Quinn and Adams, 1996; as cited in Quinn et al., 1997) note that in the Columbia River, based on passage data at Ice Harbor Dam, migration usually ceases at temperatures above 21 ° C. Fish and Hanava, ( 1948; as cited by USEPA, 1971) found that during an extremely warm year ( 1941) sockeye were observed congregating in small previously unused cold tributary creeks when the temperature in the Columbia rose to 21.7 23.9 ° C. Major and Mighell ( 1966) noted that entry of sockeye from the Columbia River into the Okanogan River, was blocked when rising or stable daily average temperatures were above 21.1 ° C, but that migration would resume if temperatures were falling. Hatch et al. ( 1992) found that when water temperatures reached daily average temperatures of 22.8 ° C, all migration of sockeye salmon ceased, that the bulk of the migration occurred below 22.2 ° C, and that surges of migration occurred when temperatures fell to below 21.1 ° C.

Constant or daily average temperatures in the range of 15.5 17 ° C have been found by numerous authors to cause excessive depletion of energy reserves and prespawning losses, and 17 ° C has been set as the limit beyond which detrimental physiologic effects would Page 86 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards become hazardous. Since maximum temperatures in the range of 17 19 ° C have also been identified in association with increased losses in migrating sockeye, caution should be exercised in selecting daily maximum values. Based on the available research, temperatures should not exceed a maximum 21 day average of 14 15 ° C, and the 7 day average daily maximum temperatures should not be greater than 16 17 ° C to support the migration of adult sockeye salmon. This temperature range is generally associated with an absence of prespawning mortality and will avoid high losses of stored energy reserves. To reduce the potential for causing blockages to migrating fish, the single daily maximum temperatures should not exceed 21 22 ° C, particularly when the migrating fish are acclimated to lower ( 2 6 ° C) water temperatures as they move upstream.

Steelhead Trout Most fish returning to Washington's streams are believed to have been at sea for 2 years. Fish that have been at sea for three years make up 18.5 33% of the returning fish, and only a few are at sea for 4 years ( 1 3.9%). The largest steelhead are generally those with the longest oceanic phase ( Wydoski and Whitney, 1979).

Snyder and Blahm ( 1971; as cited in Monan et al., 1975) found that temperatures of 23.9 ° C created a barrier to the migration of steelhead trout from the Columbia to the Snake River that remained until temperatures declined to nearly 21.1 ° C. Strickland ( 1967; as cited in Stabler, 1981) also noted that steelhead destined for the Snake River do not leave the relatively cooler waters of the Columbia River until the Snake cools to 21 ° C or lower. Fish and Hanavan ( 1948; as cited in Stabler, 1981 and USEPA, 1971) reported that steelhead trout entered minor typically unused tributaries and died there when the temperatures in the Columbia River ranged from 21.6 to 23.8 ° C. On the Deschutes River in Oregon, nearly all steelhead reportedly stopped migrating past Pelton Dam when the water in the ladder averaged between 20 21 ° C and the water below the dam was 13 14 ° C ( Don Ratliff, personal communication, as cited in Stabler, 1981). Stabler ( 1981) noted that Fessler ( 1977) and Everest ( 1973) found that steelhead halt their migration and will enter nonparent streams when water temperatures exceed 21 ° C. While not a study on migration, Nielsen et al. ( 1994) found temperatures of 22 ° C elicited an avoidance reaction in steelhead trout. They noted that foraging began to decline when stream temperatures reached approximately 22 ° C; although, it was noted that juvenile steelhead were seen actively feeding in surface waters with ambient temperatures up to 24 ° C. Fish moved to cool portions of stratified pools when temperatures exceeded 22 ° C, but not at or below 22 ° C, and would return to their original stream territories once ambient stream temperatures fell to about 23 ° C. Based on the above referenced studies, daily average temperatures of 21 24 are associated with avoidance behavior and migration blockage in steelhead trout.

Support for assuming 21 22 ° C creates significant enough stress in steelhead as to create a potential barrier to migration is also found in lethality studies of Coutant ( 1970) and Becker ( 1973). Citing what appears to be the same study, these authors concluded that the incipient lethal temperature for migrating adult steelhead was near a constant 21 22 ° C. They noted Evaluating Standards for Protecting Aquatic Life in Page 87 Washington's Surface Water quality Standards that adults appear to be more susceptible to high temperatures than are juveniles, which are typically used in lethality studies.

Concerns over disease may warrant restricting temperatures to levels well below that which would result in direct barriers to migrating steelhead. Diseases of native fishes is discussed and incorporated separately in this paper. In setting a criteria for the full protection of migration, it is also important to consider chronic and sublethal effects caused by warm waters. Migrating spring and summer steelhead will be passing through during the peak temperatures of summer as they move upstream to holding areas where they will wait until the following stream. While often repeat spawners, steelhead still rely on their muscle and fat reserves to hold them over through to the completion of spawning and return to the ocean. In addition to concerns over disease, the metabolic demands of swimming, negotiating obstacles, and supplying the basal metabolic requirements while holding leaves little reserves left for digging redds and spawning once they reach their spawning streams. The warmer the water the more energy will be required to survive until spawning is completed and thus the greater chance that fitness will be affected and that higher pre and post spawning mortalities will occur. For these reasons it would be unwise to assume that any temperature regime that does not form a blockage to migration or cause direct lethality will fully protect migrating steelhead.

Where fish may hold in waterbody segments for long periods of time prior to spawning, as is common for spring and summer run steelhead, daily maximum temperatures should not exceed the range previously identified as fully protective for juvenile rearing. At this point in the life stage of the adults when feeding is not occurring, even cooler waters would be preferable. Based on the preceding, it is estimated that to fully protect the adult migration of steelhead trout the 7 day average of the daily maximum temperatures should not exceed 17 18 ° C. Single daily maximum temperatures should not exceed 21 22 ° C.

Cutthroat Trout Gresswell ( 1995) suggests that cutthroat generally migrate when temperatures approach 5 ° C ( citing Varely and Gresswell, 1988, Byorth, 1990, and Thurow and King, 1994). In one cutthroat stream into Yellowstone Lake maximum daily water temperatures at the time of peak spawning ranged from 10 14.2 ° C over a 13 year period ( USFWS, unpubl. data; as cited in Gresswell, 1995).

Migrations of resident and potamadromous cutthroat trout occupy largely the same habitat used for juvenile rearing. Thus for these forms, there is little specific basis for establishing a specific migration criteria higher than the fully protective range identified for juvenile rearing. The anadromous forms of cutthroat, unlike the Pacific salmon, may make numerous journeys to the marine waters and back again. Thus they may need to repeatedly pass through any suboptimal temperature regime, however, since they may feed on their return migrations through fresh waters, they may be subject to less sublethal stress effects than the Pacific salmon. It is recommended that any standard applied to protect the anadromous migration of the Pacific salmon also be applied to cutthroat trout. Such a temperature value Page 88 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards would likely be protective if the 7 day average of the daily maximum temperatures seldom exceeded 17 18 ° C and the single daily maximum temperature does not exceed 21 22 ° C.

Table 4.16. Barriers to migration of salmon and trout:

Species Barrier to Migration Comment Author Chinook 21 22 ( 21.5) Stabler, 1981; Bumgarner et al., 1997; Hallock, Elwell, and Fry, 1970; Thompson, 1945, Ratliff, 1977, Fish and Hanavan, 1948, Major and Mighell, 1967, and Alabaster, 1988 18.9 ( maximum) Partial blockage associated with low ( 5ppm) oxygen levels Hallock et al., 1970 17.2: 21.7 and 22.2: 26.1 Temperature differences that caused blockage Thompson, 1945 9 11 ( change) Temperature differences that formed blockage Gray, 1990 Sockeye 21 Migration ceases Quinn and Adams, 1996 Congregated in cold tributaries when main stem reached 21.7 23.9 Fish and Hanava, 1948 21.1 Blocked migration into tributary unless temperatures were falling Major and Mighell, 1966 22.8 ( daily average) Bulk of migration occurred below 22.2 and surges occurred when temperatures fell to below 21.1 Hatch et al., 1992 23.9 Barrier until tributary temperature declined to nearly 21.1 Snyder and Blahm, 1971 21 Barrier for entry into tributary Strickland, 1967 Steelhead 21.7 23.9 ( 22.8) Congregated in cold tributaries when main stem reached 21.7 23.9 Fish and Hanava, 1948 20 21 ( 20.5) Average temperature causing blockage when fish were coming from water of 13 14 Ratliff, Personal communication 21 Stabler, 1981 Temperatures of 21 22 ° C are commonly cited as creating barriers to migration. While some researchers have found that fish will travel through waters as warm as 24 ° C, this is generally uncommon. Temperatures below 21 ° C have also been noted as causing blockages, but again Evaluating Standards for Protecting Aquatic Life in Page 89 Washington's Surface Water quality Standards this is generally uncommon and has been in association with fish encountering significant changes in temperature or encountering high temperatures in combination with low ( stressful) oxygen levels. Most of the authors reviewed were not clear about the metric, but most appeared to be referring to the daily average temperature. Some, however, may have been referring to the absolute temperature at the time of measurement, and thus would be assessing something closer to the daily maximum temperature. To bound the estimate on the temperatures creating migratory blockages, the commonly cited literature range for blockage should be treated both as potentially related to the daily maximum temperature or the daily average temperature. This would result in the estimate that the 7DADMax temperature threshold that would generally prevent migration blockages would occur within the ranges of 20.05 21.05 ° C or 23.6 24.6 ° C, respectively. This would create a potential range within which migration blockages may occur of a 7DADMax of 20.05 24.6 ° C ( 22.1 ° C). The acute nature of blockages, the undescribed temperature metrics reported by most authors, and the general trait of larger rivers such as the Columbia River being more thermally stable suggests the upper range of this estimate may underestimate the effects of temperature in the field.

While barriers to migration have a direct effect on adult migrants, warm temperatures can harm migrants in many other important ways. These include prespawning mortality, decreased migratory performance, reduced fecundity and egg viability, and increased disease rates that affect both the spawners and their offspring. For this reason any criteria set to protect adult migration should consider more than just the temperature that creates a barrier to migration.

Average daily temperatures of 15.5 20 ° C have been most frequently associated with prespawning mortality, thermal stress, and reduced reproductive success in adult migrants both in laboratory studies and natural streams. Concerns over the effect of temperature on egg carrying females was discussed previously in the section on reproductive success. Some examples are included in this evaluation of migratory effects that represent ambient river studies conducted at the lower reaches of main stem rivers. This is because these studies better fit with the concept of protecting migratory pathways than studies done specifically on ripe females. The studies examined here are typically expressed as a daily average exposure, which would be approximately equal to a 7DADMax of 18.1 22.6 ° C ( 20.4 ° C). Considering the lethal endpoints under consideration here, it is suggested that only the lower portion of this range should be considered potentially acceptable. For these reasons, it is concluded that to protect migrating fish from prespawning losses in main stem rivers the 7DADMax temperatures should not exceed 18.1 20.4 ° C ( 19.25). It is important to note that females carrying ripe eggs would be expected to have egg losses at these temperatures, and so it is important not apply this temperature estimate in headwater rivers where migrating fish are likely to be carrying ripe eggs. Page 90 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Table 4.17. Migratory effects to salmon and trout other than barriers.

Species Prespawning Mortality or Egg Loss Migration Criteria Estimates Migration Stressors Comments Author Chinook 20 ( mean) 23 ( max) River temperature associated with high ( 25%) losses Mcdonald et al., 2000 18 20 Thermo regulatory behavior in sub yearling fall Chinook at 18 20 and heat shock proteins within several hours at 20 Sauter and Maule, 1997 7.2 15.6 Piper et al., 1982 3.3 13.3 ( spring) 13.9 20 ( summer) 10.6 19.4 ( fall) Migration recommendation for different runs Bell, 1973 Coho 7.2 15.6 Beschta et al., 1987 > 20 Reduced quality and rapid deterioration of eggs in utero in migrants Flett et al., 1996 16.7 ( no effect) No apparent adverse effects to eggs in utero Bouck et al., 1970 Chum 8.3 15.6 Beschta et al., 1987 Sockeye 16.2 Depletion of fat reserves and reproductive organ abnormalities at 16.2 Bouck, 1977 17.5 19.5 ( maximum) High prespawning mortalities in river. Temperatures greater than 15.5 ( daily ave) higher mortality from columnaris disease Gilhousen, 1990 20 ( average) 20 ( average) Mean daily river temperatures above 20 resulted in signs of significant stress, poor spawning success, prespawning mortality, and poor egg quality Mcdonald et al., 2000 19 ( constant) Laboratory exposure over two weeks at 19 depressed maturation, but 15 did not. Clarke, Personal comm. 18 22 ( mean daily) Threshold of Fraser Rv. at mouth for successful reproduction Mcdonald, 2000 Evaluating Standards for Protecting Aquatic Life in Page 91 Washington's Surface Water quality Standards Holding of Adult Spawners: It is important to recognize that many stocks of salmon do not migrate directly through to their spawning streams, but instead hold in upper main stem rivers throughout the warmest period of the summer until the fall when they ascend the tributaries and begin spawning. This section has not included an evaluation of the temperature requirements of these holding areas. Because adult fish do not feed while they are holding, maintaining cold waters are expected to be especially important to reduce metabolic demands and stress in areas used for over summer holding. It is concluded that the temperature determined previously for the protection of juvenile rearing ( 7DADMax 16.5 ° C) also be considered for application to these holding areas, at a minimum. Or alternatively, temperatures should be maintained at levels determined previously to prevent prespawning losses to eggs ( 7DADMax 14.2 ° C).

vi) Lethality to Adults and Juveniles Constant Laboratory Exposure Studies:

Chinook Salmon Beacham and Withler ( 1991) transferred juvenile chinook salmon from 14 ° C saline water to a series of test temperatures and noted genetic differences in the resistance times of southern versus northern stocks. They also found that 55% mortality occurred within three days after transfers to saline waters with temperatures as low as 20.3 21.5 ° C. They found 87% mortality occurred within 2 days at 22.4 ° C. In tests using adult " jack" chinook salmon the authors established an upper incipient lethal temperature of 21 22 ° C. Orsi ( 1971; as cited in CDWR, 1988) found that 50% mortality in fingerlings acclimated to 15.6 ° C occurred within 48 hours at 21.1 ° C, however, by slowly acclimating fish to 21.1 ° C the author raised the lethal endpoint to 24.7 ° C. Becker ( 1973) noted that tests conducted with Jack chinook salmon produced 50% mortality at 21 22 ° C ( this was likely the same tests conducted in Coutant, 1970, in which case the acclimation was at best the prevailing temperature of the Columbia River). Brett et al. ( 1982) found that 21.5 ° C was the lethal limit of spring chinook acclimated previously at 10 ° C and that minor increases in mortality ( up to 5%) occurred at 20 ° C. Brett ( 1956) found that acclimations of 5, 10, 15, and 20 ° C produced 50% mortality at test temperatures of 21.5, 24.3, 25, and 25.1 ° C. Brett et al. ( 1982) established the lethal level to be 25 ° C at an acclimation of 20 ° C. Snyder and Blahm ( 1971), however, reported no mortality in chinook subjected to a change from 10 to 21.1 ° C over a 3 day test.

Some authors have noted temperatures that result in almost instantaneous lethality to chinook salmon. Orsi ( 1971; as cited in CDWR, 1988) found that fingerlings acclimated to 21.1 ° C suffered complete mortality when exposed to 31.1 ° C water for 4 6 minutes, and 50% mortality occurred in fish acclimated to 18.3 ° C and exposed to 28.3 ° C from 4 6 minutes. In a study by Snyder and Blahm ( 1971) a temperature of 26.7 ° C has resulted in mortalities beginning after just 100 seconds of exposure and complete mortality after 4 minutes, while at Page 92 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards 32.2 ° C it only takes 4 seconds for mortality to begin and complete mortality after 11 seconds. Further, Gray ( 1990) found that temperature plumes above 25.1 ° C caused spasmodic muscle contractions in passing chinook salmon. Gray ( 1990) cited research showing that juvenile salmonids are more susceptible to predation at 10 20% of the thermal dose causing loss of equilibrium.

Coho Salmon In constant exposure tests, the upper lethal levels producing 50% mortality in juvenile coho was 25 ° C at an acclimation temperature of 20 ° C ( DeHart, 1974; Brett, 1956), but at an acclimation of 5 ° C, Brett ( 1956) found the lethal level declined to 22.9 ° C. McGeer, Baranyi, and Iwama ( 1991) exposed stocks from six hatcheries to a 1 ° C/ hour increase in temperature and found the point of 50% mortality ranged from 23.8 24.4 ° C. While all test fish survived up to 23 ° C none survived beyond 25.5 ° C. While juvenile coho are reasonably tolerant to short term peaks in temperature, adults may be far less tolerant. Using migrating adult fish taken during the summer from the Columbia River, Coutant ( 1970, and Becker, 1973) determined the lethal limit to be 21 22 ° C.

Chum Salmon Chum acclimated to cold waters ( 5 ° C) have an upper lethal temperature of 21.8 ° C, which increase to 22.6 and 23.1 ° C at acclimation temperatures of 10 and 15 ° C ( Brett, 1956). In work by Snyder and Blam ( 1971) it was found that 50% mortality occurred in less than 50 minutes to a test population transferred from 15.6 ° C to 26.7 ° C. A transfer from 15.6 ° C to 29.4 ° C resulted in 50% mortality in only 60 seconds, and at 32.2 ° C it only required 15 seconds to cause 100% mortality. Lethal low temperatures range from 6.5 ° C and 4.7 ° C at acclimation temperatures of 20 ° C and 15 ° C, to 0.5 ° C at a 10 ° C acclimation.

Pink Salmon Brett ( 1952) found that pink salmon could not be acclimated to 24 ° C and were unable to survive for one week at 25 ° C. Brett ( 1952) found that at acclimations of 5 ° C the LT50 occurred within one hour of exposures to 22.5 ° C and 23 ° C. With acclimation to 10 ° C the LT50 also occurred at 22.5 ° C, and at an acclimation of 20 ° C, it occurred at 23.9.

Sockeye Salmon Bouck and Chapman ( 1975) found that adult sockeye could not survive long periods at 20 ° C or 22 ° C, and determined that the LT50 for these temperatures occurred at 11.7 days and 3.2 days, respectively. At the lower acclimation temperatures of 5 and 10 ° C, Brett found that juvenile sockeye had lethal levels of 22.2 ° C and 23.4 ° C in a week long test. At acclimations between 15 23 ° C, the LT50s for juvenile sockeye were variable within the range of 24 24.8 ° C ( Brett, 1952; Beschta et al., 1987; Servizi and Jensen, 1977). Brett ( 1952) determined the lower acutely lethal temperatures for juvenile sockeye salmon. He found that Evaluating Standards for Protecting Aquatic Life in Page 93 Washington's Surface Water quality Standards at acclimations of 15 and 20 ° C the temperatures that produced 50% mortality in a one week test were 4.1 and 4.7 ° C, and that fish acclimated to 10 ° C had a lower lethal level of 3.1 ° C.

Steelhead and Rainbow Trout In evaluating the effect of high water temperature on steelhead, Nielsen et al. ( 1994) found that the upper lethal temperature is approximately 24 ° C for juvenile steelhead. Redding and Schreck ( 1979) subjected juvenile steelhead previously acclimated to 12 ° C to a rapid rise ( 6.25 hours) to 26.5 ° C where it was maintained for the duration of the test. All fish died within 20.5 hours. In a separate test the temperature was held at 26 ° C, and all fish died within 31 hours. Coutant ( 1970; and Becker, 1973), however, examined the upper lethal temperatures for adult steelhead taken at peak migrating temperatures from the Columbia River in Washington. Coutant concluded from his work that the incipient lethal temperature for migrating adult steelhead was closer to 21 22 ° C. Most laboratory studies use juveniles of the larger species of fish due to the difficulty of handling adult salmon and steelhead in laboratory tanks. It has been noted previously that adult Pacific salmon may have lower incipient lethal levels than that for juveniles, and it could be that this relationship may hold true for steelhead as well.

Temperatures as low as 23 ° C have been found to produce 50% mortality ( LT50) in rainbow trout with a week's constant exposure in fish previously acclimated to very cold ( 4 ° C) waters ( Sonski, 1982; Threader and Houston, 1983, as cited in Taylor and Barton, 1992), with the lethal temperature rising to 24 ° C in moderately cold water ( 6 11 ° C) acclimated fish ( Black, 1953; Stauffer et al., 1984; Bidgood, 1980, as cited in Taylor and Barton, 1992). However, at most acclimation temperatures likely to be encountered during the spring through fall seasons ( 12 20 ° C) lethal levels are consistently in the range of 25 26 ° C ( Bidgood and Berst, 1969; Hokanson et al., 1987). With cautious acclimation to temperatures in the range of 23 24 ° C, rainbow trout may not experience LT50 level effects until temperatures are held for a week at 26 ° C ( Charlon et al., 1970, as cited in Grande and Anderson, 1991). Even with careful acclimation, 27 ° C results in high or complete mortality in less than 24 hours ( Charlon, Barbier, and Bonnet, 1970), and temperatures of 29 30 ° C result in 50% mortality in periods of 1 2 hours ( Kaya, 1978; Craigie, 1963, and Alabaster and Welcomme, 1962; as cited in Taylor and Barton, 1992). Some authors conducted critical thermal maximum ( CTM) tests on rainbow trout. In this type of test, water temperatures are continuously increased at a rapid rate until the test fish either loose equilibrium or die completely. CTM values at prior acclimations of 10 to 25 ° C ranged from 27.6 to 32 ° C, respectively, in testing by Myrick and Cech ( 2000).

Cutthroat Trout Heath ( 1963) subjected sea run cutthroat to a cyclic temperature regime of 10 20 ° C and calculated a critical thermal maximum ( CTM) of 29.77. At constant acclimations of 10, 15, and 20 ° C, the corresponding CTM values were 27.63, 29.06, and 29.88 ° C. De Staso and Rahel ( 1994) reported at CTM of 28 ° C at some unknown acclimation temperature. Pauley et al. ( 1989) cite research concluding that equilibrium and ability to swim is lost with a rise in Page 94 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards temperature to 28 30 ° C. Feldmuth and Eriksen ( 1978, as cited in McIntyre and Rieman, 1995) estimated that the CTM for westslope cutthroat trout was 27.1 ° C, a value lower than those estimated for brook trout ( 29.8 ° C), brown trout ( 29.6 ° C) and rainbow trout ( 31.6 ° C). Golden ( 1976) tested the temperature tolerance of zero age coastal cutthroat stocks from western Oregon. In CTM tests where the temperature is rapidly increased until the fish die or loose equilibrium, acclimation to 10 and 23 ° C yielded CTM values of 28.03 and 30.62 ° C. At a fluctuating equilibriums of 7.8 10 ° C and 13 23 ° C the CTM values were 27.64 and 30.31 ° C.

Golden ( 1978) tested the lethality of significantly fluctuating temperature regimes with cutthroat trout. Incipient lethal levels ( ILL) were 25.5 ° C and 25.7 ° C for fish acclimated to 23 ° C and a fluctuating regime of 13 23 ° C, respectively. Golden estimated losses in one week of 10% or less at a fluctuating cycle of 13 27 ° C.

Vigg and Koch ( 1980) measured the lethal limits of two stocks of Lahontan cutthroat in three water types and found that alkalinity profoundly influences the results. In waters with alkalinity of 1,487 mg/ l the lethal range was 18.5 20.2 ° C, in waters with alkalinity of 357 mg/ l the range was 20.2 21.1 ° C, and at an alkalinity of 69 mg/ l the lethal range was 21.8 23.0 ° C for the two species. Kramer ( 1975; as cited in Vigg and Koch, 1980) found they were able to hold a Humboldt River strain of cutthroat at 24 ° C for two weeks without any mortality, but with feeding inhibition.

Dickerson et al. ( 1999, and unpublished data as cited in Dunham, 1999) tested the lethal tolerance levels of Lahontan cutthroat. Survival was 100% at 24 ° C but declined to 35% at 26 ° C. At 28 ° C mortality was complete in 48 hours.

Were it not for the studies of Lahontan cutthroat trout by Vigg and Koch ( 1980), it would be easy to conclude that cutthroat trout would only be expected to have 50% mortality ( LT50) over a one week's exposure to constant temperatures above approximately 24 ° C. While it is clear that in many cases no mortality would occur as a consequence of short term exposure to infrequent daily maximum temperatures as high as 26 ° C, the data of Vigg and Koch ( 1980) suggest more caution may be warranted. They calculated LT50 values of 20.2 21.1 ° C and 22 23 ° C using two stocks of cutthroat and two water sources with alkalinity levels comparable to what is regularly found in Washington. More work is needed to clear up the question of whether native stocks demonstrate lower lethal thresholds in natural waters with high alkalinity levels, prior to assuming the data of Vigg and Koch ( 1980) to be anomalous.

Table 4.18. The following summarizes the results of laboratory tests subjecting salmon and trout to constant test temperatures. The column on acclimation provides the temperature to which the fish were acclimated to prior to being moved to the test temperature, and the endpoint reported is the percent of mortality that occurred at each lethal temperature level ( LT).

Author or Study Species Acclimation Temp. ( ° C) Temperatur e of Test Time to Endpoint Endpoint Reported Comment Evaluating Standards for Protecting Aquatic Life in Page 95 Washington's Surface Water quality Standards ( ° C) ( seconds) Beacham and Withler, 1991 Chinook 14 20.9 259200 LT55 LT55 in 3 days with transfers to 20.3 21.5 ( mean 20.9 ° C). 14 22.4 172800 LT87 2 days 14 21.5 604800 LT50 Adults 7 day 21 22 ( mean 21.5 ° C). Orsi, 1971 Chinook 15.6 21.1 172800 LT50 2 days 21.1 24.7 172800 LT50 2 days 18.3 28.3 300 LT50 4 6 minutes 21.1 31.1 300 LT100 4 6 minutes Becker, 1973 and Coutant, 1970 Chinook Summer ambient 21.5 604800 LT50 Adults 7 day 21 22 ( mean 21.5 ° C) Brett, 1982 Chinook 10 21.5 604800 LT50 Spring run 10 20 604800 LT5 Spring run 20 25 604800 LT50 Spring run Snyder and Blahm, 1971 Chinook 10 21.1 259200 LT0 3 days  no mortality 10 26.7 100 LT1 100 seconds 10 26.7 240 LT100 4 minutes 10 32.2 4 LT1 4 seconds 10 32.2 11 LT100 11 seconds Brett, 1956 Chinook 5 21.5 604800 LT50 10 24.3 604800 LT50 15 25 604800 LT50 20 25.1 604800 LT50 DeHart, 1974 Coho 20 25 604800 LT50 Brett, 1956 Coho 20 25 604800 LT50 Coho 5 22.9 604800 LT50 Becker, 1973 and Coutant, 1970 Coho Summer ambient 21.5 604800 LT50 Adults 7 day 21 22 ( mean 21.5 ° C) Brett, 1956 Chum 5 21.8 604800 LT50 Chum 10 22.6 604800 LT50 Chum 15 23.1 604800 LT50 Snyder and Blam, 1971 Chum 15.6 26.7 3000 LT50 50 minutes 15.6 29.4 60 LT50 60 seconds 15.6 32.2 15 LT100 15 seconds Brett, 1952 Pink 5 22.5 3600 LT50 1 hour LT50 at both 22.5 and 23 ° C. 10 22.5 604800 LT50 20 23.9 604800 LT50 24 Could not be acclimated to 24 ° C or survive one week at 25 ° C. Brett, 1952 Sockeye 5 22.2 604800 LT50 10 23.4 604800 LT50 Bouck and Chapman, 1975 Sockeye 20 1010880 LT50 Adults  11.7 days 22 276480 LT50 Adults   3.2 days Brett, 1952; Servizi and Jensen, 1977 Sockeye 15 23 24 24.8 ( 24.4) 604800 LT50 Page 96 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Nielsen, Lisle, and Ozaki, 1994 Steelhea d 24 604800 LT50 Upper lethal temperature for juveniles Redding and Schreck, 1979 Steelhea d 12 26 73800 LT100 Complete mortality in 20.5 hours with rapid rise to test temperature 12 26 111600 LT100 Complete mortality in 31 hours with immediate transfer to test temperature Becker, 1973 and Coutant, 1970 Steelhea d Summer ambient 21.5 604800 LT50 Adults 7 day 21 22 ( mean 21.5 ° C) Sonski, 1982 Rainbow Trout 4 23 604800 LT50 Threader and Houston, 1983 Rainbow Trout 4 23 604800 LT50 Black, 1953 Rainbow Trout 6 11 24 604800 LT50 Stauffer et al., 1984 Rainbow Trout 6 11 24 604800 LT50 Bidgood, 1980 Rainbow Trout 6 11 24 604800 LT50 Bidgood and Berst, 1969 Rainbow Trout 12 20 25 26 604800 LT50 Hokanson et. al., 1987 Rainbow Trout 12 20 25 26 604800 LT50 Charlon et al., 1970 Rainbow Trout 23 24 26 604800 LT50 Charlon, Barbier, and Bonnet, 1970 Rainbow Trout High 27 86400 LT50 LT100 High to complete mortality in less than 24 hours Kaya, 1978 Rainbow Trout High 29 30 3600 7200 LT50 1 2 hours Craigie, 1963 Rainbow Trout High 29 30 3600 7200 LT50 1 2 hours Alabaster and Welcomme, 1962 Rainbow Trout High 29 30 3600 7200 LT50 1 2 hours Golden, 1978 Cutthroat Trout 23 25.5 604800 LT50 13 23 25.7 604800 LT50 Fluctuating acclimation regime Vigg and Koch, 1980 Cutthroat Trout  Lahontan 18.5 20.2 ( 19.35) 604800 LT50 Alkalinity 1,487 mg/ l   two stocks of Lahontan and two water sources 20.2 21.1 ( 20.65) 604800 LT50 Alkalinity 357 mg/ l   two stocks of Lahontan and two water sources 21.8 23.0 ( 22.4) 604800 LT50 Alkalinity 69 mg/ l   two stocks of Lahontan and two water sources Kramer, 1975 Cutthroat Trout 24 129600 LT0 No mortality in two weeks using Humboldt River strain of cutthroat Dickerson et al., 1999 Cutthroat Trout  Lahontan 24 604800 LT0 Lahontan Evaluating Standards for Protecting Aquatic Life in Page 97 Washington's Surface Water quality Standards 26 604800 LT35 Lahontan 28 172800 LT100 2 days   complete mortality in Lahontan Typical Constant Laboratory Exposures Producing Fifty Percent Mortality:

The results from constant temperature testing that resulted in fifty percent mortality in 3 12 days of exposure ( shown in the table above) can be used to assess weekly temperatures that will not result in excess lethality. Of the 38 tests assessed, 90% of the values were between 20.5 25.6 ° C, the inter quartile range was 21.9 24.6 ° C, and the median was 23.1 ° C. The 5th and 95th percentiles for the distribution are used herein to calculate expected thresholds to avoid the possibility of using anomalous extreme data points. Converting from an LT50 to an LT1 estimated mortality rate ( by subtracting 2 ° C) suggests a constant exposure to a temperature above 18.5 23.6 ° C for a period of a week or more may result in the direct mortality to salmon and trout. Converting the constant laboratory test exposure estimate to a field exposure regime is especially difficult for this form of lethality data. Because the exposure times necessary to cause lethality reduce as temperatures continue to increase above the incipient lethal limit it is not appropriate to treat the laboratory results as weekly average temperatures. However, using the results directly as 7DADMax thresholds would overstate the risks since the time spent above the threshold will be only a small portion of each day while the original tests exposed fish to these temperatures for 24 hours per day. Thus a more defensible estimate would be one that falls between these two approaches rather than using the specific values contained in either. Treating the constant laboratory exposure as a weekly average temperature would result in the estimate of a 7DADMax of 21.68 26.78 ° C ( 24.23), and using it directly would result in the estimate of a 7DADMax of 18.5 23.6 ° C ( 21.05). Using these two approaches to bound the estimate results in the expectation that mortality will occur as 7DADMax temperatures exceed 21.05 24.23 with the best estimate expected to be the midpoint of the distribution ( 22.64 ° C).

Regression of Constant Laboratory Exposures Producing Fifty Percent Mortality:

Although, the relationship between acclimation temperatures and test temperatures resulting in 50% mortality is strong within individual studies, the relationship is weak when all of the various studies are combined for analysis. This is illustrated in figure 4.1 below.

Figure 4.1. Combined lethality data for all salmon and trout species ( based on 7 day LT50 estimates) from Table 4.18 above. Page 98 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Acclimation Combined LT50 Estimated LT1 with Temperature ( ° C) for all Salmonids( ° C) NAS Adjustment ( ° C) 10 22.50 20.50 12 22.93 20.93 14 23.37 21.37 16 23.79 21.79 18 24.23 22.23 20 24.66 22.66 The regression equation in figure 4.1 above, can be used to predict temperatures at which significant lethality ( 50%) would be expected with a constant exposure for 7 days at various prior acclimation temperatures. Since the results are based on 50% mortality, they should be adjusted to better reflect temperatures that would not directly kill fish. The USEPA recommends that states subtract 2 ° C from LT50 results to obtain an estimate that would result in 1% or less mortality ( LT1) under the same exposure assumptions. Fish acclimate to ambient temperatures approximately equal to the average temperature, and often fish that are migrating from the ocean or from cooler tributary systems will not be fully acclimated to warm prevailing temperatures in main stem rivers. For this reason, acclimation temperatures from 12 16 ° C may best represent the condition of migrating fish during the summer period ( yielding LT1 estimates of 20.93 21.79 ° C). Juvenile fish that reside within a system, may be acclimated to warmer temperatures. However, even resident fish will not be as fully acclimated as those used in tests to estimate an ultimate incipient lethal temperature ( the absolute highest LT50 that can be produced with slow and careful laboratory acclimation). Based on the foregoing, a constant temperature exposure for 7 days would be expected to cause no more than LT1 levels of mortality at temperatures of 20.93 21.79 ° C. Converting the constant laboratory test exposure to a field exposure regime is especially difficult for this form of lethality data. Because the exposure times necessary to cause lethality reduce as temperatures continue to increase above the incipient lethal limit it is not appropriate to treat the laboratory results as weekly average temperatures. However, using the results directly as 7DADMax thresholds would overstate the risks since the time spent above the threshold will be only a small portion of each day while the original tests exposed fish to these temperatures LT50 Results for Salmon and Trout at Constant Temperature Exposures y = 0.2153x + 20.351 R2 = 0.3206 20 21 22 23 24 25 26 27 9 14 19 24 Acclimation Temperatures ( C) Temperature of LT50 Evaluating Standards for Protecting Aquatic Life in Page 99 Washington's Surface Water quality Standards for 24 hours per day. Thus the more defensible estimate would be one that falls between these two approaches, rather than containing values from either. Treating the constant laboratory exposure as a weekly average temperature would result in the estimate of a 7DADMax of 24.11 24.97 ° C ( 24.54) using it directly would result in the estimate of a 7DADMax of 20.93 21.79 ° C ( 21.36). Using these two approaches to bound the estimate results in the estimate that mortality will occur as 7DADMax temperatures exceed 21.36 24.54 with the best estimate expected to be the mean of the distribution ( 22.95 ° C).

Modeling Lethality of Fluctuating Temperature Regimes:

The concept of resistance time is very important to estimating potential lethality. It is well demonstrated that it is the time spent above a lethal threshold that determines whether or not short term lethal effects will occur. Different peak temperatures ( e. g., 22, 24, 27, 30 ° C), may all be lethal to an organism, but the organism can likely withstand these temperatures for variable lengths of time. A population of fish may be able to withstand 21 ° C for 7 days of constant exposure without any mortality, but have 50% of the population die after 2 days at 24 ° C. At 27 ° C 50% mortality may occur after less than 2 hours of exposure, and at 30 ° C, complete mortality may occur in just a few minutes.

In considering the effect of repeated hot days, it is important to incorporate the potential for cumulative effects over a series of days. DeHart ( 1974) found that lethal effects occur in relation to the area of the temperature time curve that is above a fish's incipient lethal level ( ILL); an accumulation of thermal effects occurs over periods of several days when the daily temperature cycle fluctuates above the incipient lethal level; and the time above the incipient lethal level influences the thermal resistance time independent of the lower temperatures experienced in fluctuating tests. In other words, the ability of a fish to resist a single day's exposure to a lethal temperature may not be sufficient, and fifteen minutes spent at 4 ° C over the ILL is of more consequence than the same time spent at 2 ° C over the ILL.

The results from laboratory lethality tests conducted at constant temperatures can be used to estimate lethality under fluctuating temperature conditions. This can be done by creating a simple model of the time to mortality using the laboratory studies of a duration of 7 days or less from table 4.18 above. Each temperature value is assigned a lethality indices which represents the proportion of a lethal exposure that occurs within a single day. Lethal loading stress is assumed to be cumulative such that the model can predict the number of consecutive days until 50% mortality will occur under any combination of diel temperature fluctuations. Because of the great variability in 7 day LT50 values, only a single representative value is used to represent this particular exposure period. A constant temperature of 21.85 ° C was chosen to represent an 7 day LT50 temperature, which represented the 25th percentile of the distribution of LT50 values. Alternatively, 23 ° C was considered since it represents both the regressed LT50 value at the lower expected acclimation temperature and is the median of the distribution of LT50 results. However, taking this alternative approach would have risked extrapolating the estimate beyond 50% of the actual test endpoints, and would not well incorporate the observed pattern of adult fish showing greater lethality at similar temperatures as juveniles who are the subjects of most of the tests. Page 100 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Figure 4.2 below shows a power curve regression of the LT50 data with a single representative value included to moderate the variability in the tests conducted for seven days. The equation of the regression line can be used to predict fifty percent lethality rates at any given duration of exposure. This equation ( y = 5E+ 28x 17.402) is used herein to model lethality under fluctuating temperature environments.

Figure 4.2. Regression of LT50 data with a single composite value for all 7 day tests.

LT50 Results for Salmon and Trout Using a Single Representative 7 Day Value  Power Curve y = 5E+ 28x 17.402 R2 = 0.7541 0 200000 400000 600000 800000 1000000 1200000 19 21 23 25 27 29 31 Test temperature Time to LT50 ( seconds)

If it is assumed that fish are acclimated to a series of temperatures ( representing the daily mean of a fluctuating environment) then the number of days until fifty percent mortality would be expected can be estimated ( See table 4.19 below). Since the 7 day exposure tests were composited using the 25th percentile of the 7 day LT50 values, the estimates would generally suggest that most ( 75% or more) stocks would have a greater degree of protection. The results of this modeled analysis suggest that at acclimation temperatures in the range of what can be expected in natural streams during the summer months ( 15 20 ° C) fifty percent mortality may occur to some stocks with a 7 day exposure at daily maximum temperatures of 22.13 22.47 ° C ( 22.3). This estimate is then converted to a temperature range that would be unlikely to result in any mortality ( an estimated LT1) by subtracting 2 ° C. This results in the estimate that direct mortality will be prevented if the 7DADMax temperature is maintained below 20.13 20.47 ° C ( 20.3). Temperature of Test ( ° C) Time to LT50 Endpoint ( seconds) 29.4 60 28.3 300 26.7 3000 29.5 5400 29.5 5400 29.5 5400 21.1 172800 24.7 172800 20.9 259200 22 276480 21.85 604800 20 1010880 Evaluating Standards for Protecting Aquatic Life in Page 101 Washington's Surface Water quality Standards Table 4.19. Modeled results showing the days to LT50 at various daily mean and daily maximum temperatures and assuming a 4.13 ° C per day change in temperature.

Laboratory Studies with Fluctuating Temperatures:

Coho Salmon DeHart ( 1974) reported that a cyclic temperature regime having 6 hours a day over 25 ° C produced 50% mortality in 1.5 cycles. In a 20 day test with highly fluctuating daily temperatures ( 5 23 ° C) having an average of 11 ° C, however, Thomas et al. ( 1986) found no increase in mortality. Acclimated age 0 and age 2 fish did not begin dying until the diel temperature range reached 4 25 ° C. Thomas et al. also reported that juvenile coho were able to feed and grow in fluctuating temperatures that approached their upper lethal limits. The studies of DeHart ( 1974) and Thomas et al. ( 1986) suggest that daily maximum temperatures of 25 ° C produce a risk of direct mortality, the level of that mortality may vary substantially but can be as high as 50%. The levels of fluctuations in the Thomas et al. work were so great as to significantly limit the time fish spent above temperatures that can be lethal with longerterm exposure. Converting the LT50 estimate at 25 ° C to an LT1 estimate by subtracting 2 ° C ( USEPA recommendation), yields the prediction that daily maximum temperatures below 23 ° C should prevent direct lethality in coho salmon over short term ( one week or less) exposures. The safety of taking this approach is also supported by the direct evidence of Thomas et al. ( 1986) where daily maximums of 23 ° C ( diel range 5 23 ° C) did not result in an increase in mortality. Daily mean Daily Max Days to LT50 15 22.13 6.802 16 22.13 6.81 17 22.13 6.836 18 22.47 6.911 19 22.13 7.12 20 22.13 7.743 Page 102 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Steelhead and Rainbow Trout Under fluctuating temperature test conditions, rainbow trout have been found to experience 50% mortality in a week of daily cycles from 21 27 ° C ( Lee, 1980). If 2 ° C is subtracted to reduce the level of mortality from 50% to 1% or less, this would change the daily maximum temperature to 25 ° C to prevent direct mortality.

Cutthroat Trout Golden ( 1976) tested the temperature tolerance of zero age coastal cutthroat stocks from western Oregon. It was found that seven diel cycles of 13 27 ° C resulted in 0 20% mortality. However, by increasing the peak temperature in the cycle 0.5 ° C ( 13 27.5 ° C) mortalities increased to 50 90% within 1 to 1.5 cycles. In CTM tests where the temperature is rapidly increased until the fish die or loose equilibrium, acclimation to 10 and 23 ° C yielded CTM values of 28.03 and 30.62 ° C. At a fluctuating equilibriums of 7.8 10 ° C and 13 23 ° C the CTM values were 27.64 and 30.31 ° C. Golden ( 1978) tested the lethality of significantly fluctuating temperature regimes with cutthroat trout. Incipient lethal levels ( ILL) were 25.5 ° C and 25.7 ° C for fish acclimated to 23 ° C and a fluctuating regime of 13 23 ° C, respectively. Golden estimated losses in one week of 10% or less at a fluctuating cycle of 13 27 ° C. Golden ( 1978) found that high mortality could still occur with temperatures as high as 25.5 25.7 ° C at constant exposures, even for cutthroat acclimated to high ( 23 ° C) daily maximum temperatures. The work of Golden ( 7976, 1978) suggests that 50% mortality can occur and temperatures from 25.5 27 ° C even where fish have been well acclimated to warm waters. After converting this range to one in which 1% or less ( LT1) mortality would be expected ( by subtracting 2 ° C) it would be expected that direct mortality could be avoided by maintaining daily maximum temperatures below 23 25 ° C. Since many of the test fish were carefully acclimated to warm waters prior to testing, the upper end of this range may pose greater risks to migratory stocks.

Dickerson et al. ( 1999, and unpublished data as cited in Dunham, 1999) tested the lethal tolerance levels of Lahontan cutthroat. Survival was 100% at 24 ° C but declined to 35% at 26 ° C. At 28 ° C mortality was complete in 48 hours. In a separate test of fluctuating ( 20 26 ° C) and constant ( 13, 20, and 23 ° C) temperatures no mortality occurred. Dunham ( 1999) concluded from a review of the literature that Lahontan cutthroat can survive weekly exposure to daily temperature fluctuations of 20 26 ° C, including 1 hour exposures to temperatures of up to 26 ° C.

The works of Dickerson ( 1999) and Golden ( 1976, 1978) can be used to support the position that cutthroat trout may be capable of tolerating daily maximum temperatures as high as 23 26 ° C ( 24.5) for up to a week of exposure without experiencing direct mortality. However, without the non indigenous Lahontan cutthroat data the estimate of lethality would change to 23 25 ° C ( 24 ° C) and should be viewed as a more defensible estimate of lethality in Washington's cutthroat trout populations. Evaluating Standards for Protecting Aquatic Life in Page 103 Washington's Surface Water quality Standards Summary of fluctuating lethality studies: In many of the fluctuating exposure studies reviewed, the laboratory test water had high diel fluctuations ( 14 ° C). These fluctuations are greater than what would often occur in natural waters and acts to significantly limit the amount of time spent each day spent above incipient lethal levels. The studies also included fish that were pre acclimated to relatively warm temperatures, and thus some natural migratory stocks may be at slightly higher risks. The works also included a non indigenous species of cutthroat that is widely found in desert environments and which may have different lethal thresholds than Washington's native cutthroat. Thus caution should be exercised in using the results from this line of evidence. Based on the fluctuating laboratory tests cited above, daily maximum temperatures above 23 25 ° C should be considered capable of causing direct mortality to salmon and trout. Since even very slight ( 0.5 ° C) temperatures increases in the daily maximum temperature have been shown to produce significant increases in mortality in this range, these values may best be treated as single daily maximum thresholds. However, the single daily maximum range of 23 25 ° C can also be converted to the standard metric of a 7DADMax temperature ( by subtracting 0.95 ° C). This approach yields the estimate that to avoid direct mortality the 7DADMax temperature should remain below 22.05 24.05 ° C ( 23.05).

Field Studies of Lethality:

Chinook Salmon The previously mentioned studies of lethality were predominantly conducted in a laboratory environment. Baker et al. ( 1995), however, modeled the escapement of smolts from the lower Sacramento River and determined an upper lethal temperature of 23 ° C. Burck ( 1993) used live box tests with juvenile chinook salmon, and found that daily maximum temperatures in the range of 25.5 26.6 ° C were lethal to all of the test fish after a single daily cycle of exposure ( daily minimums ranged from 13.3 16.1 ° C). Daily maximums in the range of 23.8 to 25.5 ° C ( minimums ranging from 11.1 13.3 ° C) resulted in 80% mortality over the four day test period. No mortality occurred in the three controls that had daily maximum temperatures from 14.4 17.2 ° C. While 50% mortality occurred in one treatment with maximums of 20.5 21.6 ° C, no mortality occurred in four other treatments with daily maximums in the range of 20.0 22.7 ° C. We can roughly compare Burck's data with values found in standardized laboratory tests using chinook salmon. If we assume the temperature midway between the daily maximum and the daily average is the acclimation temperature, then these live box tests generally demonstrated that at an acclimation temperature of 20.6 ° C the lethal temperature was 25.6 ° C, and at an acclimation of 18.3 ° C the lethal level was 24.7 ° C. At an acclimation temperature of 16.5 ° C, however, there was inconsistent but typically complete survival at up to 21.6 ° C.

High mortality has been observed in fish held in rivers with daily maximum temperatures of 23.8 25.5 ° C over a four day period. Reducing this range by 2 ° C would convert it to a range for daily maximum temperatures at which mortality would not be expected. This would yield the range of 21.8 23.5 ° C ( 22.65). This range was derived from daily maximum Page 104 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards temperatures over a four day exposure period. This range can be used to create a range that is based on a 7DADMax temperature metric. The estimate can also be bounded by treating the range as if it were representing either the 7DADMax temperature directly ( 7DADMax 21.8 23.5 ° C) and also as if it represents the single daily maximum temperature ( since it may have been the warmest day that triggered the mortality) and converting ( subtracting 0.95 ° C) that value to a 7DADMax estimate ( 20.85 22.55 ° C). This approach suggests that direct mortality would be prevented by maintaining the 7DADMax temperature below 20.85 23.5 ° C ( 22.18).

Steelhead and Rainbow Trout Sonski ( 1983) noted having success with culturing rainbow trout in ponds that that reached a summer maximum of 28.9 ° C, and Chandrasekaran and Subb Rao ( 1979) noted that rainbow trout in India were largely able to survive in rearing ponds with months having daily maximum temperatures in the range of 26 29 ° C. Neither of these works estimated lethality directly and cannot reasonably be used to suggest safe temperature ranges for rainbow trout. They can however be used to suggest that losses can sometimes be moderate ( acceptable from a fish culturing standpoint) at temperatures that reach highs of 26 29 ° C.

Summary of field studies: Only two of the four citations actually provide estimates of lethal temperature ranges. These two studies both can be used to support the estimate that lethality should be expected as the 7DADMax temperature exceeds 20.85 23.5 ° C ( 22.18). The rearing pond observations that were also reviewed suggest that mortality rates sometimes may not become significant in cultured rainbow trout even though daily maximum temperatures may reach 26 29 ° C.

General Measures of Lethal Stress:

Cutthroat Trout Titus and Vanicek ( 1988; as cited in Muoneke and Childress, 1994) reported that mortality of cutthroat trout caught and released by angling was less than 2% at temperatures below 17 ° C but rose to 49% as the temperature neared 21 ° C. Evaluating Standards for Protecting Aquatic Life in Page 105 Washington's Surface Water quality Standards Summary of Lines of Evidence on Lethality:

Table 4.19. Direct lethality to salmon and trout with short term exposure ( 7 days).

Line of Evidence 7DADMax ( ° C) Midpoint ( ° C) Comments Ninety percentile range of constant laboratory tests with 1% or less mortality estimated. 21.05 24.23 22.64 Based on the 5th and 95th percentiles of the distribution of 7 day LT50 results at acclimations from 5 to 23 ° C. Constant laboratory tests regression of 1% or less mortality estimate. 21.36 24.54 22.95 Regression of all of the lethality data for acclimations between 12 and 16 ° C.

Modeled exposure to fluctuating temperatures based on constant laboratory tests. 20.13 20.47 20.3 Assumes a steady diel fluctuation of 4.13 ° C per day for a 7 day period. LT50 converted to an LT1 by subtracting 2 ° C. Fluctuating laboratory exposure studies. 22.05 24.05 23.05 Generally based on high diel fluctuations and including a non indigenous form of cutthroat trout. Field Studies with Fluctuating exposures 20.85 23.5 22.18 Based primarily on a study of chinook held a range of temperature exposures in a NW river. Best estimate of threshold 21.09 23.36 mid. pt 22.23 The absolute range is a 7DADMax of 20.13 24.54 ° C, with a mean range of 21.09 23.36 ° C, and with an overall midpoint of 22.23 ° C. The lower end of this range is based on the results of several studies using different species in a controlled laboratory environment at moderate acclimation temperatures. This gives it greater weight than if only one species was tested or the results came from only one study at low acclimation temperatures. Extra caution is warranted because actual exposure periods greater than 7 days at very near but not exceeding the estimated lethal threshold can exert a cumulative stress ( lowering the temperature that would cause lethality over the longer period of exposure). For these reasons, the lower half of the potentially protective range ( 21.09 22.23 ° C, midpoint of 21.66) should be considered to be a more confident estimate for statewide use. Therefore, to prevent direct lethality it is concluded that the 7DADMax should be maintained below 21.66 ° C, or single daily maximum ( adding 0.95 for conversion) temperatures maintained below 22.61 ° C.

Near Instantaneous Lethality Page 106 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards In the previous discussion the period of exposure was selected to represent a reasonable chronic field exposure ( i. e., a 7 day duration). Higher temperatures, however, will exert lethal stress in much shorter periods of time, such that at some temperature lethality will occur almost instantaneously. Since wastewater can sometimes be discharged at very high temperatures ( 33 40 ° C) there is a need to ensure that lethal barriers are not permitted to occur in Washington's waters.

Data is available on exposure periods from 4 to almost 4,000 seconds have been used to evaluate the risk of instantaneous high water temperatures. The purpose of this analysis is to determine if a limit should be placed on the temperature of water discharged to waters of the state. The premise of such a restriction would be that at a given high temperature fish passing through the plume of hot water will be immediately killed.

Data is available for numerous fish species with the tests conducted a various acclimation temperatures and recording several important mortality endpoints ( see table below). These endpoints ranged from when deaths began in the test population ( herein described as the LC1) through where 50 percent of the population had died ( LC50) to where 100 percent mortality ( LC100) occurred. Also included are the results of a study that recorded the points where short term exposures caused an identifiable increase in mortality due to increased predation.

The complete data set was examined by separating out different acclimation ranges and different endpoints, by only looking at endpoints with significant mortality occurring in less than 10 minutes, and by lumping all the data together to examine the general endpoint of lethality. This process was used as a form of sensitivity analysis to gain better confidence and understanding of the strength associated with extrapolating beyond the lowest tested endpoint duration of 4 seconds. It is assumed here that extrapolation to a 1 second exposure duration represents instantaneous exposure and thus should be used to define instantaneous lethality. The power curve that best represented the data was used to create the extrapolation equation used in the following discussion. The following is intended to provide a general understanding of the analyses that were conducted, but does not represent an exhaustive description.

Separation by acclimation temperature and by test endpoints resulted in predicted 1 second LC1 ( deaths beginning) to LC100 ( all dead) values ranging from of 32.76 ° C to 34.32 ° C at moderate acclimation temperatures of 15 15.6 ° C. The 1 second endpoints at cold acclimation temperatures ( 9 10 ° C) ranged from 32.45 ° C to 34.34 ° C. Since sensitivity to temperature is well demonstrated to be dependent upon prior acclimation temperature, this analysis is believed to be the most appropriate. In extrapolation from a single study using rainbow trout at an unknown acclimation temperature, it was found that increased predation rates may occur with a 1 second exposure to 33.47 ° C. Since all of these data sets were small, analyses were also made that lumped together the acclimation temperatures. This resulted in an estimated 1 second LC1 ( deaths beginning) to LC100 ( all dead) values ranging from 32.59 ° C to 34.69 ° C. In examining only the LC50 endpoints that occurred within 4 minutes or less, it was estimated that the 1 second LC50 ( 50% dead) would occur at 34.69 ° C. And Evaluating Standards for Protecting Aquatic Life in Page 107 Washington's Surface Water quality Standards when examining all of the available short term mortality data together, to create the largest data set for extrapolation, it was predicted that some mortality will occur with a 1 second exposure of 33.18 ° C. The point of this discussion is to demonstrate that the estimations cluster between 32.5 to 34.6 ° C, a very narrow range. Taking the midpoint of this range to further improve confidence in using an extrapolation would suggest that an almost instantaneous exposure to temperatures of 33.5 ° C or greater will likely result in at least some mortality to passing fish. Given that 100% mortality has been demonstrated at 32 ° C in 11 seconds at low acclimation temperatures ( 9 10 ° C) and 50% mortality in 8 seconds, and that mortality has been noted at low acclimation temperatures to begin in 4 seconds the estimate should not be considered overly conservative. The fact that greater sensitivity can be expected at even lower winter and early spring acclimation temperatures ( 4 8 ° C), and the fact that lethal exposures are cumulative with all temperatures above the lethal threshold, suggests temperatures greater than 33 ° C should not be allowed where that water would result in the entrainment of fish for a duration of 1 second or longer. For this reason, discharges with temperatures greater than 33 ° C should be evaluated for possible risks of creating a lethal barrier to organisms. The changing velocity and temperature of the discharge plume should be examined to ensure that time spent at or above 33 ° C does not exceed 1 second ( it should generally be assume the organism is entrained and is moving along with the plume in the analysis).

Figure 4.20. The following is an example of one of the data subsets examined:

Acclim. Temp. ( ° C) Temperature of Test ( ° C) Time ( sec.) Endpoint of Test Predicted Endpoint Temperatures 15.6 26.7 2,970 LC50 26.94052 15 28 1,350 LC50 27.505 15.6 29.4 26 LC50 30.51586 15.6 32.2 10 LC50 31.29244 Predicted 2 32.64542 Predicted 1 33.246 The following table summarizes the data used for the analysis of lethality. Median Mortality at Warm Acclimation ( 15 15.6C)  LC50 Power curve 2,970 1,350 26 10 y = 33.246x 0.0263 R2 = 0.8644 25 26 27 28 29 30 31 32 33 34 35 0 500 1,000 1,500 2,000 2,500 3,000 3,500 Time ( seconds) Temperature ( C) Page 108 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Table 4.21. Summary of data used to determine risk of near instantaneous lethality.

Author or Study Species Acclimation Temp. ( ° C) Temperature of Test ( ° C) Time to Effect ( seconds) Endpoint Reported Snyder and Blahm, 1971 Chum 15.6 26.7 2,640 LC1 15.6 26.7 2,970 LC50 15.6 26.7 3,960 LC100 15.6 29.4 15 LC1 15.6 29.4 26 LC50 15.6 29.4 60 LC100 15.6 32.2 6 LC1 15.6 32.2 10 LC50 15.6 32.2 15 LC100 10 26.7 100 LC1 10 26.7 240 LC50 10 26.7 2,220 LC100 10 32 4 LC1 10 32 8 LC50 10 32 11 LC100 Coutant, 1972( a) Chinook 15 28 1,350 LC50 Rainbow 17 19 30.5 900 LC50 Lyytikainen, Koskela, and Rissanen ( 1997) Char 15 29 120 LC50 18 29 240 LC50 Baroudy and Elliott, 1994 Char 5 23.3 600 LC50 5 24.1 600 LC50 5 25.7 600 LC50 Groves and Mighell, 1970 Salmon 9 30 10 LC16 9 30 35 LC100 Coutant, 1972( b) Rainbow 30 33 Increased Predation 28 120 Increased Predation 26 1,920 Increased Predation c) Temperature Influenced Fish Diseases Temperature affects both the occurrence and severity of many diseases and infections important to fish and other aquatic life. While some diseases are associated with holding fish at very cold temperatures, and some are prevalent across the full spectrum of temperatures Evaluating Standards for Protecting Aquatic Life in Page 109 Washington's Surface Water quality Standards occurring in Washington's waters, many are facilitated by temperatures within or slightly above the fully protective temperature range for the growth of our native fishes. This discussion is limited to those diseases that are known to cause illness in populations of wild fish that are facilitated by temperatures at the upper end of the physiologically protective range of our indigenous fish. The intent is to identify where a stream temperature standard may need to be set below this upper end to prevent, or at least reduce the severity of, disease outbreaks in natural fish populations. It must be recognized, however, that temperature standards by themselves will not eliminate the risk of disease in fish. Besides warm water diseases, native fishes are harmed by numerous very important cold water fish diseases, such as bacterial kidney disease. It is of course reasonable that most fish pathogens thrive in cold waters here in the northwest since the pathogens themselves have evolved along with our native fishes.

Fish diseases can be divided into four types of infections: 1) bacterial, 2) viral, 3) fungal, and 4) parasitic. Regardless of the type of infection, temperature affects both the virulence of the disease as well as the immune system of the host fish. When environmental conditions are optimal for the disease it grows more rapidly and is often more virulent. If the environmental conditions are more optimal for the disease then they are for the fish, then there is a greater likelihood that the disease will be able to overcome the host's defense systems and create serious illness ( Wedemeyer and Goodyear, 1984). Just as each disease causing organism has an optimum temperature range, they also have lethal boundaries or limits of activity. If the temperature is above or below these thresholds, the disease causing organism will be unable to reproduce or grow, and thus will be unable to affect disease in fish. Catastrophic outbreaks of many bacterial diseases are associated with water temperatures that are optimal for the bacterium but above the optimal temperature for the infected fish.

While some diseases will have thresholds of temperature above or below which the disease organism is unable to grow, most diseases are able to grow at some temperature that occurs during the year in Washington's waters. The primary goal, therefore, cannot be to set standards at which diseases organisms will not exist. A complicating factor in evaluating diseases is that most have multiple, sometimes hundreds, of strains. Individual strains can have significantly different characteristics for optimal infection and virulence. Since researchers often do not specify specific strains examined, this creates variability in research results that may very well just be the consequence of testing different strains. Further, native fish differ in susceptibility to these diseases both by subspecies and by individual stock ( Li et al., 1987, and others).

The focus of this effort is to identify pathogens that: 1) occur in freshwaters; 2) are enhanced by increasing water temperatures in the upper optimal range of our native fishes ( roughly 14 18 ° C); and 3) have been associated with serious outbreaks of disease in indigenous wild fish populations.

In reviewing the literature, only three diseases appear to meet all three criteria, these are two parasites ( Ichthyophthirius multifillis and Ceratomyxa shasta) and columnaris disease. While numerous other diseases are documented to be influenced by warming temperatures, these others tend to be primarily problems associated with intensive fish culturing facilities, Page 110 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards or are associated with species and temperatures not common in our natural waters. Since there is little suggestion that any of these other diseases pose a significant threat to the welfare of our native fishes, they will be used only broadly to discuss how temperatures influence the health of fish and in support of the findings for the two specific diseases discussed below.

Ichthyophthiriasis. Post ( 1987) notes that the etiological agent for ichthyophthiriasis is the largest protozoan found on fishes. Occurring on both hatchery and wild fish ( Bell, 1986), ichthyophthiriasis is considered one of the most prevalent diseases of fishes ( Post, 1987). Bell ( 1986) notes that outbreaks in fingerlings often occur at temperatures above 15.5 ° C, and the optimum temperature for the organisms is 25 27 ° C. Post ( 1987) notes that temperatures over 12 15 ° C are more suitable for reproduction, and that disastrous losses have occurred in trout culture where water warms to near 20 ° C.

Ceratomyxiasis Shasta. An obligate parasite widespread in the Northwestern U. S. where anadromous salmonids return from the ocean to spawn. While not important to adult fish, C. shasta may be devastating to very young salmonids ( Post, 1987) and is a parasite of concern for northwest salmonids ( Bartholomew, Rohevec, and Fryer, 1989; and Conrad and Decew 1961; as cited by Hoffman and Bauer, 1971). Bartholomew, Rohevec, and Fryer ( 1989) note it is important because it not only causes losses in hatchery reared and wild juvenile salmonids but also contributes to prespawning mortality in adult salmon.

Infections of Ceratomyxa shasta are temperature dependent ( Yamamoto and Sanders 1979, and Udey et al. 1975; as cited in Bartholomew, Rohevec, and Fryer, 1989). Udey et al. ( 1975) found that rainbow trout exposed to the infective stage of C. shasta and held at water temperatures of 6.7 to 23.3 ° C had little or no ability to overcome the infection, and that the mean time from exposure to death was directly correlated to temperature ( about 155 days at 6.7 ° C and 14 days at 23.3 ° C). In rainbow trout the disease process was suppressed at 3.9 ° C; however, when the infected fish were subsequently transferred to water at 17.8 ° C, many died. Mortality in exposed rainbow trout was greater than 92% at temperatures above 12.2 ° C, 84 75% at 9.4 6.7 ° C, and zero at 3.9 ° C ( Fryer and Pilcher, 1974). In juvenile coho salmon mortality was 92 100% at 20.6 ° C and above, 57 59% at 17.8 ° C, 13 31% at 15 12.2 ° C, and 4 0% at 9.4 ° C and lower.

Evidence suggests that only salmonids are susceptible to C. shasta infections, but that susceptibility may vary within species. Juvenile salmonids originating from waters containing the infective stage of the parasite have been found to be more resistant than strains from areas free of the infective stage ( Johnson 1975, Zinn et al. 1977, Buchanan et al. 1983, and Hoffmaster 1985; as cited in Bartholomew, Rohevec, and Fryer, 1989). Sanders et al., ( 1970; as cited in Li et al., 1987) reported that infected coho show an increasing susceptibility as temperature rises: mortality below 10 ° C is 2% at most, 22% at 15 ° C, and 84% at 20.5 ° C. In contrast, mortality of infected juvenile steelhead trout can be as high as 80% and is independent of temperature. Ratliff ( 1983) studied the infective stage of Ceratomyxa shasta in the Deschutes River of central Oregon and found that C. shasta emanates from the bottoms reservoirs, and that the infective period began in the spring when Evaluating Standards for Protecting Aquatic Life in Page 111 Washington's Surface Water quality Standards river temperatures were between 6.9 and 8.6 ° C. The author noted that based on his observations C. shasta spores are more likely observed when test fish are held during the incubation period at 10 ° C rather than at warmer temperatures. Waters where infected fish have been found do not necessarily contain the infective stage of the parasite ( Johnson et al. 1979; as cited in Bartholomew, Rohevec, and Fryer, 1989), and even in the Columbia River Basin where infected fish migrate and distribute spores throughout the drainage, the infective stage has not been demonstrated in many tributaries. The authors ( Bartholomew, Rohevec, and Fryer, 1989) suggest that the geographic isolation of the disease supports the position that presence of the spores is insufficient to cause transmission and disease, and that a yet unidentified factor ( perhaps an intermediate host) is required for the completion of the life cycle of this parasite.

Columnaris Disease. There is little doubt that columnaris disease is the most important warm water disease for our native salmonid populations. Frequent and catastrophic losses to natural populations throughout the Pacific northwest are well document throughout the literature. For this reason, the prevention of human caused additional losses from columnaris disease should be considered a critical element in setting temperature standards for the state of Washington.

In evaluating the research it is important to recognize that there are probably at least 1,200 strains of columnaris in Washington, and that strains can be categorized as possessing low, medium, and high levels of virulence ( Pacha, 1961). High virulence strains are infective and capable of producing high rates of mortality at low temperatures, while low virulence strains are problematic only at higher temperatures ( Bell, 1986). Since only a handful of authors categorized the strains they were evaluating, care must be exercised in broadly applying the conclusions of any one study. Table 4.22 below summarizes the results noted in the literature.

The milestones of 12 13, 15 16, 18 20 ° C are cited extensively in both field and laboratory research, and show generally consistent levels of increasing risk of columnaris disease. In field studies it has been noted that as river temperatures rise to about 10 12.8 ° C, researchers begin isolating columnaris strains from water ( Fujihara and Nakatani, 1970). Temperatures above 13 ° C were associated with the occurrence columnaris in thirteen species of fish collected from the Columbia River watershed ( Fujihara and Huntgate, 1970). In the Fraser River in Canada it was found that prespawning mortality of sockeye was eliminated by maintaining average temperatures on the spawning grounds of 12.8 ° C ( Colgrove and Wood, 1966). This finding was generally supported by the work of Johnson and Brice ( 1952, as cited in Colgrove and Wood, 1966) that exposed four species of salmonids to columnaris for six months and found that no mortalities developed when daily maximum temperatures were 12.8 ° C or less. At maximum temperatures of 15.6 18.3 ° C, mortalities increased to 0.7 15.5% in three species but remained zero in the fourth, and at maximum temperatures 18.3 21.1 ° C all four species showed high mortalities ( 37.5 82%). These results are supported by other researchers studying columnaris under natural environmental conditions. Page 112 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards The spread of columnaris throughout the Columbia River basin has been noted to be linked to the water temperatures occurring during individual years. In warmer years, columnaris disease is widespread throughout the entire basin, but in cooler years, the first major exposure occurred at McNary Dam and the warmer tributaries ( Pacha and Ordal, 1970). A difference of heating or cooling natural river water 2.2 ° C from its natural ( 17.7 21.7 ° C) condition was shown to increase and decrease mortality rates in naturally exposed fish ( Fujihara, Olson, and Nakatani, 1971). While the decrease resulted in only a modest decrease ( 4.2%) in mortality ( 6.2 versus 10.4%), the increase resulted in a more substantial increase ( 19.5%) in mortality ( 29.9 versus 10.4%).

At river temperatures of about 15 ° C isolation of columnaris cultures is typically quite successful ( Ordal and Pacha, 1963; Pacha and Ordal, 1970), with 15 ° C found also to be a demarcation point between high ( 54%) and moderate ( 22%) levels of infection in the crowded spawning channels of the Columbia River. Scrap fish collected from waters throughout the Columbia River basin were found to exhibit the disease when warmed to 16.7 ° C ( Pacha and Ordal, 1970). At river temperatures above 18.8 ° C strains of low and intermediate virulence can be readily isolated from fish ( Pacha, 1961; Bell, 1986). Major outbreaks are said to almost always occur during periods in which the water temperature was 18.3 21.1 ° C ( Pacha, 1961), and an average mid summer river temperature of 20.3 ° C was associated with a catastrophic outbreak in sockeye salmon in the Columbia River ( Fish, 1948).

Laboratory tests generally confirm what has been found through these field or controlled channel studies. A complication is created by looking strictly at mortality rates from these laboratory tests. Fish are generally injected with or exposed to high doses of the pathogen, and some are inoculated with high virulent strains while others with low or intermediate virulent strains. Putting aside these general problems with comparing laboratory test results we can see the same basic patterns emerge as were found in field research. Constant temperatures of less than 12 ° C result in low to no infections or mortalities ( Fryer and Pilcher, 1974; Post, 1987; Fujihara and Nakatani, 1970; Ordal and Pacha, 1963). Constant temperatures of 15 18 ° C have produced a wide range of mortalities, but is most characterized by moderate ( typically 20 60%) to heavy ( 80 100%) mortality. In this range, authors that have made the distinction have shown high virulence strains to be commonly associated with the highest mortality ( see table 4.22 for references). At constant temperature exposures of 20 23.6 ° C, mortalities of infected fish are consistently very high ( 70 100%) ( Ordal and Rucker, 1944; Fryer and Picher, 1974; Fish and Rucker, 1943; as cited in Ordal and Pacha, 1963; Holt et. al., 1975). Evaluating Standards for Protecting Aquatic Life in Page 113 Washington's Surface Water quality Standards Table 4.22. Summary of literature findings for columnaris disease.

Approximate Temperature Range or Direction Categories of Effects of Interest noted in the literature associated with the temperature range Citation from the Literature < 12 Seldom infectious; difficult to isolate in the field; and low ( 0 8%) fatalities experimentally infected fish. Fryer and Pilcher, 1974; Post, 1987; Fujihara and Nakatani, 1970; Ordal and Pacha, 1963 13 Organism begins to be isolated in the water and fish; not associated with measurable prespawning mortality; moderate ( 0 20%) to high ( 20 100%) mortality in experimentally infected fish. Holt et al., 1975; Fryer and Pilcher, 1974; Fujihara and Nakatani, 1970; Johnson and Brice, 1952 as cited in Pacha, and Colgrove and Wood, 1966; Fish, 1944; USEPA, 1976; Fujihara and Huntgate, 1970; Colgrove and Wood, 1966 14.4 Average river temperature not leading to disease. Colgrove and Wood, 1966 < 15 15.6 Rarely a problem; mortality from low virulence strains decline; incidence of disease in river declines to 22%. Amend, 1970; as cited in Austin and Austin; Johnson and Brice, 1952 and Rucker, 1944 as cited in Pacha, 1961; Garnjobst, 1945, as cited in Colgrove and Wood, 1966; Fujihara and Olson, 1962, as cited in Colgrove and Wood, 1966 15 16.7 Moderate ( 31 56%) mortalities become more consistent. in infected test fish; disease appears in Scrap fish after temperature elevation; epizootics in aquarium. Holt et al., 1975; USEPA, 1976; Fryer and Pilcher, 1974; Pacha and Ordal; Colgrove and Wood, 1966, as cited in Pacha and Ordal, 1970; Post, 1987 15.6 16 Moderate ( 60%) mortality of injured fish; high mortality ( 80 100%) from high virulence strains; prespawning mortality 63 81%, two week average temperature necessary to initiate pathological effects in river; moderately high ( 30 64%) mortality in infected test fish. Post, 1987; Pacha and Ordal, 1970; Colgrove and Wood, 1966; Fish, 1944; Ordal and Pacha, 1963; Ordal and Rucker, 1944, as cited in Pacha and Ordal, 1970 > 15 15.6 Easy to isolate in the field; associated with seasonal mortality in hatcheries; mortality and morbidity become factors in natural waters; outbreaks of high virulence strains; initiated mortalities in migrating sockeye; disease incidence in river becomes high ( 54%). Ordal and Pacha, 1963; Fujihara and Nakatani, 1970; Post, 1987; Bell, 1986; Colgrove and Wood, as cited by Gilhousen, 1970; Fujihara and Olson, 1962, as cited in Colgrove and Wood, 1966 13 18 Low ( 0.6 7.7%), moderate ( 20 50%), and high ( 60 100%) mortality in exposed test fish. Known virulent strains resulting in highest mortality. Fryer and Pilcher, 1974; Johnson and Brice, 1952, as cited in Pacha, 1961; Pacha and Ordal, 1970 15.6 18.3 Low ( 0.7 15.5%) mortality in three species of Johnson and Brice, 1952, as cited Page 114 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards salmonids in Colgrove and Wood, 1966 15.9 19.9 Fluctuating river temp with low ( 6.2%) mortality. Fujihara, Olson, and Nakatani, 1971 17 18 Mortality sometimes moderate ( 37 50%) but mostly very high ( 99 100%) in infected test fish; explosive infections; high mortality from all strain types. Fryer and Pilcher, 1974; Holt et al., 1975; USEPA, 1976; Pacha and Ordal, 1970 17 21.7 Fluctuating river temp with 10.4% mortality. Fujihara, Olson and Nakatani, 1971 < 18 Deaths greatly diminish. Ordal and Pacha, 1963 > 18 Mortality high from all strains, low and moderate strains isolated. Johnson and Brice, 1952, and Rucker, 1944, as cited in Pacha, 1961 18 22 Mortalities moderate to high ( 37.5 82%) in infected fish; most outbreaks; fish found releasing columnaris; Epizootics. Johnson and Brice, 1952, as cited in Colgrove and Wood, 1966, and as cited in Pacha, 1961; Fujihara and Nakatani, 1970; Amend, 1970, as cited in Austin and Austin, 1987; and Davis, 1922, Nigrelli and Hunter, 1945, Isom, 1960, and Johnson and Brice, 1952, as cited in Pacha, 1961 19.9 23.9 Fluctuating river temp with 29% mortality. Fujihara, Olson and Nakatani, 1971 20 21 Outbreaks of low virulence strains; mortality high ( 70 100%) in infected test fish, catastrophic outbreak, 28 75% morbidity in river population; outbreaks in physically stressed fish; serious epidemics. Bell, 1986; Ordal and Pacha, 1963; Pacha and Ordal, 1970; Fish, 1948; Holt et. al., 1948; Fryer and Pilcher, 1974; Post, 1987; Fish, 1944 22.2 23.6 Mortality 100% in infected test fish; summer maximum associated with devastating outbreak. Ordal and Rucker, 1944, as cited in Pacha and Ordal, 1970; Fish, 1948; Fryer and Pilcher, 1974 25 37 Optimum growth temperature for organism. Garnjobst, 1945, as cited in Colgrove and Wood, 1966; Pacha, 1961; Post, 1987 Based on a review of the available literature, it is concluded that for columnaris, Ceratomyxiasis Shasta, and Ichthyophthiriasis, as well as for warm water induced diseases in general, the following general statements hold true:

1. Average temperatures below 12 13 ° C significantly and often completely eliminate both infection and mortality; 2. Average temperatures above 15 16 ° C are associated with often serious rates of infection and noticeable mortality; and 3. Average temperatures above 18 20 ° C are commonly associated with very severe infections and often catastrophic outbreaks of many fish diseases. Evaluating Standards for Protecting Aquatic Life in Page 115 Washington's Surface Water quality Standards Treating these ranges as either daily or monthly average temperature may best bracket the exposure periods associated with the spread of disease causing organisms. Adding 0.58 ° C and 3.18 ° C, respectively, converts a maximum summer daily and monthly average temperatures to estimated 7DADMax temperature metrics. This approach yields the following estimates ( Table 4 24):

Table 4.24. Warm water disease risk to salmon and trout.

Disease Incidence Level 7DADMax ( ° C) Midpoint ( ° C) Virtual elimination of warmwater disease effects 12.58 16.18 14.38 Avoiding serious rates of infection and mortality 15.58 19.18 17.38 Severe infections and catastrophic outbreaks 18.58 23.18 20.88 To reduce the risks of serious infection and mortality from warm water mediated bacterial and parasitic diseases, it is concluded that the 7 day average of the daily maximum temperatures ( 7DADMax) should not exceed 15.58 19.18 ° C ( 17.38). This approach will provide safe harbor for resident species and critical life stages as well as serving to reduce or eliminate disease caused prespawning mortalities in migrating fish. When average river temperatures exceed 20 ° C, or 7DADMax temperatures exceed 20.88 ° C, explosive infection rates and the risk of catastrophic population level outbreaks in natural populations become a serious concern.

The research evaluated in this paper has focused on protecting cold water fish communities. Therefore, the above conclusions may not be applicable, and are therefore not recommended for application, to any designated habitat for warm water fish species. Information on the disease threats to native warm water fishes was not discovered during the review of the available literature. For warm water fish habitat it is recommended that temperatures be maintained within the range of what otherwise is expected to produce healthy warm water fish communities. By maintain the general health of these species it will also increase their resistance to potential diseases.

d) Smoltification and Sea Water Adaptation Smoltification is the name given to the physiological, morphological, and changes that occur in anadromous fish as they prepare to leave fresh waters for life in saline marine waters ( Clarke and Hirano, 1995; Wedemeyer, Saunders, and Clarke, 1980; Sauter and Maule, 1997, 1999). The greatest concerns at this stage of life would be that: 1) parr fail to migrate because of temperatures that are too warm ( Clarke, Shlebourn, and Brett, 1981), 2) that they will migrate but not be fully capable of living in marine waters ( Marine, 1997), or 3) that delays in smoltification could require that juvenile fish remain in the estuarine environment longer and experience enhanced predation.

Pennel and Barton ( 1996) provided an excellent summary of the process of smoltification: In marine and estuarine waters the salinity in the water surrounding the fish is greater than the Page 116 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards salinity of the internal body fluids. The gradient produced tends to draw out the water from the body of the fish while salts from the surrounding water diffuse inward. The lost water can be replaced by drinking the saline marine water but salt must be removed from the body to prevent detrimental accumulation. The process of removing sodium ions from the blood takes place in through special cells in the gills. Sodium ions are transported from the area of high concentration of the cells to the external environment down a concentration gradient via sodium channels. Energy to drive the sodium pump comes from the conversion of adenosine triphosphate ( ATP) to adenosine diphosphate ( ADP), a reaction catalyzed by the enzyme sodium/ potassium adenosine triphosphatase ( Na+/ K+ ATPase). In order to maintain neutrality, Cl diffuses directly from the chloride cell into the apical space and external environment, with the activity of the chloride cell probably under hormonal control ( Pennel and Barton, 1996). A major change that occurs during smoltification is a dramatic increase in the number and activity of chloride cells in the gills. An increase in Na+/ K+ ATPase activity indicates chloride cell activity and monitoring this activity is one of the useful smolt indicators. changes such as saltwater preference and migratory behavior ( Folmar and Dichoff 1980; as cited in Pennel and Barton, 1996) often become evident as the juvenile fish become smolts. A performance monitoring method to evaluate functional smolts is the saltwater challenge test. The saltwater challenge test is used to determine if smolts are capable of regulating their blood Na+. Fish are placed into a known concentration of salt water and blood samples are taken from fish 24 hours later for Na+ analysis. If the fish are capable of regulating blood Na+ levels to < 170 meq/ l, they are considered as functional smolts ( Pennel and Barton, 1996).

This ability to regulate and maintain the osmotic gradient across a fish's body surface, whether the fish is exposed to the hydrating conditions of fresh water or the dehydrating conditions of sea water, is referred to as osmoregulation. While salmonid stocks that move to the estuarine environments early as young fry or juveniles ( chum, pink, some populations of coho, and to some extent ocean type chinook) tend to develop a more rapid tolerance to saline waters, those that have an extended period of freshwater residence as juveniles ( coho, sockeye, and stream type chinook) possess a limited capacity for ionic regulation in hyperosmotic media prior to reaching the smolt stage ( Clarke and Hirano, 1995).

While the evidence suggests that smoltification is triggered by endogenous rhythms ( Hoar, 1988; Wagner, 1974); growth ( Ewing et al., 1979), photoperiod ( Folmar et al., 1982 Wagner, 1974), and temperature all critically influence the timing, extent, and success of the transition process. Temperature influences smoltification in at least two primary ways. The first is that juvenile fish must generally reach a critical size to be capable of successfully smolting ( Clarke and Shelbourn, 1985; Mahnken and Waknitz, 1979). The second is that temperature affects critical enzyme activities that control the ability to excrete salts from the blood   and thus to be able to live for an extended period in saline waters ( Zaugg and Wagner, 1973; Wagner, 1974; Wedemeyer, Saunders, and Clarke, 1980; Duston, Saunders, and Knox, 1991).

Laboratory and field work associating temperature with the smoltification of salmonids has to date focused on steelhead trout, chinook salmon and coho salmon, all species that have a Evaluating Standards for Protecting Aquatic Life in Page 117 Washington's Surface Water quality Standards considerable period of fresh water rearing prior to moving to marine waters. The following summarizes the studies reviewed on these species:

Steelhead Trout In Washington, migratory smolts usually move to sea during April through June, with a peak about mid April ( Wydoski and Whitney, 1979). Zaugg et al. ( 1972), Zaugg and Wagner ( 1973), and Adams, Zaugg and McLain ( 1973) suggest that temperatures higher than about 12 13 ° C may alter the juvenile migratory behavior and physiological condition of steelhead trout. In their work these authors found that fish held at 15 ° C and 20 ° C experience high rates of mortality with subsequent transfer to sea water ( 30ppt). The authors also noted that smolts held at 10 ° C were unable to maintain high NaK ATPase activity throughout the smolt season since at the beginning of the season the increase in activity for this group was similar to that in the 6.5 ° C group. Steelhead maintained at 6.5 or 10 º C, however, experienced an elevation of Na+, K+ stimulated ATPase activity and assumed the characteristic slender, silvery appearance of smolts. Adams, Zaugg, and McLain ( 1975) evaluated winter and summer steelhead trout metamorphosis at six different growth temperatures ranging from 6 to 15 º C. Salt water survival in 35% sea water at 10 º C was used to determine the extent of transformation. The highest temperature where a transformation was indicated was 11.3 º C. By April fish reared at 6 º C had elevated ATPase levels typical of smolts or migratory animals and showed 92% survival in sea water. Ten and 11.3 º C reared fish showed a shortlived elevation in ATPase in mid April alone concurrently with 100% sea water survival at that time. Only in 6 º C reared animals did the salt water survival ability continue into May. Zaugg ( 1981) found exposures of fish to 13 ° C resulted in a delay in migration, fewer total fish attempting migration, and lower gill Na+ K+ ATPase activity. Wagner ( 1974) found that parr smolt transformation in steelhead appears to be based on endogenous rhythm. Wagner also found a tendency for fish reared at a normal temperature cycle ( 6.9 18.6 ° C) to migrate in greater numbers than those that experienced a constant temperature regime ( 12.3 ° C). This was consistent with Wagner ( 1971) where fish reared under constant photoperiods and normal temperatures also migrated in greater numbers than fish receiving a similar photoperiod but a constant temperature. Zaugg ( 2001) summarized a study done in 1977 assessing the effect of barging and trucking on the state of smoltification in Dworshak steelhead. Smolts held in water below 10 ° C had no trouble in maintaining elevated ATPase activities, whether of hatchery or wild origin. However, barged two year old steelhead smolts held in the Columbia River water ( 12.5 13.6 ° C) reverted to parr like gill ATPase activities within approximately 2 weeks ( from May 6 to May 21). Smolts held in water below 10 ° C retained a smolt level gill ATPase activity at least through June 8 when the experiment was terminated. Zaugg ( 2001) summarized the work reported by Dr. H. W. Lorz in December, 1974, to the Annual Northwest Fish Culture Conference. Three groups of winter steelhead were reared at the laboratory under normal photoperiod but different constant temperatures ( 8, 12, and 16 ° C). Only the fish reared at 16 ° C did not show an increase in ATPase activity during April. Samples of the fish were released into a small coastal stream. The fish reared at 16 ° C did not migrate at the same rate as those fish reared at lower temperatures, with a portion of these fish showing a three week delay. However, measurements from downstream migrants showed that the ATPase activity had increased Page 118 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards during this three to four week period. This study supports the position that there is a close relationship between elevated gill Na+ K+ stimulated ATPase activity and seaward migratory movement; as well as providing information on the deleterious effect of elevated temperature on parr smolt transformation. In a second part of this study, two groups of steelhead were maintained in laboratory tanks, one with water at 8 ° C and the other at 16 ° C into May. At the time when elevated enzyme activity was observed in the fish held at 8 ° C, enzyme activity remained low and unchanged in fish held at 16 ° C. Fish held at 16 ° C were then subjected to six different temperature regimes ( 0/ 24, 4/ 18, 6/ 16, 10/ 12, 14/ 18, 24/ 0) ( time at 8 ° C / time at 16 ° C). The fish maintained at 24hr/ day at 16 ° C failed to develop elevated ATPase activity as did also the fish held in 4/ 18, 6/ 16, 10/ 12, 14/ 18. Only the fish held for 24 hours per day at 8 ° C exhibited an increase in ATPase activity, which occurred in the 5th week.

Chinook salmon Once juvenile chinook grow to an appropriate size they will migrate to the ocean ( Ewing et al., 1979; Clarke and Shelbourn, 1985). Out going migrations typically occur during the first and second years of life ( Wydoski and Whitney, 1979) but since success is related to smolt size, some fish will not be ready until their third year. Clarke and Shelbourn ( 1985) found that optimum regulation of plasma sodium concentrations in ocean type fall chinook salmon occurred with transfer from 13.8 º C fresh water to 10.2 º C sea water. They also noted that severe descaling in their freshwater holding tanks occurred in groups of smolts reared at 16 or 17 ° C, as well as with groups transferred from 8 12 ° C freshwater to 14 ° C seawater. Marine ( 1997) conducted laboratory tests on fall run chinook salmon from Sacramento River hatchery stocks to determine the chronic effects of varying temperatures from 13 to 24 ° C on growth and smoltification patterns ( Na+ K+ ATPase activity and seawater challenges). The control test was 15 ° C ( fluctuated from 13 16 ° C), the intermediate was 18.5 ° C ( 17 20 ° C), and the extreme was 21.5 ° C ( 21 24 ° C). The author concluded that both acceleration and inhibition of chinook smolt development may occur at temperatures above 17 ° C and significant inhibition of gill ATPase activity and associated reductions of hypoosmoregulatory capacity may occur when chronic elevated temperatures exceed 20 ° C. Wedemeyer ( 1980; as cited in USEPA, 2001) noted that Fall chinook undergo a greater desmoltification rate at 15 ° C than coho do at that temperature range. Clarke, Shelbourn, and Brett ( 1981) found that while acclimation to brackish water ( 15 20ppt) had little effect on osmoregulatory performance of coho and chinook reared at 10 ° C, it did maintain performance in chinook at 15 ° C to the end of the experiment. The authors also found a dramatic regression of hypo osmoregulatory capacity of chinook smolts held in fresh water at 15 ° C from week 7 to week 13. However, no such loss was observed in fish rear in 10 or 15ppt salinity. Marine ( 1997) found that smolts from the control ( 13 16 ° C) lot experienced higher ATPase levels and broader time periods of elevation, and better survival in seawater challenges than smolts reared in the warmer test lots ( 17 20 ° C and 21 24 ° C). The possibility that temperatures above 17 ° C exerts stress on migrating smolts is further supported by the work of Connor, Burge, and Bennett ( 1999; as cited in USEPA, 2001) that found subyearling chinook move into the main current of the Columbia River to avoid increasing nearshore temperatures, with this effect becoming significant above 17 ° C. It is further supported by the work of Sauter and Maule ( 1997, 1999) which found cessation in feeding behavior in Evaluating Standards for Protecting Aquatic Life in Page 119 Washington's Surface Water quality Standards smolting fall chinook at temperatures above 18 ° C and a decreased temperature preference ( from 17.7 to 11.2 ° C). Exposure to water temperatures of 20 ° C for several hours induced heat shock proteins ( Sauter et al., in review, and M. Hargis, personal comm.; as cited in Sauter and Maule, 1997). Zaugg ( 2001) summarized studies done by Bill Muir of the NMFS. It was observed that tagged yearling spring chinook salmon subjected to advanced photoperiod schedules and a 10 day exposure to elevated water temperatures ( 11 12 ° C) prior to release at the Dworshak hatchery migrated more rapidly and were detected in greater numbers at downstream dams than controls or fish exposed only to advanced photoperiods ( no increase in water temperature). Dr. Zaugg notes that it appears that this level of temperature increase might actually benefit chinook and coho salmon, and that steelhead smolts appear to be the most sensitive to elevated temperatures. Roper and Scarneccia ( 1999; as cited in USEPA, 2001) found that approximately 50% of the spring chinook emigration occurs in the range of 12.5 15 ° C and the upper tail of this run is generally complete before 20 ° C in exceeded. Connor, Burge, and Bennett ( 1999; as cited in USEPA, 2001) note that as temperatures increase above 17 ° C, sub yearling chinook rearing in nearshore areas of the Columbia River on their way to the ocean can be forced to enter the main current to avoid increasing temperatures along river margins. This is an indication that their may be indirect effects on smolts caused by warmer waters in addition to the direct effect on smoltification patterns.

Coho salmon Zaugg and McLain ( 1976; as cited by Zaugg, 2001 and) found that ATPase reached a maximum one month earlier in fish reared at 10 ° C than those reared at 6 ° C, and that activity rose even earlier at 15 ° C but was only transitory in those held at 20 ° C. Cold water ( 6 ° C) was also found to preserve the elevated activity while higher temperatures ( 10 and 15 ° C) caused decreases after an initial accelerated increase. Additionally, Clarke and Hirano ( 1995) noted; however, that diurnal and seasonal temperature cycles may alter the timing of smolting. Juvenile steelhead trout reared on a simulated seasonal temperature cycle ( 6.9 18.6 ° C) exhibited greater migratory behavior and more pronounced elevation of gill sodium, potassium activated Na+ K+ ATPase activity than those reared at constant 12.3 ° C ( Zaugg and Wagner 1973, and Wagner 1974). Adams et al. ( 1975; as cited in USEPA, 2001) found that 15 ° C was linked to impairment of smoltification, ability of smolts to migrate, and survival during smolt migration in coho salmon. Zaugg ( 2001) noted that in coho salmon that had reverted to parr and were subsequently released still migrated to the lower Columbia River very rapidly, and migrants captured there showed elevated ATPase levels. Although, ATPase levels were low at the time of release in June and July, these fish were capable of regenerating smolt level enzyme activities during migration in the warm waters of the Columbia during June and July. Migrants in the June and July releases migrated more rapidly than those released in May when ATPase activities were elevated in the holding ponds, and they had the greatest rate of survival to adults.

Discussion on Smoltification Studies: Page 120 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Zaugg ( 2001) has noted that there is considerable risk in using the results obtained from temperature experiments conducted in the laboratory in predicting what may occur in the natural environment with similar temperatures. Fish held in confined conditions fail to undergo full smolt development. Once released from the confined environments, normal smolt development occurs as downstream migration proceeds. He noted that while his earlier work suggested an upper limit of 12 13 ° C existed for migrating steelhead based on confined laboratory conditions, we must now use some degree of caution in applying this suggested upper limit to the natural waters. He noted that once fish are actively migrating downstream and are in the process of transformation, it may take substantially warmer waters to make them revert. In a discussion on the use of the available research to set temperature criteria, Dr. Zaugg supported the premise that it may be most important to ensure that temperature conditions in the tributaries and headwater systems allow for the initiation of the smoltification process. However, it must be recognized, however, that not all migratory juveniles will have a long journey to marine waters, and not all will be able to hold in an estuarine environment if smoltification is not satisfactory upon arrival at the mouth of the tributary. Thus some caution must be exercised in assuming that the process of migration will be sufficient to allow smolts to successfully transition for life at sea. The laboratory results for steelhead trout strongly suggest that a constant exposure to temperatures greater than 12 13 ° C may hinder ATPase activity, and that temperatures greater than 15 16 ° C may disallow development altogether in multiple species. These results were obtained in tests conducted at constant temperatures, and would best be represented by weekly or monthly average temperatures. This position is supported by the work showing that steelhead trout reared on a simulated seasonal temperature cycle ( 6.9 18.6 ° C   mean 12.79 ° C) exhibited greater migratory behavior and more pronounced elevation of gill sodium, potassiumactivated Na+ K+ ATPase activity than those reared at constant 12.3 ° C. Treating the constant temperatures as a weekly average temperature results in the suggestion that a 7DADMax limit of 15.18 16.18 ° C may be necessary to allow normal ATPase development in smolts, and that a 7DADMax of 18.18 19.18 ° C may prevent or stop smoltification entirely.

To protect the smoltification capability of juvenile salmonids, it is concluded that the 7 day average of the daily maximum temperatures ( 7 DADM) should not exceed 15.18 16.18 ° C. Except for the Columbia and Snake Rivers this temperature threshold is viewed as appropriate for application throughout the entire juvenile migration path. These two major rivers are cited as exceptions because they provide a significant migratory time and terminate in a large estuary; both features that have been well demonstrated to assist in the full development of successful smolts, even under temperature conditions determined adverse in laboratory testing.

e) Miscellaneous Indigenous Species With the possible exception of two amphibian species, the tailed frog and the torrent salamander, and two fish species, the mountain whitefish and the smelt, no other aquatic organisms have been identified that appear as sensitive overall to temperature increases as the native salmonids and char. This paper has focused on protecting species sensitive to Evaluating Standards for Protecting Aquatic Life in Page 121 Washington's Surface Water quality Standards temperature increases, however, it is important to remember that some of our native populations thrive in waters warmer than what is fully protective for salmonids ( Wydoski and Whitney, 1979; Black, 1953; Li et al., 1993; Reeves et al., 1987; Cech, Mitchell, and Wragg, 1984, and others).

For the water quality standards to be fully protective in the ecological sense, they must recognize the continuum of temperature changes from upstream to downstream and between ecoregions and waterbody forms. The water quality standards should acknowledge that certain waters that are naturally not fully protective for salmonids may be ideally suited for other native species. It is appropriate that some of these naturally warmer waters have separate standards that consider more accurately the warm water tolerant communities that have historically existed.

i) Sensitive Amphibians Three stream dwelling amphibians are of concern when it comes to temperature alterations. These are the Rhycotriton species ( 3 species of torrent salamanders), the Dicamptodon species ( Pacific and Copes giant salamanders), and Ascaphus truei ( tailed frog).

Rhyacotriton species are found in temperatures ranging from 5.9 10.9 ° C, and eggs have been found at 8 9 ° C then taken to the lab and incubated successfully at 8 9 ° C. Like most amphibians, Rhyacotriton can withstand high daily peak temperatures. When acclimated in a laboratory to temperatures of 13 14 ° C, Rhycotriton has a critical thermal maximum ( CTM) of 27.8 29 ° C ( Kelsey, 1998). Welsh and Lind ( 1996) suggest that suitable temperatures for Rhyacotriton are from 6.5 15 ° C, with highest abundance of salamanders occurring in a narrow range of about 8 13 ° C. The authors, using unpublished data developed while conducting critical thermal maximum testing, note that signs of thermal stress were noted at 17.2 ° C.

Dicamptodon species have larvae noted to develop at 12 16 ° C in the field. Larvae may develop for 2 years prior to becoming adult salamanders. Adults spawn in the spring when waters are warming, but may also spawn in the fall. While the Pacific giant salamander becomes a terrestrial salamander, the Copes giant salamander does not ( Kelsey, 1998).

Ascaphys truei is typically found in waters from 4.4 14 ° C. Embryonic development can occur between 5 18 ° C. Tadpoles from 1 2 years old prefer waters around 5 8 ° C, but 3 4 year olds prefer waters of 12 16 ° C. A. truei larvae have a critical thermal maximum of 28.9 30.1 ° C and adults of 23 24 ° C; when both are acclimated at 23 ° C. The nine day LT50 for tailed frog larvae was determined to be 23 ° C. Tadpoles may develop from 1 to 4 years, depending on the individual stream, before metamorphosis ( Kelsey, 1998). Hawkins et al ( 1988) found that variations in tadpole densities were high at maximum stream temperatures below 18 ° C and below that temperature substrate size and imbeddedness characteristics determined dispersal patterns. The authors suggest that low densities in nonforested Page 122 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards watersheds may be better explained by the sensitivity of adults to desiccation rather than the effect of moderately warm water temperatures.

As noted by Hawkins et al. ( 1988) tailed frog ( Ascaphus truei) tadpoles appear to be particularly well suited to life in swift streams. The body is streamlined and ventrally flattened, and the mouth is modified into a powerful suctorial disc. Tadpoles use the oral sucker to cling to rock surfaces, move against the flow of water, and scrape periphyton from streambed surfaces. Diatoms are apparently the main food source for these tadpoles ( Metter, 1964; as cited by Hawkins et al., 1988). In most West Coast streams, eggs hatch in late summer and tadpoles transform to adults almost exactly two years later ( Metter, 1967; as cited by Hawkins et al., 1988).

Claussen ( 1973) found that adult A. truei had an incipient lethal temperature limit of 24.1 ° C after 45 hours of exposure and 25.8 ° C after 7.3 hours, and that adults preferred temperatures of 16.5 18 ° C in laboratory tests conducted on wet sand. Claussen reported the adult frogs were kept in good health in the laboratory in terrariums kept at room temperature ( 19 24 ° C) for many months. Brown ( 1975; as cited by Hawkins, 1988) reportedly found that 18.5 ° C was the upper limiting temperature for egg development. De Vlaming and Bury ( 1970; as cited by Hawkins, 1988) are reported to have found that age 1+ tadpoles preferred 5 8 ° C and age 2+ tadpoles preferred 12 16 ° C, and that both cohorts avoided temperatures greater than 22 ° C and 50% of 1+ animals died within 29 days at 23 ° C.

Welsh ( 1990) studied the distribution of A. truei over a three year period at stream sites in the Pacific Northwest and found temperature to be an excellent predictor of tailed frog abundance. Higher numbers of tailed frogs occurred in streams with lower temperatures and the highest stream temperature at which he had observed tailed frogs was 14.3 ° C. Welsh suggested his work showed that while tailed frogs were found at maximum temperatures as high as 18 ° C, their densities began increasing only at stream temperatures below about 14.3 ° C and were characteristically highest in waters with temperatures below 12 ° C.

Hawkins et al ( 1988) sampled small streams near Mt. St. Helens, Washington between 1985 1987 and found that streams with little forest cover and maximum temperatures near 20 ° C had few A. truei while streams in completely or partially forested basins with maximum stream temperatures less than 18 ° C had relatively high tadpole densities. Variation in density within streams with maximum temperatures below 18 ° C were not associated with temperature differences but were instead associated with substrate size and embeddedness characteristics. In the Hawkins et al. ( 1988) suggest that while their work does not substantiate the opinion that adverse effects occur up to 20 ° C on tadpole density, temperatures in this range are within the critical limits found by other authors and their results should be used with care. Hawkins, Feminella, and Crisafulli ( unpublished status survey) found that in the streams around Mt. St. Helens, Washington, maximum tadpole densities were associated with mean maximum summer water temperatures of 16 ° C and note that since 1988 tadpole densities have been consistently higher in nonforested ( warmer) than in forested ( cooler) streams. Crisafulli ( personal communication) noted that the ability of tailed frog to thrive in the deforested areas of the volcano's blast zone may be related to the Evaluating Standards for Protecting Aquatic Life in Page 123 Washington's Surface Water quality Standards generally cool moist weather that is experienced in that region of the state which helps avoid desiccation of adult frogs. The concern being that work done in other regions associating tailed frog abundance to stream temperatures may be measuring the association of cool moist mature forest conditions to temperature rather than accurately gauging the importance of the specific stream temperatures to tailed frog health. Since flow, sediment, and riparian area conditions well all tend to be more favorable in the cooler headwater areas, this may confound efforts to gauge the importance of temperature compared with these other commonly associated factors.

Larvae of all of these stream breeding amphibians rely primarily on the perennial flows of 1st and 2nd order streams ( mostly Type 4 and 5, but also some smaller Type 3 streams). Their rates of growth, and thus time prior to metamorphosis, is affected by temperature and food. Warmer waters within their tolerance range may speed up development ( Kelsey, 1998).

The paucity of controlled research data on the temperature requirements of amphibians, and the potentially strong conflicts among the existing research, makes establishing a temperature standard aimed at ensuring their protection somewhat problematic. With lethal tolerances as high as most salmon and trout, the reported distributional associations with temperature must be considered with caution. Since these amphibians commonly occur high in the drainage, often at and above the upper limits of many fish species, they are typically able to associate with shallow groundwater dominated seeps and springs. Stream breeding amphibians, particularly the torrent salamanders and the tailed frog, may in fact have lower optimal temperatures than salmon and trout, but at this point the scientific information is not strong enough to reach this conclusion and does not suggest that establishing a species specific temperature limits are clearly warranted. There is clearly a need for more controlled studies on the temperature requirements of our stream breeding amphibians, and the question of whether more stringent temperature standards needs to be set for these species should be revisited periodically to ensure that new information and understandings are taken into account in setting and revising water quality standards.

ii) Other Sensitive Fish Species Smelt and mountain whitefish were identified through the literature as possessing sensitive temperature limits. The studies on smelt indicate they have a lower lethal temperature limit than do the salmonids and a lower optimum temperature preferendum. Longfin smelt ( Spirinchus thaleichthys) was identified as having a limit of occurrence of 18.3 ° C by Wydoski and Whitney ( 1979). This corresponds well to acute exposure testing using the Eulachon smelt ( Thaleichthys pacificus) by Snyder and Blahm ( 1971) who found a change from 10 to 18 ° C resulted in 50% mortality to adults in less than one hour, and 50% mortality occurring in 26 minutes at an exposure of 21 ° C. While temperature increases from 10 ° C to 13 ° C and 15 ° C, did not induce mortality over a 50 hour holding time, none of the females exposed to the higher test temperatures deposited their eggs. USEPA ( 1971) notes that in temperature studies on the eulachon, Smith and Saalfeld ( 1955; as cited in USEPA, 1971) reported the fish entered the Columbia River when the temperature was between 2 and 10 ° C Page 124 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards but they migrate up to and beyond the Cowlitz River ( RM 68) when the Columbia is approximately 4.4 ° C. The smelt run was delayed five weeks from entering the Cowlitz River because of low water temperatures during December 1968 and January 1969 ( Snyder, 1970; as cited in USEPA, 1971). Eulachon eggs appear to be more tolerant than adults to temperature increases. The eggs can withstand a temperature of 14 ° C from a base temperature of 4 to 8 ° C without appreciable mortalities ( Parente and Ambrogetti, 1970; as cited in USEPA, 1971), but a 3 ° C increase halts maturation of adult females. In tests in 1968 and again in 1969, it was observed that female smelt exposed to water heated 3.9 ° C above river temperatures were reluctant to spawn. Adult female smelt are less tolerant of temperature changes than other fish. Bell ( 1986) in a general review on the temperature requirements of fish suggested that the range for smelt was 3.8 12.7 ° C, and the preferred spawning range was 7.2 8.3 ° C. The spawning range identified by Bell, closely matches that observed for longfin smelt in the Cedar River in Washington. Wydoski and Whitney ( 1979) suggest that spawning occurs primarily in late February ( with a range of mid January to mid April) when the river was between 4.4 7.2 ° C. They also note a British Columbia stock that hatches at 9.4 10.6 ° C approximately 25 days after spawning. Given that adult spawners and outgoing juveniles may be in fresh waters as late as March to mid April, and their temperature requirements may be more strict than most salmonids, the protection of smelt is an important consideration in setting water quality standards. In waters supporting smelt, it is estimated that the 7 day average of the daily maximum temperatures should not exceed 12 14 ° C prior to May 1; with no single daily maximum temperature greater than 16 ° C to fully protect reproduction. This will allow most stocks to spawn and have the newly hatched juveniles return to the sea ( or lake where a landlocked population) under tolerable temperature conditions.

Information on the temperature requirements of the mountain whitefish ( Prosopium williamsoni Girard) is more limited to that for the smelt. Eaton et al. ( 1995) calculated that a weekly mean temperature of 23.2 º C was the 95th percentile of the distribution of mountain whitefish in field studies and suggested this value as a measure of the species temperature tolerance. Wydoski and Whitney ( 1979) and Daily ( 1971) note that mountain whitefish are found in both streams and lakes throughout the state of Washington, generally in large streams with average temperatures of 8.8 to 11.1 ° C. Whitefish are generally nocturnal autumn spawners that spawn from October into December and at temperatures below 4.4 to 5.5 ° C have been associated with spawning activity ( Brown, 1952; as cited by Daily, 1971). Mountain whitefish eggs require low temperatures for optimum development. They hatch in about 5 months at 1.7 ° C and in about 1 month at 8.9 ° C ( Sigler and Miller 1963, and Simon 1946; as cited in Davis, 1971). Daily ( 1971) noted that adult mountain whitefish are reported to prefer pool and meadow areas of cool streams where water depths exceed three feet. Sigler ( 1951) and La Rivers ( 1962) are cited by Daily ( 1971) as suggesting high water temperatures limit whitefish to elevations above 4,500 feet in California, Nevada, and Utah.

Northcote and Ennis ( 1994) note that mountain whitefish are often the most abundant sport fish species in many rivers of western North America ( Sigler and Miller 1963, and Brown 1971; as cited in Northcote and Ennis, 1994). Hagen ( 1970; as cited in Northcote and Ennis, 1994) found that in Phelps Lake spawning began in September at temperatures over 11 ° C but Evaluating Standards for Protecting Aquatic Life in Page 125 Washington's Surface Water quality Standards may extend into November at near 7 ° C. Spawning starts in late September in the Sheep River and extends to mid October at temperatures varying daily from 8 to 0 ° C ( Thompson and Davies, 1976; as cited in Northcote and Ennis, 1994). Other authors reportedly found spawning at temperatures as high as 9 ° C and as low as near zero, but usually in the 3 to 5 ° C range. Brown ( 1952; as cited in Northcote and Ennis, 1994) found that in the west Gallatin River, Montana, fish do not spawn until water temperatures drop below 5.5 ° C with peak spawning activity later in higher elevation tributaries at temperatures just over 2 ° C. Rajagopal ( 1975, 1979; as cited by Northcote and Ennis, 1994) studied the developmental rate of mountain whitefish eggs and gave 6 ° C as the upper optimal temperature for successful development. At temperatures between 9 and 11 ° C some hatching occurred but there were high levels of mortality and abnormality; all eggs died at temperatures of 12 and 15 ° C.

The information is not sufficient to justify setting a separate criteria for mountain whitefish, and since mountain whitefish occur in general along with salmon and trout in our streams and lakes, any assignment of criteria to protect these other salmonids would also be used to protect mountain whitefish populations. Based on the above cited literature findings, it appears that mountain whitefish have summer growth tolerances similar to the Pacific salmon and trouts, but they may have spawning requirements that are more sensitive. The generally late spawning habits of the mountain whitefish assist in their protection; however, human actions that cause uncharacteristic seasonal warming may cause harm to mountain whitefish during their incubation. In waters used for the incubation of mountain whitefish, average temperatures during incubation should be maintained at or below 6 ° C. The strength of the literature findings is not sufficient for setting a separate temperature threshold for mountain whitefish. It can, however, be used in support of setting incubation criteria for the Pacific salmon and trout. Treating this average temperature as either a weekly average or season wide average temperature helps bound the estimate for an incubation threshold and allows conversion to the standard 7DADMax metric used in this document. Taking this approach results in the estimate that to fully protect mountain whitefish incubation the 7DADMax temperature should be maintained below 7.47 10.64 ° C ( 9.1).

iii) Stream Macroinvertebrates Only a relatively small number of studies were found that tested the thermal tolerance of stream macroinvertebrates. Most of the species examined have thermal limits higher than the Pacific salmon and trout species found in Washington ( Sprague, 1963; Nebeker and Lemke, 1968; Moulton et al., 1993; Sherberger et al., 1977, as cited in Beschta et al., 1987; Craddock, 1970 and Hair, 1971, as cited in USEPA, 1971). However, two sets of studies were found that suggest individual species may sometimes as sensitive, and in some cases more sensitive, as our indigenous salmonids.

Gaufin and Hern ( 1971; as cited in Moulton et al., 1993) reported a range of 21.7 to 30.1 º C in mean lethal level ( median lethal temperature) for six species of caddisflies held at 6.4 º C. The lowest lethal level 21.7 º C was observed for Parapsyche elsis Milne, ( Hydropsychidae) Page 126 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards an inhabitant of cold, fast flowing mountain streams while the highest lethal level ( 30.1 º C) was recorded for Hydropsyche sp. collected from a marsh lake outflow.

USEPA ( 1971) conducted 96 hour lethality studies to examine the heat tolerance of late instar larvae of 15 species of aquatic insects and one species of amphipod. USEPA reported that a marked difference in sensitivity was apparent in the different species. A mayfly, Cinygmula par Eaton, died at 11.7 ° C and was the most sensitive of all the species tested. This species is found in very cold clear mountain streams. The freshwater shrimp, Gammarus limnaeus Smith, proved to be surprisingly sensitive to temperature increases, with 50% lethality at 14.5 ° C. Ephemerella doddsi Needham, a small, widely distributed mayfly characteristic of cold turbulent streams in the Intermountain Region, was also very sensitive with a TLm ( median lethal threshold) value of 15.4 ° C. A lotic species of mayfly, Hexagenia limbata Guerin, was much more tolerant than other mayflies tested with a TLm of 26.6 ° C. Considerable difference existed between the three stoneflies tested. Isogenus aestivalis ( Needham and Claassen) was quite sensitive, 50% dying at 16 ° C, while Pteronarcella badia ( Hagen) and Pteronarcys californica Newport, two closely related species survived increases to 24.6 and 26.6 ° C, respectively. Six species of caddis flies were tested and clearly reflected thermal differences in their habitat requirements. Parapsyche elsis Milne, which is largely restricted to cold, fast flowing mountain streams, had a TLm of 21.8 ° C while Hydropsyche sp. Taken from a slow flowing stream draining a marshy lake was very tolerant with a TLm of 30.1 ° C. In long term ( 12 30 days) thermal bioassays of five aquatic insects, the stonefly Pternorcella badi was most sensitive with 50% mortality occurring at 18.1 20.5 ° C within 24 30 days ( its 96 hour TLm was 22.55 ° C). Ephemerlla grandis Eaton experienced 50% mortality in 12 days at 21.5 ° C ( its 96 hour TLm was also 21.5 ° C). Pteronarcys californica Newport experienced 50% mortality in 25 days at 20 ° C ( its 96 hour TLm was 27 ° C). None of the three most sensitive species tested in the 96 hour tests ( C. par, E. doddsi, and G. limnaeus) were included in these long term tests.