Summary of Reported Spawning Temperatures: While both salmon and trout have been occasionally cited has having a spawning range that extends as high as 17.2 17.8 ° C ( 7DADMax 16.35 16.95 ° C), these are uncommon citations and are sometimes described as poorer quality spawning streams. Generally, maximum temperatures below 12.8 14.5 ° C ( 7DADMax 11.95 13.65 ° C) appear to most consistently define the thermal conditions under which spawning will be initiated in the fall spawning Pacific salmon. Spring spawning species such as Steelhead trout and cutthroat trout commonly begin spawning as temperature warm above 4 6 ° C. Most authors reviewed place the late spring spawning temperature range, or define quality spawning stream summer maximum temperatures, as being 12.8 13 ° C ( 7DADMax 11.95 12.15 ° C). Thus for all salmonids, temperatures below 12.8 14.5 ° C ( 7DADMax 11.95 13.65 ° C) are generally viewed as the upper limit for spawning. For the purpose of this analysis, the studies are being treated as if they were representing the daily maximum temperature, unless the author suggested otherwise. This interpretation by itself could be viewed as being biased towards the protective side. However, it is reasonable in light of the way temperature ranges are typically used in the literature ( as extreme point estimates), and in light of the fact that the temperature ranges are not typically related to an estimate of reproductive success.

Prespawning Effects of Temperature:

The effect of temperature exposure prior to actual spawning can effect the development of viable offspring and needs to be considered in setting a temperature standard. It has been found that temperature can effect both the health of the spawners and their potential reproductive success prior to the act of spawning. One of the ways in which temperature affects the health of spawners is by increasing the risk of mortality from warm water diseases ( Schreck et al., 1994; Bumgarner et al., 1997; and ODFW, 1992) prior to spawning ( disease is discussed separately in this paper). Another way that warm water affects the success of spawners is through its effect on the health of the unfertilized eggs as well as the maturation Evaluating Standards for Protecting Aquatic Life in Page 41 Washington's Surface Water quality Standards timing of adult salmon. This information is important to setting temperatures in both spawning streams and along the final migratory route taken by adult spawners.

Chinook Salmon Several researchers have examined the effects of holding mature adult chinook prior to spawning at warm temperatures. Holding mature adults at warm temperatures has been found to the reduce the survival of eggs ( Hinze, 1959; as cited in CDWR, 1988). Rice ( 1960) found that holding broodstock at temperatures above 15.6 ° C reduced survival of eggs to the eyed stage by 12.7% as compared to holding broodstock at 8.3 15.6 ° C ( mean 11.95 ° C). Adult immigrants held at temperatures greater than 15.6 or less than 3.3 ° C were also found to produce eggs that are less viable in a study by Hinze, Culver, and Rice ( 1956; as cited in CDWR, 1988). The greatest survival ( 95%) was from adults taken at temperatures in the range of 11.7 12.2 ° C. Berman and Quinn ( 1989) cite a personal communication with the manager of the Kalama State Fish Hatchery as finding egg moralities of 50% or more from adults held in river waters fluctuating from 14.4 19.4 ° C ( mean 16.9 ° C). The current supervisor of the Kalama Falls Hatchery, Ron Castaneda, notes that they still attribute some increased losses to holding temperature around 15.6 17.8 ° C; although, they have not had conditions of mortality as high as 50%. Similarly, Marine ( 1992; as cited in USEPA, 2001) noted that conventional hatchery practice is to consider chinook broodstock stressed at temperatures above 15 ° C, and noted that survival declines dramatically in holding ponds when temperatures exceed 17 ° C. M. Everson with the Oregon Department of Fish and Wildlife is cited in a personal communication by Marine ( 1992; as cited in USEPA, 2001) as acknowledging that wild spring chinook in the lower Rouge River exhibited high prespawning mortality in 1992 when water temperatures ranged from 18 21 ° C. The information cited above suggests that average temperature exposures of 15.6 17 ° C are associated with reduction in reproductive success. Average temperatures of approximately 12 ° C were associated with high survival rates.

Sockeye Salmon Andrew and Geen ( 1960) noted that average daily temperatures in excess of 12.8 ° C during the spawning period appear to increase the numbers of female sockeye salmon that die unspawned. In one year when the average daily water temperatures at the peak of spawning ranged from 12.8 15.6 ° C ( mean 14.2 ° C), spawning success was only 45%.

Steelhead and Rainbow Trout Smith et al. ( 1983) and Piper et al. ( 1982) cite work demonstrating that adult brood fish should be held at temperatures below 12.2 13.3 ° C prior to spawning to produce good quality eggs, while holding temperatures above 13 ° C have been found to reduce invivo postovulatory egg survival ( Flett et al., 1996, and Billard and Gillet, 1981; as cited in Billard, 1985). Temperatures of 18 ° C or higher have been found to reduce the volume of male sperm, and a temperature of 20 ° C has found to cause a drop in egg fertility invivo to 5% after four and one half days ( Billard and Breton, 1977). But at 10 ° C, fertility of the eggs held in Page 42 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards the hen trout remained high. Steroid biosynthesis has been noted to be suppressed in rainbow trout testes at 17 ° C ( Manning and Kime, 1985; as cited in Macdonald et al., 2000). Saki et al. ( 1975; as cited in De Gaudemar and Beal, 1998) found that embryonic and post hatching survival in O. mykiss decreased significantly if they remained ripe in the body cavity for more than 5 7 days after ovulation, and fertility could approach zero after two weeks ( Stein and Hochs, 1979; as cited in De Gaudemar and Beal, 1998). To avoid invitro damage to the eggs of steelhead and rainbow trout it appears that constant temperatures should be maintained below 12.2 13.3 ° C.

Summary on Prespawning Effects: A consistent finding among the studies reviewed was that average temperatures greater than 12 13 ° C ( 7DADMax of 13.48 14.48 ° C when study results are treated as daily average, and 13.96 14.96 ° C when treated as a weekly average) ( conversion assumes a diel variation of 2 4 ° C) pose a real risk of reducing spawner viability, and that high losses can occur when average temperatures exceed 14 ° C ( 7DADMax 15.48 15.96 ° C) in the weeks immediately prior to spawning. An important consideration is that the viability of the eggs in ripe fish will decline both with time held in utero and with increasing temperatures above 12 ° C, thus temperatures should be suitable for spawning within a few days of when ripe adults arrive on the spawning grounds to avoid losses. It seems most appropriate to treat the laboratory test results that were based on constant test exposures as daily average and weekly average temperatures ( both are used to create the likely range within which the best estimate would occur) when converting to the standardized 7DADMax metric used in this analysis. This is because the period of time that exposure would be effecting ripe eggs and adult fish in spawning condition would be around one to four weeks. Thus to avoid prespawning losses of eggs the highest 7DADMax temperature should not exceed 13.48 14.96 ° C. Given that the effect of concern is a lethal endpoint ( rather then sublethal such as a reduction of growth) it would be most advisable not to assume the upper end of this range is fully protective.

Incubation and Pre emergent Development Chinook Salmon Once spawning has taken place, the eggs of chinook salmon hatch in about 2 months and the young remain in the gravel for 2 3 weeks prior to emerging. Many researchers have tested incubation survival at constant exposure to various test temperatures. Complete mortality ( 100%) has been noted at incubation temperatures from 13.9 to 19.4 ° C ( Donaldson, 1955; Garling and Masterson, 1985; Seymour, 1956; Eddy, 1972, as cited in Raleigh, Miller, and Nelson, 1986). Significant mortality ( over 50%) has been noted at constant incubation temperatures from 9.9 to 16.7 ° C ( Donaldson, 1955; Seymour, 1956; Burrows, 1963, and Bailey and Evans, 1971; as cited in Alderdice and Velsen, 1978; Hinze, 1959; as cited in Healy, 1979). A constant incubation temperature of 8 ° C produced more robust alevin and fry than constant exposure to either 4 or 12 ° C in a study by Murry and Beacham ( 1986), and Velsen ( 1987) compiled data showing that the best survival (> 92.9%) occurred between 7.2 9.6 ° C. Heming ( 1982), however, found good survival at both 10 ° C and 12 ° C. Heming Evaluating Standards for Protecting Aquatic Life in Page 43 Washington's Surface Water quality Standards tested the survival in both incubation trays and artificial redds. Survival rates declined as the temperatures increased from 6 to 8, 10, and 12 ° C. The greatest survival ( 91.7 98%) occurred at 6 and 8 ° C, but it was still very good ( 90.2 95.9%) at 10 ° C. Incubation at 12 ° C consistently had the lowest survival ( 84.6 89.3%). Heming also tested survival rates from incubation to hatching against survival rates from hatching through complete yolk absorption. His work suggests higher incubation temperatures may create a metabolic energy deficit for pre emergent salmon that increases mortality. Once alevin have hatched and absorbed their yolk sacs they will need to make a transition to active feeding. Heming and McInery ( 1982) found that temperatures of 6, 8, and 10 ° C resulted in an average survival of 98.4% during this transitional period, while 12 ° C was associated with a decrease in survival to 89.2%. Heming ( 1982; as cited in Beacham and Murray, 1986) found the maximum conversion of yolk to tissue weight occurred at 6 ° C or below. Seymour ( 1956) noted a 9 fold increase in abnormalities in fry incubated at 15.6 ° C and higher when compared to those incubated between 4.4 12.8 ° C. Seymour also noted that fry incubated at 4.4 ° C emerged larger than those reared at higher temperatures, however, subsequent fry growth was maximized at 12.8 ° C. Considered together, the work of the authors cited above strongly suggest that constant temperatures above 8 9 ° C or below 5 ° C may reduce the survival of chinook salmon embryos and alevins. A constant 10 ° C has been shown to produce mixed results with some authors finding high survival rates and others noting significant losses. While constant temperatures of 11 12 ° C can still result in good success, the results are consistently less than what is produced at lower temperatures.

Some researchers have tried to mimic the naturally fluctuating and falling temperatures actually experienced by incubating eggs, or have made stepwise reductions in the incubation temperatures as incubation progressed. Initial incubation temperatures from 15.6 16.7 ° C have been associated with significant to total losses of young fish through the incubation to early fry development phase ( Healy; 1979; Brice, 1953; CDWR, 1988; Jewett, 1970; as cited in CDWR, 1988). Rice ( 1960) found that source waters declining from 15.6 8.3 ° C resulted in satisfactory egg development, though did not provide survival rates and may not have considered survival through to the fry stage. Johnson and Brice ( 1953) found survival to often exceed 90% where initial water temperatures ( as a daily mean) were below 12.2 ° C. Healy ( 1979) found that highest survival ( 97%) occurred in creek water where the daily maximum reached 12.8 ° C only a few times during the first two weeks of development; but also noted that survival was still very good ( 90 94%) where the initial daily maximum temperatures were between 12.8 14.2 ° C. Olson and Nakatani ( 1969) found 53.7 88% survival in egg lots started at 12.5 ° C, experiencing a brief increase to 14.7 ° C ( daily mean) in the first week, and then quickly dropping back to 12 12.5 ° C and assuming a seasonal downward trend in temperature ( test water paralleled both diel and seasonal fluctuations   and no control lots were provided). Olson and Foster ( 1955) found the greatest survival at an initial test temperature ( daily mean) of 11.6 ° C ( 92.2%), but reported no appreciable differences in survival rates at initial test temperatures of 13.8, 15, and 16 ° C ( 89.9 83.9%) ( test water paralleled seasonal daily average temperatures). Seymour ( 1956) tested four geographically distinct stocks of chinook. Taking into consideration both mortality and growth rate, the optimum temperature was estimated as 11.1 ° C for eggs and fry. The mortality rate was considered low at all stages of development for lots reared between 4.4 ° C Page 44 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards and 12.8 ° C ( daily mean). Lots with initial temperatures of 18.3 ° had the highest mortality ( 11, 24, 40, and 100%). In the cyclic and fluctuating temperature tests reviewed here, having temperatures at the beginning of incubation that are below 11 12.8 ° ( daily mean) are typically associated with excellent survival rates. This range compares well with the optimal temperature range of 8 12 ° C recommended by the Independent Scientific Group ( 1996).

Donaldson ( 1955) transferred eggs to more optimal ( 10 12.8 ° C) constant incubation temperatures after various periods of exposure to higher temperatures. He found that tolerance to temperature exposure varies with the stage of development. He also found 20% mortality could be induced by exposing eggs to 19.4 ° C for one day, 18.3 ° C for thee days and 17.2 ° C for less than ten days. Donaldson's work lends further support to the observations made by other authors such as Jewett ( 1970; as cited in CDWR, 1988) that the latent effects of holding eggs at higher than optimal temperatures continues through the period of absorption of the yolk sac, thus using mortality estimates at the time of hatching underestimate the total temperature induced mortality. Donaldson found the developmental stages associated with the greatest percentages of temperature induced mortality were: 1) the time up until the closure of the blastopore ( 200 T. U.); 2) the period just previous to and during hatching; and 3) when fry are adapting themselves to feeding. He also found that when eggs were exposed to test temperatures ( 17.2, 18.3, and 19.4 ° C) past the eye pigmentation stage ( 350 T. U.) the time necessary for complete hatching doubled, and the frequency of common abnormalities increased with both the higher temperatures and longer exposures. Donaldson's work also suggests that a week or more exposure at an average of 17 ° C would likely cause at least moderate mortality ( 20%), even if the water were quickly and substantially cooled after that initial exposure. Murry and Beacham ( 1986) found that initial incubation at 4 ° C reduced survival even with later transfer ( at completion of epiboly) to warmer waters ( 8 ° C and 12 ° C). Transfers after epiboly or completion of eye pigmentation from 4 to 12 ° C and from 12 to 4 ° C also caused an increase in alevin mortality. The authors also found that a decreasing temperature regime produced longer and heavier alevins and fry. Combs ( 1965) found that eggs developed to the 128 cell stage at 5.8 ° C could then tolerate 1.7 ° C for the remainder of the incubation period with only moderate losses. Mortality of 14.5% was observed with a transfer time of 72 hours, while only 3.3% mortality occurred with a transfer at 144 hours. These three works taken together suggest that the effects of suboptimal initial incubation temperatures may not be nullified by later changes in the temperature regime to more optimal levels; that sudden changes in temperature at either early or later stages of development, regardless of the direction of that change, can be harmful to pre emergent life stages; and that initial incubation at optimal temperatures may condition eggs and embryos such that they can withstand very low winter temperature regimes. Neitzel and Becker ( 1985) also conducted work on the effects of short term increases in temperature that can be used to support daily maximum temperature criteria. Neitzel and Becker ( 1985) used chinook salmon to try and determine the effects of short term de watering of redds by hydropower facilities. Neitzel and Becker found that sudden increases in temperatures from 10 ° C to above 22 ° C for 1 8 hours significantly reduced survival of cleavage eggs in chinook salmon. Controls held at 10 ° C experienced very low mortalities ( less than 2%). Mortality in treatment groups was 8 10% at 22 ° C after 2 hours exposure, and was 22% after a one hour Evaluating Standards for Protecting Aquatic Life in Page 45 Washington's Surface Water quality Standards exposure at 23.5 ° C. They further found that decreasing the temperature from 10 ° C to near freezing ( 0.0 ° C) for up to 24 hours did not increase mortality in eggs, embryos, or alevin.

Considering the work of Donaldson ( 1955) and Neitzel and Becker ( 1985) together allows a reasonable estimate of temperatures that would avoid causing acute effects to eggs and embryos. Donaldson found that a constant 24 hour exposure to 19.4 ° C caused modest lethality. This is relatively comparable to Neitzel and Becker's findings that, a 1 8 hour exposure to 22 ° C caused moderate lethality. Adjusting this range ( 19.4 22 ° C) by a reduction of 2 ° C would be expected to reduce the likelihood of any mortality occurring at all, and produces a single daily maximum or one hour duration limit of 17.4 20 ° C to fully protect incubating eggs and embryos from acute lethality.

While there is some disagreement, the literature is very consistent overall regarding the optimal incubation requirements for chinook salmon. To provide full protection from fertilization through initial fry development for chinook salmon, average daily temperatures should remain below 11 12.8 ° C at the initiation of incubation, and the seasonal average should not exceed 8 9 ° C throughout the incubation through emergence period. To protect eggs and embryos from acutely lethal conditions the highest single day maximum should not exceed 17.5 20 ° C.

Coho Salmon Embryo survival is consistently maximized in tests conducted at constant temperature exposures between 2.5 6.5 ° C, and is only slightly less successful between 1.3 10.9 ° C ( Dong, 1981; Tang et al., 1987; Murry et al., 1988; Velsen, 1987). Davidson and Hutchinson ( 1938; as cited in Sandercock, 1991) suggested the optimum temperature for egg incubation is from 4 11 ° C. Mortalities tend to become moderate ( 21 26%) between 11 12.5 ° C, and between 12.5 ° C and 13.5 ° C mortalities of 50% can be expected. Above 14 14.4 ° C, tests commonly report at or near 100% mortality. Alevin survival may be excellent ( 97%) between 1.3 10.9 ° C ( Dong, 1981; Tang et al., 1987), and the most robust fry are at incubation temperatures between 4 8 ° C ( Dong, 1981; Murry et al., 1988). Alevin mortalities of 51 59% occur at 12.5 ° C ( Dong, 1981), and 100% mortality occurs at 14 14.4 ° C ( Dong, 1981; Murry et al., 1988).

From the studies discussed above we can be relatively confident that egg survival would be consistently maximized at exposure to constant temperatures between 2.5 6.5 ° C, but may still be excellent for many stocks at temperatures between 1.3 10.9 ° C. Alevin and fry survival and health may be optimized at exposure to constant temperatures between 4 8 ° C, but survival may remain excellent up to 10.9 ° C. Based on the preceding, the incubation of coho salmon should be fully support by maintaining the average temperature throughout the incubation period should at or below 8 10 ° C.

There is no information available that suggests coho salmon embryos and alevin would be more sensitive to short term ( daily peak) increases in temperature than any other Pacific salmon. The one study reviewed that looks at short term temperature changes for coho was Page 46 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards that by Tang et al. ( 1987). In that study, incubation temperatures were increased from 10.2 to 17 ° C and lowered from 10.2 to 4 ° C for eight hours. In neither test did these modest changes result in any statistically significant increase in mortality. Additionally, one field study reported coho alevins surviving very " substantial" daily peak temperatures with no clear change in later juvenile abundance ( summer peak stream temperatures of 24 and 30 ° C were noted; although, its is highly unlikely the eggs were actually exposed to these temperatures and were most likely protected by placement in groundwater seeps) ( Hall and Lantz, 1969). Since no clear basis has been found for setting a daily peak temperature specific to coho incubation, it is suggested that the daily maximum value chosen for chinook be considered appropriate for coho salmon as well.

Pink Salmon The range for successful incubation has been suggested to be from 4.4 ° C to 13.3 ° C ( Bonar et al., 1989). Murray and Beacham ( 1986) reported excellent survival ( 91 97%) with initial fertilization occurring at constant 14 ° C and a 0.5 ° C drop in temperature every three days down to 5 ° C. When they allowed temperatures to drop further to 4 and 2 ° C survival was reduced. Murray and McPhail found survival of 94% from fertilization to emergence at 5 ° C, and Beacham and Murray ( 1986) found the greatest survival for 5 stocks and 21 families of pink salmon tested at 8 ° C. Velsen ( 1987) compiled data that showed the best, though highly variable, survival ( generally > 89.5%) occurred between 8 13 ° C. Survival decreased at an incubation temperature of 11 ° C in a test by Murray and McPhail ( 1988), and was 50% at 15 15.5 ° C ( Beacham and Murray, 1990). Temperatures of 5 8 ° C produced the largest alevins in a study by Murray and McPhail ( 1988), and 8 ° C produced the longest ( Beacham and Murray, 1986) and fry heaviest ( Murray and McPhail, 1988). Konecki et al. ( 1995) incubated embryos from ten western Washington populations and found significant variation ( 1 3 weeks) in incubation rates   suggesting that some differences in temperature optimums may occur between stocks.

Survival of the alevin life stage was found to be generally excellent (> 97%) for 21 families of pink salmon tested at temperatures ranging from 4 12 ° C ( Beacham and Murray, 1986). Survival to emergence was reported as low at 14 ° C ( Murray and McPhail, 1988). Examining low incubation temperatures, Beacham and Murray ( 1986) found that temperatures of 4 ° C consistently resulted in the lowest survival for 5 stocks and 21 families of pink salmon, and in a 1990 study found 50% mortality at 5 ° C. Complete mortality has been found at an incubation temperature of 2 ° C ( Murray and McPhail, 1988; Beacham and Murray, 1990; Bailey and Evans, 1971). Murray and Beacham ( 1986) transferred embryos in a late stage of development from 8 ° C to 1 ° C and found that while northern stocks had 100% survival, southern stocks experienced moralities ranging from 38 60%.

Based on the research cited above, constant temperatures in the range of 4.5 12 ° C, and a constantly declining temperature regime beginning at 14 ° C are capable of producing excellent and perhaps optimal survival rates of incubating pink salmon. However, a constant temperature of 8 ° C appears to produce the most consistently optimal results; and while tests up to 12 13.3 ° C were found to produce excellent results, several tests found temperatures of Evaluating Standards for Protecting Aquatic Life in Page 47 Washington's Surface Water quality Standards 11 12 ° C to produce lower survival and smaller fry. Further, in natural streams the temperatures will not dependably decline at a steady rate, and constant temperatures of 15 16 ° C have resulted in high mortality. In consideration of all of these issues it should be assumed that constant temperatures in the range of 8 10 ° C represent upper range for fully supporting the embryonic development of pink salmon. Therefore, to fully protect the incubation of pink salmon the daily average temperature at the initiation of incubation should be maintained below 12 14 ° C and the average temperature throughout incubation through emergence should be not exceed 8 10 ° C.

Chum Salmon Incubation survival from fertilization to emergence is variable, but can be excellent anywhere from 4 12 ° C ( Murray and Beacham, 1986; Beacham and Murray, 1985). In the initial period of embryonic development temperatures in the range of 8 12 ° C produce the highest survival. However in later stages of incubation, temperatures in the range of 5 8 ° C produce the best survival as well as the largest and heaviest alevin and fry ( Beacham and Murray, 1986). Temperatures of 12 ° C in the later developmental stages can result in heavy losses in some stocks ( Beacham and Murray, 1985; Beacham and Murray, 1986). The optimal temperature range for conversion of yolk to tissue weight was estimated to be from 6 10 ° C ( Beacham and Murray, 1986), and optimal respiration efficiency has been estimated to range from 11 12.5 ° C for prolarvae and larvae ( Zinichev and Zotin, 1988). Constant incubation at temperatures of 14 ° C and 16 ° C as well as at 2.5 ° C have been associated with embryonic mortalities of 50% ( Beacham and Murray, 1990). The alevin stage of development ( late), however, was shown to have very high survival rates when exposed to temperatures as low as 2 ° C. Beacham and Murray ( 1987) found that 10 ° C resulted in higher growth and survival ( 96%) of emergent fry. Fry survival rates were 62% at 13 ° C, and 73% at 16 ° C.

Based on the literature reviewed, constant incubation temperatures from 4 12 ° C can produce excellent and incubation results; however, some researchers have noted reductions in survival occurring at the ends of this range. Constant incubation temperatures in the range 6 10 ° C would be most consistently fully protective for chum salmon. Average temperatures at the initiation of incubation should not exceed 11 12 ° C to allow for the full protection of developing eggs. To provide for the full protection of the period of development from incubation through emergence in chum salmon, the daily average temperature at the beginning of the incubation period should not exceed 11 12 ° C and the seasonal average temperature should not 8 10 ° C. Page 48 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Sockeye Salmon Murray and McPhail ( 1988) and Combs ( 1965) report that sockeye salmon are more tolerant of low incubation temperatures and less tolerant of high incubation temperatures than the other Pacific Salmon. At constant exposure, Combs ( 1965) reported that temperatures within the range of 4.4 12.7 ° C produced similarly high survival rates ( 85.8 90.9%), with the highest occurring at 5.8 ° C. Combs found incremental increases in mortality of 53 67% occurred when the temperature was lowered from 5.8 to 4.4 ° C or raised from 12.7 to 14.2 ° C. Velsen ( 1987) found that while survival rates were highly inconsistent between 1.1 15 ° C, the best survival generally occurred between 3.1 5.8 ( generally > 90%), with fair survival (> 70%) occurring in the range of 2.1 12.7 ° C, and survival rates consistently poor ( 17 76%) above 14 ° C. Murray and McPhail ( 1988) found that survival was highest at 8 ° C ( 79%) but only 40% at both 11 and 5 ° C. Andrew and Geen ( 1960) reported that in the first two years of a four year field study, eggs initially incubated at temperatures of 7.2 ° C had lower survival than those initially incubated at 10, 12.8, and 15.6 ° C. In a follow up experiment the following two years, they found that eggs exposed to temperatures of 15.6 to 16.7 ° C for " short periods of time" suffered severe losses during the period of exposure, and that temperatures of 16.7 18.3 ° C caused extensive losses both during and following the exposure. In a study by Craig et al. ( 1996) the temperature range of 8 10 ° C resulted in the optimum 1: 1 male to female sex ratio in offspring; although, the study design really only allows the conclusion that temperature in the early stage of development affects sex determination.

In the studies cited above, constant temperatures in the range of 4 12.7 ° C produce variable but oftentimes excellent survival rates in sockeye salmon; but that the range 6 10 ° C appears most consistently optimum. Severe losses have been noted at and above 15.6 ° C, even with short term exposure under fluctuating field conditions, and poor survival occurred at constant temperatures of 14 14.2 and above. Taken together this information suggests that daily average temperatures in the early incubation period should not exceed 11 12.7 ° C, and the average temperature throughout the period of incubation to emergence should not exceed 8 10 ° C to fully protect the incubation success of sockeye salmon.

Steelhead and Rainbow Trout Fuss ( 1998) considered the range 5.6 11.1 ° C as being optimal for steelhead egg survival in the Washington State hatchery program, and Bell ( 1986) suggests that 10 ° C is the preferred hatching temperature for steelhead eggs. Rombough ( 1988) found less than 4% embryonic mortality at 6, 9, and 12 ° C, but noted an increase to 15% mortality at 15 ° C. Alevin mortality was less than 5% at all temperatures tested, but alevins hatching at 15 ° C were considerably smaller and appeared less well developed than those incubated at the lower test temperatures. Redding and Schreck ( 1979) similarly found that emergent fry were larger at 12 ° C than at 16 ° C.

Velsen ( 1987) compiled data on the incubation survival of both anadromous ( steelhead) and non anadromous rainbow trout that showed survival was consistently high (> 92%) between Evaluating Standards for Protecting Aquatic Life in Page 49 Washington's Surface Water quality Standards 4 9 ° C, and fair (> 78%) between 3 15 ° C, but very poor ( 7%) above 16 ° C. Kamler and Kato ( 1983) tested incubation survival of rainbow trout at 9, 10, 12, 14, and 16 ° C. They found the highest survival of eggs at 10 ° C and 12 ° C, slightly lower survival at 14 ° C, and abrupt drops in survival at both 9 ° C and 16 ° C. Survival to the swim up stage in two strains of rainbow trout had 94 98% survival at 7 ° C, 72 95% at 4 ° C, and < 12 41% survival at 2 ° C ( Stonecypher and Hubert, 1994). Kwain ( 1975) found the lowest mortalities of rainbow trout occurred at 7 and 10 ° C, and Kashiwagi et al. ( 1987; as cited in Taylor and Barton, 1992) found optimal hatching occurred at 10 ° C. Humpesh ( 1985) found that optimal hatching (> 90%) occurred between 7 11 ° C in rainbow trout, and Alekseeva ( 1987; as cited in Taylor and Barton, 1992) suggested that optimal incubation occurs with temperatures rising from 5.3 10.5 ° C. Constant temperatures 10 12 ° C commonly form the upper end of the temperature range that provides excellent support for the incubation and hatching of anadromous and non anadromous forms of O. Mykiss. Losses become moderate at temperatures of 14 15 ° C and severe above 16 ° C. Maintaining a seasonal average temperature of 7 10 ° C appears to provide for the most consistent occurrence of optimal survival and development in O. Mykiss. Thus, it can be reasonably concluded that the average temperature throughout the development of O. Mykiss should not exceed be 7 10 ° C, and the maximum daily average temperature at the time of hatching should be maintained below 11 12 ° C.

Statewide spawning dates were not found for non anadromous rainbow trout. In the absence of such information, it is suggested that dates associated with the anadromous forms of O. mykiss be considered if need arises to set dates of application for the spawning and incubation criteria.

Cutthroat Trout Eggs of sea run cutthroat incubate for 6 7 weeks before they hatch and the alevin remain in the gravel for about another 2 weeks before they emerge ( Trotter, 1989; Pauley et al. 1989). Fry may emerge from March through June, depending on the location and time of spawning, but peak emergence occurs in mid April ( Trotter, 1989; Wydoski and Whitney, 1979).

Pauley et al. ( 1989) cite studies demonstrating that the optimum temperature for incubation is 10 11 ° C. Bell ( 1986) has suggested that the range for hatching of cutthroat trout eggs is from 4.4 12.8 ° C. Smith et al. ( 1983) found that west slope cutthroat trout eggs held in creek water with a fluctuating temperature of 2 10 ° C had significantly better survival than eggs held at a constant 10 ° C. Stonecypher and Hubert ( 1994) found that survival to swim up stage in Snake River cutthroat trout was 95% at 7 ° C, approximately 87% at 4 ° C, and less than 16% at 2 ° C. Hubert and Gern ( 1995) found 68.6% survival in a control population held at 7 ° C when testing the effects of lowering incubation temperatures in the early stage of development. Mortality rates were no different from controls when temperatures were lowered to 3 ° C at least 13 15 days after fertilization but were higher if the cooling took place sooner. Page 50 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards It is somewhat problematic to set standards for the incubation of cutthroat trout that can be reasonably applied statewide. As a spring spawning species that often spawns high in the watershed, cutthroat trout have a very broad period of spawning when examined statewide. Stocks that exist in lower or warmer watersheds will spawn as early as February when temperatures rise above 6 ° C, while stocks that exist in high elevation snow fed streams may need to wait until late June or July for waters to be sufficiently warm ( 6 11 ° C) to allow successful spawning. Were it not for risk of egg loss due to late winter and spring freshets, one could suggest that the spring spawning strategy is relatively unencumbered by changes in the temperature regime. While earlier spawning subjects cutthroat eggs to higher risks of physical damage, the earlier hatch also places surviving resident fry in a good position to maximize summer growth and thus increase their survival opportunities over the following winter. It may well be that the superior growth obtained in the oceanic phase of anadromous forms may make minor differences in weight gains from earlier emergence of less value, but this relationship remains to be tested. In general, specific stocks will have tailored their spawning and emergence periods to optimize both incubation survival and early fry growth. Significant changes in the temperature regime, such as earlier spring warming will bring unknown risks to individual populations. Therefore, while a fully protective temperature regime is suggested in this document for cutthroat trout, it would be best tailored to the historic patterns of spawning found in specific stocks. To initiate spawning in most stocks the water temperatures must at least warm to daily maximums of 6 7 ° C, though some stocks may not begin spawning until temperatures reach 11 ° C. Specific studies on incubation survival suggest, however, that incubation may be optimized with constant temperature exposures in the range of 7 11 ° C; although, the data suggests their could sometimes be incubation losses at constant water temperatures of 10 11 ° C. Statewide, most cutthroat spawn in mid February and hatch by the end of March. It is suggested that in the absence of more watershed specific information April 1 could be used to compare the incubation threshold recommendations statewide. Given that the studies reviewed create some contradictions, it is believed that the middle portion of the possible fully protective range should be considered most defensible for use in setting any final recommendations. To fully protect the period of incubation through emergence in cutthroat trout, the available information suggests that the average temperature throughout the entire development period should not exceed 8 9 ° C, and the daily average temperatures should not exceed 11 12 ° C until after emergence.

Summary of Laboratory and Field Studies on Incubation Success: Across all species of salmonids examined, full protection would be achieved by maintaining an overall average temperature throughout the period of incubation through emergence of 8 9 ° C, and by not exceeding 12 12.8 ° C as a daily average temperature at the initiation of incubation in fall spawning stocks and at the time of emergence in spring spawning stocks ( see Table 4.4, below). Evaluating Standards for Protecting Aquatic Life in Page 51 Washington's Surface Water quality Standards Table 4.4. Constant or average temperature exposures estimated to allow for full protection of the incubation of individual salmon and trout species.

Species Daily Average Temperature at Initiation Seasonal Average Temperature Chinook 11 12.8 8 9 Coho  8 10 Chum 12 14 8 10 Pink 11 12 8 10 Sockeye 11 12.7 8 10 Steelhead/ Rainbow 11 12 7 10 Cutthroat 11 12 8 9 Summary 11.16 12.58 ( mid. 11.87) 7.86 9.71 ( mid. 8.79)

Converting these temperatures to a standardized 7DADMax metric will facilitate the comparison with other lines of evidence on this life stage. It seems appropriate to assume the overall average temperature ( based on constant temperature exposure throughout the incubation period) represents a seasonal average ( which gives a 7DADMax of 11.29 12.29, and the initial incubation temperature ( based on tests that allowed temperatures to cool during incubation and that recorded temperature as a daily average) is represented best as either a daily average ( 7DADMax 13.48 13.77 ° C) or a weekly average ( 7DADMax 13.96 14.76 ° C) ( conversions are based on assuming stream diel temperature ranges of 2 4 ° C).

Table 4.5. Spawning and incubation requirements of salmon and trout.

Line of Evidence 7DADM  Range ( ° C) Median ( ° C) General observations on spawning initiation ( generally field observations) 11.95 13.65 12.8 Prespawning effects ( lab and field studies) 13.48 14.96 14.22 Incubation success ( as highest 1 week period) 13.48 14.76 14.12 Incubation success ( as a average across the entire life stage) 11.29 12.29 11.79 Best Estimate of Threshold 12.55 13.92 mid. pt. 13.24 The range of these independent lines of evidence is 11.29 14.96 ° C with a mean range of 12.55 13.92 ° C and an overall midpoint of 13.24 ° C. This suggests that to fully protect salmon and trout during the period from incubation through emergence, temperatures should not exceed a 7 DADMAx of 13.24 ° C. After cross checking the conclusion against each independent line of evidence, no overriding factors of disagreement appear to exist. The largest disagreement is with the season wide estimate of incubation success, however, this seems well counterbalanced by the estimate of initial incubation temperatures relating to full protection. The similarity between species for each line of evidence, and the similarity Page 52 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards between each of the lines of evidence lend greater credibility to the overall estimate of a temperature regime that will fully protect the salmonids from incubation through emergence.

To protect eggs and embryos from acutely lethal conditions that may arise under unique situations, the highest single day maximum should not exceed 17.5 20 ° C. ( Note: the conversion estimates would have been raised by 1.12,1.22, and 1.35 ° C for the daily average, weekly average, and seasonal average estimates, respectively, if it were assumed the streams would have an average seasonal diel fluctuation of 4 6 ° C rather than 2 4 ° C, however, a lower range seems more appropriate for use in the incubation period).

iii) Juvenile Rearing General Introduction:

Attaining good growth is very important to the survival of young salmon. In a study by Burrows ( 1963), it was found that doubling the weight of sockeye salmon fingerlings released from a hatchery resulted in a tripling of the adult return rate. However, in determining temperatures that will fully protect juvenile salmonids, growth is not the only endpoint of concern. It is important to note that disease, predation, and smoltification concerns are all important issues that need to be considered. Additionally, when considering growth rates, it is important to distinguish between studies conducted under constant and cyclic temperature regimes, and to recognize that the feeding rates used in testing will affect the results of the test. As food becomes more limited, the temperature that provides for optimal growth declines. As food becomes more plentiful, fish can grow larger in warmer waters. Since most tests are conducted at high to very high rations, the results must be cautiously applied to natural stream environments where food availability can be more limiting.

Laboratory Growth Studies Conducted at Constant Temperatures:

Chinook Salmon In constant temperature experiments conducted at high feeding rates, maximum growth tends to be associated with temperatures in the range of 15 19 ° C ( Hillman, 1991; Cech and Myrick, 1999; Brett et al., 1982; Banks et al., 1971). Banks et al. ( 1971) found that growth was similar at 15.6 ° C and 18.3 ° C, with 15.6 ° C being slightly higher in 2 of 4 test lots. In the two lots where 18.3 ° C produced better growth; however, the fish in this warmer water showed higher rates of disease incidence. Temperatures above 19 ° C were associated with reduced feeding and growth, as well as increased problems with disease. Marine and Cech ( 1998, as cited in USEPA, 2001) found that growth was substantially reduced at 21 24 ° C when compared to 13 16 ° C. Brett et al. ( 1982) estimated that under natural ration levels the optimum of 19 ° C would be reduced to 14.8 ° C and no growth would be possible at 21.4 ° C. Seymour ( 1956) studied three Washington and one California stock of chinook salmon and Evaluating Standards for Protecting Aquatic Life in Page 53 Washington's Surface Water quality Standards concluded that the general optimum temperature for growth and survival of chinook fingerlings was 14.4 ° C. Zaugg and Wagner ( 1973) found that at the end of a 16 week test, growth was roughly 27% greater at 12 ° C than at 8 ° C. Based on the foregoing works, maximum growth should be expected with constant exposure at 15.6 19 ° C. The increase in growth above 15.6 ° C, however, was inconsistently greater, and under natural rations the maximum growth rate may decline by as much as 4.2 ° C ( 14.8 ° C).

Coho Salmon Maximum growth of coho fed to satiation in the laboratory occurred at constant 17 ° C in a study by Shelbourn ( 1980).

Sockeye Salmon Brett et al. ( 1969; as cited in USEPA, 2001) found that optimum growth occurs at 15 ° C on unrestricted rations, but when the feeding rate was reduced to 1.5% of body weight/ day the optimal growth rate lowered to 10 ° C and growth was zero at 15 ° C. Brett and Glass ( 1973) noted that 10 ° C resulted in the most efficient use of food and that the reduction from 15 to 10 ° C created a 33% reduction in the demand for food. Brett and Groves ( 1979) note that at temperatures below 10 ° C food conversion efficiency rises most rapidly from the base level ( maintenance ration) and reaches peak efficiency at an intermediate ration. This relation changes progressively with rising temperature such that at 17 ° C and above the highest efficiency occurs on a maximum ration diet. They note that for sockeye salmon, over the complete range of tolerable temperatures maximum food conversion efficiency occurs at 11 ° C. Brett ( 1971; as cited in USEPA, 2001) found swimming capacity, metabolic scope, growth on excess rations, and ingestion were maximized at 15 ° C, and that 15 ° C was also the final preferendum temperature. Wurtsbaugh and Davis ( 1977) found that optimum growth occurred at 16.5 ° C on full rations. Donaldson and Foster ( 1941; as cited in Brett, Hollands, and Alderdice, 1958) discovered that growth in young sockeye tends to be poor to none at all at temperatures above 21 ° C and below 4 ° C. Brett ( 1956) noted that sockeye juveniles may cease feeding entirely when temperatures reach 21 ° C. Temperatures in the range of 4 7 ° C have been associated with poor growth ( Brett, 1956). The foregoing works suggest that maximum growth may occur at constant temperatures of 15 16.5 ° C under unrestricted rations, but that under severely restricted rations the point of maximum growth may decline as much as 5 ° C ( to 10 ° C).

Steelhead and Rainbow Trout Olson and Tempelton ( undated manuscript; as cited in USEPA, 1973) reportedly found that the most favorable range for steelhead growth was between 5 17 ° C, with a physiological optimum in the vicinity of 15 ° C. The amount of food necessary to maintain the fishes' weight increased rapidly as temperatures rose above 12 ° C with no growth occurring at approximately 23 ° C despite the presence of excess food. It was suggested that the most efficient growth, within the consumption ranges believed to occur in nature, is at the temperature of 5 14 ° C in the early spring, 11 14 ° C in early summer, 14 17 ° C in late Page 54 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards summer, 11 17 ° C in fall, and 5 8 ° C in winter. Behnke ( 1992) cites work showing that rainbow trout reduce and finally cease feeding as temperatures rise to between 22 25 ° C, often well below the lethal temperature.

Cech and Myrick ( 1999) tested winter run steelhead from the American river in California at three different temperature ( 11, 15 and 19 ° C) and ration levels that varied from 82% to 100% of satiation. They found that while a 12% reduction in feeding rate resulted in a statistically significant reduction of growth at 19 ° C, the growth rate was still higher than that observed at any feeding levels at 11 ° C and 15 ° C. This suggests that the maximum growth rate under more moderate level of feeding would likely occur between 15 19 ° C.

Behnke ( 1992, citing Dwyer et al. 1981, 1983a, 1983b) suggested that the optimum temperature for the growth and food assimilation in salmonids occurs between 13 16 ° C. Taylor and Barton ( 1992) recommended temperature criteria for Alberta in British Columbia of 12 19 ° C as a 7 day average. In a review on rainbow trout, Moyle ( 1976) opined that the optimal temperature for growth and the completion of most life history stages was 13 21. The optimal temperature range was cited by Bell ( 1986) as being 12.2 18.9 ° C with the most optimal set at 13.9 ° C. Piper et al. ( 1982) in a hatchery management review paper set the optimal at 10 16.7 ° C. Mckee and Wolf ( 1963; cited in Wedemeyer et al., date absent from copy) are reported to have found 13 ° C to be optimal.

Behnke suggests that redband trout from an Oregon desert basin have been demonstrated to have an optimum feeding temperature at some untested temperature higher than 19 ° C ( citing unpublished work from the U. S. Fish and Wildlife Service, Cultural Development Center, Boozeman, Montana). This was contrasted to work done at the same research facility on other forms of rainbow trout that showed growth optimum feeding peaked at 10 16 ° C. Behnke ( 1992) suggests that the work done to date demonstrates that the desert redband have a functional feeding temperature that is higher than rainbow trout that have evolved in less harsh environments of temperature and water flow. Kaya ( 1978) compared an introduced population of interior rainbow trout from the Firehole River in Montana to two hatchery strains. Temperatures in the Firehole River at times reach summer maximums as high as 29.5 ° C due to thermal springs. The planted stock has been living in the river for approximately 20 generations, yet it was found that neither the functional feeding temperature or the upper incipient lethal temperature had increased in comparison to the hatchery stocks.

Reimers ( 1957) found that raising water temperatures ( from 9.4 to 16.7 ° C) at the conclusion of starvation testing, increased metabolic demands sufficiently to cause mortality in the weakened fish, and found that fish that began the trials as well nourished hatchery rainbow trout survived better than stream conditioned wild brown trout. This was to point out the importance of beginning the winter period with good energy reserves.

Hokanson et al. ( 1997) found that a constant exposure to 17.2 ° C produced the greatest growth rates in trout fed to satiation over a 30 day test period. Maximum growth was estimated to occur between 15 20 ° C ( mean 17.5 ° C) by Cho and Kaushik ( 1990; as cited in Evaluating Standards for Protecting Aquatic Life in Page 55 Washington's Surface Water quality Standards Dockray et al., 1996). Sadler et al. ( 1986) found that growth and food conversion efficiency were greater at 16 ° C as compared with 10 ° C. Myrick and Cech ( 2000) found that the growth rates of two strains of rainbow trout from California tended to increase as temperatures increased from 10 to 19 ° C, with the significant increase occurring from 10 14 ° C, and to decrease to near zero as temperatures increased from 19 to 25 ° C. They also found that while the growth of the two strains was similar at low temperatures, the hatchery strain grew much better then the wild strain when exposed to temperatures in the upper range ( 22 and 25 ° C). The authors noted that the increasing trend in food consumption and growth rates for the two strains between 14 19 ° C, suggests the optimal temperature lies between these to temperatures. Huggins ( 1975) suggested older fish sometimes demonstrate more intermediate temperature preferences. While the conclusions of the foregoing authors are highly variable, the estimates at the low end of the range all come from recommendation papers or indirect citations. For this reason, preference is being given the conclusions of research papers directly reviewed. It is therefore estimated that growth may be maximized at temperatures as high as 17.2 19 ° C under satiation rations.

Cutthroat Trout Pauley et al. ( 1989) cite research concluding that the optimal temperature for juveniles is 15 ° C, and that equilibrium and ability to swim is lost between 28 30 ° C. Hickman and Raleigh ( 1982; as cited by Barton, 1996) suggest that the optimal range for cutthroat trout is 12 15 ° C. Data reviewed by Carlander ( 1969; as cited in Gresswell, 1995) suggest optimum water temperatures between 4.4 and 15.5 ° C for Yellowstone cutthroat trout. A temperature of 15 15.5 ° C is consistently cited as optimal for the growth of cutthroat trout.

Table 4.6. The following summarizes the conclusions from laboratory tests where the fish were exposed to constant test temperatures:

Species Temperature ( ° C) Feeding Rate Comments Author Chinook 15.6 and 18.3 Satiation Highest growth each in 2 of 4 tests, Higher disease at 18.3 Banks et al., 1971 19 Satiation Brett et al., 1982 14.8 60% of satiation A 4.2C reduction from max at satiation feeding Brett et al., 1982 14.4 Satiation Three Washington and one Calif. stocks Seymour, 1956 Coho 17 Satiation Shelbourn, 1980 Sockeye 15 Satiation Brett et al., 1969 10 1.5% body A 5C reduction from Brett et al., Page 56 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards wt. max at satiation 1969 16.5 Satiation Wurtsbaug and Davis, 1977 17 Satiation Highest growth efficiency Groves, 1979 Steelhead 15 Satiation Olson and Tempelton 19 Satiation and 88% Cech and Myrick, 1999 13.9 Satiation Bell, 1986 13 Satiation Mckee and Wolf Redband 19 Satiation Maximum may be higher Behnke, 1992 Rainbow 17.2 Satiation Hokanson et al., 1997 17.5 Satiation Cho and Kaushik, 1990 19 Satiation Myrick and Cech, 2000 15 Satiation Based on peak of plotted results Grabowski, 1973 Cutthroat 15 Satiation Pauley, 1989 17.5 Satiation Based on peak of plotted results Clarke, 1978 Summary 16.41( mean) Satiation Range 13 19 Optimal growth rates under high feeding levels have been found at constant temperature exposures from 13 19 ° C with a mean of 16.41 ° C. However, most studies group the estimate more narrowly, between 14 17.5 ° C ( 15.75 ° C). When feeding is reduced substantially, however, the temperature that will allow for maximum growth has been noted to decrease by 4 5 ° C. Thus under natural feeding regimes, where food availability is more restricted during the high temperature months of summer, maximum growth rates would be more likely to be obtained at a constant temperatures of 11 13.5 ° C ( assuming a 4 ° C reduction due to restricted feeding). If treated as either a weekly average or summer average temperature regime this constant temperature range would be converted to estimated 7 DADMax temperature ranges of 14.18 16.68 ° C ( 15.43) and 15.64 18.14 ° C ( 16.89), respectively. Evaluating Standards for Protecting Aquatic Life in Page 57 Washington's Surface Water quality Standards Ranges Identified in the Literature as Optimal for Growth:

The upper end of the ranges estimated as optimal for growth in the literature ranged from 15 21 ° C with a midpoint of 18 ° C ( Table 4.7). It was not always clear from the literature why the authors chose the specific ranges that were recommended, whether or not they had tried to set the ranges to maximum growth, or what temperature metric ( i. e., daily average, daily maximum, etc.) they were associating with their recommended ranges. Thus, this line of evidence should be considered with caution.

Table 4.7. A summary of the ranges identified in the literature as producing optimal growth conditions Species Estimated Optimal Range Comments Author Steelhead and Rainbow Trout 14 17 Estimate for the late Summer regime Behnke, 1992 10 16 Growth optimum feeding Behnke, 1992 5 17 Olson and Templeton 13 16 Dwyer et al., 1981, 1983a, 1983b 12 19 Recommended 7 day average criteria Taylor and Barton, 1992 13 21 Moyle, 1976 12.2 18.9 Bell, 1986 15 20 Cho and Kaushik, 1990 14 19 Optimal temperature lies between 14 19 Myrick and Cech, 2000 Cutthroat Trout 12 15 Raleigh, 1982 4.4 15.5 Carlander, 1969 Summary Upper Range: 15 21 ( 18)

Comparison Test Regimes with Better Growth:

The results in the table 4.8 below should only be used to generally support other studies since they did not determine specific temperatures that resulted in maximum growth. These results suggest, however, that constant temperatures above 21 ° C and below 10 ° C may be detrimental to growth, and that constant temperatures in the range of 12 14.5 are generally favorable. When feeding is reduced substantially, however, the temperature that will allow for similar levels of growth may be decreased substantially ( 4 5 ° C). Thus under natural feeding regimes, where food availability is more restricted during the high temperature months of summer, maximum growth rates would be more likely to be obtained at a constant temperatures of 8 10.5 ° C ( assuming a 4 ° C reduction due to restricted feeding). If treated as either a weekly average or summer average temperature regime this constant temperature Page 58 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards range would be converted to estimated 7 DADMax temperature ranges of 11.18 13.68 ° C ( 12.43) and 12.64 15.14 ° C ( 13.89), respectively. This line of evidence when viewed on its own merits suggests that relatively good growth will occur with 7DADMax temperatures of 11.18 15.14 ° C as compared with temperatures significantly ( 4 ° C or more) warmer or colder.

Table 4.8. Tests Comparing Growth at Only Two Contrasting Temperatures:

Species Better growth Worse growth Feeding Ceased Author Chinook 13 16 ( 14.5) 21 24 ( 22.5) Marine and Cech, 1998 12 8 Zaugg and Wagner, 1973 Sockeye < 4 and > 21, poor to no growth Donaldson and Foster, 1941 4 7 21 Brett, 1956 Steelhead and Rainbow Trout 22 25 Behnke, 1992 23 no growth Olson and Templeton, 1973 16 better conversion efficiency 10 Laboratory Growth Studies   Fluctuating Temperatures:

Chinook Salmon Neilson and Green ( 1985) found that in comparing fluctuating to constant test conditions, that growth was enhanced through naturally cyclic temperature regimes, suggesting that food utilization in fluctuating environments may be higher ( although it should be noted that this is not a consistent finding among authors). Marine ( 1997) conducted a 2.5 month test on Sacramento River hatchery stocks under satiation rations and a fluctuating temperature regime ( 13 24 ° C) that generally followed the seasonal pattern of the source water. Marine concluded that his work suggests the upper optimum for growth is about 18 ° C ( approx. range 17 20 ° C). Fish reared at the next highest range ( 21 24 ° C), however, experienced significantly less growth than those reared in the control group ( 13 16 ° C). Hillman ( 1991) conducted tests in a controlled laboratory stream environment with chinook salmon. He found that chinook salmon production was 1.2 times greater in cold than warm water ( i. e., a 20% reduction in weight when reared at 18 21 ° C ( mean 19.5 ° C) when compared with 12 15 ° C ( mean 13.5 ° C) when fed twice per day in experimental channels). The two works cited above suggest that average temperatures below 19 ° C are necessary to support maximum Evaluating Standards for Protecting Aquatic Life in Page 59 Washington's Surface Water quality Standards growth rates in chinook salmon, and that the average temperature that produces maximum growth rates likely lies between 15 18 ° C ( median 16.5 ° C).

Coho Salmon In a controlled study by Everson ( 1973), test fish were subjected to different fluctuating temperature regimes. The greatest growth occurred in coho at the lowest test regime of 12.1 20.8 ° C ( median 16.5 ° C). Everson also found that juveniles fed moderate rations and subjected to higher fluctuating test temperatures did not reach sizes typical of smolts at the time of downstream migration.

Sockeye Salmon Biette and Geen ( 1980, as cited in USEPA, 2001) tested growth under variable rations ( 4 6.9%) and fluctuating temperature regimes similar to what the fish voluntarily experience in a lake ( fluctuating two times per day from 5 9 ° C to 12 18 ° C)( approximate mean 11 ° C). In this work, sockeye grew as well or more rapidly under the natural feeding and temperature regime than at constant temperatures from 6.2 15.9 ° C ( mean 11.05 ° C); however, at satiation rations growth was better under the constant temperature regimes. Clarke ( 1978) found that under yearling sockeye salmon exposed to diel thermocycles are able to acclimate their growth to a temperature above the mean of the cycle. Specific growth in weight on the 7 13 ° C ( mean 10 ° C) cycle over 42 days was equivalent to that on a constant 11.4 ° C, and on the 5 15 ° C ( mean 10 ° C) cycle it was equivalent to a constant 13.9 ° C. Clarke found that growth was greater at the 5 15 ° C cycle than at a 7 13 ° C cycle. In constant exposure testing on maximum rations, growth was linear over the range of 7.5 17.5 ° C. The work of Clarke suggests that maximum growth would be produced at constant temperatures of 17.5 ° C.

Steelhead and Rainbow Trout Grabowski ( 1973) tested three constant temperatures ( 8, 15, and 18 ° C) and one fluctuating temperature regime ( 8 18 ° C, mean 13 ° C) over eight weeks with juvenile steelhead on maximum rations. The author found that steelhead grew best at the constant 15 ° C and second best in the fluctuating with its mean of 13 ° C. When the author plotted the data using the midpoint of the fluctuating test as a surrogate for a constant test condition, it showed almost linear growth from 8 to 15 ° C with a steep drop as the temperature approached 18 ° C. The percentage weight gains at 8 and 18 ° C were very similar and both substantially lower than the similar gains obtained at the mean of 13 ° C and the constant 15 ° C.

Wurtsbaugh and Davis ( 1977) studied the effects of ration size and temperature on the growth of juvenile steelhead trout through a series of laboratory and field studies. In 25 day laboratory tests, creek water was used as a control, and was heated 3 and 6 ° C above its natural fluctuating ( dielly and seasonally) temperature to create two alternative test conditions. From this work, the authors concluded that trout growth would be enhanced by average seasonal rearing temperature increases to approximately 16.5 ° C under satiation feeding, but if the food of wild fish is limited, any substantial temperature increase would Page 60 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards result in decreased growth. By examining the fish fed at rates more comparable to those observed in a natural creek, the maximum growth rates observed occurred at mean temperatures of 13.3 ° C in the Fall test ( 1.7%/ day compared to 1.3%/ day at 16.4 ° C) at 15.2 ° C in the Spring test ( 1.6%/ day compared to 1.4%/ day at 12.6 ° C), and at 16.2 ° C in the summer test ( 1.2%/ day compared to 1.1%/ day at a mean of 19.5 ° C). It is worthy of emphasizing that while the summer growth at a mean of 19.5 ° C ( range of 16 23.9 ° C) was only slightly less than growth at 16.2 ° C under moderate laboratory rations ( 7.9 and 6.8%/ day, respectively), at the next lowest ration tested ( 6.0%/ day) growth rates at 19.5 ° C fell sharply to 0.1%/ day. The authors calculated that maintenance requirements of the fish increased more than three fold ( 2.2 7.4%/ day) over the temperature range of 6.9 to 22.5 ° C.

Dockray et al. ( 1996) conducted a 90 day test in which temperatures were allowed to fluctuating with the natural regime of the city source water, which followed the pattern of Lake Ontario, plus 2 ° C to test the potential effects of global warming. The authors found that during the first 50 days of the 90 day test that the temperature increase of 2 ° C was beneficial to growth up to daily average of 18 ° C, after which further increases in the daily temperature inhibited long term growth. In a follow up study, Linton et al. ( 1998) noted that rainbow trout fed to satiation continued to feed and grow at a mean temperature of 20.5 ° C, that a 30% reduction in food intake occurred at 22 ° C, and that juvenile fish continued to feed near their thermal maximum. Linton et al. ( 1998) found that increasing the temperature regime by 2 ° C over the natural ( base) level for Lake Ontario trout resulted in increased spring and early summer growth that was lost in the latter part of the summer due to suppression of appetite and growth. Mortality rates increased from 6 to 13.1% in the warmer test water during the late summer in the first summer of testing when the mean monthly base temperature in August was 23 ° C. Mortality was almost nonexistent through the following summer which had a mean August base temperature of 18 ° C. The threshold temperature for the cessation of feeding, and subsequently growth, differed from > 20 ° C to < 20 ° C over the two summers, and thus also fish size and age. Hokanson et al. ( 1997) found that a constant exposure to 17.2 ° C produced the greatest growth rates in trout fed to satiation over a 30 day test period. Increased mortality was observed at temperatures in excess of this growth optimum. They also noted that in fluctuating temperature experiments that growth was accelerated where the mean temperature is below the constant temperature optimum ( 17.2 ° C), and growth was retarded by mean fluctuating temperatures above this optimum. The highest growth rate in the fluctuating temperature environment occurred at a mean of 15.5 ° C ( range of 11.7 19.3 ° C). A statistically non significant decrease occurred at a mean of 17.3 ° C ( range of 13.5 21.1 ° C). Through their work the authors also concluded that rainbow trout acclimate to some value between the mean and the maximum daily temperatures. The foregoing works suggest that maximum growth will be obtained at average daily temperatures between 15.5 and 18 ° C.

Cutthroat Trout Dickerson et al. ( 1999, and unpub. data; as cited in Dunham, 1999) found that Lahontan cutthroat growth rates in a test with temperatures fluctuating from 20 26 ° C ( mean of 23 ° C) Evaluating Standards for Protecting Aquatic Life in Page 61 Washington's Surface Water quality Standards were similar to groups of fish held at a constant 23 ° C, and after two weeks was not significantly different from fish held at a constant 20 ° C.

Table 4.9. Growth studies conducted in laboratory test waters with fluctuating temperature exposures.

Species Temperature ( range and mean) Results Feeding level Comments Author Chinook 13 16 ( 14.5) 17 20 ( 18.5) 21 24 ( 22.5) Optimal 17 20, with 13 16 having significantl y better growth than 21 24 Satiation 2.5 month test following source water regime Marine, 1997 12 15 ( 13.5) 18 21 ( 19.5) 12 15 significantl y better than 18 21 Satiation 18 21 had 20% less growth and 12 15 Hillman, 1991 Coho 12.1 20.8 ( 16.5) Greater growth than higher regimes tested Satiation Juveniles fed moderate rations did not reach typical size of smolts Everson, 1973 Sockeye 5 9 to 12 18 ( approx 11) Variable from 4 to 6.9% body weight Grew more rapidly under natural feeding regime and fluctuation temperatures than at constant 11.05C, but constant better under satiation feeding. Biette and Geen, 1980 Cutthroat 7 13( 10) 5 15( 10) 5 15( 10) had greater growth than 7 13( 10) Satiation Clarke, 1978 Steelhea d and Rainbow 8 18 ( 13) Better growth in a constant 15 Satiation Weight gains similar at 8 and 18 and both Grabowski, 1973 Page 62 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Trout than the fluctuating 8 18 ( 13) substantially lower than at 13 and 15. 16.5 average seasonal temp considered to enhance growth Satiation ( 6.8%/ day ) Heated creek water ( 3 and 6C) followed natural regime for 25 days Wurtsbaugh and Davis, 1977 16.2 summer average seasonal considered to enhance growth under natural feeding Restricted to rates seen in control stream ( 1.2%/ day ) Heated creek water ( 3 and 6C) followed natural regime for 25 days Wurtsbaugh and Davis, 1977 Increases beneficial up to daily average of 18 Satiation Fluctuated with source water plus 2C over 90 days. Dockray et al., 1996 11.7 19.3 ( 15.5) 13 21.1 ( 17.3) Highest growth rate in 11.7 19.3 ( 15.5), with nonsignificant decrease in 13 21.1 ( 17.3) 60 day test Hokanson et al., 1997 The results of these fluctuating temperature tests is highly variable due at least in part to the high variability in test methodology. Better growth conditions varied from regular daily ranges of 5 15 ° C to 11.7 19.3 ° C over the course of the studies ( typically month long studies), to a monthly ( described as seasonal) average of 16.5 ° C, and a highest daily mean of 18 ° C in a seasonally ( 90 day) rising temperature regime. This could be simplified and viewed as a range of 10 16.5 ° C as a monthly average and a maximum daily average of 18 ° C. Treating the monthly average as either a weekly average or a summer average, to bound the potential best range, would result in a 7DADMax of 13.16 19.68 ° C ( 16.42) and 14.64 21.14 ° C ( 17.89), respectively. Thus the 7DADMax temperature that would result in maximum growth would most likely occur between 13.16 21.14 ° C ( 17.15). Evaluating Standards for Protecting Aquatic Life in Page 63 Washington's Surface Water quality Standards Field Studies on Growth:

Chinook Salmon In studying growth in a natural stream, Bisson and Davis ( 1976; as cited in ODFW, 1992) reported that juvenile chinook grew faster in a stream where temperatures peaked at 16 ° C compared with a stream where temperatures peaked at 20 ° C.

Coho Salmon Averett ( 1969; as cited by Everson, 1973) proposed that August September stream temperatures should fluctuate between 11 17 ° C ( mean 14 ° C) for optimal growth. Holtby ( 1988) reviewing a long term study of coho in an experimentally harvested watershed determined that coho had likely benefited from changes in maximum stream temperature from 12 ° C to 15 ° C ( which would be approximately equal to a maximum weekly average of 14.56 ° C). Similarly, Thedinga and Koski ( 1984) found that smolt size and condition factor was greater in years in which stream temperatures fluctuating annually from 4 13.5 ° C than in years with temperatures of near 0 to 11 12 ° C. They associated greater smolt return rates with this greater growth. In a field study by Martin et al. ( 1984) the stream having the lowest growth was the warmest surveyed, and had average monthly temperatures of 12 17 ° C and peak monthly temperatures of 21 26 through the summer months. The foregoing does not provide a basis for estimating a maximum growth temperature, but can be used to support the position that weekly average temperatures of 14 15 ° C would be more beneficial to growth under natural conditions than lower temperature regimes. It also suggests that extreme daily fluctuations and daily maximum temperatures of 21 26 ° C can be detrimental to growth even under natural conditions.

Steelhead and Rainbow Trout De Leeuw ( 1982) found that stream temperature increases that raised the summer maximum temperature from 12 ° C to 16.5 ° C were associated with an increase in growth rates in three streams in British Columbia, Canada.

Bisson and Davis ( 1976; as cited in Li et al., 1994) found that streams with daily maximum temperatures in the range of 16 23 ° C had greater standing crops of trout than streams with warmer maximum temperatures ( 26 31 ° C). Ebersole et al. ( 2001) found that in tributaries to the Grande Rhonde River in Oregon, rainbow trout density declined as mean daily maximum temperatures ( for the two week period prior to survey) warmed above 16 ° C; reaching zero at approximately 24 ° C. While the decline in fish density was highly variable in the range of 16 to 20 ° C, it was a steady decline with very low densities at temperatures above 20 ° C. Page 64 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Cutthroat Trout Temperature increases in general are not always found to restrict cutthroat populations. Aho ( 1976) found coastal cutthroat preferring an unshaded section of stream in the Cascade mountains of Oregon. Density was twice as high and biomass was 49 65% greater in the unshaded section. He suggested that earlier fry emergence in the warmer unshaded section probably played a role in creating the greater fish weights. The highest weekly mean temperature was 14 ° C in the unshaded area, with the highest one hour temperature being 17 ° C. This compared to a daily maximum temperature of 14 ° C in the shaded section. Cutthroat were the only fish species present in the study stream so any relationship to potential competition could not be evaluated. Martin ( 1985) studied the affect of removing the vegetative canopy along a 1000 meter section of a third order stream on the Olympic Peninsula used only by cutthroat trout. Fish density increased in the upper 500 meter treatment reach in comparison to the 200 meter control section established just above the treatment reach. Summer daily maximum temperatures in this upper treatment ranged from 13.8 ° C at the boundary with the control section to about 16.1 ° C at the bottom of this upper treatment section 500 meters downstream. In the second treatment reach, which extended from 500 to 1000 meters below the control section, the average fish weight increased but density went down. Temperatures in this reach changed from 16.1 ° C at the upper boundary of the treatment reach to 17.3 ° C at the lower boundary of the lower treatment reach. The daily maximum temperature was 15.2 ° C in the midpoint of the upper treatment reach where fish density increased.

Martin ( 1984) in studying a small upper watershed creek on the Olympic Peninsula found that higher water temperatures during the summer caused metabolism and thus food consumption to increase in a population of cutthroat trout. He found that growth rates declined from a spring high to a low in the winter, and was below the maximum possible during periods of optimum water temperature. Food consumption followed the seasonal trend in food abundance and was limited by the available food supply.

Table 4.10. Summary results from growth studies conducted in the field.

Species Better growth Worse growth Author Chinook 16 ( daily max) 20 Bisson and Davis, 1976 Coho 15 ( daily max) 12 Holtby, 1988 4 13.5 ( annual ranges) 0 12 Size and condition factor Thedinga and Koski, 1984 12 17 ( average monthly) Lowest growth stream Had peak temperatures of 21 26 Martin et al., 1984 Steelhead and Rainbow Trout 16.5 ( daily max) 12 De Leeuw, 1982 16 23 ( daily max) 26 31 Greater standing crops Bisson and Davis, 1976 Greater than 16 Density declined Ebersole et al., Evaluating Standards for Protecting Aquatic Life in Page 65 Washington's Surface Water quality Standards ( mean daily) above 16 and was zero at 24. Steady decline above 20 2001 Cutthroat 14 ( weekly mean) 17 ( daily max) Site with highest weekly mean of 14 had twice the biomas. Highest one hour temperature was 17. Aho, 1976 15.2 ( difference along reach 13.8 16.1) ( daily max) 16.7( difference along reach 16.1 17.3) Density increased in reach at 15.2, density declined but average size increased at 16.7. Martin, 1985 In the field studies cited above, daily maximum stream temperatures from 15 17 ° C were consistently cited in association with streams having better standing crops of fish. This temperature range would be approximately equal to a 7DADMax range of 14.05 16.05 ° C. It is important to recognize that most of these studies did not evaluate stream temperatures just one or two degrees higher than those found to have better growth. Thus the conclusion is somewhat restricted to the statement that under natural feeding and temperature regimes salmonid populations will be fully supported at 7DADMax temperatures from 14 16 ° C.

Predation and Competition Involving Juvenile Fish:

Chinook Salmon In examining the effect of temperature upon predation rates of juvenile chinook, Marine ( 1997) found that striped bass predation upon the juvenile fish was very intense in their intermediate test at 17 20 ° C ( mean 18.5 ° C). Hillman ( 1991) examined the interaction between chinook salmon and redside shiner in both the Wenatchee River in Washington and in controlled laboratory streams. Immigration of shiners began as river temperatures reached 15 ° C and as their numbers increased the shiners were able to push the chinook out of the most favorable portions of the river for feeding. Similarly, in the laboratory tests Hillman found that chinook production was 1.2 times greater in cold water ( 12 15 ° C, mean 13.5 ° C) than warm water ( 18 21 ° C, mean 19.5 ° C   resulted in a 20% reduction in weight) in alloparty. In sympatry, shiners affected the distribution, activity, and production of chinook in warm water, but not in cold water. Based on the preceding, average temperatures in the range of 13.5 15 ° C favors the cold water chinook salmon over common non salmonid competitors. Average temperatures of 18.5 19.5 ° C would place the chinook salmon at a significant disadvantage for occupying and defending important habitat.

Steelhead and Rainbow Trout Page 66 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Juvenile competition, particularly with warm water and non salmonid species, is a concern that is sometimes expressed in association with warm summer rearing temperatures. Reeves et al. ( 1987) found that steelhead production was decreased by 54% in the presence of redside shiner in waters in the range of 19 22 ° C ( mean 20.1 ° C), but was not reduced in cooler waters ( 12 15 ° C, mean 13.5 ° C). They also noted that production of steelhead in a fluctuating 19 22 ° C waterway was less than half of that in a fluctuating 12 15 ° C waterway. While warmer waters favor redside shiner over steelhead, colder waters may favor other species. It has been suggested, for example, that in cooler waters brook trout can outcompete juvenile steelhead. In trying to explain the patterns of species distributions observed in the upper Columbia river tributaries, Mullan et al. ( 1992; using the work of Cherry et al., 1975) note that sympatry occurs between O. mykiss and brook trout in the range of 15 18 ° C ( mean 16.5 ° C), that temperatures above 18 ° C favors O. mykiss, and that temperatures less than 15 ° C favors brook trout. They also note, however, that under natural food rations, the level of optimal competition is likely to be lower. Cunjak and Green ( 1986) found that rainbow trout were able to compete better with brook trout at 19 ° C than at either 8 or 13 ° C. In tests of the interaction between rainbow trout and bull trout in the Columbia River drainage in British Columbia, Haas ( 2001) found that rainbow trout do particularly better than bull trout when maximum temperatures approach 14 15 ° C. Trying to set temperature threshold recommendations that will prevent a competitive advantage with an introduced coldwater salmonid, however, is not viewed as appropriate given the extensive overlap of their preferred thermal ranges. Based on the preceding, it appears that average temperatures of 20 ° C or warmer place steelhead at a competitive disadvantage over warm water competitors like redside shiner, while average temperature of 13.5 ° C or less do not.

Cutthroat Trout DeStaso and Rahel ( 1994) found that Colorado cutthroat trout competed nearly equally with brook trout at 10 ° C, but at 20 ° C the brook trout were dominant. Schroeter ( 1988; as cited in Dunham, 1999) found that Lahontan cutthroat were equal competitors with brook trout at 15 ° C. Nilsson and Northcote ( 1981) found interestingly enough that in sympatry the presence of more aggressive rainbow trout actually resulted in higher growth rates in cutthroat trout than the growth rates shown by the cutthroat in allopatry.

Summary on Competition and Predation Trying to set temperature standards that will prevent competition with an introduced cold water species is not viewed as appropriate give the extensive overlap of their preferred thermal ranges with Washington's native cold water species. It is more appropriate to focus this discussion on temperatures that allow coolwater or warmwater species to out compete our native salmon and trout. Table 4.11 below summarizes the studies on competition and predation. The literature suggests that as average river temperatures increase to about 15 ° C competitors begin to gain a competitive edge that becomes very significant as the average temperature reaches 18.5 20 ° C. In converting these average ranges they may best represent Evaluating Standards for Protecting Aquatic Life in Page 67 Washington's Surface Water quality Standards either daily average or weekly average temperatures. This results in an estimate that as the 7DADMax temperature exceeds 17.60 18.18 ° C ( 17.89) coolwater species will begin to displace juvenile salmon and trout from the best feeding habitats, and that the impact on growth would be severe at 22.05 23.18 ° C ( 22.62) even if such displacement did not occur.

Table 4.11. Studies on predation and competition with salmon and trout.

Species Increased predation or competition Type of Study Author Chinook 17 20 ( 18.5) Laboratory Intense increase in predation from striped bass Marine, 1997 15 ( average) Field Redside shiner immigrated and began to push out juvenile salmon Hillman, 1991 18 21 ( 19.5) Laboratory Redside shiner caused a 20% reduction in weight compared to competition at 12 15 ( 13.5) Hillman, 1991 Steelhead and Rainbow Trout 19 22 ( 20.1) Laboratory Redside shiner caused a 54% reduction in production compared to competition at 12 15( 13.5) Reeves et al., 1987 Less than 15 favors brook trout Sympatry with brook trout 15 18 under satiation rations. Mullan et al., 1992 8 13 Brook trout are better able to compete Cunjak and Green, 1986 Below 14 ( maximum temperatures) Bull Trout Haas, 2001 Cutthroat Trout 20 and above Colorado cutthroat are in sympatry with Brook trout at 10 DeStaso and Rahel, 1994 Lahontan cutthroat equal with brook trout at 15 Schroeter, 1998 Temperature Preferences in the Laboratory: Page 68 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Chinook Salmon Brett ( 1951; as cited in Ferguson, 1958) reportedly found that the final preferendum temperature for chinook is 11.7 ° C. Sauter and Maule ( 2000) found that the mean temperature preference of fall chinook decreased from a high of 17.77 to a low of 11.12 ° C during smoltification, while yearling spring chinook salmon showed no change in their preference for a mean temperature of 16.69 ° C.

Coho Salmon Piper et al. ( 1982) suggested that maximum temperatures between 9.4 14.4 ° C are optimal or selectively preferred by juvenile coho; however, Bell ( 1986) suggested the preferred range for coho is 4.4 9.4 ° C. Konnecki, Woody and Quinn ( 1995) studied two groups of coho and found that the preference temperature changed with the parental stock used. Coho from parental stock originating from cold ground water supplied streams preferred 9.6 ° C ( range 6 16 ° C), while those from stock originating from warmer streams preferred 11.6 ° C ( range 7 21 ° C).

Chum Salmon Juvenile chum salmon reportedly prefer temperatures between 11 14.6 ° C, and are considered to be optimally maintained at 13 13.5 ° C ( Kepshire, 1971; as cited in Brett, 1979). Ferguson ( 1958) suggests that the final temperature preferendum for chum salmon is 14.1 ° C. In a 1952 study, Brett found that juvenile sockeye avoided temperatures above 15 ° C and selected 12 14 ° C when provided an opportunity.

Pink Salmon Bell ( 1986) and Bonar et al. ( 1989) suggest pink salmon prefer waters in the range of about 5.6 14.5 ° C, while Ferguson sets the final preferendum at 11.7 ° C and Brett ( 1952) determined pink salmon acclimated to temperatures below 15 ° C select temperatures in the range of 12 14 ° C.

Sockeye Salmon Ferguson ( 1958) used earlier work by Brett ( 1951) to determine that the final preferendum for sockeye was 14.5 ° C. Brett ( 1971; as cited in USEPA, 2001) found swimming capacity, metabolic scope, growth on excess rations, and ingestion were maximized at 15 ° C, and that 15 ° C was also the final preferendum temperature.

Steelhead and Rainbow Trout Evaluating Standards for Protecting Aquatic Life in Page 69 Washington's Surface Water quality Standards Hahn ( 1977) compared the preference decisions of fry and yearling steelhead exposed to three constant ( 8.5 ° C, 13.5 ° C, and 18.5 ° C) and one fluctuating ( 8 19 ° C) temperature regime. Hahn found that as many fish remained in the fluctuating regime ( which has a mean of 13.5 ° C) as in the constant 13.5 ° C regime; twice as many fish remained in the fluctuating regime compared with the constant 18.5 ° C; and twice as many remained in the constant 8.5 ° C as in the fluctuating regime. By inference, Hahn concluded that twice as many fish preferred a constant 13.5 ° C to a constant 18.5 ° C, and twice as many preferred a constant 8.5 ° C to a constant 13.5 ° C. Hahn's work suggests that juvenile steelhead may have a preference for water temperatures between 8.5 13.5 ° C. It also suggests that the daily average temperature may roughly equal a constant exposure test scenario for the purpose of translating laboratory tests into water quality criteria.

Ferguson ( 1958) cites 13.6 ° C as the final preferendum temperature for rainbow trout. The work of Li et al. ( 1993; and 1994) and Li et al. ( 1991; as cited in Spence et al., 1996), studying interior populations of rainbow trout, suggest that while rainbow trout showed no avoidance reactions when stream temperatures were below 20 ° C, they actively avoided staying in waters warmer than 23 25 ° C. McCauley and Huggins ( 1975) found that five large ( 150 250 grams) rainbow trout had a preferred mean temperature of 16.7 ° C, and that the fish actively cycled between 13.8 ° C and 18 ° C. The work and literature citations of Kwain and McCauley ( 1978) ( citing Huggins 1978 Garside and Tait, 1958, Christie as reported in Fry, 1971, and McCauley et al., 1977) support the position that rainbow trout temperature final preferendum decline from 17 21 ° C in first six months of life to eventually centering on 13 ° C as overyearlings. McCauley and Pond ( 1971) found that underyearling rainbow trout showed a preference for 17 20 ° C in laboratory tests.

Summary of Laboratory Temperature Preference Studies The results of preference testing depends upon acclimation temperature, length of test, breadth of temperature gradients used, and age of fish. Fish will actively cycle between temperature regimes during the test period, which is typically one hour in length, and their time spent in different temperature zones is used to determine where they spent most of their time ( preference is in essence the mode of the distribution). While the range of temperatures through which fish commonly cycled during the tests extended from 4.4 21 ° C, preferred temperatures ranged from 9.6 17.7 ° C. The majority of the preferred temperatures were from 11.6 16.7 ° C ( see Table 4.12, below). These preferred tests would best relate to a daily mean temperature. A daily mean of 11.6 16.7 ° C would be roughly equivalent to a 7DADMax of 14.2 19.3 ° C ( 16.75).

Table 4.12. Results of laboratory studies examining temperature preferences.

Species Preferred Preferred Comments Author Page 70 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards temperature Range Chinook 11.7 Final preferendum Brett, 1951 17.7 to 11.12 Fall Chinook decrease in preference during smoltification Sauter and Maule, 2000 16.69 Spring chinook Sauter and Maule, 2000 Coho 4.4 9.4 Bell, 1986 9.4 14.4 9 Piper et al., 1982 9.6 6 16 Parental stock from colder water Konnecki et al., 1995 11.6 7 21 Parental stock from warmer water Konnecki et al., 1995 Chum 11 14.6 Kepshire, 1971 14.1 Ferguson, 1958 12 14 Brett, 1952 Pink 5.6 14.5 Bell, 1986 and Bonar et al., 1989 11.7 Ferguson, 1958 12 14 Acclimated below 15 Brett, 1952 Sockeye 14.5 Used work of Brett, 1951 Ferguson, 1958 15 Final preferendum Brett, 1971 Steelhead and rainbow trout 8.5 13.5 Hahn, 1977 13.6 Final preferendum Ferguson, 1958 Actively avoided 23 25 Li et al., 1991, 1993, and 1994 16.7 13.8 18 Cycled between 13.8 18 McCauley and Huggins, 1975 17 21 First six months of life. Kwain and McCauley, 1978 13 Overyearlings Kwain and McCauley, 1978 17 20 Underyearlings McCauley and Pond, 1971 Evaluating Standards for Protecting Aquatic Life in Page 71 Washington's Surface Water quality Standards Swimming Performance and Scope of Activity:

Coho Salmon In tests on swimming performance, Griffiths and Alderdice ( 1972) and Brett et al.( 1958) found that optimum swimming performance in juvenile coho salmon occurred at a combination of acclimation and test temperatures near 20 ° C. Griffiths and Alderdice reported that above 20 ° C swimming performance experienced a marked reduction. Delacy et al. ( 1956) and Paulik et al. ( 1957) also studied the swimming performance of coho salmon. They found that coho could recover to approximately to 31% after a one hour rest and to 70% within three hours of exhaustive swimming effort, and recover fully overnight. They also noted that eggs taken from coho salmon repeatedly fatigued in their testing exhibited normal fertility and survival. A significant swimming performance decrement was associated with pre test activity of the salmon, and salmon that swam longer before fatigue required more recuperation time; suggesting that the salmon are highly susceptible to fatigue. Beamish ( 1978; as cited in USEPA, 2001), in a literature review indicated that coho reach a maximum speed at approximately 17 18 ° C.

Sockeye Salmon Brett ( 1971; as cited in USEPA, 2001) found swimming capacity, metabolic scope, growth on excess rations, and ingestion were maximized at 15 ° C, and that 15 ° C was also the final preferendum temperature. In tests on physiological performance, juvenile sockeye reach their maximum swimming speed at 15 ° C ( Brett and Glass, 1973; Brett et al., 1958). Brett et al. ( 1958) noted that the capacity of young sockeye to stem a normal river current of 1.0 ft/ sec. for more than an hour is limited to a relatively small temperature range of 12.5 17.5 ° C. Beamish ( 1979; as cited in USEPA, 2001) found that sockeye reached maximum speed at 15 ° C.

Mcdonald et al. ( 2000) used field studies to conclude that optimal swimming performance occurs at 17 ° C and that a 20% reduction occurs at 21 ° C. Brett ( 1983) in discussing the energetic needs of sockeye suggested that the protected environment of a growth metabolism tank or hatchery pond may not correspond well with the search attack avoid escape patterns of real life. An attack or escape episode involving 20 second burst speed was shown, in terms of energy expended, to be equal to that of 15 minutes of active metabolism ( maximum sustained swimming speed) or about 3 hours of basal metabolism ( cites Brett and Groves, 1979). Brett suggests the additional energy requirements of real life cannot be disregarded; nor can it be conceived as incessantly present. Hinch and Bratty ( 2000) found that Fraser River sockeye used a " burst and then sustained" swimming pattern to negotiate obstacles, and that fish that maintained the " burst" phase too long failed to negotiate significant obstacles and often dropped back downstream failing to complete their migration. This work showed two important facts, the first being that sockeye may be near the limits of their performance while migrating through rapids and that fatigue can result in the permanent loss of the migrants, and that fish may use techniques to perform better in the field than in laboratory experiments. That such stressors may be additionally selective against individuals Page 72 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards is also likely. The work by Hinch and Rand ( 1998) and others has shown that males suffer more swimming impairment then females and that small fish must expend more energy than larger fish.

Steelhead and Rainbow Trout Cech and Myrick ( 1999) found that winter run steelhead swimming velocities increased slightly with an increase in temperature from 11 ° C to 15 ° C and decreased slightly with an increase in temperature from 15 ° C to 19 ° C. Dickson and Kramer ( 1971) found that the maximum scope of activity occurred at 20 ° C in rainbow trout.

Cutthroat Trout Dwyer, and Kramer ( 1975; as cited in Dunham, 1999; and Gresswell, 1995) found the greatest scope for activity in cutthroat trout to be at 15 ° C.

Table 4.13. Studies examining swimming speed and maximum scope for activity.

Species Maximum performance Prolonged performance Author Coho 20 A marked reduction occurred above 20 Griffiths and Alderdice, 1972 20 Brett et al., 1958 17 18 Literature review Beamish, 1978 Sockeye 15 Brett, 1971 15 Brett and Glass, 1973 15 Brett et al., 1958 12.5 17.5 Capacity to stem normal current for more than one hour limited to range of 12.5 17.5 Brett et al., 1958 15 Beamish, 1979 17 Based on field studies. 20% reduction at 21 Mcdonald, 2000 Steelhead and 15 Cech and Evaluating Standards for Protecting Aquatic Life in Page 73 Washington's Surface Water quality Standards rainbow trout Myrick, 1999 20 Maximum scope for activity Dickson and Kramer, 1971 Cutthroat 15 Maximum scope for activity Dwyer and Kramer, 1975,

15 Maximum scope for activity Gresswell, 1995 Maximum swimming speed and maximum scope for activity have been noted at temperatures ranging from 15 20 ° C ( 17.5) in salmon and trout. The short term tests that were used to base most of these estimates on, and the real time effects of temperature ( the effect of temperature is essentially immediate on swimming performance) suggests these estimates may best transfer to some daily maximum metric. The biological consequences of having a shortperiod of each day not allowing for maximal performance is difficult to ascertain. However, the works of Brett ( 1958) and Mcdonald ( 2000) were designed to better transfer swimming performance estimates to the field, and suggest a more narrow temperature range ( 12.5 17.5 ° C, and 17 ° C, respectively) of temperatures. Based on these factors it seems reasonable to assume that exposure to temperatures above 17 17.5 ° C may have detrimental biological consequences in cases where overcoming predators and river obstacles is necessary. Since these temperature effects are not apparently affected by average exposures, it is believed that a 7DADMax of 17 17.5 ° C should be considered the upper temperature regime that will fully protect the swimming performance of salmon and trout in riverine environments.

Field Distribution Restrictions in Juvenile Fish:

Chinook Salmon In the work of Torgersen et al. ( 1999) fish from portions of the John Day River basin in Oregon were found strongly associated with cool water segments in the middle fork where temperatures ranged from 22 24 ° C along its length, but were much less related to temperature fluctuations in the cooler north Fork where temperatures ranged from 15 22 ° C along its length. In an unpublished report to the USEPA and the National Science Foundation ( 1999) Torgersen, Baxter, Li, and McIntosh further discuss the spatial distribution of fish in the John Day. They noted that the cross over point where cold water fish no longer dominate over warm water fish occurred where afternoon temperatures reached 17 ° C. The general range for chinook salmon has been suggested as extending from 0.0 0.6 ° C to 25 ° C, with an optimal or preferred range extending from 6.7 10 ° C to 13.9 14.4 ° C ( Bell, 1986; Piper et al., 1982). Page 74 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Coho Salmon In trying to determine the cause for coho losses from streams on the west side of Mount St. Helens, Martin et al. ( 1986) found that summer mortality was correlated with both high monthly average temperatures and maximum August diel fluctuations. One creek experiencing high mortality exceeded 25 ° C for 10 days in one year and 30 days in the next. Bisson et al. ( 1988) found that growth remained positive in streams that exceeded 24.5 ° C, but that at about 22 ° C the coho seek out cool water areas. Hall and Lantz ( 1969) found no statistically significant change in coho abundance in a clear cut test stream where maximum summer temperatures were increased from 16.1 16.6 ° C to 24 30 ° C, even though cutthroat trout populations experienced a decline of 75%. In a study of salmonid distributions in a coastal Oregon river drainage, Frissell, Nawa, and Liss ( 1992) found that cutthroat, coho, and chinook salmon dropped out in sequence as daily maximum temperatures increased, with rainbow trout being the only species found in waters exceeding 23 ° C. An abrupt loss of coho and chinook was found to occur between 21 and 23 ° C, and while small numbers of coho were found in the warmer waters, they were always found in association with small cool pockets of otherwise warm reaches.

Chum Salmon Juvenile and adult chum salmon have been observed in waters with temperatures ranging from 0 25.6 ° C ( Bell, 1986). Bonar et al. ( 1989) considered 10.1 ° C to be the optimal temperature for adults in marine waters.

Pink Salmon Pink salmon are noted as being found in temperatures ranging from 0 25.6 ° C ( Bell, 1986), while Sheridan ( 1962) has stated that the range in Alaskan waters extends from 7.2 18.3 ° C. Welch et al. ( 1995) determined that the upper thermal boundary for the offshore marine occurrence of pink salmon was 10.4 ° C.

Sockeye Salmon While sockeye salmon are noted to occur within the range of 0.6 21 ° C ( Piper et al., 1982), the range of temperatures under which they perform optimally may be more restricted. The optimal temperature for juvenile rearing was identified 10 15 ° C by Piper et al. ( 1982), and 10.6 12.2 ° C by Bell ( 1986).

Steelhead and Rainbow Trout Frissel et al. ( 1992) studied the distribution of rainbow trout and found that while they could be found in water temperatures over 23 ° C, there was a general threshold response for age 1+ fish above 22 ° C and for age 2+ fish above 21 ° C. Evaluating Standards for Protecting Aquatic Life in Page 75 Washington's Surface Water quality Standards The work of Li et al. ( 1993; and 1994) and Li et al. ( 1991; as cited in Spence et al., 1996), studying interior populations of rainbow trout, suggest that while rainbow trout showed no avoidance reactions when stream temperatures were below 20 ° C, they actively avoided staying in waters warmer than 23 25 ° C. While the works of Li et al. ( 1991, 1993, and 1994) were conducted on interior populations of trout ( likely to have been redband trout), Behnke ( 1992) reported finding redband trout in the desert basins of southern Oregon and northern Nevada that regularly encounter temperatures that kill other trout. Trout in these intermittent desert streams were found actively feeding in water of 28.3 ° C.

Kaya et al. ( 1977) found that daily maximum temperatures exceeding 25 ° C caused rainbow trout to move out of the main stem of the Firehole River in Montana. These fish would move into tributary streams that averaged 6 10 ° C lower in temperature. Behnke ( 1992) in a review of the Kaya ( 1978) study concluded that thousands of years of adaptation to a desiccating environment have enabled the Oregon desert redband trout to feed at high temperatures, but 60 70 years seem too few to have allowed the planted rainbow trout to expand their functional feeding temperature in the Firehole River. While there are observations of redband trout feeding and surviving at relatively high temperatures for a salmonid ( 28 ° C, Behnke 1992; 27.4 ° C, Sonski 1986 and 27 ° C, Bowers et al. 1979 as cited in USEPA, 2001), it is unclear whether temperatures were measured at the location of the stream where the fish were found. These trout may rely on microhabitats or thermal refugia to maintain populations in desert environments ( Ebersole et al. 2001). Thus it may not be appropriate to use these observations to conclude that such temperatures are not harmful. However, the basis for the argument that interior redband may have warmer optimum limits then the coastal rainbow stocks seems likely, even if it is not well established in the literature. It is believed that the upper range of what is sometimes found as fully protective for rainbow trout should be applied specifically to these interior non anadromous redband trout.

Cutthroat Trout Bell ( 1986) used a review of the literature to conclude that the range for cutthroat trout was from 0.6 22.7 ° C, and the preferred range was from 9.4 12.7 ° C. Hall and Lantz ( 1969) found a 75% reduction in a cutthroat trout population in response to experimental logging of riparian canopies in three coastal streams. Prior to treatment, these streams had monthly average temperatures ranging from 6.1 12.8 ° C and maximum temperatures ranging from 16.1 16.6 ° C. In the treatment stream experiencing the greatest canopy removal, daily maximum temperatures increased to 24 and 30 ° C in the two years following treatment. These results compared well with the work of Frissell et al. ( 1992) who studied the distribution of salmonids in a small coastal river system in southwest Oregon. They found that cutthroat, coho, and chinook salmon dropped out in sequence as maximum temperatures increased, with rainbow trout the only species present in waters exceeding 23 ° C. Cutthroat were absent, and coho salmon rare in segments exceeding 21 ° C. While Varely and Gresswell ( 1988; as cited in Gresswell, 1995) reported that Yellowstone cutthroat are found in geothermally heated streams with ambient temperatures of 27 ° C, they report these fish are found associated with cooler thermal refuges. Varley and Gresswell ( 1988) suggested that the optimum water temperature for Yellowstone cutthroat trout is from 5.5 15.5 ° . Kelly Page 76 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards ( 1993: as cited in Gresswell, 1995), however, reportedly found that cutthroat were excluded from a tributary to the Yellowstone River because summer water temperatures often exceeded 22 ° C. Dunham et al. ( unpub.; as cited in Dunham, 1999) found Lahontan cutthroat appear to have distributional limits that correspond closely to maximum water temperatures of 26 ° C. Pauley et al. ( 1989) suggest that cutthroat trout are not usually found in waters where the maximum temperature exceeds 22 ° C even though they may tolerate brief periods of temperatures as high as 26 ° C.

Table 4.14. Summary of information on the field distribution of salmonid and trout in relation to temperature.

Species Temperature for range Optimal or preferred range Author Chinook 15 22 Range of river temperatures where fish not found in association with refugia Torgersen et al., 1999( a)

17 ( daily max) Point where warm water fish begin to dominate Torgersen et al., 1999( b)

0.0 0.6 to 25 6.7 10 to 13.9 14.4 General observed range Bell, 1986, and Piper et al., 1982 Coho 22 Begin to seek out refugia Bisson et al., 1988 24 30 ( daily max) No change in abundance with rise from 16.1 16.6 to 24 30 Hall and Lantz, 1969 21 23 ( daily max) Abrupt loss in coho Frissel et al., 1992 Chum 0 25.6 General observed range Bell, 1986 10.1 Optimal in marine water Bonar et al., 1989 Pink 0 25.6 General observed range Bell, 1986 7.2 18.3 In Alaska Sheridan, 1962 10.4 Upper thermal boundary in marine water Welch et al., 1995 Sockeye 0.6 21 10 15 General observed range Piper et al., 1982 10.6 12.2 Bell, 1986 Steelhead and rainbow trout 22 ( age 1+) 21 ( age 2+) General threshold Frissel et al., 1992 Evaluating Standards for Protecting Aquatic Life in Page 77 Washington's Surface Water quality Standards response 27, 27.4, 28.3 Redband trout found actively feeding Bowers, et al., 1979, Sonski, 1986, and Behnke, 1992 25 ( daily max) 15 19 Caused rainbow trout to move from main stem Kaya et al., 1977 23 25 20 Redband actively avoided 23 25, but not 20 Li et al., 1991, 1993, and 1994 Cutthroat trout 0.6 22.7 9.4 12.7 General observed range Bell, 1986 16.1 16.6 ( daily max) Increase from 16.1 16.6 to 24 30 resulted in a 75% population reduction Hall and Lantz, 1969 21 ( daily max) Absent in segments exceeding 21 Frissel et al., 1992 27 5 15.5 Yellowstone cutthroat found in river at 27 in association with refugia Varley and Gresswell, 1988 22 Yellowstone cutthroat reported to be excluded above 22 Kelly, 1993 26 ( daily max) Lahontan cutthroat distributional limits Dunham et al., 1999 22 ( daily max) Seldom found above Pauley et al., 1989 While some authors report finding salmon and trout in the range of 24 30 ° C, most found that their presence was dependent upon cold water refugia. The general pattern of the findings cited above seems to suggest that daily maximum river temperatures of 21 22 will create a distributional limit to finding salmon and trout, and that healthy populations are more likely to be found within the range of 10 19 ° C. Most authors, however, place the optimal range below 17 ° C and Torgersen et al., ( 1999b) additionally found that warm water species begin to dominate above 17 ° C. Thus based on this line of evidence, a 7DADMax of 16.05 ° C should be considered the limit for finding strong populations of salmon and trout, and river temperatures above a 7DADMax of 20.05 21.05 ° C should be considered to create a thermal Page 78 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards barrier to the general summer distribution of salmon and trout. Beyond this temperature barrier, the presence of salmon and trout may be primarily dependent on the availability of cold water refugia. There is reason to suspect that redband trout may have slightly higher temperature ranges than the other native salmon and trout. The information is scant and should be used with caution, but it suggests that the healthy distribution of redband trout may be better described by 18.05 ° C as 7DADMax, and 22.05 ° C may more appropriately describe the thermal barrier for redband populations.

General Findings and Recommendations Found in the Literature:

Chinook Salmon The Independent Scientific Group ( 1996) concluded that juvenile chinook salmon rearing is optimal where temperatures are maintained in the range of 12 17 ° C; and suggests 15 ° C is most optimal.

Coho Salmon Servizi and Martens ( 1991) found that susceptibility to sediment toxicity increased by 33% at 18 ° C, and Shelbourn ( 1980) determined that hypo osmoregulatory capacity is optimized at 14 ° C.

Steelhead and Rainbow Trout Bell ( 1986) recommended that temperatures generally be maintained in the range of 7.3 14.5 ° C for optimal rearing of juvenile steelhead. Evaluating Standards for Protecting Aquatic Life in Page 79 Washington's Surface Water quality Standards Conclusion on Juvenile Rearing of Salmon and Trout:

Table 4.15. The multiple lines of evidence for juvenile rearing of salmon and trout.

Line of Evidence 7DADMax ( ° C) Midpoint Comments Laboratory Growth Studies Conducted at Constant Temperatures 14.18 18.14 16.16 Based on well controlled laboratory tests.

Ranges Identified in Literature as Optimal for Growth 15 21 18 Basis for estimates and intended metrics unclear.

Comparison Test Regimes With Better Growth 11.8 15.4 13.6 Maximum growth temperatures were not determined, only favorable growth compared to one other significantly warmer or cooler temperature. Laboratory Growth Studies in Fluctuating Temperature Regimes 13.16 21.14 17.15 Based on well controlled laboratory tests.

Field Studies on Growth 14.05 16.05 15.05 Regime with better standing crops. Specific temperature limits were not determined. Predation and Competition 17.60 18.18 17.89 Displacement of juvenile salmon and trout Temperature Preferences in the Laboratory 14.2 19.3 16.75 Mode of distribution of fish cycling between temperature zones Swimming Performance and Scope for Activity 17 17.5 17.25 Based primarily on controlled laboratory studies.

Field Distribution  Healthy 16.05 16.05 Basis and methodology generally unclear for most literature estimates. Thus this estimate relies on the general upper range considered healthy, and temperatures above which coldwater species begin to loose dominance Best estimate of threshold 14.78 18.08 mid. pt. 16.43 Using all nine lines of evidence cited above, the upper limit to defining a healthy summer rearing temperature would occur within the range of 14.78 18.08 ° C as a 7DADMax, with an Page 80 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards overall mean of 16.43 ° C. While each line of evidence has unique strengths and weaknesses, the second and third lines of evidence are particularly questionable. The second line of evidence consists of technically unsubstantiated recommendations of specific authors, and the range produced in the third line of evidence is driven by comparisons tests that only compared and contrasted two very different test regimes ( e. g., only compared 8 to 12) without any effort to identify maximum growth. Without these two very weak lines of evidence, the range within which favorable juvenile rearing would be expected changes to a 7DADMax of 15.18 18.05 ° C ( 16.62 ° C). Since both estimates would round out to the same ½ degree value, it is recommended that a 7DADMax of 16.5 ° C be considered fully protective of juvenile rearing.

iv) Juvenile Winter Holding Chinook Salmon Temperature declines below 1.1 5 ° C can cause fish to become dormant and move into the substrate. Once fish have initiated hiding behavior, it may take temperatures rising again to above 7 ° C to bring them back out ( Chapman and Bjornn, 1969). While this natural behavior is a healthy response for winter survival, unseasonably cold discharges causing water temperatures to unseasonably fall below 5 7 ° C need to be avoided. Dropping the temperature to 2.5 ° C for even a few days may result in mortality to chinook that were acclimated to a river temperature of 15 ° C ( Brett, 1956). To avoid initiating unseasonable hiding behavior, to avoid lethal effects, and to encourage strong growth rates the daily low temperature should typically exceed 7 ° C during the growing season.

Steelhead and Rainbow Trout After steelhead fry emerge from the gravel they move to the slow moving waters of the stream margins, shifting to faster and deeper waters as they grow larger ( Chapman and Bjornn, 1969). Martin et al. ( 1991) and Wydoski and Whitney ( 1979) note the importance of cover to juvenile steelhead. Large woody debris, substrate, and turbulence are all identified as important habitat for young juveniles. Temperature is believed to affect the habitat selection and migration of juveniles. Mullan et al. ( 1992) found that fry emigrate from cold headwater streams to down stream reaches to rear in warmer waters. Chapman and Bjornn ( 1969) found that young steelhead may move downstream in the fall to over winter in larger streams. Chapman and Bjornn ( 1969) found that 5 5.5 ° C marked the boundary between activity and inactivity in steelhead, with fish entering the substrate. They found that steelhead emigration could be stopped by warming the water from 7.2 ° C to 11 12.2 ° C. Mullan et al. ( 1992) suggest that while steelhead juveniles may reside in the dark frozen snow covered tributaries near 0 ° C for up to 5 months, 6 ° C may form the boundary that allows winter growth to occur.

Some controlled field studies have shed some light on the winter rearing habits of rainbow trout. Rainbow trout actively feed at very cold temperatures ( 0 0.6 ° C) even under ice Evaluating Standards for Protecting Aquatic Life in Page 81 Washington's Surface Water quality Standards covered streams. Their winter feeding habits are primary controlled by the availability of food. They consume dislodged insects, and feed on insects that emerge at more moderate temperatures ( 4.4 ° C or more). Winter mortality is likely due to a combination of factors including insufficient food supply, and physical damage from snow slumps and ice scour ( Needham and Jones, 1959; Needham and Slater, 1944; Maciolek and Needham, 1952; and Reimers, 1957).

Cutthroat Trout Jokober et al. ( 1998) found that westslope cutthroat trout made extensive migrations downstream to escape winter conditions that resulted in supercooling (< 1 ° C) of the water and anchor ice formation.

v) Adult Migration Barriers to Migration of Salmon and Trout:

Chinook Salmon After spending 3 4 years in the ocean mature chinook salmon begin their return migrations to freshwaters to spawn. Temperatures can create serious problems for migrating salmon. In addition to posing the threat of direct lethality to adult spawners, temperatures can create blockages that stop migrating fish, create conditions that result in high mortality of spawners from disease, and reduce the overall fitness of migrants. Since migrating salmon do not feed in freshwaters they must enter freshwater with sufficient fat and muscle reserves to supply their metabolic requirements up to and through the act of spawning. The increased active and basal metabolic demands caused by traveling and holding in warmer waters uses up stored energy reserves at a more rapid rate. This can result in a decrease in the quality and quantity of eggs as well as an overall reduction in the fitness of the adult fish that need to migrate and negotiate obstacles, excavate and guard redds, and complete the act of spawning. Berman and Quinn ( 1991) demonstrated that in the months prior to spawning, spring run chinook actively sought out cool water refuges in the Yakima River, in Washington. These fish were able to maintain average internal temperatures 2 5 ° C below the ambient river condition, which may have reduced their metabolic demand by 12 20%. Mcdonald et al. ( 2000) found that chinook salmon in the Fraser River in Canada suffered unusually large losses ( 25%) where mean daily river temperatures frequently exceeded 20 ° C and reached a high of 23 ° C. The most widespread concern with warm temperatures is from prespawning mortality due to an increased incidence of diseases. These diseases can directly kill or impair healthy fish, or act secondarily through infection of the minor wounds that normally occur in migrating fish. Disease is a serious concern and is discussed and incorporated separately in the recommendations of this paper.

Daily maximum temperatures rising above 21 22 ° C are widely cited as causing barriers to migrating chinook salmon ( Stabler, 1981; Bumgarner et al., 1997; Hallock, Elwell, and Fry, Page 82 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards 1970; Thompson, 1945, as cited in Snyder and Blahm, 1971; Don Ratliff, 1977, as cited in Stabler, 1981; Fish and Hanavan, 1948, and Major and Mighell, 1967, as cited in USEPA, 1971; and Alabaster, 1988, as cited by USEPA, 2001). Hallock, Elwell, and Fry ( 1970) suggested that maximum temperatures of 18.9 ° C in association with low dissolved oxygen levels ( 5ppm) created a partial block of migrating chinook salmon. However, some authors note chinook not showing avoidance for temperatures as high as 24.4 ° C ( Gray, 1990; Dunham, 1968; as cited in CDWR, 1988). However, Thompson ( 1945; as cited in Snyder and Blahm, 1971) suggested that it was the difference in temperatures that stopped chinook from migrating from the Columbia to the Snake River. Differences were 17.2: 21.7 ° C and 22.2: 26.1 ° C when blockages occurred, with migration resuming when the difference approached 1.6 ° C. Similarly, Gray ( 1990) suggested that incremental increases of 9 11 ° C formed a barrier to migration. Temperatures above 20 21 ° C are certainly stressful for chinook salmon. Sauter and Maule ( 1997) reported cessation of feeding as well as thermoregulatory behavior in sub yearling fall chinook held between 18 20 ° C, with exposure to 20 ° C for several hours inducing heat shock proteins ( Sauter et al., in review, and M. Hargis, personal comm.; as cited in Sauter and Maule, 1997). In a field study by Frissel, Nawa, and Liss ( 1992), it was found that maximum water temperatures in a coastal river system in Oregon were linked to the presence or absence of various species of salmonids. While it was noted that cutthroat were absent and coho salmon rare or absent in segments exceeding 21 ° C, chinook dropped out completely only at 23 ° C; although, their presence in such waters was associated with positioning in small cool pockets in otherwise warm reaches. Some authors have suggested criteria for the protection of migrating chinook salmon. Piper et al. ( 1982) considering this important life stage suggested that 7.2 15.6 ° C was necessary to protect upstream migration and maturation. Bell ( 1973; as cited by Everest et al., 1985) suggested that temperatures should be within the range of 3.3 13.3 ° C for spring chinook, 13.9 20 ° C for summer chinook, and 10.6 19.4 ° C for fall chinook. Support for assuming a general 20 21 ° C threshold for salmon migration can also be found in the technical literature on lethality studies. As summarized below, temperatures of 20 22 ° C, particularly at lower prior acclimation temperatures, can be directly lethal to chinook salmon ( Brett, 1956; Brett et al., 1982; Coutant, 1970; Beacham and Withler, 1991; Becker, 1973; Orsi, 1971; as cited in CDWR, 1988) with a 7 day exposure. It also appears from the available evidence that adults may be more sensitive than the juveniles which are most typically tested ( Becker, 1973). Based on the technical literature, it is concluded that to prevent a risk of causing blockage of migrating chinook salmon daily maximum temperatures should not exceed 21 22 ° C, particularly when the migrating fish will be acclimated to lower ( 2 6 ° C) water temperatures as they travel upstream.

Many runs of chinook will need to hold or travel during the summer when stream temperatures are at a maximum in the lower and mid elevation rivers. Therefore, criteria to protect migration should be set to protect against chronic sublethal effects as well as acute effects such as blockages and lethality. While chinook adults can almost certainly withstand occasional daily peak temperature cycles up to 22 ° C, the general condition encountered by these migrating fish should approach more optimal conditions. This will avoid unhealthy levels of stress and utilization of stored energy reserves. It is concluded that summer daily maximum temperatures during migration should generally remain within or below the range Evaluating Standards for Protecting Aquatic Life in Page 83 Washington's Surface Water quality Standards identified previously as fully protective for juvenile chinook salmon rearing, and single daily maximum temperatures be maintained below 20 21 ° C wherever possible.

Where fish may hold in waterbody segments for long periods of time prior to spawning, as is commonly the case for spring chinook, special protection may be warranted on a casespecific basis. To protect adult fish that are holding throughout the summer, temperature limits should be established that recognizes these fish are living off their stored energy reserves and may be in a ripe condition in the later portion the summer or early Fall. Three physiological endpoints seem especially relevant in guiding the selection of an appropriate summer holding criteria. The first is the preferendum values ( constant 11.7 ° C, and a range of 6.7 14.4 ° C), the second is the fully protective rearing threshold ( an average of 14 15 ° C, and a 7 day average of the daily maximum temperatures of 16.5 ° C) and the third is the temperature regime identified to protect eggs invivo in ripe females ( weekly average temperatures below ( 13 15 ° C). In consideration of these factors it is concluded that where chinook are holding over the summer, the average water temperatures should be maintained below 13 14 ° C and the 7 day average of the daily maximum temperatures maintained below 16 17 ° C.

Coho Salmon While adults can migrate through waters warmer than considered fully protective for juvenile rearing, the same thresholds which produce metabolic stress with juveniles are likely to produce stress in adults that can lead to lethal and sublethal effects. Beschta et al. ( 1987) suggested as a basis for water quality criteria that upstream migration occurs between 7.2 15.6 ° C. Studies with other species support the work of Thomas et al. ( 1986) in showing that adults may actually be somewhat more temperature sensitive than juveniles. Sensitivity is enhanced in adults through the fact that they do not feed during their freshwater migration and must rely on their stored fat and muscle reserves to see them through the spawning process. The stress of higher temperatures not only influences the health of the spawner, but to some extent it also can effect the quality of unfertilized eggs carried by the hen salmon. In tests evaluating the effects of holding ripe adult coho at warm temperatures, Bouck et al. ( 1970; as cited in USEPA, 1971) found no apparent adverse effects to eggs in utero caused by prolonged exposure to 16.7 ° C. Flett et al. ( 1996), however, found that adults migrating through waters often warmer than 20 ° C experienced reduced quality and more rapid deterioration of eggs. For these reasons it would be prudent to maintain temperatures close to the range considered fully protective for juvenile coho ( i. e., 7DADMax temperatures below 16.5 ° C) over the migration routes used by adult spawners. Page 84 Evaluating Standards for Protecting Aquatic Life in Washington's Surface Water quality Standards Chum Salmon Studies were not found that establish a specific basis for setting adult upstream migration temperature threshold. Beschta et al. ( 1987) has suggested as a basis for establishing water quality criteria that upstream migration is protected by keeping water temperatures in the range of 8.3 15.6 ° C. While adults can certainly withstand much higher temperatures for short periods of exposure without directly lethal effects, the potential of warm waters ( above 14 ° C) to reduce the number of viable eggs, as shown in other fish species, should be cause for some caution. Since chum salmon spawn just above tidewater and have very short migrations in most watersheds, their time in migration and thus the potential for sublethal effects appears at least somewhat naturally mitigated in most cases. Recommendations to prevent barriers to migration and to protect other mature Pacific salmon spawners ripe with eggs should also be applied for chum salmon.

Pink Salmon Unlike most Pacific salmon, the pink salmon that occur in Washington have relatively short migrations and concerns over disease and over depleting energy reserves are less than with the other salmon. However, migrating adults will pass through the lower reaches of major rivers near the period of maximum seasonal temperatures and disease is still a concern that should be considered in setting any final temperature recommendations ( discussed and incorporated separately). It is also worthy of consideration that pink salmon have lower maximum sustained swimming speeds than sockeye salmon ( 20% less) and require more energy to support the same speed ( 30% higher) ( Brett, 1982; as cited in Brett, 1995). While no specific recommendation is warranted for pink salmon migration, the literature reviewed herein suggests that caution should be exercised in applying the upper end of the optimal range to waters that may support longer than typical migrations or periods of holding by pink salmon.

Sockeye Salmon Migration exerts a tremendous strain on salmon. Idler and Clemens ( 1959) found that female sockeye salmon in the Fraser River may use between 91.4 96% of their body fat reserves, and 53 61% of their protein reserves from the time of entrance to completion of spawning. As noted by Brett ( 1983), migration and egg production uses up most of the energy stored from ocean feeding and leaves " all too slim a safe margin of energy reserves".

Linley ( 1993; as cited in Quinn et al., 1997) reportedly found that populations with arduous migrations show lower levels of reproductive output ( ovary weight) than populations with shorter migrations. At a constant 16.2 ° C, depletion of fat reserves and reproductive organ abnormalities were noted by Bouk ( 1977), and Gilhousen ( 1990) found that high prespawning mortalities were associated with adult salmon migrating through waters having daily maximum temperatures between 17.5 19 ° C. Temperatures above 15.5 ° C ( as an apparent daily average value) were also noted by Gilhousen ( 1990) as being linked to higher prespawning mortality from columnaris disease in adult Fraser River sockeye salmon. Evaluating Standards for Protecting Aquatic Life in Page 85 Washington's Surface Water quality Standards Mcdonald et al. ( 2000) in a comprehensive study of the migratory success of Fraser River sockeye in relation to temperatures found that during unusually warm years ( mean daily temperatures above 20 ° C) hormonal and stress indicators suggested that fish were suffering significant physical stress and maturation impairment. Temperature conditions detrimentally effected the ability of the fish to migrate successfully through rapids. Poor spawning success, poor egg quality and viability, and senescent death prior to spawning were all observed. The authors reference unpublished laboratory work of Dr. Craig Clarke showing that laboratory exposure to 19 ° C over a two week period significantly depressed hormones controlling maturation, but exposure to 15 ° C did not. This was noted as consistent with findings with rainbow trout showing that temperatures of 17 ° C can reduce steroid synthesis in rainbow trout testes ( citing Manning and Kime, 1985). Mcdonald et al. ( 2000) suggested that the upper threshold for successful reproduction of migrating sockeye salmon occurs with mean daily temperatures at the lower Fraser River ( Hells Gate) between of 18 22 ° C. The authors also note that field studies suggest the temperature for optimum swimming endurance is 17 ° C and that a 20% reduction occurs at 21 ° C. The authors conclude that migration blockages, susceptibility to disease, impaired maturation processes, increases to stress parameters, reduced efficiency of energy use, and reduced swimming performance all become more hazardous as daily mean temperatures exceed 17 ° C.

Paulik ( 1960) found that sockeye subjected to daily swimming tests did not live as long as control fish, and postulated that as migrating salmon move upstream their swimming capacity declines such that performance is progressively reduced. DeLacy et al. ( 1956) using eggs from coho salmon and steelhead trout found, however, that the viability of sex products did not seem to be affected by repeated exhaustive testing.

Welch et al. ( 1995) found that the upper thermal limit to the off shore occurrence of sockeye salmon was 8.9 ° C, and 8.9 ° C was found to be the maximum holding temperature in lakes by migrating adults ( Wydoski and Whitney, 1979).