United States Environmental Protection Agency EPA 910 D 01 005 May 2001 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 T ribal Fish Commission Shelley Spalding, U. S. Fish and Wildlife Service Debra Sturdevant, Oregon Department of Environmental Quality Mark Hicks, Washington Department of Ecology Summary of Technical Literature Examining the Physiological Effects of Temperature Contents ABSTRACT . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1 INTRODUCTION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2 SUMMARY OF THERMAL REQUIREMENTS . . . . . . . . . . . . . . . . . . . . . . . . . . . 3 What are 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 are the major differences in thermal tolerance among and within important families? 24 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 of Technical Literature Examining the Physiological Effects of Temperature 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, product ion, 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 does 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 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 o f temperature in migratory respo nse and seawater adaptation? . . . . . . 65 How can multiple stresses during the smolting 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 asso ciated 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 on MWAT? . . . . . . . . . . . . . . . . . . . . . . . . . 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 Incubat ion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 89 Growth. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91 Migration. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91 Spawning. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 91 What are the thermal requirements for Lahontan cutthroat trout? . . . . . . . . . . . . . . . . . 92 Growth. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92 Summary of Technical Literature Examining the Physiological Effects of Temperature Thermal stress   heat shock proteins. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 92 Occurrence. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93 Lethal effects. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 93 What are the thermal requirements for westslope cutthroat trout? . . . . . . . . . . . . . . . . . 94 Incubat ion 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 1 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 rat e increases as a function of temperature. Fish are metabolically 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 may be blocked at 69.8 73.4 ° F ( 21 23 ° C); and temperatures of 42.8 50 ° F ( 6 10 ° C) or lower during incubation result in maximum 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, westslope cutthroat trout, and mountain whitefish, little information is available on the effect s of temperature on their physiology. 2 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 populat ions. Temperature exerts its control through its effect on the physiology of the individual species and their life 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 and can 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 t he 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, McCullough 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 t his 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 extrapo late, 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. 3 Summary of Technical Literature Examining the Physiological Effects of Temperature SUMMARY OF THERMAL REQUIREMENTS What are the therm al requirem ents for incu bation an d 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 t he rate of embryo and alevin development, the amount of dissolved oxygen in the water, and, to a significant extent, the survival of early fry ( 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 t o produce relatively high survival to hatching and emergence, with approximately 42.8 50 ° F ( 6 10 ° C) being o ptimum for most salmonid species. However, although salmonids should avoid temperatures that are 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 wat ers too cold for other salmonid species ( Balon 1980). The literature suggests t hat 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 t heir 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 ot her 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 4 Summary of Technical Literature Examining the Physiological Effects of Temperature 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. If growth rates are too low during the summer rearing period, body fat is not sufficient to sust ain a fish during the winter rearing period ( Hokanson 1977). If the size during overwintering is too small or the growth rate prior to emigrat ion 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 salmonids, 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).

Table 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 by Garling 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 mykiss) 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 Siemien 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) 5 Summary of Technical Literature Examining the Physiological Effects of Temperature Bull trout ( Salvelinus confluentus) 12 16 McMahon et al. ( 1999)

Optimum growth temperature is that temperature which pro vides the most favorable conditions for growth. Other biological 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 labo ratory 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 ( i. e., 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 co nditions for salmonids residing in the center of their distribution in the field. Instead it indicates that art ificially 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 the full 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 positio n. 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. 6 Summary of Technical Literature Examining the Physiological Effects of Temperature 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, t he 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 by smolts leads to poor ocean survival ( Metcalfe and Tho rpe 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 t o 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 smolts upon entering the marine environment.

Effects o f temperature on the smolting process have been studied in terms of changes in 7 Summary of Technical Literature Examining the Physiological Effects of Temperature growth, condition facto r, body silvering, body moisture and lipid content, salinity tolerance, and gill Na K ATPase 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 smoltification range from approximately 53.6 59 ° F ( 12 15 ° C) or more ( Table 2). St eelhead 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 lowered 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 smolt ification and survival require considerat ion 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) 8 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 the mainstem 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 distance/ time.

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 low, 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 may be 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. Predaceous 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 cont rols 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 in Macdonald et al. in press). Critical swimming performance 9 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 glycogen 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 et 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 migrat ion.

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 et al. ( in press) studied 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 bot h 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 10 Summary of Technical Literature Examining the Physiological Effects of Temperature success, the authors found significant impairment ( only 10% success) in stocks that Table 3. Studi es that identify thermal blockages to adult salmon migration Species River Temperature cited as blocking migration Reference chinook, sockeye, steelhead Columbia 71 75 ° F ( 21.7 23.9 ° C) Fish and Hanavan ( 1948)

spring chinook Clearwater, Idaho 69.8 ° F ( 21 ° C) Stabler ( 1981)

spring chinook Tucan non 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) Stuehrenberg et al. ( 1978) ( as cited by Dauble and Mueller 1993).

fall ch inook Sacramento 66.2 69.8 ° F ( 19 21 ° C) ( oxygen ~ 5 mg/ L) Hallock et al. ( 1970)

steelhead Snake 69.8 ° F ( 21 ° C) Stricklan d ( 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 t he Fraser during 1998 ( a record warm year) compared with success during cooler years. Dr . Craig Clarke ( 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 labo ratory 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 o f deliberate attempts by hatchery managers to creat e a run t hat does not overlap with a wild run, t he 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 11 Summary of Technical Literature Examining the Physiological Effects of Temperature resist disease may all be of concern in the higher temperature range for migration. Just as distribution of juveniles 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 migrat ion 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 t he 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 lower 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 t o 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, co ho, chum), temperatures typically reach t heir annual highs during migration and/ o r 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 coldwater 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 12 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 incubat ion 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 appro ximately 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 may be 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 o f 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 ( Wedemeyer 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 may be 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 const ant 13 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 indicat es 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 crit eria 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 ( see 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 14 Summary of Technical Literature Examining the Physiological Effects of Temperature substrate embeddedness) 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 Sacramen to River Orsi ( 1971, as cited by CDWR 1988) 21.1 24.9 Oncorhynchus kisutch coho salmon Nil e Cr . Hatch ery, British Columbia Brett ( 1952) 20 23 25.0 25.0 Oncorhynchus nerka sockeye salmon Issaquah Hatch 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 Nil e Cr . Hatch ery, 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 rainbow trout Lake Superior Hokanson et al. ( 1977) 16 25.6 France Charlon et al. ( 1970) 24 26.4 Lakes Erie, Onta rio, 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 cited by Threader and Houston 1983) 20 26.7 Summerland Hatchery, British Columbia Black ( 1953) 11 24 Firehole River, MT Ennis Hatchery Winthrop Hatchery Kaya ( 1978) 24.5 24.5 24.5 26.2 26.2 26.2 15 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 Ander son 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 Lohr et 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 wat er, and the relative health of the exposed fish. The following general pat terns can be ident ified from laboratory and field research: constant 16 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 t he 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 t he marine environment and may result in smolts attempting to ret urn to freshwaters to wait unt il 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 fall. There are several factors to consider in setting a criterion for these life 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 ° C). 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) are 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, steelhead, 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 very 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 17 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 literat ure 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 t han 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 ° C).

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 developed 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 effects that become increasingly significant both above and below incipient lethal levels ( e. g., disease, migration blockages, 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 waterbody must 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 behavior and defines distribution. Char are cold water fish that are 18 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 dist ribution and include the most northerly distribution of any fish found in freshwater. Char may be anadromous, resident, or freshwater migratory.

3. Litt le information is available for the physiological requirements of bull trout and Dolly Varden. Available research for bull trout includes information for incubat ion, 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 lower 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 lower ( 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 on a 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 salmonid 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 henshawi); 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. 19 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 t he 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 t o assess the possible confounding variables such as whether wild fish or hatchery progeny were used, feeding rations, competition, o r 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 o n 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 statist ically according to its minimum, mean, or maximum temperature. However, from day to day these values can change, resulting in continually changing co nditions 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 t o identify the " effective acclimation temperature," t hat 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. 20 Summary of Technical Literature Examining the Physiological Effects of Temperature Laboratory tests of survival under thermal stress have several distinct advantages. Laboratory studies allow both acclimation and exposure temperature to be precisely controlled. Acclimation and exposure temperatures can be made either co nstant or fluctuating, and if fluctuating, they can conform to precise, repeatable cyclic patterns. Under laboratory conditions, we know precisely what temperatures fish are actually experiencing. That is, fish are 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 tho se 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 fro m stress ( Milligan et al. 2000). Attention must be given to photoperiod for certain performances to be meaningfully represented ( Clarke et al. 1992). Disturbance t o 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 whet her fish are allowed to seek their temperature preference within a vertical versus a horizontal thermal gradient.

Field t esting 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 experiment al apparatus at st reamside. This method would rely on art ificial equipment ( t anks) t o 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 21 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 then 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 may be estimated by this summation technique for a single cycle ( McCullough 1999, cumulative mortification, see Fry et al. 1946 as cited by Kilgour and McCauley 1986). Alternatively, mortality from a constanttemperature exposure can be contrasted with that from a cycle having the same mean 22 Summary of Technical Literature Examining the Physiological Effects of Temperature temperature. Results of this comparison vary with the magnitude o f 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 t o 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 pro vides 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 acclimatio n followed by stepped or co ntinuous 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 cycle involving high maximum temperatures, the CTM experiment based on thermal regime number 7 ( or its co usin, 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 23 Summary of Technical Literature Examining the Physiological Effects of Temperature Is there enough significant gen etic 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 of 68 ° F ( 20 ° C) to salmon bearing streams of northeastern Oregon and 57.9 ° F ( 14.4 ° C) to Oregon Coast Range streams. The technical committee concluded that there was no evidence fo r significant genet ic 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 itself has 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 adaptat ions, and within these const raints 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 fro m 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 family 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 evolutiona ry differences among salmonid spec ies in the Pa cific Northwest? 24 Summary of Technical Literature Examining the Physiological Effects of Temperature Within the species O. tshawytscha ( chinook salmon) there is great variation in run timing, life histories, and habitat select ion. 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 California and from temperate coastal mountain streams to continental interior streams.

There are many possible explanations why salmon have not made a significant adaptation to high temperatures in streams of the Pacific Northwest. Temperature t olerance 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 o cean rearing phase, where t he 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 ot her fish families. Given the data compilation for Salmonidae in this report ( Table 4) and the compilation by Coutant ( 1972) ( see 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) ( Table 13), and 91 98.6 ° F ( 33 37 ° C) ( Table 14), respectively. The range for Salmonidae accounts for the response of chinook, coho, sockeye, 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 are effective competitors to t he coldwater 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 pot ential adaptations would likely be expressed. If the differences among species within a family are so minimal, it is unlikely that 25 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 pot ential methodological variations. These researchers found t hat 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 ° C), 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 att ributed 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, and 29.4 ° C,) respectively, were determined ( Lee and Rinne 1980). All species were 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 region. 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 26 Summary of Technical Literature Examining the Physiological Effects of Temperature differentiated morphologically. In two species, each having recognized subspecies, there were no differences in UILT 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 t his 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 o f Salvelinus spp. McCauley found that two stocks of Salvelinus fontinalis failed to reveal any difference in response. However, McCauley repo rted 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 ° C), CTM values were 41.8 ° C ± 0.4 SD and 40.9 ° C ± 0.4 SD, respect ively ( 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 expo sure, but the cumulative mortality curves were very different. The st ream 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 27 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 sign ificant gene tic flexibility within a stock tha t would allow for ad aptation 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 bet ter 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 the UILT for salmonids may vary by population, depending on their hist ory of adaptation to temperature regimes. Differences in thermal to lerance were noted in time to death. At 70.7 ° F ( 21.5 ° C) the entire stream type t est populat ion ( i. e., all families of the stream type populat ion) 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 indicat e 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 rat e 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 28 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 st arting weight 3.3 4.5 g) and October 15 ( ending weights 10.5 13.9g). Growth was modeled with the equation log e G = a + b log e W.

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 t o 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, the Mt. 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 sto cks 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 29 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 Cech 2000). 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 so urce of variation in critical swimming speed than is genetic differences. However, at 50 ° F ( 10 ° C), Myrick and Cech ( 2000) noted a significantly great er critical swimming velocity in strains of co astal 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. 30 Summary of Technical Literature Examining the Physiological Effects of Temperature 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 temperat ure 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 Cech ( 2000).