### Ralph Abele Chief, Water Quality Branch EPA Region 1 5 Post Office Square #

### 100 Boston, MA 02109 UNITED STATES DEPARTMENT OF COMMERCE National Oceanic and AtmosphericAdministration 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 WaterTemperatureTolerances ofAtlantic Salmon Dear Mr. Abele: This is inresponse to your letterreceived May 7, 2015 requesting only technical assistance on the existingtemperature criteriafound in the Maine Water Quality Standards and whether or not these currenttemperature criteria are protective ofthe listed Atlantic salmon (Salmo salar) 

### and its designated critical habitat. 

### NMFS Listed Species undertheEndangered Species Act and Designated Critical Habitat The GulfofMaine DistinctPopulation Segment (GOM DPS) ofAtlantic salmon (Salmo salar) 

### is listed as endangered underthe Endangered Species Act (ESA). The GOM DPS includes all anadromous Atlantic salmon whose freshwater range occurs in the watersheds from the Androscoggin River northward alongthe Maine coastto the Dennys River

. Included are all associated conservation hatchery populations used to supplementthese natural populations; currently, such conservation hatchery populations are maintained at Green Lake National Fish Hatchery (GLNFH) and Craig BrookNational Fish Hatchery (CBNFH). Critical habitat has been designated for listed Atlantic salmonpursuant to section 4(a)(3) ofthe 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 oflake habitat within the range ofthe GOM DPS. These areas includethose physical and biological features essential to the conservation ofthe species

.The entire occupied range ofthe GOM DPS in which critical habitat is designated is withinthe State ofMaine. 

### ThermalTolerance for Atlantic Salmon Survival, Growth, and Development The following information on water temperature tolerances ofAtlantic salmon is excerpted from the "Habitatrequirements and management considerations for Atlantic salmon (Salmo salar) 

### in the GulfofMaine Distinct Population Segment (GOM DPS)" (Kircheis and Liebich 2007) and from the final rule designating critical habitat for the GOM DPS published in the FederalRegister (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 parrand large parrhave similartemperature tolerances (Elliott 1991). Watertemperature influences growth, survival and behaviorof juvenile Atlantic salmon. Juvenile salmon canbe exposed to very warm temperatures (> 20°C) in the summerand near freezing temperatures in the winter, and have evolved with a series ofphysiological and behavioral strategies that enable them to adapt to the wide range ofthermal 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 watertemperatures surpass 19°C, feeding and behavioral activities are directed towards maintenance and survival. Duringthe winterwhen temperatures approach freezing, parrreduce energy expenditures by spending less time defending territories, feeding less, and moving into slower velocity microhabitats (Cunjak 1996). Though parr are capable ofadapting to a broad range oftemperatures, they do have an upper and lowertemperature threshold for survival. A study conducted in Big Brook, TerraNovaNational Park, Newfoundland, progressively acclimated parrto 27.5°C in freshwater. The upper lethal temperature was determinedby 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 higherupper lethal limits during shorter exposure times. Fry (1947) indicated graphically that Atlantic salmon acclimatedto 25°C possessed an upper lethal temperature of about 28.5°C. This level was determined from shortertests which produced medianresistance intervals ofless than 1,000 minutes. Itwas assumed that it would not be possibleto obtain less than 100% mortality in the testing range of28-30°C for exposures of 10,000 minutes (Garside 1973). A study conducted by Elliott (1991) soughtto construct a thermal tolerance polygon forjuvenile 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 subjectedto 1°C positive ornegative temperature increases to determine upper and lower limits for feeding and survival overperiods of 10 minutes, 100 minutes, 1,000 minutes, and 7 days. Elliott (1991) identified a mean upper incipient temperature tolerance of22.5°C and a mean lower incipient temperature tolerance of7.0°C by the cessation offeeding activity, which is a thermal stress response that influences both growth and survival ofthe fish. Thermal Tolerance (AdultMigration) 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 caughtby 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 inthe Penobscot Riverfrom 1988 through 1992 and found that salmon continued to pass throughthe fishway at Veazie Dam in the lowerPenobscot Riverwhen temperatures were below 23°C. Whentemperatures exceeded 23°C, adult Atlantic salmon ceased

2movement through the fishway until high temperatures abated. Salmon mortalities were associated with daily average temperatures of26°to 27°C. The oxygen requirements ofAtlantic salmon are largely dependent upon the activity ofthe fish and watertemperature (Decola 1970). For every 1 0°C increase in watertemperature, an active salmon's oxygen consumption will generally double (Decola 1970). Kazakov and Khalyapina (1981) studied the oxygen consumption rates of51 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 of5 mg/1 orbelow would be inadequate for Atlantic salmon and could block migration. 

### Temperature Tolerance (SpawningandIncubation) Spawning occurs on the receding arm ofthe 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 watertemperature decreases the amount ofoxygen thatthe 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 oftemperatures 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 oftemperatures that apparently does not affect egg mortality. whereas sac fry and eggs exposed to temperatures at ornear I0°C experience excessive mortality. Peterson 

### et a/. (1977) studied the effects ofeggs and alevins raised under varied temperature regimes atdifferent points ofdevelopment. 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 greaterthan 4°C. In contrary, eggs that eyed at 8°C produced alevins that were progressively smallerthe higherthe temperature. Peterson 

### eta!. (1977) described the optimum temperature from fertilization to eye pigmentation as near 6°C. 

### Temperature Tolerance (smolt emigration) The process ofsmoltification 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 ofwide temperature variations between rivers throughout New England, almost all smolt migrations begin around the first ofMay 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 closelyrelated 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 

### etal

. 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 peakedwhen temperatures exceeded 8°C. They also reported that wild reared smolts originating from the warmertributaries ofthe West River were

3more physiologically advanced and migrations began earliercompared 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+-ATPase activity ofsmolts. McCormick 

### eta/. (1999) found significant decreases in Na+,K+-ATPase activity in smolts at the end ofthe migration period, but found that smolts in warmer rivers had reductions in Na+,K+-ATPase activity earlier then smolts found in colder rivers. In Catamaran brook in New Brunswick and Conne River in Newfoundland where watertemperatures remained cold, smolts retained Na+, K+-ATPase activity (McCormick 

### eta!. 1999). McCormick 

### eta!. (1998) stated that in warmer waters smolts will likely experience a narrowerphysiological 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 atsea) The effects oftemperature 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 attachingtemperature 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 ofsalmon into waters around Newfoundland correlates with the presence ofa 4°C isotherm (Reddin and Friedland 1993). Location ofsalmon related to these "thermal habitats" suggests that salmon can alter their migratory routes depending on SST (Reddin and Shearer1987; Reddin and Friedland 1993). The timing ofsalmon entrance into coastal waters has also been linked with environmental conditions ofcoastal waters (Reddin and Friedland 1993; Reddin 

### et al. 1997). Review ofExisting Regulations and Policy Related to Water Quality Standards You requested technical assistance as to whetherthe 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 ofany past ESA Section 7 consultation or current request for such consultation on eitherthe Gold Book standards orEPA's approval ofthe Maine DEP criteria and their effects on listed Atlantic salmon and critical habitat. The 1986 Gold Book and EPA's 1990 approval ofthe Maine DEP criteria pre-dated the Atlantic salmon ESA listing and critical habitat designation.

4

### We do nothave enough information on temperature criteriato determine whether these standards are adequately protective ofAtlantic 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 ofMaine Regulation (CMR) 060-096, Chapter 582 Maine Department ofEnvironmental Protection (DEP)) may not be sufficiently protective ofdesignated critical habitat as a five degree warming (as the state law would currently allow) could increase the temperature ofnearly every salmon river in the State ofMaine above the survival thresholds for the freshwater life stages ofAtlantic salmon (1 °F is the equivalent ofatemperature difference 0.556°C). Warming ofrivers and streams during the spring and summer could increase watertemperatures outside ofthe optimal window for feeding and possibly outside the window for survival offry and parr. Spring and summer warming may also inhibit adult migration orresult in direct or indirect mortality

. Warming ofriver temperatures in the spring would narrow the window oftime that would allow successful passage ofsalmon smolts (the life stage where salmon are transitioning from freshwater to saltwater) that can only occurbetween 5 and I0°C. Any warming ofriver temperatures in the winter would have the effect ofadvancing development ofeggs and alevins. Ifthis 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 ofnarrowing the window ofa key developmental phase. Given the precarious state ofsalmon populations in the GOM DPS, anthropogenic changes in watertemperatures that alter temperatures in a way that could interfere with Atlantic salmon migratory behaviors or embryonic andjuvenile development may pose a significant risk to the species. The current Code ofMaine Regulation (CMR) 060-096, Chapter 582 Maine Department of Environmental Protection (DEP) reads: " In no event shall any discharge cause the temperature ofany 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 ofany waters to exceed the U.S. Environmental Protection Agency's national ambient water quality criteria established to protect all species offish that are indigenous to the receiving waters at any point outside a mixing zone established by the Board." Itis not apparent to us what the size ofmixing zones would be relative to the rest ofthe waterbody or what the temperatures would be within those mixing zones. However, given salmon mortalities are associated with daily average temperatures of26° 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 ofthe Atlantic salmon's range in North America. Therefore, the GOM DPS is vulnerable to elevated water temperature regimes (Maine TAC 2002). Depending upon annual variations in streamflow and ambient air temperatures, it is likely that reaches ofmany rivers experience summer water temperatures outside the preferred range of Atlantic salmon. Anthropogenic factors that likely contribute to elevated watertemperatures 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 TAC 2002). Based on the available information, there is insufficient information to determine that the State's water quality standards are protective ofAtlantic salmon in the GulfofMaine 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 ofeffect include, but are not limited to the following:

• Cumulative effect ofmultiple 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 whetherthe 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 ofAtlantic 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 ofAtlantic salmon and its critical habitat, and we are concerned that they may adversely affect them. Should you have any questions aboutthese 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 7Team\Section 7\ Non-Fisheries\EPA\Technical Assistance\2015\ Technical Assistance for Water Temperature Tolerances ofAtlantic 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 ofthe 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.
EARLYFRY 

### 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 watertemperatures reflect the requirements ofsouthern populations and include winter temperature requirements. Northern populations have lower minima for some life stages (not included). 2. Highesttemperature for feeding after acclimation at 20.0°C

. 3. Highesttemperature for I000 minute survival after acclimation at 25.0-27

.0°C. 4. Highesttemperature for normal upstream migration. The lethal temperature for adult salmon is approximately 27

.0°C, depending upon acclimation and duration ofexposure. 

### Atlantic Salmon Critical Habitat Designation ofcritical habitat is focused on the known primary constituent elements (PCEs) within the occupied areas ofa listed species that are deemed essential to the conservation ofthe species. Within the GOM DPS, the PCEs for Atlantic salmon are I) sites for spawning and

7PCE 

### 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 -includingdissolved oxygen (Table 2)

. Table2. Matrix ofPrimary Constituent Elements (PCEs) and essential features required by Atlantic salmon used for assessing the environmental baseline ofthe action area. Conservation StatusBaseline Essential Features Fully Functioning Limited Function Not Properly Functioning
A) AdultSpawning (Oct 1st-Dec 14th): Substrate

Depth Velocity highly penneable course gravel and cobble between 1.2 to I0 em in diameter

17-30 em 31 to 46 em/sec

. 7°to 10°C**---------~-- uempera** **tur ._** ____**_._.~** pH Cover

Fisheries Interactions

B) Embryo andFryDevelopment (Oct 1stApr 14th): Temperature



### D.O. pH Depth Velocity > 5.5 Abundance ofpools 1.8-3.6metersdeep (McLaughlinand Knight 1987). Large boulders orrocks, over hangingtrees, logs, woody debris, submergedvegetation orundercut banks Abundant diverse populations of indigenous fish species

O.SOC and 7.2°C, averages nearly 6oC from fertilization to eye pigmentation atsaturation > 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.); I0- cobble 15% course sand (0.5 -2

.2 mm dia

.), and <3% fine sand (0

.06

-0.05mm dia

.)
30-76em < 17 em or> 76 em 8 to 3 Iem/sec. or46 to 83 em/sec. often oetween 7° to 1 0°C always < 7° or> 10°C between 5.0 and 5.5 < 5

.0 Limitedavailability of Absence of pools 1.8-3.6meters pools 1.8-3.6meters deep deep (McLaughlin andKnight (McLaughlin andKri.ight 1987). Large boulders orrocks, 198:7). Largeboulders or overhangingtrees, logs, woody rocks, overhangingtrees, debris, submergedvegetation or logs, woody debris, undercutbanks submergedvegetation or undercutbanks
Abundant di:verse Limited abundance and diversity populations ofindigenous ofindigenous fish species, fish species, low quantities abundant populations ofnonofnon-native species native species present

averages < 4oC, or 8 to > 10°C from fertilization to eye I0°C from fertilization to pigmentation eye pigmentation
7-8 mg/L <7mg!L 6-4.5 <4.5 NA <5

.3 or>15cm NA <4 or> 15cm/sec.Fisheries Interactions Abundantdiverse populations of indigenous fish species Abundantdiverse populations of.indigenous fish species, low quantities ofnon-native species present
Conservation Status Baseline Essential Features Fully Functioning C)ParrDevelopment: (Allyear) 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 7to 20 em/sec.

> 6 mg/1 Abundance oflarvae ofmayflies, stoneflies, chironomids, caddisflies, blackflies, aquatic annelids, and mollusks as well as numerous terrestrial invertebrates and smallfish such as alewives, dace or**minno~** No anthropogenic causes that inhibit or delay movement Abundantdiverse 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 exceed29oC at any time 2.9-6 mg/1 Presence oflarvae of mayflies, stonetlies, chironomids, caddisflies, blackflies,**~uatic** annelids, andmollusks as well as numerous**telil'estri~l** invertebrates and small fish such as alewives, dace or minnows

Presence ofanthropogenic causes that result in limited inhibition ofmovement Abundantdiverse populations ofindigenous fish species, low quantities ofnon-native species present Limited abundance and diversity ofindigenous fish species,abundantpopulationsofnonnative species

Not Properly Functioning

no gravel, boulders, orrooted aquatic macrophytes present

<1Ocm or>30cm velocity exceeds 120 em/sec

.. stream temperatures are continuously <7oC orknown to exceed 29oC
<2.9 mg/1 Absence oflarvae ofmayflies, stoneflies, chironomids, caddistlies, blackflies, aquatic annelids, andmollusks as well as numerous terrestrial invertebrates and small fish such as alewives, dace orminnows

barriers to migration known to cause direct inhibition of movement Limited abundance anddiversity ofindigenous fish species, abundabtpopulations ofnonnative speciesReferences Cited Armstrong, J.D., Kemp, P. S., Kennedy, G. J. A., Ladle, M., & Milner, N.J. 2003. Habitat requirements ofAtlantic salmon and brown trout in rivers and streams. Fisheries research, 62(2), 143-170. Bachman, R. A. 1984. Foraging behaviouroffree-ranging wild and hatchery brown trout in a stream Trans. Am. Fish. Soc., 113 (1984), pp. 1-32. Baum, E. T. 1997. Maine Atlantic Salmon: A National Treasure. Atlantic Salmon Unlimited. Hermon, ME. 224 pp. Bjornn, T., and Reiser, D. W. 1991. Habitat requirements ofsalmonids in streams. American Fisheries Society Special Publication, 19, 83-138. Cunjak, R. A. 1996. Winter habitat ofselected stream fishes and potential impacts from land use . activity. Canadian Journal ofFisheries and Aquatic Sciences, 53:267-282. Cunjak, R. A., Chadwick, E. M.P., and M. Shears. 1989. Downstream Movements and Estuarine Residence by Atlantic SalmonParr 

### (Salmo salar). CanadianJournal ofFisheries and Aquatic Sciences, 46(9), 1466-1471. Danie, D. S., J. G. Trial, and J. G. Stanley. 1984. Species profiles: life histories and environmental requirements ofcoastal fish and invertebrates (North Atlantic): Atlantic salmon. FWS/OBS-82/11.2, TREL-82-4. U.S. Fish and Wildlife Service and U.S. Army Corps of Engineers. 19 pp. DeCola, J. N. 1970. Waterquality requirements. U.S. Department ofthe Interior, Federal Water Quality Administration. Needham Heights, MA. 42 pp. Doudoroff, P., and Warren, C. E. 1965. Dissolved oxygenrequirements offishes. Duston, J., R. 

### L. Saunders, and D. E. Knox. 1991. Effects ofincreases in freshwater temperature on loss ofsmolt characteristics in Atlantic salmon 

### (Salmo salar). Canadian Journal ofFisheries and Aquatic Sciences 48(2): 164-169. Elliott, J. M. 1991. Tolerance and resistance to thermal stress injuvenile Atlantic salmon, 

### Salmo salar. Freshwater Biology 25(1): 61-70. Elson, P. F. 1969. High temperature and river ascent by Atlantic salmon. 1969/M:12. ICES (International Council for the Exploration ofthe Sea) C.M. Charlottenlund, Denmark. 12 pp.

10Elson, P. F. 1975. Atlantic salmon rivers, smolt production and optimal spawnings: an overview ofnatural productions. In NewEngland Atlantic salmon restoration conference 1975. J.R. Bohhe and L. Sochasky, eds. International Atlantic Salmon Foundation Special Publication Series 6: 96- 119. Fay, C., M. Bartron, S. Craig, A. Hecht, J. Pruden, R. Saunders, T. Sheehan, and J. Trial. 2006. Status Review for Anadromous Atlantic Salmon (Salmo salar) in the United States. Report to the National Marine Fisheries Service and U.S. Fish and Wildlife Service. 294 pages Fried, S.M., McCleave, J.D., & LaBar, G. W. 1978. Seaward migration ofhatchery-reared Atlantic salmon, Salmo salar, smolts in the Penobscot River estuary, Maine: riverine movements. Journal ofthe Fisheries Board ofCanada, 35(1), 76-87. Friedland, K.D., and Reddin, D.O. 1993. Marine survival ofAtlantic salmon from indices of post-smoltgrowth and seatemperature. In: Salmon in the sea and new enhancement strategies. Edited by D. Mills. FishingNews Books, Blackwell Scientific Publications Ltd. pp. 119-138 Friedland, K.D., D.O. Reddin, and J.F. Kocik. 1993. Marine Survival ofN. American and European Atlantic salmon: effects ofgrowth and environment. ICES J. ofMarine Sci. 50: 481- 492 Fry, F.E.J. 1947. Effects ofthe environment on animal activity. Univ. Toronto Studies Bioi. Ser. No. 55. Pub!. Ontario Fish. Res. Lab. 68. 62pp. Garside, E. T. 1973. Ultimate upper lethal temperature ofAtlantic salmonSa/mo salar L.Canadian Journal ofZoology 51 (8): 898-900. Giger, R. D. 1973. Streamflowrequirements ofsalmonids. Grant, J. W., Steingrimsson, S. 

## 6., Keeley, E. R., & Cunjak, R. A. 1998. Implications of territory size for the measurement and prediction ofsalmonid abundance in streams. Canadian Journal ofFisheries and Aquatic Sciences, 55(S1), 181-190. Gunnes, K. 1979. Survival and development ofAtlantic salmon eggs and fry at three different temperatures. Aquaculture 16(3): 211-218. Hansen, L. P., and B. Jonsson. 1989. Salmon ranching experiments in the River Imsa: effect of timing ofAtlantic salmon (Sa/mo salar) smolt migration on survival to adults. Aquaculture, 82(1), 367-373. Hansen, L. P., & Quinn, T. P. 1998. The marine phase ofthe Atlantic salmon (Salmo salar) life cycle, with comparisons to Pacific salmon. Canadian Journal ofFisheries and Aquatic Sciences, 55(S1 ), 104-118. Heggenes, J., Bagliniere, J. L., & Cunjak, R. A. 1999. Spatial niche variability for young Atlantic salmon (Salmo sa/ar) and brown trout (S. trutta) in heterogeneous streams. Ecology of FreshwaterFish, 8(1), 1-21.

IIHolm, M., Huse, 

### 1.,**De~ving,** K. B., and J. Aure. 1982. Behaviour ofAtlantic salmon smolts during seaward migration Int. Counc. Explor. Sea, C.M. 1988/M: 7. Hyvarinen, P., Suuronen, P., and T. Laaksonen. 2006. Short-term movements ofwild and reared Atlantic salmon smolts in a brackish water estuary-preliminary study. Fish. Man. Ecol. 13:399- 401. Jensen, A. J., B. 

### 0. Johnsen, and T. G. Heggberget. 1991. Initial feeding time ofAtlantic salmon, 

### Salmo salar, alevins compared to riverflow and watertemperature inNorwegian streams. Environmental Biology ofFishes 30(4): 379-385 Johnston, C. E., and R. L. Saunders. 1981. Parr-smolttransformation ofyearling Atlantic salmon 

### (Salmo salar) at several rearing temperatures. CanadianJournal ofFisheries and Aquatic Sciences, 38(10), 1189-1198 Jonsson, B. and J. Ruud-Hansen. 1985. Watertemperature as the primary influence on timing of seaward migrations ofAtlantic salmon 

### (Salmo salar) smolts. Canadian Journal ofFisheries and Aquatic Sciences 42(3): 593-595. Jonsson, Bror, and NinaJonsson. 2004. "Factors affecting marine production ofAtlantic salmon (Salmo salar)." Canadian Journal ofFisheries and Aquatic Sciences 61.12: 2369-2383. Jordan, R. M., and K. F. Beland. 1981. Atlantic salmon spawning and evaluation ofnatural spawning success. Atlantic SeaRun Salmon Commission. Augusta, ME Kalleberg, H. 1958. Observations in a stream tank ofterritoriality and competition injuvenile salmon and trout 

### (Salmo salar L. and

### S. trutta L.). Institute ofFreshwaterResearch Drottningholm Report, 39, 55-98. Kazakov, R.V., and Khalyapina, L.M. 1981. Oxygen consumption ofadult Atlantic salmon 

### (Salmo salar L.) males and females in fish culture. Aquaculture 25: 289-292. Kircheis, D. and T. Liebich. 2007. Habitat requirements and management considerations for Atlantic salmon 

### (Salmo salar) in the GulfofMaine Distinct Population Segment (GOM DPS). Greater Atlantic Regional Fisheries Office, Gloucester, MA. 01930. LaBar, G. W., J.D. McCleave, and S.M. Fried. 1978. Seaward migration ofhatcheryreared Atlantic salmon 

### (Salmo salar) smolts in the Penobscot Riverestuary, Maine: open-water movements. Journal du Conseil. International Council for the Exploration ofthe Sea 38(2): 257- 269. Lacroix, G. L., & McCurdy, P. 1996. Migratory behaviourofpost-smoltAtlantic salmon during initial stages ofseaward migration. Journal ofFish Biology, 49(6), 1086-1101.

12Lacroix, G. 

### L., Knox, D., and P. McCurdy. 2004. Effects ofimplanted dummy acoustic transmitters onjuvenile Atlantic salmon. Transactions oftheAmerican Fisheries Society, 133(1), 211-220. Larsson, P. 0. 1977. The importance oftime and place ofrelease ofsalmon and seatrout on the results ofstocking. ICES CM 1977/M: 42, 4. McCleave, J.D. 1978. Rhythmic aspects ofestuarine migration ofhatchery-reared Atlantic salmon 

### (Salmo salar) smolts. Journal ofFish Biology, 12(6), 559-570. McCormick, S.D., Hansen, 

### L. P., Quinn, T. P., & Saunders, R. 

### L. 1998. Movement, migration, and smolting ofAtlantic salmon 

### (Salmo salar). Canadian Journal ofFisheries and Aquatic Sciences, 55(S1), 77-92. McCormick, S. D., Cunjak, R. A., Dempson, 

### B., O'Dea, M. F., 

### & Carey, J. 

### B. 1999. Temperature-related loss ofsmolt characteristics in Atlantic salmon 

### (Salmo salar) in the wild

. Canadian Journal ofFisheries and Aquatic Sciences, 56(9), 1649-1667. McCormick, S. D., Shrimpton, J. M., Moriyama, S., and B. T. Bjornsson. 2002. Effects ofan advanced temperature cycle on smolt development and endocrinology indicate that temperature is not a zeitgeber for smolting in Atlantic salmon. Journal ofExperimental Biology, 205(22), 3553-3560. McLaughlin, E., and A. Knight. 1987. Habitat criteria for Atlantic salmon. Special Report, US Fish and Wildlife Service, Laconia, New Hampshire. Moore, A., Potter, E. C. E., Milner, N.J., and S. Bamber. 1995. The migratory behaviour of wild Atlantic salmon 

### (Salmo salar) smolts in the estuary ofthe River Conwy, North Wales. Can

. J. Fish. Aquat. Sci. 52: 1923 -1935. Osterdahl, 

### L. 1969. The smoltrun ofa small Swedish river. In: Symposium ofsalmon and trout in streams. Ed. T.G. Northcote. University ofBritish Columbia, Vancouver, British Columbia, Canada. Peterson, R. H. 1978. Physical characteristics ofAtlantic salmon spawning gravel in someNew Brunswick streams. Fisheries and Environmental Sciences, Fisheries and Oceans Canada, Biological Station St. Andrews, NewBrunswick. Reddin, D. G. and W.M. Shearer. 1987. Sea-surface temperature and distribution ofAtlantic salmon in the Northwest Atlantic Ocean. American Fisheries Society Symposium. Reddin, D.G and K.D. Friedland. 1993. Marine environmental factors influencing the movement and survival ofAtlantic salmon. pages 70-103. In: Mills, E.D. 1993

. Salmon in the sea. Fishing News Books, Blackwell Scientific, Cambridge, MA.

13

### Reddin, D.G and P.B. Short. 1991. Postsmolt Atlantic salmon (Salmo salar) 

### in the Labrador Sea. Can. J. Fish Aquat. Sci. 48: 2-6. Reddin, D.G. 1988. Ocean life ofAtlantic salmon (Salmo salar L.) 

### in the Northwest Atlantic. p. 483-511. In: D. Mills and D. Piggins [eds.] Atlantic Salmon: Planning for the Future. Proceedings ofthe 3rd International Atlantic Salmon symposium. Reddin, D.G., 

### J. Helbig, A. Thomas, B.G. Whitehouse and K.D. Friedland. 1997. Survival of Atlantic salmon (Salmo salar L.) 

### related to marine climate. In: Wild Atlantic Salmon: New Challenges- New Techniques. Proceedings ofthe Fifth Int. Atlantic Salmon Symposium, Galway, Ireland. Ruggles, C. P. 1980. A review ofthe downstream migration ofAtlantic salmon. Canadian Technical Report ofFisheries and Aquatic Sciences No. 952. Freshwater and Anadromous Division Research Branch, Department ofFisheries and Oceans. Halifax, NS. 39 pp. Saunders, R., Hachey, M.A., & 

### Fay, C. W

. 2006. Maine's diadromous fish community: past, present, and implications for Atlantic salmon recovery. Fisheries, 31(11), 537-547. Shepard, S. L. 

### 1991. Report on Radio Telemetry Investigations ofAtlantic Salmon Smolt Migration in the Penobscot River. Bangor Hydro-Electric Company. 38 pp. and appendices. Shepard, S. L. 

### 1995. Atlantic Salmon Spawning Migrations in the Penobscot River, Maine: Fishways, Flows and High Temperatures. M.S. Thesis. University ofMaine. Orono, ME. 112 pp. Solomon, D.J. 1978. Migration ofsmolts ofAtlantic salmon (Salmo salar L.) 

### and sea trout (Salmo trutta L.) 

### in a chalkstream. Environmental Biology ofFishes. 3(2): 223-229. Symons, P. E. K., and M. Heland. 1978. Stream habitats and behavioral interactions ofunder yearling and yearling Atlantic salmon (Salmo salar). 

### Journal ofthe Fisheries Board ofCanada, 35(2), 175-183. Thorpe, J. E., and R.I. G Morgan. 1978. Periodicity in Atlantic salmon Salmo salar L. 

### smolt migration. Journal ofFish Biology, 12(6), 541-548. Whalen, K. G., D. L. 

### Parish, and M. E. Mather. 1999. Effect ofice formation on selection habitats and winter distribution ofpost-young-of-the-year Atlantic salmon parr. Can. J. Fish. Aquat. Sci. 56(1): 87-96. Wickett, W. P. 1954. The oxygen supply to salmon eggs in spawning beds. Journal ofthe Fisheries Board ofCanada, 11(6), 933-953.

14