
Parsnip Reservoir,
Oregon
Sonski (1983a)
20
23
27.4
26.8
Parsnip Reservoir,
Oregon
Sonski (1984)
20
23
26.2
26.2
Firehole River,
Wyoming
20
23
27.2
26.3
Wytheville rainbow
20
23
26.8
27.0
Salmo salar
Atlantic
salmon
England
Bishai (1960)
20
23.5
Salmo trutta
brown trout
England
Bishai (1960)
20
23.5
Frost and Brown
(1967)
23
25.3
Cherry et al.
(1977)
?
23
England
Alabaster and
Downing (1966)
(as cited by Grande
and Anderson
1991)
20
26.3
Salvelinus
fontinalis
brook trout
Ontario
Fry, Hart, and
Walker (1946)
20
24
25.3
25.5
Cherry et al.
(1977)
?
24
Salvelinus
namaycush
lake trout
Ontario
Fry and Gibson
(1953)
20
24.0-24.5
Thymallus arcticus
Arctic
grayling
Montana
Lohret al. (1996)
20
25
Alaska
LaPerriere and
Carlson (1973) (as
cited by Lohr et al.
1996)
?
24.5
14.4°F (8°C) from temperatures producing optimal growth under satiation feeding. In
the natural environment, food is often limited to less than satiation levels.
c. Disease occurrence and severity are primarily determined by the specific strain of the
pathogen, the temperature of the water, and the relative health of the exposed fish. The
following general patterns can be identified from laboratory and field research: constant
Summary ofTechnical Literature Examining the Physiological Effects of Temperature 15
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temperatures below 53.6-55.4°F (12- 13°C) often reduce or eliminate both infection and
mortality, temperatures above 59-60.8°F (15-16°C) are often associated with high rates
of infection and notable mortality temperatures above 64.4-68°F (18-20°C) are often
associated with serious rates of infection and catastrophic outbreaks of many fish
diseases.
d. At the time of smoltification, anadromous salmonids experience reduced ATPase levels
at constant or acclimation temperatures greater than 51.8-55.4°F (11-13°C). Reduced
ATPase levels may result in delayed or ineffective transition to the marine environment
and may result in smolts attempting to return to freshwaters to wait until the next
spring. Temperatures above 64.4°F (18°C) may inhibit feeding in smolts, and
temperatures of 57.2-59°F (14-15°C) may cause cessation of the seaward migration.
3. Stream temperatures vary through the spawning and egg incubation period, particularly for
species that spawn in late summer and fell. There are several factors to consider in setting a
criterion for these Kfe history stages: temperatures that affect survival of gametes in adults
prior to spawning, temperatures that affect the initiation of spawning behavior, temperatures
that maximize the survival of eggs upon deposition in gravels and early embryo stages, and
temperatures that allow for the correct timing and size of fry at hatch and emergence. In
summary, it appears that a range of temperatures from 42 to 55°F (5.6-12.8°C) allows for
successful spawning and incubation for different species of salmon.
a. For fall-spawning fish, spawning may be initiated in the field at temperatures of 57.2-
60.8°F (14-16°Q. Experiments done at constant incubation temperatures, however,
show that survival of eggs under these conditions is low. Consequently, spawning
temperatures >57.2°F (14°C) arc considered to provide marginal to poor egg survival
for these early-spawning fish.
b. For fall-spawning fish, spawning that is initiated as daily maximum temperatures fall
below 53.6-57.2°F (12-14°C) results in greater incubation success, with 55°F (12.8°C)
being adequate for most salmon species.
c. In laboratory studies, constant temperatures of 42.8-50°F (6- 10°C) or lower during
incubation consistently result in maximum survival and size at emergence for Pacific
salmon, stcelhead, and coastal cutthroat trout.
d. Constant incubation temperatures as low as 39.2°F (4°C) and as high as 53.6°F (12°C)
can result in good to veiy good survival to hatching and emergence, with
approximately 46.4°F (8°C) being optimal for most salmon species.
4. Laboratory and field studies show that when adult fish are exposed to constant or average
temperatures above 55.4-60°F (13-15.6°C) during the final part of the upstream migration
or during holding prior to spawning, there is a detrimental effect on the size, number, and/or
fertility of eggs held in vivo.
5. Many studies have been done on the acute lethality of warm water temperatures on
SummaryofTcchnical Literature Examining the Physiological Effects of Temperature 16
-------
salmonids. Laboratory tests of acute lethality measure the temperature at which 50% of the
fish die after 1 to 7 d of exposure to a constant temperature (upper incipient lethal
temperature, or UILT).
a. The range in UILT values found in multiple tests of various species of juvenile
salmonids is 73.4-75.2°F (23-24°C) when acclimation temperatures are between 50 and
59°F (10 and 15°C). Although UUILT (ultimate upper incipient lethal temperature)
values reported in the literature and in this paper are up to 78.8°F (26°C), fish in the
field will not necessarily be acclimated to warm temperatures as they are in laboratory
tests of UUILT. Therefore, UILT values in the field may be 1.8-3.6°F
(1 -2°C) lower than the UUILT values derived in the laboratory.
b. The range in UILT values for adult salmonids is 69.8-71.6°F (21-22°C) when
acclimation temperatures are approximately 66.2°F (19°C). Adults appear to have
lethal tolerances 3.6-5.4°F (2-3°C) lower than the juvenile fish typically used in lethality
testing.
c. When fish are acclimated below 53.6°F (12°C), substantial lethality (LT50) can be
expected to occur almost instantly (1-60 s) at temperatures above 86-93.2°F
(30-34°Q.
d. Migratory fish, particularly anadromous fish, may not be fully acclimated to warm
mainstem temperatures.
e. In a fluctuating environment, multiple-day exposure to lethal temperatures may create
cumulative effects.
6. For all salmonids, figures can be compiled from the literature to depict temperature
requirements by species and life stage. Such a diagram was devebped by McCullough
(1999) for spring chinook. The value of such diagrams is to highlight the ranges for normal
function and high survival (e.g., egg incubation, adult migration), optimum growth ranges
(e.g., juvenile stage), and thresholds for eflfects that become increasingly significant both
above and below incipient lethal levels (e.g., disease, migration bbekages, cold effects on
egg incubation). For any life stage, there are multiple potential effects on survival, fitness,
and growth. Recommendations for temperature criteria for a waterbodymust account for
the most sensitive species, most sensitive life stages of a species for any season, and the
multiple effects on each life stage.
What conclusions can you draw for bull trout and Dolly Varden?
1. Bull trout (S. confluentus) are not actually trout, but are char. Bull trout and Dolly Varden
(S. malma) are the only native char found in Idaho, Washington, and Oregon. Members of
the genus char live in the coldest, cleanest, and often most secluded waters.
2. All char are fall spawners and cold water temperatures seem to be the proximate cue that
initiates spawning behavbr and defines distributbn. Char are cold-water fish that are
Summary of Technical Literature Examining the Phjsiological Effects of Temperature
17
-------
especially sensitive to thermal change and find optimal rearing conditions in a wide variety of
stream sizes that can provide the coldest water possible in the Pacific Northwest. Char are
Holarctic in distribution and include the most northerly distribution of any fish found in
freshwater. Char may be anadromous, resident, or freshwater migratory.
3. Little information is available for the physiological requirements of bull trout and Dolly
Varden. Available research for bull trout includes information for incubation, fry and alevin
growth and survival, growth rates for juvenile fish under variable feeding regimes, and
juvenile lethality. This is substantially less than the broad range of metrics available for many
other salmonids; however, it does include some important physiological characteristics for
setting temperature criteria. Evidence from laboratory studies and distribution data indicates
that bull trout have optimum temperature requirements substantially bwer than the other
salmonids examined in this paper, and that water temperatures protective of bull trout will
require establishment of separate temperature criteria.
a. Optimal incubation for bull trout eggs occurs at constant temperatures in the range of
35.6-42.8°F (2-6°C), with highest incubation success at 39.2°F (4°C). Temperatures in
the range of 42.8-46.4°F (6-8°C) can produce variable but often substantially reduced
egg survival and size at emergence.
b. Under laboratory conditions, maximum growth temperature declines as ration declines.
Growth rates in the studies conducted at satiation and 66% satiation were highest at
constant temperatures of 60.8°F (16°C), although the growth rate was less in the bwer
(66%) ration test than at 100% satiation At the 33% satiation ration the growth rate
was maximized at 46.4-53.6°F (8-12°C). This conclusion is based ona single set of
experiments on bull trout. Much more extensive studies of brown trout growth rates
under a series of rations show similar declines in growth rate with decreased ration.
From these studies we would expect growth optima to decline with each increment of
decline in ration.
c. The UILT for juvenile bull trout is 71.6-73.4°F (22-23°C) for a 7-d exposure.
What conclusions can you draw for other salmonids?
1. Interior native sahnonid species found in Oregon, Washington, and Idaho include Westslope
(O. clarki lewisi), Yellowstone (O. clarki bouvieri), Bonneville (O. clarki utah), and
Lahontan cutthroat trout (O. clarki hens ha vvz); redband trout (O. mykiss gairdneri); and
mountain whitefish (Propsipium williamsoni).
2. Little information is available on the effects of temperature on the physiology of these
salmonids. Although a few laboratory study results are available, we have referenced field
distribution data.
3. Mountain whitefish were not reviewed because of limited information. It is assumed that
temperature criteria established to protect other salmonid species protect whitefish where
they occur.
SummaryofTechnical Literature Examining the Philological Effects of Temperature
18
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SUPPORTING DISCUSSION AND LITERATURE-GENERAL ISSUES
Laboratory and Field Studies
What are the advantages and disadvantages of laboratory and field data?
Our understanding of thermal effects on salmonids is based on a combination of laboratory
and field evidence. In the adult life stage, much of the information available comes from field
studies; on the other hand, for the juvenile life stages, most information on thermal effects comes
from laboratory studies.
Some argue that laboratory studies have limited use in setting standards because of
unrealistic conditions. In truth, each type of study is capable of providing useful information. In
determining the usefulness and applicability of laboratory study results, it is important to assess
the possible confounding variables such as whether wild fish or hatchery progeny were used,
feeding rations, competition, or other ecological issues that may or may not be described in the
methods for the laboratory study.
Reisenbichler and Rubin (1999) provide strong evidence that salmonids' fitness for natural
spawning and rearing can be rapidly and substantially reduced through artificial propagation.
Genetic differences in behavior and physiology can occur in the offspring of hatchery fish.
Hatchery fish are often raised in waters with constant temperature and in warmer water more
conducive to rapid growth at satiation feeding.
Laboratory studies of thermal effects on salmonids are most often conducted under constant
temperature conditions, although what is considered constant can fluctuate as much as 1.8°F
(1 °C). It is obvious that in natural stream systems, temperatures fluctuate hourly. This pattern
can be represented as a sine wave, with a maximum temperature in midafternoon and a minimum
temperature in early morning. This cycle is summarized statistically according to its minimum,
mean, or maximum temperature. However, from day to day these values can change, resulting in
continually changing conditions in the stream. If temperature cycles were identical (i.e., their
pattern and minimum and maximum remained steady) for several consecutive days, it would be
easier to biologically describe acclimation conditions. Under such a repetitive cycle, a scientific
challenge would be to identify the "effective acclimation temperature," that is, the temperature in
a fluctuating thermal environment that produces acclimation equivalent to a constant-temperature
acclimation.
Fluctuating temperature conditions lead to major issues that make it difficult to predict
thermal effects. From laboratory tests using constant temperatures it is known that survival is a
function of exposure temperature and exposure time, but the magnitude of the effect also depends
on prior acclimation temperature. If water temperatures are variable during both the acclimation
and the exposure phases of a test, it becomes difficult to make an accurate prediction of effects
based on constant-temperature laboratory studies. Likewise, in the absence of any laboratory
studies, it would be difficult to create a predictive model of survival under a thermal regime in
which acclimation and exposure history are both varying.
Summary of Technical Literature Examining the Physiological Effects of Temperature
19
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Laboratory tests of survival under thermal stress have several distinct advantages.
Laboratory studies albw both acclimation and exposure temperature to be precisely controlled.
Acclimation and exposure temperatures can be made either constant or fluctuating, and if
fluctuating, they can conform to precise, repeatable cyclic patterns. Under laboratory conditions,
wc know precisely what temperatures fish are actually experiencing. That is, fish arc not able to
seek thermal refuges during survival tests as they could in the field. In the laboratory the
condition (diseases, prior feeding history, gut contents prior to testing) of the test organisms can
be controlled.
Laboratory results can sometimes be an artifact of laboratory methods, conditions, or
apparatus. For example, "tank effects" can result from behavioral interactions between test
organisms. If crowding is an issue, fish can be stressed from agonistic behavior. If current speeds
are not similar to those the fish would experience in a field setting, many unexpected effects could
occur. For example, various performances of a population can change with current
speed—behavior, energy expenditure during swimming, oxygen uptake rate in the gills, or
recovery from stress (Milligan et al. 2000). Attention must be given to photoperiod for certain
performances to be meaningfully represented (Clarke et al. 1992). Disturbance to test organisms
during testing must be controlled (e.g., minimizing startling the fish during observation). For
some kinds of tests, such as temperature preference, equipment can affect results. For example, it
can make a difference whether fish are allowed to seek their temperature preference within a
vertical versus a horizontal thermal gradient.
Field testing of fish survival under high temperatures is not usually done. One possible field
method is to catch fish from a stream after having monitored the ambient temperature conditions
for several days. This acclimation history would then be used as a basis for interpreting exposure
results. Fish could be tested in an experimental apparatus at streamside. This method would rely
on artificial equipment (tanks) to test their response, but would involve uncertainty in effective
acclimation temperature. An alternative method could be to monitor fish densities weekly and
water temperatures hourly in a stream reach netted off to prevent emigration or immigration.
This would be a "realistic" field test, but would involve uncertainty in effective acclimation
temperature and difficulty in integrating exposure temperatures. Also, reduction in fish density
would be attributable to natural mortality factors (developmental causes, disease, predation) that
would need to be controlled, as well as temperature effects.
If such methods were feasible, the improved realism would be helpful. For example, it
would be useful to know the influence of food availability as mediated by thermal regime and
other environmental conditions (light, nutrients, organic inputs, competition for food and space),
as well as associated natural disease occurrence, in regulating mortality under thermal stress from
acclimation phase to exposure phase in the field. These combined effects during acclimation
would likely result in greater mortality under field conditions than in laboratory settings, in which
multiple stresses are limited. Although these multiple effects constitute the realism that ecologists
are interested in, the best chance of adequately understanding these effects is to study them in
controlled laboratory tests and then compare predictions from laboratory experience with field
data.
If our most precise understanding of thermal effects is from laboratory tests, what
SummaryofTechnical literature Examining the Physiological Effects of Temperature
20
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methods can be used?
Tests of survival under thermal stress have conventionally been done using either the ILT
(incipient lethal temperature) or the CTM (critical thermal maximum) methods. It has generally
been accepted that the ILT methodology presents the best means of assessing acute effects
because it does not allow for the variable levels of partial acclimation that occur in CTM tests
having varying rates of heating. In the ILT method the test endpoint is death; in the CTM test,
the endpoint is either loss of equilibrium or death.
Conventional use of the ILT method is to acclimate test organisms at a constant temperature
and thai immediately transfer them to a constant test temperature. This and other methods are
possible as shown in the table below:
No.
Acclimation
Exposure
Methodology
1
constant
constant
conventional ILT (e.g., Fry
1947, Brett 1952)
2
constant
cyclic
Hokanson et al. (1997),
Golden (1976)
3
cyclic
constant
Threader and Houston (1983)
4
cyclic
cyclic
Golden (1976)
5
constant
constant, with multiple
exposures
6
constant
stepped increase
CTM variant
7
constant
continuous increase
conventional CTM (e.g.,
Becker and Genoway 1979,
Elliott and Elliott 1955)
Test condition 1 is the conventional ILT methodology and allows the most accurate
knowledge of effective temperatures. Given data from these tests, it is possible to determine the
percentage mortality of a salmonid test population at temperatures such as 77, 78.8, 80.6, 82.4,
and 84.2°F (25, 26, 27, 28, and 29°C), for example, as well as time to death. With a
mathematical expression of these results, it is feasible to estimate percentages of a lethal dose that
could be acquired during exposure to a cyclic temperature regime.
Test condition 2 allows accurate knowledge of acclimation history. Subsequent exposure to
a cyclic regime could produce mortality in a test population that could be attributed to a mean
temperature, maximum temperature, or some intermediate temperature. Mortality under a cycle
could also be predicted from knowledge of exposure times at each thermal increment under a
cyclic regime and application of mortality rate coefficients for each temperature increment (e.g.,
Coutant 1972) developed in constant-temperature experiments. A lethal dose maybe estimated
by this summation technique for a single cycle (McCuIlough 1999, cumulative mortification, see
Fry et al 1946 as cited by Kilgour and McCauley 1986). Alternatively, mortality from a constant-
temperature exposure can be contrasted with that from a cycle having the same mean
Summary ofTechnical Literature Examining the Physiological Effects of Temperature 21
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temperature. Results of this comparison vary with the magnitude of the cycle and whether the
mean temperature is less than or greater than the optimal temperature (Hokanson et al. 1977).
Condition 3 presents the best opportunity to estimate an equivalent acclimation temperature
for a cyclic temperature regime in the acclimation phase. Percentage survival is determined in a
constant temperature exposure environment, given acclimation to a cyclic regime. This is then
related to that constant acclimation temperature that would have provided the same survival (or
growth or swimming speed, depending on experiment) as observed in a cyclic temperature
exposure. Experiments such as this demonstrate that equivalent acclimation temperatures in a
cyclic thermal regime are equal to acclimation to temperatures ranging from the mean to the
maximum of the cycle (Heath 1963, Golden 1975, Clarke 1978, Jensen 1990), with much
evidence indicating that a temperature intermediate between the mean and the maximum is a good
representation of equivalent acclimation temperature.
Condition 4 provides a temperature environment during acclimation and exposure phases
that can mimic reasonably occurring field situations. This provides the most "natural" laboratory
conditions, but imposes the need to compare results with combinations of constant acclimation
and/or exposure temperatures. Mortality data obtained for cyclic temperature exposures from this
method are best interpreted against data for constant temperature exposure. Otherwise,
cumulative percentage of a lethal dose could be established as in condition 2 exposure based on
constant temperature laboratory data and the derived survival coefficient for each test
temperature.
Condition 5 provides a constant acclimation and a constant exposure temperature. This
framework would be effective in testing cumulative mortality from multiple exposures.
Cumulative exposures were tested by DeHart (1975), Golden (1975, 1976), and Golden and
Schreck (1978) using cyclic temperatures. They found that mortality could be produced if 100%
of a lethal dose were accumulated in periods of approximately 2 d. A more effective test of
cumulative mortality could be gained by multiple exposures to constant temperatures. It would be
helpful to know whether lethal doses can be accumulated over 3, 4, 5, or more consecutive days.
Constant temperature acclimation followed by stepped or continuous increases in
temperature provides survival results similar to those of CTM tests. Depending on the rate of
increase, a certain degree of partial acclimation can occur, leading to a test endpoint. If the
heating rate approximates that found in field conditions under a thermal c>cle involving high
maximum temperatures, the CTM experiment based on thermal regime number 7 (or its cousin,
number 6) can be helpful in inferring harmful temperature fluctuations. There are some difficulties
in making effective use of CTM data. As in all laboratory or field experiments, properly inferring
effective acclimation temperature is an issue. In the CTM test, the heating rate determines the
degree of partial acclimation that is feasible. Variability in response of individuals needs to be
considered in using CTM data because mortality occurs at temperatures below the median level.
Also, CTM data are based on uniform heating rates. In the field, if high temperatures are
sustained for variable time periods, exposure time and subsequent mortality to the most lethal
conditions can vary substantially.
Potential for Variation Among Stocks or Species of Salmonids
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
22
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Is there enough significant genetic variation among stocks or among species to
warrant geographically specific water temperature standards?
At the time of the 1994 Oregon Triennial Water Quality Review, which involved water
temperature criteria, Oregon's water temperature standards applied a standard of68°F (20°C) to
salmon-bearing streams of northeastern Oregon and 57.9°F (14.4°Q to Oregon Coast Range
streams. The technical committee concluded that there was no evidence for significant genetic
variation in sensitivity to high water temperatures such that different standards (especially ones
differing by 10.1°F [5.6°C]) could be justified for different regions of the State.
Climatic conditions vary substantially among regions of the State and the entire Pacific
Northwest. Maximum and minimum annual air temperatures, rainfall and streamflow patterns
and magnitudes, cloud cover, humidity, and other climatic features all influence downstream
water temperatures and trends. Climate also indirectly influences density and type of riparian
vegetation that itselfhas a role in controlling water temperature. Regional environmental
variations can establish a template to which a species might make evolutionary adaptations. For
example, a species found in a region with streams having a range of maximum summer water
temperatures from 46.4 to 78.8°F (8-26°C) (headwaters to mouth) might become adapted over
time to warmer water temperatures than the same species located in a region having temperatures
ranging only from 46.4 to 68°F (8-20°C). These hypothetical examples may represent historical
extreme conditions in large stream systems in coastal versus eastern Oregon streams. Such
conditions could potentially have led to evolutionary adaptations, resulting in development of
subspecies differences in thermal tolerance.
Acclimation is different from adaptation. Adaptation is the evolutionary process leading to
genetic changes that produce modifications in morphology, physiology, and so on. Acclimation is
a short-term change in physiological readiness to confront daily shifts in environmental conditions.
The extent of the ability to tolerate environmental conditions (e.g., water temperature extremes) is
limited by evolutionary adaptations, and within these constraints is further modified by
acclimation.
The literature on genetic variation in thermal effects indicates occasionally significant but
very small differences among stocks and increasing differences among subspecies, species, and
families of fishes. Many differences that had been attributed in the literature to stock differences
are now considered to be statistical problems in analysis, fish behavioral responses under test
conditions, or allowing insufficient time for fish to shift from field conditions to test conditions
(Mathur and Silver 1980, Konecki et aL 1993). It is also possible that tests intended to
differentiate stock performance (e.g., survival, growth) could inadvertently use test individuals
emphasizing one or a small number of lamily groups. For example, when tested at suboptimal
temperatures, family groups of rainbow trout showed much greater variation in growth rates than
at optimal temperatures (Wangila and Dick 1979).
Are there evolutionary differences among salmonid species in the Pacific Northwest?
Summary of Technical Literature Examining the Physiological Effects of Temperature 23
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Within the species O. tshawytscha (chinook salmon) there is great variation in run timing,
life histories, and habitat selection. This species has stream-type and ocean-type forms, featuring
significant differences in length of freshwater residency. Even so, no subspecies have been
designated for chinook or any other salmon species. Genetic variation does exist, however,
within the chinook and other salmonids in the Pacific Northwest, as shown in classification tree
diagrams drawn by agencies such as the National Marine Fisheries Service (NMFS). These
genetic relationships are based on enzyme frequencies. An accumulation of genetic differences
between populations can eventually become great enough that subspecies are recognized.
However, this has apparently not happened within the salmon, despite the fact that species such as
chinook range from Alaska to mid-Cabfbrnia and from temperate coastal mountain streams to
continental interior streams.
There arc many possible explanations why salmon have not made a significant adaptation to
high temperatures in streams of the Pacific Northwest. Temperature tolerance is probably
controlled by multiple genes, and consequently would be a core characteristic of the species not
easily modified through evolutionary change without a radical shift in associated physiological
systems. Also, the majority of the life cycle of salmon and steelhead is spent in the ocean rearing
phase, where the smolt, subadults, and adults seek waters with temperatures less than 59°F
(15°C) (Welch et al. 1995). It would be unlikely for optimal growth conditions and associated
physiological processes to be radically different in freshwater systems than in ocean environments,
especially when food abundance in freshwater is so much more limited.
What are the major differences in thermal tolerance among and within important
families?
One way to look at evolutionary differences among salmonids is to compare the Salmonidae
with other fish families. Given the data compilation for Salmonidae in this report (Table 4) and
the compilation by Coutant (1972) (sec McCullough 1999, Tables 13 and 14), one can infer a
range of UUILT for the families Salmonidae, Cyprinidae, and Centrarchidae to be 73-78°F
(23-25.6°C), 84-91°F (29-33°C) (Tabb 13), and91-98.6°F(33-37°Q (Table 14), respectively.
The range for Salmonidae accounts for the response of chinook, coho, sockcye, chum, and pink
salmon; steelhead; Atlantic salmon; and brown, brook, and lake trout. There appears to be very
little variation in UUILT among species in family groups, except for a higher lethal limit for
redband trout and a lower one for bull trout. These two species appear to broaden the UUILT
range to 71.6-80.6°F (22-27°C) for the Salmonidae. The Cyprinidae and Centrarchidae are
significantly more tolerant of warm water. However, they arc effective competitors to the cold-
water species that are the primary native species in the Pacific Northwest, because they are very
active feeders at temperatures >68°F (20°C). This capability allows Cyprinidae and Centrarchidae
to increasingly exclude cold-water species at temperatures in this range. This is a partial
explanation for the disappearance of salmonids from streams when maximum temperatures are in
the range of 71.6-75.2°F (22-24°C) (see McCullough 1999).
The small range in UUILT among all the salmonids surveyed and the lack of overlap with
the ranges expressed by the cyprinids and centrarchids indicates fundamental differences among
major families of fish and a narrow window within which potential adaptations would likely be
expressed. If the differences among species within a family are so minimal, it is unlikely that
Summary of Technical Literature Examining the Physiological Effects of Temperature
24
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significant differences would emerge within a species (i.e., at a stock level).
The UUILT values listed above for salmonids represent essentially the juvenile life stages.
Studies have been cited here showing that UUILT values for adult salmon tend to be 3.6-5.4°F
(2-3°C) lower than those for juveniles of the species. This response of adults in freshwater may
be linked to the preferred temperatures in ocean environments that the fish inhabited for several
years prior to their entry into rivers.
Differences in response in thermal tests can usually be attributed in part to test conditions.
Numerous factors can be listed as reasons for differences in responses among studies for a given
species. Different test results appear to be more common in tests of temperature preference than
in UILT tests. Test apparatus has a role in determining results as well as season, sex, size, and so
on. Because preference involves behavioral traits and appears to be less precise an index to
estimate, UILT values are emphasized in this discussion.
Studies of UILT on salmonids, cyprinids, and centrarchids conducted by Cherry et al. (1977)
can be assumed to eliminate potential methodological variations. These researchers found that the
UUILTs for these fish families were 73.4-77, 78.8-96.8, and 95-96.8°F (23-25, 26-36, and
35-36°Q, respectively. The salmonids tested in this study included rainbow trout, brown trout,
and brook trout. Brett (1952) measured UUILT on several salmon species (O. tshawytscha, O.
kisutch, O. gorbuscha, O. keta, and O. nerka). Brett's work is the most complete analysis of
thermal effects on fish physiology available in the literature. It provides a useful comparison of
these five species and can also be said to eliminate variation attributed to methodology. He found
that among species of Pacific salmon the UUILT values varied only from 74.8 to 77.2°F (23.8-
25.1°C). Similarly, when CTM method was used to test thermal tolerance of five species of trout
(rainbow, brown, brook, Gila, and Arizona trout), CTM values of 84.9, 85.8, 85.6, 85.3, and
84.9°F (29.4, 29.9, 29.8, 29.6, and29.4°C,) respectively, were determined (Lee and Rinne 1980).
All species ware collected in the southwestern United States. The rainbow, brown, and brook
trout were introduced and the Gila and Arizona trout were native to this climatic regjoa Despite
these differences in geographic origin, species, and cultural history (hatchery/wild), CTM values
differed by a maximum of 0.9°F (0.5°C) among species. (Note that CTM and UILT test
methodologies are fundamentally different and yield different kinds of information on thermal
tolerance.)
A recent study (Myrick and Cech 2000) of thermal physiology in two rainbow trout strains
(Eagle Lake and Mt. Shasta) from California lakes revealed no strain-related differences in
thermal tolerance, and moreover found that CTM values for these rainbow trout strains were very
similar to values found for many other salmonids, including brook trout, brown trout, Atlantic
salmon, Gila trout, another rainbow trout stock, and Little Kern River golden trout.
What is the variation in thermal response within a species?
One of the most extensive and earliest evaluations of geographic variation in UILT available
is by Hart (1952). Comparisons were made of stocks from 10 species ranging in distribution from
Ontario to Tennessee to Florida. Stock differences in UILT were found in only three of these
species, but in these cases the stocks were taxonomically distinct subspecies that also were
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
25
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differentiated morphologically. In two species, each having recognized subspecies, there were no
differences inUILT or lower incipient lethal temperature (LILT) values. Another two species
having subspecies were not different in UILT but might have differed in LILT. In two species
having no recognized subspecies, the stocks sampled over this large geographic range had no
geographic differences in UILT. Hart concluded that the southern stocks of a species had no
greater resistance to high temperature than the northern stocks, the exception being if they were
taxonomically and morphologically distinct. Even then there were not always differences.
Among the species studied, each tended to occupy similar thermal regimes across the extent of its
range.
Similar results were found by McCauley (1958) in thermal tolerance tests of Salvelinus spp.
McCauley found that two stocks of Salvelinus fontinalis failed to reveal any difference in
response. However, McCauley reported a difference in response between two subspecies of S.
alpinus, (S. a. willughbii and S. a. alpinus). However, the geometric mean resistance at 1,000
min exposure occurred at approximately 76.5°F (24.7°C) with S. a. willughbii and at 75.9°F
(24.4°C) with S. a. alpinus. Even though McCauley reported a highly significant difference
between the subspecies, the actual difference in thermal tolerance was negligible in a management
context.
In CTM tests of two stocks of Lahontan cutthroat trout, Vigg and Koch (1980) found that
variation owing to strain differences was approximately 0.18-0.9°F (0.1-0.5°C), but that
differences owing to water source (i.e., alkalinity) were 36.8-7.2°F (2.7-2.9°C). Konecki et al.
(1993) found that when acclimatization effects were eliminated for Washington coho stocks
collected from streams with greatly different thermal environments, there was no significant
difference in CTM values. Sonski's (1984) test of three stocks of rainbow trout, including
redband trout, revealed no more than 1,4°F (0.8°C) difference in UILT values. In thermal testing
of two subspecies of largemouth bass (Florida and northern) acclimated to 89.6°F (32°Q, CTM
values were 41.8°C ± 0.4 SD and 40.9°C ± 0.4 SD, respectively (Fields et al. 1987). But the
authors questioned whether these differences were biologically meaningful; they considered the
chronic thermal maximum to be more meaningful. These values were 39.2°C ± 0.64 and 37.3°C ±
0.60, respectively. These differences were expressed only at the highest (i.e., 89.6°F [32°C])
acclimation temperature and may indicate a selective advantage of the Florida subspecies over the
northern under conditions of high thermal stress. Again, these differences are only expressed at a
subspecies level and are not great in magnitude.
Beacham and Withler (1991) studied the survival of ocean-type and stream-type juvenile
chinook in high water temperatures. Twenty separate full-sib families of the ocean-type
(hatchery) and 32 full-sib families of the stream-type chinook (wild) were produced from gamete
collections and matings of 1 male with each of 2 females. The stream-type population, rearing at
70.7°F (21.5°C), had a total mortality of 79% after 16 d. The ocean-type population, rearing at
71,6°F (22°C), had a total mortality of 74% after 18 d. These populations responded very
similarly to high temperature (approximately 71.6°F [22°C]) in about 18 d of exposure, but the
cumulative mortality curves were very different. The stream-type population had approximately
70%) mortality after 8 d, whereas the ocean-type population suffered only 3%> mortality in the
same time period. These different patterns of mortality are likely a result of adaptive differences
in the populations (Beacham and Withler 1991). The authors speculated that ocean-type chinook
Summary of Technical Literature Examining the Physiological Effects of Temperature 26
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are better adapted to warmer water conditions because they spend a greater portion of their life
cycle in coastal waters.
A study of thermal influences on physiology of two rainbow trout strains (Eagle Lake and
Mt. Shasta) revealed no differences in thermal tolerance as measured by the CTM method
(Myrick and Cech 2000). The Eagle Lake rainbow trout (O. m. aquiliarum), originally native to
Pine Creek, California, has been artificially propagated since 1956 because of concerns for habitat
degradation. The Mt. Shasta strain is an inbred hatchery strain derived from a southeast Idaho
trout farm and Hot Creek strain rainbow. In addition, the authors found no differences in
conversion efficiency, oxygen consumption rates, or swimming performance.
Is there significant genetic flexibility within a stock that would allow for adaptation to
thermal regimes?
Beacham and Withler (1991) hypothesized that the ocean-type population, having a shorter
period of freshwater residence than the stream-type population, is better adapted to warmer
waters as found in the ocean and also in its freshwater habitats. Consequently, the ocean-type
population is better adapted to short-term exposure to high water temperature than is the
stream-type population. It is interesting that despite the differences in response to temperature
within the first few days, the two British Columbia populations had similar cumulative mortalities
over a 16- to 18-d period.
These authors speculated that theUILT for salmonidsmay vary by population, depending on
their history of adaptation to temperature regimes. Differences in thermal tolerance were noted in
time to death. At 70.7°F (21.5°C) the entire stream-type test population (i.e., all families of the
stream-type population) had a mean time to death of 3.4 (0.10) d. At 71.6°F (22°C) the
ocean-type population had a mean time to death of 13.3 (0.11) d. The standard error for the
stream-type population in time to death was approximately 3%; that among the ocean-type
population was approximately 0.8%. The ocean-type population had a greater short-term
tolerance of warm water temperatures than the stream-type population, but had a reduced
additive genetic variation in mean time to death. The estimated heritability of mortality rate and
time to death for the ocean-type chinook population was zero. These results indicate that the
ocean-type population had very little capacity for increased adaptation to warmer water
temperatures because it was fully adapted to the warmer summer conditions found in its coastal
stream. However, the stream-type population had additive genetic variation for survival at high
temperatures and time to death that could allow it to further adapt to high water temperatures.
Besides survival, what other key biotic responses influenced by temperature vary
among stocks?
Growth. Growth is a good indicator of performance of a species at various temperatures.
When fed to satiation, chinook achieved maximum growth rates at 66°F (19°C) (Brett et al.
1982). However, at this temperature, under satiation feeding, Big Qualicum chinook juveniles
(approximately 3 g) grew at a rate of 3.5%/d, whereas the Nechako stock had a significantly
lower growth rate of only 2.9%/d. Brett et al. (1982) considered this difference to be a
genetically controlled means for one stock to achieve greater growth, especially in the optimum
SummaryofTechnical Literature Examining the Physiological Effects of Temperature
27
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temperature range. In addition, examination of growth rates on Sacramento River chinook
revealed that at 68-69.8°F (20-21 °C), sublethal growth stress becomes significant for fish fed to
satiation (Marine 1997). These data indicate consistency in temperature thresholds, whereas
actual growth rates differ somewhat among stocks.
Wangila and Dick (1988) studied the growth response of two strains of rainbow trout (O.
mykiss) and their hybrid at 45 and 59°F (7 and 15°C). The two strains, Mt. Lassen and
Tagwerker, were symbolized as LAS and TAG. There were four families of LAS, three of TAG,
and four crosses of LAS x TAG. Each family was produced by matings of a single pair of
parents. Progeny of each family were divided into four groups of 75 individuals each, two of
which were tested at 45°F (7°C) and the other two at 59°F (15°C). Trout were fed three times
per day to satiation, so growth rates should be considered maximum at each temperature.
Wangila and Dick found significant differences among strains and hybrid in specific growth rates
as a function of body weight during growth between July 8 (mean starting weight 3.3-4.5 g) and
October 15 (ending weights 10.5-13.9g). Growth was modeled with the equation logcG = a + b
log eW.
Slopes for the regression of specific growth rate on mean weight were significantly different
among the two strains and hybrid at 45°F (7°C), but not at 59°F (15°C). The high degree of
heterogeneity of slopes at 45°F (7°C) suggests that genetic differences were significant among
stocks when growth took place at temperatures far below the growth optimum However, at
temperatures near the growth optimum, heterogeneity in slopes for this regression was very low.
This study leaves unanswered how the stocks would respond under a temperature above the
growth optimum. It could be that under stress, one stock would be able to convert more of its
food intake to growth, or its ability to feed at high temperatures might be greater than for the
competing stock.
Sadler et al. (1986) tested differences in specific growth rate (a measure that assumes
exponential growth) for two rainbow trout strains at constant temperatures of 50°F (10°C) and
61°F (16°C). Significant differences in strain N and S occurred at 10°C (1.80 ± 0.04 vs. 2.03 ±
0.02) (±SE) and at 16°C (2.29 ± 0.11 vs. 3.00 ± 0.09), respectively. Both stocks achieved higher
growth rates at the higher temperatures, which would be nearer the preferred temperature of
rainbow. The authors attributed the greater growth rate of the S stock (Soap Lake, US,
domesticated stock) to its hatchery selection for high growth rate compared with the N strain
derived from wild stock from a river in Ontario.
A study of two strains of rainbow trout from California lakes (Eagle Lake subspecies and
Mt. Shasta strain) revealed no differences in food consumption, gross conversion efficiency,
resting routine oxygen consumption rate, upper CTM, or critical swimming velocity. However,
over a temperature range including 50, 57.2, 66.2, 71.6, and 77°F (10, 14, 19, 22, and 25°C)
constant temperature growth experiments, theMt. Shasta strain had a significantly greater growth
rate than the Eagle Lake strain only at 71.6 and 77°F (22 and 25°C). At 71.6 and 77°F (22 and
25°C), growth rates for these two strains were 2.97% vs. 3.51 % body weight/d and -0.35% and
0.05% body weight/d, respectively. When compared with other rainbow stocks from widely
separated geographic locales at 71.6°F (22°C), the growth rates were similar to those from
Rainbow Springs Hatchery, Ontario, reported by Alsop and Wood (1997), lower than those for
SummaryofTechnical Literature Examining the Physiological Effects of Temperature
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Lake Superior rainbow trout (3.94% body weight/d) (Hokanson et al. 1997), and greater than
reported for Oregon juvenile steelhead (1.7% body weight/d, at 72.5°F [22.5°C]) (Wurtsbaugh
and Davis 1977b, as reported by Myrick and Cech2000). However, Myrick and Cech (2000)
attributed much of the difference among stocks to differences in juvenile weight. Weight of test
specimens in the studies above by Myrick and Cech (2000), Hokanson et al. (1997), Wurtsbaugh
and Davis (1997b), and Alsop and Wood (1997) were 2.3-4.2 g, 0.2-0.3 g, 1-1.2 g, and 6-7 g,
respectively. On the basis of studies of growth at constant temperatures within the overall range
50-77°F (10-25°C), Myrick and Cech (2000) inferred an optimal growth rate between 57.2 and
66.2°F (14 and 19°C), bracketing the optima found by both Hokanson et aL (1977) and Briggs
and Post (1997, cited by Myrick and Cech 2000).
Swimming speed. Myrick and Cech (2000) measured the critical swimming velocities of
two rainbow trout strains assumed to be genetically different (juvenile Eagle Lake and Mt. Shasta
trout from California lakes) over a temperature range from 50 to 66.2°F (10-19°C). They
reported that length-specific critical swimming velocities were not statistically different. By
plotting critical swimming speeds (Figure 1) from the literature summarized by Myrick and Cech
(2000), it appears that the various trout stocks (rainbow/steelhead and golden trout) had
swimming optima of 57.2-59°F (14-15°C). Only the Little Kern River golden trout exhibited a
sharp decline in critical velocity at temperatures above 57.2°F (14°C). No studies were
conducted at temperatures greater than 68°F (20°C), but one would assume that at some
temperature between 68 and 77°F (20 and 25°C) a more dramatic decline in swimming speed
would take place. The literature summarized in Figure 1 indicates that critical swimming velocity
(BL/s or body length per second) generally declines with total body length in juveniles over the
range 85-287 mm, although this conclusion is formed by lumping all trout stocks. Body length
then appears to be more significant as a source of variation in critical swimming speed than is
genetic differences. However, at 50°F (10°C), Myrick and Cech (2000) noted a significantly
greater critical swimming velocity in strains of coastal cutthroat trout (Aberdeen strain) and
steelhead (Aberdeen strain) than for Eagle Lake rainbow, Mt. Shasta rainbow, Little Kern River
golden trout, and coastal cutthroat trout (Shelton strain), which were more similar. Stocks tested
at 50°F (10°C) varied in length from 89 to 120 mm. Differences in swimming speed were not
obviously related to body length.
SummaryofTechnical Literature Examining the Phjsiological Effects of Temperature
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-~ 102-113 mm
109-120 mm
136-164 mm
85-96 mm
287 mm
10 15
Water temperature (C)
20
25
—~— Eagle Lake rainbow trout
—m— Little Kern River golden trout
- - Mt. Shasta rainbow trout
»x— rainbow trout
—«— steelhead (Nimbus strain)
SUPPORTING DISCUSSION AND LITERATURE-SUBLETHAL EFFECTS
Incubation and Early Fry Development
Which temperatures provide optimum conditions for incubation and early fry
development in the following species?
Chinook salmon. Once spawning has taken place, the eggs of chinook salmon hatch in
about 2 months and the young remain in the gravel for 2-3 wk before emerging. Many
researchers have tested incubation survival at constant exposure to various test temperatures.
Complete mortality (100%) has been noted at incubation temperatures from 57 to 66.9°F (13.9-
19.4°C) (Donaldson 1955, Garling and Masterson 1985, Seymour 1956, Eddy 1972, as cited in
Raleigh et al. 1986). Significant mortality (over 50%) has been noted at constant incubation
temperatures from 49.8 to 62°F (9.9-16.7°C) (Donaldson 1955, Seymour 1956, Burrows 1963,
Bailey and Evans 1971, as cited in Alderdice and Velsen 1978; Hinze 1959, as cited in Healy
1979). A constant incubation temperature of 46.4°F (8°C) produced more robust alevin and fry
Figure 1. Critical swimming velocity as a function of water temperature. Data source was tabulated in Myrick and
Ccch (2000).
Summary of Technical Literature Examining the Physiological Effects of Temperature 30
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survival than constant exposure to either 39.2 or 53.6°F (4 or 12°C) in a study by Murray and
Beacham (1986), and Velsen (1987) compiled data showing that the best survival (>92.9%)
occurred between 44.9 and 49.2°F (7.2 and 9.6°C). Heming (1982), however, found good
survival at both 50 and 53.6°F (10 and 12°C). Heming tested survival in both incubation trays
and artificial redds. Survival rates declined as the temperatures increased from 42.8 to 46.4, 50,
and 53.6°F (6-8, 10, and 12°C). The greatest survival (91.7%-98%) occurred at 42.8 and 46.4°F
(6 and 8°C), but it was still very good (90.2%-95.9%) at 50°F (10°C). Incubation at 53.6°F
(12°C) consistently had the lowest survival (84.6%-89.3%). Heming also tested survival rates
from incubation to hatching against survival rates from hatching through complete yolk
absorption. His work suggests higher incubation temperatures may create a metabolic energy
deficit for pre-emergent salmon that increases mortality. Once alevin have hatched and absorbed
their yolk sacs they will need to make a transition to active feeding. Heming and Mclnery (1982)
found that temperatures of 42.8, 46.4, and 50°F (6, 8, and 10°C) resulted in an average survival
of 98.4% during this transitional period, while 53.6°F (12°C) was associated with a decrease in
survival to 89.2%. The maximum conversion of yolk to tissue weight was reported by Heming
(1982) (as cited by Beacham and Murray 1986) to occur at 42.8°F (6°C) or below. Seymour
(1956) noted a ninefold increase in abnormalities in fry incubated at 60°F (15.6°C) and higher
when compared with those incubated between 39.9 and 55°F (4.4-12.8°C). Seymour also noted
that fry incubated at 39.9°F (4.4°C) emerged at a larger size than those reared at higher
temperatures; however, subsequent fry growth was maximized at 55°F (12.8°C).
Considered together, the work of the authors cited above most strongly suggests that
constant temperatures above 48.2-50°F (9-10°C) and below 41°F (5°C) may reduce the survival
of chinook salmon embryos and alevins. Although constant temperatures of 51.8-53.6°F
(11-12°C) can still result in good success, the results are consistently less than what is produced
at lower temperatures. As discussed previously in this paper, constant laboratory test
temperatures of 48.2-50°F (9-10°C) should be considered roughly equivalent to naturally
fluctuating stream temperatures with daily maximums of51.8-53.6°F (11-12^).
Some researchers have tried to mimic the naturally fluctuating and falling temperatures
actually experienced by incubating eggs, or have stepwise reduced the incubation temperatures as
incubation progressed. Initial incubation temperatures from 60 to 62°F (15.6-16.7°C) have been
associated with significant to total losses of young fish through the incubation to early fry
development phase (Healy 1979, Johnson and Brice 1953, California Department of Water
Resources [CDWR] 1988, and Jewett 1970 as cited in CDWR 1988). Rice (1960) found that
source waters declining from 60 to 46.9°F (15.6-8.3^) resulted in satisfactory egg development,
although he did not provide survival rates or clearly consider survival through to the fry stage.
Johnson and Brice (1953) found survival often exceeded 90% where initial water temperatures (as
a daily mean) were below 53.9T (12.2°C). Healy (1979) found that highest survival (97%)
occurred in creek water where the daily maximum reached 55°F (12.8°C) only a few times during
the first 2 wk of development, but also noted that survival was still very good (90%-94%) where
the initial temperatures were between 55 and 57.5°F (12.8 and 14.2°C). Olson and Nakatani
(1969) found 53.7%-88% survival in egg tots started at 54.5°F (12.5°C), experiencing a brief
increase to 58.4°F (14.7°C) in the first wk, and then quickly dropping back to 53.6-54.5°F (12-
12.5°C) and assuming a seasonal downward trend in temperature (test water paralleled both diel
and seasonal fluctuations). Olson and Foster (1955) found the greatest survival at an initial test
SummaryofTcchnical Literature Examining the Ph>siological Effects of Temperature
31
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temperature of 52.8°F (11.6°C) (92.2%), but reported no appreciable differences in survival rates
at initial test temperatures of 56.8, 59, and 60.8°F (13.8, 15, and 16°C) (89.9%-83.9%) (test
water paralleled seasonal daily average temperatures). Seymour (1956) tested four geographically
distinct stocks of chinook. Taking into consideration both mortality and growth rate, the
optimum temperature was estimated as 52°F (11.1 °C) for eggs and fry. The mortality rate was
considered low at all stages of development for lots reared between 39.9 and 55°F (4.4-12.8°C).
Lots with initial temperatures of 64.9°F (18.3°C) had the highest mortality (11%, 24%, 40%, and
100%>). In the cyclic and fluctuating temperature tests reviewed here, temperatures at the
beginning ofincubation that arebebw 51.8-55°F (11-12.8°C) are typically associated with
optimal survival rates. This compares well with the adjusted optimal range of 52.7-54.5°F
(11.5-12.5°C) suggested above based on examining the constant temperature exposure studies.
This range also compares well with the optimal temperature range of 46.4-53.6°F (8-12°C)
recommended by the Independent Scientific Group (1996) study.
Donaldson (1955) transferred eggs to more optimal 50-55°F (10-12.8°C) incubation
temperatures after various periods of exposure to higher temperatures. He found that tolerance
to temperature exposure varies with the stage of development. He also found 20% mortality
could be induced by exposing eggs to 66.9°F (19.4°C) for 1 d, 64.9°F (18.3°C) for 3 d, and
62.9°F (17.2°C) for less than 10 d. Donaldson's work lends further support to the observations
made by other authors such as Jewett (1970, as cited inCDWR 1988) that the latent effects of
holding eggs at higher than optimal temperatures continues through the period of absorption of
the yolk sac; thus, using mortality estimates at the time of hatching underestimates the total
temperature-induced mortality. Donaldson found the developmental stages associated with the
greatest percentages of temperature induced mortality were: (1) the time up until the closure of
the blastopore (200 T.U.); (2) the period just previous to and during hatching; and (3) when fry
are adapting themselves to feeding. He also found that when eggs were exposed to test
temperatures 62.9, 64.9, and 66.9°F (17.2, 18.3, and 19.4°C) past the eye pigmentation stage
(350 T.U.), the time necessary for complete hatching doubled, and the frequency of common
abnormalities increased with both the higher temperatures and longer exposures. Murray and
Beacham (1986) found that initial incubation at 39.2°F (4°C) reduced survival even with later
transfer (at completion of epiboly) to warmer waters 46.4 and 53.6°F (8 and 12°C). Transfers
after epiboly or completionof e>e pigmentation from 39.2 to 53.6°F (4-12°C) and from 53.6 to
39.2°F (12-4°C) also caused an increase in alevin mortality. The authors also found that
decreasing temperature produced longer and heavier alevins and fry. Combs (1965) found that
eggs developed to the 128-cell stage at 42.4°F (5.8°C) could then tolerate 35°F (1.7°C) for the
remainder of the incubation period with only moderate losses. Mortality of 14.5%> was observed
with a transfer time of 72 h, whereas only 3.3%> mortality occurred with a transfer at 144 h.
These three works together suggest that the effects of suboptimal initial incubation temperatures
may not be nullified by later changes in the temperature regime to more optimal levels; that
sudden changes in temperature at either early or later stages of development, regardless of the
direction of that change, can be harmful to pre-emergent life stages; and that initial incubation at
optimal temperatures may condition eggs and embryos such that they can withstand very bw
winter temperature regimes.
In addition to Donaldson (1955), Neitzel and Becker (1985) conducted work on the effects
of short-term increases in temperature that can be used to support daily maximum temperature
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
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criteria. Neitzel and Becker used chinook salmon to determine the effects of short-term
dewatering of redds by hydropower facilities. Neitzel and Becker found that sudden increases in
temperatures from 50°F to above 71.6°F (10-22°C ) for 1-8 h significantly reduced survival of
cleavage eggs in chinook salmon. Controls held at 50°F (10°C) had very low mortalities (less
than 2%). Mortality in treatment groups was 8%-10% at 71,6°F (22°C) after 2-h exposure, and
was 22% after a 1-h exposure at 74.3 °F (23.5°C). They further found that decreasing the
temperature from 50°F (10°C) to near freezing 32°F (0°C) for up to 24-h did not increase
mortality in eggs, embryos, or alevin. Considering the work of Neitzel and Becker, it would
appear that chinook salmon eggs and embryos are relatively tolerant of short-term increases in
temperature up to 71.6°F (22°C). However, because Donaldson (1955) found that 66.9°F
(19.4°C) produced 20% mortality in 1 d and 64.9°F (18.3°C) produced 20% in 3 d, setting a
more restrictive single daily maximum temperature limit is certainly warranted. Furthermore, as
described above, incubation conditions where daily maximum temperatures were in the range of
57.9-60.8°F (14.4-15.6°C) produced reduced survival rates, so further caution maybe warranted
in allowing daily maximum temperatures to exceed 56.3-58.1°F (13.5-14.5°C) during incubation.
Although there is some disagreement, the literature is consistent overall regarding optimal
incubation requirements for chinook salmon. Providing for optimal protection from fertilization
through initial fry development requires that constant or acclimation temperatures be maintained
below 48.2-50°F (9-10°C) and that individual daily maximum temperatures generally not exceed
56.3-58.1°F(13.5-14.5°C).
Coho salmon. Embryo survival is consistently maximized in tests at constant temperature
exposures between 36.5 and 43.7°F (2.5-6.5°Q and is only slightly less successful between 34.4
and 51.6°F (1.3-10.9°C) (Dong 1981, Tang et aL 1987, Murray et al 1988, Velsen 1987).
Davidson and Hutchinson (1938, as cited in Sandercock 1991) suggested that optimum
temperature for egg incubation is 39.2-51.8°F (4-11°C). Mortalities tend to become moderate
(74%-79%) at 51.8-54.5°F (11-12.5°C), and at 54.5-56.3°F (12.5-13.5°C), mortalities of 50%
can be expected. Above 57.2-57.9°F (14-14.4qC), tests commonly report 100% mortality or
close to it. Alevin survival may be excellent (97%) at 34.3-51.6°F (1.3-10.9°C) (Dong 1981,
Tang et al. 1987), and the most robust fry are at incubation temperatures of 39.2-46.4°F (4-8°C)
(Dong 1981, Murray et al. 1988). Alevin mortalities of 51 %-59% occur at 54.5°F (12.5°C)
(Dong 1981), and 100% mortality occurs at 57.2-57.9°F (14-14.4°C) (Dong 1981, Murray et al.
1988).
From the studies discussed above, we are relatively confident that egg survival is consistently
best at exposure to constant temperatures of 36.5-43.7°F (2.5-6.5°C), but may still be excellent
for manystocks at temperatures of 34.4-51.5°F (1.3-10.9°C). Alevin and fry survival and health
may be best at exposure to constant temperatures of 39.2-46.4°F (4-8°C), but survival may
remain excellent up to 51.6°F (10.9°C). This review of the available literature suggests that a
constant 44.6-50°F (7- 10°C) may form the upper threshold for optimal development of coho
salmon eggs and alevin. Adjusting this laboratory-based naturally fluctuating stream environment
(as discussed previously) results in the recommendation that to fully support the pre-emergent
stages of coho development, the 7-d average of daily maximum temperatures should not exceed
48.2-53.6°F (9-12°C).
SummaryofTechnical Literature Examining the Phjsiological Effects of Temperature 33
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No information is available that suggests coho salmon embryos and alevins are more
sensitive to short-term (daily peak) increases in temperature than any other Pacific salmon. The
one study reviewed that looks at short-term temperature changes for coho was by Tang et al.
(1987). In that study, incubation temperatures were increased from 50.3 to 62.6°F (10.2-17°C)
and lowered from 50.3 to 39.2°F (10.2-4°C) for 8 h. In neither test did these modest changes
result in any statistically significant increase in mortality. Additionally, one field study reported
coho alevins capable of at least partial survival (substantial change in later numbers of juveniles)
when daily peak temperatures rose from 14 to 20°C during the month of May while some were
still in the gravels. The control stream had no change in later abundance of juveniles and had
temperatures of 51,8-54.5°F (11-12.5°C) (visually interpolated from graph) during May. In the
impacted stream, summer maximum temperatures in two successive years were 75.2 and 86°F (24
and 30°C), and in the unimpacted stream, summer temperatures remained below 59°F (15°C)
(Hall and Lantz 1969). In the review ofthe literature, no clear basis was found for setting a daily
peak temperature specific to coho incubation.
Chum salmon. Incubation survival from fertilization to emergence is variable, but can be
excellent anywhere from 39.2 to 53.5°F (4- 12°C) (Murray and Beacham 1986, Beacham and
Murray 1985). In the initial period of embryo development, temperatures of 46.4-53.6°F
(8-12°C) produce the highest survival. However, in later stages of incubation, temperatures of
41-46.4°F (5-8°C) produce the best survival as well as the largest and heaviest alevinand fry
(Beacham and Murray 1986). Temperatures of 53.6°F (12°C) in the later developmental stages
can result in heavy losses in some stocks (Beacham and Murray 1985, Beacham and Murray
1986). The optimal temperature range for conversion of yolk to tissue weight was estimated to
be 42.8-50°F (6-10°C) (Beacham and Murray 1986), and optimal respiration efficiency has been
estimated to range from 51.8 to 54.5 °F (1 1-12.5°C) for pro larvae and larvae (Zinichev and Zotin
1988). Constant incubation at temperatures of 57.7 and 60.8°F (14 and 16°C) as well as at
36.5°F (2.5°C) have been associated with embryonic mortalities of 50% (Beacham and Murray
1990). The alevin stages of development (late), however, were shown to have very high survival
rates when exposed to temperatures as low as 35.6°F (2°C).
Based on the literature reviewed, constant incubation temperatures from 39.2 to 53.6°F (4-
12°C) commonly produce excellent incubation results; however, some researchers have noted less
than optimal survival occurring at the edges of this range. It appears that constant initial
incubation temperatures of 46.4-50°F (8-10°C) would be most consistently optimal for chum
salmon. In reviewing the literature, no specific basis was found for setting a daily peak
temperature for incubating chum.
Pink salmon. The range for successful incubation has been suggested to be from 39.9 to
55.9°F (4.4 to 13.3°C) (Beschta et al. 1987, Bonar et al. 1989). Murray and Beacham (1986)
reported excellent survival (91 %-97%) with initial fertilization occurring at 57.2°F (14°Q and a
0.9°F (0.5°C) drop in temperature every 3 d down to 41°F (5°C). When they allowed
temperatures to drop further to 39.2 and 35.6°F (4 and 2°C), survival was reduced. Murray and
McPhail found survival of 94% from fertilization to emergence at 41 °F (5°C), and Beacham and
Murray (1986) found the greatest survival for 5 stocks and 21 families of pink salmon tested at
46.4°F (8°C). Velsen (1987) compiled data showing that the best, although highly variable,
survival (generally >89.5%) occurred between 46.4 and 55.4°F (8 and 13°C). Survival decreased
SummaryofTechnical Literature Examining the Ph>siological Effects of Temperature
34
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at an incubation temperature of 51.8°F (11°C) in a test by Murray and McPhail (1988), and was
50% at 59-60°F (15- 15.5°C) (Beacham and Murray 1990). Temperatures of 41-46.4°F (5-8°C)
produced the largest alevins in a study by Murray and McPhail (1988), and 46.4°F (8°C)
produced the longest (Beacham and Murray 1986) and heaviest (Murray and McPhail 1988) fty.
Survival ofthe alevinlife stage was found to be generally excellent (>97%) for 21 families of
pink salmon tested at temperatures ranging from 39.2 to 35.6°F (4-2°C) (Beacham and Murray
1986). Survival to emergence was reportedly low, at 57.2°F (14°Q (Murray and McPhail 1988).
Examining bw incubation temperatures, Beacham and Murray (1986) found that
temperatures of 39.2°F (4°C) consistently resulted in the lowest survival for 5 stocks and 21
families of pink salmon, and in a 1990 study found 50% mortality at 41 °F (5°C). Murray and
McPhail (1988), Beacham and Murray (1990), and Bailey and Evans (1971) found 100%
mortality at incubation temperatures of 35.6°F (2°C). Murray and Beacham (1986) transferred
embryos in a late stage of development from 46.4°F to 33.8°F (1 -8°C) and found that while
northern stocks had 100% survival, southern stocks had mortalities ranging from 38% to 60%.
Based on the research cited above, constant temperatures of 40.1-53.6°F (4.5-12°C) and a
constantly declining temperature regime beginning at 57.2°F (14°C) can produce excellent and
perhaps optimal survival rates of incubating pink salmon. However, a constant temperature of
46.4°F (8°C) appears to produce the most consistently optimal results; and although tests up to
53.6-55.9°F (12-13.3°C) were found to produce optimal results, several tests found temperatures
of 51.8-53.6°F (11-12°C) (as well as ones conducted at 40.1-41°F [4.5-5°C]) to produce less
survival and smaller fiy. Furthermore, in natural streams the temperatures do not decline at a
steady rate, and tenperatures of59-60.8°F(15-16°Q have resulted in high mortality. In
consideration of all of these issues, we should assume that constant or acclimation temperatures in
the range of 46.4-50°F (8-10°C) represent optimal conditions for embryonic development. No
specific information was reviewed that examined the effect of short-term and infrequent peaks of
temperature on developing pink salmon.
Sockeye salmon. Murray and McPhail (198 8) and Combs (1965) reported that sockeye
salmon are more tolerant of low incubation temperatures and less tolerant of high incubation
temperatures than the other Pacific salmon. At constant exposure, Combs (1965) reported that
temperatures of 39.9-54.8°F (4.4-12.7°C) produced similarly high survival rates (85.8%-90.9%),
with the highest occurring at 42.4°F (5.8°C). Combs found that incremental increases in mortality
of 53%-67% occurred when the temperature was lowered from 42.4 to 39.9°F (5.8 to 4.4°Q or
raised from 54.8 to 57.5°F (12.7-14.2°C). Velsen (1987) found that while survival rates were
highly inconsistent between 34 and 59°F (1.1-15°C), the best survival generally occurred between
35.8 and 42.4°F (3.1 and 5.8) (generally >90%), with fair survival (>70%) occurring in the range
35.8-54.9°F (2.1-12.7^), and survival rates consistently poor (17%-76%) above 57.2°F (14°Q.
Murray and McPhail (1988) found that survival was highest at 46.4°F (8°C) (79%) but only 40%
at both 51.8 and 41°F (11 and 5°Q. Andrew and Geen (1960) reported that in the first 2 years of
a 4-year field study, the Salmon Commission found that eggs initially incubated at temperatures of
45°F (7.2°C) had lower survival than those initially incubated at 50, 55, and 60°F (10, 12.8, and
15.6°C). In a followup ejqperiment the following 2 years, they found that eggs exposed to
temperatures of 60-62°F (15.6-16.7°C) for short periods suffered severe losses during the
Summary of Technical literature Examining the Physiological Effects of Temperature 35
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exposure, and that temperatures of 62-64,9°F (16.7-18.3°C) caused extensive losses both during
and following exposure. In a study by Craig et al. (1996), the temperature range of 46.4-50°F
(8-10°C) resulted in the optimum 1:1 male-to-female sex ratio in offspring, although the study
design really only allows the conclusion that temperature in the early stage of development affects
sex determination.
The data on sockeye incubation survival are highly variable. Overall, however, it can be said
that constant or acclimation temperatures in the range of 39.2-54.5°F (4-12.5°C) produce variable
but often excellent survival rates in sockeye salmon, but that the range 46.4-50°F (8-10°C)
appears most consistently optimum. No specific studies were found to suggest a basis for a single
daily maximum temperature limit during the incubation period for sockeye salmon.
Steelhead. In establishing a State standard to protect spawning, we should consider
temperature recommendations established to protect embryo development. Fuss (1998)
considered the range 42-52°F (5.6-11,1°C) to be optimal for steelhead egg survival in the
Washington State hatchery program, and Bell (1986) suggested that 50°F (10°C) is the preferred
hatching temperature for steelhead eggs. Rombough (1988) found less than 4% embryonic
mortality at 42.8, 48.2, and 53.6°F (6, 9, and 12°C), but noted an increase to 15% mortality at
59°F (15°C). Alevin mortality was less than 5% at all temperatures tested, but alevins hatching at
59°F (15°C) were considerably smaller and appeared less well developed than those incubated at
the lower test temperatures. Redding and Schreck (1979) similarly found that emergent fry were
larger at 53.6°F(12°C) than at 60.8T (16°Q. Based on the works reviewed above, it appears
that an optimal constant incubation temperature occurs below 51.8-53.6°F (11-12°C). No
specific research results were found that could be used to suggest a single daily maximum
temperature limit for waters containing incubating steelhead.
Nonanadromous rainbow trout. Kamler and Kato (1983) tested incubation survival at
48.2, 50, 53.6, 57.2, and 60.8°F (9, 10, 12, 14, and 16°C). They found the highest survivalof
eggs at 50 and 53.6°F (10 and 12°C), slightly lower survival at 57.2F (14°C), and abrupt drops in
survival at both 48.2°F (9°C) and 60.8°F (16°Q. Velsen(1987) compiled data on the incubation
survival of both rainbow trout and steelhead trout that showed survival was consistently high
(>92%) between 39.2 and 48.2°F (4 and 9°C), and fair (>78%) between 37.4 and 59°F (3 and
15°Q, but very poor (7%) above 60.8°F (16°Q. Survival to the swim-up stage in two strains of
rainbow trout had 94%-98% survival at 44.6°F (7°C), 72%-95% at 39.2°F (4°C), and < 12%-41 %
survival at 35.6°F (2°C) (Stonecypher and Hubert 1994). Kwain (1975) found that the lowest
mortalities occurred at 44.6 and 50°F (7 and 10°C), Billard and Breton (1977) found a drop in
fertility at temperatures higher than 50°F (10°C), and Kashiwagi et al. (1987, as cited in Taylor
and Barton 1992) found optimal hatching occurred at 50°F (10°C). Humpesh (1985) found that
optimal hatching (>90%) occurred between 44.6 and 51.8°F (7 and 11°C), and Alekseeva (1987,
as cited in Taylor and Barton 1992) suggested that optimal incubation occurs with temperatures
rising from 41.5°Fto 50.9°F (5.3-10.5^0). Rombough (1988, as cited in Taylor and Barton
1992) found that at temperatures less than 53.6°F (12°Q there was less than 4% mortality.
Constant temperatures above 53.6°F (12°C) have produced variable, but generally tower survival
during incubation temperatures, with often severe losses occurring at temperatures of 59-60.8°F
(15- 16°C) (Velsen 1987, Billard and Breton 1977, Kwain 1975, Kamler and Kato 1983, and
Rombough 1988, as cited in Taylor and Barton).
Summary of Technical Literature Examining the Phjsiological Effects of Temperature 36
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On the basis of the literature cited above, we can generally conclude that constant or
acclimation temperatures in the range of 44.6-50°F (7-10°C) are optimal for incubation and
embryonic development of rainbow trout. No specific studies were found that test the ability of
O. mykiss eggs or alevin to survive high single daily maximim temperatures.
Cutthroat trout. Eggs of sca-run cutthroat incubate 6-7 wk before they hatch, and the
alevin remain in the gravel for about another 2 wk before they emerge (Trotter 1989, Pauley et al.
1989). Fry may emerge from March through June, depending on the location and time of
spawning, but peak emergence occurs in mid-April (Trotter 1989, Wydoskiand Whitney 1979).
Pauley et al. (1989) cite studies demonstrating that the optimum temperature for incubation is 50-
60.8°F (10-11°C). Bell (1986) has suggested that the range for hatching of cutthroat trout eggs is
from 39.9 to 55°F (4.4-2.8°C). Smith et al. (1983) found that west-slope cutthroat trout eggs
held in creek water with a fluctuating temperature of 35.6-50°F (2-10°C) had significantly better
survival than eggs held at a constant 50°F (10°C).
Hubert and Gem (1995) found 68.6% survival in a control population held at 44.6°F (7°C)
when testing the effects of lowering incubation temperatures in the early stage of development.
Mortality rates were no different from controls when temperatures were lowered to 37.4°F (3°C)
at least 13-15 d after fertilization but were higher if the cooling took place sooner. Stonecypher
and Hubert (1994) found that survival to swim-up stage in Snake River cutthroat trout was 95%
at 44.6°F (7°C), approximately 87% at 39.2°F (4°Q, and less than 16% at 35.6°F (2°C).
It is somewhat problematic to set standards to protect the incubation of cutthroat trout that
can be reasonably applied statewide. Cutthroat are a spring spawning species that often spawns
high in the watershed and has a very broad period of spawning when examined statewide. Stocks
that exist in lower or warmer watersheds spawn as early as February when temperatures rise
above 42.8°F (6°C), whereas stocks that exist in high-elevation snow-melt streams may need to
wait until late June or July for waters to be sufficiently warm (42.8-51.8°F [6-ll°C]) for
successful spawning. If there were no risk o f egg loss from sudden late winter and spring
freshets, we could suggest that the spring spawning strategy is relatively unencumbered by
changes in the temperature regime. Although earlier spawning exposes cutthroat eggs to higher
rides of physical damage, the earlier hatch also places surviving resident fry in a good position to
maximize summer growth and thus increase their survival opportunities over the following winter.
It may well be that the superior growth of anadromous salmonids in the ocean phase makes
increases in weight gain from earlier emergence of less value, but this relationship remains to be
tested. In general, specific stocks will have adapted their spawning and emergence periods to
optimize both incubation survival and early fry growth. Significant changes in the temperature
regime, such as earlier spring warming, will bring unknown risks to individual populations.
Therefore, although an optimal temperature regime is recommended in this paper for cutthroat
trout, it would be best to tailor it to the historic spawning patterns found in specific stocks. To
initiate spawning in most stocks, the water temperatures must at least warm up to daily
maximums of 42.8-44,6°F (6-7°C), although some stocks may not begin spawning until
temperatures reach 51.8°F (11°C). Specific studies on incubation survival suggest that incubation
maybe optimized with constant or acclimation temperatures in the rarge of 44.6-50°F (7-10°C).
No specific basis was found in the literature for setting single daily maximum criteria for the
incubation of cutthroat trout.
Summary of Technical Literature Examining the Physiological Effects of Temperature 37
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What are the conclusions for incubation requirements?
Spawning signals the beginning of the life-cycle stage (egg deposition and initial egg
incubation) that is most sensitive to warm waters. Critical spawning temperatures for a variety of
salmonids are summarized in Table 5. Because the spawning period, egg fertilization, and initial
incubation are sensitive life stages dependent on thermal regimes, special consideration must be
given to ensure that criteria to protect incubation are applied at the proper time of year.
Table S. Upper optimal temperature regimes based on constant or acclimation temperatures necessary
to achieve full spawning protection of the nine key cold-water fish species indigenous to the Pacific
Northwest
Fish species
Critical spawn temperatures
Upper optimal temperature range
°F (°C)
Single daily maximum temperature
°F (°C)
Chinook
48.2-50 (9-10)
56.3-58.1 (13.5-14.5)
Pink
50-53.6 (10-12)
Chum
46.4-50 (8-10)
Char
35.6-42.8 (2-6)
42.8 (6)
Sock eye
46.4-50 (8-10)
Coho
44.6-50(7-10)
Cutthroat
44.6-50 (7-10)
Rain bow
44.6-50 (7-10)
Steelhead
51.8-53.6(11-12)
Growth
For growth, what are the demands for energy and how is the balance determined by
temperature?
In terms of energy budgets, fish production energy (P) equals the sum of growth (G),
reproduction (Rp), shed scales (Ex), and secretions (S), as shown in the following equation:
P = G + Rp + Ex + S.
Energy assimilated from food equals the difference between energy ingested and defecated,
or A = I - F.
Energy assimilated is distributed into production (P), respiration (R), and excretion (U), as
Summary of Technical Literature Examining the Physiological Effects of Temperature 38
-------
follows:
A = P + R + U.
The symbols used above follow terminology of Ricker (1968) and Odum (1968).
Energy is needed to maintain the basic metabolic rate and is fundamental to sustain life. In
addition, some energy must be diverted to activity (swimming) to perform the functions of food
capture, escape from predators, migration, and soon. If the active metabolism is not sufficiently
high, energy is not available for feeding activity and, subsequently, growth and reproduction.
When water temperatures rise toward lethal conditions, resting metabolism rate increases
dramatically and feeding rate declines to zero. When water temperatures are high, most of the
fish's assimilated energy maybe required simply to keep up with basic metabolic demand. When
active metabolism (energy expenditure for swimming) declines so the fish can divert available
energy to basic metabolic demands, feeding declines. And, even when food is available, feeding
no longer occurs if the temperature is above the feeding temperature limit. This may have an
adaptive benefit, because digesting food under high temperature conditions incurs a metabolic
demand (specific dynamic action). The more overall energy the fish expends in basic metabolism
and food digestion, given a declining food intake, the lower will be the assimilated energy that the
fish can utilize for growth, reproduction, or resistance to environmental extremes. This latter use
of energy is needed for resistance to disease and recuperation from cumulative stresses of
predator avoidance, migration, high temperature stress, and so on (Kelsch 1996).
Why is it important to be concerned with growth rate, production, and fish density?
Production is the elaboration of tissue by a population ova- a specified period of time,
regardless of the fete of the tissue (Warren 1971). Production energy is stored as body tissue
growth, gametes, or released as secretions (e.g., mucus). Production (e.g., growth) for any time
period in which growth rate is relatively constant can be calculated as the product of the growth
rate (e.g., mg/g/d) and mcanbiomass (e.g., g/m2). Production for longer time periods is
calculated as the summation of production for the short time intervals in which growth rate is
relatively constant. Production can also be computed graphically as the area under the curve
where number of individuals in the population at an instant in time is plotted against the mean
weight of those individuals (Warren 1971). Regardless what method is used to calculate
production, production is clearly a function of population size, survival, and growth rate, which in
turn may be influenced by water temperature, other water quality factors, food availability, level
ofpredation, and so on.
Temperature regime is an important influence on fish density. Control on density can occur
through a combination of survival effects, behavioral avoidance, and interspecific competition. Li
et al. (1993) reported a decline in steelhead biomass from 18 g/m2 at a maximum summer water
temperature of 60.8°F (16°Q in tributaries of the John Day River to 0 g/m2 at a maximum
temperature of 82.4°F (28°C). The sharp reduction in biomass with increasing temperature is an
indication of either progressive mortality or emigration from zones exceeding temperature
preferenda. Likewise, Ebersole et al. (in press) reported for tributaries of the Grande Ronde
River, Oregon, that rainbow trout density declined steadily between a mean daily maximum
SummaryofTechnical Literature Examining the Physiological Effects of Temperature 39
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temperature of 53.6°F (12°C) to zero at approximately 75.2°F (24°C). The literature on the
effect of water temperature in controlling fish density is extensive (McCullough 1999).
Because fish are mobile and migration to avoid high water temperatures is sometimes an
option, it is not easy to extrapolate temperature-fish density effects to a whole watershed to
estimate total population size or population production. Nonetheless, the numerous studies
showing a decline in fish density with increasing water temperature probably indicate lethal and
sublethal effects and preference for habitats in which growth is optimum as much as they indicate
simple avoidance behavior. Production is calculated as the product of growth rate and mean
biomass (see above). Energy stored as production is distributed primarily in somatic growth and
reproduction. The ability to divert energy to reproduction is feasible when there is sufficient
scope for activity and this depends on ambient temperatures and food availability. In addition,
population viability is related to population abundance.
What is the optimum range or optimum temperature for growth of various salmonids?
Chinook. Chinook production in an experimentally modeled stream at 53.6°F (12°C) was
65% higher than at 60.8°F (16°C) (Bisson and Davis 1976, as cited by CDWR 1988, p. 31). An
optimum growth temperature of 59°F (15°C) was recommended by Banks et al. (1971 as cited by
GarKng and Masterson 1985). Brett et aL (1982) recommended 58.6°F (14.8°C)as the growth
optimum for juvenile chinook feeding on a food ration of 60% of the maximum (assumed to be a
typical level in nature). Marine and Cech (1998) determined that growth rates of fall chinook
under sublethal rearing temperatures (69.8-75.2°F [21-24°C]) were substantially less than growth
rates at 55.4-60.8°F (13-16°C). Wilson et al. (1987) recommended 50.9°F (10.5°C) as the
midpoint of the growth optimum for Alaskan chinook, based on studies in southeastern and
southcentral Alaska. Preferred rearing temperatures for chinook were reported as high as 58.3°F
(14.6°C) (Reiser and Bjornn 1979). The preferred temperature range for fingerlings was 53.6-
55.4°F (12-13°Q (based on determination of mean of the distribution) when the fish were
acclimated to temperatures ranging from 50 to 75.2°F (10-24°C) (Brett 1952). If growth
temperatures are maintained between 50 and 60°F (10-15.6°Q, growth rate would be >80% of
the maximum level observed in feeding at 60% satiation (a level considered by Brett et al. [1982]
to correspond to naturally occurring food availability levels). Growth rate under 60% satiation
feeding at 58.6°F (14.8°C) is expected to be approximately 1.8%/d (Brett et al. 1982). Lower
levels of food availability would reduce the optimum growth temperature. Temperatures above
60°F (15.6 °C) significantly increase the risk of mortality from warm-water diseases. A synthesis
of this evidence leads to a recommended optimum production temperature zone of 50-60°F
(10.0-15.6°C).
The optimal growth zone of 50-60°F (10-15.6°C) falls within the range for positive growth
at 40.1°F (4.5°C) (lower limit) and 66.4aF (19.1°C) (upper limit) (see Armour 1990). The 39.4
and 66.4°F (4.1 and 19.1°C) limits tabulated in Armour (1990) are zero net growth limits for a
chinook population. Brett et al. (1982) reported a zero individual growth rate under 60%
satiation feeding at 70.5°F (21.4°C) (see Figure 2). If chinook were to have unlimited rations, the
optimum growth temperature would be approximately 66.2°F (19°C) (Brett et al. 1982).
Sockeye. Good growth of sockeye, with low mortality, occurred at 53-62°F (11.7-16.7°C)
SummaryofTechnical Literature Examining the Physiological Effects of Temperature
40
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(Donaldson and Foster 1941). The upper limit to growth was similar to that observed by Brett et
al. (1982) for chinook feeding at 60% of satiation. Sockeye (7-12 months old) feeding at
satiation had a growth rate optimum at approximately 59°F (15°C). Growth rates declined at
both higher and lower temperatures. Growth rates reached zero at approximately 75.2°F (24°C)
under satiation feeding. When feeding rate was towered to 1.5%/d, the optimum growth
temperature declined drastically to 41°F (5°C). At this feeding rate, growth rate (%/d) was zero
at approximately 59°F (15°C) (Brett et al. 1969). Feeding rates of Skaha Lake sock eye at 62°F
(16.7°C) were 2.3%-3.2%/d (fresh weight; based on a sample of the 2-wk periods having mean
temperatures of 62°F [16.7°C]). Feeding rates were approximately 2.2%/d at 50°F (10°C), but
the optimum growth occurred at this low temperature (Donaldson and Foster 1941). Optimum
DETERMINED
NECHAKO CURVE
3.5-
SUBLETHAL
GROWTH
STRESS
Rmax = R1.0
3.0-
2.5-
R0.
o
ID
2.0
R0 6
X
H
O 1-5"
Od
O
PATH of optimum
TEMPERATURE
1.0-
DEDUCED RIVER
RELATION
0.5
0.0
16 18 20
TEMPERATURE (C)
Figure 2. Optimum growth rates of spring chinook under various feeding regimes
and constant temperatures.
growth temperature was 59°F (15°C) at a ration of6%/d, but this declined to an optimum growth
temperature of 41°F (5°Q at a ration of 1.5%/d (Brett et al. 1969).
Summary of Technical Literature Examining the Physiological Effects of Temperature
41
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Stcclhead. Wurtsbaugh and Davis (1977) studied growth of steclhead trout in laboratory
streams under three fluctuating temperature regimes (natural cycle, natural +5.4°F [3°C], and
natural +10.8°F [6°C]) in all four seasons and found that trout growth could be enhanced by
temperature increases up to 61.7°F (16.5°C). During the summer season the control temperature
(natural cycle) was 61.2°F (16.2°C) (mean) and the elevated temperatures averaged 67.1°F
(19.5^C) and 72.5°F (22.5°C). The average diel temperature range for the summer growth period
was about 3 8.1 °F (3,4°C) under the three treatments. Growth rates under food consumption
rates of 5%-l5% dry body wt/d were higher under the control temperature regime than at the
elevated fluctuating regimes. Under the high temperature regime (mean of72.5°F [22.5°C])
growth rate was zero at a food consumption rate of 7%/d. Gross food conversion efficiency
decreased as temperatures increased from 61.2 to 72.5°F (16.2-22.5°C). Maintenance rations
increased by a iactor of three over the temperature range 44.4-72.5°F (6.9-22.5°C).
What more is specifically known about growth rearing requirements of rainbow trout?
Final preferred and optimal temperatures for rainbow trout have been reported at 53.6-
66.2°F (12-19°C) (Bell 1986, Taylor and Barton 1992), and scope of activity and growth for
juvenile fish are commonly reported to be optimal between 59 and 69.8°F (15-21°C) on a
satiation diet (Moyle 1976, McCaulcy and Pond 1971, Dickson and Kramer 1971, Kwain and
McCauley 1978, and Huggins 1978 as cited in Kwain and McCauley 1978). However, some
authors have suggested lower optimal temperature ranges. Piper et al. (1982) set the optimal at
50-62.1°F( 10-16.7°C), although Sadler et aL (1986) found that growth and food conversion
efficiency were greater at 60.8°F (16°C) compared with 50°F (10°C). McCauley and Huggins
(1975) found that large (150-250 g) rainbow trout had a preferred mean temperature of 62.1°F
(16.7°C), and that the fish actively traveled at temperatures between 56.8 and 64.4°F (13.8-1 8°C)
in a thermal gradient. Behnke (1992) suggested that the optimum temperature for growth and
food assimilation in salmonids occurs between 55.2 and 60.8°F (13-16°C). Ferguson (1958) cites
56.5°F (13.6°C) as the final preferred temperature for rainbow trout, and Mckee and Wolf(1963,
cited in Wedemeyer et al., no date) found 55.4°F (13°C) to be optimum Kwain and McCauley
(1978) suggest that fish over 1 year old may have a final preferred temperature of 55.4°F (13°C)
(citing the works of Garside and Tait 1958, Christie as reported in Fry 1971, and McCauley et al.
1977, as cited in Kwain and McCauley 1978) although as noted above, the work of McCauley
and Huggins (1975) suggests that older fish sometimes demonstrate more intermediate
temperature preferences.
Dockrayet al. (1996) found that in a fluctuating temperature environment, temperature
increases benefited growth up to daily maximum temperatures of 64.4°F (18°C), above which
long-term growth was inhibited. De Leeuw (1982) found that stream temperature increases that
raised the summertime maximum temperature from 53.6 to 61.7°F (12-16.5°C) were associated
with an increase in growth rates in three streams in British Columbia, Canada. Hokanson et al.
(1977) found that a constant exposure to 63°F (17.2°C) produced the greatest growth rates in
trout fed to satiation over a 40-d test period. Increased mortality was observed in temperatures
above this growth optimum. They also noted that in fluctuating temperature experiments, growth
was accelerated when the mean temperature was below the constant temperature optimum (63 °F
[17.2°C]), and growth was retarded by mean fluctuating temperatures above this optimum. The
highest growth rate in the fluctuating temperature environment occurred at a mean of 59.9°F
SummaryofTechnical Literature Examining the Physiological Effects of Temperature 42
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(15.5°C)(range of53-66.7°F [11.7-19.3 °C]). A statistically nonsignificant decrease occurred at a
mean of 63.1°F (17.3°C) (range of 56.3-70°F [ 13.5-21.1 °C]). The authors also concluded that
rainbow trout acclimate to some temperature between the mean and the maximum daily
temperatures. Sometimes, warmer waters may provide secondary benefits to rainbow trout.
Cunjak and Green (1986) found that rainbow trout were able to compete better with brook trout
at 66.2°F (19°C) than at either 46.4 or 55.4°F (8 or 13"C).
Bisson and Davis (1976, as cited in Li et al. 1994) found that streams with daily maximum
temperatures of 60.8-73.4T (16-23°C) had greater standing crops of trout than did streams with
warmer maximum temperatures (78.8-87.8°F [26-31°C]). Frissell et al. (1992) studied the
distribution of rainbow trout and found that although they could be found in water temperatures
over 73.4°F (23°C), there was a general threshold response for age 1+ fish above 71.6°F (22°C)
and for age 2+ fish above 69.8°F (2 1°C). Consistent with these results, Li et al. (1993, 1994, and
1991 as cited in Spence ct aL 1996) noted that even though rainbow trout might not show
avoidance reactions when stream temperatures were below 68°F (20°Q, they actively avoided
waters warmer than 73.4-77°F (23-25°C). Linton et al. (1997) noted that rainbow trout fed to
satiation continued to feed and grow at a mean temperature of 68.9°F (20.5CC), a 30% reduction
in food intake occurred at 71.6°F (22°C), and juvenile fish continued to feed near their thermal
maximum. Linton et al. (1997) found that increasing the temperature regime by 3.6°F (2°C) over
the natural (base) level for Lake Ontario trout resulted in increased spring and early summer
growth, which was lost later in the summer due to suppression of appetite and growth. Mortality
rates increased from 6% to 13.1% in the warmer test water during the late summer in the first
summer of testing when the mean monthly base temperature in August was 73.4T (23°Q.
Mortality was almost nonexistent through the following summer, which had a mean August base
temperature of 64.4°F (18°C) (the test waters should have had a mean of 68°F [20°C]). The
threshold temperature for cessation of feeding, and subsequently growth, differed from >68°F
(20°C) to <68°F (20°C) over the two summers, and thus also fish size and age. Behnkc (1992)
cited work showing that trout reduce and finally cease feeding as temperatures rise to between
71.6 and77°F (22-25°C), often well below the lethal temperature.
Although the works of Li et aL (1991, 1993, 1994) cited above were conducted on interior
forms of rainbow trout, Behnke (1992) reported finding redband trout in the desert basins of
southern Oregon and northern Nevada where temperatures regularly kill other trout. Trout in
these intermittent desert streams were found actively feeding in water of 82.9°F (28.3°C).
Behnke suggested that redband trout from an Oregon desert basin have an optimum feeding
temperature at some untested temperature higher than 66.2°F (19°C). These desert redband
might have a functional feeding temperature that is higher than that of rainbow trout, which have
evolved in less harsh environments of temperature and water flow. A test was evaluated that
compared an introduced population of rainbow trout in the Firehole River in Montana with two
hatchery stocks. Temperatures in the Firehole River in summer at times reached as high as 85.1 °F
(29.5^) due to thermal springs. The introduced population had been living in the river for
approximately 20 generations, yet it was found that neither the functional feeding temperature nor
the upper incipient lethal temperature had increased compared with the hatchery stocks. The
author concluded that thousands of jears of adaptation to a diy environment have enabled Oregon
desert redband trout to feed at high temperatures, but 60-70 years seem too few to have allowed
the introduced rainbow trout to raise their functional feeding temperature in the Firehole River.
Summary of Technical Literature Examining the Phjsiological Effects of Temperature 43
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Kaya et aL (1977) found that daily maximum temperatures exceeding 77T (25°C) caused
rainbow trout to move out of the mainstem of the Firehole River in Montana. These fish would
move into tributary streams that averaged 10.8-18T (6-10°C) lower in temperature.
The above research shows a wide range in the estimates of optimal temperature for rearing
rainbow trout. This wide range may reflect the fact that the individual subspecies and specific
stocks have evolved differently to fit the characteristics of their home streams. Also, different
ages and sizes of fish were used in the research. Equally plausible is that some of the
temperatures for redband trout that were higher than noted for rainbow trout or other salmonids
might have been based on an improper assumption that temperatures measured in the vicinity of
the fish were actually those that the fish inhabited—that is, fish might actually inhabit microhabitat
or habitat-scale refiigia to maintain their populations in otherwise hostile conditions (see Ebersole
et al. in press). Because criteria must protect both adult and juvenile forms of rainbow trout, an
optimal temperature regime seems to most consistently occur in the range of 55.4-60.8°F
(13-16°Q.
What is the relationship between growth temperatures and other physiological
responses?
When fish demonstrate temperature preference in a thermal gradient, this is an adaptive
mechanism that allows them to be positioned in an environment where they can achieve optimum
physiological performance (Coutant 1987, Hutchison and Maness 1979). Hutchison and Maness
(1979) cited numerous physiological processes that achieve optimum performance near the
thermal preferendum: growth rate, appetite, food conversion efficiency, digestion, egestion,
metabolic scope, oxygen debt load, maximum sustained speed, maximum volitional speed, resting
and active blood pressure, active cardiac work, cardiac scope, learning and memory, immune
response, renal function, hormone secretion, reproductive function, elimination of anaerobically
produced lactate, and enzyme activity.
Temperatures preferred or avoided are highly correlated with key physiological indices
(Stauffer 1980). Final temperature preference is correlated with optimal growth temperature
(Jobling 1981, Kellogg and Gift 1983, Christie and Regicr 1988). Kellogg and Gift (1983) found
for four fish species that nearly all preferred temperatures measured were in a range that provided
75% ofmaximum growth rate. The physiological optimum is derived by averaging the growth
optimum and preferred temperature (Brett 1971). Preferred temperature also is correlated with
the temperature providing the maximum metabolic scope. This, in turn, is related to the
temperature providing the maximum critical swimming speed (Kelsch and Neill 1990). Also, fish
tend to be more immunologically resistant to pathogens at their preferred temperatures (Sniezko
1974, Cuchens and Clem 1977, Avtalion et al. 1980, O'Neil 1980, Rijkers et al. 1980, Avtalion
1981, Wishkovsky and Avtalion 1982, all cited in ODEQ 1995).
The preferred temperature range for chinook fingerlings was 53.6-55.4°F (12-13°C) (based
on determination ofmean ofthe distribution) when acclimated to temperatures ranging from 50 to
75.2°F (10-24°C) (Brett 1952). If growth temperatures are maintained between 50 and 60°F (10-
15.6°C), growth rate would be >80% ofthe maximum level observed in feeding at 60% satiation
(a level considered by Brett et aL [1982] to correspond to naturally occurring food availability
SummaryofTechnical Literature Examining die Physiological Effects of Temperature
44
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levels).
For sockeye, Brett (1971) found that swimming capacity, metabolic scope, growth on excess
rations, and ingestion were maximized at 59°F (15°Q. The temperature producing the growth
optimum (59°F[15°C]) also was the final thermal preferendum determined by acute tests (Brett
1952, 1971). A correlation between final preferred temperature and optimum growth has been
found in numerous other fish species (Christie and Regier 1988). In coho, it was found that
swimming speed was maximum at 68°F (20°C), but growth reached a maximum on excess food
rations at 62.6-68°F (17-20°C) (Griffiths and Alderdice 1972).
What are temperature feeding limits for salmonids?
Temperature feeding limits are the upper and lower temperatures that result in inhibition of
feeding. The ability to consume food does not guarantee that growth occurs. Food intake rate
and conversion efficiency (assimilation rate) at any temperature dictate the amount of energy
assimilated. However, if metabolism rate exceeds energy assimilation rate, no energy is available
for growth. In feet, the fish would lose weight because energy stored in tissue is used for
metabolism.
Brett et al. (1982) observed feeding behavior of juvenile chinook from the Nechako River, in
British Columbia, and the Big Qualicum River, on Vancouver Island. They reported good feeding
response to unlimited food supply at 71.6°F (22°C), but feeding became more sporadic between
73.4 and 77°F (23-25°C), at which point it ceased.
Fingerling sockeye began losing appetite at 73.9°F (23.3°C) and stopped feeding at 75.2°F
(24°C). Maximum feeding rate was measured as 8% dry body wt/d at 68°F (20°C). Redband
trout can be expected to set the upper limit for feeding response for all salmonids of the Pacific
Northwest. No feeding was observed by Sonski (1982 as cited by Sonski 1984) for juvenile
redband at 77.9-80.6°F (25.5-27°C). Comparing thermal tolerance by three rainbow trout
species, Sonski (1984) found that no redband trout or Wytheville rainbow would feed at
temperatures >78.8T (26°Q. The Firehole River stock would not feed beyond 80°F (26.7°C).
In CTM (critical thermal maximum) experiments in which the heating rate was 3.6°F
(2°C)/d, five species of juvenile salmonids were observed feeding up to temperatures that were
1.8-3.6°F (1-2°C) less than the LT50 (Grande and Anderson 1991). Lake trout, brook trout,
brown trout, rainbow trout, and Atlantic salmon were observed feeding at temperatures of 74.8,
78.2, 79.1, 79.9, and 82.6°F (23.8, 25.7, 26.2, 26.6, and 28.1 °C), respectively, reached during
CTM experiments. A similar CTM experiment with Salmo apache in which temperature was
increased 1,8-2.7°F (1 -1.5°C)/d showed that fish began refusing food at 68°F (20°C) and totally
stopped feeding at 70.1 °F (21.2°C) (Alcorn 1976). In northern California streams, juvenile
steelhead were seen actively feeding in water temperatures as high as 75.2°F (24°C) (Nielsen et al.
1994). However, once temperatures reached 71.6°F (22°C), rate of foraging began to decline.
How is feeding rate affected by acclimation temperature?
The highest temperature for normal feeding in brown trout varies with acclimation
SummaryofTechnical Literature Examining the Physiological Effects of Temperature
45
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temperature, as is probable for all fish species. Elliott (1981) determined that the highest
temperature for normal feeding in brown trout that were acclimated to 59°F (15°C) was 19.1°C ±
0.27 (SE). Similarly, Frost and Brown (1967) determined that feeding rate declined sharply
above 66.2°F (19°Q in brown trout. When fish were acclimated to 68°F (20°C), no feeding took
place. Under cold temperature regimes, when brown trout were acclimated to water at 50°F
(10°C), normal feeding occurred when fish were subjected to 2.9°C ±0.27. When acclimated to
even lower temperature 41°F (5°C), normal feeding occurred at 0.4°C ±0.21.
What are temperature growth limits for salntonids ?
Temperature growth limits for salmonids are those lower and upper temperatures that result
in zero growth on an individual basis or zero net growth of the population. The zero net growth
temperature is the temperature at which net elaboration of tissue of the population is zero or the
temperature at which fish mortality balances the gain in growth.
With chinook, the bounds for positive growth occur at 40.1 °F (4.5 °C) (lower limit) and
66.4°F (19.1°C) (upper limit) (see Armour 1990). The 39.4°F (4.1°C) and 66.4°F (19.1°C) limits
tabulated in Armour (1990) are zero net growth limits for a chinook population. Brett et al.
(1982) reported a zero individual growth rate under 60% satiation feeding at 70.5°F (21.4°C).
Juvenile sockeye had a positive growth response between 39.2 and 69.8°F (4-21 °C) in
laboratory experiments with feeding to satiation once pa- day (Donaldson and Foster 1941).
Growth rate was negative at 73°F (22.8°C), and at this tenperature mortality was significant.
Good growth with low mortality occurred at 53-62°F (11.7-16.7°C) (Donaldson and Foster
1941). The upper limit to growth was similar to that observed by Brett et al. (1982) for chinook
feeding at 60% of satiation rations.
Brown trout growth can be high in the temperature range 44.6-66.2°F (7- 19°C), but growth
is poor above 68°F (20°Q (Frost and Brown 1967).
Wurtsbaugh and Davis (1977) studied growth of steelhead trout in laboratory streams under
three fluctuating temperature regimes (natural cycle, natural +5.4°F [3°C], and natural +10.8°F
[6°C]) in all four seasons and found that trout growth could be enhanced by temperature increases
up to 61.7°F (16.5°C). During the summer season the control temperature (natural cycle) was
61.1 °F (16.2°C) (mean) and the elevated temperatures averaged 67.1 and 72.5°F (19.5 and
22.5°C). The average diel temperature range for the summer growth period was about 6.1°F
(3.4°C) under the three treatments. Growth rates under food consumption of 5%-15% dry body
wt/d were higher under the control temperature regime than at the elevated fluctuating regimes.
Undo- the high temperature regime (mean of72.5°F [22.5°C]), growth rate was zero at a food
consumption rate of 7%/d.
How does food availability affect growth of salmonids at different temperature
exposures?
In a laboratory setting, feeding rations can be controlled by the researchers. Feeding to
satiation at a frequency of three to five times a day is not uncommon in growth experiments and is
SummaryofTechnical Literature Examining the Physiological Effects of Temperature 46
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considered to provide growth rates comparable to those under continuous feeding with excess
food In other studies, varying feeding regimes maybe used to determine the temperature effects
on growth at different levels of food availability.
In the field, stream productivity and nutrient availability to salmonids depend on many
factors including light; nutrients including inputs of litter, decomposing salmon carcasses, and
coarse woody debris; sediment loading; temperature; and streamflow (Murphy 1998, Bilby et al.
1996). Other factors that may limit fish feeding in the wild include suitable instream cover and
species- or density-dependent competition and predation (Richardson 1993).
Food limitations in trout streams commonly cause reductions in summer growth (Cada et al.
1987, Enseign and Strange 1990). If there is food limitation in the field, growth rates will be less
than maximum for salmon and bull trout at temperatures that produce maximum growth under
satiation feeding. Growth rates have been observed in the field that are less than those predicted
in the laboratory under excess feeding and suggest that food limitation could be the cause (Preall
and Ringler 1989, Cada et al. 1987). With food limitation, the upper temperature that produces
zero growth would decline to a lower temperature. Under conditions where fish have reduced
feeding rates due to food limitation, conversion efficiency can increase somewhat to compensate
for the limitation in total energy intake. However, if the food limitation is significant, the energy
demands of standard metabolism may be difficult to satisfy (Cada et al. 1987). This may limit the
scope of activity required to acquire food. Behavioral inhibition in swimming at higher
temperatures and lack of competitive ability in foraging compared with fish tolerant of warm
water can place salmonids at a disadvantage in deriving maintenance energy requirements.
Gut fullness may be an indicator of food availability. Gut fullness was monitored on several
fish species on various dates from late July to mid-October in several tributaries of the upper
Yakima River as an index of food availability (James et al. 1998). During this sampling period,
temperatures were >57.2°F (14°C). Species monitored included mountain white fish, spring
chinook, red side shiner, and rainbow trout. A high degree of diet overlap was found among the
four fish species studied, indicating that competition for food is possible. Gut fullness and diet
overlap together were assumed to indicate degree of competition. Summertime gut fullness for
spring chinook averaged 14%, while mountain whitcfish, rainbow trout, and redside shiner
averaged 32%, 10%, and 10%, respectively. Low stomach fullness may indicate a low availability
of food due to production of food and intense competition. It is not clear from this research,
however, what gut fullness level would be expected under satiation feeding. Growth rates are the
bottom line. Comparison of growth rates at various feeding levels in the laboratory with rates in
the field under comparable temperatures appears to be the most direct means to infer food supply.
If food becomes limited, the positive growth zone can shrink dramatically (ie., the maxirmm
temperature at which growth is positive declines) and the optimum growth zone shifts to lower
temperatures to compensate for elevated respiration/growth ratios (Elliott 1981, p. 231).
McMahon et al. (1999) found that growth curves for bull trout clearly depict a shift to maximum
growth at lower temperatures (46 and 53°F [8 and 12°C]) when energy availability is low. Elliott
found that for brown trout the temperature at which growth is zero drops from 66.2 to 46.4°F
(19-8°C) when food rations are reduced from maximum to 12.5% of maximum. Because the
growth optimum falls within 50-60°F (10-15.6°C) for chinook and because diseases become a
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
47
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significant mortality risk beyond this level, water temperatures in major salmon-rearing reaches
must be managed on a stream network level from headwaters to mainstem so that temperatures
can be maintained below 60°F (15.6°C) within the historic salmon rearing area and below 53.6°F
(12°C) in bull trout historic rearing areas. Given that food rations under field conditions are
typically less than satiation levels, a reduced growth zone expands the upper temperature zone
and causes loading stresses. This argues for keeping temperatures no higher than the optimum
growth range.
Is there evidence for food limitation in natural streams?
A stream's capacity to produce food greatly affects both abundance and growth of fish.
Some of the highest freshwater production value have been reported for trout in New Zealand;
production values reported for the Pacific Northwest are considerably lower, by at least an order
of magnitude (Bisson and Bilby 1998).
Factors influencing stream productivity include nutrient availability, input of organic matter
from external sources, the channel's capacity to store and process organic matter, and light
(Cederholm et al. 2000). The river continuum concept describes the predictable differences in
stream productivity with changes in stream size (Vannote et al. 1980). Headwater streams in the
Pacific Northwest are characterized by low levels of primary and secondary productivity (Gregory
et al. 1987). In a large watershed, first- to third-order streams may produce only 10%-20% of the
annual gross primary production, despite having more than 80% of total stream length (Murphy
1998). Coho, steelhead, cutthroat, bull trout, and spring chinook are among the salmonids that
utilize these small headwater streams for spawning and rearing.
Productivity of Northwest streams has been further diminished by the recent decline of
Pacific salmon. The role salmon populations play in maintaining ecosystem function by recycling
energy and nutrients from the North Pacific Ocean to the inland Northwest has been
acknowledged in numerous studies (see Cederhom et aL 2000). The carcasses of spawned-out
salmon greatly influence the productivity of the otherwise generally oligotrophy ecosystems of
the Pacific Northwest (Cederholm et al. 2000). With declines of Pacific salmon, it is estimated
that only 3% of the marine-derived biomass once delivered by anadromous salmon to the rivers of
Puget Sound, the Washington coast, the Columbia River, and the Oregon coast is currently
reaching those streams (Grcsh et al. 2000 in Cederholm et aL 2000).
Growth rates of wild rainbow trout in the field have generally been reported as < 1 %/d (sec
review by Wurtsbaugh and Davis 1977) but were higher in the laboratory in every season under
the natural temperature regime (mean seasonal temperatures in the laboratory of 50, 44.4, 48.9
and 61.1°F [10, 6.9, 9.4, and 16.2°C] in autumn, winter, spring, and summer, respectively) when
fish were fed to satiation. This study revealed that trout growth was improved by increasing
temperatures up to a maximum of 61.7°F (16.5 °C), but that this threshold applies to the field only
undo" satiation feeding. Because the researchers measured field growth rates in an Oregon
coastal stream that indicated food limitation, they concluded that temperatures less than 61.7°F
(16.5°C) would be optimal.
In the field an increase in water temperature, when produced by canopy removal, can lead to
Summary ofTcchnical Literature Examining the Physiological Effects of Temperature
48
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increased primary production. Greater primary and secondary production can increase food
availability to fish (Murphy and Hall 1981, Hawkins et al. 1983) provided that substrate
sedimentation does not increase with canopy removal. However, as temperatures continue to
increase, primary production can be in the form of algae not readily consumed or digested by
benthic macroinvertebrates (e.g., blue-green algae rather than diatoms) (McCullough 1975,
McCullough et al. 1979), and macroinvertebrate production can be dominated by species not
readily available to salmonids in the drift (Li et al. 1994). Even if food quality remains high with
increasing temperature, feeding rate and growth decline beyond the optimum temperature.
Additionally, over the long run, increases in primary production in early serai stage may eventually
be outweighed by longer-lasting reductions as a result of increased shade in later serai stages
(Murphy and Hall 1981). Second-growth hardwoods and young conifers produce a denser
canopy and lack the gaps commonly found in old-growth forests (Murphy 1998).
Can growth rates be predicted under field conditions using thermal history identified
under laboratory conditions?
Growth rates under controlled field conditions can be related to growth rates obtained under
laboratory conditions if feeding rates and temperatures are known; however, many subtle
variables in the field (recruitment to or movement out of the study area, varied caloric content of
forage, inter- and intraspecies interactions) can complicate these comparisons. Differences
between laboratory and field growth rates can be attributable to a great number of iactors.
Typically, temperatures in laboratory experiments arc kept constant (i.e., fluctuating less
than ± 1.8°F [1°C] around the mean). First, to compare laboratory and field growth rate we must
know the field water temperature regime. Growth rates should be measured over days to weeks
to improve the ability to detect a change. The temperature regime must be described by an index
(e.g., daily mean, daily maximum) in order to relate it to laboratory growth rates. For example, if
growth rate under a constant laboratory temperature of 50°F (10°C) is 2%/d and under field
conditions a 2%/d growth rate is experienced by fish under a 50°F (10°C) ± 3.6°F (2°C) diel
temperature regime, then we might conclude that the mean diel temperature in the field
adequately represents the growth conditions. However, food is generally limiting in the field. If
this is the case and if the mean field temperature adequately represents the growth response, we
would expect field growth rate to be lower than laboratory rates at the same constant mean
temperature. The situation can be more complicated, however, because growth rate is related to
acclimation temperature. In a fluctuating temperature regime, fish can acclimate to a temperature
between the mean and maximum of the cycle. If this is so, the feeding rate in the field (and
consequently growth rate) might be higher than under a constant diel temperature equal to the
mean of the cycle, despite the lower food availability. That is, there may be some compensation
for lower food availability due to fluctuating temperature conditions. In summary, field growth
depends on the food availability and quality, the effective acclimation temperature, and the
exposure temperature.
The ability to model brown trout growth in the laboratory and field under fluctuating
temperatures arose from Elliott's (1975a, b) studies of brown trout growth under constant
temperatures. This model has often been found capable of predicting growth under both constant
and fluctuating temperatures (Elliott 1994). Elliott (1975a) found that growth rates in the
Summary of Technical Literature Examining the Physiological Effects of Temperature 49
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laboratory over 42-d periods in which temperature fluctuated as much as ±4.1°F (2.3°C) around
the mean for the entire period closely matched those predicted by entering the mean temperature
into the growth model. Growth experiments in the field (a small stream near Windermere,
England) were also conducted. In one experiment, temperature increased from 44.2°F (6.8°C) in
March to 53.8°F (12.1 °C) in June; in another, temperature decreased from 55.2°F (12.9°C) in
August to 45°F (7.2°C) in November. Estimates of growth in the field made by entering the mean
weekly temperatures (calculated as the mean of seven daily mean temperatures) into the growth
model revealed good agreement between predicted and actual final weights in a 4-wk growth
period. Edwards et al. (1979) modeled brown trout growth on 10 British streams and were able
to show that predicted growth was 60%-90% of potential growth, assuming feeding on maximum
rations. Predicted monthly growth based on mean monthly terrperaturcs was 2% different from
computations based on temperatures taken every 4 h. Likewise, Prealland Ringler (1989)
developed a computer model of brown trout growth based on Elliott's work and predicted
potential growth for populations in three central New York streams based on initial weight,
condition factor, and weekly mean temperature. These authors measured actual growth under
fluctuating temperatures in the field that were 60%-90% of potential, as determined from their
model. Jensen (1990) measured growth on 12 populations in Norwegian rivers and determined
that mean growth rates of anadromous brown trout parr were 76%-136% of the maximum
inferred from the temperature regime.
Jensen (1990) concluded from his field work that growth rates exceeding laboratory-derived
maxima under constant temperatures and satiation feeding could be explained by interpopulation
genetic differences or the ability of fish in the field to feed at greater rates under fluctuating
temperatures than under constant temperatures. It is also possible that the ability to assess
temperatures actually experienced in the field is poor and not well represented by mean reach
temperature. Jensen (1990) noted that in two streams growth was best predicted by using the
75% temperature (the median between the mean and maximum), whereas for another stream
growth was best predicted using mean temperature. Assuming that Jensen could measure the
actual diel cycle experienced by brown trout in these streams, the similar ability of the 75%
temperature in predicting growth and in estimating equivalent acclimation temperatures in UILT
tests is interesting. It appears that physiological conditioning offish in fluctuating temperatures
adjusts their growth and thermal tolerance toward levels that would be predicted under constant
temperatures located between the mean and the maximum.
Another possible explanation not given by Jensen (1990) for greater growth rates in the field
is that food quality in the field is better than that provided in laboratory experiments. Also, fat
content of macroinvertebrates in the drift could be higher than the average of prey available in the
benthos and provide a high-calorie diet. Food quantity, however, is often considered limiting to
fish growth in the field (Brett et al. 1982). Growth rates of wild rainbow trout in the field have
generally been reported as < 1 %/d (see review by Wurtsbaugh and Davis 1977), but were higher
than this in the laboratory in every season under the natural temperature regime (mean seasonal
temperatures in the laboratory of 50, 44.4, 48.9, 48.9 and 61.1°F [10, 6.9, 9.4, and 16.2°C] in
autumn, winter, spring, and summer, respectively) when fish were fed to satiation.
Other studies have noted that mean temperatures are useful in predicting growth rates.
Growth rates of sockeye fry (Babine Lake, BC, stock) were measured at satiation feeding (3
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
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times/d) from March to mid-May under three temperature regimes: constant 50°F (10°C),
declining 23.4 to 12.6°F (13 to 7°C), and increasing 12.6-23.4°F (7 to 13°Q. Mean temperature
was 50°F (10°C) in each treatment. Rate of temperature change in the declining or increasing
treatments was 1.8°F (l°C)/wk over a 56-d period. Although mean temperature can be a suitable
index to growth rate under a fluctuating temperature regime, the studies above did not subject fish
to either extreme temperature maxima or extreme diel fluctuations.
Has acclimation to a temperature higher than the mean of a diel cycle been
demonstrated?
In addition to the research discussed above, Clarke (1978) measured growth rates ofjuvenile
sockeye in the laboratory at constant and fluctuating temperatures. At constant temperatures
ranging from 45.5 to 63.5°F (7.5-17.5°C), growth rates increased linearly. This response was
defined by the equation y = 0.0660x - 0.311, where x is mean temperature and y is growth rate
(%wt/d). At 45.5°F (7.5°C), growth rate was approximately 0.2%/d and at 63.5°F (17.5°C) it
was approximately 0.8%/d. At a constant 50°F (lO'U) regime, growth rate was 0.35%/d
(estimated by regression for all constant temperature growth experiments), but under fluctuating
regimes of 44.6-55.4°F (7-13°C) and 41-59°F (5- 15°C) (mean daily temperatures of 50°F
[10°C]), growth rates were about 0.47%/d and 0.63%/d, respectively. This study indicated that
specific growth rate (as%wt/d) at 44.6-55.4°F (7-13°C) was equivalent to that observed at a
constant temperature of 52.5°F (11.4°C). Under the diel regime with great amplitude (41-59°F
[5-15°C]), growth was equivalent to that observed at a constant temperature of 57°F(13.9°C).
This indicates that under diel fluctuating regimes, there was an acclimation to an equivalent
temperature between the mean and the maximum temperature. In terms of growth rates, this
acclimation effect was similar to that observed in survival under thermal stress with prior
acclimation in cyclic diel temperature regimes.
Are there seasonal differences in growth rates not related to temperature?
Jensen (1990) noted that a decreasing autumn temperature trend caused growth to be less at
a given temperature than at the same temperature under a generally increasing temperature trend
in spring. Such a seasonal effect has been observed in brown trout and Atlantic salmon by some
authors, but others have not detected any seasonal difference at comparable temperatures (Jensen
1990). A study by Mortensen (1985 as cited by Jensen 1990) indicated that 0+ and 1+ brown
trout growth rate in the field during spring was accurately predicted using Elliott's model, but
growth rate was only 60%-90% of predicted rates in summer and 0%-30% in winter. Jensen
attributed the realized growth rate to seasonal limitation in food availability.
What research seems to best describe the influence of fluctuating temperature on
growth?
Probably the best study of the effect of fluctuating temperature on salmonids is that of
Hokanson et al. (1977). It is especially useful as a central point for evaluating other studies
because of the range of temperatures evaluated, the fact that both growth and survival were
evaluated, and its consistency with the vast literature on thermal effects.
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Hokanson and colleagues studied growth and survival of rainbow trout (O. mykiss) juveniles
reared on maximum rations under fluctuating temperatures (T°F ± 6.8°F [3.8°C]) versus constant
temperatures. The physiological optimum (PO) temperature of rainbow trout is 60.8-64,4°F
(16-18°C). These authors noted that specific growth rate at mean temperatures less than PO was
lower for a given mean temperature under a constant (T°F) versus a fluctuating (T°F ± 6.8°F
[3.8°C]) temperature regime. This indicates a benefit of a fluctuating regime when the mean
temperature is less than PO. In this temperature zone, a constant temperature of T+2.2°F (1,5°C)
provided comparable specific growth rate to juveniles reared at T°F ± 6.8°F (3.8°C). In other
words, we would have to increase an initial constant temperature by2.7°F (1.5°C) to provide
growth rates equivalent to those exhibited under a fluctuating regime having a mean equal to the
initial constant temperature. However, specific growth rates at mean temperatures greater than
PO were higher at constant than fluctuating temperatures having the same mean temperature.
This indicates that when water temperature under field conditions is greater than PO, it is not safe
to assume that a fluctuating regime is protective on the basis of its mean, even if the mean itself is
not injurious under constant temperature experiments. The negative influence of the diel cycle
appears to come from exposure to temperatures higher than the mean when the mean is greater
than PO.
This pattern led Hokanson and colleagues to suggest that the growth of rainbow trout
appears to be accelerated under fluctuating temperatures when the mean temperature is below the
constant temperature optimum for growth and retarded by fluctuating temperatures when the
mean is higher. Hokanson et al. suggested that water quality standards (based on weekly mean
values) should be set such that the average weekly temperature is below the constant test
temperature producing maximum growth. They determined that rainbow trout growth rates
under fluctuating regimes do not correspond to those in a constant temperature regime having a
mean equal to that for the cycle. Rather, they acclimate to some value between the mean and
maximum daily temperatures and consequently their growth rates reflect this "effective"
temperature. Looked at another way, the optimal fluctuating regime had a mean of 59.9°F
(15.5°C) with a rangeof 53-66.7°F (11.7-19.3°C), and the optimal constant test temperature of
63°F (17.2°C) fell approximately midway between the daily mean and the daily maximum of the
optimal fluctuating test.
Most of the research on optimal growth temperatures is conducted at a constant
temperature. Water quality standards, however, must apply to naturally fluctuating thermal
environments. Because temperature directly affects the metabolism of fish, a fish kept
continuously in warm water will experience more metabolic enhancement than one that
experiences the same temperature for only 1 or 2 hours per day. Thus, constant test results
cannot be reasonably applied directly to the daily maximum temperature in a fluctuating stream
environment. Although the constant temperature test results could be used to represent daily
mean temperatures, it is believed that the daily maximum temperature is more influential to the
biology and should be the focus of any standards developed.
Clarke (1978) studied individual specific growth rates of underpaying sockeye salmon after
42 d at five constant temperatures ranging from 45.5 to 63.5°F (7.5-7.5°Q and two diel cycles of
44.6-55.4°F (7-13°C) and 41-59°F (5-15°C). At constant temperature, there was a linear increase
in growth rate over the range 45.5-63.5°F (7.5-17.5°C). Both thermocycles had a mean of 50°F
SummaryofTechnical Literature Examining the Physiological Effects of Temperature
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(10°C), but growth was greater on the 41-59°F (5- 15°C) cycle. The author notes that the
equivalent constant temperature for specific growth rate in length on the 44.6-55.4°F (7- 13°C)
cycle was increased significantly from 50°F (10°C) in one replicate (54.1 °F [12.3 °C]) but not in
the other (51.4°F [10.8°C]). Specific growth rate in length on the 41-59°F (5-15°C) cycle was
equivalent to that on a constant temperature of 59.5°F (15.3°C). Specific growth rate in weight
on the 44.6-55.4°F (7- 13°C) cycle was equivalent to that on a constant 52.5°F (11.4°C); on the
41-59°F (5-15°C) cycle it was the equivalent of a constant 57°F (13.9°C). This study concludes
that under year ling so eke ye salmon exposed to diel thermo cycles are able to acclimate their
growth rates to a temperature above the mean of the cycle.
Dickerson et al. (1999 and unpublished data, as cited in Dunham 1999) conducted
experiments with hatchery-reared Pyramid Lake strain Lahontan cutthroat trout. Fish were
exposed to 1 wk fluctuating temperatures (68-78.8°F [20-26°C]; mean = 73.4°F [23°C]) and to
constant temperatures of 55.4, 68, and 73.4°F (13, 20, and 23°C). Growth rates in the fluctuating
temperature tests were lower than for fish exposed to constant temperatures of 55.4 and 68°F (13
and 20°C), but were similar to groups of fish held at a constant 73.4°F (23°C).
Hahn (1977) investigated the effects of fluctuating (46.4-66.2°F [8- 19°C]) and constant
(47.3, 56.3, 65.3°F [8.5, 13.5, 18.5°C]) temperatures on steelhead trout fry and yearlings. He
found that as many fish remained in the fluctuating regime as in the constant 56.3°F (13.5°C)
temperature water; twice as many remained in the fluctuating temperature regime as remained in
the constant 65.3°F (18.5°C) temperatures; and twice as many fish remained in constant 47.3°F
(8.5°C) water as in the fluctuating temperature regime. By inference, Hahn found the relationship
among the three constant temperatures was the same as the relationship of each to the fluctuating
temperature: twice as many fish in 56.3°F (1 3.5°C) as in 65.3°F (1 8.5°C), twice as many fish in
47.3 °F (8.5 °C) as in 56.3°F (13.5°C), and four times as many fish in 47.3°F (8.5°C) as in 65.3 °F
(18.5°C). We can conclude from Hahn's work that juveniles had equal preference for constant
(56.3°F [13.5°C]) water and fluctuating (46.4-66.2°F [8-19°C]) water with a mean of 56.3°F
(13,5°C). Although not a growth test, the Hahn study supports the general premise that daily
mean temperatures are reasonable approximations of constant exposure test temperatures.
Grabowski (1973) conducted growth experiments with steelhead trout. Fish were fed a
percentage of body weight according to feeding charts twice per day based on temperature and
changes in body weight. To evaluate growth, fish were subjected to four test temperatures for 8
wk. These four regimes were a fluctuating test from 46.4 to 64.4°F (8-1 8°C) (mean 55.4°F
[13°C]) and constant tests held at 46.4, 59, and 64.4°F (8, 15, and 18°Q. Steelhead grew better
at 59°F (15°C) than at other temperatures. Fish in the fluctuating test had the second highest
growth rate and actual weight gain. Growth rate in the fluctuating test was only 13% less than
that at the constant test of 59°F (15°C), while growth rates at 46.4 and64.4°F (8 and 18°C) were
47% and 21% less, respectively. Plotting the data using the midpoint in the fluctuating test as a
surrogate for a constant test condition creates near linear growth from 46.4 to 59°F (8-15°C),
with a steep drop as temperature progresses to 64.4 °F (18°C). Thus the mean of the fluctuating
treatment appears generally comparable to a constant test temperature of the same value.
Thomas et al. (1986) investigated the effects of diel temperature cycles oncoho salmon.
Temperature cycles (50-55.4, 48.2-59, 46.4-62.6, and 43.7-68°F [10-13, 9-15, 8-17, and
Summary of Technical Literature Examining the Physiological Effects of Temperature
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6.5-20°C]) were used to simulate observed temperatures inclearcuts of southeastern Alaska.
Different levels of feeding, including starvation, were used in each of the tests. Cyclic
temperatures for 40 d, averaging 51,8°F (11 °Q daily, did not influence growth of age-0 fish on
any ration in comparison to the controls (kept at a constant 51.8°F [11°C]). Plasma Cortisol and
glucose concentrations were significantly greater in fish maintained for 20 d in the 43.7-68°F
(6.5-20°C) cycle, which may be an indicator of long-term stress. Thus, in the work by Thomas et
al. (1986) the daily mean of the fluctuating test and the constant test exposures produced
essentially equivalent results, but stress conditions were noted to occur in cycles with daily peak
temperatures of 68°F (20°C).
Everson (1973) used the data of Averett (1969) to show that growth rates and gross
efficiencies of food conversion offish kept at moderate constant temperatures (59.9°F [15.5°C])
were somewhat greater than those of fish exposed to temperatures that fluctuated about a similar
mean value (60°F [15.6°C]), whereas at higher average temperatures the fluctuation of
temperature markedly benefited the growth and food conversion efficiency of the fish. Thus
Everson showed support for the assumption that fluctuating temperatures can produce greater
benefits to growth than can higher constant temperatures.
What is the range of laboratory growth rates under fluctuating temperature vs.
constant temperature?
There appears to be considerable controversy regarding the effect of fluctuating
temperatures vs. constant temperatures on juvenile growth rate. Peterson and Martin-Robichaud
(1989) studied growth of Atlantic salmon under daily temperature cycles of 53.6-68°F (12-20°C)
and 60.8-68°F (16-20°C) relative to constant temperatures of 60.8 and 68°F (16 and 20°C) and
could find no differences.
Thomas et al. (1986) measured growth of juvenile coho for 40-d periods under constant
51.8°F (11°C) temperature vs. diel temperature cycles of 50, 55.4, 48.2, 59, 46.4, 62.6, and 43.7-
68°F (10-13, 9-15, 8-17, and 6.5-20°C), all ofwhich averaged 51.8°F (11°C). Theyfound that
the growth rates of 0+ age fish at any of the food rations were not significantly different among
temperature regimes, although the growth at 4% and 8% ration (i.e., 8% of body weight/day) was
better than at 1%.
Konstantinov et al. (1989) reported that under fluctuating thermal regimes coho salmon have
a decreased respiration rate and increased growth rate relative to that at constant temperatures.
This coupling of respiration and growth causes greater efficiency in use of assimilated energy in
growth. Konstantinov and Zdanovich (1986 as cited by Behnke 1992) measured greater growth
rates in several fish species under fluctuating vs. constant temperature regimes. Konstantinov et
al. (1989), summarizing several of their studies on effect of fluctuating thermal regimes on fish,
stated that growth rate under a fluctuating regime tends to be 10%-40% greater than at constant
temperatures equal to the mean of the cycle.
Biette and Geen (1980) reported variable response of0+ age sockeyeto cyclic temperature
regimes relative to constant temperatures depending on food ration. Under zooplankton rations
equal to 4.0%-6.9% dry body weight/d and a fluctuating temperature similar to that experienced
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in the field in diel migrations, sockeyc grew as well or more rapidly than under constant
temperatures of 60.6, 59.5, 52.3, or 43.1°F (15.9, 15.3, 11.3, or 6.2°C). This ration was
estimated to be comparable to that consumed under field conditions in Babine Lake. Rearing
sockeye underwent diel vertical migrations between the hypolimnion, having temperatures of 41-
48.2°F (5-9°C), and the epiHmnion, with 53.6-64.4°F (12-18°C) water. During periods of
maximum lake temperature, sockeye inhabited the epilimnion for 2 h in early afternoon and 2 h in
early evening. At higher food rations, growth at constant high or intermediate temperatures
exceeded that under cyclic temperatures. At both high and low rations, food conversion
efficiency and growth were greater in a constant temperature regime than under fluctuating
conditions during daily vertical migrations in the field.
Wurtsbaugh and Davis (1977) studied growth of steelhead trout in laboratory streams under
three fluctuating temperature regimes (natural cycle, natural +5.4°F [3°C], and natural +10.8°F
[6°C]) in all four seasons and found that trout growth could be enhanced by temperature increases
up to 29.7°F (16.5°C). During the summer season the control temperature (natural cycle) was
61.1 °F (16.2°C) (mean) and the elevated temperatures averaged 67.1 and 72.5°F (19.5 and
22.5°C). The average diel temperature range for the summer growth period was about 6.1°F
(3.4°C) under the three treatments. Growth rates under food consumption rates of 5%-15% dry
body wt/d were higher under the control temperature regime than at the elevated fluctuating
regimes. Under the high temperature regime (mean of72.5°F [22.5°C]) growth rate was zero at a
food consumption rate of 7%/d. Gross food conversion efficiency decreased as temperatures
increased from 61.1 to 72.5°F (16.2-22.5°C). Maintenance rations increased by a factor of three
over the temperature range 44.4-72.5°F (6.9-22.5°C). This study revealed that trout growth was
improved by increasing temperatures up to a maximum of 61.7°F (16.5 °C), but that this threshold
applies to the field only under satiation feeding. Because researchers measured field growth rates
in an Oregon coastal stream indicating food limitation, they concluded that temperatures less than
61.7T (16.5°Q would be optimal for the trout. Food limitations in trout streams not
uncommonly cause great reductions in summer growth (Cada et al. 1987).
Laboratory growth experiments were run on juvenile rainbow trout reared in Lake Ontario
water (Dockray et al. 1996). Growth was measured for juveniles over a 90-d period in which
"control" temperatures followed the ambient lake diel fluctuations and also varied in daily mean
temperature from 55.4 to 75.2°F (13-24°C) over this summer period A water treatment fecility
resulted in increasing control temperatures by 3.6°F (2°C) over background for each day of the
growth study. Growth rate over this period was significantly less for the warmer regime, having
mean daily temperatures of 59-78.8°F (15-26°C). A comparison of the day 0-30 initial growth
period with the day 60-90 growth period is revealing. The initial period had daily control
temperatures varying from 55.4 to 64.4°F (13-18°C); the final period had temperature variation
from 66.2 to 75.2°F (19-24°C). The treatment temperature regime was equal to the daily control
temperatures +3.6°F (2°C). In the first 30-d period, food conversion efficiencies were 42.4% and
45.6%, respectively, for the control and treatment fish. For the final 30-d period, conversion
efficiencies were 27.3% and 6.2%, respectively. The warmer temperature regimes in the final
30-d period substantially reduced conversion efficiency from the initial period. This effect was
very pronounced in the 69.8-78.8°F (21 -26°C) regime for treatment fish in the final 30-d growth
period. In addition, growth was just barely positive for the last 30-d growth period for fish in the
69.8-78.8°F (21-26°C) regime.
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Troughs stocked at high density with rainbow trout were supplied with Columbia River
water in tests of growth rate and disease susceptibility (Fujihara et al. 1971). Water in troughs
was maintained at ambient conditions for July (63.8-71 °F, mean 67.4°F [17.7-21.7°C, mean
19.7°C]), ambicnt-4°F (2.2°C), and ambient+4°F (2.2°C). Growth rate under the reduced
temperature was 44% greater than under the ambient condition, even though mortality rates
associated with cohimnaris disease were comparable.
In another study on O. mykiss (steelhead parr from Dworshak National Fish Hatchery,
Idaho), growth rate under a fluctuating temperature with feeding 2 times/d to satiation was
contrasted with growth at constant temperatures of 46.4, 59, and 64.4°F (8, 15, and 18°C) for 2-
and 8-wk periods. Best steelhead growth occurred at 59°F (15°C). By contrast, instantaneous
growth rate under the fluctuating temperature was 11% less (Grabowski 1973). The thermocycle
was sinusoidal, so a mean temperature of 55.4°F (13°C) can be inferred. Growth at constant
temperatures of 46.4 and 64.4°F (8 and 18°C) was 36% and 29% less than at 59°F (15°C)
(Grabowski 1973). These data allow one to hypothesize that the effective growth temperature for
the 46.4-64.4°F (8-18°C) cycle was close to 59°F (15°C), but it is not possible to determine
whether it was slightly above or below 59°F (lS^).
In summary, laboratory studies indicate that increasing food rations between 1% and 8%
body weight/d results in an increased growth rate (Thomas ct al. 1986, Elliott 1994). Growth
rates have been found to be no different under fluctuating than under constant temperature equal
to the mean ofthe cycle (Peterson and Martin-Robichaud 1989, Thomas ct al. 1986). In contrast,
growth rates under fluctuating regimes have been reported as greater than at constant
temperatures equal to the mean of the cycle (Konstantinov et al. 1989, Konstantinov and
Zdanovich 1986, Clarke 1978, Biette and Geen 1980). The study byBiette and Geen (1980)
indicates that a fluctuating temperature regime might confer a growth advantage on juvenile
sockeye under bw, rather than high, food availability as typically found in lake environments.
Enhanced growth under a fluctuating temperature regime might reflect an acclimation to a
temperature higher than the mean of the cycle, similar to responses exhibited in tests of lethal
temperatures in survival studies.
Other studies have reported that fluctuating temperature regimes are not all equal. For
example, under three fluctuating regimes in which diel temperature varied approximately 6.1°F
(3.4°C) in each, steelhead growth rate was greatest in the fluctuating regime with the lowest mean
(61.7°F [16.5°C]) as opposed to those with means of 67.1 and 72.5°F (19.5 and 22.5°C)
(Wurtsbaugh and Davis 1977). A very similar result was obtained with rainbow trout (Fujihara et
al. 1971), in which the highest growth rate occurred at the lowest mean temperature (63.5°F
[17.5°C]) in a fluctuating regime. In another study with steelhead, highest growth rate occurred
at 59°F (1 5°C) under constant temperatures (Grabowski 1973). In this study a fluctuating regime
(46.4-64.4°F [8-18°C]) with a mean of 55.4°F (13°C) had a growth rate less than that at 59°F
(15°C). Studies that indicate a reduction of growth rate under fluctuating temperatures occurs
when fluctuations extend above the zone of best constant temperature growth (approx. 55.4-
60.8°F [13-16°C]) for salmonids under satiation feeding. Fluctuating temperatures appear to
provide a growth benefit to salmonids when the mean of the cycle is lower than the constant
temperature growth optimum. In this manner all the studies cited above are consistent with
findings ofHokansonet al. (1977).
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Smoltification
How is smoltification measured?
The rate of silvering during smoltification is related to temperature, presmoh size, migration
timing, and photoperiod (McMahon and Hartman 1988). Silvering generally increases with
increased temperatures (Hoar 1988). During the smolt transformation, body lipids decrease in
quality and quantity and the smolt assumes a lower condition factor (weight per unit length)
(Hoar 1988). Survival of smolts in the marine environment depends heavily on the degree of
smoltification, which can be measured in terms of ability to regulate plasma sodium
concentrations and grow in seawater (Mahnkenand Waknitz 1979, Clarke and Shelbourn 1985).
What is physiological stress and at what temperatures does it occur in salmonids?
Many stressors can induce physiological stress in salmonids. These include temperature
(high, low, or thermal shock), hyperosmotic stress (when juveniles enter the saline waters of the
estuary or ocean), migration (physical exertion), crowding, and other factors. Stress can be
detected via changes in the endocrine system. A promising indicator of smoltifcation is the sharp
increase in thyroxine (T4) in bbod plasma (Wedemeyer et al. 1980). Numerous other
physiological tests are available to index the degree of stress on fish health (Wedemeyer 1980,
Iwama et al. 1998, Beckman et al. 2000). Among these are measures of plasma glucose and
Cortisol as indices of acute or chronic stress (Wedemeyer 1980), changes in gill ATPase activity
(Zaugg 1981), and heat shock protein production (Iwama ct al. 1998).
Not all stress or associated endocrine changes are bad. Migration upstream in adults and
downstream in juveniles or the smoltification process are stressful but essential aspects of salmon
life history. These processes involve instantaneous to seasonal shifts in endocrine balance that
reflect physiological processes over time. During smoltification there is a predictable pattern of
gill ATPase activity throughout the downstream migration (Beckman et al. 2000). However, any
physiological process can be disrupted. In terms of thermal influence, this can alter developmental
rates (shift the timing of life history events), or impair or inhibit functions. Impairment caused by
thermal stress can be increased when it is combined with other stressors (e.g., low dissolved
oxygen). Habitat destruction and water pollution can act together, leading to a cumulative stress.
The magnitude of the stress can be detected using endocrine (ATPase, Cortisol), biochemical
(e.g., lipid), morphological (e.g., body shape, condition factor, degree of silvering), or
developmental (stage of egg development) indicators to detect deviation from normal range or
rate of change.
Thermal stress is any temperature change that significantly alters biological functions of an
organism and lowers probability of survival (Elliott 1981). Stress was categorized by Fry (1947
as cited by Elliott 1981) and Brett (1958) as lethal (leading to death within the resistance time),
limiting (restricting essential metabolites or interfering with energy metabolism or respiration),
inhibiting (interfering with normal functions such as reproduction, endocrine and ionic balance,
and feeding functions), and loading (increased burden on metabolism that controls growth and
activity). The latter three stresses can be lethal when continued over a long period (Elliott 1981).
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Loading stress increases with temperature above the positive growth zone, but it also
increases with reduction in food availability because this shrinks the growth zone. Thermal stress
can have a cumulative effect between the feeding limit (temperature at which feeding ceases,
slightly beyond the chinook growth limit of 66.4°F [19.1 °C]) and the UILT (Elliott 198 1). Within
this zone the combined effects of food limitation, low oxygen concentration, high turbidity,
competition for space, and temperature can result in death (Elliott 1981, Wedemeyer and McLeay
1981). This is the so-called tolerance zone, identified by Elliott as the exposure/acclimation
temperature bounded by the UILT for 7-d exposure. Reduced oxygen concentration and other
factors can accentuate thermal stress (Wedemeyer and McLeay 1981) even within the growth
zone and can lower the optimum growth temperature.
What are the seasons for passage of smolts of common anadromous species and how
would this information be used?
The timing of smolt passage relative to the water temperature regime of migration habitat is
vital to surviving the passage, feeding, avoiding predators, avoiding disease, and improving the
level of smolt ificat ion during emigration. Some general dates of smolt passage past selected dams
on the Columbia and Snake Rivers are given in Table 6 as a representation of the issues that need
to be considered. For example, passage of any species or life history type can occupy an
extensive time period. To allow full protection of the run, the total duration of the run must be
known. However, there is considerable year-to-year variation in timing. In addition, the
downstream passage of smolts and adults of the same stock may be different. That is, protection
of a stock involves providing suitable water temperatures for all life stages.
What are heat shock proteins and what do they indicate?
Heat shock proteins (HSPs) are expressed in response to biotic and abiotic stressors (e.g.,
heat or cold shock, anoxia, diseases, chemical contaminants including heavy metals). These
unique proteins are produced in cells and tissues of many organisms, including fish (Dietz 1994,
Iwama et al. 1998) under environmental stress. They have many biochemical roles, including
proper folding of cellular proteins and restoring thermally denatured proteins to their native state.
Temperatures at which HSPs are induced can be mediated by acclimation temperature (Dietz
1994). Although HSPs can be related to thermal tolerance, their presence also indicates
environmental stress. Although they help repair cellular protein damage caused by stressors such
as high temperature, they are a useful indicator of thermal stress that requires tissue repair (Currie
and Tufts 1997) and leads to irreparable cell damage.
What temperature range is recommended for reducing physiological stress?
The optimum temperature range provides for feeding activity, normal physiological
response, and normal behavior (i.e., without thermal stress symptoms) and is slightly wider than
the growth range. Deviation from this range implies greater stress, leading to greater impairment
in physiological functions and greater mortality. Stresses of migration and acclimation to
saltwater activate many low-grade infections by freshwater disease organisms (Wedemeyer et al.
1980) and the mortalities produced by these diseases go largely unnoticed. Optimum
temperatures likewise minimize physiological stress. Growth temperatures that are optimum or
SummaryofTechnical Literature Examining the Ph)siological Effects of Temperature 58
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lower tend to be minimally subject to warm-water diseases.
Tabic 6. Historical dates of smolt migration past selected dams oil the Columbia and Snake Rivers. Data
from Fish Passage Center (1993)
Monitoring Sites
(dams)
Species
Historical Passage Dates'
10%
50%
90%
Lower Grani te
Chinook l's
4/17
4/27
5/24
Chinook 0's
na
na
na
Steelhead
4/28
5/12
6/01
Sock eye
na
na
na
Rock Island
Chinook l's
4/22
5/07
5/22
Chinook 0's
6/06
7/04
8/02
Steelhead
5/06
5/15
5/31
Coho
5/13
5/21
5/29
Sock eye
4/19
5/02
5/26
McNary
Chinook l's
4/23
5/10
5/23
Chinook 0's
6/15
7/03
7/20
Steelhead
4/29
5/18
6/02
Coho
5/16
5/21
5/31
Sock eye
5/01
5/16
6/03
John Day
Chinook l's
4/28
5/15
5/30
Chinook 0's
6/08
7/21
9/01
Steelhead
4/26
5/15
5/31
Coho
5/06
5/13
5/31
Sockeye
5/10
5/22
6/04
Bonneville
Chinook l's
4/19
5/02
5/21
Chinook 0's
na
na
na
Brights2
6/07
6/27
7/29
Steelhead
4/26
5/14
5/31
Coho
4/27
5/10
6/01
Sock eye
5/11
5/23
6/04
1 Historical percentiles are based on passage data for 7 years (1984-90) at Lower Granite and McNary dams; 6
years (1985-90) at Rock Island Dam; 4 years (1986-89) at John Day Dam; and 4 years (1987-90) at Bonneville
Dam for spring migrants and 3 years (1988-90) for summer migrants.
2"Brights" at Bonneville Dam refers to subyearling chinook arriving after June 1; this excludes most "tule" fall
chinook originating from Spring Creek hatchery.
Why might it be advisable to use naturally reared vs. hatchery-reared salmonids to
measure physiological status?
Significant differences between conditions in the field and in the hatchery can lead to
different physiological responses in these environments. For example, these environments may
have different seasonal temperature profiles, photoperiod, nutrition, and social interactions, which
could produce variations in developmental timing, growth rate, size at age, and body composition
(Beckman et al. 2000). Consequently, the physiological status of hatchery-reared fish may not
Summary of Technical Literature Examining the Physiological Effects of Temperature 59
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relect that of naturally reared fish.
Differences in physiological indicators between hatchery and wild salmonids were reported
for Columbia River chinook (Congleton et al. 2000). Cortisol concentrations were higher in wild
than hatchery chinook in early, mid-, and late season. In this study, Cortisol was used as an
indicator of stress in barge transportation. However, for both wild and hatchery fish, Cortisol
declined during the barging in early and late season, but not mid-season. This effect was
produced by social interaction with the high densities of steelhead that were loaded on barges in
mid-season, causing stress in chinook. In addition, ATPase activity was significantly lower in
migrating hatchery steelhead and chinook in the Columbia River than in the wild fish of these
species. These differences were greatest in late April to early May. Hatchery rearing can result in
suppression of gill ATPase activity for at least 7 wk after release (Congleton et al. 2000).
How does physiological status of smolting salmon change seasonally?
Few studies on smolting salmonids monitor a broad range of physiological indicators, much
less study salmon in the wild throughout the year. Beckman et al. (2000) reported endocrine and
physiological status of naturally reared spring chinook juveniles in the Yakima River, Washington.
Status was measured in terms of condition factor, weight, stomach fullness, body appearance,
liver glycogen, body lipid, gill Na+-K+ ATPase, plasma thyroxine (T4), and plasma insulin-like
growth factor-I (IGF-I). The smolting period (April-May) was characterized by an increase in
ATPase activity, plasma T4, and IGF-I. At the same time there was a decrease in condition
factor, body lipid, and liver glycogen. Body lipid reached a high in late summer (5%-8%) and a
low during winter of 2%-3.5%, and then increased to 4% by March. Body lipid again declined
during April-May, when smolting occurred. Condition followed the same pattern as whole-body
lipid content. Body weight of juveniles increased dramatically from February to May. A similar
decline in body lipid content was reported for chinook and steelhead from the American River,
California (Castleberry et al. 1991). High lipid content in juveniles is associated with high adult
return rates. For example, fell chinook smolts with 7.9% whole body lipid had an adult return
rate nearly 1.9 times greater than those having only 4.1% (Burrows 1969 as cited by Castleberry
et al. 1991).
In springtime, plasma T4, IGF-I, and gill ATPase increased as fish migrated downstream in
the Yakima River (Beckman et al. 2000). These indicators of smoltification have been reported in
other studies. Other reported changes include increased growth rate, increases in plasma growth
hormone (GH), and metabolic rates (Hoar 1988, as reported by Beckman et al. 2000). During
smoltification there are two distinct phases—first anabolic, then catabolic. The anabolic phase in
Yakima River spring chinook occurs from January through March and is characterized by an
increase in condition factor, IGF-I, weight, and lipid. The catabolic phase which follows from
April through May is characterized by an increase in condition factor and IGF-I, but a decline in
weight and lipid content. A high plasma GH causes depletion of glycogen and lipid.
How does photoperiod influence growth rate and subsequent saltwater readiness of
smolts?
Juveniles migrating downstream from freshwater to saltwater exhibit saltwater readiness in
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
60
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their ability to regulate plasma sodium concentrations. If high water temperatures impair
smoltification processes, including the ability to regulate plasma sodium, survival in saltwater
would be reduced. The ability of a juvenile to regulate plasma sodium depends on its growth rate
and consequent size. Growth rate is a function of temperature and food availability. A study of
spring chinook growth rate under satiation feeding found that photo period experience at first
feeding (i.e., after emergence) helps to set the potential growth rate. Juveniles exposed to a
short-day photoperiod from February to mid-April followed by a bng-day photoperiod had a
significantly greater growth rate and final body weight by midsummer than juveniles that
experienced only along-day photoperiod (Clarke et al. 1992). A long-day photoperiod after
emergence is apparently a developmental cue that produces a slower growth rate than in fish
exposed to a short- then long-day photoperiod at the same temperature. This cue causes juveniles
to overwinter at bast 1 year before emigration. In saltwater challenge tests, the ability of
juveniles to regulate plasma sodium by midsummer depended on their experiencing the natural
sequence of photoperiods. It is questionable whether juvenibs that experienced a long-day
photoperiod at emergence would actually attempt to emigrate in the first summer. Growth rate
and body size are vital in determining tendency to emigrate and subsequent survival (Bilton et al.
1982). The study by Clarke et aL (1992) does highlight the need to consider photoperiod history
from emergence through rearing as well as food availability and temperature in comparisons of
growth rates between stocks.
Salmon parr feed throughout the summer in streams, gaining weight, length, and lipid
content (see Beckman et al. 2000). As autumn approaches, Atlantic salmon parr may become
segregated into two size groups, indbating their ability to smolt the following spring (upper
modal group) or the need to spend another year growing in freshwater (lower modal group)
(Metcalfe and Thorpe 1992). Overwintering salmon undergo a period of anorexia (foss of body
fat) coinciding with a loss of appetite and cessation of growth, even when food is present. The
onset of anorexia is controlled by photoperiod (Thorpe 1986, as cited by Metcalfe and Thorpe
1992). However, the loss in body fat is controlled by variable "defended" energy levels. That is,
fish that will smolt in the spring maintain a higher appetite and feeding rate. This balances energy
costs of maintaining a feeding station and capturing food against the gain in growth rate
and ability to smolt early, thereby avoiding mortality in a second overwintering period.
Are smolts affected by high temperatures during migration?
Migratbn during the smolt phase can be lethal. For example, in the lower Sacramento
River, a 50% mortality was estimated over a 48-km migration distance, based on smolt releases
during the May-June perbd, 1983-1990. These mortalitbs were associated with temperatures of
73.4 ± 1.9°F (23 ± 1.1°C) (Baker et al. 1995).
In addition to thermally induced mortality during migration, smolting juveniles can be
indirectly affected by high temperatures. For example, subyearling chinook rearing innearshore
areas of the Columbia River can be forced into the main current to avoid increasing temperatures
along river margins. This becomes significant above 62.6°F (17°Q (Connor et aL 1999).
Reduced food in marginal areas of the river coupled with high water temperatures reduces the
capability of the river to rear fish to proper smolt condition (Coutant 1999).
Summary of Technical Literature Examining the Ph>siological Effects of Temperature
61
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Gill ATPase is a useful indicator of smoltification. In the Columbia River, high levels of gill
ATPase activity are frequently associated with longest travel time downstream through the dams.
However, subycarling fell chinook have occasionally exhibited slowest travel times with highest
ATPase levels (Tiffan et al. 2000). Rapid juvenile growth in premigrants typically accompanies
increasing ATPase levels, leading to increased ability to osmoregulate in seawater. Migration in
an impounded river may alter the relationship between ATPase and time of ocean entry. Tiffan et
al. (2000) determined that ATPase activity increased for Hanford Reach fall chinook from
Hanford Reach to McNary Dam and decreased afterward. Even though saltwater mortality
declined over this migration path, the decline in ATPase activity in 1994 appeared to be greater
than in 1995. The greater 1994 loss may account for that year's higher mortality rate in saltwater
challenges. Chinook smolts often migrate during reduced streamflows and elevated water
temperatures. Mainstem dams cause significant delays in migration rates, and smolts in reservoir
forebays undergo prolonged exposure to surface temperatures as high as 77°F (25^) or more
(Vcnditti et al. 2000). Such high temperatures limit fall chinook production by impairing the
ability of juveniles to grow, smolt, and maintain appropriate migration timing. Late emigration
results in the lowest survival rates (Connor et al. 1999).
Are smolts subject to cumulative stresses from thermal exposure?
Temperatures of 64.9-70°F (18.3-21.1°C) place smolts under either lethal or loading stresses
that can impair metabolic activity (Brett 1958). For example, in subycarling fall chinook in the
Columbia River, temperatures of64.4-68°F (18-20°Q inhibit feeding. Heat shock proteins are
produced after exposure to 68°F (20°C) for several hours (Sauter and Maule 1997).
What temperatures are required to inhibit smoltification in steelhead and salmon?
Smolt transformation in steelhead rearing in water >52.3 °F (11.3 °C) was inhibited (Adams
et al. 1973); rearing temperatures >55.4°F (13°C) prevent increases in ATPase activity (Hoar
1988). This effect is stronger in steelhead than in coho, chinook, or Atlantic salmon (Adams et al.
1973, Adams et al. 1975 as cited by Johnston and Saunders 1981). Temperatures >56.5°F
(13.6°C) do not permit smoltification in summer steelhead (Zaugg et al. 1972, as cited byZaugg
and Wagner 1973). In winter steelhead, a temperature of 54.1°F (12.3°C) is nearly the upper
limit for smolting (Zaugg and Wagner 1973). Zaugg (1981) found that a temperature of 53.6°F
(12°C) could inhibit successful migration to the ocean in winter steelhead. Because ocean entry in
the Columbia River normally occurs in mid and late May and river temperatures typically reach
53.6°F (12°C) by mid-May, failure of steelhead smolts to enter the ocean maybe attributed to low
water flow and associated high water temperatures (Zaugg 198 1). Dawley et al. (1979 as cited by
Zaugg 1981) observed that peak steelhead migration to the ocean, as determined by capture at
Jones Beach, coincided with river temperatures above 53.6°F (12°Q.
In the American River, California juvenile steelhead (young-of-the-year) were captured
during their downstream migration for measurement of Na+ -K+ ATPase (Castleberry et al.
1991). The authors reported that ATPase activity increased from capture temperatures of 60.8°F
(16°C) to 68°F (20°C), and that increased river temperatures did not suppress smoltification, but
may have enhanced it. However, they also noted that ATPase activity was uniform for fish of
standard lengths from 60 to 100 mm. The authors interpreted this evidence to mean that
Summary of Technical Literature Examining the Physiological Effects of Temperature 62
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steelhead did not develop into smolts at sizes below 100 mm SL. Furthermore, they did not
sample steelhead longer than 100 mm but indicated they were not common. In the American
River, steelhead emerged from early April through early May and were abundant in the
middle-lower river site from early May to early June. At this period, temperatures cycled daily
from 61.7 to 66.2°F (16.5-19°C). In addition, capture temperatures up to mid-May were often as
much as 3.6°F (2°C) greater than the average temperature for the 2-wk period prior to capture,
meaning that the correlation of ATPase with temperature may not be as meaningful as believed.
This study did not deal with yearling steelhead and did not describe successful smolt migration.
Steelhead usually do not migrate to sea until reaching age 1 to 3 years (Moyle 1976, as cited by
Castleberry et al. 1991), so it is not clear what relevance ATPase activity in age-0 juveniles has to
smolt saltwater readiness, but it does indicate temperature ranges that juveniles experience in their
pre-smolt migrations. These data do not appear to challenge the large body of literature detailing
the sensitivity of steelhead smolts to migration temperatures >53.6-55.4T (12-13°C).
Some smoltification processes are greatly retarded by water temperatures >55.4°F (13°C),
and in some Pacific salmonids smolt stage cannot be attained at 60.8°F (16°C) (see references
cited by Johnston and Saunders 1981). An apparent exception is that temperatures as high as
59°F (15°C) have been used to increase growth rate and onset of smolting in coho. However,
desmoltification is also high at this temperature. Laboratory tests clearly showed that a high
constant temperature regime of 68°F (20°C) during coho emigration caused a very restricted peak
in gill ATPase activity compared with a normal 50°F (10°C) temperature regime. Under the
elevated temperature regime, ATPase activity plummeted prior to ocean entry (Zaugg and
McLain 1976). Fall chinook undergo an even greater desmoltification rate at temperatures of
59°F (15°C) (Wedemeyer et al. 1980). In work on Central Valley chinook stocks from California,
Marine (1997) found that normal smolt development patterns can be altered or inhibited with
prolonged rearing in a temperature range of 62.6-75.2°F (17-24°C) compared with rearing in a
range o f 55.4-60.8°F (13- 16°C). Evidence for the effects o f temperatures exceeding 62.6°F
(17°C) came from changes in gill ATPase activity, reduced survival in acute scawater exposure,
and a reduced hypo-osmoregulatory capability. In addition, juvenile chinook exposed for 2.5
months to 62.6-75.2°F (17-24°C) incurred increased loss to predation compared with juveniles
exposed in the range 55.4-60.8°F (13-16°C), although the causal mechanism was not identified.
Sock eye terminate their downstream migration if water temperature exceeds 53.6-57.2°F
(12-14°C) (Brett et al. 1958), although coho can withstand some further increases. The influence
on the smoltification process, though, may be common to both species.
What temperatures are required to reverse smoltification in steelhead?
Yearling steelhead held at 43.7°F (6.5°C) and transferred to 59°F (15°C) had a marked
reduction in gill ATPase activity, indicating a reversal of some smolting changes (Wedemeysr et
al. 1980). When temperatures exceeded 55.4°F (13°C), gill Na-K-ATPase activity declined in fish
that had already begun smoltification, and there was a decreased ability to migrate (Zaugg and
Wagner 1973). Zaugg and Wagner (1973) considered this effect, operating well below lethal
limits, to have serious implications for survival of steelhead because it inhibited migratory ability.
Can incubation temperature affect smolt emigration timing?
Summary of Technical Literature Examining the Ph>siological Effects of Temperature
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Temperature regime can influence time of snolt emigration. Research on Carnation Creek,
British Columbia, revealed that most variation in chum and coho emigration dates was attributed
to mean stream temperatures between peak spawning and emergence (Holtby et aL 1989). Shifts
in this portion of the annual temperature regime were linked to land-use practices (Hartman et al.
1984). Alteration in the emigration date in turn can affect survival in the marine environment
(Thedinga and Koski 1984, Holtby et al. 1989). From laboratory studies, it would appear that an
accelerated temperature regime during springtime would result in either earlier emigration (caused
by more rapid development to the smolt stage) or less success in smoltification (caused by high
temperature desmoltification or inhibitory effects) (seeZaugg and Wagner 1973).
What river temperatures are associated with peaks in migration?
Most steelhead emigration occurs before river temperatures rise above 53.6°F (12°C).
Emigration can extend into temperatures as high as 61.7°F (16.5°C). The 53.6°F (12°C) limiting
temperature normally does not occur until mid-May, but in low-flow years can occur in late April;
this shift in thermal regime may cause a reduction in steelhead survival (Zaugg 1981). The South
Umpqua River, a southern Oregon coastal river subject to thermal extremes, has a wild spring
chinook run. This stock begins emigration when stream temperatures exceed 50°F (10°C).
Approximately 50% of the emigration takes place at 54.5-59°F (12.5-15°Q and the upper tail of
the run is generally complete before 68°F (20°C) is exceeded. Large fish that are presumably
most ready to enter the ocean delay entry until temperatures warm beyond 50°F (10°C) (Roper
and Scarnecchia 1999). In spring chinook from the American River, California, juvenile levels of
gill Na+-K+ ATPase increased with increasing standard length between 30 and 80 mm and
capture temperature from 53.6 to 64.4°F (12-18°C) (Castleberry et al. 1991). However, juveniles
were no longer found in the Iowa- river in early May. Maximum daily terrperatures ranged from
64.4 to 69.8°F (18-21°C) and minimum daily temperatures were as low as 59°F (15°C). Juveniles
were found in the middle upper site in late June when diel temperatures fluctuated regularly
between approximately 59 and 64.4°F (15 and 18°C). These chinook typically enter the ocean
2-4 months after emergence at a size of 40-80 mm (sizes of juveniles captured at monitoring
sites). These data indicate that temperatures as high as 64.4°F (18°C) do not prevent ATPase
levels from increasing, but temperatures beyond this appear to eliminate juveniles from affected
river reaches.
How do freshwater and ocean temperatures affect time of ocean entry?
The relation of the temperature of the lower reach of a river entering the ocean and the
temperature of the ocean itself is important in determining growth rates in the early ocean phase
and survival. Two of the most important factors regulating seawater adaptability, such as ability
to regulate plasma sodium, are freshwater rearing temperature and time of transfer to seawater.
The relative growth rate of fall chinook in seawater was greatest after rearing in freshwater in
temperatures of 46.4-57.2°F (8-14°C), followed by transfer to 55.4-58.1 °F (13-14.5°C) in early
May to early June. Freshwater rearing at 60.8°F (16°C) resulted in growth rates that were 70%
of those at 50°F (10°C) (i.e., a temperature within the preferred range).
Smolts must be able to regulate plasma sodium, maintain their silver color (indicative of their
degree of smoltification), and maintain a high growth rate. The temperatures present in the
SummaryofTechnical Literature Examining the Physiological Effects of Temperature
64
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freshwater environment and ocean during the smolt's emigration and ocean entry, as well as its
timing of ocean entry, are critical in determining initial growth rates. Freshwater temperatures
must be low enough during emigration so that complete smoltification can take place prior to
ocean entry. If all these conditions are met (and also the size of migrants leaving the natal
tributaries is optimum), a smolt will likely be able to maintain critical size before ocean entry.
Otherwise, desmoltification can take place, smolts fail to maintain a critical size, and they become
parr-revertants (Mahnken and Waknitz 1979, Folmar et al. 1982). By losing their smolt status,
juveniles fail to enter the ocean, die, or attempt to rear in the lower river to await smoltification in
a subsequent year, which is unlikely.
Hatchery releases should be timed to avoid extreme temperatures during smoltification to
ensure maximim passage survival Releases should coincide with historic migration times,
however (Wedemeyer et al. 1980). If historic migration timing now coincides with adverse
temperatures, naturally produced salmon and steelhead are likely to be affected. Altered (e.g.,
earlier) times of release of hatchery fish to avoid human-caused thermal stress may result in
inappropriate ocean entry timing and lower overall survival.
What is the role of temperature in migratory response and seawater adaptation?
A maximum temperature of approximately 53.6°F (12°C) is recommended for chinook and
coho to maintain migratory response and seawater adaptation in juveniles (Wedemeyer et al.
1980, CDWR 1988, p. 4).
Wedemeyer et al. (1980) recommended that winter and spring hatchery water temperatures
below 53.6°F (12°C) would protect the smoltification process for chinook, coho, and steelhead.
Their recommendations apply to proper physiological development during the smoltification
process, timing of saltwater entry, and high marine survival.
How can multiple stresses during the smolting phase be reduced?
Infection offish with freshwater diseases should be minimized because the stresses of
migration and acclimation to saltwater can increase mortality from disease (Wedemeyer et al.
1980). Warm-water diseases can be transmitted through hatchery practices, by contagion in
migration through dam passageways, and in barging.
Human-caused increases in estuary temperature must be restricted. In addition, numerous
chemical contaminants, such as herbicides, that can become concentrated in the estuary have been
shown to inhibit smolt function and migratory behavior (Wedemeyer et al. 1980). The
smoltification process is physiologically stressful to fish. Additional stresses associated with
elevated temperature or other pollutants should be avoided. (See Multiple Effects issue paper for
a detailed discussion of these effects.)
Swimming Speed
How is swimming speed measured?
SummaryofTechnical Literature Examining the Phjsiological Effects of Temperature 65
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Sustained swimming performance is a swimming speed that can be maintained for long
periods (>200 min) without fatigue. This activity is totally aerobic, so no oxygen debt builds up.
Sustained swimming during migration tends to occur at 15%-20% of maximum swimming speed
(Bell 1991). Some tests have documented swimming for periods of 2 wk without fatigue for a
variety of species. Prolonged swimming speeds define a performance of shorter duration (20 s-
200 min) that involves both aerobic and anaerobic metabolism Exhaustion of glycogen stores can
result in fatigue. Within the range of speeds that define prolonged swimming at a particular
temperature, the faster the speed, the more anaerobic metabolism is responsible. Critical
swimming speed is a special case of prolonged swimming. It may be measured in fish swimming
at a particular temperature (either a temperature to which they arc fully acclimated or as an acute
performance at a test temperature) or by increasing swimming velocity in increments (such as 10
cm/s) to determine the maximum speed at which swimming can be maintained for a fixed period
(e.g., 60 min). If a fish can swim 60 min continuously at 50 cm/s but only a fraction of that time
at 60 cm/s, the critical speed is interpolated. A median performance for a test group offish is
taken as the critical swimming speed. Comparisons among sizes within a species can be made in
terms of body length/s rather than cnVs. Burst swimming is the maximum swimming rate that can
be achieved for periods up to 20 s and is largely independent of temperature. This is essential for
prey capture, predator avoidance, and rapid migration through swift water. During burst
swimming, fish consume some oxygen but are powered mostly by anaerobic metabolism. Burst
swimming can reach approximately 22 ft/s in chinook, coho, and sockeye and up to 27 ft/s in
steclhead (Bell 1991).
It is interesting to compare swim speeds determined from laboratory studies with those from
field studies. Hinch and Rand (1998) used electromyogram radiotelemetry on Fraser River
sockeye to measure tail beat frequency (TBF). TBF was then converted to swim speeds using
laboratory regressions of TBF against swim speed. Swim speeds varied by reach within study
sections in accordance with constrictions, channel form, and probably associated flow patterns. In
a 7.6-km study section in the lower Fraser River, including the Fraser River canyon, average swim
speeds varied from approximately 75 to 125 cm/s in the 10 consecutive study reaches. In this
river section, water temperatures ranged from 60.8 to 66.2°F (16-19°C) during tracking. Speeds
varied by river reach depending on constrictions and channel bank form. Male sockeye swam at
mean speeds of 118 cm/s and females at 90 cm/s. In another study year, male average swim speed
was only about half as fast (i.e., 62 cm/s). Near the spawning grounds approximately 900 km
further upstream, water temperatures ranged from 68 to 71.6°F (20-22°C) and average swim
speeds declined to 50-60 cm/s (Hinch and Rand 1998). This decline in swim speed may be
associated with the warm river temperatures. Other explanations might be that those individuals
that migrate at very high swim speeds when encountering complex flow patterns (see Hinch and
Bratty 2000) were already eliminated from the population by exhaustion, or the population in
general might have suffered energy depletion that impaired swimming capacity.
Combinations of swimming speeds and time periods exceeding critical time limits may build
up lactic acid in tissues and require resting periods of up to 3 hours before further swimming can
occur (Paulik et al. 1957). Rate of recovery from anaerobic metabolism is a function of water
temperature and oxygen concentration.
At what swimming speeds do metabolic transitions occur?
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Data from Bainbridge (1960, 1962) for rainbow trout and Brett (1964) for sockcyc, as
summarized in a single figure by Beamish (1978), illustrate the sharp differentiation among
sustained, prolonged, and burst swimming performances at a fixed temperature. As swimming
speed is reduced in the prolonged swimming zone (ie., performance time of 20 s-200 min),
swimming can eventually be performed without fatigue; this point denotes the transition to
sustained swimming (i.e., the temperature-swimming time period combination that allows
continuous swimming for long periods). At higher swimming speeds in the prolonged swimming
zone, a transition occurs in the plot of log (time to fatigue) versus velocity that denotes a
transition from prolonged to burst swimming (Beamish 1978). This transition (ie., of the critical
swimming speed) occurs at approximately 3 and 5 body lengths/s in rainbow and sockeye,
respectively. At these velocities, fatigue occurs in approximately 20 s. Burst swimming speed
increases only as time to fatigue decreases. Because of evidence such as this for many fish
species, 20 s is generally taken as the period producing this metabolic transition.
Critical swimming speed is a physiological performance measure that can indicate the ability
of a fish to function in a natural flowing-water environment. It indicates ability to capture prey
and avoid predators (Castleberry et al. 1991). Sharp reductions in critical swimming speed at high
temperatures indicate environmental risk for a given life stage and fish size (see Griffiths and
Alderdice 1972, Brett and Glass 1973).
Why is swimming speed vital to adults during migration?
During adult migration, swimming speed is important in maintaining progress toward
holding or spawning areas upstream. At falls, rapids, or fish ladders, adult migratory fish must
often be able to swim in the sustained speed range, and for challenges at significant falls or under
high water velocities, instantaneous burst swimming must be available. The swimming velocity
needed to leap a falls depends on the height of the falls; the higher the falls, the greater the speed
that must be attained when thrusting through the water surface.
Water temperature and oxygen concentrations are significant controls on swimming speed.
However, progress upstream also depends on other factors, such as water velocities along the
migratory path and barriers to migration (e.g., falls, debris jams, or dams). In moderate water
velocities, as found in reservoirs, migration rates of chinook can match or exceed those in free-
flowing reaches (Bjornn 1998c, as cited byNMFS 1999). Very high flows can impede migration.
Under normal river flow rates the tradeoffs between difficult passage at dams and easier
swimming in reservoirs make it difficult to estimate the net effect (NPPC 1999). It is possible that
to the degree that adults would be stressed by repeated dam passage enroute to spawning
grounds. Maintenance of migratory ability remains dependent on proper flow direction and
olfactory cues and cool temperatures (NPPC 1999). If water temperature is high and/or oxygen
concentrations arc low, swimming speed and migration rates can be impaired; fish may refuse to
migrate, migrate back downstream, or seek shelter in tributaries or other cold-water refuges if
such are available (NMFS 1999, draft white paper). Under these conditions, net upstream
movement maybe reduced or extremely delayed. Holding in warmed pools can result in spread of
warm-water diseases.
Summary of Technical Literature Examining the Physiological Effects of Temperature 67
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Swimming speeds can be substantially impaired at temperatures above the swimming
optimum. Fraser River sockeye have an optimum temperature of 62.6°F (17°C) for swimming
endurance, but this is reduced 20% at 69.8°F (21°C) (Macdonald ct aL in press). This takes on
ecological significance given the varying temperatures in the river. At Hell's Gate on the Fraser
River, temperatures were >64.4°F (18°C) for a 60-d period during summer; upstream
temperatures reached a maximum of>71.6°F (22°C). Zones of elevated temperature create
stressful conditions that impair swimming capability in demanding passage conditions (Macdonald
et al. in press). The tendency for some sockeye migrants at Hell's Gate to become hyperactive
and exhibit a "burst-then-sustained speed" pattern under high flows at passage constrictions
would make them even more susceptible to combined effects of high temperature and hypoxia if
these conditions coincided with high flows (Hinch and Bratty2000).
Why is swimming speed vital to smolts during migration?
Smohs migrating downstream have different problems with current velocities than do adults.
For adults, high current velocity can impede upstream migration, but with moderate temperatures
and oxygen concentrations, their upstream movement tends to be easier because they can seek
conditions in which sustained or prolonged swimming speed exceeds current velocity, thus
allowing net upstream travel. Smolts, on the other hand, benefit from rapid current flow because
their downstream progress depends on water velocity rather than swimming speed. Downstream
migrants, such as subyearling fall chinook, are capable of controlling their downstream rate of
travel by swimming toward shore, where they feed in shallows. If marginal areas are too warm
and if the warm water, fine sediment substrate conditions, and slow water do not produce
abundant macroinvertebrates that can serve as prey (see Coutant 1999), growth rates and survival
may be low.
With downstream smolt migration, swimming speeds must not be impaired because
swimming is vital to controlling rate of descent and avoiding obstacles. Temperature must not be
so high that swimming is inhibited. In addition, for juveniles (including smolts), nonimpairment of
swimming capability is important because of the increased vulnerability to predation that
accompanies the effect of high water temperature on swimming performance (Bams 1967,
Schrcck 1990, Kruzynski and Birtwell 1994, all as cited by Marine 1997). However, some
reduction in swimming capacity is expected during smoltification (Smith 1982, as cited by
Castlebcrry et al. 1991), resulting in reduced ability to maintain position in current and the
tendency to be swept downstream more rapidly.
How does temperature affect juvenile swimming speed?
Brett (1958) provided a useful graph of the relationship between cruising speed (ft/s) and
acclimation temperature for underyearling sockeye and coho. Sockeye acclimated to 59°F (15°C)
achieved their maximum cruising speed (approx. 1.12 ft/s). Coho acclimated to 68°F (20°C)
attained their maximum cruising speed (approx. 1.02 ft/s). Sockeye swimming speed was reduced
to approximately 58% of maximum as water temperature was increased to upper incipient lethal
levels. Coho swimming speeds were reduced to approximately 91% of maximum at these
temperatures. This information reveals a decline in performance when acclimation temperature
increases above optimal levels. The percentage decline in swimming performance appeared to be
Summary of Technical Literature Examining the Phjsiological Effects of Temperature
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greater in sockeye than in coho. However, upper incipient lethal levels would not permit
indefinite swimming because lethal effects would emerge. In addition, sublethal effects such as
energy depletion and exhaustion would likely occur. Although swimming performances of adults
would be expected to follow a similar pattern (i.e., optimum at an intermediate temperature with
decline at higher and lower temperatures), adults are much more sensitive to thermal stress than
are juveniles (Becker 1973).
How do temperature and oxygen jointly affect juvenile swimming speed?
Davis et al. (1963) found that as oxygen concentrations declined below 9.0 mg/L, maximum
swimming speed of coho was reduced. Swimming performance increased from 59°F to 68°F (10-
20°C), as noted in the previously cited studies by Brett (1958). Dahlberg et al. (1968) studied
coho final swimming speed at 68°F (20°C) under various oxygen concentrations and found a
dramatic reduction in swimming speed below a dissolved concentration of 7-8 mg/L. With a DO
of 5 mg/L (53% saturation) swimming speed was reduced 10% below maximum. Further
reductions in DO caused a precipitous reduction in final speed (See Temperature Interactions
issue paper for additional detail on effects.)
How are physiological optimum, growth optimum, preferred temperature, swimming
maximum, and metabolic scope derived?
The physiological optimum is derived by averaging the growth optimum and preferred
temperature (Brett 1971). Preferred temperature also is correlated with the temperature
providing the maximum metabolic scope. This, in turn, is related to the temperature providing the
maximum critical swimming speed (Kelsch and Neill 1990). Swimming speed is highest at the
preferred temperature (Kelsh 1996).
How can allocation of energy to metabolism and swimming be used to interpret fitness
and resistance to disease?
The standard metabolic rate (SMR) is calculated in terms of oxygen consumption
extrapolated to zero activity and indicates the resting metabolic rate of unfed fish(Priede 1985).
The scope for activity defines the performance capacity of the organism. The rate of oxygen
consumption at the maximum aerobic swimming rate defines the active metabolic rate (Priede
1985, Evans 1990), which is that found for a fasted fish swimming at critical speed (Beamish
1978, Kelsh and Neill 1990). The specific dynamic action (SDA) is the metabolic rate attributable
to digestion of a meal. In fish, feeding and peak digestion tend to be cyclic and are correlated
with water temperature and photoperiod. In addition, power (i.e., the short-term allocation of
metabolic resources, see Priede 1985) devoted to SDA is related to the size and quality (e.g.,
protein content) of the meal consumed. Therefore, the power demand for SDA varies and
consumes variable portions of the available energy defined by the scope for activity. In ecological
terms, the greater the available power at any given temperature in excess ofthe basic demands of
SMR and SDA, the greater the fitness (Evans 1990). Fish operating under a temperature that
allows only a small power output in excess of SMR and SDA needs have little ability to deal with
additional power demands caused by disease, the need to apply burst swimming to escape
predators or swim against currents, and so on. The seriousness of this situation is reflected in the
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danger of feeding cultured fish at high temperatures, despite the fact that more energy is required.
With the heightened power demand for SDA at high temperatures, any unnecessary stress can
lead to metabolic power overload and mortality (Priede 1985).
In addition to the correlation between the maximum scope for activity and preferred
temperatures, median survival has other ecological importance. Survival of an individual fish is
probably maximized by temperatures in the mid-range of its scope for activity. The temperature
range that maximizes scope for activity tends to be correlated with the center of distribution of the
species and maximum production. The ability of the organism to adapt to its thermal environment
is related to its ability to maximize available power (Evans 1990).
How do temperature, light intensity, andphotoperiod influence swimming speed?
A plot of prolonged swimming performances for a variety of species relative to temperature,
as summarized by Beamish (1978), indicates that sockeye attain maximum speed at 59°F (15°C),
whereas coho and lake trout reach maximum prolonged swimming speeds at approximately 62.6-
64.4°F (17-18°Q.
Diel changes in swimming speed by factors of approximately 2-3 have been observed in
sockeye in coastal waters (Madison et al. 1972) and chinook in the Columbia River (Johnson
1960); speeds were lower at night than during the day. Quinn (1988 as cited by Quinn et al.
1997) also reported that sockeye swimming speeds were lower in coastal waters at night. Light
intensity or photoperiod apparently provides a behavioral regulation of swimming speed.
However, Hatch et al. (1993), using video time-lapse recording, detected significant adult sockeye
movement past Zosel Dam on the Okanogan River between 2000 and 0600 h. In fact, most
passage occurred during nighttime. Such was not the case at Tumwater Dam on the Wenatchee
River, where daytime passage was predominant. Sockeye on the Okanogan can apparently take
advantage of nighttime passage. Provided that nighttime water temperature is lower than daytime
temperature, sockeye might escape significant thermal stress. High net migration rates (up to 3.4
km/h) were observed in these sockeye populations (Quinn et al. 1997), which could either
decrease exposure time to thermal stress or produce dangerous levels of fatigue under warm river
conditions.
How do fish size and acclimation temperature affect swimming?
Small-size sockeye held a swimming advantage relative to larger size sockeye over the
length range 8-60 cm (Brett and Glass 1973). That is, critical swimming speed (60-min sustained
speed) was 6.7 body lengths/s at the smallest size and decreased to 2.1 body lengths/s at the
maximum size when measured at 68°F (20°C).
Swimming performance also depends on prior acclimation temperature in relation to
exposure temperature. This effect can be measured in acute temperature exposure tests. Griffiths
and Alderdice (1972) found that for juvenile coho over a temperature range of approximately
35.6-77°F (2-25°C), a low acclimation temperature of 35.6°F (2°C) produced maximum critical
speed (5 lengths/s) at a test temperature of 57.2°F (14°C). As acclimation temperature was
increased, so did the test temperature producing the maximum critical speed At an acclimation
Summary of Technical Literature Examining the Ph>sioIogical Effects of Temperature
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temperature of 68°F (20°Q, a test temperature of 68°F (20°C) produced a critical speed of 6.0
lengths/s. Critical swimming speed declined dramatically as test temperature was increased above
68°F (20°C). An acclimation and test temperature of 68°F (20°C) provided the highest critical
swimming performance (Griffiths and Alderdice 1972). For juvenile coho salmon a temperature
of 68°F (20°C) appeared to provide maximum metabolic scope and swimming speed, given
unlimited food.
Can disease affect swimming speed?
Tests of critical swimming performance on Fraser River adult sockeye at 66.2-69.8°F
(19-21 °Q indicated that diseases, including fungal infections, reduced swimming speed 35% from
control conditions (Jain et al. 1998, as cited by Macdonald et al. in press).
What is known about swimming speed for three species of char?
Beamish (1980) measured critical swimming speed for three species of char: arctic char,
Salvelinus alpinus; brook trout, S.fontinalis; and lake char, S. namaycush, at 41, 50, and 59°F
(5, 10, and 15°C). Median critical swimming speed for each species increased with temperature
over the range of 41 to 59°F (5-15°C). Swimming performance and oxygen uptake decreased as
temperatures exceeded 59°F (15°Q.
Can swimming act as an indicator of sublethal stress?
Swimming performances have been suggested for assessing sublethal effects of water quality
(temperature and other combined pollutants) on fish (Brett 1967, as cited by Beamish 1978).
Upstream migration requires a combination of all three modes of swimming (sustained,
prolonged, and burst). Swimming to exhaustion in coho requires up to 18-24 h for complete
recovery (Paulik et al. 1957). After 3 h of rest, recovery is only 67% complete. Exhaustion may
be produced by repeated attempts to negotiate falls or fish ladders, escape predators, or struggle
against the line of a sport angler. But Iowa- energy reserves, decreased scope for activity, or
unacceptable delays in reaching holding or spawning areas because of need for metabolic recovery
mean that the cumulative effect of swimming stress may result in prcspawning mortality or
reduced reproductive success.
How are adult swimming speeds and migration rate related?
Brett (1965 as cited by Brett 1983) plotted the swimming efficiency of 2.3-kg sockeye as the
energy cost (kcal/kg/km) vs. swimming speed (km/h). Low speeds (<1 knVh) required too much
energy expenditure because of the large metabolism requirement in a prolonged migration period.
Intermediate speeds (1.0-2.6 km/h) had the least energy expenditure. Optimum efficiency was
achieved at 1.8 km/h. Interestingly, the mean current velocity of the Columbia River is 7 km/h,
whereas maximum sustainable swimming speed is 5 km/h. The energy expenditure observed in
sockeye was equated to a swimming speed of 4.3 km/h by Brett (1965 as cited by Brett 1983).
This implies that sockeye must be able to travel largely in low-velocity currents to conserve
energy. Fastest migration speeds, determined by radio tracking in mid-run spring chinnok in the
Willamette River (late May-early June) were 1.8 km/h, although most of the migration occurred at
Summary of Technical Literature Examining the Ph>siological Effects of Temperature
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speeds of 1.3-1.7 knVh at 55.4-66.2°F (13-19°C) (Schreck et al. 1994). Further investigation of
energy and swimming speeds is needed because the total distances traveled are uncertain. Adult
salmonid migration can involve considerable downstream and upstream expbration for a given
net distance traveled upstream (Schreck et al. 1994). If frequent fall-back through dams occurs,
total travel distances and energy expenditure could become great, placing the individuals in
considerable biocnergetic stress.
Recent studies using EMG radio telemetry on volitionally swimming adult sockeye in the
Fraser and Nechako Rivers in British Columbia revealed the average swim and migration speeds
in different river reaches that presented various migration challenges attributable to channel
constriction. Average swim speeds in these reaches varied from 1.8 to 4.5 km/h. Migration
speeds in these same reaches ranged from 0.2 to 2.2 km/h (Hinch and Rand 1998). Swim speeds
were nuch more constant than migration speeds, indicating that sockeye have a preferred or
optimum swim speed (Hinch and Rand 1998). However, application of EMG telemetry at Hell's
Gate, a major constriction in the Fraser River, showed that adult sockeye that were unsuccessful
at passing this impediment swam for prolonged periods at speeds exceeding critical velocity,
depleted energy reserves, and required prolonged recovery periods (Hinch and Bratty 2000).
Although complex flow conditions associated with channel constrictions and fish ladders can lead
to fatigue in unsuccessful upstream migrants, low oxygen concentration and high temperature can
reduce the success rate even further (Hinch and Bratty 2000). By modeling bioenergetics of
sockeye swimming up the Fraser River and accounting for the temperature variations as
experienced over a 44-year period in which maximum temperatures of 69.8°F (21 °C) occurred
periodically, it was determined that 8% ofthe sockeye run over this time period was subject to
energy depbtion and prespawning mortality (Rand and Hinch 1998). Because as much as 20% of
initial energy must be conserved to complete spawning, factors that contribute to energy depiction
(high temperature, high velocity flows, passage barriers and constrictions, confusing flow
patterns) need to be reduced.
Adult Migration to Reproduction
What temperatures are associated with migration?
Migration is generally considered to occur or be feasible to some extent for summer and fall
chinook at 57-68°F (13.9-20.0^) and 51-66.9°F (10.6-19.4°C), respectively (Bell 1991).
However, a migration threshold at a temperature of 69.8-71.6°F (21-22°C) is documented by
numerous studies across major migratory salmonid species in the Columbia River (Table 3).
Summer water temperatures in many streams of the Pacific Northwest can be high enough to
cause migration difficulties. The Snake River provides an example. In each of the Snake River
reservoirs there is an approximately 2-month period during which water temperatures exceed
69.8°F (21°C) (Dauble and Mueller 1993, p. 39). At Lower Granite reservoir this period extends
from mid-July to mid-September. This period in which water temperature exceeds adult
migration thresholds overlaps the adult migration periods of summer chinook, fall chinook,
sockeye, and summer steelhead (Dauble and Mueller 1993, Fish Passage Center data sheet) (also
see Table 7) and the smolt outmigration of fall chinook and sockeye at Lower Granite Dam (Fish
Passage Center 1998). Even spring chinook migration to spawning grounds can be inhibited for
SummaryofTechnical Literature Examining the Physiological Effects of Temperature 72
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continuous periods of more than 2 months by temperatures in major tributaries of the Snake (i.e.,
Tucannon River) (Bumgarner et al. 1997). Chinook, sockeye, and steelhead of the Snake River
Tabic 7. Adult migration period for chinook and stcclhcad
Reservoir
Spring chinook
Summer chinook
Fall chinook
Steelhead
Ice Harbor
4/1-6/8
6/12-8/11
8/12-10/31
4/1-10/31
Lower Monumental
4/1-6/13
6/14-8/13
8/14-10/31
4/1-10/31
Little Goose
4/14-6/15
6/16-8/15
8/16-11/15
4/1-10/31
Lower Granite
3/1-6/17
6/18-8/17
8/18-12/15
4/1-10/31
Note: Adult sockcjc passage at Lower Granite Dam extends from June 15 to August 20 (Dauble and Mueller 1993).
Steelhead migration includes the group A run from April 1 to August 25 and the B run from August 26 to October 31.
are all listed under the ESA as either threatened or endangered, migrate during periods affected by
warm water, and require consideration for their migration success and survival.
Fall chinook historically entered the Snake River from late August through November with a
peak in September (Snake River Subbasin Plan 1990). At Ice Harbor Reservoir during 1990,
water temperatures were 73.4°F (23°C) on August 15 (i.e., the initiation of the migration period)
but declined to only 71.6°F (22°C) by September 16 (Karr et al. 1992). As an example of the
problem posed for fall chinook migration, 1990 water temperatures in Lower Granite Reservoir
peaked on approximately August 13 at 77°F (25°C) and gradually declined to about 69.8°F
(21°C) by September 16 (Karr et al. 1992). Temperature histories for Snake reservoirs such as
these indicate that migration blockages of 4 wk can occur. Since September 1990, attempts have
been made to reduce Snake River reservoir temperatures by releasing water from Dworshak
Dam. Releases of cold water of up to 14 kefs have been made to improve fish migration and
survival.
Periodic inability to migrate because of high water temperatures was almost certainly one of
a number of environmental challenges presented to salmon under historic conditions. However,
unimpounded rivers have thermal regimes that are different from those of impounded rivers. Even
if a free-flowing river experienced a maximum daily temperature that impeded upstream
migration, it would not have continuous temperatures beyond the migration threshold, nor would
they be present for many consecutive days. A healthy stream system would provide abundant
cold-water refuges along the entire migration route. Large reservoirs on mainstem rivers, channel
alterations (loss of pools via removal of large woody debris or sedimentation, channelization), and
altered cold-water input sources (e.g., wetland loss, interception of shallow groundwater flow by
the road system) lengthen exposure to temperatures that could block migration, shift maximum
temperatures to later in the year, eliminate cold-water refuges, result in more constant daily
temperatures, and heat river margin habitats (Coutant 1999). These habitats would be best for
Summary of Technical Literature Examining the Physiological Effects of Temperature
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juvenile rearing (especially fell chinook migrating slowly to the ocean), if not for the high
temperatures present during summer and early autumn months.
If adults or smolts were able to seek colder water at depth, they could avoid the migration
barriers. However, there is very little temperature stratification in the reservoirs (Bennett et al.
1997, Karr et al. 1998). Adult salmon in the vicinity of the Snake River mouth are known to hold
in the much cooler Columbia River to avoid adverse temperatures. However, they have a limited
opportunity to then migrate through the Snake River, find a mate, and spawn. This window is
predetermined by their stored body energy, their maturation during holding, and their need to
deposit eggs in sufficient time for development and emergence. Although salmon have some
inherent flexibility in their life c>cle, this can easily be overwhelmed by stresses imposed in river
management. In addition, salmon's range of tolerance to high temperatures in their environment
can easily be exceeded, lowering their survival.
The year 1998 set record high temperatures throughout the Fraser River Watershed in
British Columbia, Canada. It also set records for high losses to the river's sockeye salmon run.
Macdonald et al. (in press) evaluated the effects of temperature, flows, disease, and other
stressors to determine the likely cause of the estimated in-river loss of 3,394,000 adult fish and
increased prespawning mortality in some early-run stocks. Temperature was the main cause of
both en route and prespawning losses to the 1998 Fraser River sockeye runs. Mean daily water
temperatures at Hell's Gate (a lower mainstem site) were the highest recorded for most days
during the summer of 1998, frequently exceeding 68°F (20°C) in late July and early August
(warmest mean summer temperatures in the 51 years of record). From their review of the
historical database, the authors suspected that losses in spawning runs occur when mean river
temperatures exceed 62.6-64.4°F (17-18°C) for prolonged periods. They noted that chinook
salmon also appear susceptible to high temperatures in the Fraser River system In 1998
unusually large losses (25% of population) occurred in the South Thompson River, where
summer mean temperatures were frequently above 68°F (20°C) and reached a high of
approximately 73.4°F (23°Q. The only other >ear with reports of large chinook fosses was 1994,
also an unusually warm year.
Migration stress and reproductive impairment in salmon populations may result from the
cumulative effects of exposure to less than optimum environmental conditions. Macdonald et al.
(in press) suggested that migration blockages, susceptibility to disease, impaired maturation,
increases to stress parameters, reduced efficiency of energy use, and reduced swimming
performance are all more common as daily mean temperatures exceed 62.6°F (17°C). The
authors found that measuring physiological indicators of stress and reproductive condition is
useful in evaluating the effects of temperature on migratory sockeye salmon.
How can stress during migration affect later reproductive success in salmonids?
Macdonald et al. (in press) monitored stress and reproductive state in both prespawning and
postspawning sockeye from the Horsefly River stock (midsummer run). The Horsefly River stock
entered the Fraser River during the warmest period of the year. During migration to the spawning
grounds, temperatures were well over 68°F (20°C). Four stress parameters and three
reproductive parameters were examined. In addition, some of the fish collected were artificially
Summary of Technical Literature Examining the Physiological Effects of Temperature
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spawned and their eggs placed in capsules in the gravel of their natal stream and examined to
determine both fertilization and hatching success.
In 1998, Horsefly sockeye (midrun stock) females had plasma Cortisol levels (a primary
indicator of stress) that reflected exposure to acute stress and that were generally higher than
those in other migrating Fraser River sockeye stocks in previous years. The levels of lactate (a
secondary indicator of stress) in Horsefly salmon at all reproductive stages examined showed that
these fish had engaged in stressful exercise even though the flow rates in 1998 were substantially
lower than in 1997, when water flows created very challenging migration conditions. There were
several indications that the early portion of the 1998 Horsefly run was suffering from impaired
maturation. Many of the females, particularly those in poor condition, had low estradiol and
progesterone levels, possibly from high-temperature stress that caused suppression of estrogen
synthesis and an inability to switch to the synthesis of 17,2 OP (an indicator of final maturation in
males and females). These processes are known to be linked. Testosterone (an indicator of
maturation in males and females) also was depressed in females in poor condition, further
evidence that these fish would probably not reach maturity or spawn viable eggs. Elevated but
sublethal temperatures are known to negatively affect secretion of the hormones controlling
sexual maturation in sockeye salmon in the Fraser River. The likely physiological consequences
of these reduced hormone levels are poor spawning success, poor egg quality and viability, and
senescent death prior to spawning. All three of these reproductive impairment problems were
evident in 1998 in each of the stock groups.
What temperatures are recommended for holding?
Hatchery managers have long known that highest survival of chinook adults occurs when
water temperatures do not exceed 57.2°F (14°C) (Leitritz and Lewis 1976, Piper et al. 1982).
Fish (1944) reported very high holding survival of sockeye when temperatures were <60°F
(15.6°C), but survival was only 51% under a fluctuating regime of 48.9-73.9°F (9.4-23.3°Q.
Can temperature affect viability of gametes developing in adults?
Temperature can influence the reproductive success of fish well before spawning.
Prespawning effects can be separated into at least two time periods: before ovulation and after
ovulation. Before ovulation, reproductive success can be hampered by mortality to the adult
spawncr (Andrew and Geen 1960, Bouck et aL 1975, Schreck et al. 1994, Cooper and Henry
1962, as cited inGilhousen 1980) and interference with ovulation and spermatogenesis. After
ovulation, reproductive success can be harmed through decreased egg and sperm fitness and
reduced embryonic survival rates. Here we discuss only the impact of temperature on ovulation
and subsequent egg survival.
Hatchery managers have bng known that highest survival of chinook adults occurs at water
temperatures less than 57.2°F (14°Q (Leitritz and Lewis 1976, Piper et al. 1982). When adults
hold in higher water temperatures, egg survival increasingly declines (Hinze 1959, Hinze et al.
1956, as cited by Marine 1992).
After ovulation in females and sperm maturation in males, the effect of elevated water
Summary of Technical Literature Examining the Physiological Effects of Temperature 75
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temperature on rainbow trout egg and sperm viability becomes important (Billard 1985). Holding
females at 68°F (20°C) for 70 h reduced viability of eggs held in the body cavity, compared with
holding females at 50°F (10°Q (Billard and Breton 1977, as cited by Billard 1985). To promote
female maturation and egg development, holding at temperatures from 42 to 55.9°F (5.6-13.3°C)
is essential (Leitritz and Lewis 1976).
Smith et al. (1983) and Piper et al. (1982) cited work demonstrating that rainbow trout adult
broodfish should beheld at temperatures below 53.9-55.9°F (12.2-13.3°C) before spawning to
produce good-quality eggs, whereas holding temperatures above 55.4°F (13°C) have been found
to reduce in vivo postovulatory egg survival (Flett et al. 1996, Billard and Gillct 1981, as cited in
Billard 1985). Temperatures of 64.4°F (1 8°C) or higher were found to reduce the volume of male
sperm, and a temperature of 68°F (20°C) was found to cause a drop in egg fertility in vivo to 5%
after 4.5 d (Billard and Breton 1977). At 50°F (10°C), fertility of the eggs held in the hen trout
remained high. Saki et al. (1975, as cited in de Gaudemar and Beal 1998) found that embryonic
and posthatching survival in O. mykiss decreased significantly if eggs remained ripe in the body
cavity for more than 5-7 d after ovulation, and fertility could approach zero after 2 wk (Stein and
Hochs 1979, as cited inde Gaudemar and Beal 1998).
When ripe adult chinook females were exposed to temperatures beyond the range 55.9-60°F
(13.3-15.6°C), prespawning adult mortality became pronounced and survival of eggs to the eyed
stage decreased. Prespawning adults exposed to prolonged temperatures of 60-62°F
(15.6-16.7°C) had survival of eggs to the eyed stage of 70% when incubated at 5 4.8- 55.9 °F
(12.7-13.3°C) and survival of 50% when incubated at 60-62°F (15.6-16.7°C). Adults exposed to
55-59°F (2.8-15°C) water temperature had egg survival of 80% to the eyed stage when then
incubated at the same temperatures (Hinze 1959, as cited by CDWR 1988). The highest survival
of eggs (95%) to the eyed stage was in those taken from adults held at 53-53.9°F (11,7-12.2°C)
(Hinze et al. 1956 as cited by CDWR 1988). Eggs taken from chinook held at constant
temperatures >55.4-59°F (13- 15°C) have poor viability (Hinze et al. 1956, as cited by Marine
1992, Rice 1960, Leitritz and Lewis 1976).
Berman (1990) held adults at 63.5-66.2°F (17.5-19°C) for a 2-wk period before spawning.
Control fish were held at 57.2-59.9°F (14-15.5°C). Progeny ofthe elevated treatment group had
higher prehatch mortality and a much greater rate of developmental abnormalities than the control
group. In addition, alevin weight and length were less in the elevated group. The smaller alevin
size could be attributable to the smaller size of eggs in the elevated group. It is interesting that
even though no differences were observed in fertilization rates of eggs between the elevated and
control groups, numerous delayed effects occurred.
Two coho stocks migrating to spawning grounds in eastern Lake Erie had very different
survival of embryos to hatch, attributable to the water temperatures on the migration route. The
stock that migrated in waters >59°F (20°C) in mid-August to early September had deformed eggs
with mean survival rates to hatching of low to 0%, depending on the year. The neighboring stock
had very little warm shoal water to traverse during migration, were exposed to temperatures 3.6-
7.2°F (2-4°C) lower, and had normal eggs with high viability (84% embryo survival) (Flett et al.
1996).
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Hokansonet al. (1973) measured a significant effect of prespawning temperature exposure
on brook trout broodstock. When brook trout were spawned at 50.7°F (10.4°C) or at 55.7°F
(13.2°C) and subsequently reared at 50°F (10°C), percentage of normal hatching was 65% and
38%, respectively. When brook trout were spawned at 50.7°F (10.4°C) or 55.7°F (13.2°C) and
subsequently reared at 60.8°F (16°Q, percentage of normal hatching was 0% in each case.
Percentage of normal hatching was >90% at constant incubation temperatures of 40.8-46.4°F (6-
8°C) and declined steadily to 0% at 60.8°F (16°C). The highest percentage of viable eggs per
female was found at 46.4°F (8°C). An increase in spawning temperature from 50 to 60.8°F (10-
16°C) resulted in a steady decline to near zero in spawnings per female, viable eggs per female,
and total eggs per female. The temperature range 42.8-60.8°F (6-16°C) may represent the right
portion of a bell-shaped survival curve. This study provides important evidence that adult holding
water temperatures and temperature at fertilization are as important as incubation temperature in
determining egg viability. In female brook trout the maximum temperature for maturation and
ovulation is 60.8-66.2°F (16-19°C). Males can achieve functional maturity at temperatures as
high as 62.2°F (19°C). However, at 66.2 °F (19°C) development of ova becomes inhibited and
ova can be resorbed. Hokanson et al. recommended that for brook trout in the month prior to
spawning, maximum water temperature should be <66.2°F (19°C) and mean temperature should
be <60.8°F (16°C). During the breeding season maximum water temperature should be <53,6°F
(12°C). Optimal spawning activity, gamete viability, and embryo survival would take place at
mean spawning temperatures <48.2°F (9°Q.
Egg survival during egg development has also been studied in rainbow trout. Postovulation
survival of eggs in the body cavity of rainbow trout females held at >55.4°F (13°C) was rruch
lower than at lower holding temperatures (Billard and Gillet 1981, as cited by BiHard 1985).
Forced delays in spawning, such as are frequently caused by difficulties in passing dams, can
cause decreases in reproductive success. In Atlantic salmon a delay in spawning from any source
causes overripening in females. Prolonged holding of eggs after ovulation reduces egg viability
and increases retention and malformation. As little as a 1-wk delay in spawning after full
maturation causes a marked reduction in egg quality (de Gaudemar and Bcall 1998).
In addition to the effects on egg viability caused by holding adult female salmon at elevated
water temperature (>59-60.8°F [15-16°C]), warm water can also lower viability of eggs of
nonanadromous salmonid adults by influencing their nutrition during their feeding period (see
Hokanson 1977). A lowered food intake leading up to egg deposition, when growth is normally
rapid, may accompany elevated water temperature. Poor growing conditions for salmonids that
achieve maturity in freshwater can result in poor reproductive success (Coutant 1977). A rapid
decline in quality of rainbow trout eggs within the body cavity after ovulation has been reported at
holding temperatures of 55.4-59°F (1 3-15°C) by numerous authors (see citations in Flett et al.
1996, Billard 1985, Smith et al. 1983). Cutthroat females held at tenperatures fluctuating from
35.6 to 50°F (2- 10°C) produced eggs of significantly higher quality than females held at 50°F
(10°C) (Smith et aL 1983).
Bouck et al. (1975) studied survival of sockeye acclimated to 55.4°F (13°Q and adjusted to
test temperatures at a rate of 3.6°F (2°C)/d. Adults holding at a test temperature of 71.6°F
(22°C) died after 3.2 d from thermal effects. Holding for 11.7 d at 68°F (20°C) resulted in 100%
Summary of Technical Literature Examining the Physiological Effects of Temperature 77
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mortality from indirect thermal effects (infection by columnaris). Fish held at 61.7°F (16.5°C) had
lower health and reproductive indices than fish held at 50°F (10°C). Among these indices were
the absence of fat reserves at 61.7°F (16.5°C) vs. abundant reserves at 50°F (10°C), the doubling
of weight loss, enlarged liver, and reduced egg size at the higher temperature. The noninfectious
pathology at 61.7°F (16.5°C) occurs precisely during the major period of reproductive
development in the Columbia River. For these reasons, Bouck et al. concluded that 50°F (10°C)
was more favorable for maturing sockcye than61.7°F (16.5°C), and in addition, did not subject
these fish to the greater risk of thermal death and disease associated with 60.8 and 68°F (16 and
20°C) holding.
Water temperatures can speed up, slow down, or stop entirely the ripening of gonads and
ovulation in fish (Flett et aL 1996, Gilhousen 1990, Gillet 1991 as cited in Baroudy and Elliott
1994, and Reingold 1968 as cited in Bailey and Evans 1971). Billard and Breton (1977) found
that temperatures as high as 64.4°F (18°C) had no adverse effect on male rainbow trout
spermatogenesis, but sperm volume and gonadotrope secretion were both higher at 50°F (10°Q
than at 64.4°F (18°C). At temperatures above 55.4°F (13°C), ovulation may still occur in
rainbow trout, but postovulatory egg survival in the body cavity is much shorter. Taranger and
Hansen (1993) used Atlantic salmon (Salmo salar) to test the timing of ovulation under different
temperature regimes. Water temperature was either increased from 50°F (10°C) to 55.4-57.2°F
(13-14°C) (warm water), decreased abruptly from 50°F (10°C) to 41-44°F (5-7°Q (cold water)
or gradually decreased from 50 to 46.4°F (10-8°C) (ambient control) from November 1 onward.
Median ovulation time was delayed by 5 wk in the warm-water group compared with ambient
controls, with 43% of the females remaining nonovulated at the end of the study. Only minor
effects were observed on timing of ovulation in the cold-water group compared with the ambient
controls. Survival of eggs to the eyed stage was significantly higher in the cold-water group
(92.1%) than in both the ambient control group (84.5%) and the warm-water group (76.6%).
The results indicate that high water temperature during the spawning season may inhibit ovulation
and have a detrimental effect on gamete quality. Morrison and Smith (1986, as cited in Taranger
and Hansen 1993) found that low water temperature delayed ovulation in winter spawning
rainbow trout and that an increase in water temperature could accelerate ovulation.
Although eggs in the body cavity of the female arc less sensitive than they are outside the
female (roughly several weeks compared with a few days) (Billard and Gillet 1981, Billard and
Breton 1977), once ovulation has occurred the quality of the eggs will begin to decline as they
overripen (Gillet 1991 as cited in Baroudy and Elliott 1994, Bouck and Chapman 1975, Flett et
al. 19%, Sakaiet al. 1987 as cited in Flett et al. 1996, de Gaudemar and Beal 1998). Bry (1981),
as cited in Flett et al. (1996), found that eggs retained in the body cavity after ovulation show a
high, significant decline in quality by 9-12 d after ovulation at 54°F (13°C). Escaffre et al. (1977),
as cited in Flett et al. (1996), reported a rapid decline in egg quality when water temperature
exceeded 57.2-59°F (14-15°C). De Gaudemar and Beal (1998) found that 8 d after ovulation in
Atlantic salmon, egg survival already seemed affected. In rainbow trout, Sakai et al. (1975), as
cited in de Gaudemar and Beal (1998), showed a decrease in embryonic and posthatching survival
if ova were kept more than 5-7 d in the abdominal cavity after ovulation. They also found that
after 15 d ova underwent a decrease in fertility, which could even be close to zero after 2 wk
according to Stein and Hochs (1979), as cited in de Gaudemar and Beal (1998).
Summary of Technical Literature Examining the Physiological Effects of Temperature
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Bouck and Chapman (1975) found that 50°F (10°C) would be more favorable for sexually
maturing adult sockeye salmon than 61.7°F (16.5°C). Body weight losses for females averaged
8.5% at 50°F (10°C) and 13.2% at 61.7°F (16.5°C). Although fat reserves were abundant in the
50°F (10°C) group, they were absent at 61.7°F (16.5°C). Higher temperatures, 61.7°F versus
50°F (16.5 vs. 10°C), were associated with advanced development of secondary sexual
characteristics (snout and dark skin) and diminished development of gonads. Females bore similar
numbers of eggs at 50 and 61.7°F (10 and 16.5°C), but eggs were 11 % less in weight in the
61.7°F (16.5°C) group, which was correlated with percentage body weight loss. Bouck (1977)
found results very similar to those reported in Bouck and Chapman (1975).
Exposure of ripe adults and eggs to water temperatures above 55.9°F (13.3°C) is commonly
assumed to result in greater than normal losses and abnormalities of young fish (Morat and
Richardson 1983, Weidlcin 1971, Dunham 1968, as cited in CDWR 1988). Rice (1960) tested
hatchery holding facilities to determine the best conditions for holding, spawning, and incubating
chinook salmon stocks from the American River in California He determined that a facility with
temperatures below 44.96°F (7.2°C) was too cold for successful incubation, but one with
temperatures ranging between 46.94 and 60°F (8.3 and 15.6°Q was satisfactory for egg
development.
Billard and Breton (1977) found that temperatures above 55.4°F (13°C) allowed ovulation
to occur in rainbow trout, but postovulatory egg survival time in the body cavity was much
shorter than at lower temperatures. The authors noted that in vivo survival of ovulated eggs (4 d)
in rainbow trout was high (approximately 95%) for 70 h at 68°F (20°C), but beyond this point
survival dropped rapidly and dramatically (to approximately 5% at 110 h). This demonstrated
that rainbow trout broodfish must be held at water temperatures not exceeding 55.9°F (13.3°C)
(preferably not above 53.9°F [12.2°C]) for a period of 2-6 months before spawning to produce
eggs of good quality (Smith et al. 1983 as cited by Bruin and Waldsdorf 1975, Leitritz and Lewis
1976).
Temperatures shown to affect salmonid egg quality vary. Ffctt et al. (1996) suspected that
the low survival to hatching observed in adult coho salmon migrants was caused by traveling
through waters warmer than 68°F (20°C). Temperatures greater than 60°F (15.6°C) were noted
to decrease egg survival and contribute to coagulated yolk in sac-fry (Hinze et al. 1956 as cited by
CDWR 1988, Olson and Foster 1957). Greatest survival occurred in eggs taken from fish when
water temperature was in the 53.1-54°F (11.7-12.2°C) range. Furthermore, it was noted that
early embryonic damage may be manifested during the latter part of the fry stage and just after
feeding has begun in the fingerling stage, so rates of survival to hatching may underestimate the
detrimental effect of prespawning temperatures. Rice (1960) found that holding broodstock in
hatchery waters that were consistently above 60°F (15.6°C) reduced survival of eggs to the eyed
stage by 12.7% compared with holding the broodstock between 46.9 and60°F (8.3-15.6°Q.
Bouck et al. (1970, as cited in EPA and NMFS 1971), however, found no apparent adverse
effects on coho salmon eggs in utero after prolonged exposure of adult fish to 62°F (16.7°C).
When females hold in warm water, eggs tend to be smaller with less stored energy, which means
less energy for alevin development and the necessity for earlier feeding to sustain life. Berman
and Quinn (1989) cited a personal communication with B. Ready, the manager of the Kalama
State Fish Hatchery, showing egg mortalities of 50% or more from adults held in river waters
Summary of Technical Literature Examining the Physiological Effects of Temperature
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fluctuating from 57.9 to 66.9°F (14.4-19.4 °C). The current supervisor of the Kalama Falls
Hatchery, Ron Castaneda, acknowledges that they incur some increased losses at holding
temperatures around 60-64°F (15.6-17.8°C), but they have not had mortality as high as 50%. It is
perhaps useful to note that this hatchery incubates in the natural river water as well.
In an unpublished 1995 study, Dr. Craig Clarke (cited in Macdonald et al. in press) exposed
early Stuart sockeye salmon captured at Hell's Gate to two temperature treatments (59 and
66.2°F [15 and 19°C]) for 2 wk. Two weeks of exposure to 66.2°F (19°C) in the laboratory
reduced plasma testosterone levels significantly in both sexes compared with 59°F (15°C)
exposure. Levels of 11-ketotestosterone and estradiol were low and below the detection limit in
many fish at 66.2°F (19°C). Furthermore, circulating levels of the major hormones controlling
sexual maturation were also depressed at 62.2°F (19°C). Similarly, Manning and Kime (1985 as
cited in Macdonald et al. in press) found that steroid biosynthesis was suppressed in rainbow trout
testes at 62.6°F (17°C). Clearly, the potential for suppression of sexual development and
intergenerational impairment existed in 1998 when migration temperatures exceeded 62.2°F
(19°C) at many locations and times. This possibility was supported further by an experimental
assessment of the spawning success of the early Stuart and Horsefly stocks. Macdonald et al. (in
press) monitored stress and reproductive state in both prespawning and postspawning sockeye
from the Horsefly River Stock (midsummer run). The Horsefly River stock entered the Fraser
River of British Columbia during the warmest period of the year. During migration to the
spawning grounds, temperatures were well in excess of 68°F (20°C). Four stress parameters and
three reproductive parameters were examined. In addition, a portion of the fish collected were
artificially spawned and their eggs placed in capsules in the gravel of their natal stream and
examined to determine both fertilization and hatching success. Fertilization success was found to
be lower in 1998 than in 1997. Horsefly fish that arrived on the spawning grounds in early 1998
suffered even lower fertilization success rates than the Stuart fish, and only 10% of their eggs
hatched Egg hatching success (but not fertilization success) was influenced by the condition of
the spawning female as estimated by stress and reproductive parameters. Females that arrived late
tended to have lower levels of testosterone and spawned eggs that hatched more successfully.
These late arrivals likely experienced less severe water temperatures during their entire migration
than did early fish. The likely difference at Hell's Gate was that mean daily temperatures were
64.4-66.2°F (18-19°C) versus 69.8-71.6°F (21-22°C). These observations suggested that the
upper threshold temperature for successful migration lies between 64.4 and 71.6°F (18 and 22°C).
Based on the information revbwed above, it can be concluded that holding migratory fish at
constant temperatures above 55.4-60.1°F (13-15.6°C) may impede spawning success. Maximum
constant temperatures of 50-54.5°F (10- 12.5°C) may provide better reproductive conditions in
most salmon and trout.
How is survival of prespawning adults affected by water temperature?
Leitritz and Lewis (1976) and Piper et al. (1982) recommended chinook broodstock holding
temperatures of42.8-57.2°F (6-14°Q. Conventional hatchery practice is to consider chinook
broodstock thermally stressed at temperatures >59°F (15°C); survival declines dramatically when
temperatures exceed 62.6°F (17°C) (Marine 1992). Raleigh et aL (1986) described adult chinook
prespawning temperatures as maximal in the range 46.4-54.5°F (8-12.5°C) but declining to zero
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
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at 75.2°F (24°C). A study by Fish (1944) revealed that adult chinook survival under fluctuating
temperature regimes of48.9-73.9°F (9.4-23.3°C) (mean = 10.8°F [16°C]) was only 36%, but at
52-60°F (11.1-15.6°C) (mcan= 53°F [11.9°C]) survival was 75% after holding in ponds for
approximately 2 months. This study highlights the benefit of holding adults under cold water
temperatures to promote survival. However, in this Grand Coulee Fish Salvage Program, disease
outbreaks (especially columnaris) in the holding pond environments made cold-water holding
particularly necessary to inhibit pathogens.
Prespawning mortality of wild spring chinook in the Warm Springs River varied from 34%
to 75% during the period 1977-1986. In 1980 and 1981 prespawning mortality averaged 74%.
BKD was implicated in this high mortality because it was responsible for mortality in the hatchery.
Even though all adults released to the Warm Springs River above the hatchery were inoculated for
BKD in 1982-1986, mortality was still high (24%-59%). In the Rogue River, Oregon,
furunculosis and columnaris were the primaiy cause of mortality of wild and hatchery adults from
1977 to 1981. Prespawning mortality in wild and hatchery fish was 12% and 36%, respectively,
during this period (Cramer ct al. 1985 as cited by Lindsay et al. 1989). Wild spring chinook in the
lower Rogue River exhibited high prespawning mortality in May-July 1992 as water temperature
ranged from 64.4 to 69.8°F (18-21°C) (M. Everson, ODFW, pers. comm., as cited by Marine
1992). The foregoing studies point out the variability of prespawning salmonid mortality in the
wild and the magnitude of disease effects observed under thermal stress.
What temperature ranges are associated with the adult spawning period?
There is conflict between the fish's inherent temperature preferences and its need to spawn
within a limited time frame. That is, given a prolonged high-temperature period during adult
holding, adults may be forced to spawn during adverse conditions, leading to poor egg and sperm,
embryo, alevin, or fry survival. For this reason, fish habitat managers must use discretion in
selecting suitable spawning temperatures. Even though fish may have been observed spawning
under warm temperatures, as during the initial days of the spawning period, there is no guarantee
that embryo survival is high for the early-spawning fish. There is some plasticity in timing of life
stage events relative to annual climatic patterns (i.e., if sufficient energy remains in the adult body
in the prespawning stage, some delay in spawning is feasible), and adjustments can be made
throughout the life cycle, but inability to compensate fully tends to be expressed as population
mortality, poor growth, reduced fecundity, and reduced fitness.
Spawning ofchinook in a wide variety of locations has been reported for a composite
temperature range of 35.9-66°F (2.2-18.9°C) (Mattson 1948, Burner 1951, both as cited by
Raleigh et al. 1986, Crawford et al. 1976 as cited by Vigg and Watkins 1991, Olson and Foster
1955, Chambers 1956 as cited by Andrew and Geen 1960, Snyder et al. 1966 as cited by Parker
and Krenkel 1969, Wilson et al. 1987). Recommended spawning temperatures for spring,
summer, and fall chinook given by Reiser and Bjornn (1979) and Bjornn and Reiser (1991) in
their literature review were 42-57°F (5.6-13.9°Q. These limits were extracted from Bell (1986).
EPA and NMFS (1971) recommended a maximum temperature of 55°F (12.8°C). Bell (1991)
gave a range of 42-57.5°F (5.6-14.2°C) as the preferred spawning zone, with 51.8°F (11°C) as a
preferred temperature based on an extensive summary of literature.
SummaryofTcchnical Literature Examining the Physiological Effects of Temperature 81
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What temperatures or thermal regimes are required to initiate spawning?
In autumn-spawning species such as the Pacific salmon, it can be assumed that the highest
temperatures associated with the spawning period are temperatures that allow spawning to be
initiated. For chinook, the extreme high temperature at spawning was 66°F (18.9°C). However,
egg survival at these temperatures cannot be assumed. In general, 60.4°F (16°C) is the maximum
associated with initiation of fall chinook spawning (Groves and Chandler 1999).
It has been reported that spawning is initiated when temperatures decline. Chambers (1956
as cited by Raleigh et al. 1986) found that spring chinook normally spawn as water temperature
declines from 55 to 40.1°F (12.8-4.5°C) and fall chinook spawn under a 56.1-41°F (13.4-5°C)
decline. The critical temperature threshold of approximately 55°F (12.8°C) and declining
temperature are apparently associated with ability to complete the spawning act, maximum
long-term viability of eggs and alevins, and better resistance to death by disease in adults and
eggs. Although prespawning mortality attributed to bioenergetic stress may be a significant factor
in overall adult mortality up to spawning time, it is uncertain how to separate disease and
bioenergetic stress effects.
Spawning can be initiated only under a limited temperature range. In the Hanford Reach of
the Columbia River, the median date for peak spawning was November 11, based on surveys from
1948 to 1992. On this date the mean weekly temperature was 54.5°F (12.5°Q and the maximum
weekly temperature was 57.2°F (14°C) (Dauble and Watson 1997). However, in both the
Hanford Reach and Snake River spawning zones, spawning activity begins as weekly mean water
temperatures decline below 60.8°F (16°C) and continues up to 41°F (5°C) (Groves and Chandler
1999). Because studies of egg survival and development after fertilization for chinook and other
salmon species indicate reduced survival under temperatures of 53.6-60.8°F (12-16°C), preferred
spawning temperatures of 55°F (12.8°C) (maximum) have typically been recommended (see EPA
andNMFS 1971, review of McCullough 1999). These data indicate that it is essential for
mainstem temperatures to decline rapidly below 60.8°F (16°Q so that spawning activities can
commence and also so that egg survival continues to improve during the spawning period.
Fall chinook, sockeye, and coho were all reported to spawn on falling temperatures starting
at peaks of51-55°F (10.6-12.8°C) (Chambers 1956 as cited by Andrew andGeen 1960).
Sockeye spawning success was only 45% when mean daily temperatures during spawning were
57.9-61°F (14.4-16.1 °C). On the Fraser River, spawning temperatures >55°F (12.8°C) were
associated with an increasing number of females that died without spawning (Andrew and Geen
1960). Temperatures >53.6°F (12°C) can inhibit or delay spawning by Atlantic salmon (Beall and
Marty 1983, as cited by de Gaudemar and Beall 1998). In the laboratory, brook trout spawning
was typically initiated at 50°F (10°C) but occurred under temperatures as high as 60.8°F (16°C)
(Hokanson et al. 1973). Spawning of brook trout begins to occur after the weekly mean
temperature falls below 55.4°F (13°C) (approximately early October). During the spawning
period, water temperatures steadily decline from approximately 55 to 44.8°F (12.8-7.1°C)
(Hokanson et al. 1973). Based on a survey of temperature effects on all aspects of spawning in
fall-spawning salmonids, it appears that spawning temperatures in the spring and fell chinook
spawning habitats having a 55°F (12.8°C) peak and that a declining trend would satisfy biological
requirements. Keying the spawning period to rapidly falling temperatures is common among
SummaryofTechnical Literature Examining the Physiological Effects of Temperature
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fall-spawning salmonids and has been documented for chinook of the Pacific Northwest (Groves
and Chandler 1999, Lindsay et al. 1986).
Although spawning for bull trout may begin as early as mid-August, spawning activity is
reported to be initiated when water temperatures begin to fall to 48.2°F (9°C) or lower (McPhail
and Murray 1979, Shepard et aL 1982, Kraemer 1994, Brenkemen 1998). Both the coastal
rainbow and the redband trout spawn in the spring, stimulated by rising water temperatures.
Behnke (1992) suggested that along the Pacific coast a water temperature of about 37.4-42.8°F
(3-6°C) may initiate some spawning activity, but spawning does not usually occur until
temperatures reach 42.8-48.2°F (6-9°C). Although this spawning activity would typically occur
from late December through April, in some very cold headwater streams local temperatures may
delay spawning until July or August for some stocks. Beschta et al. (1987) suggested that
rainbow trout spawn between 35.9 and 68°F (2.2 and 20°C), Bell (1986) set the range at 35.9-
66°F (2.2-18.9°Q, and Piper et al. (1982) concluded the range was 50-55°F (10-12.8°C).
Conclusions for spawning. Egg mortality, alevin development linked to thermal exposure
of eggs in ripe females or newly deposited in gravel, and egg maturation are negatively affected by
exposure to temperatures above approximately 54.5-57.2°F (12.5-14°C). Therefore, a spawning
temperature range of 42-55°F (5.6- 12.8°C) (maximum) appears to be a reasonable
recommendation for Pacific salmon, unless colder thermal regimes are natural in any tributary.
SUPPORTING DISCUSSION AND LITERATURE-LETHAL EFFECTS
What is the utility of UILT data and how has it been applied?
Upper incipient lethal temperature data were tabulated in NAS (1972) for juveniles and
adults of many fish species. UILT values for many salmonid species have since been added to the
literature; a cross-section is summarized in Table 4, extracted from McCullough (1999). The
UILT values correspond to the highest acclimation temperatures, and consequently, are very
similar to UUILT values. Given prior acclimation to temperatures lower than listed in the table,
however, the UILT values would likely be lower. This means that in the field, mortality can be
induced at temperatures significantly lower than UUILT levels.
Studies of the effect of elevated water temperature on survival of a wide variety of salmonids
using transfer to high constant temperature (UILT experiments) show much consistency among
species. In those tests in which acclimation temperature was 68°F (20°C) and the UILT was
approximately equal to the UUILT, UILT values found ranged from 73.4 to 80.6°F (23-27°Q.
Redband trout tend to be the most heat resistant of the salmonids; UILT values for all other
species ranged from 73.4 to 78.8°F (23-26°Q.
NAS (1972) recommended that for any acclimation temperature, short-term exposure be
limited to UILT (factor of safety, 3.6°F [2°C]). This assumes that at the UILT temperature, 50%
of the population would die within the test period (at least 1,000 min), but if the temperature is
reduced by 3.6°F (2°Q, no mortalities would occur in this time period. Although this assumption
may generally be valid, it also relies on no incidence of disease or other sublethal effects. When
SummaryofTechnical Literature Examining the Physiological Effects of Temperature 83
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this method was proposed, cumulative effects of repeat exposure to high temperatures were not
well known (see DeHart 1975, Golden 1975, Golden 1976, Golden andSchreck 1978).
Although temperatures of73.4-78.8°F (23-26°C) are generally considered the UUILT for
most salmonids, UILT values are typically 1.8-3.6°F (1-2°C) less than UUILT. The UILT values
are incipient lethal temperatures that correspond to acclimation temperatures lower than the
UUILT. Because we can never assume that fish in the field will be acclimated to the highest
acclimation temperature, the more appropriate lethal temperature in the field may be up to 3.6°F
(2°C) less than UUILT. The factor of safety would then have to be applied to this value, and
even then the additional sublethal or cumulative lethal concerns remain.
The 73.4-78.8°F (23-26°C) UUILT range for salmonids applies to the juvenile life stage.
Although information on salmon adults is much more limited, it indicates that adults are far more
sensitive than juveniles to high temperatures. Becker (1973) identified the thermal tolerance of
chinook jacks to be 69.8-71.6°F (21°-22°C) on the basis of a 168 h TLM test. Coutant (1970)
identified the incipient lethal temperature for chinook jacks as 71.6°F (22°C) with prior
acclimation to 66.2°F (19°C) (estimated from ambient river temperatures). Columbia River
steelhead, acclimated to a river temperature of 66.2°F (19°C) had a lethal threshold of 69.8°F
(21°C) (Coutant 1970). These lethal limits are 9.9°F (5.5°C) lower than for juvenile rainbow
acclimated to 64.4°F (18°C) (Alabaster and Welcomme 1962, as cited by Coutant 1972).
Servizi and Jensen (1977) found that the geometric mean survival times (GMST) for adult
sockeye were less than for juveniles. They also reported that the median survival times (MST) for
adult coho found by Coutant (1969) were similar to those of sockeye over the exposure range
80.6-86°F (27-30°C). The GMST for adult sockeye was 1,000 minat 75.2°F (24°C) with
acclimation at 60.4-64.9°F (15.8-18.3°C). Survival time at 78.8°F (26°C) was only 100 min.
Time to loss of equilibrium and survival time of adults were plotted vs. exposure temperature on
the same graph. The curve for loss of equilibrium was considerably lower than the time-to-death
curve. For this reason, Servizi and Jensen (1977) considered the loss of equilibrium temperature
more ecologically significant. Furthermore, because sockeye exposed to temperatures of
approximately 64.4-69.8°F (18-21°Q become highly susceptible to Flexibacter columnaris,
researchers took this temperature range as a greater thermal threat to continued stock survival.
Although UUILT or UILT temperatures are well known and consistent for the various
salmonids, they are probably not useful in setting temperature standards. Certainly they represent
the upper limits to tolerance, but salmonids in a stream system tend to be restricted to maximum
temperatures that are 3.6-7.2°F (2-4°C) lower than UILT values. In general, a maximum
temperature of 71.6-75,2°F (22-24°C) represents the normal upper temperature limit in the field
(sec McCullough 1999). As this limit is approached, juvenile density declines to zero. Using the
presence/absence threshold as a temperature standard for salmon habitat can only be done when
density Ls at or near zero.
Although the UILT has limited value in establishing the temperature standard itself, the a
and b coefficients for a given acclimation temperature are useful in estimating exposure times that
will result in 50% mortality. In addition, NAS (1972) recommended (MWAT) as an index to
tolerable prolonged exposures. This index was estimated as either:
Summary ofTechnical Literature Examining the Physiological Effects of Temperature 84
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[(opt. temp. + zng temp.)/2],
where the zng or zero net growth temperature is that temperature which results in zero net
growth of a population (i.e., subtracting tissue lost as population mortality from that added in
growth)
or
opt. temp. + (UILT - opt. temp)/3.
Each formula is based on the assumption that adequate growth rates can be maintained if the
weekly average maximum temperature falls between the optimum and the UILT or the zero net
growth temperature. However, the decline in growth rate can be very steep if temperature is
above the optimum. Consequently, limiting reductions in growth rates to, for example, 80% of
maximum levels can lead to much greater reductions in growth, given errors estimating the
relationship or managing temperature in a watershed.
Are there potential weaknesses in reliance on MWAT?
Hokanson et al. (1977) advised caution in using short-term exposure experiments to
calculate long-term exposures, such as with MWAT. They reported for O. mykiss that, given a
physiological optimum of 60.8-64.4°F (16-18°C) and a UILT of 78°F (25.6°C) (at 60.8°F [16°C]
acclimation), one would calculate an MWAT of 66.2°F (19°Q and a maximum temperature
(applying the 2°C safety factor of Coutant 1972) of 75.2°F (24°C) for short-term exposure.
Measurement of rainbow trout growth showed that at a fluctuating temperature of 71.6 ± 6.8°F
(22 ± 3.8°C) specific growth rate was zero. Under this temperature regime mortality rate was
42.8%/d during the first 7 d. For experiments within the optimum range (59.9-63.1 °F
[15.5°C-17.3°C] for a fluctuating regime), average specific mortality was 0.36%/d. Combining
data on specific growth and mortality rates, the authors were able to predict yield for a
hypothetical population under the temperature regimes. A rainbow trout population would
exhibit zero increase over a 40-d period (maintenance) at a constant temperature of 73.4°F (23°C)
and a fluctuating temperature with a mean of 69.8 ± 6.8°F (21 ± 3.8°Q because growth balances
mortality. Several sources report temperatures of69.8-73.4° (21-23°C) as the upper limit of
rainbow trout distribution in the field (Hokanson et al. 1977). Numerous authors have reported
upper limits to salmonid distribution as approximately 71.6-75.2°F (22-24°C).
With this laboratory information and corroborating field information, Hokanson et al. (1977)
recommended a mean weekly temperature of 62.6 ± 3.6°F (17 ± 2X1) for rainbow trout so that
maximum yield is not reduced more than 27% under normal fluctuating temperature regimes.
Production has been shown to be substantially reduced even just above the physiological
optimum. This paper has great significance. It was published 5 years after the National Academy
of Sciences recommended the use of MWAT to establish prolonged exposure temperatures. The
NAS acknowledged that growth rate should be expressed as net bi'omass gain or net growth.
Yield is that portion of the population available to humans; the remainder is lost as mortality,
which can be substantial if temperatures are high. Also, if temperatures are high, much of the
energy assimilated from food is tost as excessive metabolism If the MWAT is 66.2°F (19°C),
Summary ofTechnical Literature Examining the Physiological Effects of Temperature
85
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and yield is reduced 27% from maximum, even at a mean weekly temperature of 62.6 ± 3.6°F (17
± 2°C) it is obvious that MWAT is not protective.
In addition to concern for the inadequacy of the MWAT, this criterion also covered
reproduction and development needs of salmonids. A quote from NAS (1972) is useful:
Uniform elevations of temperature by a few degrees during the spawning period, while
maintaining short-term temperature cycles and seasonal thermal patterns, appear to have
little overall effect on the reproductive cycle of resident aquatic species, other than to
advance the timing for spring spawners or delay it for fall spawners. Such shifts are often
seen in nature, although no quantitative measurements of reproductive success have been
made in this connection.
However, significant recent research has shown that calculated MWAT temperatures (e.g., 66.2°F
(19°C) for rainbow trout) result in damage to gametes during reproductive stages. On the basis
of these technical findings, any temperature criterion that can result in a 27% reduction in biomass
and affect gamete viability must be questioned.
How can UILT data be evaluated against UUILT data?
Temperatures as low as 73.4°F (23°C) have been found to produce 50% mortality (LT50)
over the course of a week in rainbow trout acclimated to very cold (39.2°F [4°C]) waters (Sonski
1982, Threader and Houston 1983 as cited in Taylor and Barton 1992), with the lethal
temperature rising to 75.2°F (24°C) in moderately cold-water-acclimated 42.8-51.8°F (6-11°C)
fish (Black 1953, Stauffer et al. 1984, Bidgood 1980 as cited in Taylor and Barton 1992).
However, at most acclimation temperatures likely to be encountered during the spring through fall
seasons (53.6-68°F [12-20°C]), lethal levels are consistently in the range of 77-78.8°F (25-26°C)
(Bidgood and Berst 1969, Hokanson et al. 1977). With cautious acclimation to temperatures in
the range of 73.4-75.2°F (23-24°C), rainbow trout may not experience LT50 effects until a week
at 78.8°F (26°C) (Charlon et aL 1970 as cited in Grande and Anderson 1991). Even with careful
acclimation, 77°F (27°C) results in high or complete mortality in less than 24 hours (Charlon et al.
1970), and temperatures of 84.2-86°F (29-30°C) result in 50% mortality in 1-2 hours (Kaya 1978,
Craigie 1963, Alabaster and Welcomme 1962 as cited in Taylor and Barton 1992).
How can prolonged exposure to cyclic temperatures be evaluated?
Under fluctuating temperature test conditions, rainbow trout have experienced 50%
mortality in aweek of daily cycles from 69.8 to 77°F (21-27°Q (Lee 1980). Sonski(1983),
however, was able to culture rainbow trout in ponds that reached 84°F (28.9°C), and
Chandrasekaran and Subb Rao (1979) reported that rainbow trout were largely able to survive in
rearing ponds with months of daily maximum temperatures of 78.8-84.2°F (26-29°Q.
It seems inportant, given the low lethal levels reported in the literature, to evaluate whether
individual research results would unduly influence the temperature recommendations. In Figures
3 and 4, lethality data for salmon and char species (extracted from the summary by Hicks 2000)
are combined and examined in two different ways to develop a stronger basis for regional daily
SummaryofTechnical Literature Examining the Philological Effects of Temperature
86
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maximum criteria.
In Figure 3, all of the available 7-d LT50 data (50% of test organisms die over a 7-d
constant exposure test) for char and salmonids are presented by acclimation temperature. This
distribution is then used to make criteria recommendations for acclimation temperatures. At low
acclimation temperatures, constant exposure to just above 72.5°F (22.5°C) would be expected to
result in 50% mortality over a week. Reducing this value to a level where no lethality would be
expected to any adults or juveniles would result in a daily maximum not to exceed 68.9°F
(20.5°C).
Figure 4 considers resistance against short exposures to high temperatures, as might occur in
a natural fluctuating stream environment. Resistance time is very important to estimating
potential lethality; it is the time spent above a lethal threshold that determines whether short-term
lethal effects will occur. Different peak temperatures (e.g., 71.6, 75.2, 80.6, and 86°F [22, 24,
27, and 30°C]), may be lethal to an organism, but the organism can likely withstand these
temperatures for variable lengths of time. A population of fish may be able to withstand 69.8°F
(21 °C) for 7 d of constant exposure without any mortality, but have 50% of the population die
after 2 d at 75.2°F (24°C). At 80.6°F (27°C), 50% mortality may occur after less than 2 h of
exposure, and at 86°F (30°C) complete mortality may occur in just a few minutes.
In considering the effect of repeated hot days, it is important to incorporate cumulative
effects. DeHart (1975) found that lethal effects depend on the area of the temperature time curve
that is above a fish's UILT. Thermal effects accumulate over several days when the daily
temperature cycle fluctuates above the UILT, and the time above the UILT influences the thermal
resistance time regardless of any lower test temperatures. In other words, the ability of a fish to
resist a single day's exposure to a lethal temperature may not be sufficient, and 15 minutes spent
at 7.2°F (4°C) over the UILT is of more consequence than the same time spent at 3.6°F (2°C)
over the UILT.
In Figure 3, LT50 results are plotted for durations of 1 hour or less. At acclimation levels
less than 53.6°F (12°C), 50% mortality can be expected at 77°F (25°C) with a 1-h exposure, or at
75.5°F (24.2°C) with a 2-h exposure. Reducing these values to levels where no lethality would be
expected would result in temperatures not exceeding 73.4 or 71.6°F (23 or 22°C), respectively.
Because adults are considered more sensitive than juveniles (all of the 1-h or less data were for
juvenile fish), and the effects of lethal exposures are cumulative, we can assume that death may
occur with repeated exposure to daily maximum temperatures greater than 69.8-71.6°F
(21-22°Q. This estimate is very similar to the results (68.9-70T [20.5-21.1 °C]) at low
acclimation temperatures in the approach shown in Figure 2.
Acclimation Temperature °F (°C)
Combined LT50 for all Salmonids
Estimated LT1 with NAS
Adjustment
41 (5)
72.46 (22.48)
68.9 (20.5)
50(10)
73.56 (23.09)
70 (21.1)
39 (15)
74.66 (23.7)
71.06 (21.7)
Summary ofTcchnical Literature Examining the Physiological Effects of Temperature 87
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30
y = 0.1222x+21.868
R2 = 0.2453
5
0 -I 1 1 1 1
0 5 10 15 20 25
Acclimation Temperature
68 (20)
75.75 (24.31)
72.14 (22.3)
Figure 3. Combined lethality data for all salmonid species (based on 7-d LT50 constant temperature exposure test
results).
SUPPORTING DISCUSSION AND LITERATURE-SUBLETHAL AND LETHAL
EFFECTS FOR NATIVE CHAR, REDBAND TROUT, AND CUTTHROAT
TROUT SPECIES
What are the thermal requirements of bull trout and Dolly Varden?
Incubation. For bulltrout, McPhail and Murray (1979) compared egg survival and water
temperature and reported the highest egg survival to hatching (80-95%) in water temperatures of
35.6-39.2°F (2-4°C). Shortest hatch, largest alevins, and largest hatching fry were also
associated with these bw temperatures 35.6-39.2°F (2-4°C).
Research suggesting that spawning docs not peak until temperatures fall to below 44.6°F
(7°C) is consistent with the results of studies determining temperatures necessary for the
Summary ofTechnical Literature Examining the Ph>siological Effects of Temperature
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successful incubation of char eggs. These studies show that char require temperatures below
42.8°F (6°C) to achieve optimal egg survival (Buchanan and Gregory 1997). It is generally
agreed that poor survival occurs at temperatures above 44.6-46.4°F (7-8°C). Under test
conditions where temperatures were held constant, 46.4-50°F (8-10°Q resulted in very poor
survival of eggs (0%-20%) in tests by McPhail and Murray (1 979), and test temperatures in the
range of 44.6-51.8°F (7-11°C) were reported
0
20
y= 1.1342Ln(x) +29.632
R2 =0.8481
40
I
60
80
Time in Minutes
Time to LT50 Temperature (C)
1 sec 34.32
30 sec 30.42
1 min 29.62
60 min 24.99
120 min 24.2
Figurc4. Instantaneous mortalityfor char andsalmon combined (based on LT50 data for exposures of less than 1
hour and acclimation to <12C).
to result in poor survival in hatchery culture by Brown (1985). McPhail and Murray (1979) found
a temperature of42.8°F (6°C) to produce variable survival rates (60%-90%), and the range of
Summary of Technical Literature Examining the Physiological Effects of Temperature 89
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35.6-39.2°F (2-4°C) produced the best survival (80%-95%). In studies on the related species of
Arctic char, Humpesch (1985) reported optimal incubation to occur at 41°F (5°C).
In conclusion, for bulltrout, temperatures felling to 48.2°F (9°C) and below may initiate
spawning, but colder temperatures during incubation and yolk absorption produce the largest size
and greatest number of fry (McPhail and Murray 1979). Although spawning tends to peak at
44.6°F (7^), water temperatures continue to decline as the spawning season progresses and drop
toward the optimum incubation temperatures of 35.6-42.8°F (2-6°Q. Bull trout tend to select
redds directly adjacent to or below areas of groundwater upwelling, resulting in relatively
constant cold water temperatures for egg incubation with little diel fluctuation (Baxter and Hauer
2000).
Growth. In a laboratory study by McMahon et al. (1999), limited rations lowered the
optimal temperature for growth. For satiation-fed and 66% of satiation-fed juvenile bull trout,
optimum growth occurred at a temperature range of 53.6-60.8°F (12-16°C). When energy
availability was tow (one-third satiation-fed fish), maximum growth occurred at lower
temperatures (46.4-53.6°F [8-12°C]). In a related species, Arctic char, the upper thermal limits to
both feeding and growth were 70.7-71.2°F (21.5-21.8°Q (Thyrel et al 1999).
In a study analyzing the temperature effects on bull trout distribution in 581 sites, Rieman
and Chandler (1999) found that juvenile/small bull trout appeared most likely to occur at
summer-mean temperatures of 42.8-48.2°F (6-9°C) or single maximums of 51.8-57.2°F (11-
14°C). When given a choice of temperatures from 46.4 to 59°F (8-1 5°C) in a large plunge pool,
juvenile bull trout showed a clear preference for the coldest water available (6.4-48.2T [8-9°C])
(Bonneau and Scarnecchia 1996).
Migration. Upstream spring migration of adult bull trout may be related to water
temperatures and flows. In Rapid River, Idaho, a review of trap counts and temperature for 1985
through 1992 reported a general trend of increasing upstream bull trout counts as water
temperatures reached 50°F (10°Q (Elle et al. 1994). McPhail and Murray (1979) found peak
upstream movement coincided with water temperatures of 50-53.6°F(10-12°Q.
Spawning. Bull trout spawning areas are often associated with cold-water springs,
groundwater infiltration, and the coldest streams in a given watershed (Pratt 1992, Rieman and
Mclntyrc 1993, Rieman et al. 1997). Bull trout spawning is initiated as temperatures drop to
48.2°F (9°C) or lower, and egg mortality is lowest and alevin development is strongest at colder
temperatures (McPhail and Murray 1979). In Indian Creek, tributary to the Yakima River, bull
trout spawning activity peaked when stream temperatures were 42.8-46.4°F (6-8°C) (James and
Sexauer 1994). In the North Fork Skokomish River, bulltrout spawned in October after water
temperatures dropped below 43.7°F (6.5°C) (Brenkman 1998). Mean daily river temperatures
ranged from 38.3 to 45.5°F (3.5-7.5°C) during the remainder of the spawning period. This does
not differ significantly from descriptions of temperatures initiating bull trout spawning in Montana
(Shcpardet al. 1982), Oregon (Ratliffe 1992), or Washington (Kraemer 1994).
Although spawning for bull trout may begin as early as mid-August, spawning activity is
reported to be initiated when water temperatures begin to decrease and fall to 48.2°F (9°C) or
Summary of Technical Literature Examining the Physiological Effects of Temperature 90
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lower and does not peak until temperatures fall below 44.6°F (7°Q (McPhailand Murray 1979,
Shepard et al. 1982, Kraemer 1994, Brenkemen 1998). Kraemer (1994) noted that when stream
temperatures rise to above 46.4°F (8°C) once spawning has been initiated, spawning usually stops
or slows.
Bull trout require a narrow range of cold temperatures to rear and reproduce and may thrive
in waters too cold for other salmonid species (Baton 1980). McPhail and Murray (1979) reported
that 0%-20%, 60%-90%, and 80%-95% of bull trout eggs from a British Columbia river survived
to hatching at water temperatures of46.4-50, 42.8, and 35.6-39.2°F (8-10, 6, and 2-4°C),
respectively. In Montana, Weaver and White (1985) found that 39.2-42.8°F (4-6°C) was needed
for bull trout egg development. Buchanan and Gregory (1997) defined a range of 33.8-42.8°F
(1-6°C) that would meet bull trout egg incubation requirements in Oregon.
Although data are not shown directly for char species, other salmonids are known to
undergo some conditioning in the early stage of incubation that allows excellent survival at very
low temperatures. Where conditioning does not occur, and the eggs are incubated at an early
stage at very low temperatures, significant reductions in survival have been noted (Murray and
Beacham 1986, Seymour 1956). Thus even if 35.6°F (2°Q issuboptimal at a constant incubation
temperature, natural seasonal declines in temperature to 35.6°F (2°Q in the incubation period
may not decrease survival. This assumption is supported by work showing that newly hatched
Arctic char (Salvelinus alpinus) alevins are tolerant of temperatures near 32°F (0°C) (Baroudy
and Elliott 1994) and that the lower limit for hatching in Arctic char is less than 33.8°F (l'XD).
On the basis of the information examined, the initiation of spawning behavior and in vivo egg
development will be fully supported by keeping maximum temperatures in the spawning areas
below 44.6-46.4°F (7-8°C) during the spawning season. Given that excellent survival has been
noted in tests at 42.8 and 43.7°F (6 and 6.5°C), that some increased problems with disease may be
initiated at the higher end of this range, and that a variety of impacts to spawning have been noted
above 44.6°F (7°C), it appears that constant or acclimation temperatures in the range of 37.4-
42.8T (3-6°C) are optimal for the incubation of char. Because char are highly resistant to low
temperatures and low temperatures discourage disease organisms, water temperatures that swiftly
decline to 35.6-39.2°F (2-4°C) as the incubation season progresses appear highly favorable.
What are the therm al requirem ents for Lahontan cutthroat trout?
Growth. Laboratory studies of growth conducted at constant temperatures showed that
growth remained the same at temperatures of55.4, 68, and 71.6°F (13, 20, and22°Q (Dickerson
et aL 1999, as cited in Dunham 1999). Growth was significantly reduced at 75.2°F (24°C). Tests
done under a fluctuating temperature regime of 68-78,8°F (20-26°C) with a daily mean of 73.4°F
(23°C) for 1 wk showed growth rates were lower under this temperature regime than for fish
exposed to constant temperatures of 55 and 68°F (13 and 20°C). The growth rates under the
fluctuating regime were similar to growth rates of fish held at a constant 73.4°F (23°C).
Thermal stress—heat shock proteins. Lahontan cutthroat trout begin to produce heat
shock proteins immediately when exposed to 78.8°F (26°C) water temperature. Fish exposed to
75.2°F (24°C) water temperature began to produce heat shock proteins within 24 h. Fish exposed
Summary ofTechnical Literature Examining the Physiological Effects of Temperature 91
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to 71,6°F (22°C) water temperature did not produce heat shock proteins, even after 5 d of
exposure.
Occurrence. Dunham (1999) found that the distribution limit of most Lahontan populations
corresponded closely to a maximum summer water temperature of 78.8°F (26°C). The Willow
Creek population in Oregon occurred in water with daily maximum temperatures up to 83°F
(28.4°C).
Lethal effects. It has often been assumed that Lahontan cutthroat trout have a greater
tolerance for warm water than other salmonids because of their geographic distribution in warm
climates. Although there are not abundant studies of Lahontan cutthroat thermal requirements,
good evidence indicates that this species is comparable to other salmon and trout in its response
to warm water.
Critical thermal maximum (CTM) tests of thermal resistance were conducted on two strains
of Lahontan cutthroat trout by Vigg and Koch (1980). The two strains tested were Marble Bluff
and the Summit Lake strain found in Pyramid Lake. The test was designed to determine the effect
of alkalinity on CTM values. In both strains it was found that as alkalinity increased from 69 to
1,487 mg/L, the CTM decreased. Average CTM values determined for the death (D) temperature
endpoint were approximately 72.3-67.2°F (22.4-19.6°C) over this alkalinity range (average values
for the two strains). This CTM study employed a stepped temperature increase equal to 1.8°F
(l°C)/d up to an exposure temperature of68°F (20°C), starting from an acclimation temperature
of 60.8°F (16°C). After 68°F (20°C) was reached, the increments were 1.8°F (l°C)/4d. Because
of the stepped increases and the two different rates of heating, the study methodology is not
completely analogous to conventional CTM technique. The initial period of increase to 68°F
(20°C), however, could be considered to provide nearly full acclimation (given a 4-d acclimation
at each step) before the subsequent heating schedule. The temperature increase rates for the two
exposure periods averaged approximately 0.04°C/h and 0.0 l°C/h, respectively (averaging the
thermal increase over the step time interval). CTM tests provide results that have a different
meaning from UILT test results. Comparison of CTM values for other salmonids that have
corresponding UILT values is useful to understand the relative thermal tolerance of Lahontan
cutthroat. For example, appropriate comparisons of CTM values among species can be made by
contrasting the Lahontan results with CTM values for salmonids whose temperature increase rates
are 0.018-0.14°F (0.01-0.08°C)/h and starting from acclimation temperatures of 60.8-68°F (16-
20°C) (McCullough 1999). Grande and Anderson (1991) measured a CTM of 79.3°F (26.3°C)
for 2- to 3-month-old rainbow trout, 81°F (27.2°C) for 3- to 4-month-old brook trout, and 78.6°F
(25.9°C) for 2- to 4-month-old lake trout. Elliott and Elliott (1995) reported CTM of 81.9°F
(27.74°C) for Atlantic salmon and 76.6°F (24.8°C) for brown trout. The Lahontan cutthroat
studies reported CTM for a death endpoint; the Grande and Anderson studies also used a death
endpoint. If a loss of equilibrium (LE) endpoint is used to record CTM, the critical temperature is
generally slightly lower than if a death endpoint is used. For example, at a heating rate of 1.8°F
(l°C)/h, Becker and Gcnoway (1979) measured aCTM for coho salmon as 81.8 and 81.7°F(27.7
and 27.6°C) for the LE- and death-temperature endpoints, respectively. However, at a 64.4°F
(18°C)/h heating rate, these values were 83.6 and85.4°F (28.7 and29.7°C), respectively. In
conclusion, the CTM values for Lahontan cutthroat trout, compared with other salmonids tested
in a similar manner (i.e., rainbow trout, brook trout, lake trout, Atlantic salmon, brown trout), are
Summary of Technical Literature Examining the Physiological Effects of Temperature
92
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much lower. UILT values determined in other studies (see Table 4) for all the species that were
contrasted above with Lahontan ranged from 73.4 to 79.5°F (23-26,4°C). Using CTM data as a
guide, these results appear to indicate that Lahontan cutthroat would likely have lower UILT
values than these other salmonids.
Dickers on and coworkers (1999, and unpublished data, in Dunham 1999) found in
laboratory tests at constant temperatures that survival was 100% at 752°F (24°C) but dropped to
35% at 78.8°F (26°C). Tests done under a fluctuating temperature regime of 68-78.8°F
(20-26°C) with a daily mean of 73.4°F (23°C) for 1 wk showed no mortality even though this
regime provided 1-h/d exposure to 78.8°F (26°C) for 7 consecutive days, a temperature that
produced mortality during tonga- exposures (Dickeison and Vinyard 1999). These data indicate
that the UILT is probably between 77 and 78.8°F (25 and 26°C). However, temperature
adjustment rates, starting from an initial temperature of 55.4°F (13°C), were 7.2°F/d (4°C7d) up
to the test temperature. That is, a conventional time period for acclimation was not allowed prior
to the final exposure temperature. This could result in a slight underprediction of UUILT.
What are the thermal requirements for westslope cutthroat trout?
Incubation and egg survival. In a study by Shepard et al. (1982), westslope cutthroat
trout in the Flathead River basin, Montana, emerged in July and August following incubation
temperatures ranging from 35.6 to 50°F (2-10°C). Fry were approximately 20 mm long at
emergence. Adult westslope cutthroat trout held in cool 35.6-39.2°F (2-4°C) water temperatures
produced more viable eggs than those held in constant water temperatures of 50°F (10°C) (Smith
et al. 1983, in Shepard et al. 1982).
Growth. Westslope cutthroat streams are typically cold, nutrient-poor waters in which
conditions for growth tend to be less than optimal (Liknes and Graham 1988).
Spawning. Initiation and timing of spawning activity is related to water temperatures.
Adults move into tributaries during high streamflows and spawn in the spring when water
temperatures are near 50°F (10°C) (Scott and Crossman 1973).
Occurrence. Westslope cutthroat trout and bulltrout have similar life history patterns,
often occupy the same headwater streams, and restrict themselves to the coldest sections of
streams (Jakober et al. 1998, Behnke 1992). Westslope trout prefer cooler water temperatures
than do both brook trout and Yellowstone cutthroat trout (B. Shepard, personal communication).
Westslope cutthroat trout and redband trout may occur in the same system. They can be
allopatric or sympatric, but the redband generally inhabit lower reaches and cutthroat trout (often
with bull trout) dominate the upper, higher gradient sections where annual temperature units are
considerably less (Mullan et al. 1992).
What are the thermal requirem ents for redband trout?
Growth and feeding. Dwyer et al. (1986) conducted temperature experiments at 39.2,
44.6, 50, 60.8, and 66.2°F (4, 7, 10, 13, 16, and 19°C) on rainbow trout and redband trout
Summary of Technical Literature Examining the Physiological Effects of Temperature
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collected from Threemile Creek, Catlow Basin. Redband trout from Threemile Creek showed the
best growth at 66.2° (19°C) (no higher temperatures were tested), whereas rainbow trout
exhibited the best growth at 59-60.8°F (15-16°C).
In a study by Sonski (1982, as cited bySonski 1983b), redband trout reached their maximum
growth rate at 68°F (20°Q. Growth rates were less at both 59°F (15°C) and 73°F (22.8°C).
Redband trout are thought to exhibit the upper limit for feeding response for all salmonids of
the Pacific Northwest. No feeding was observed bySonski (1982 as cited bySonski 1984) for
juvenile redband at temperatures above 77.9-80.6°F (25.5-27°C). In a comparison of thermal
tolerance by three rainbow trout species, Sonski (1984) found that no redband trout or Wytheville
rainbow fed at temperatures higher than 78.8°F (26°C), and the Firehole River rainbow would not
feed beyond 80°F (26.7°C).
Metabolic activity and swimming speed. Gamperl (in litt.) conducted temperature studies
in Bridge Creek ("warm" stream) and Little Blitzen River ("cold" stream) in the Harney basin.
Gamperl's studies found that despite the two streams' different thermal histories, redband trout
from each stream exhibited a similar preferred temperature of 55°F (12.8°C). Bridge Creek trout
had greater metabolic power and improved swimming efficiency at 75.2°F (24°C) than at 53.6-
57.2°F (12-14°C) compared with the Little Blitzen River redband, which had similar values for
metabolic power and swimming performance at 53.6-57.2°F (12-14°Q and 75.2°F (24°C).
Gamperl concluded that some populations of redband trout can tolerate, and may have adapted
to, warm environmental temperatures. However, these studies should be taken as preliminary
because they were not replicated.
Occurrence. There are observations of redband trout feeding and surviving at relatively
high temperatures for a salmonid (82.4°F [28°C], Behnke 1992; 81.3°F [27.4°C] Sonski 1986;
80.6°F [27°C] Bowers et al. 1979), although it is unclear whether temperatures were measured in
the vicinity of the stream that the fish actually inhabited. These trout may rely on microhabitats or
thermal refuges to maintain populations in desert environments (see Ebersole et al. in press).
Lethal effects. In a comparison of thermal resistance among redband trout, Firehole River
rainbow, and Wytheville rainbow, Sonski (1984) found very little difference. He measured UILT
values for subyearling trout acclimated at 73.4°F (23°Q of 79.1, 79.3, and 80.6°F (26.2, 26.3,
and 27.0°C), respectively. These values are probably equivalent to UUILT values because it
appears that resistance was not improved by acclimation beyond 59°F (15°C). It is interesting
that redband trout were not significantly different in their thermal tolerance from other rainbow
stocks, despite their reputation as being tolerant of higher water temperatures.
Summary ofTcchnical Literature Examining the Physiological Effects of Temperature 94
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