Ralph Abele 

Chief, Water Quality Branch 

EPA Region 1 

5 Post Office Square # 100 

Boston, MA 021 09 

UNITED STATES DEPARTMENT OF COMMERCE 

National Oceanic and Atmospheric Administration 

NATIONAL MARINE FISHERIES SERVICE 

GREATER ATLANTIC REGIONAL FISHERIES OFFICE 

55 Great Republic Drive 

Gloucester, MA 01930-2276 

MAY 1 3 2015 

Re: Technical Assistance for Water Temperature Tolerances of Atlantic Salmon 

Dear Mr. Abele: 

This is in response to your letter received May 7, 2015 requesting only technical assistance on 

the existing temperature criteria found in the Maine Water Quality Standards and whether or not 

these current temperature criteria are protective of the listed Atlantic salmon (Salmo salar) and 

its designated critical habitat. 

NMFS Listed Species under the Endangered Species Act and Designated Critical Habitat 

The Gulf of Maine Distinct Population Segment (GOM DPS) of Atlantic salmon (Salmo salar) is 

listed as endangered under the Endangered Species Act (ESA). The GOM DPS includes all 

anadromous Atlantic salmon whose freshwater range occurs in the watersheds from the 

Androscoggin River northward along the Maine coast to the Dennys River. Included are all 

associated conservation hatchery populations used to supplement these natural populations; 

currently, such conservation hatchery populations are maintained at Green Lake National Fish 

Hatchery (GLNFH) and Craig Brook National Fish Hatchery (CBNFH). 

Critical habitat has been designated for listed Atlantic salmon pursuant to section 4(a)(3) of the 

ESA. The critical habitat designation for the GOM DPS includes 45 specific areas occupied by 

Atlantic salmon at the time oflisting. This comprises approximately 19,571 kilometers of 

perennial river, stream, and estuary habitat, and 799 square kilometers of lake habitat within the 

range of the GOM DPS. These areas include those physical and biological features essential to 

the conservation ofthe species. The entire occupied range of the GOM DPS in which critical 

habitat is designated is within the State of Maine. 

Thermal Tolerance for Atlantic Salmon Survival, Growth, and Development 

The following information on water temperature tolerances of Atlantic salmon is excerpted from 

the "Habitat requirements and management considerations for Atlantic salmon (Salmo salar) in 

the Gulf of Maine Distinct Population Segment (GOM DPS)" (Kircheis and Liebich 2007) and 

from the final rule designating critical habitat for the GOM DPS published in the Federal 
Register (74 FR 29300) on June 19, 2009 which identifies the primary constituent elements of 

Atlantic salmon habitat (see 50 CFR §226.217). 

Thermal Tolerance (Juvenile Feeding) 

Small parr and large parr have similar temperature tolerances (Elliott 1991 ). Water temperature 

influences growth, survival and behavior of juvenile Atlantic salmon. Juvenile salmon can be 

exposed to very warm temperatures (> 20°C) in the summer and near freezing temperatures in 

the winter, and have evolved with a series of physiological and behavioral strategies that enable 

them to adapt to the wide range of thermal conditions that they may encounter. Atlantic salmon 

are cold water fish and have a thermal tolerance zone where activity and growth is optimal 

(Decola 1970). The optimal temperature for parr for feeding and growth ranges from 15° to l9°C 

(Decola 1970). When water temperatures surpass 19°C, feeding and behavioral activities are 

directed towards maintenance and survival. During the winter when temperatures approach 

freezing, parr reduce energy expenditures by spending less time defending territories, feeding 

less, and moving into slower velocity microhabitats (Cunjak 1996). 

Though parr are capable of adapting to a broad range of temperatures, they do have an upper and 

lower temperature threshold for survival. A study conducted in Big Brook, Terra Nova National 

Park, Newfoundland, progressively acclimated parr to 27.5°C in freshwater. The upper lethal 

temperature was determined by probit analysis to be 27.8°C +/- 0.41 after 10,000 min exposure 

(Garside 1973). This limit is dependent on acclimation rates, more rapid acclimations may result 

in slightly higher upper lethal limits during shorter exposure times. Fry ( 194 7) indicated 

graphically that Atlantic salmon acclimated to 25°C possessed an upper lethal temperature of 

about 28.5°C. This level was determined from shorter tests which produced median resistance 

intervals of less than 1 ,000 minutes. It was assumed that it would not be possible to obtain less 

than 100% mortality in the testing range of 28-30°C for exposures of 10,000 minutes (Garside 

1973). 

A study conducted by Elliott (1991) sought to construct a thermal tolerance polygon for juvenile 

Atlantic salmon using fish from two populations. Juvenile salmon were acclimated to 5°C 

temperature increments ranging from 5°C to 25°C as well as 27°C and were then subjected to 1 °C 

positive or negative temperature increases to determine upper and lower limits for feeding and 

survival over periods of 10 minutes, 100 minutes, 1 ,000 minutes, and 7 days. Elliott ( 1991) 

identified a mean upper incipient temperature tolerance of 22.5°C and a mean lower incipient 

temperature tolerance of7.0°C by the cessation of feeding activity, which is a thermal stress 

response that influences both growth and survival of the fish. 

Thermal Tolerance (Adult Migration) 

Adult salmon migratory behaviors are significantly influenced by temperature and dissolved 

oxygen. Most migratory movement is conducted when temperatures range between 14 - 20°C 

(Elson 1969). Danie eta!. (1984) notes that at temperatures above 20°C adult salmon are rarely 

caught by angling and further states that temperatures between 20°C and 27°C reduces resistance 

to disease and are therefore indirectly lethal. Shepard (1995) assessed the migratory behaviors of 

adult Atlantic salmon in the Penobscot River from 1988 through 1992 and found that salmon 

continued to pass through the fishway at Veazie Dam in the lower Penobscot River when 

temperatures were below 23°C. When temperatures exceeded 23°C, adult Atlantic salmon ceased 

2 
movement through the fishway until high temperatures abated. Salmon mortalities were 

associated with daily average temperatures of26° to 27°C. 

The oxygen requirements of Atlantic salmon are largely dependent upon the activity of the fish 

and water temperature (Decola 1970). For every 1 0°C increase in water temperature, an active 

salmon's oxygen consumption will generally double (Decola 1970). Kazakov and Khalyapina 

( 1981) studied the oxygen consumption rates of 51 adult Atlantic salmon using a respirometer. 

At minimal activity, oxygen consumption rates remained stable when oxygen concentrations 

were depressed to 4.5-5.0 mg/1. At further decreases in oxygen, the fishes breathing function 

became depressed. When oxygen concentrations reached 2.0- 2.5 mg/1, fish became excitable 

and tried to surface. Fish died when oxygen concentrations were reduced to 1.5- 1.7 mg/1. 

Decola (1970) states that sustained DO concentrations of 5 mg/1 or below would be inadequate 

for Atlantic salmon and could block migration. 

Temperature Tolerance (Spawning and Incubation) 

Spawning occurs on the receding arm of the annual temperature cycle and often occurs near the 

upper tolerance limit for successful egg incubation. Temperature governs metabolism which in 

tum increases oxygen consumption (Decola 1970). In contrast, an increase in water temperature 

decreases the amount of oxygen that the water can hold. During the embryonic stage when tissue 

and organs are developing, the demand for oxygen is quite high and, therefore, only a na_rrow 

range of temperatures can be tolerated. As the fish matures and organs develop, the ability to 

tolerate warmer temperatures increases. Decola ( 1970) describes a temperature range between 

0.5° and 7.2°C as a range of temperatures that apparently does not affect egg mortality. whereas 

sac fry and eggs exposed to temperatures at or near I 0°C experience excessive mortality. 

Peterson et a/. ( 1977) studied the effects of eggs and alevins raised under varied temperature 

regimes at different points of development. Eggs incubated at less than 4°C immediately after 

fertilization experienced more than 20% mortality compared to less than 5% mortality when eggs 

were incubated at temperatures greater than 4°C. In contrary, eggs that eyed at 8°C produced 

alevins that were progressively smaller the higher the temperature. Peterson eta!. (1977) 

described the optimum temperature from fertilization to eye pigmentation as near 6°C. 

Temperature Tolerance (smolt emigration) 

The process of smoltification is triggered in response to environmental cues. Photoperiod and 

temperature have the greatest influence on regulating the smolting process. Increase in day 

length is necessary for smolting to occur (Duston and Saunders 1990). McCormick eta!. (1999) 

noted that in spite of wide temperature variations between rivers throughout New England, 

almost all smolt migrations begin around the first of May and are nearly complete by the first 

week in June. However, the time that it takes for the smoltification process to be completed 

appears to be closely related to water temperature; when water temperatures are increased, the 

smolting process is advanced, as evident by increases in Na+, K + ATPase activity (Johnston and 

Saunders 1981; McCormick eta/. 1998; McCormick et al. 2002). Osterdahl (1969) and Solomon 

(1978) reported that downstream smolt migration occurs when temperatures are at or slightly 

above 10°C. Whalen et al. (1999) reported that smolt migration in the West River in Vermont 

began when temperatures exceeded 5°C and peaked when temperatures exceeded 8°C. They also 

reported that wild reared smolts originating from the warmer tributaries of the West River were 

3 
more physiologically advanced and migrations began earlier compared to wild reared smolts 

originating from the colder tributaries. 

In addition to playing a role in regulating the smoltitication process, high temperatures also are 

responsible for the cessation ofNa+,K +-A TPase activity of smolts. McCormick eta/. (1999) 

found significant decreases in Na+,K +-ATPase activity in smolts at the end of the migration 

period, but found that smolts in warmer rivers had reductions in Na+,K +-A TPase activity earlier 

then smolts found in colder rivers. In Catamaran brook in New Brunswick and Conne River in 

Newfoundland where water temperatures remained cold, smolts retained Na+, K +-ATPase 

activity (McCormick eta!. 1999). McCormick eta!. ( 1998) stated that in warmer waters smolts 

will likely experience a narrower physiological smolt window then they otherwise would in cold 

water. 

Flow does not play a role in the smoltification process, though it does appear to play an 

impm1ant role in stimulating a migration response. Whalen et a/. ( 1999) recorded that there was 

no apparent downstream migration following a high tlow event in mid to late April in a Vermont 

river when water temperatures were between 3° and 6°C; however, when water temperatures 

reached 8° to 12°C, small peaks in discharge resulted in corresponding increases in smolt 

migration. 

Temperature Tolerance (adultfeeding at sea) 

The effects of temperature and climate on Atlantic salmon are reviewed by Friedland et al. 

(1993), Hansen and Quinn (1998), Jonsson and Jonsson (2004), Reddin (1988). Reddin and 

Friedland (1993), and Ritter (1989). By comparing sea surface temperature (SST) with 

experimental catch rates, and by attaching temperature monitors to fish, researchers have 

determined that the preferred temperature range for salmon in the spring falls between 7-13°C, 

although most catches occur between 4-8°C (Friedland eta/. 1993; Friedland and Reddin 1993; 

Reddin and Shearer 1987; Reddin 1988; Reddin and Short 1991; Reddin eta/. 1997). The 

movement of salmon into waters around Newfoundland correlates with the presence of a 4°C 

isotherm (Reddin and Friedland 1993). Location of salmon related to these "thermal habitats" 

suggests that salmon can alter their migratory routes depending on SST (Reddin and 

Shearer 198 7; Reddin and Friedland 1993 ). The timing of salmon entrance into coastal waters has 

also been linked with environmental conditions of coastal waters (Reddin and Friedland 1993; 

Reddin et al. 1997). 

Review of Existing Regulations and Policy Related to Water Quality Standards 

You requested technical assistance as to whether the current Maine DEP temperature criteria are 

protective for the listed salmon and its critical habitat. You state that the Maine DEP criteria are 

consistent with EPA's ambient water quality criteria found in EPA's 1986 Gold Book. We are 

not aware of any past ESA Section 7 consultation or current request for such consultation on 

either the Gold Book standards or EPA's approval of the Maine DEP criteria and their effects on 

listed Atlantic salmon and critical habitat. The 1986 Gold Book and EPA's 1990 approval of the 

Maine DEP criteria pre-dated the Atlantic salmon ESA listing and critical habitat designation. 

4 
We do not have enough information on temperature criteria to determine whether these standards 

are adequately protective of Atlantic salmon and their designated critical habitat. In fact, we are 

concerned that they may not be sufficiently protective. We are particularly concerned that the 

five degree (Fahrenheit) limit (Code of Maine Regulation (CMR) 060-096, Chapter 582 Maine 

Department of Environmental Protection (DEP)) may not be sufficiently protective of designated 

critical habitat as a five degree warming (as the state law would currently allow) could increase 

the temperature of nearly every salmon river in the State of Maine above the survival thresholds 

for the freshwater life stages of Atlantic salmon (1 °F is the equivalent of a temperature 

difference 0.556°C). Warming of rivers and streams during the spring and summer could 

increase water temperatures outside of the optimal window for feeding and possibly outside the 

window for survival of fry and parr. Spring and summer warming may also inhibit adult 

migration or result in direct or indirect mortality. Warming of river temperatures in the spring 

would narrow the window of time that would allow successful passage of salmon smolts (the life 

stage where salmon are transitioning from freshwater to saltwater) that can only occur between 5 

and I 0°C. Any warming of river temperatures in the winter would have the effect of advancing 

development of eggs and alevins. If this occurs too quickly, they may use up available energy 

stores in the egg before food in the river is available. This too could have the effect of narrowing 

the window of a key developmental phase. Given the precarious state of salmon populations in 

the GOM DPS, anthropogenic changes in water temperatures that alter temperatures in a way 

that could interfere with Atlantic salmon migratory behaviors or embryonic and juvenile 

development may pose a significant risk to the species. 

The current Code of Maine Regulation (CMR) 060-096, Chapter 582 Maine Department of 

Environmental Protection (DEP) reads: " In no event shall any discharge cause the temperature 

of any freshwater body to exceed 85 degrees Fahrenheit (29°C) at a point outside a mixing zone 

established by the Board, nor shall such discharge cause the temperature of any waters to exceed 

the U.S. Environmental Protection Agency's national ambient water quality criteria established to 

protect all species of fish that are indigenous to the receiving waters at any point outside a 

mixing zone established by the Board." It is not apparent to us what the size of mixing zones 

would be relative to the rest of the waterbody or what the temperatures would be within those 

mixing zones. However, given salmon mortalities are associated with daily average 

temperatures of 26° to 27°C and sub-lethal effects are associated with temperatures lower than 

that, we are concerned that the standards would appear to allow temperatures above 85° F (29°C) 

in a mixing zone, where salmon may be present. 

Maine is near the southern extent of the Atlantic salmon's range in North America. Therefore, 

the GOM DPS is vulnerable to elevated water temperature regimes (Maine T AC 2002). 

Depending upon annual variations in streamflow and ambient air temperatures, it is likely that 

reaches of many rivers experience summer water temperatures outside the preferred range of 

Atlantic salmon. Anthropogenic factors that likely contribute to elevated water temperatures 

include improper or unregulated land use practices, impounded reaches, industrial processing or 

cooling water discharge, low flows that increase net insolation (exposure to sun), and broad 

climatic changes (Maine T AC 2002). 

Based on the available information, there is insufficient information to determine that the State's 

water quality standards are protective of Atlantic salmon in the Gulf of Maine DPS, and we are 

concerned that the State's water quality standards may have an adverse effect on Atlantic salmon 

5 
and their designated Critical Habitat. Critical elements that must be addressed to determine the 

level of effect include, but are not limited to the following: 

• Cumulative effect of multiple discharges, climate change, and other activities that 

warm waters; 

• Long term effect as it relates to climate predictions and annual and inter annual 

climate variability that influence temperature 

• Specific information on mixing zones, their size, or characteristics; 

Conclusion 

You requested technical assistance as to whether the current Maine DEP temperature criteria are 

protective for the listed salmon and its critical habitat. Above, we summarized available 

information regarding temperature and its effects on various life stages of Atlantic salmon. We 

have also appended two tables summarizing temperature studies and Atlantic salmon critical 

habitat features. We conclude that we lack information to determine that Maine's standards are 

protective of Atlantic salmon and its critical habitat, and we are concerned that they may 

adversely affect them. Should you have any questions about these technical assistance comments 

or wish to initiate ESA section 7 consultation, please contact Max Tritt at (207) 866-3756 or by 

email (Max.Tritt@noaa.gov). 

EC: Tritt, NMFS/PRD 

Abele, EPA 

Sincerely, 

O John K. Bullar 

/f(f1 Regional Administrator 

/ 

File Code: H:Section 7 Team\Section 7\Non-Fisheries\EPA\Technical Assistance\2015\ Technical Assistance for Water 

Temperature Tolerances of Atlantic Salmon. 

6 
Table 1. Atlantic salmon temperature (°C) requirements for freshwater life stages. Data are from 

published studies on Atlantic salmon, including experimental data and in situ measurements over 

the range of the species (North America and Europe). 

LIFE STAGE OPTIMUM MINI MAX REFERENCES 

&ACTIVITY RANGE 

SPAWNING 5-8 4.4 10 DeCola '70; Danie eta!. '84; 

McLaughlin and Knight '87. 

INCUBATION 4-7.2 0.5 12 DeCola '70; Gunnes '79; Danie eta!. 

'84; McLaughlin and Knight '87. 

EARLY FRY 8-19 0.5 23.5 Danie eta!. '84; Jensen eta!. '91. 

JUVENILES 

FEEDING 15-19 3.8 22.52 DeCola '70; Elson '75; Danie eta/. 

'84; Elliott '91. 

SURVIVAL 0.5-20 0 29.03 Garside '73; Elliott '91. 

RIVER 

MIGRATION 

SMOLT 7-14.3 5 19 LaBar eta/. '78; Ruggles '80; Jonsson 

and Rudd-Hansen '85; Duston eta/. 

'91; Shepard '91; Elson '69; DeCola 

'70; Danie eta!. '84. 

ADULT 14-20 8 234 Shepard '95. 

Notes. 

I. Minimum water temperatures reflect the requirements of southern populations and include winter 

temperature requirements. Northern populations have lower minima for some life stages (not included). 

2. Highest temperature for feeding after acclimation at 20.0°C. 

3. Highest temperature for I 000 minute survival after acclimation at 25.0-27.0°C. 

4. Highest temperature for normal upstream migration. The lethal temperature for adult salmon is 

approximately 27.0°C, depending upon acclimation and duration of exposure. 

Atlantic Salmon Critical Habitat 

Designation of critical habitat is focused on the known primary constituent elements (PCEs) 

within the occupied areas of a listed species that are deemed essential to the conservation of the 

species. Within the GOM DPS, the PCEs for Atlantic salmon are I) sites for spawning and 

7 
PCE 

rearing, and 2) sites for migration (excluding marine migration). Each PCE is comprised of 

unique biotic and abiotic features deemed essential to the survival, growth, and development to a 

specific Atlantic salmon life stage -including dissolved oxygen (Table 2). 

Table 2. Matrix of Primary Constituent Elements (PCEs) and essential features required by 

Atlantic salmon used for assessing the environmental baseline of the action area. 

Conservation Status Baseline 

Essential Features Fully Functioning Limited Function Not Properly Functioning 

A) Adult Spawning (Oct 1st- Dec 14th): 

Substrate 

Depth 

Velocity 

highly penneable 

course gravel and 

cobble between 1.2 to 

I 0 em in diameter 

17-30 em 

31 to 46 em/sec. 

---------~-- uemperatur ._ ____ _._.~ 7°to 10°C 

pH 

Cover 

Fisheries 

Interactions 

B) Embryo and Fry Development (Oct 1stApr 14th): 

Temperature 

D.O. 

pH 

Depth 

Velocity 

> 5.5 

Abundance of pools 

1.8-3.6 meters deep 

(McLaughlin and 

Knight 1987). Large 

boulders or rocks, over 

hanging trees, logs, 

woody debris, 

submerged vegetation 

or undercut banks 

Abundant diverse 

populations of 

indigenous fish 

species 

O.SOC and 7.2°C, 

averages nearly 6oC 

from fertilization to 

eye pigmentation 

at saturation 

> 6.0 

5.3-15cm 

4 - 15cm/sec. 

8 

40- 60% cobble (22.5-256 more than 20% sand (particle size 

mm dia.) 40-50% gravel 0.06 to 2.2 mm), no gravel or 

(2.2- 22.2 mm dia.); I 0- cobble 

15% course sand (0.5 -2.2 

mm dia.), and <3% fine 

sand (0.06-0.05mm dia.) 

30-76 em < 17 em or> 76 em 

8 to 3 I em/sec. or 46 to 83 

em/sec. 

often oetween 7° to 1 0°C always < 7° or> 10°C 

between 5.0 and 5.5 < 5.0 

Limited availability of Absence of pools 1.8-3.6 meters 

pools 1.8-3.6 meters deep deep (McLaughlin and Knight 

(McLaughlin and Kri.ight 1987). Large boulders or rocks, 

198:7). Large boulders or over hanging trees, logs, woody 

rocks, over hanging trees, debris, submerged vegetation or 

logs, woody debris, undercut banks 

submerged vegetation or 

undercut banks 

Abundant di:verse Limited abundance and diversity 

populations of indigenous of indigenous fish species, 

fish species, low quantities abundant populations of nonof non-native species native species 

present 

averages < 4oC, or 8 to > 10°C from fertilization to eye 

I 0°C from fertilization to pigmentation 

eye pigmentation 

7-8 mg/L <7 mg!L 

6-4.5 <4.5 

NA <5.3 or>15cm 

NA <4 or> 15cm/sec. 
Fisheries 

Interactions 

Abundant diverse 

populations of 

indigenous fish 

species 

Abundant diverse 

populations of .indigenous 

fish species, low quantities 

of non-native species 

present 

Conservation Status Baseline 

Essential Features Fully Functioning 

C) Parr Development: (All year) 

Substrate 

Depth 

Velocity 

Temperature 

D.O. 

Food 

Passage 

Fisheries 

Interactions 

gravel between 1.6 

and 6.4 em in diameter 

and boulders between 

30 and 51.2 em in 

diameter. May contain 

rooted aquatic 

macrophytes 

l'Ocmto 30cm 

7 to 20 em/sec. 

> 6 mg/1 

Abundance of larvae 

of mayflies, stone flies, 

chironomids, 

caddisflies, blackflies, 

aquatic annelids, and 

mollusks as well as 

numerous terrestrial 

invertebrates and 

small fish such as 

alewives, dace or 

minno~ 

No anthropogenic 

causes that inhibit or 

delay movement 

Abundant diverse 

populations of 

indigenous fish 

species 

9 

Limited Function 

gravel < 1.2cm and/or 

boulders > 51.2. May 

contain rooted aquatic 

macrophytes 

NA 

< 7cm/sec. or> 20 em/sec. 

generally between 7-

22.5oC, but does not 

exceed 29oC at any time 

2.9-6 mg/1 

Presence of larvae of 

mayflies, stonetlies, 

chironomids, caddisflies, 

blackflies, ~uatic 

annelids, and mollusks as 

well as numerous telil'estri~l 

invertebrates and small fish 

such as alewives, dace or 

minnows 

Presence of anthropogenic 

causes that result in limited 

inhibition of movement 

Abundant diverse 

populations of indigenous 

fish species, low quantities 

of non-native species 

present 

Limited abundance and diversity 

of indigenous fish species, 

abundantpopulationsofnonnative species 

Not Properly Functioning 

no gravel, boulders, or rooted 

aquatic macrophytes present 

<1 Ocm or >30cm 

velocity exceeds 120 em/sec .. 

stream temperatures are 

continuously <7oC or known to 

exceed 29oC 

< 2.9 mg/1 

Absence of larvae of mayflies, 

stoneflies, chironomids, 

caddistlies, blackflies, aquatic 

annelids, and mollusks as well as 

numerous terrestrial invertebrates 

and small fish such as alewives, 

dace or minnows 

barriers to migration known to 

cause direct inhibition of 

movement 

Limited abundance and diversity 

of indigenous fish species, 

abundabt populations of nonnative species 
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II 
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