NOAA Technical Memorandum NMFS-NWFSC-49

The Net-pen Salmon

Farming Industry

in the Pacific Northwest 

September 2001

U.S. DEPARTMENT OF COMMERCE

National Oceanic and Atmospheric Administration

National Marine Fisheries Service
NOAA Technical Memorandum

 NMFS Series

The Northwest Fisheries Science Center of the National Marine Fisheries Service, NOAA, uses the

NOAA Technical Memorandum NMFS series to issue

informal scientific and technical publications when

complete formal review and editorial processing are

not appropriate or feasible due to time constraints.

Documents published in this series may be referenced

in the scientific and technical literature.

The NMFS-NWFSC Technical Memorandum series of

the Northwest Fisheries Science Center continues the

NMFS-F/NWC series established in 1970 by the

Northwest & Alaska Fisheries Science Center, which

has since been split into the Northwest Fisheries

Science Center and the Alaska Fisheries Science

Center. The NMFS-AFSC Technical Memorandum

series is now being used by the Alaska Fisheries

Science Center.

Reference throughout this document to trade names

does not imply endorsement by the National Marine

Fisheries Service, NOAA.

This document should be cited as follows:

Nash, C.E. (editor). 2001. The net-pen salmon farming

Industry in the Pacific Northwest. U.S. Dept. Commer.,

NOAA Tech. Memo. NMFS-NWFSC-49, 125 p.
NOAA Technical Memorandum NMFS-NWFSC-49

The Net-pen Salmon

Farming Industry

in the Pacific Northwest

Edited by Colin Nash

From contributions by

Kenneth M. Brooks (consultant)*,

William T. Fairgrieve, Robert N. Iwamoto,

Conrad V.W. Mahnken, Colin E. Nash,

Michael B. Rust, Mark S. Strom, and

F. William Waknitz

Northwest Fisheries Science Center

Resource Enhancement and Utilization Technologies Division

2725 Montlake Boulevard East

Seattle, Washington 98112

*Aquatic Environmental Sciences

644 Old Eaglemount Road

Port Townsend, Washington 98368

September 2001

U.S. DEPARTMENT OF COMMERCE

Donald L. Evans, Secretary

National Oceanic and Atmospheric Administration

Scott B. Gudes, Acting Administrator

National Marine Fisheries Service

William T. Hogarth, Acting Assistant Administrator for Fisheries
ii

Most NOAA Technical Memorandums NMFS-NWFSC are

available on-line at the Northwest Fisheries Science Center

web site (http://www.nwfsc.noaa.gov)

Copies are also available from:

National Technical Information Service

5285 Port Royal Road

Springfield, VA 22161

phone orders (1-800-553-6847)

e-mail orders (orders@ntis.fedworld.gov)
iii

Acknowledgements

Thirty-five copies of this document in draft were circulated globally in April and May,

2001 for review and comment. The authors acknowledge the added contributions of the

following individuals:

Hans Ackefors (University of Stockholm, Sweden)

Kevin H. Amos (Washington Department of Fish and Wildlife)

Andrew Appleby (Washington Department of Fish and Wildlife)

Faye M. Dong (University of Washington, Seattle, Washington)

John Forster (Forster Consulting Inc., Port Angeles, Washington)

Peter Granger (Washington Fish Growers Association, Bellingham, Washington)

James P. McVey (National Sea Grant Program, NOAA, Washington D.C.)

John E. Rensel (Rensel Associates Aquatic Science Consultants, Arlington, Washington)

Andrew J.L. Thomson (Fisheries and Oceans, Nanaimo, B.C. Canada)
iv
v

Acronyms of Organizations and Common Terms

ACE US Army Corps of Engineers

ADF&G Alaska Department of Fish and Game

ALL Aquatic Lands Lease

APHA American Public Health Association

BC British Columbia (Canada)

BCSAR British Columbia Salmon Aquaculture Review

BCSGA British Columbia Salmon Growers Association (Canada)

BMP Best Management Practice

CFOI Census of Fatal Occupational Injuries

CFR Code of Federal Regulations (Food and Drug Administration)

COP Code of Practice

DOC United States Department of Commerce

DOI United States Department of the Interior

DFO Department of Fisheries and Oceans (Canada)

EAO Environmental Assessment Office (Canada BC)

EEZ Extended Economic Zone

EPA United States Environmental Protection Agency

ESA Endangered Species Act 1974

ESU Evolutionarily Significant Unit

EU European Union

FAO Food and Agriculture Organization (United Nations)

FDA United States Food and Drug Administration

FPC Fish Passage Control (Oregon)

HACCP Hazard Analysis Critical Control Point

HGMP Hatchery and Genetic Management Plan

HIE Highlands and Islands Enterprises (Scotland)

HPA Hydraulic Project Approval

GDP Gross Domestic Product

GDU Genetic Diversity Unit

GESAMP Joint Group of Experts on Scientific Aspects of Marine

Environmental Protection (United Nations)

GLP Good Laboratory Practice

GM Genetically Modified

GMO Genetically Modified Organism

ICOR Interagency Committee for Outdoor Recreation (Washington State)

INAD Investigational New Animal Drug

JSA Joint Sub-Committee on Aquaculture

MLLW Mean Low Low Water

NADP National Aquaculture Development Plan

NBSGA New Brunswick Salmon Growers Association (Canada)

NMFS National Marine Fisheries Service (NOAA)

NOAA National Oceanographic and Atmospheric Administration

NPAFC North Pacific Anadromous Fish Commission
vi

NPDES National Pollution Discharge Elimination System Permit

NRC Natural Resources Consultants

NSGCP National Sea Grant College Program (NOAA)

NSSP National Shellfish Sanitation Program

NWFSC Northwest Fisheries Science Center

NWIFC Northwest Indian Fisheries Commission

OAR Office of Oceanic and Atmospheric Research (NOAA)

ODFW Oregon Department of Fish and Wildlife

ODIN Official Documentation and Information from Norway

OSU Oregon State University

PCHB Pollution Control Hearings Board (Washington State)

PNP Private Non-Profit (Aquaculture Organizations, Alaska)

PNWFHPC Pacific Northwest Fish Health Protection Committee

PSMFC Pacific States Marine Fisheries Commission

PSEP Puget Sound Estuary Protocols

PSGA Puget Sound Gillnetters Association

PSWQAT Puget Sound Water Quality Action Team

RCW Regulatory Code of Washington

REUT Resource Enhancement and Utilization Technologies Division

(Northwest Fisheries Science Center)

SCAN Scientific Committee on Animal Nutrition (European Union)

SEPA (Washington) State Environmental Policy Act

SEPA Scottish Environmental Protection Agency

SIC Standard Industrial Classification (Index)

SMA (Washington) Shoreline Management Act

SOAEFD Scottish Office, Agriculture Environment and Fisheries

Department

SSFA Shetland Salmon Farmers Association (Scotland)

USCG United States Coast Guard

USDA United States Department of Agriculture

USFWS United States Fish and Wildlife Service

USOFR United States Office of Federal Regulations

WAC (State of) Washington Administrative Code

WDA State of Washington Department of Agriculture

WDF State of Washington Department of Fisheries (before 1991)

WDFW State of Washington Department of Fish and Wildlife

WDL State of Washington Department of Licensing

WDNR State of Washington Department of Natural Resources

WDOE State of Washington Department of Ecology

WFGA Washington Fish Growers Association

WHO World Health Organization (United Nations)

WMP (BC Canada) Waste Management Policy

WRAC Western Regional Aquaculture Center

WSGP Washington Sea Grant Program
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Abbreviations of Technical Terms and Symbols

AET Apparent effects threshold

AVS Acid volatile sulfides

BHA Butylated hydroxyanisol

BHT Butylated hydroxytoluene

BOD Biological oxygen demand

DIN Dissolved inorganic nitrogen

Eh Redox potential

ER-L, ER-M Effects range low and medium

FCR Feed conversion ratio

H' Shannon-Wiener diversity index

J' Pielou's evenness index

MPN Most probable number

NIS Non-indigenous species

NIZ Neutral impact zone

NOEC No observed effect concentration

NOEL No observed effect level

ORP Oxidation-reduction potential

PCBs Polychlorinated biphenols

PCA Principal components analysis

PEC Predicted environmental concentration

PEL Probable effects level

PNEC Predicted no-effect concentration

RPD Reduction-oxidation potential discontinuity

S

= Total sediment sulfides

SAC Sediment assimilative capacity

SIZ Sediment impact zone

TEL Threshold effects level

TOC Total organic carbon

TVS Total volatile solids
viii

Abbreviations of Diseases and Pathogens

BKD Bacterial kidney disease

BSE Bovine spongiform encephalitis

CS Ceratomyxa

CWD Coldwater disease

EIBS Erythrocytic inclusion body syndrome

ERM Enteric redmouth disease

FC Fecal coliform

FC-MPN Fecal coliform most probable number

FUR Furunculosis

ICH Ichthyopthirius

IHN Infectious hematopoietic necrosis

IPN Infectious pancreatic necrosis

MC Whirling disease

PKD Proliferative kidney disease

VHS Viral hemorrhagic septicemia
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EXECUTIVE SUMMARY

The US Government advocates a strong policy for national aquaculture development. The

Department of Commerce (DOC) has set specific 25-year goals to offset the annual $7 billion

imbalance in seafood trade, and to double employment and the export value of goods and

services. The policy is reflected in strategies proposed by the National Oceanic and

Atmospheric Administration (NOAA) and its three line agencies responsible for certain

aquaculture-related activities. With its broad mandate for stewardship of the nation's marine

and coastal living resources, NOAA recommends that aquaculture development and

environmental protection proceed hand in hand to meet public needs. Thus, in keeping with

the Government's firm commitment to the United Nations Food and Agriculture

Organization's (FAO) Code of Conduct for Responsible Fisheries, the line agencies of NOAA

are encouraging the fisheries and aquaculture sectors to develop national Codes of Conduct,

and their sub-sectors to develop and abide by Best Management Practices (BMPs).

The National Aquaculture Act of 1980 recognized that the principal responsibility for national

development lay with the private sector. Therefore, to increase overall effectiveness of

federal research, transfer, and assistance programs for the private sector, the Act created the

Joint Subcommittee for Aquaculture (JSA). JSA published a National Aquaculture Plan in

1983, which has been recently updated. A review of all the current government policy

statements and the National Aquaculture Development Plan 2000 reveals considerable verbal

(but not financial) encouragement for private initiatives. The Plan recognizes that aquaculture

is not a unique industry with unique hazards. Its systems and practices, and its products,

parallel those of many other industries and human activities. Apart from the single and

pandemic caveat of protection for the environment there are no directives which promote one

aquaculture system or practice over another, elevate one genera or species above another, or

forward or forbid the use of any specific technology. In summary, there is no political

attempt to rate or rank a sub-sector, or to advance or suppress any specific activity because of

any known risk.

The sub-sector of salmon farming in saltwater is a minor part of the national aquaculture

industry, but it is a valuable economic asset contributing 11% to the total value of all

aquaculture products. Only 45 commercial farms produce salmonids in marine net-pens

directly for food, which is just 1% of all production facilities registered in the country, and

<6% of all facilities in marine and coastal waters. Another 244 federal, state, or tribal

facilities in the freshwater environment produce anadromous Pacific and Atlantic salmon for

restoration of the commercial fisheries, recreational fisheries, or conservation, and another

362 freshwater facilities produce salmonids for both food fish and recreational fisheries.

Because of its particular niche in marine and coastal waters, American net-pen technology has

resulted in considerable growth of secondary producers in the aquaculture industry, and

contributes a disproportionate share to the export of national goods and services.

Despite the economic success of net-pen salmon farming in the USA, this review of scientific

and other literature reveals that there are many perceived and real issues with this industry

which concern the American public. These areas of risk and uncertainty occur in many facets

of the industry - from the effects of salmon farming on the environment, to competition with
x

other economies for the same resources, and the human health and safety of farming or

consuming farm products. However, based on the evidence available in the existing literature

and in ongoing research, it is apparent that the degrees of risk vary considerably from issue to

issue.

Risk and Uncertainty in the Pacific Northwest Industry

A. Issues which carry the most risk

After a review of the available scientific literature, the following three issues of net-pen

salmon farming in the Pacific Northwest appear to carry the most risk. All potentially impact

the environment.

1. The impact of bio-deposits (fish feces and uneaten feed) from farm operations on the

environment beneath the net-pens.

Bio-deposits from salmon farms settle onto sediments near the net-pens and can have definite

effects on their chemistry together with their benthic and infaunal biota. Firstly, with regard

to the chemistry, changes can be anticipated in total volatile solids and sulfur chemistry in the

sediments in the immediate vicinity of operational net-pens, together with decreased redox

potential. Sedimentation rates remain fairly constant irrespective of farm size, which

currently is about 1,500 mt, and a typical total volatile solids (TVS) loading is 32.9 g/m2-day

for the perimeter of such a farm near peak production. This value is reasonably close to a

theoretical average of 25.7 g TVS/m2-day calculated for an entire 18-month production cycle.

Reduced accumulation of volatile organic material under farms can extend to distances of 145

to 205 m from the net-pen perimeter during peak production. The magnitude of the change in

any of these parameters is correlated with the degree of flushing in and around each farm site.

Secondly, with regard to the benthic biota, the accumulation of bio-deposits can enrich

benthic communities but the actual affects depend on the hydrodynamics of each particular

site. At poorly circulated sites these accumulations can exceed the aerobic assimilative

capacity of sediments, leading to reduced oxygen tension and significant changes in the

benthic community. Under extreme conditions sediments can become anoxic and

depauperate. However, under any circumstances these effects are ephemeral and conditions

have returned to normal within a period of weeks to years during fallow periods in all cases

studied.

Thirdly, with regard to the infaunal communities, the accumulation of organic wastes in the

sediments can change their abundance and diversity. But prolonged case studies reveal

significant differences between poorly-flushed and well-flushed sites. At poorly-flushed sites

benthic effects are highly dependent on farm management practices. Very high salmon

production levels and other activities, such as cleaning nets in-situ, result in significant

changes in both abundance and diversity of infauna to distances as great as 30:m from the netpen’s perimeter. At reduced production levels, and in the absence of in-situ net cleaning, the

impacts are restricted to as little 15 m, or less, downstream from the net-pens. At well-flushed

sites the abundance and diversity of infaunal organisms is positively correlated with total
xi

organic carbon, suggesting that the farm stimulates the infaunal community throughout the

area.

2. The impact on benthic communities by the accumulation of heavy metals in the sediments

below the net-pens.

Both copper, from marine anti-fouling compounds used on net-pens, and zinc, from fish

feeds, can be toxic in their ionic forms to marine organisms. Levels of copper are elevated

around some net-pen farms which use government-approved anti-fouling paints on structures

or, more likely, treat their nets with approved commercial compounds containing copper. The

detected additions of copper in the water following the installation of newly-treated nets are

biologically insignificant, except to organisms which settle on the nets. Zinc is an essential

trace element for salmon nutrition, and it is added to feeds as part of the mineral supplement.

Sediment concentrations of zinc are typically increased near salmon farms and the

concentrations at a few farms in British Columbia have exceeded Washington State's

sediment quality criteria (270 ìg zinc/g dry sediment).

The degree of risk is dependent on several factors. Firstly, the concentration of sulfide in the

sediment is important, as typically elevated concentrations near salmon farms reduce the bioavailability of both copper and zinc thus making the observed concentrations non-toxic.

Long-term studies have demonstrated that the metal concentrations return to background

during the period of chemical remediation, and there is no evidence of a long-term buildup of

these metals under salmon farms. Secondly, the formulation of the feed is relevant, as the

majority of feed manufacturers now use reduced amounts of a more bio-available proteinated

form of zinc, or a methionine analog. Monitoring of zinc continues to determine the efficacy

of this change in reducing even the temporary accumulation of zinc in sediments under

salmon farms. Finally, management practices play a role, as the potential rate of

accumulation of copper in sediments can be significantly reduced by washing the nets at

upland facilities and properly disposing of the waste in an approved landfill.

3. The impact on non-target organisms by the use of therapeutic compounds (both

pharmaceuticals and pesticides) at net-pen farms.

In European salmon farms therapeutic compounds are used for the control of sea lice, both for

the health of the fish and to reduce their potential as vectors. The commonly used compounds

are all non-specific within the Class Crustacea, and several are broad-spectrum biocides with

potential to affect many phyla adversely.

The degree of risk is greatly reduced by government regulation for the use of specific

therapeutic compounds following extensive research in vitro and in situ on their effects on

marine organisms. Case studies show that some of these compounds can be detected in

sediments close to the perimeter of net-pen farms, but the levels resulting from their

authorized use do not show significant widespread adverse affects on either pelagic or benthic

resources. In the Pacific Northwest the use of pharmaceuticals to control sea lice has not been

practiced in Washington State for over 15 years because they have not presented significant
xii

problems to growers, but some sea lice control agents have been used infrequently in British

Columbia.

Note: One more issue might be included in this first category, although the degree of risk is

uncertain as there is little scientific information available. This is the impact on human health

through consumption of feed-borne organic toxicants. Farmed fish are exposed to dioxins

through feed ingredients, and dioxins are found in virtually all feedstuffs of animal origin,

especially those containing fish meal and oils. Dioxins can be accumulated and transferred up

the food chain. But the degree of risk is uncertain, as the impact of dioxin and dioxin-like

compounds on human health is a recent discovery. Currently the Codex Alimentarius

Commission is making efforts to reduce the risk by specifying stringent quality control of the

ingredients for all animal feeds, and the potential for substituting plant proteins and oils for

fish meal and fish oil in salmon diets. Although observation of the Codex by the 165 member

countries is voluntary, the USA is an active signatory (see the section on Managing Risk and

Uncertainty, which follows).

B. Issues which carry a low risk

Puget Sound is a stressed ecosystem and one continuously being degraded by further human

intervention. For the last 25 years it has been an area of intense annual population growth

(1.5%) and is now home to 4 million people, with 1.4 million more projected by 2020. It is an

area noted for recreational sailing and fishing, and there has been a corresponding growth in

the number of support facilities for these water-borne activities. Salmon net-pen farming is

another intervention competing for space and water-use, albeit minute by comparison. There

are only 10 salmon net-pen farms active on sites in Puget Sound and unlike marinas, which

deplete oxygen levels and elevate water temperatures, they are porous structures.

Nonetheless, there are a number of facets of the net-pen salmon industry in Puget Sound

which appear to carry a low risk. The majority of these eight issues concern the environment

in the immediate vicinity of the farms themselves.

4. The physiological effect of low dissolved oxygen levels on other biota in the water

column.

Fish stocked intensively in contained areas are known to have a high oxygen demand.

Decades of monitoring in Washington State have found a maximum oxygen reduction of 2

mg/L in water passing through salmon net-pens where large biomasses of fish were being fed.

In most cases the reduction in dissolved oxygen has been < 0.5 mg/L. Salmon are more

sensitive than most other species to depressed oxygen levels and 6.0 mg/L is considered a

minimum concentration for optimum health. Therefore, if there was a localized effect

associated with net-pen culture, the farmed salmon would be the first organisms affected. At

coastal (oceanic) sites, farmed salmon are infrequently subjected to low dissolved oxygen

concentrations when oxygen deficient up-welled water naturally intrudes into the growing

area. However, these are oceanographic events which have nothing to do with the culture of

fish or shellfish. In even the most poorly flushed farm in Puget Sound the culture facility

does not consume quantities of oxygen sufficient to affect other organisms.
xiii

5. The toxic effect of hydrogen sulfide and ammonia from the bio-deposits below a net-pen

farm on other biota in the water column.

The accumulation of any highly-organic sediment produces ammonia and hydrogen sulfide

once the oxygen is depleted. These gases most frequently cycle between oxidized and

reduced states within superficial sediment layers where they modify the infaunal community.

They are infrequently released into the water column. Although there is evidence from in situ

studies that total sulfide concentrations in surface sediments in areas of high organic loading

can exceed 20,000 ìM, there is little soluble hydrogen sulfide in the water column even under

poorly flushed sites. Less than 1.9% of the gases at the sediment-water interface are sulfide,

and this can be reduced to 0.05% at a distance 3 m above the sediment. The majority of these

gases are methane and carbon dioxide. In a well-sited farm concentrations of hydrogen

sulfide gas rising through the water column are rapidly reduced by oxidation, diffusion, and

mechanical mixing. For these reasons it is unlikely that toxic conditions caused by hydrogen

sulfide will ever occur unless there were extremely large emissions at the sediment-water

interface in shallow water.

6. The toxic effect of algal blooms enhanced by the dissolved inorganic wastes in the water

column around net-pen farms.

Enhancement of a harmful algal bloom by the inorganic nutrients discharged from salmon

farms in Puget Sound is feasible but highly unlikely to occur in the Pacific Northwest. First,

apart from the summer months, the natural atmospheric and geographical parameters of the

region reduce light availability for photosynthesis, and the waters are vertically well mixed

which reduces the time phytoplankton spend in the euphotic zone. Second, the physical

characteristics of locations permitted for salmon farming are not conducive to the

accumulation of nutrients, even when the water body is nutrient limited. Decades of

monitoring have shown minimal increases in inorganic nutrient concentrations downstream

from even the few sites having restricted water exchange. Small increases observed at 6 m

downstream during slack tide have been statistically insignificant at a distance of 30 m

downstream. Nutrient-limited embayments in Washington State have been identified and

salmon aquaculture activities in these locations are discouraged and carefully managed when

allowed.

7. Changes in the epifaunal community caused by the accumulation of organic wastes in

sediments below net-pen farms.

The effects on a wide variety of epifaunal communities have been studied in detail and the

results are well-documented. One case study, with long-term (up to 10 years) monitoring,

reveals significant numbers of fish, shrimp and other megafauna inhabiting the site, which

appears to function as an artificial reef. Other salmon farms in close proximity all share the

same characteristics, even attracting larger predators to the enhanced epifaunal communities.
xiv

8. The proliferation of human pathogens in the aquatic environment.

Wild salmonids carry genera of marine bacteria, such as Vibrio, Acinetobacter, and

Aeromonas, some species of which are pathogenic to humans. The concern is that fish feces

and waste feed might enhance populations of these pathogens. There is no evidence in the

literature, or in the epidemiological records of Washington State, of any documented case in

which the handling or consumption of farmed salmon has led to infectious disease in

consumers or farm workers. There are many differences in the physical and chemical

composition of salmon farm waste compared with human sewage discharge, and the former

does not disperse over large areas but remains localized where it is metabolized by naturallyoccurring marine bacteria and invertebrates. There is no credible evidence supporting a

hypothesis that salmon farming increases the risk of infectious disease in humans or wild

populations of animals.

9. The proliferation of fish and shellfish pathogens in the aquatic environment.

Public health concerns for the safety of fish and shellfish in the vicinity of discharges of

industrial and residential waste are real, and vigilance is maintained by stringent regulations

and monitoring programs. The accumulation of wastes from net-pen farms is perceived as

another source of human and environmental pathogens. However, there is little evidence

substantiating this hypothesis. Viruses pathogenic to fish have no documented effect on

human beings because they are taxa-specific. Fecal coliform bacteria are unlikely to persist in

net-pen sediments rich in total organic carbon as they are specific to warm-blooded animals.

Sources of fecal coliform bacteria near salmon farms are more likely to be mammals (such as

seals and sea-lions) or birds. In situ monitoring at some well-flushed net-pen farms revealed

slightly more fecal coliform bacteria in water and shellfish tissues at stations closest to the

farm perimeter. The sources of observed bacteria were not determined. However, all water

and shellfish tissues examined were consistently of high quality and met all bacteriological

requirements imposed by the National Shellfish Sanitation Program.

10. The increased incidences of disease among wild fish.

Maintaining animal or plant populations in intensive concentrations can be conducive to an

outbreak of disease. The specific diseases and their prevalence in Atlantic salmon stocks

cultured in net-pens in Puget Sound are not shown to be any different than those of the more

numerous cultured stocks of Pacific salmon in hatcheries, which in turn are not known to have

a high risk for infecting wild salmonids. All Pacific and Atlantic salmon stocks currently

cultured in Washington are inspected annually for bacterial and viral pathogens, and the

movement of fish from place to place is regulated by permit.

11. The displacement of wild salmon in the marketplace by farmed salmonids.

Salmon farmers and traditional Pacific salmon fishermen sell the same generic product, and

therefore compete in the marketplace. Regulations specific to Washington State require

farmed fish to be identified for the consumer. In terms of supply, salmon production by the

net-pen salmon industry in the USA has been a counterbalance to the declining commercial
xv

and tribal landings of Pacific salmon to meet increasing consumer demands for seafood. But

in terms of demand there are distinct differences in the species produced by the two

industries, and there are also differences in products available to consumers. Farmed fish are

sold mostly as whole dressed fish and fresh fillets, while the typical disposition of the total

annual wild catch (not by species) of the five Pacific species is whole fish, fresh and frozen,

and canned products.

In terms of price and availability, Atlantic salmon has an all-year round advantage and

therefore a competitive edge over Pacific salmon harvested in the commercial fisheries. They

are also relatively cheap to produce for the market. Per harvested fish, the cost to the private

producer of farmed Atlantic salmon is currently about $1 per pound, head on, gutted weight.

However, irrespective of its origin, production of salmon in Washington has little or no

measurable effect on prices determined by global supply and demand, or reducing the large

importation of farmed salmon from Norway and Chile.

C. Issues which carry very little or no risk

Despite the fact that two of the issues in this final category have many sub-sets, all three

issues are deemed to carry very little or no risk. Two are specific to the environment of the

Pacific Northwest, and the third concerns human health and safety in general.

12. The escape of Atlantic salmon - a non-native species.

Since a reporting regulation was imposed in 1996, the records show that some 600,000

farmed salmon escaped between 1996 and 1999. These were mostly fish between 0.5 - 1.5 kg

in weight. Only 2,500 of these particular escapees were subsequently accounted for. In

addition, between 1951 and 1991 the State made 27 releases of 76,000 smolts of Atlantic

salmon of various sizes into the Puget Sound Basin in attempts to establish this prized species

on the west coast. Many escapees were taken immediately by recreational fishermen angling

close to the net-pen farms, and a few others were taken at random by commercial fishermen in

Puget Sound and beyond. A few fish (which may have originated in either Washington or

British Columbia) have been recovered as far away as the Alaskan Peninsula. However, the

numbers recovered have always been small and the rest remain unaccounted for, and it is

assumed that the domesticated existence and docile behavior of farm fish makes them easy

victims of predators, especially the large populations of marine mammals which now exist

throughout the Pacific Northwest.

The following list summarizes the sub-issues of concern regarding escaped Atlantic salmon in

Puget Sound which appear to carry little or no risk.

(i) Hybridization with other salmonids

There is no evidence of adverse genetic impacts associated with escaped Atlantic salmon on

the west coast of North America as they do not have congeneric wild individuals with which

to interact. Hybrids between Atlantic salmon and the Pacific salmonid species can be

produced in vitro, but with difficulty. Hybrids between Atlantic salmon and brown trout,

another non-native species, are more easily produced in vitro, and occur readily in nature.
xvi

Atlantic salmon x Pacific salmonid hybrids are not observed in nature, whether for introduced

Atlantic salmon in North America, or for introduced North American salmonids to Europe

and the other continents. By comparison, successful hybridization between some North

American salmonids is regularly recorded.

(ii) Colonization of salmonid habitat

Atlantic salmon are unlikely to colonize salmon habitat in the Pacific Northwest. Accidents

occur, and farm fish of various sizes occasionally escape in large numbers. About 1 million

Atlantic salmon have escaped from net-pen farms in Puget Sound and British Columbia since

1990. Only a few were accounted for in recreational and commercial fisheries. In addition to

escapes, deliberate releases of Atlantic salmon to establish local self-sustaining populations

have been made in the Pacific Northwest since the beginning of the century, with the last

release in 1991. Although routine monitoring programs occasionally find naturally-produced

juveniles, naturally-produced adults have yet to be observed.

(iii) Competition with native species for forage

Like all salmonids Atlantic salmon are high on the food chain. But few prey items of any sort

have been found in the stomach contents of escaped Atlantic salmon which have been

recaptured. As survival in the wild is extremely low for escaped farm fish, it is assumed that

their domestic upbringing makes them poor at foraging successfully for themselves.

Therefore, the few natural prey items any escaped fish might consume is negligible, especially

when compared with the competitive food requirements of the juvenile Pacific salmon

deliberately released into Puget Sound and its tributaries from hatcheries.

(iv) Predation on indigenous species

All salmonids are predators. However, all analyses of the stomachs of recovered farm

Atlantic salmon, and of the few naturally-produced juveniles caught in the wild, have failed to

show evidence of preying on native salmonid species. This is not the case of other introduced

non-native species which are known to be voracious predators of juvenile Pacific salmonids.

Some of these non-native predators have been deliberately and/or accidentally introduced and

are now managed for sustained natural reproduction to enhance recreational fisheries and for

their contribution to sport fishing revenues.

(v) Vectors for the introduction of exotic pathogens

Provided no new stocks or eggs of Atlantic salmon are introduced into the region, farm

Atlantic salmon cannot be a vector for the introduction of an exotic pathogen into Washington

State. The extensive movement of aquatic animals and plants globally is known to carry the

risk of introducing exotic diseases but movement of fish into and within Pacific Northwest

states is now well-regulated with the requirement for disease-free certification. No Atlantic

salmon stocks have been transferred into the State of Washington since 1991.

13. The impact of antibiotic-resistant bacteria on native salmonids.

Drugs are used in all hatcheries and rearing facilities, and over-use of drugs is known to

increase the resistance of many bacteria. Therefore there is the potential for development of

antibiotic-resistant bacteria in net-pen salmon farms or Atlantic salmon smolt hatcheries
xvii

which could in time impact native salmonids. All drugs used in fish culture in the USA are

scientifically safe and efficacious, and approved by the FDA. Drug resistance has been

commonly observed in public fish hatcheries in Washington State for over 40 years and no

resulting adverse impacts on wild salmonids have been reported.

14. Impacts on human health and safety.

The consumption of salmon farm products and/or working in and around the vicinity of netpen salmon farms are perceived by some people to be concerns of human health and safety.

The following list summarizes these sub-issues of concern regarding human health and safety

which appear to carry little or no risk, either directly or indirectly.

(i) Heavy metal contamination of farm products

The three main sources of heavy-metal contamination found in coastal waters where fish and

shellfish are farmed include industrial and municipal waste discharge, anti-fouling paints, and

various organic pesticides, herbicides, and hydrocarbons. Problems with industrial and

municipal waste discharges have long been recognized, and exposure to toxic chemicals from

these sources are minimized by licensing farming areas away from sources of contamination.

The hazards of heavy metal contamination, principally methyl mercury and tributyl-tin, are

currently addressed by regulatory controls. As intensive farming relies on high quality

formulated diets, the ingredients are regularly monitored to avoid possible contamination of

feed with methyl mercury; and the use of tributyl-tin, once a common biocide used in antifouling bottom paints and for treating net-pens structures, is totally banned in North America.

(ii) Rendered animal products in animal feeds

The use of rendered animal proteins, once common in formulated feeds for many species of

fish as well as other farm animals, has been curtailed by public concern over possible

amplification of bovine spongiform encephalopathy (BSE), or 'mad cow disease'. Although

not specifically prohibited by regulation, rules designed to prevent cross-contamination of

feeds and feed ingredients at time of manufacture have effectively eliminated the use of these

ingredients from salmon feeds. There are no scientific studies on the potential for BSE

transmission to humans through discharge of BSE prions into the aquatic environment, but

based on studies of the discharges from rendering plants to aquifers used for drinking water,

the possibility of infection by this route is remote.

(iii) Genetically modified (GM) ingredients in fish feeds

Although safety concerns regarding the use of GM ingredients in animal feeds have not been

substantiated scientifically, most feed suppliers continue to offer only GM-free feeds. The

use of GM oilseeds and grains in animal and human foods has gained considerable public

attention in North America because of uncertainties regarding their effects on human health

and the environment.

(iv) Other ingredients and additives in animal feeds

The use of pigments, hormones, antioxidants, and vitamin/mineral supplements in animal

feeds is strictly controlled by FDA regulations. Although growth hormones are given

commonly to other farm animals, such as poultry and cattle, their use in food fish is
xviii

prohibited. Additives such as pigments, antioxidants, and other nutritional supplements have

been proven safe and their use in fish feeds is permitted by FDA regulation.

(v) Residual medicines and drugs in farmed products

Antibiotic residues in any farmed animals, including fish, is of concern to consumers because

they might induce allergic reactions, have toxic effects, or simply increase antibiotic

resistance in human pathogens. All drugs used in aquatic species farmed in the USA have

been proven safe and efficacious, and are undetectable at the time of harvest when withdrawal

times prescribed by the FDA are followed. At present only two antibiotics are registered and

sold for use in the USA as feed additives for disease control in farmed fish. The use of

parasiticides and vaccines is similarly restricted by FDA regulation. There could be a risk to

consumers if these chemical compounds and vaccines were misused or administered by

untrained workers.

(vi) Biological hazards in farm products

Potential biological hazards include parasites, bacterial and viral infections, or naturally

produced toxins. To date there have been no reported cases of any fish parasites or

pathogenic organism from farmed fish causing disease in humans. Most hazards have been

eliminated by strict adherence to BMPs on the farm and at harvest, and/or by HACCP

regulations during processing.

(vii) Transgenic farm fish

The perceived hazards of transgenic farms products, such as human allergies or unnatural

competitors in the ecosystem, are hypothetical issues for net-pen salmon farming in Puget

Sound. There is no evidence in the literature that transgenic fish have been raised or are being

raised in the Pacific Northwest, and there are no plans to raise them.

(viii) Workers' safety

Compared with commercial fishing, which is identified as one of the most hazardous of

occupations, net-pen salmon farms provide a safe working environment. Some fatalities and

injuries in the national aquaculture industry from physical accidents have been reported but

not specifically among net-pen salmon farmers.

(ix) Public safety and navigational hazards

There is no evidence that floating net-pen structures in Puget Sound are a hazard to the safe

navigation of Washington's large and diverse boating communities. Firstly, permits from the

US Coast Guard and Army Corps of Engineers are required for each farm to ensure that it

complies with navigation and water safety regulations. Secondly, the complexes are small in

total area. The ten active sites, which range in size from 2 - 24 acres, occupy only 131 acres

of navigable surface waters from the State. The actual surface areas of the net-pen structures

themselves occupy only 21.2 acres in total, with each complex ranging from 0.48 - 3.9 acres.

By comparison the State has 77 aquatic land sites leased for commercial shellfish production,

with a total area of 81,500 acres.
xix

(x) The impact on nearby property values

In the competition for coastal sites between the salmon farming industry (requiring access and

good quality water conditions), and residential real estate (requiring access and industry-free

views) there is no evidence that the sight and presence of net-pen operations has impacted the

values of coastal properties in Puget Sound.

Managing Risk and Uncertainty

A. The environment

There is considerable evidence available in the scientific literature to evaluate any potential

risk of net-pen salmon farming on the environment of the Pacific Northwest. Most issues

have been studied in great detail for some 20 years, and in many similar environments in

different parts of the world. The results are well documented, and a common denominator is

that the potential for environmental impact depends primarily on the site of each individual

farm. The most important rule in the management of risk is therefore the careful selection of

the site.

Responsible permitting of each site is also playing an important management role. The

National Pollution Discharge Elimination System (NPDES) permit has been effective in

regulating the degree of allowable effect, but its impact must now be supplemented with the

strict adherence by site operators to a well-defined set of industry BMPs which are based on

good scientific information. These BMPs can be specific to a particular farm, or they can be

overarching for the entire industry.

Scientific evidence in the literature indicates that the potential changes in the sediments below

operating net-pen farms bear the most risk for the environment. Continuous monitoring of the

sediments under and around farm sites for many years has produced an extensive database of

chemical and biological information, and specific parameters are now being used to predict

the environmental effects. Key parameters include, inter alia, sediment grain size, total

volatile solids or total organic carbon, redox potential, free sulfide concentrations and

ultimately invertebrate community assessment. Modeling programs are also beginning to

provide insight into the environmental response to farm waste, but these are not yet adequate

to make reasonable quantitative predictions.

Long-term monitoring of the sediments has also revealed that chemical and biological

recovery of the substrate under and around farm sites occurs naturally without human

intervention or mitigation. In situ data show that physicochemical recovery can occur within

weeks or months at some sites, and within two or three years at others. Biological

remediation of the sediments follows after a period of chemical remediation, and the speed of

recovery depends on the seasonal recruitment of new infauna.

B. Human health and safety

Net-pen salmon farming is a relatively new global industry, but one which is very highly

regulated in the USA. Atlantic salmon cannot be farmed in the Pacific Northwest or along the
xx

Northeastern Atlantic coast under any conditions which might pose a hazard to human health

by exposure to environmental contaminants, pathogens, or infectious disease organisms.

Farm salmon cannot be treated with any chemo-therapeutic compounds not approved by the

US Food and Drug Administration (FDA). The health and safety of the farm workers are

protected similarly by labor and industrial regulations.

The United Nations Food and Agriculture Organization (FAO) in 1995 formally adopted a

Code of Conduct for Responsible Aquaculture, which was followed in 1997 by a detailed

document called Responsible Aquaculture at the Production Level. These documents detailed

areas of concern regarding the responsible, safe, and effective use of feeds and feed additives,

chemicals and chemotherapeutants, and other aquaculture practices which might reduce health

and safety risks to humans. Food safety issues associated with farmed aquatic organisms have

been subsequently evaluated by the World Health Organization in a working committee of the

Codex Alimentarius Commission. The USA, which has agreed to abide by the intentions of

all these international codes, has also developed national guidelines regulating the safety of all

seafood, including farmed products. These are administered by the FDA.

The literature reveals that the net-pen salmon farming industry in the Pacific Northwest is

integrating all these safety assurance and quality control measures at all levels of the farm-totable food-safety continuum. It has been applying Hazard Analysis and Critical Control Point

(HACCP) methods wherever possible since their inception, and is in the final stages of

publishing its own BMP.

C. Farm escapes

Accidents have occurred enabling farmed salmon to escape. Such incidents are likely to

continue following some unique meteorological event or human error. The possible negative

consequences of such events have been limited in part by implementation of pre-prepared

recovery plans, some of which have included deregulating catch limits for public fishing on

escaped farm fish, and by programs to monitor the background populations of fish in nearby

watersheds. These responses will continue to be effective management practices to minimize

impact, together with further advances in the technology. Improvements in the design and

engineering of net-pens and their anchorages, and the use of new net materials, are continuing

to reduce the incidents of loss following structural failure or damage from large predators.
1

TABLE OF CONTENTS

TABLE OF CONTENTS.....................................................................................................1

FOREWORD.................................................................................................................. 3

1. GENERAL DEVELOPMENT OF AQUACULTURE IN THE USA.......................... 5

1.1 Federal Leadership for the National Aquaculture Industry .................................... 5

1.2 The National Salmon Aquaculture Sector............................................................. 6

2. SALMON AQUACULTURE IN THE STATE OF WASHINGTON ......................... 9

2.1 Salmon Production for Restoration and Conservation ........................................... 9

2.2 Salmon Production for Food............................................................................... 11

2.3 Interactions of Farming with Commercial and Recreational Fishing ................... 12

2.4 Interactions of Farming with Recreational Activities in Puget Sound.................. 16

2.5 Economic Benefits of Salmon Farming to the State ............................................ 17

2.5.1 The contribution of salmon farming to seafood production............................ 17

2.5.2 The impact on employment and wages.......................................................... 18

2.5.3 The impact on coastal property values........................................................... 19

2.6 The Regulatory Structure for Commercial Enterprises........................................ 20

2.7 The Regulatory Structure for Public and Tribal Hatcheries ................................. 23

3. POTENTIAL ISSUES FOR HUMAN HEALTH AND SAFETY............................. 25

3.1 General Food Safety ........................................................................................... 25

3.2 Chemicals and Chemical Contamination............................................................. 26

3.2.1 Heavy metals................................................................................................ 26

3.2.2 Manufactured feeds....................................................................................... 27

3.2.3 Chemotherapeutants...................................................................................... 31

3.3 Biological Safety ................................................................................................ 33

3.4 Quality and Safety of the Products....................................................................... 34

3.5 Worker Safety .................................................................................................... 35

4. SALMON FARMING AND THE ENVIRONMENT............................................... 36

4.1 The Effects of Organic Wastes from Net-pen Salmon Farms .............................. 36

4.1.1 Waste feed.................................................................................................... 36

4.1.2 Fish feces...................................................................................................... 37

4.1.3 Fish carcasses as wastes................................................................................ 38

4.1.4 Bio-fouling organisms as wastes................................................................... 38

4.1.5 Measurement of organic wastes .................................................................... 39

4.2 Dissolved Inorganic Wastes................................................................................ 41

4.2.1 Dissolved nitrogen and phosphorus............................................................... 41

4.2.2 Heavy metal accumulation in sediments........................................................ 42

4.3 Pathogenic Organisms in the Vicinity of Net-pen Salmon Farms......................... 45

4.3.1 Fecal coliform bacteria.................................................................................. 45

4.3.2 Farm wastes.................................................................................................. 46

4.4 The Effects of Therapeutic Compounds.............................................................. 47

4.5 Farm Sediments.................................................................................................. 51

4.5.1 Monitoring environmental effects on sediments............................................ 51

4.5.2 Biological changes in the water column and sediments ................................. 53

4.5.3 Hydrogen sulfide gas production in sediments .............................................. 55
2

4.5.4 Dissolved oxygen.......................................................................................... 56

4.5.5 Changes in the local fish community............................................................. 56

4.5.6 Physicochemical changes in the sediment near salmon farms........................ 57

4.5.7 Biological effects.......................................................................................... 57

4.5.8 Case histories describing benthic responses to salmon farming.......................59

4.6. Recovery and Remediation of Sediments........................................................... 60

4.6.1 Chemical remediation ................................................................................... 60

4.6.2 Biological remediation.................................................................................. 61

4.6.3 The assimilative capacity of the local environment ....................................... 65

4.7 Managing the Environmental Effects Associated with Salmon Farms................. 65

4.7.1 Monitoring experiences................................................................................. 65

4.7.2 Management by modeling salmon farm wastes ............................................. 68

4.7.3 Risk management through NPDES permit standards..................................... 69

4.7.4 Risk management practices in British Columbia ........................................... 72

5. ATLANTIC SALMON and the LOCAL ECOSYSTEMS ........................................ 74

5.1 General Issues of Artificial Propagation of Salmonids......................................... 74

5.2 Genetic Interactions of Artificially-Propagated Pacific and Atlantic Salmon........ 75

5.2.1 Hybridization................................................................................................ 75

5.2.2 Genetic dilution and alteration of the wild salmonid gene pool...................... 77

5.2.3 Colonization by Atlantic salmon ................................................................... 78

5.2.4 Interactions of wild salmon and transgenic fish............................................. 79

5.3 Epidemics and the Transmission of Waterborne Disease..................................... 80

5.3.1 The origin and disease status of Atlantic salmon stocks in Puget Sound ........ 80

5.3.2 Disease of salmonids..................................................................................... 80

5.3.3 Infectious disease therapy ............................................................................. 83

5.3.4 Disease interactions between wild and propagated salmonids........................ 84

5.3.5 The scale of artificial propagation ................................................................. 85

5.3.6 Disease control policies in Washington and the USA.................................... 86

5.4 Potential Ecological Impacts of Atlantic Salmon in the Pacific Northwest ........... 87

5.4.1 Social interactions between Pacific and Atlantic salmon ............................... 87

5.4.2 Predation by Atlantic salmon ........................................................................ 88

5.5 Potential Impacts of Propagated Pacific Salmon .................................................. 88

5.6 Adverse Impacts of Non-indigenous Fish Introductions...................................... 91

5.7 A Perspective of Salmon Culture in Northwest Waters....................................... 94

5.8 NMFS Biological Status Reviews of West Coast Pacific Salmon Stocks............. 96

6. POST SCRIPT ......................................................................................................... 97

7. REFERENCES ........................................................................................................ 98
3

FOREWORD

Many government regulators are now encouraging all intensive food production

industries, including capture fisheries, to adopt and observe protocols and methodologies

to make their activities more compatible with the environment. The majority of these

industries are responsive to this challenge and are beginning to comply through selfdeveloped codes of practice and best management practices.

A code of practice (COP) describes a set of general practices and standards to guide

human conduct in a specific endeavor in order to maintain conformity and consistency.

COPs are voluntary in principle but invariably the overarching organization, such as the

Federation of European Aquaculture Producers (FEAP), makes them obligatory in

universal interest (FEAP 2000). Best management practices (BMP), on the other hand,

describe a specific (and often detailed) set of protocols, practices, or procedures to

manage and carry out specific operations in a responsible manner, with respect to the

social and ecological environment, based on the best available scientific information and

an assessment of risk. BMPs are voluntary in principle but invariably the overarching

organization makes them mandatory in the interest of the specific industry.

Each element in any code of practice is based on the best scientific information available

or the most practical experiences. Consequently a code of practice is not a finite entity in

itself but a never-ending dynamic process ready to incorporate each relevant scientific

discovery and each new technical experience. In 1997 the Environmental Assessment

Office of British Columbia (EAO) published the British Columbia Salmon Aquaculture

Review (BCSAR). A section of this comprehensive document (EAO 1997) discussed

key environmental issues based on reviews of over 750 scientific and technical papers,

and many pertinent government documents. This background information greatly

assisted the British Columbia Salmon Farmers Association (BCSFA) to develop its

individual code of practice in 1999 (BCSFA 1999), and the New Brunswick Salmon

Growers Association will complete its code in 2001 (N. Halse, NBSGA, personal

communication). The same efforts have been made in other countries, and in 2000 the

Shetland Salmon Farmers Association of Scotland produced its code of best practices

(SSFA 2000).

Government and salmon farmers in the US on both the west and east coasts have not

moved as quickly as those in Canada, or indeed as those in Norway, Scotland, and

Ireland. This is because most of the sub-sectors of American aquaculture are very small,

unlike those of US agriculture, and individual farmer's associations do not have the

capacity or scientific information on which to develop appropriate codes. Consequently,

research staff of the Northwest Fisheries Science Center (NWFSC) has prepared this

scientific review to help salmon farmers in the Pacific Northwest codify their industry.

Research by scientists of the NWFSC first instigated the industry of net-pen salmon

farming in saltwater in North America at the Manchester Research Station in the early

1970s. Subsequently salmon have been farmed extensively in the Pacific Northwest in
4

the protected waters of the Georgia Straits and Puget Sound. Therefore it is fitting that

the NWFSC is guiding the local industry to be compatible with its ecological

surroundings.

This document is the result of the efforts of the Resource Enhancement and Utilization

Technologies Division (REUT) of the NWFSC. It is not a comprehensive review of the

literature on net-pen salmon farming from its historical beginning, like the BCSAR, and

it is not trying to update the BCSAR with citations to information after 1996. The

document is intended to stand in its own right and fulfil a set of three objectives:

• First, from the perspective of the US and local stakeholders it annotates the best

scientific information regarding local issues arising from or affecting development of

net-pen salmon farming in the Pacific Northwest.

• Second, together with other literature reviews, it completes an information base for all

stakeholders to make a qualified and quantified analysis and assessment of any risks

associated with salmon farming in the area.

• Third, together with these risk assessment studies, it will assist salmon farmers to

develop an appropriate COP for their industries, and in particular the salmon farm and

hatchery managers in the Pacific Northwest, to develop a set of BMPs for their

specific activity.
5

1. GENERAL DEVELOPMENT OF AQUACULTURE IN THE USA

The first chapter initially summarizes the national leadership for development and

growth of the aquaculture sector by a range of government policies and legislation

spread over half a century. It explains government direction was first to mitigate

for displaced wildlife resources but now its objectives are to reduce imbalances in

seafood trade, enhance commercial fisheries, and assist conservation of

endangered species. It notes that national development has been guided for

twenty years by the National Aquaculture Act of 1980, and a National

Aquaculture Development Plan which has been continually under review and

updated. The second part of the chapter summarizes the national salmon

aquaculture sector. It provides current data for the two key pillars of the sector,

specifically production for enhancement of commercial and recreational salmon

fisheries, and production of food-fish for domestic and export markets. It

explains briefly the different commercial end-products of salmon aquaculture, and

the contribution to the national economy made by the industry's producers of

good and services.

1.1 Federal Leadership for the National Aquaculture Industry

Modern aquaculture is not new technology to the USA. Early attempts to culture fish and

shellfish in North America date back to the 1850s and 1860s, and it was the intensity of

the early pioneers to raise fish to enhance the indigenous fisheries which persuaded the

US Government to create the US Fish Commission in 1871. The Commission, in time,

became the Bureau of Commercial Fisheries and subsequently the National Marine

Fisheries Service (NMFS).

Early development of aquaculture in the US was continuously expanded by legislation.

Predominantly it was federal legislation to compensate for salmon fisheries affected by

federal water projects in the Columbia River Basin. The Federal Power Act of 1920 and

the Fish and Wildlife Coordination Act of 1934 were responsible for over $400 million

spent on salmon hatcheries and fish passages constructed at that time, and in 1938 the

Mitchell Act authorized appropriation of federal tax revenues annually to restore and

enhance the salmon resources of the Columbia Basin as a whole. As a result, a

substantial technical and scientific research and information base was established in the

country on almost every aspect of the biology and culture of Pacific salmon. This

knowledge and experience was a significant factor in the farming of both North

American and European salmonids some 30 years later.

Encouraging development of aquaculture in the US was again the government's policy

behind the National Aquaculture Act of 1980. Recognizing the growing diversity of

modern aquaculture, and multi-agency responsibilities, the 1980 Act established a

coordinating group, the Joint Subcommittee on Aquaculture (JSA) which continues in

existence today. The JSA has been responsible for developing and updating the National

Aquaculture Development Plan (NADP 2000), which identifies the relative roles of the
6

Department of Agriculture (USDA), the Department of Commerce (DOC), and the

Department of the Interior (DOI).

Within DOC, the National Oceanic and Atmospheric Administration (NOAA) has a

strong statutory base for the promotion and regulation of marine-related aquaculture.

Historically this has been achieved through NMFS programs and the National Sea Grant

College Program (NSGCP) in the Office of Oceanic and Atmospheric Research (OAR).

In 1999 the Secretary of Commerce signed an Aquaculture Policy for DOC identifying

seven specific objectives. Among quantified targets for the aquaculture sector to achieve

by the year 2025, the policy strongly emphasized technological development and growth

in harmony with the environment. The same message is evident in the NOAA policy on

aquaculture, signed in 1998. The underlying goal is for development through

environmentally sound production practices. Particularly noted is the use of aquaculture

technologies for the enhancement of threatened populations but also avoiding negative

impacts on any wild stocks. The policies of both DOC and NOAA are very evident in the

draft National Marine Aquaculture Act of 1999 for further development of aquaculture

into the exclusive economic zone (EEZ).

In conclusion, the federal government continues to encourage sector development

through applicable legislation, funding programs, and agency policies. It has set 25-year

targets for increased domestic production to help offset the large annual trade deficit in

seafood, and to double employment and exports of goods and services. In addition, it

wants new technologies for increased diversification of the industry, and for enhancement

of wild stocks. Finally, it demands economic development with the necessary safeguards

for the environment to be enforced through total compliance with industrial codes for

responsible aquaculture.

NADP 2000 is not detailed regarding different aquaculture products or production

technologies. Irrespective of any sub-sector, the Plan repeats the challenge for better

knowledge about possible interactions between aquaculture and the natural environment

to minimize, (i) the potential for habitat degradation, (ii) transmission of diseases, (iii)

potential genetic dilution of wild stocks through interbreeding with cultivated strains, (iv)

introduction of non-indigenous species into natural waters, and (v) discharges of wastes,

toxins, and excess nutrients (JSA 1999).

1.2 The National Salmon Aquaculture Sector

The Census of Aquaculture recently published by USDA (USDA 1999) reports the value

of salmon produced and sold for food or food/sport in 1998 was $104 million, or about

11% of the total value of national aquaculture products. The Census notes that 244 farms

produced salmon for restoration or conservation purposes. It defines these farms as

mostly non-commercial operations, such as federal, state, or tribal facilities (which were

mostly hatcheries), academic, and private research facilities with products valued above

$1,000 in the year of the Census. Within this total, the Census records that 238 farms

produced 2.4 billion fish (288 million lb or some 130,000 mt), and 47 farms produced 71

million salmon eggs or seed for distribution. Another 362 farms produced trout for
7

restoration or conservation, of which 360 farms produced 177 million fish (32 million lb

or 1,450 mt), and 72 farms produced 163 million eggs or seed for distribution.

In addition the Census notes that 47 farms in the country produced salmon commercially,

of which 45 raised food-size fish. This number is about 1% of all the aquaculture farms

recorded in the country. It is assumed that almost all these salmon farms are saltwater

farms. The Census records that there are only 815 of the 4,028 recorded aquaculture

facilities and/or farms in the country which operate with or within saltwater, and the

majority raise mollusks or tropical fish.

The word 'farm' in the literature can be confusing, as the definition adopted by the Census

is specific to its own use. Typically, 'farm' applies to a physical complex for production

but this, in turn, can refer to a complex on a single registered site, or a number of

complexes operated by a single business which owns or leases a number of registered

sites close together. Using its definition of a commercial or non-commercial place from

which $1,000 of products were sold, the Census shows that the majority of salmon farms

operate in the States of Alaska (19), Maine (12), and Washington (9). But Alaska

prohibits private farming of all fish species, and therefore the number refers to salmon

hatcheries operated by private non-profit corporations (PNPs) which rear to release and

subsequently harvest – an aquaculture practice known as 'ocean ranching.'

The word 'farm' can in fact be applied to any location where primary production of

aquatic animals and plants takes place. There are five primary producers in the salmon

aquaculture sub-sector in the USA, and their end products are:

(i) certified disease-free eggs from a freshwater hatchery,

(ii) pre-smolted juveniles from a freshwater nursery farm,

(iii) smolted juveniles from a saltwater nursery farm,

(iv) marketable fish from the saltwater grow-out farm, and

(v) marketable products after processing.

Active in these areas are both non-commercial and commercial enterprises. The noncommercial enterprises are all the federal, state, and tribal organizations that own and

operate only hatcheries and other licensed rearing facilities to produce pre-smolts and

smolts for release to enhance commercial and recreational fisheries. Commercial

enterprises are private companies which invariably own or have controlling interests in at

least four end-products, and possibly all five. The Western Regional Aquaculture Center

(WRAC) noted that the State of Washington Department of Fisheries and Wildlife

(WDFW) had close to 1,000 aquaculture licenses on file in 1995, of which 74 were for

salmon and 187 for trout production (WRAC 1999). These numbers included both active

and non-active licenses, as licenses are not required to be updated annually.

There are many secondary producers in the industry throughout the country. Their

manufactured end products include, for example, (i) hardware, such as craned vehicles,

service boats, floating cages, net-pens, feed silos, egg incubators, hatchery tanks, raceway

tanks, pumps, pipes, etc., (ii) formulated feeds, (iii) technical apparatus and laboratory

equipment, (iv) veterinary medicines and drugs, and (v) a variety of expert services.

Again, many commercial enterprises active in primary production are active in secondary
8

production, particularly with ownership or controlling interest of subsidiaries in fish

nutrition and health. Within the last 2 years several large companies in Europe and North

America have spread their business risk throughout the global salmon industry by

consolidating their hold on substantial lengths of the value chain.

Secondary producers are very important to the national economy. In a recent aquaculture

policy statement, DOC recognized that the annual value of US exports of goods and

services was $500 million, and set a goal of $2.5 billion by the year 2025 (DOC 1999).
9

2. SALMON AQUACULTURE IN THE STATE OF WASHINGTON

The second chapter is predominantly regional in scope and deals mostly with the

pros and cons of salmon aquaculture in the State of Washington. The first section

provides quantified data regarding aquaculture for restoration and conservation of

salmon fisheries, and some economic costs and benefits. The second section

provides data regarding the physical extent of the commercial salmon farming

industry for food production, making comparisons with other parts of the US and

overseas. The third section describes some of the interactions of the salmon

farming industry in Puget Sound with commercial and recreational fishing

activities, in particular with other fish populations and in the marketplace. The

fourth section deals with economic benefits to the State, particularly at the

regional and local levels. These include the contribution to seafood production,

the impact on employment and wages, and the impact on coastal property values.

The two final sections concern the current regulatory structure for commercial

enterprises raising food fish in the State of Washington, and the regulatory

structure for public and tribal hatcheries raising juvenile salmon for commercial

and recreational fisheries.

2.1 Salmon Production for Restoration and Conservation

The State of Washington has one of the largest artificial production systems for

salmonids in the world. Its hatcheries program operates 24 complexes (groups of

hatcheries) with more than 90 rearing facilities (WDFW 2000). These include production

hatcheries, net-pens, acclimation sites, and rearing ponds, as well as several remote eggincubator locations and small-scale cooperative rearing programs with community and

educational groups. Washington hatcheries produce approximately 75% of all coho and

chinook salmon, and 88% of all steelhead trout harvested statewide. Trout hatcheries

produce over 90% of the statewide harvest. Approximately 700,000 adult salmonids of

several species return to hatcheries each year, and more than 300 million eggs are

collected from them for future generations. All fish raised in State hatcheries are released

into the open waters of Washington. In 1995 some 201 million salmon, 8.5 million

steelhead, and 22.6 million trout and warm-water fish were released. In addition, there

are 12 federal and 17 tribal rearing facilities which produce another 50 million salmonids

for release (WDNR 2000a).

Between 1951 and 1991 WDFW also made 27 releases of Atlantic salmon in attempts to

establish the species in State waters. A total of 76,031 parr and smolts were released

varying in size between 0.25g and 450g (Amos and Appleby 1999). Until 1979 the

origin of the stocks was Gaspé River in Canada, most of which came through

broodstocks held in Oregon. From 1980 the stocks were a mix of origins, including

Gaspé River, the Penobscot and St. John's Rivers (Maine), together with some landlocked

stocks from Grand Lakes (Maine).
10

The State of Oregon, which shares the Columbia Basin with the States of Washington

and Idaho, currently operates 34 hatcheries and 15 other rearing facilities. Annually

these facilities release about 43 million Pacific salmon, 5.7 million steelhead, and 8.3

million trout. In the last decade about 80% of all trout, and 70% of all steelhead and coho

harvested in Oregon were propagated artificially (ODFW 2000). More recently, net-pen

complexes have been used for conditioning and releasing salmon in areas around the

mouth of the Columbia River to create local commercial and recreational fisheries. The

Clatsop County Economic Development project near Astoria released about 3.5 million

coho, and 1.1 million chinook in 2000 (OSU 2000), and expected a return of 5,000 spring

chinook from its previous releases.

Using 1990s data for the production, release, and survival of Pacific salmon from

Columbia Basin hatcheries, where the juveniles may be retained for up to 18 months,

Radtke (2000) calculated that the hatchery cost per harvested coho salmon was $58.89,

with an economic value per harvested fish (7 lb. at $1.00/lb.) of $76.07. For

spring/summer chinook (12 lb. at $1.50/lb.) the costs per harvested fish were $404.55 and

$109.36, respectively, and for fall chinook (15 lb. at $1.25/lb.) they were $35.00 and

$114.5, respectively. For steelhead (9 lb. at $0.60/lb.) the costs were $292.86 and $74.8,

respectively. He also estimated the (fixed plus variable) cost per smolt from hatcheries in

Oregon into the Columbia Basin for salmon (all species) to be between $7.20–7.42 per lb

of smolt. Current estimates by WDFW (K. Amos, WDFW, personal communication) put

the cost at between $3–4 per lb. of smolt. This is because outside the Basin hatcheries

generally retain many stocks for a month or less, primarily chum salmon, which results in

a lower cost per smolt.

Puget Sound has a large number of artificial propagation facilities releasing juvenile

salmonids into its freshwater basin every year. Based on historical data over 30–40

years, a total of 30 facilities together released about 29 million coho every year (NMFS

1995). Some 43 facilities released 65 million chum (NMFS 1997a), and 69 rearing

facilities released about 44 million chinook (NMFS 1998). There are also 10 facilities

which release some 1.5 million-winter steelhead and 400,000 summer steelhead, mostly

smolts, (NMFS 1996). Collectively, these facilities now release about 50 million juvenile

salmon (equivalent to some 300 mt of fish) into the Puget Sound Basin on an annual

basis. The reductions in number of fish released are due in part to changes in hatchery

strategies to lessen the potential adverse impacts on wild salmonids.

Forster (1995), in his evaluation of cost trends in farmed salmon, reported the current

(1994/95) production cost of an Atlantic salmon smolt (100 g in weight, or 3.5 oz) in

Chile, Norway, and Canada was between $0.75–1.25 each, which included $0.5–0.15 for

the eyed egg, and $0.12–0.20 for the feed. Prices asked by smolt producers, however,

might be $1.50–4.00, depending on the size at sale, with $2.00 being the average for a

100g fish. Grez (Salmones Camanchaca S.A. Chile, personal communication) reported

that fixed and variable production costs for rainbow trout and coho salmon smolts in

Chile in 1996 were $0.21–0.26, and a little more for Atlantic salmon depending on the

source and cost of eggs. Rainbow trout and coho salmon smolts were sold for $0.55–0.65

each, and Atlantic salmon smolts for about $1.00.
11

In his report to the State of Alaska Department of Commerce and Economic

Development, Forster (1995) estimated that the cost to the private producer of farmed

Atlantic salmon was $1.14–2.03 per pound, head on, gutted weight. Based on advances

in technology and increased farm efficiencies, he projected that production costs for the

year 2000 would be between $0.73–1.19 per pound, head-on, gutted weight. His current

estimate is that it is about $1.00 (J. Forster, Forster Consulting, personal communication).

2.2 Salmon Production for Food

A production site for salmon farming invariably consists of a complex of on-shore

buildings and tanks, and offshore floating cages or net-pens. Floating cages are usually

associated with the freshwater nurseries for smolt production, and net-pens are associated

with grow-out and production of marketable fish in marine waters. The 1998 Census of

Aquaculture (USDA 1999) defines cages as structures 'normally used in larger, open

bodies of water such as lakes or rivers,' while net-pens are 'enclosures usually placed in

protected bays or inlets used to produce fish.'

Weston (1986), in his study of the environmental effects of floating mariculture in Puget

Sound, recorded nine sites where Pacific coho and/or Atlantic salmon were raised

commercially in net-pen facilities. Another permit had been granted, and others were

pending. There were also three more sites for non-commercial culture, which is for

research or to enhance fisheries. In addition there were five major and eight minor netpen facilities used by tribes or sportsmen's clubs for delayed release of coho and chinook

salmon. By 1990 there were 13 commercial sites, each limited to a total surface area of

less than 2 acres, or 8,100 m2 (WDF 1990). In response to the listing of Puget Sound

chinook salmon as threatened under ESA, chinook salmon releases from minor-net-pen

sites have been reduced or terminated (NWIFC 2000).

In its summary of the status of aquaculture for 1997, WRAC (1999) reported that net-pen

salmon farming in the Pacific Northwest only occurred in Washington. Earlier in the

1990s net-pen rearing of salmon had been practiced in Oregon, California, and Idaho but

had since ceased. Atlantic salmon dominated production (99%) in Washington, with the

remainder being coho, chinook, and steelhead trout.

All salmon production sites in Washington, whether on or off land, are licensed

appropriately. Sites are owned outright or leased (tenured). Companies may own and/or

lease several sites, and consequently some sites are continuously active; others are

developed but not always in use, and a few may be inactive and undeveloped. WRAC

(1999) reported six companies with leases to sites in Washington in 1997. These

included Domsea Farms Inc. (5 sites), Global Aqua US Inc. (3 sites), Moore-Clark Co.

(USA) Inc. (3 sites and a hatchery), Scan Am (3 sites), Sea Farm Washington (3 sites),

and British Petroleum (1 site).

In the last five years there has been considerable restructuring in the salmon aquaculture

industry worldwide with some companies consolidating their position through merger

and/or purchase of smaller companies. Consequently, the global industry is now

dominated by a few international companies, although individual farms may still operate
12

under the name of the registered leaseholder. In Washington four different companies

now hold the leases to 12 licensed net-pen production sites. These are:

• Cypress Island Inc., which has three leases by Cypress Island outside Anacortes and

one lease in Skagit Bay; and (once under Northwest Farms) three leases in Rich

Passage, one in Port Angeles harbor (formed by combining two previous leases), and

one by Hartstene Island currently not in use.

• Sunpoint Systems, which has one lease in Rich Passage.

• Jamestown S'Klallum Tribe, which has one lease in Discovery Bay but not in use.

• Ocean Spar Technologies, a sea-cage manufacturing company which has one lease by

Whiskey Creek near Port Angeles for research and development trials, but not in use.

In the State of Washington, statistics provided by WDNR (2001) indicate there are

166.67 acres currently leased by companies for commercial salmon net-pens, and a

further 38.67 acres currently leased by the State, tribes, and private enterprises for netpens used for the delayed release of Pacific salmon, and 0.39 acres for herring net-pens.

All these sites have a different limit for the water surface area leased (for anchorages and

navigational protection) and the internal surface area for the net-pens in production. The

10 commercial sites currently operational in Puget Sound have a total of 131 acres under

lease from the State (ranging from 2–24 acres in size), with 21.5 acres permitted for the

internal pen structures (range 21,000–170,000 sq. ft) (K. Bright, WFGA, personal

communication). This area is little more than the larger marinas located on State-owned

aquatic lands, any of which can be 15–20 acres in size.

The number of commercial net-pen farms in Washington is small by comparison with

that on the east coast (Maine) and other countries. Maine has 42 permitted sites for

salmon, and two for steelhead, of which six are currently idle (J. McGonigle, Maine

Aquaculture Association, personal communication). Producers in Maine, of which there

are 14 companies, are in the process of moving to single-year-class cultivation over the

next two years. This should result in about one-third of the sites lying fallow each year.

In eastern Canada the industry is largely confined to New Brunswick. In New Brunswick

there are about 60 farming companies, each with one or more permitted sites. There are

also a few sites in Nova Scotia and Newfoundland. In western Canada there are 122

registered net-pen sites in British Columbia (BC), of which 104 are active (BCSFA

1999). The Highlands and Islands Enterprise (HIE) of Scotland recorded 440 growing

sites registered in 1997 with the Agriculture, Environment and Fisheries Department of

the Scottish Office (SOAEFD). Of these, 128 were fully stocked all year round, 202

were in rotation, and 100 were classified as inactive (HIE 1999).

2.3 Interactions of Farming with Commercial and Recreational Fishing

In a commentary on regional fisheries, the Marine Advisory Services of the Washington

Sea Grant Program (WSGP 2001) stated that commercial fishing was a significant

industry in Washington State, with nearly 3 billion lb. of fish and shellfish harvested

annually, with a wholesale value over $1.6 billion. However, the report also added that

commercial fisheries around the world were collapsing and efforts in fisheries science
13

were turning more to conservation of resources and finding ways to harvest fish stocks in

a sustainable manner.

The commercial fisheries of Puget Sound reflect these global trends. WDFW (1994)

reported that commercial salmon harvest levels in the State of Washington had declined

from a peak of over 10 million fish in 1985 to about 7 million fish in 1993, with most of

these fish produced in hatcheries. Similarly recreational salmon fishing levels had

declined from a peak of 1,100,000 fish in 1979 to just over 600,000 fish in 1993. More

recent data by Didier (1998) put preliminary estimates of commercial salmon catch in the

State in 1998 as only 1,618,300 fish, together with141,604 fish in the subsistence catch

by the tribes; and the sport salmon (recreational) harvest in 1997 was down to 451,425

fish. Data for the 2000 landings and prices of salmon in Washington provided by Pacific

Fishing (2001) gave figures of 1,475,315 fish (5,342 mt) that landed in the State, with a

value of $8.5 million. Both landings and prices were considerably above those for 1999.

Much of the decline in the commercial harvest can be attributed to the shift from a

terminal harvest to a high catch-per-unit effort in the offshore fishery. Eriksson and

Eriksson (1993) described the parallel of the Swedish salmon fisheries in the Baltic Sea

in their study of wild and hatchery propagated stocks over the 40-year post-war period.

They concluded that wild fish were unable to cope with the present exploitation rates, and

without the effective compensatory program, a reduction in stock-size of the magnitude

shown by wild salmon in the Baltic would decrease the catch-per-unit effort to such a

degree that there would be no economic incentive for a commercial salmon fishery.

In addition to fluctuating changes in ocean conditions, declines in the commercial harvest

can also be attributed to the increased interest in recreational fishing in Puget Sound, and

competitive pressure on the habitat. Drinkwin and Ransom (1999) projected another 1.4

million people would settle in the Puget Sound Basin by 2020, which would further

degrade the already-stressed ecosystem. Their indicators included continued declines in

bottom-fish populations, restrictions on shellfish harvesting, and rapid loss of freshwater,

estuarine, and near-shore habitats. All these indicators are impacted by the increase in

aquatic recreational activities, particularly recreational boating (see Section 2.4).

The decline in some fisheries populations in Puget Sound has reached significantly low

levels. For example, in 1999 chinook salmon in Puget Sound and summer chum salmon

in Hood Canal were listed as threatened by NMFS under the federal Endangered Species

Act of 1973 (ESA). However, not all aquatic species are in decline. In its current report

on the health of Puget Sound, PSWQAT (2000) noted that the waters of the Sound were

still home to over 220 species of fish, 26 different kinds of marine mammals, 100 species

of sea birds, and thousands of species of marine invertebrates. Some species were

migratory, while others remained in the Sound all year round. Some populations, such as

harbor seals and California sea lions, were increasing rapidly. The trends in the counts of

harbor seals indicated some 12,000 now living in the Puget Sound region, or double the

number recorded in 1985. They attribute these increasing numbers to protection under

the Marine Mammal Act of 1972, variable abundance of food resources, such as Pacific

herring and Pacific hake, decreasing levels of contamination in the water, and tolerant
14

interaction with human interventions. As major fish predators in Puget Sound they must

be contributing to the decline of some fisheries. In a study on the impacts of California

sea lions and Pacific harbor seals on salmonids in the west coast States, NMFS (1997b)

estimated that the total bio-mass consumption by these pinnipeds along the coasts (a

minimum of about 217,400 mt) amounted to almost half of the commercial harvest of the

three States.

There is no evidence in the literature that the presence of 10 operational net-pen salmon

farms in Puget Sound has contributed to the decline of the fisheries populations. In fact

Henriksson (1991), in his study on the effects of fish farming on natural fish communities

in the Baltic Sea, described an overall recruitment by small fish around farms compared

with reference areas, followed by the increased abundance of certain fish species such as,

inter alia, perch, roach, white bream, and bleak. However, Crutchfield (1989) noted that

fishermen opposed the growing salmon net-pen industry for encroachment on fishing

grounds or transfer/over-wintering lay-up areas. He believed this was a legitimate

complaint at the time but suggested it could be rectified easily by restricting net-pen

farms in such sites, although this would add another site burden to farmers.

There is little evidence in the literature that deliberate releases or escapes of farmed fish

from operational net-pen sites have resulted in the sustained natural production of a

population providing a new commercial resource in Puget Sound. Rensel et al. (1988), in

a 5-year tagging study with farmed coho salmon, showed that the annual estimated

recovery (estimated catch plus escapement) averaged 17.1%, which was similar to

recovery rates of coho salmon released from other facilities at about the same time. They

estimated approximately only 0.2% of the released coho salmon survived to enter streams

in the general vicinity of the net-pens. They concluded that the Puget Sound commercial

net fishery benefited most from the program.

In Washington, in addition to the 27 releases of Atlantic salmon made by WDFW

between 1951 and 1991, records by WDFW (Amos and Appleby 1999) indicated a total

of 613,639 Atlantic salmon escaped from farms between 1996 and 1999. There had been

escapes also in previous years (1990–1995), evidenced by the fact that fish were taken in

the commercial and recreational catches, but at that time reporting was not a regulatory

requirement. However, a sustained natural population has not been established.

Similarly attempts to establish Atlantic salmon in the waters of British Columbia were

made between 1905 and 1935. These have also been supplemented with reported escapes

of 286,885 farm Atlantic salmon between 1988 and 2000 (McKinnell et al. 1997, and

A.*Thomson, DFO, personal communication) but again no sustained natural production

has been recorded. A total of 9,096 were recovered up to 1995, mostly in the area where

the abundance of salmon farms was the highest. Wing et al. (1998) report that 89

Atlantic salmon which had escaped from marine aquaculture facilities in British

Columbia and Washington were caught in Alaska fisheries between 1990 and 1995. New

data by Thomson (DFO, personal communication) puts the number at 556 by 2001.
15

Losses of fish from net-pens are not always due to escapes. Moring (1989), in his

documentation of unexplained losses of chinook salmon from small (5.5 m3)

experimental saltwater cages with intact netting were on average 8–38% for individual

locations, and 2.5–46.5% for individual cages. He attributed the losses to rapid

decomposition of carcasses, scavenging by birds, mammals, and fishes, and to a lesser

extent escapes. Actual unaccounted-for losses from commercial net-pens are currently in

the order of ±2–5% (P. Granger, WFGA, personal communication). This is primarily

because unexplained losses are few. In practice, fish arrive from hatcheries inventoried,

and further inventories are taken each time they are moved for grading or changing nets.

The accuracy of the inventory depends on how the fish are being handled.

Escapes have also occurred from net-pen salmon farms in Norway, Chile, and Tasmania.

In Norway, Gausen and Moen (1990) reported that escaped fish entered Norwegian rivers

in great numbers, but most (>20%) were found only in rivers having farms situated closer

than 20 km from the outlet. Lura and Saegrov (1991) documented the successful

spawning of farmed female Atlantic salmon in Norwegian rivers, where it is a native

species, and Lura et al. (1993) recorded some differences in spawning behavior between

a single farmed fish and wild fish. For example, the redd of the female farmed fish had

more pockets (nine versus an average of two) but fewer eggs (459 compared with an

average 707). Jonsson et al. (1991) described differences in life history and migratory

behavior between wild and hatchery-reared Atlantic salmon. In the sea, wild salmon

survived twice as well as hatchery fish, ascended the rivers earlier, and were injured less

during spawning. Hatchery-reared fish, on the other hand, stayed for a shorter period in

the rivers, and a larger proportion returned to sea without spawning.

Crutchfield (1989) reported that fishermen opposed the net-pen industry for adverse

effects of farmed fish on market prices. He recognized that this was a complex point, but

thought competition between farm and wild fish would broaden as farm salmon could be

found year-round and wild salmon in relatively narrow windows – normally four months

of the year, but much less in Washington where trollers and gill-netters were restricted.

He concluded that farmed salmon would either moderate price increases or actually cut

real-price increases for domestic wild salmon. However, he added that imports were

much greater than the supplies of equal-quality troll-caught chinook and coho. Again, his

conclusions proved to be correct, as evidenced by the imports of Atlantic salmon in 2000

which totaled over 130,000 mt with a value of $741 million (USDA 2001), mostly from

Chile and Canada.

From his economic and futuristic survey of the industry, Crutchfield (1989) indicated that

79% of wholesalers and distributors felt that fresh farmed Atlantic salmon were a direct

substitute for fresh Pacific fish, and that 26% felt that farmed Atlantic salmon competed

directly with frozen Pacific salmon. He said that exports of US wild salmon to Europe,

which was about 10–15% by value of total production, would feel the impact of farmed

salmon most severely. European smoked fish processors had all gone over to Atlantic

salmon. However, he concluded that all the conjecture was insignificant as the output of

farmed salmon in Washington in the long-term had little or no measurable effect on

prices determined by worldwide supply and demand.
16

2.4 Interactions of Farming with Recreational Activities in Puget Sound

The State of Washington Department of Licensing (WDL) reported that the number of

registered recreational boats in the State was about 250,000 (WDL 1997). This was

double the number of boats registered in 1984. A more recent statistic (PSWQAT 2001)

stated that people living in Puget Sound own more than 165,000 power boats, 21,500

sailboats, 43,500 canoes and kayaks, and numerous other watercraft. This had

necessitated the installation of 43 new pump-out stations in the Puget Sound Basin since

1994, with the construction of 15 more on line.

Goodwin and Farrel (1991) published a directory of marinas and moorage facilities in the

State in 1991, and listed 379. Kitsap County had 26 facilities and 2,968 wet moorage

slips. The 20 facilities in Kitsap County which completed the survey data offered a total

of more than 4 miles of dock and guest-dock space to recreational boats. The State's

Interagency Committee for Outdoor Recreation (ICOR) made a comprehensive field

inventory of motorized boat launches in the State in 1997 and identified 984 such sites

(ICOR 2000). The typical marina or yacht club in Puget Sound leases between 2–20

acres of aquatic lands from the State (WDNR 2001). More importantly, these facilities

displace areas which have probably been near-shore habitat for juvenile fish.

Based upon past studies of marinas for the State's Department of Fisheries, Cardwell et

al. (1980) considered reduced dissolved oxygen (DO) and increased water temperature

the greatest potential threat to aquatic life in Puget Sound marinas. Although coliform

contamination of shellfish, the leaching of antifouling paints, and the introduction of

hydrocarbons via the exhausts of outboard motors posed potential or real threats, they

stated this could all be controlled if marinas were well managed and had sufficient

flushing to prevent large temperature and DO changes. Although they recognized that

the statistical relationship between flushing and changes in these parameters measured in

the study was weak, they judged that a minimum flushing rate of 30% was adequate for

the purpose. This value was based on a 1.82 m tidal range computed for a 24-hr period.

If the marina was in an estuary where tidal ranges never attained 1.82 m, then the

minimum overall flushing rate was about 15%.

Subsequently, Cardwell and Koons (1981) documented several water quality

perturbations within marinas and moorage facilities. Pollutant inputs included runoff

from parking lots and storm drains, hydrocarbons from outboard motor exhaust, heavy

metals from antifouling paints, and biocides such as creosote and pentachlorphenol in

wood piling and docks. Indirect effects resulted from nocturnal diminutions in dissolved

oxygen due to respiration of phytoplankton blooms and diurnal elevations in water

temperature due to solar radiation.

In an earlier study on the effects of hydrocarbons on marine organisms consumed by

humans, Clark et al. (1974) exposed mussels and oysters to a diluted effluent from a twocycle outboard motor in a running seawater system. The organisms displayed

physiological stress, degeneration of gill tissue, and uptake of paraffin hydrocarbons from

the effluent. Mussels showed an immediate response to the pollutant as well as a
17

significant delayed mortality after removal. The oysters were less affected as they had

the capability of closing for longer periods of time.

Milliken and Lee (1990) carried out a comprehensive review of literature on recreational

boating and pollution dating back over 40 years. They focused on four of the principal

pollution problems associated with recreational boating, namely sewage, engine

pollution, anti-fouling paints, and plastics debris. Regarding boat sewage, they found

that, although the volume of wastewater discharged from recreational boats was small,

the organic matter in the wastewater were concentrated, and consequently the biological

oxygen demand (BOD) was much higher than that of raw municipal sewage or treated

municipal sewage. Furthermore, the concentrations built up around the marinas as they

were usually sheltered and poorly flushed. They also found that there was both a positive

and negative correlation between the density of boats and fecal coliform concentrations in

the water, but that background fecal coliform levels from overland storm-water runoff

exceeded that caused by boats.

WDFW (1997a) reported that anglers took 1.5 million trips to Puget Sound and the coast

in 1996 to catch 'food fish' – the State-designated category for salmon, sturgeon, carp,

and most marine fish. Departmental statistics in the 1996–1997 Annual Report (WDFW

1997b) indicate that 358,954 fishing licenses for food fish were sold in 1996, together

with 596,898 licenses for game fish (primarily freshwater species), and 89,393 licenses

for steelhead. Zook (1999) estimated that recreational angling for non-native game fish

contributed about $735 million annually to the State's economy.

2.5 Economic Benefits of Salmon Farming to the State

Dicks et al. (1996), in a study on the economy-wide impacts of US aquaculture,

concluded that, in 1992, the aquatic farming industry generated approximately $5.6

billion in gross domestic product (GDP) and over 181,000 jobs. Production activities

accounted for about 8% of the income and 16,500 jobs, while upstream activities, such as

equipment, supplies, feed, seed, fertilizer, labor, and financing, accounted for about 23%

of the income and 40,500 jobs. Downstream activities, such as transport, storage,

processing, manufacture, distribution, and sale of products, etc., accounted for 69% of the

income and approximately 125,000 jobs.

Stokes (1988) concluded there were many economic net gains statewide from salmon

farming in the State of Washington. In a study of 64 benefit-cost and sensitivity analyses

for ratios of gross economic gains (household income) to potential losses (adverse

property consequences), and reflecting a wide combination of data, the ratios all

exceeded unity. Average results for all calculations and results calculated under

assumptions favorable to the industry indicated substantial net economic gains. The

study had three tasks, regional input-output analysis, state fiscal analysis, and property

value analysis.

2.5.1 The contribution of salmon farming to seafood production

In its annual summary of national fisheries statistics, DOC estimated commercial

aquaculture production in 1997 of 314,657 mt (693.7 million lb) with a value of $886
18

million (DOC 1998). Total exports of edible fishery products were 915,000 mt (2.0

billion lb) valued at $2.7 billion. The total imports of edible fishery products were 1.5

million mt (3.3 billion lb) valued at $7.8 billion.

With regard to salmon, the DOC fisheries statistics estimated exports of fresh and frozen

salmon in 1997 were 86,157 mt (189.9 million lb) valued at $307.5 million. Canned

salmon exports were 37,023 mt (81.6 million lb) valued at $135.4 million. Imports of

fresh and frozen salmon in 1997 were 73,847 mt (162.6 million lb) valued at $344.4

million, and imports of canned salmon were 557 mt (28.8 million lb) valued at $4.8

million. In an early review of the economics and future of salmon farming in the Pacific

Northwest, Crutchfield (1989) concluded that a fully developed salmon industry in Puget

Sound would make a positive contribution to the economies of the region but would do

little to reduce the imbalance of international trade or even the trade in seafood. He

estimated that salmon imports were less than one-tenth of one percent of the $150 million

international trade deficit, and a salmon farming industry would have little or no impact.

USDA more recently reported (USDA 2001) that Atlantic salmon imports in 2000

reached 289 million lb (131,000 mt), as shipments increased in all three main categories

(fresh whole fish, frozen whole fish, and fresh and frozen fillets). Imports of fillets

remained the fastest growing category and made up over 50% of imports. The majority

of imports came from Chile (filleted products) and Canada (fresh fish), with Chile taking

over as top supplier with shipments rising by 51%. The value of Atlantic salmon imports

in 2000 was $741 million, and the market continues to expand.

In a comparative review of 1999, Northern Aquaculture (2000) reported that actual

production of salmon in Washington in 1999 was 5,500 mt, with a value C$38 million

(just below US$30 at that time). Production was about the same as in 1998. In Maine

production of Atlantic salmon was 12,100 mt (down 8%) with a value of C$111 million.

In Canada BC production was 47,000 mt of Atlantic and Pacific salmon (chinook and

coho). This figure was up 19% over 1998. The value was C$347, of which 86% was for

Atlantic salmon. In New Brunswick production of Atlantic salmon and steelhead was

about 27,000 mt, with a value of about C$140 million.

The Washington Fish Growers Association FGA (WFGA) reported that total production

in Washington in 1999 was 14 million lb. dressed weight (6,545 mt) of Atlantic salmon

(99%) and steelhead (1%). The total value was about $30 million. About 95% of the

farmed products were sold on the national markets as whole dressed fish, and 5% were

exported as fresh fillets (P. Granger, WFGA, personal communication).

2.5.2 The impact on employment and wages

Crutchfield (1989) predicted that a fully developed net-pen salmon industry in Puget

Sound would be useful in contributing to employment in the area but would not be a

significant factor. His prediction has proved to be very accurate.

Some earlier estimates regarding employment in the industry were rather optimistic.

Inveen (1987) suggested primary employment in a typical net-pen operation in Puget
19

Sound was 8–10 persons with an average annual wage of $19,000 (range $14,500–

30,000). Capital investment required was about $750,000–1 million, with annual

operating expenses of $1.4 million (feed 30%, labor 14%, smolts 12%, other 44%).

Assuming eight more jobs in secondary activities, the total contribution to employment

by 10 farms would be 160–200 jobs. This was similar to employment profiles in

Norway. Stokes (1988) in a report to WDFW estimated that the State economy would

gain $38–48 million in output, $11–21 million in household income, and 257–303 jobs

from the existence of five Atlantic salmon farms in the State, with typical production

figures of 1 million lb/annum and $5 million revenue. The average impact on the

(Kitsap) County for one operational site would be $5.8–6.8 million in output, $1.1–2.1

million in household income, and 40–51 jobs.

For the state of the industry in 1999, with 10 operational sites, WFGA reported current

employment in the local industry of 65 full-time positions, 5 part-time positions, and

approximately 200 more employed indirectly down the line (P. Granger, WFGA,

personal communication). By comparison, Young et al. (1998) reported 1,000 full and

part-time employees in the net-pen salmon industry in Maine, with 38 operational sites,

which equated to about 750 full-time jobs. In addition, about 500 full-time jobs in Maine

were directly dependent on contracted employment with salmon farms, such as trucking,

diving, health management, and other services. Indirect impacts of employment induced

in the local communities by salmon farms represented another 1,000 jobs.

BCSFA (2000) reported that the salmon farming industry in Canada employed 3,400

people, mostly on the BC coast. In 1999 the BC salmon industry produced 47,000 mt of

salmon valued at C$347 million.

Estimated wages for a direct employee in the industry in Washington were up to about

$45,000, and for an indirect employee about $35,000 (P. Granger, WFGA, personal

communication). These wages continued to be above average for the collective

agriculture sector (which includes forestry and fishing) in Kitsap County, which

accommodates most of the net-pen sites. Kitsap County (2000b) reported that the annual

average wage (1994) for this sector was $16,268. This was higher than the statewide

average of $13,767 primarily, it noted, because of a small number of highly paid workers

in aquaculture and fishing. However, about 70% of jobs in the collective agriculture

sector were in agricultural services industries, with the largest industries being lawn and

garden services, and non-livestock veterinarian services.

2.5.3 The impact on coastal property values

In a study of Puget Sound waters for coastal sites for net-pen fish farms, Weston (1986)

provided interim tidal velocity and water quality guidelines to minimize their impact.

Only 19 areas were identified as acceptable, relevant to specific farm capacity and the

proximity of special habitats. Five more areas, in Puget Sound Basin and beyond, were

acceptable without limitation.

Parameters relevant to the existence of shoreline industries or private properties, or any

anticipated real estate developments, were not included in Weston's early guidelines,
20

although the Basin was in the middle of major population growth and property

development. In its period summary on the health of Puget Sound, PWSWQAT (2000)

noted the Sound was currently home to almost exactly 4 million people, or double the

population of the 1960s. Annual growth was about 50,000 people (1.5%) and the

population was expected to reach 5 million people by the year 2020.

The majority of preferred net-pen farm sites identified by Weston (1986) were located in

waters around Kitsap County and Mason County. In the last 25 years (1970–1995) the

population of Kitsap County, in the middle of the Sound, has increased 116.8%,

compared with 59.1% across the State. Much of this was due to the immigration of

47,104 persons between 1980 and 1995 (Kitsap County 2000a). Property development

was a priority and principal activity, as the collective finance, insurance, and real estate

employment sector showed an increase in employment by 255% (1970–1995), of which

real estate garnered one-third of the jobs (Kitsap County 2000b).

Alpine Appraisers (1988) undertook a comparative study of visual and market effects of

net-pen fish farms on property values around Puget Sound. They concluded that floating

net-pens had no effect on upland property values in the area studied (Mason County and

Kitsap County), and that they had ‘minimal’, if any, visual impact at distances over 2,400

lineal feet. Stokes (1988), in a statistical analysis of 335 property listings and assessed

value in water-front areas throughout Puget Sound in the vicinity of net-pen complexes,

determined the average front footage price of $409 had a standard deviation of $290, half

of which could be accounted for by general location (County), land type (high-low bank),

and improvements (water, sewer, etc.). The remaining, or 'residual' price variation, was

presumed to result, at least in part, from variations in visual aesthetic quality.

Parsons (1991) studied the effect of coastal-land-use restrictions on housing prices in the

State of Maryland. He found that housing prices in the critical area with water frontage

increased by 46–62% due to restrictions, compared with 14–27% without water frontage,

13–21% for those just outside the area, and 4–11% for those three miles away. The direct

beneficiaries of coastal-land-use restrictions were the current owners of housing in the

community, while the losers were owners of undeveloped or restricted land, renters, and

future owners.

Garrod and Willis (1992) studied the effect of selected countryside characteristics on

house prices in a rural area of England covering 4,800 km2. They found that many

variables (such as within 1 km proximity to woodland, river or canal, or rural settlement)

had a positive influence on house prices of 7–10%, 4–9%, 8–12%, respectively.

Furthermore, the characteristics of an open water view or gradient slope had no

observable effect; and being close to wetlands or having woodland or urban views had

the effect of reducing house prices.

2.6 The Regulatory Structure for Commercial Enterprises

The policies and regulations (and their enforcement) for aquaculture introductions in the

State of Washington and the Province of British Columbia were reviewed and

summarized in detail by Elston (1997) in his study of pathways and management of
21

marine non-indigenous species (NIS) into the shared waters of British Columbia and

Washington. Aquaculture had been identified as one of six pathways for NIS

introductions for the study, and in his final report to the Puget Sound Water Quality

Authority, the US Environmental Protection Agency, and the Department of Fisheries

and Oceans Canada, he stated that the adequacy of information available to assess the

relative risks of introductions through aquaculture was good. This was because for more

than a decade Washington and British Columbia had in place state/provincial (and

federal) procedures specific to aquaculture. He noted that intentional introduction of

aquaculture species was then far more restricted than in the past. He stated that

technology could assist further in reducing the risk from exotic species introductions by,

for example, culturing only strains of sterile organisms. Elston concluded that the risk

from aquaculture introductions from aquaculture was well-defined, the industry was

highly regulated, and active processes were underway for continuous review of

aquaculture activities as they involved NIS.

Traditionally the policy of the State of Washington has been supportive of aquaculture.

The State was one of the first to recognize that aquaculture was a form of agriculture and

enacted legislation in 1985 which designated the Department of Agriculture as the lead

agency, with WDF responsible for disease control and prevention regulations. The

current policy of the State fosters the commercial and recreational use of the aquatic

environment for production of food, fiber, income, and public enjoyment from stateowned aquatic lands, and identifies aquaculture among legitimate uses. In its policy

implementation manual for the use of the State's aquatic resources (WDNR 2000b)

aquaculture is specifically designated as an aquatic land use of statewide value. WDNR

generally encourages this use, and it takes precedence over other water-dependent uses

which have only local interest values. While commenting on the possible environmental

impact on aquaculture by surrounding activities, and vice versa in a discussion on netpens and floating rafts, the manual states again that aquaculture remains a favored use of

state-owned aquatic lands. WDNR (1999) recently published a technical report on the

potential offshore finfish aquaculture in the State.

Amos and Appleby (1999) summarized the roles and responsibilities of the regulatory

authorities in the State of Washington with regard to the management of salmon farming

in State waters, and particularly Atlantic salmon farming. Their summary forms the basis

of the following annotations of the regulatory structure for commercial enterprises

producing either Pacific or Atlantic salmon.

(i) WDFW has management and regulatory authority over all free-ranging fish in the

State. The authority of WDFW over commercial fish culture in State waters is restricted

to disease control and protection of wildlife in general.

• The Finfish Import and Transfer Permit (WAC 220–77–030) assures that diseases,

pests, and predators are not introduced or transferred. In addition, under a legal

settlement, WDFW is required to kill and conduct biological examination of any

Atlantic salmon encountered by agency staff.
22

• Hydraulic Project Approval (RCW 75.20.100, WAC 220–120), or HPA, assures that

all construction projects ensure protection of wildlife and habitats. However, the

authority of WDFW to require HPAs of aquaculture workers at their sites is not clear.

WDFW, in association with the State of Washington Department of Ecology (WDOE)

and Department of Natural Resources (WDNR), provides guidance to state and local

agencies siting farms to avoid adverse impacts on the environment. In association with

the State Department of Agriculture (WDA), it develops disease control regulations with

regard to human health and safety.

(ii) WDOE has regulatory authority over discharges of pollutants into State waters for the

protection, preservation, and enhancement of the environment.

• The National Pollution Discharge Elimination System Permit (40 Regulation CFR,

Part 122.21), or NPDES, assures compliance with state and federal water quality

laws.

• The Water Discharge Permit (RCW 90.48) assures that discharges and wastes do not

adversely affect water quality and standards.

Under the Clean Water Act and the Water Pollution Control Act, WDOE can take

regulatory action against net-pen operators who allow Atlantic salmon to escape. This

follows the determination by the Pollution Control Hearings Board (PCHB) that Atlantic

salmon are 'pollutants.' The PCHB also adjudicates appeals over permits issued by

WDOE. In association with WDFW and WDNR, WDOE provides guidance to state and

local agencies on siting farms to avoid adverse impacts on the environment.

(iii) WDNR has regulatory authority over state-owned aquatic lands, including all

bedlands of Puget Sound, navigable rivers, lakes, and other waters. The authority also

extends over lands covered and exposed by the tide, and most shores of navigable lakes

and other fresh waters.

• The Aquatic Lands Lease (RCW 79.90–79.96), or ALL, assures the specification of

all uses of the land and the proposed facilities.

WDNR, in association with WDFW and WDOE, provides guidance to state and local

agencies on siting farms to avoid adverse impacts on the environment.

(iv) WDA is responsible for assuring the safety of the State's food supply, providing

protection from diseases and pests, and facilitating movement of agriculture products in

domestic and international markets. With WDFW it jointly develops disease control

regulations with regard to human health and safety.

(v) Local counties in the State of Washington act as lead agencies for applying the

environmental policies of the State, and the management of their respective county

shorelines.

• The State Environmental Policy Act (RCW 43.21C, WAC 197–11), or SEPA, assures

consideration of social and environmental impacts of proposed actions.
23

• The Shoreline Management Act (RCW 90.58), or SMA, assures appropriate and

orderly development of state shorelines, management of their uses, and preservation

of their natural character.

(vi) A number of federal agencies [NMFS, the US Army Corps of Engineers (ACE), US

Fish and Wildlife Service (USFWS), US Coast Guard (USCG), and the Environmental

Protection Agency (EPA)], together with respective State agencies, have management

and regulatory authority over the use of all waters by the public.

• The Section 10 Permit assures protection of public interest, including navigation,

water safety, and water quality.

(vii) NMFS administers the ESA for anadromous salmonids. It may require commercial

salmon farmers to obtain permits to take fish for their use due to the impact on listed

species. Jointly in collaboration with USFWS and WDNR, NMFS permits the use of

predator control methods (non-lethal) for birds and mammals in accordance with permit

restrictions.

(viii) The US Food and Drug Administration (FDA) is responsible for the protection of

consumers by enforcing the Federal Food, Drug, and Cosmetic Act, and several related

public health laws. It is also responsible for the safety of feed and drugs for pets and

farm animals. Salmon farmers are restricted to the use and conditions of veterinary

medicines, drugs, growth enhancers, and other chemical supplements licensed by FDA.

(ix) The Treaty Tribes of the State of Washington co-manage fisheries resources in the

State with WDFW and thus have input into disease control regulations (see (i), above).

2.7 The Regulatory Structure for Public and Tribal Hatcheries

Public and tribal hatcheries producing Pacific salmon (and other fish) in the State of

Washington must conform to the same general regulations regarding commercial

hatcheries and farms. These regulations, as described, are all concerned with protection

of the environment, or the health and safety of other plants and animals, including human

consumers. However, since 1994, when a number of Pacific salmonid species in the

region were listed for protection under ESA, there are some differences in regulations for

public and tribal hatcheries. The production of listed fish in public and tribal hatcheries

is now restricted to recovery purposes only, and not for subsequent commercial or

recreational harvest.

Certain sections of the ESA pertain to the necessary taking of listed fish for public and

tribal hatchery operations, and also for research. For example, in Section 7 of the Act,

hatcheries in ESUs where there are single listed stocks are permitted a directed take of

fish for recovery operations, and an incidental take in ESUs with mixed-stocks.

In an attempt to avoid further layering of regulations the NMFS is proposing to adopt a

new approach. Through the so-called 4(d) Rules, public and tribal authorities (and the

private sector) can develop their own conservation strategies to be approved by NMFS.
24

After approval of a specific conservation program, any activities appropriately

implemented will automatically be in compliance with the ESA and will not require

individual permitting.

As part of this approach the NMFS has been working with management agencies in the

region to develop Hatchery and Genetic Management Plans (HGMPs). The HGMP

procedure provides a thorough description of each hatchery operation, including the

facilities used, methods employed to propagate and release fish, and measures of

performance. There are also sections dealing with the status of listed stocks which may

be affected by the plan, anticipated listed-fish 'take' levels, and a description of measures

to minimize risk to listed fish. However, once completed, accepted, and followed,

hatchery managers are assured that their activities are all in compliance with ESA and no

further permitting is required.
25

3. POTENTIAL ISSUES FOR HUMAN HEALTH AND SAFETY

The third chapter is specific to the potential issues for human health and safety

from net-pen salmon farming in the Pacific Northwest region. It is sub-divided

into five parts. After a brief introduction to global and national responsibilities

for food safety, the second part deals with the chemicals and chemical

contaminants in materials used in farm production operations. Possible sources

include metallic paints, feed ingredients, and chemo-therapeutants. The third part

concerns the transmission of diseases, and the common pathogenic diseases are

reviewed. The fourth part deals with the processing and quality of farm products,

specifically the proximate composition of farm fish, and differences between farm

and wild salmon species. The final part concerns worker safety.

3.1 General Food Safety

In 1995 the members of the United Nations Food and Agriculture Organization (FAO)

formally adopted a Code of Conduct for Responsible Fisheries. The Code, which was

then published (FAO 1995), advocated safe and high quality fisheries products. Article 9

of the Code, which was specific to aquaculture, was then broken out and detailed in a

subsidiary document called, Aquaculture Development (FAO 1997). The section on

Responsible Aquaculture at the Production Level called for the global aquaculture

industry to make safe and effective use of feeds, feed additives, chemo-therapeutants, and

other chemicals, and to promote the use of aquaculture practices and methods which

reduced the hazards. As a signatory of the FAO Code, the US has ensured that its

national aquaculture industry will abide by all the intentions contained in Article 9.

The terminology used in this Chapter is adopted from the World Health Organization

(WHO) report on Food safety issues associated with products from aquaculture (WHO

1999). The terms 'hazard' and 'risk' have specific definitions. A 'hazard' is a biological,

chemical, or physical agent in food, or a condition of food, with the potential to cause

harm. A 'risk' is an estimate of the probability and severity in exposed populations of the

adverse health effects resulting from a hazard(s) in food.

The greatest risk to human health from seafood occurs from post-harvest contamination

and loss of product quality. However, this section confines its review to the risks to

human health from hazards which might be incurred in the pre-harvest production of

farm salmon raised in marine net-pens. When appropriate, it compares the risk with

products from wild harvests, other forms of aquaculture, and agriculture.

Potential hazards to food safety by the consumption of farm salmon raised in net-pens, or

by human contact with farm operations, may include:

• Toxic chemicals and chemical compounds which have been accumulated by the fish

from their aquatic environment, or from their food, or as residues from veterinary

medicines.
26

• Pathogenic organisms in the fish, such as parasites, viruses, and bacterial pathogens,

which may also be harmful to humans.

The overall risks of feed-borne human illnesses from cooked seafood (wild and cultured)

are low compared with risks from other animal products. Otwell (1989) pointed out that

the estimated risk of disease from consuming a 4–oz serving of cooked seafood was 1 in

5 million servings, but for chicken it was 1 in 25,000 servings. However, unlike other

meat products, seafood is often eaten raw or lightly cooked, and the estimated risk rises

to 1 in 250 servings for the consumption of uncooked shellfish. The risk from

consumption of uncooked fish is also higher than for cooked fish.

Primary responsibility for regulating all seafood safety, including farm products, rests

with the FDA. The FDA performs its functions by adopting BMPs, approving hazard

analysis and critical control points (HACCP) plans, and promulgating regulations.

Enforcement is primarily through inspection of handling and processing plants to ensure

compliance with BMPs, HACCAP plans, and regulations. The FDA also approves and

regulates the use of drugs and additives used in all domestic and farm animal feeds,

which includes feeds used by the aquaculture industry.

3.2 Chemicals and Chemical Contamination

Toxic chemicals and chemical compounds are accumulated by fish and shellfish from

their aquatic environment and from their food. Chemical contaminants which are

potentially hazardous to humans through seafood consumption, including farmed salmon,

are heavy metals, feed-borne toxicants, and chemo-therapeutics.

Human illnesses resulting from chemicals in the environment are more commonly

associated with long-term exposure. Jensen and Greenlees (1997) found that illness

associated with a single meal was rare. Moreover, areas of chemical contamination

tended to be concentrated in space and sometimes in time. For the most part, sensible

precautions and local regulations have ensured that fish farm facilities have been situated

where risks of chemical contamination were minimized. Sites have always been far from

industries associated with environmental pollutants and the out-fall of human sewage

treatment plants.

3.2.1 Heavy metals

Metal ions enter fish by absorption through the gills or from food. The latter is more

common. In general, fish regulate the concentrations of metal compounds in muscle

tissue within tight limits. Consequently, concentrations of inorganic metals do not

exceed regulatory limits even when the fish are harvested from environments with high

metal concentrations. The exception to this rule is tin, in the organic form of tributyl-tin,

and mercury in its organic form of methyl-mercury, which a number of sources (Cappon

1983, Jensen and Greenlees 1997, WHO 1999) indicate can be accumulated through the

food chain.
27

Tributyl-tin was commonly used as a biocide in anti-fouling paints on recreational boats

(Milliken and Lee 1990) in the marine environment. Subsequently it was used on net-pen

structures. However, due to its rapid leaching, tributyl-tin and its breakdown products

were found in the water, sediment, and in organisms where there are concentrations of

recreational boats. Later it was demonstrated that salmon in treated pens could

accumulate tin in their tissues. The use of tributyl-tin was consequently restricted in

Europe and North America, and WHO set a limit of 3.2 μg/kg body weight for tin in

humans (WHO 1999). Based on this figure, and levels of tin found in fish reared in cages

treated with tributyl-tin, a daily consumption of 150 g of salmon by a 70 kg person would

be necessary to exceed this level. At least 13 States in the US have enacted their own

legislation on the use of tributyl-tin, in addition to that of the EPA.

Methyl-mercury bio-accumulates in the food chain, and is of particular concern for longlived predatory fish. Farmed salmon live on a diet of prepared pelleted feeds, and are

usually harvested before 3 years of age so there is less opportunity for methyl-mercury to

accumulate. There are no records of farmed salmon accumulating methyl-mercury.

However, there are examples of methyl-mercury accumulation in wild salmon. Cappon

(1983) recorded mercury levels of 0.3–0.8 mg/kg in wild salmon from the Great Lakes,

which is just below the maximum permissible limit of 1.0 mg/kg.

3.2.2 Manufactured feeds

The risks to human health from feed-borne toxins have long been known, and feed

manufacturing standards, including the composition and labeling of fish feeds, are strictly

regulated by the FDA. However, the ingredients for the compounding of animal feeds

still come from a variety of suppliers, and some risks still remain. Of particular concern

for human health are certain animal byproducts, oilseed meals, grains and byproducts,

hormones, pigments, antioxidants, and most recently some organic compounds called

'dioxins.'

(i) Animal byproducts

Rendered animal protein ingredients, including various meat and bone meals, poultry

byproducts, blood, and marine processing wastes have been used for decades to replace

some fish meal in the diets of salmonids. However, the dietary inclusion levels for most

of these products have been limited because of concerns of poor digestibility, nutritional

value, palatability, and variable product quality. Efforts to avoid excessive phosphorous

levels in hatchery effluents have also limited the use of some of animal byproduct meals,

which may include relatively high levels of indigestible phosphorous from bone.

The use of rendered animal byproducts in animal feeds has been severely constrained

since 1997 by new standards imposed by FDA in the Code of Federal Regulations (CFR)

Title 21. Regulation 21 CFR, Part 589.2000 prevents the inclusion of certain mammalian

proteins in feeds for cattle and other ruminant animals. This is intended to prevent the

establishment or amplification of bovine spongiform encephalopathy (BSE) in the US by

prohibiting the feeding of protein from ruminants (such as cattle, sheep, goats, deer, elk,

buffalo, and antelope) to ruminants. Exempt from the ban is mammalian protein derived
28

from pure pork or horses slaughtered as single-species facilities, inspected meat products,

blood and blood products, gelatin, and milk products.

Feeding of mammalian proteins to fish is not prohibited by the regulation. However, the

final regulation requires feed manufacturers who handle both prohibited mammalian

protein and non-prohibited mammalian /non-mammalian protein to follow strict measures

to prevent cross contamination of feeds which may be fed to ruminants, label finished

feeds appropriately, and maintain records of ingredient purchases and disposition of the

finished feeds. Customer concerns and changes in market availability of many of these

byproducts (e.g., meat and bone meal) have effectively eliminated these ingredients from

salmonid feeds. The use of exempt products, including blood meal and byproducts of

fish and poultry processing, still continues, although levels of dietary inclusion may be

constrained by price and availability.

Studies regarding the potential for BSE transmission to humans through discharge of

BSE prions into the aquatic environment via uneaten fish feed and feces have not been

reported in the scientific literature. However, risks from a rendering plant disposing of

cull cattle carcasses in the catchment area of a chalk aquifer used for drinking water have

been examined by Gale et al. (1998). They calculated that the risk to consumers who

drank the water was remote, and an individual consuming two liters daily for 45 million

years would have a 50% chance of any infection.

(ii) Oilseed meals, grains, and byproducts

Fish meal in salmon feeds may be partially replaced by soybean, cottonseed, and canola

meals. The dietary inclusion level is governed by available content of essential amino

acids, palatability, and whether compounds toxic to the fish or anti-nutritional factors are

present. Dabrowski et al. (1989) and Sanz et al. (1994) found that soybean meal products

could replace a high percentage (25–40%) of dietary fish meal without affecting growth

of rainbow trout. However, dietary levels of some soy products were limited by the

presence of compounds which induced intestinal enteritis in Atlantic salmon (Baeverfjord

and Krogdahl 1996) and rainbow trout (Refstie et al. 2000). Salmon feeds may also

include low levels (<10%) of wheat and wheat byproducts, such as wheat middlings, as

binding agents and sources of dietary energy.

In recent years, oilseeds and grains have been modified by genetic engineering to produce

crops with increased yield and decreased reliance on herbicides and pesticides. Few

published data are available regarding their safety and nutritional value as animal feed

ingredients. Research by Hammond et al. (1996) has shown, however, that the feeding

value (nutritional value) of soybeans to rats, chickens, catfish, and dairy cattle is not

affected by genetic modifications which impart tolerance to mid-season application of the

herbicide, glyphosate.

The use of genetically modified (GM) oilseeds and grains in animal and human foods has

gained considerable attention in the US and the European Union because of uncertainties

regarding their effects on human health and the environment. Of concern are

modifications that introduce previously unknown allergens in food products, or affect
29

native plants through cross-pollination. The FDA is unaware at the present time of

scientific data indicating that foods developed through genetic modifications differ as a

class in quality, safety, or any other attribute from those developed by convention

breeding techniques. In recognition of the importance of issues surrounding the safety of

bio-engineered foods, the Codex Alimentarius Commission (established by WHO and

FAO) in March 2000 appointed the Codex Ad-hoc Intergovernmental Task Force on

Foods Derived from Biotechnology. Its mandate is to study the safety of such foods,

their effects on the conservation and sustainable use of biological diversity, and also their

effects on human health.

Safety concerns over the use of genetically modified ingredients in animal feeds have not

been substantiated scientifically. However, consumer demand for GM-free fish in the

marketplace has resulted in some feed companies producing and offering for sale only

GM-free feeds. Suppliers are required to present documentation that all ingredients are

free from any genetically modified organism (GMO).

(iii) Growth hormones

Exposure to steroids incorporated into the diet has been shown experimentally to affect

sexual development, growth, and feed efficiency of several salmonids. Piferreri and

Donaldson (1989) found experimental feeding of low doses of 17-ß-methyltestosterone to

coho fry increased the proportion of males, whereas the estrogenic steroid 17-ß-estradiol

increased the proportion of phenotypic females. Baker et al. (1988) developed a

technique for producing phenotypic male chinook salmon from mono-sex female-eyed

eggs and fry by immersion in a solution of 17-ß-methyltestosterone and water. Human

food safety and environmental issues associated with the use of 17-ß-methyltestosterone

for sex control in fish have been reviewed by Green and Teichert-Coddington (2000).

Ostrowski and Garling (1986) found that dietary 17-ß-methyltestosterone enhanced

growth of fingerling rainbow trout without affecting feed utilization. In contrast, Yu et

al. (1979) showed that low doses of androgenic steroids improved both growth and feed

conversion of juvenile coho salmon. Some synthetic steroids have been approved by the

FDA for use in the US to increase growth, feed efficiency, and milk production in cattle.

However, the use of hormones has not been cleared for food fish.

(iv) Pigments

The characteristic red color of salmonid flesh from the deposition of dietary carotenoids

is an important factor in determining product quality and consumer acceptance. In the

wild, salmonids consume prey organisms containing small quantities of astaxanthin and

other carotenoids which are deposited in the skin and muscle. Formulated feeds used in

salmonid aquaculture are usually supplemented with astaxanthin, although a related

carotenoid, canthaxanthin, is sometimes used. Astaxanthin is an approved color additive

in the feed of salmonids (Regulation 21 CFR, Part 73.35 [USOFR 1995c]). The

maximum permitted level of astaxanthin is 80 mg/kg (72 g/mt) of finished feed. The

FDA requires that the presence of the color additive in the feed, or fish which have been

colored with the feed additive, or any product which contains artificially colored salmon
30

as an ingredient, is declared on the label or ingredient list. However, this information is

unlikely to pass to the consumer when the product is displayed out of its packaging.

(v) Antioxidants

Oxidation of lipids in feed ingredients can cause a reduction in their nutritional value and

may produce compounds toxic to fish. Hung et al. (1981) found that feeds and/or

ingredients containing high levels of unsaturated fatty acids, such as fish meal and fish

oil, treated with synthetic antioxidants prevent nutrient loss and formation of toxic

peroxide compounds. Synthetic antioxidants, such as BHA (butylated hydroxyanisol),

BHT (butylated hydroxytoluene), and ethoxyquin (1,2-dihydro-6-ethoxy-2,2,4-

timethylquinoline) are commonly used in animal feeds. Maximum levels permitted in the

finished feed by the FDA is 0.2% of the fat content for BHA and BHT, and 150 mg/kg

for ethoxyquin.

(vi) Organic toxicants

Organic compounds, such as polychlorinated biphenyls (PCBs), dibenzofurans, organic

pesticides, and halogenated aromatic hydrocarbons, etc., have all been found in wild

salmon from polluted areas, such as the Great Lakes (Cleland et al. 1987, Cleland et al.

1989, Daly et al. 1989, Seegal 1999) and the Baltic Sea (Svensson et al. 1991). Recently,

media reports on the presence of 'dioxins' in farmed salmon have gained considerable

attention, particularly among consumers in the United Kingdom and other EU countries.

Dioxin exposure is of concern because of potential effects on the immune and endocrine

functions and reproduction, as well as the development of malignant tumors (SCAN

2000).

The term dioxins describes three classes of toxic chemical compounds widely distributed

and persistent in the environment. They tend to dissolve in lipids and thus can be

accumulated in the food chain. The groups are polychlorodibenzo-p-dioxins (PCDDs),

polychlorodibenzofurans (PCDFs), and dioxin-like or co-planar biphenyls (PCBs).

PCDDs and PCDFs are by-products of certain industrial processes, such as hightemperature waste incineration, and/or those involving organic chlorine treatments

(bleaching paper during manufacture, synthesis of herbicides). PCBs were used mainly

in electrical equipment beginning in the early 1930s until their manufacture and use was

stopped in almost all industrialized countries by the late 1980s. Of the 210 possible

PCDF and PCDD congeners, 17 are considered toxic. Twelve of the 209 members of the

PCB family show dioxin-like toxicity.

The overall toxicity of a dioxin-contaminated materials or food is an additive function of

both the quantity of each congener present and its toxicity, relative to the most toxic

compound 2,3,7,8-TCDD (Seveso-dioxin), expressed as total toxic equivalents (TEQ).

WHO has proposed a tolerable daily intake (TDI) for humans of 1–4 pg WHO-TEQ/kg

body weight (Van Leeuwen and Younes 2000), with the ultimate goal to reduce human

intake levels below 1 pg TEQ/kg body weight per day. More than 90% of human dioxin

exposure is derived from food, with food of animal origin as the predominant (ca. 90%)

source. Consequently, recent efforts to reduce human dietary exposure to dioxin and

PCBs has focused on evaluating the contribution of various feed ingredients given to
31

farmed animals, including fish, and the contamination of human food products of animal

origin (SCAN 2000).

Data collected by the SCAN (2000) on basic feed ingredients (roughages, grains and

cereals, vegetable oils, animal fat and other rendered by-products, fish meal and fish oil,

as well as binders and trace element premixes) indicated that virtually all are

contaminated with dioxin to varying degrees. Feedstuffs originating from plants

generally contain low levels of dioxins (0.1–0.2 ng WHO-TEQ/kg dry matter), while fish

meal and oil, particularly those originating from European sources are highly

contaminated (fish meal 1.2 ng WHO-TEQ/kg dry matter, fish oil 4.8 ng WHO-TEQ/kg

dry matter). European fish meals and oils are about 8-fold lower in total dioxin content

than those produced from species caught in the coastal areas of less-industrialized regions

of the world (Peru, Chile). Because of the high percentage of fish meal and oil in the

diets of farmed carnivorous fish, such as salmon, the impact of using less contaminated

feed materials of fish origin on whole diet dioxin burden is considerable. According to

SCAN estimates, a typical diet for carnivorous fish containing 50% fish meal and 25%

fish oil originating from Europe might contain 1.82 ng WHO-TEQ/kg dry matter,

compared with 0.25 ng WHO-TEQ/kg dry matter if fish products from the south Pacific

were used. Further reductions may be realized by partially replacing fish meal and oil

with plant products, such as soybean meal and vegetable oils.

Little is known about transfer of dioxins from feed to fish. However, based on limited

data on transfer rates for PCBs in fish, and assuming similar behavior of ortho and nonortho cholorobiphenyls, SCAN estimated at least 60% of the total dioxin + PCB TEQ in

fish feed is likely to be transferred to fish. At present, the level of dioxin contamination

in farmed salmon has not been rigorously evaluated, and transfer rates to humans have

not been determined. However, it is likely that guidelines for tolerable limits for dioxin

in all human food products or animal origin will soon emerge.

While the potential for feed-borne hazards from organic compounds exists in farmed

salmon, Jensen and Greenlees (1997) note that this public health issue is largely avoided

in aquaculture by application of best management practices (BMPs) for site selection, and

regulations for formulation and manufacture of feeds.

3.2.3 Chemotherapeutants

Toxic chemicals and chemical compounds may residualize in fish following protracted

use of approved veterinary medicines. Aquaculture, like terrestrial animal agriculture,

relies upon good husbandry and proper use of drugs and chemicals to combat infectious

disease pathogens. Of the chemotherapeutants approved for use in aquaculture, certain

antibiotics and parasiticides are used in salmon net-pen farming.

(i) Antibiotics

Antibiotic residues in farmed seafood products are possible hazards to consumers in that

they might induce allergic reactions, have toxic effects, or modify the human gut flora.

They might also increase resistance in aquatic bacteria to antibiotics, which in turn, might

be transferred to human pathogens.
32

All drugs approved by the FDA must be shown to be safe and efficacious. Studies

required to meet these requirements typically consist of field (clinical) and laboratory

(non-clinical) trials (USOFR 1995a). Clinical studies are conducted under an

investigational new animal drug (INAD) exemption issued by FDA under the same

conditions expected under the proposed use of the drug. Laboratory studies under strictly

controlled conditions in accordance with good laboratory practices (GLP) are specified

under the Regulation 21 CFR, Part 58 (USOFR 1995b). Laboratory studies conducted

for the approval of a new animal drug for use in US aquaculture have been reviewed in

detail by Greenlees (1997).

The FDA permits certain antibiotics to be added at sub-therapeutic levels to the feeds of

poultry, swine, and cattle as growth promoters. It does not permit the use of antibiotics

as growth promoters for fish. In contrast with the results obtained with higher

vertebrates, Wagner (1954), Sniezko and Wood (1954), and Sniezko (1957) reported that

sulfonamide, tetracycline, and other antibiotics added to the diets of several salmonid

species (brook trout, brown trout, and rainbow trout) had no stimulatory effect on growth.

At the present time three antibiotics are registered in the US as feed additives for disease

control under Regulation 21 CFR, Parts 558.450, 558.575, and 558.582. Respectively,

these are oxytetracyline (terramycin), sulfadimethoxine plus ormetoprim (®Romet-30),

and sulfamerazine, although sulfamerazine is no longer marketed. For salmonids,

oxytetracyline (terramycin) has a 21-day withdrawal period before harvest, and ®Romet30 has a 42-day withdrawal period. Stoffregen et al. (1996) stated that levels in flesh

tissues were undetectable if these withdrawal times were followed. Fong and Brooks

(1989) determined that the tolerance levels of salmon for each of these antibiotics were

0.1 ppm.

(ii) Parasiticides

JSA reviewed the use of chemical compounds and vaccines in aquaculture and published

their findings in a guidebook (JSA 1994). Seafood producers operating by the JSA

guidelines introduce no hazards from residual drugs. The risk is the misuse of chemical

compounds and vaccines by untrained workers.

Formalin is the only parasiticide approved at present for farm salmon operations (JSA

1994). It is applied topically, and Fong and Brooks (1989) were unable to detect it in

salmon flesh after treatment, concluding that it was not a hazard to consumers. Other

substances with putative activity, including acetic acid, garlic, hydrogen peroxide, onion,

and sodium chloride, are currently classified by FDA as 'unapproved drugs of low

regulatory priority.' The FDA is unlikely to object to use of these substances if the

following conditions are met: (a) the drugs are used for the prescribed indications,

including species and life stage where specified, (b) they are used at the prescribed

dosages, and (c) are used according to good management practices. Also, (d) the product

is of an appropriate grade for use in food animals, and (e) an adverse effect on the

environment is unlikely. However, the use of such substances under these conditions is

not approval or affirmation of their safety and efficacy, and the FDA may take a different

position on their use in the future based on further information.
33

3.3 Biological Safety

Potential biological hazards to human health from the consumption or contact with

contaminated farm products include parasites, bacterial infections, viral infections, or

naturally produced toxins. The majority of human pathogens associated with aquaculture

products are to be found at freshwater farms, farms in tropical countries, and among

shellfish operations.

Specific hazards to human health which might be associated with net-pen farming of

salmon are anisakiasis, diphylobothriasis, rickettsialosis, vibriosis, aeromonasis,

salmonellasis, and plesiomonasis. To date there have been no reported cases of any of

these hazards being associated with farmed salmon, and WHO (1999) states that the risk

of contracting these illnesses from farmed fish is considered to be low.

(i) Aniskiasis

Anisakiasis is caused by larval ascaridiod nematode parasites which normally infect

marine mammals as the definitive host, and an invertebrate as the primary host. Marine

fish are secondary hosts, and are infected when they consume infected fish or

invertebrates. Roderick and Cheng (1989) indicated that the parasite inhabits the viscera

of live fish but relocated to the musculature upon death. They concluded that the parasite

is not likely to be a problem in farmed fish, as the viscera are removed quickly after

harvest. The parasite is killed by proper cooking or proper freezing, and only

infrequently infects humans. Human infection of this and other parasites primarily

occurs when wild fishery products are consumed raw, as in Japanese maguro (tuna) or

sake (salmon) sashimi, or after only mild processing, such as cold smoking.

Studies by Angot and Brasseur (1993), Bristow and Berland (1991), and Deardorff and

Kent (1989) have indicated that farmed salmon do not have nematodes. Consequently

the European Union (EU) exempts farmed salmon from a directive (91/493/EEC) which

requires that all (wild) Atlantic and Pacific salmon to be processed with minimal cooking

(i.e. cold smoking <60oC) must be frozen prior to sale. This is to protect the consumer

from anisakiasis and other parasites. The reason that farmed salmon are apparently free

of nematodes is that they are fed with manufactured feeds. If farmed salmon were fed

with fresh trash fish, WHO (1999) believes that the potential for aniskiasis from farmed

salmon would exist.

(ii) Diphylobothriasis

Diphylobothriasis is caused by the broad fish tapeworm, Diphyllobothrium latum. While

the majority of human infections of this parasite come from freshwater fish, Roderick and

Cheng (1989) described cases caused by the consumption of uncooked wild salmon.

They assumed that the salmon contracted the tapeworm in freshwater and carried the

parasite throughout the marine phase before capture. Diphylobothriasis is common found

among Eskimos of Alaska and Canada and inhabitants of Finland, all of whom consume

large quantities of wild caught salmon. There have been no reports of this tapeworm

associated with farmed salmon.
34

(iii) Rickettsialosis

Rickettsialosis, or 'salmon poisoning,' is caused by a digenean troglotrematid and is

primarily a problem for dogs, which have eaten uncooked wild salmon entrails. Rodrick

and Cheng (1989) described reports of this parasite in humans but rarely with serious

disease consequences. There have been no reports of this parasite associated with farmed

salmon.

(iv) Vibriosis and other bacterial diseases

Vibriosis, aeromonasis, salmonellasis and plesiomonasis are caused by bacterial

infections of Vibrio spp., Aeromonas spp. Salmonella spp. and Plesiomonas spp.,

respectively. All of these bacteria are a part of the normal aquatic flora, except for

Salmonella spp. which are associated with human and animal wastes.

The greatest potential for contamination of wild or farmed fish occurs post-harvest when

the muscle, which is sterile in healthy living fish, is exposed to external contamination.

The practice of delivering net-pen reared salmon alive to the processing plant, where

strict BMPs and HACCP practices are followed, significantly reduces the risk to public

health from bacteria and parasites. Wild caught salmon, which are landed headed and

gutted, have a slightly higher risk of contamination en route to the processing plant.

Ward (1989) noted that all these bacteria were killed by thorough cooking, and concluded

that the greater risk for the consumer was uncooked or undercooked fish, or if the product

was incorrectly handled and processed after harvest.

3.4 Quality and Safety of the Products

The public perception of seafood has traditionally been one of high quality, with a range

of products all beneficial to individual health. However, there are subtle differences

between species, and many of the positive healthy qualities can be destroyed or

contaminated by poor post-harvest handling and processing.

The proximate composition of farmed salmon (percent protein, lipid, ash and water) is

generally similar to wild salmon, except that the lipid and fatty acid composition can

differ. In general, wild salmon have a higher concentration of n-3 fatty acids as a percent

of total fat, while farmed salmon have a higher level of total fat. Sargent (1995) found

there was a similar overall level of n-3 fatty acids as a percentage of the total fillet, which

was important for human health. The fatty acid composition of farmed fish reflects the

fatty acid of the lipid source in the feed. Many authors (Nettleton 1990, Haard 1992,

Nettleton and Exler 1992) have experimented with an array of variables and all report

that it is possible to control the fatty acid composition of farmed fish.

Many food nutritionists have worked on the various sensory measures of farmed salmon,

such as taste, texture, and color of the final product. Haard (1992) reported that farmed

salmon, in general, were milder in flavor, softer in texture, and paler in color than their

wild counterparts. Sylvia et al. (1995) and Wessells and Holland (1998) noted that

consumers were able to detect differences between wild and cultured salmon, with

preferences related to regional experience with each product. The greatest determinant of

product quality for salmon from either source was freshness. Consistency in quality and
35

quantity, consistent price, and year-round availability were all considered by consumers

to be advantages of farmed salmon.

3.5 Worker Safety

According to the Bureau of Labor Statistics Census of Fatal Occupational Injuries (CFOI)

commercial fishing was the single most deadly occupation in the US between 1992 and

1996 (CFOI 1999). This is likely to still be the case. Drudi (1998) concluded that fishers

face a risk of death 20–30 times higher than all other occupations. Between 1992 and

1996 inclusive, 380 fishermen fatalities were recorded in the USA. During the same

period the occupation classified as 'Animal aquaculture' (SIC 0273) had eight fatalities,

and 'Fish hatcheries and preserves' (SIC 0921) had five fatalities (D. Drudi, personal

communication, 2000). It was not possible to isolate salmon fishers and salmon farmers

from within these numbers.

Fish farm workers face chemical hazards from mishandling drugs and chemicals used in

aquaculture. Guidelines for the use and safe handling of chemical compounds and

vaccines in the aquaculture industry in the US have been published by JSA (JSA 1994),

and many of these guidelines are being reflected by the COPs and BMPs being prepared

by individual industries for the protection of their workers.
36

4. SALMON FARMING AND THE ENVIRONMENT

The fourth chapter reviews current information on the effects of the many

activities associated with salmon aquaculture on the environment. Where

possible the review attempts to deal with these effects in quantitative terms,

and the measures which are currently used to reduce them. The chapter has

seven identified sub-sets. The first sub-section reviews the potential effects of

the organic wastes emanating from net-pen salmon farming. The origins of

such effects are uneaten or waste feed, feces from the fish, and bio-fouling

organisms on the structures. The second sub-section reviews the inorganic

wastes, specifically nitrogen and phosphorus, and heavy metals. The third subsection deals with the pathogenic organisms, which might be in the vicinity of

fish farms, and the risks to human health from wastes, which might contain

such pathogens. The next sub-section deals with the therapeutic compounds

which might be used to control parasites and diseases. The fifth sub-section

reviews the biological and chemical changes in the sediments and in the water

column both beneath the farm and downstream. Where possible, quantitative

information is provided and then applied collectively in terms of an operating

farm with reference points. The sixth sub-section reviews information on the

chemical and biological recovery of sediments under salmon farms. The final

sub-section reviews alternatives being used for management of all these

environmental effects. These include monitoring experiences with a number of

indicators and models, followed by a review of other government policies and

methodologies.

4.1 The Effects of Organic Wastes from Net-pen Salmon Farms

4.1.1 Waste feed

Early diets for farmed Atlantic salmon contained 45–50% protein, 16–22% lipids, and

17% carbohydrates. Technology now permits the production of high-energy salmon diets

containing about 30–35% lipids and 40% protein, and the minimum level of digestible

carbohydrate (about 10%) necessary to bind the pellets. These high-energy diets more

closely resemble the composition of the natural prey of salmon. More recent salmon

feeds were reported by Einen at al. (1995) and Rosenthal et al. (1995) to contain 7%

nitrogen and 1% phosphorus. Mann (EWOS Canada Ltd., personal communication)

estimates that current salmon diets contain 38–39% crude protein, 6.5% nitrogen, and 1%

phosphorus. Lipid content in current high-energy diets is 33–35%, of which half is fish

oils and half plant oils, such as flax and linseed oils, high in omega-3 fatty acids.

The amount of waste feed depends on feeding efficiency, which is principally influenced

by feed composition, feeding methodology, water currents at the site, and net-pen

configuration. Beveridge et al. (1991) stated that up to 30% of feed was lost. Rosenthal

et al. (1995) noted higher losses (up to 35%) for wet feeds, which might contain greater

than 30% moisture, than dry feeds. Weston (1986) suggested that less than 5% of dry

feed was lost at Puget Sound salmon farms. This is consistent with research by Gowen
37

and Bradbury (1987), who reported losses were least (1–5%) with dry feeds, which

contained less than 10% moisture. Findlay and Watling (1994) reported maximum feed

loss rates of 5–11%, with an average feed wastage of <5%. Dry and semi-moist feeds are

now used exclusively in the Pacific Northwest and current feed loss rates are estimated

between 3–5 % (J. Mann, EWOS Canada Ltd., personal communication).

The amount of feed loss is also dependent on feeding methods and strategies. Cross

(1990) reported that feed wastage at a commercial salmon farm in Sooke Inlet, British

Columbia (BC) was 3.6% delivered by hand and 8.8% delivered by automatic feeders.

This was probably due to the abrasion of feed pellets in some automatic feeders, which

can result in the disintegration of 4–5% of the pellets. Other automated feeding systems,

with short delivery distances and operated by compressed air valves, may disintegrate

<0.5% of the pellets (J. Mann, EWOS Canada Ltd., personal communication).

New technologies, such as feedback cones and underwater video or acoustical devices

described by Mayer and McLean (1995), are now commonly used to monitor feeding

behavior in efforts to minimize losses of uneaten feed from net-pens. Sutherland et al.

(2000) conducted a study at a salmon farm in the Broughton Archipelago, Canada BC, to

quantify suspended particulates during peak feeding times and to make point-in-time

estimates of organic loading. Based on stable carbon isotope analysis, they concluded

that very little feed was not consumed by the fish at the farm under study. In a series of

video reports to the BC Ministry of Environment documenting the environmental

conditions on the perimeter of several salmon farms in the Province, Brooks (2000a–f)

recorded no observable wasted feed pellets.

The results of this review are reasonably consistent and indicate that, as at this time, 5%

or less of the dry feed delivered to cultured salmon in net-pens is lost to the environment.

The low proportion has been due to the combination of improved feedback technologies

and the practice of quickly feeding the fish to satiation once or twice each day (mean

feeding). Improvements in feed delivery systems to minimize pellet disintegration will

probably reduce losses further well below 5%, a figure much less than the 20–30%

numbers used in many aquaculture models (see Section 4.7.2).

4.1.2 Fish feces

Weston (1986) estimated that 25–33% of feed consumed by the fish was ejected as feces.

Modern diets are approximately 87–88% digestible (J. Mann, EWOS Canada Ltd.,

personal communication). The remaining ash consists primarily of calcium and inorganic

phosphate, and represents 8.0–8.5% of the feed. This implies approximately 12.5% of

the weight of ingested feed will be ejected in feces. Subtracting 87.7% for digested

protein and 8.25% for ash, this leaves about 4% of the feed ingested to be ejected as

labile organic material in the feces. If 5% of the feed is uneaten (Findlay and Watling

1994) and feces contribute organic matter equivalent to 4% of the feed weight, then

approximately 8.8% of the labile organic carbon delivered in feed is discharged from the

net-pen structure in particulate form, contributing to the BOD of the sediments.
38

Feed conversion ratios (FCRs) of farmed fish are frequently quoted in literature, but have

not been adequately defined. They are typically measured as the ratio of the dry weight

of feed provided to the wet weight of salmon produced. They are considered an essential

metric by the aquaculture industry for assessing producer program efficiency. The FCR

is affected by genetic and environmental factors. The quality and composition of the

feed, to include palatability and nutrient balance, is also important together with fish

health and feeding methodologies. In short, the FCR integrates all aspects of the culture

operation into one simple metric.

Two types of FCR are typically defined by industry:

• The economic feed conversion ratio (EFCR) is defined as the amount of feed supplied

to a farm divided by the round dressed weight of fish produced for market. This

metric is easy to calculate and is useful in determining the economic efficiency of a

farm.

• The biological feed conversion ration (BFCR). This metric is biologically and

environmentally more meaningful but more difficult to determine. It is equal to the

feed actually consumed by the fish (feed provided less the uneaten portion) divided

by the total fish biomass produced on the farm, including escapes and mortalities.

Robinson (Stolt Sea Farm, personal communication) noted that the head-on processed

weights must be corrected for the approximate 16% loss of fish weight during

starvation, bleeding and removal of offal.

Enell and Ackefors (1992) reported that marine FCRs in Norway declined from 2.25 in

1974 to an average of 1.2–1.3 in 1992. The authors calculated that improvement resulted

in a 23% decrease in nitrogen and a 50% decrease in phosphorous loading associated

with farm operations. Rosenthal et al. (1995) estimated FCRs for Atlantic salmon to be

1.2, while Levings (1997) estimated an even lower FCR of 1.17 for operations in BC.

FCRs have probably advanced to a point where significant additional improvement will

be difficult.

4.1.3 Fish carcasses as wastes

Winsby et al. (1996) reviewed and analyzed the mortality of fish at BC net-pen salmon

farms in 1994. Their data suggested approximately 2,000 mt of salmon died at farms that

year, or approximately 9% of the total production of 22,000 mt. They concluded that

most of the salmon carcasses were removed to approved compost disposal locations.

No inappropriate disposal of salmon carcasses has been documented in the literature.

Losses of fish on net-pen salmon farms are restricted to individual fish, which may have

been attacked and killed by a predator, and numbers of fish which died as a consequence

of an algal bloom or disease epidemic. BMPs of net-pen salmon farms require physical

removal of any carcasses on a daily basis, and therefore they do not contribute to any

biological loading on the environment.

4.1.4 Bio-fouling organisms as wastes

Biological fouling is a significant factor in coastal environments and large masses of

mussels, barnacles, ascidians, and bryozoans can weigh down nets and restrict water flow
39

through a net-pen complex. Heavily fouled nets can also compromise the structural

integrity of the complex.

Weston (1986) concluded that bio-fouling organisms on net-pens, and the debris which

was released by net cleaning, were not significant sources of organic input to sediments

beneath salmon farms. Winsby et al. (1996) discussed the mechanics of removing

fouling organisms from nets associated with salmon farms. There is no literature

quantitatively describing the mass of bio-fouling which builds up on nets and floating

structures of salmon farms, or other similar marine structures.

Brooks (1994a) defined a neutral impact zone (NIZ) as that distance from the perimeter

of a salmon farm at which there was neither an apparent increase nor decrease in the

abundance and diversity of the benthic infaunal community when compared with a local

control site. In annual observations at a poorly flushed farm site, he noted that the NIZ

was influenced by several factors, including, for example, deposits of debris following

the pressure-washing of nets in situ. He observed a 30-cm deep layer of mussel debris in

sediments from the perimeter of the farm stretching a distance of 6 m downstream. The

downstream location of the NIZ increased from 12 m in 1993 to approximately 22 m in

1994, after in situ cleaning. He concluded that it was not possible to establish a cause

and effect relationship but the presence of the mussel shells undoubtedly had an effect on

the benthos.

4.1.5 Measurement of organic wastes

Brown et al. (1987) compared the areal extent of benthic impacts associated with organic

wastes from fish farms in Sweden with that from sewage treatment plant and pulp mill

effluents. They found reducing (anaerobic) sediments covering 0.6 km2 around a poorly

flushed (mean current velocity = 3.7 cm/sec) salmon farm located in shallow water (20 m

below MLLW). Significant changes in the benthic community were observed within 15 m

of the perimeter of the farm. In comparison, they cite Stanley et al. (1980) in noting that

a pulp mill in Loch Eil, Scotland had created reducing conditions in sediments extending

over an area of 5 km2. Pearson (1986) observed reducing sediments covering 23 km2

associated with a sewage disposal site at Garroch Head, Firth of Clyde, Scotland. The

impact associated with this single sewage discharge covered an area 38 times as large as

that impacted by the salmon farm.

Ellis (1996) suggested that waste feed and feces from salmon farms in BC were

equivalent to the human sewage from a city of 500,000 people, and Folke et al. (1994)

compared the waste from 100 mt of salmon with a human settlement of 850 to 3,200

persons. Ackefors and Enell (1990) criticized the assumptions upon which such

comparisons were made. Their argument was based on differences in the form of

nitrogen released from sewage treatment plants and fish farms and differences in the ratio

of carbon, nitrogen and phosphorus discharged from the two activities.

Taylor et al. (1998) found that organic enrichment adjacent to the Macaulay and Clover

Point outfalls in the city of Victoria BC, was similar to that expected at a productive

salmon farm. Adverse effects on benthic infauna associated with organic enrichment by
40

sewage treatment plants were generally restricted to distances less than 100 m from the

diffusers. They also found significantly elevated levels of 1,4-dichlorobenzene,

polycyclic aromatic hydrocarbons and mercury within 100–400 m of the same two

outfalls. These concentrations exceed Washington State Sediment Quality Standards.

Sediment toxicity associated with these outfalls was limited to adverse effects on growth

and development in laboratory bioassays. The authors concluded that the magnitude and

extent of the observed effects (<400 m from the outfalls) indicated little cause for concern

for human health. The effects at these outfalls extend four times further from the source

than is allowed at salmon farms complying with the BC Draft Waste Management Policy.

Salmon farm wastes do not contain toxic levels of metals and industrial hydrocarbons

associated with sewage treatment plants, and there are no reasonable sources of these

common contaminants on farms other than the minor exhaust from boats.

Ackefors and Enell (1994) estimated the total organic output from salmon farms on the

order of 2.5 mt wet weight per metric tonne of fish produced. Gowen et al. (1991) cited

three studies assessing the flux of carbon through salmon net-pens. In all three cases the

harvested fish retained 21–23% of the carbon in feed and it was estimated that 75–80 %

of the carbon was lost to the environment mostly in a dissolved form as CO2. Merican

and Phillips (1985) estimated that 35.6% of the carbon, 21.8% of the nitrogen, and 65.9%

of the phosphorus were lost to the environment in solid form. Other estimates of the total

suspended solids output from intensive net-cage culture of fish by Kadowaki et al.

(1980), Warrer-Hansen (1982), Enell and Lof (1983), and Merican and Phillips (1985)

range from 5–50 g suspended solids/m2-day. All these publications are more than 15

years old and therefore these values do not reflect recent improvements in fish feed and

feeding technologies.

Gowen and Bradbury (1987) estimated organic waste sedimentation rates of 27.4 g/m2-

day under Irish salmon farms, and an average of 8.2 g/m2-day immediately adjacent to

the perimeter of the net-pen. Gowen et al. (1988) measured average rates of 82.2 g dry

weight/m2-day on the perimeter of a net-pen in Washington, and Cross (1990) estimated

an average overall sedimentation rate of 42.7 g TVS/m2-day with a maximum of 94.5 g

total volatile solids (TVS)/m2-day at seven salmon farms in BC. More recent work by

Findlay and Watling (1994) in Maine measured sedimentation rates on the perimeter of

salmon farms at between 1.0–1.6 g carbon/m2-day, and Hargrave (1994) summarized

sedimentation rates from less than one to over 100 g carbon/m2-day from salmon cage

operations described by a number of authors.

Brooks, using his published data from many original sources (Brooks 2000a–f), derived a

theoretical estimate of contemporary TVS loading near fish farms. Given a feed with

11% moisture content and FCR of 1.2, the feed provided (1.2 kg x 89 % dry matter) or

1.07 kg dry feed/kg of fish produced. This:

– [(1.07 kg dry wt. feed/kg salmon produced) x 8.8% labile organic waste/dry weight] –

was in turn equal to 0.094 kg of labile volatile solids/wet weight kg of fish produced.

Thus he estimated that a salmon farm producing 1,500 mt of salmon during a 16 to 20-

month production cycle would discharge 141 mt of organic waste on a dry weight basis.
41

Furthermore, assuming a fish density of 10 kg/m3 in cages 15 m deep and a grow-out

cycle of 18 months, the annual sediment load on average would be:

(10 kg fish/m3 x 15 m deep x 0.094 kg TVS/kg fish)

(548 days)

which is equal to 25.7 g TVS/m2-day. The load would, in reality, be lower at the

beginning of the grow-out cycle and increase towards maximum biomass.

Brooks (2000e) analyzed sediments collected in canisters deployed 5 m above the bottom

at varying distances from two farms in BC and at reference stations. The mean loading

of volatile solids on the perimeter of these farms was 39.2 g TVS/m2-day. The mean

deposition of volatile material at the control stations was 6.3 g TVS/m2-day and the

contribution by the farm was approximately 32.9 g TVS/m2-day. These studies were

completed near peak salmon biomass and the observed values would therefore be greater

than the theoretical average of 25.7 g TVS/m2-day calculated above. Nonetheless, these

observed and theoretical values are reasonably close.

In summary, sedimentation rates on the perimeter of salmon net-pens have remained

fairly constant in the range 15.1–100 g TVS/m2-day despite the typical increase in farm

size from 200–300 mt in the 1980s and early 1990s to the 1,500 mt of recent years. A

recent study by Brooks (2000e) found a TVS loading of 32.9 g/m2-day on the perimeter

of a salmon farm at peak production. This value is reasonably close to a theoretical

average of 25.7 g TVS/m2-day calculated for an entire 18-month production cycle.

4.2 Dissolved Inorganic Wastes

4.2.1 Dissolved nitrogen and phosphorus

Salmon excrete 75–90% of their ammonia and ammonium waste across gill epithelia

(Gormican 1989) or in concentrated urea (Persson 1988, and Gowen et al. 1991). Brett

and Zala (1975) reported a constant urea excretion rate by sockeye salmon of 2.2 mg

N/kg per hour. Nitrogen and phosphorus are also dissolved from waste feed and feces

during and after descent to bottom sediments. All these dissolved forms of nitrogen are

readily available for uptake by phytoplankton. Silvert (1994a) suggested that 66–85% of

phosphorus in feed is lost in a dissolved form to the environment at salmon farms.

Winsby et al. (1996) reported significant variation in observable increases in soluble

nitrogen and phosphorus levels in the water column at salmon farms. Johnsen and

Wandsvik (1991) and Johnsen et al. (1993) estimated that 20.5–30.0 g of nitrogen and 6.7

g of phosphorus are released per kilogram of Atlantic salmon produced when fed modern

high-energy diets containing 30% lipid. Levings (1997) used these estimates to conclude

that 844 mt of nitrogen and 188.6 mt of phosphorus are released to marine environments

in BC each year by salmon farms. These values do not include nitrogen and phosphorus

associated with uneaten feed.

Statistically significant increases in soluble nutrients at salmon farms have infrequently

been observed in Puget Sound (Rensel 1989, and Brooks 1994a, 1994b, 1995a, and

1995b). Aquatic Lands Leases (ALLs) for salmon farms in Washington State have

required monitoring of NO3, NO2, and total ammonia (NH3 + NH4) in water samples
42

taken within one hour of slack tide at stations located 30 m up-current, and 6 m and 30 m

downstream at all permitted farms at a depth equal to one-half the depth of the

containment nets. In general, the variability between replicate samples taken at the 6 m

downstream station was as great, or greater, than any observed increase in nitrogen

between upstream and downstream stations. No significant increases in nitrogen were

observed at any of the 30 m downstream stations.

The highest observed level of toxic unionized ammonia (NH3) was 0.0004 mg-L-1. This

is lower (by a factor of 87.5) than the EPA chronic exposure (4-day) concentration limit

of 0.035 mg-L-1 at pH = 8 and T = 15oC when sensitive salmonid species are present.

Rensel (1989) studied dissolved nitrogen production at two poorly flushed farms in

Washington. He compared dissolved nitrogen and unionized ammonia concentrations

within the salmon pens with upstream and downstream levels during early ebb tides.

Upstream dissolved nitrogen levels of 0.0003 mg-L-1 were increased to 0.0023 mg-L-1 at

the center of the net-pen complex, but decreased to background levels at downstream

stations. He also observed maximum unionized ammonia levels equivalent to 6% of the

EPA criteria in the center of these net-pen complexes during slack tide.

Weston (1986) reported ambient levels of dissolved inorganic nitrogen (DIN) in Puget

Sound at 0.3 to 1.9 mg-L-1, indicating high variability. The greatest increase in DIN

reported by Brooks (1991, 1992, 1993a, 1994a, and 1995a) was 5.29 μmoles-L-1 (0.09

mg-L-1), or 8% of the mean value reported by Weston (1986).

The literature indicates that the concentration of dissolved inorganic nitrogen added to

marine water at salmon farms is very low on the perimeter of net-pen farms, and

essentially immeasurable at distances greater than 9 m from the farm perimeter.

4.2.2 Heavy metal accumulation in sediments

(i) Zinc

Zinc is an essential metal important for insulin structure and function and as a co-factor

of carbonic anhydrase. Historically it has been added to salmon feeds in trace amounts

equal to 30 to 100 mg-kg-1 of feed (see Chow and Schell 1978, and Anderson 1998).

Long et al. (1995) provide an effects range-low (ER-L) of 150 μg zinc/g dry sediment

weight, an effects range-moderate (ER-M) of 410 μg/g and an overall apparent effects

threshold (AET) of 260 μg/g. The Washington State sediment quality criterion for zinc is

270 μg Zn/g dry sediment (WAC 1991). Other available benchmarks include the (TEL +

PEL)/2 or 197.5 μg Zn/g dry sediment. Information on the development of the threshold

effects level (TEL) and the probable effects level (PEL) can be found in MacDonald

(1994). The published sediment benchmarks (in μg Zn/g dry sediment) are summarized

below. It should be noted that only the WA State AET is a statutory criterion.

Contaminant NOAA AET (TEL + PEL)/2 WA State AET

Zinc 260.0 197.5 270.0
43

Brooks (2000b) summarized 193 analyses for zinc in sediments collected near 27 salmon

farms in BC. Nineteen samples from eight farms exceeded the AET of 260 μg Zn/g dry

sediment. All of the high zinc samples also contained significantly elevated sediment

sulfide and TVS concentrations. There was a statistically significant correlation between

zinc and both TVS and total sediment sulfides (S=).

In response to the observed high sediment zinc concentration as some farms, fish feed

manufacturing companies in BC have reduced the amount of zinc in feed to the minimum

necessary to maintain salmon health. They have also changed the form of zinc from zinc

sulfate to a methionine analog, which is more bio-available.

Di Toro et al. (1992) described the relationship between sediment acid volatile sulfides,

metal concentrations, and toxicity to infauna. Acid volatile sulfides (AVS) is a reactive

pool of solid-phase sulfide that is available to bind metals and render them biologically

unavailable and non-toxic to biota. The AVS method is useful in predicting when

sediments with elevated metal concentrations are potentially toxic. Metal toxicity is

considered additive, and each must be added to obtain a sum of toxic units. This

methodology has been validated for copper and zinc (EPA 1994). None of the zinc

concentrations observed by Brooks (2000a) was toxic, as they were all associated with

sediments containing high concentrations of sulfide.

Furthermore, Brooks (2000a) reported that initially high sediment concentrations of zinc

under one salmon farm declined to background during a post production fallow period.

At the peak of production at the studied farm, sediment zinc concentrations were elevated

to 200 μg/g on the perimeter. They declined exponentially and reached a background

concentration of ca. 25 μg/g at a distance of between 30–75 m from the net-pen perimeter

on the downstream transect. Sediment-zinc concentrations were well correlated with

TVS throughout the study (r = 0.76). Sediment-zinc declined during chemical

remediation and was at background concentrations after six months of fallow. He

hypothesized that zinc was bound by sulfides in the sediments. Sediment sulfides

decrease with decreasing biological oxygen demand during chemical remediation. When

the sediments become aerobic, the sulfide is oxidized back to sulfate releasing the zinc,

which is diluted in the overlying water column. This hypothesis is consistent with

chemical theory and with evidence collected earlier by Brooks (2000b). Given that these

hypotheses stand the test of further scrutiny, no biological effects should be anticipated

from the observed concentrations of sediment zinc under salmon farms.

(ii) Copper

Levels of copper may be elevated in the environment around net-pen farms, which use

preventative treatments for bio-fouling. Several anti-fouling paints and solutions are

approved for use in the marine environment, and are therefore used on salmon farms.

Anti-predator nets and fish containment nets are increasingly treated with a copper antifouling solution to inhibit the settlement of organisms and bio-fouling. The practice

benefits the environment by reducing carbon inputs to the benthos. However, if cleaning

is accomplished in situ the displaced organisms can exacerbate organic loading to the
44

benthos under the farm. BMPs should require that nets first be removed and then washed

by hand or machine on a barge or at an upland facility.

Copper is a micronutrient. At moderately low levels the cupric ion is toxic to marine

organisms – particularly the larval stages of invertebrates. Until 1995 the EPA marine

chronic water quality criterion for copper was 2.5 μg-L-1 (EPA, 1986). Based on new

information that level is now being increased to 3.1 μg-L-1 dissolved copper (EPA, 1995).

Lewis and Metaxas (1991) examined copper concentrations immediately adjacent to

newly installed copper-treated nets at net-pen salmon farms in BC. They measured

ambient copper concentrations of 0.38 μg-L-1 in July and 0.37 μg-L-1 in August. The

concentration inside the pen was 0.54 μg-L-1 in July after a freshly treated net was

installed, and 0.54 μg-L-1 one month later in August. The small addition of copper in the

water from the treated net (0.16 to 0.17 μg-L-1) was not biologically significant except to

organisms which tried to settle on the net.

Peterson et al. (1991) compared copper levels in muscle and liver tissue from chinook

salmon grown in pens treated with ®Americoat 675, a copper based antifoulant, with

those in a pen with untreated nets. No statistically significant differences in the copper

levels in like-size fish from these two farms were observed, suggesting that the copper

released from the treated nets was not significantly concentrated by chinook salmon.

Brooks (2000d) conducted in vitro studies on the leaching of copper from ®Flexgard XI,

the most commonly used antifouling product on the west coast of North America. Initial

losses of 155 μg Cu/cm2-day declined exponentially during the period of the study.

Brooks (2000d) used the data to develop a spreadsheet model that predicts copper

concentration in the water as a function of the maximum current speeds observed at a

site, and the net-pen configuration and orientation of the complex to the currents. His

model predicted that containment nets treated with ®Flexgard XI would not exceed the

US EPA copper water quality criteria when fewer than 24 cages were installed in two

rows oriented parallel to currents flowing with a maximum speed greater than 20 cm/sec.

The model predicted that unless the configuration of net-pens or their orientation with the

currents was changed, the use of ®Flexgard XI treated nets would result in exceeding the

chronic water quality copper criterion at a small percentage of existing farms. The author

noted that assumptions used in his model were conservative, and probably predicted

higher copper concentrations than would actually be observed in the field. The model

has not been yet been tested in the field but it clearly demonstrated the need to manage

the use of antifouling products.

Brooks (2000d) compared sediment copper concentrations at salmon farms in BC using

®Flexgard XI treated nets with those at farms using untreated nets and reference stations.

Farmers in BC typically treat their nets at the beginning of each production period and

treat them again only after the fish are harvested. The mean concentration of copper in

the sediments of 117 farm stations using treated nets was 48.24 + 27.00 μg Cu/g. This

level was not significantly different than the mean concentration of 12.01 + 2.77
45

measured at the reference stations, or mean concentration of 26.3 observed at farms not

using copper treated nets (ANOVA F = 0.73; p = 0.49).

Brooks (2000d) found a great deal of variability in sediment copper concentrations at

farms using copper treated nets. The concentration of copper in 2 of these 117 samples

collected at 14 farms using copper treated nets exceeded the NOAA ER-M of 270 μg

Cu/g dry sediment, and the State of Washington sediment quality criterion of 390 μg

Cu/g. Thirteen of the samples (11%) exceeded the mean of the TEL and PEL used as a

regulatory benchmark in BC. All samples exceeding the lower benchmark were collected

at 5 of the 14 farms using copper-treated nets. Discussion with the producers revealed

that these farms washed their nets in barges during fallow periods. The fouling debris

cleaned from the nets was not retained but washed over the side. Consequently, the

concentrations observed at 5 of the 14 farms were not directly associated with the copper

treatment itself but some ancillary activity, like net washing. Other anecdotal

information revealed also that the copper – latex paint was abraded from the nets during

washing and that significant quantities of the latex chips (with copper imbedded) were

then washed over the side of the barge with the fouling organisms. The copper bound in

the latex would then leach out over time. Brooks (2000d) concluded that all coppertreated nets should be removed after harvesting the fish, and washed and retreated at

upland stations. Furthermore, all debris should be buried at an approved landfill site.

4.3 Pathogenic Organisms in the Vicinity of Net-pen Salmon Farms

4.3.1 Fecal coliform bacteria

The National Shellfish Sanitation Program (NSSP) certifies commercial shellfish beds in

the US and their harvest is governed by some very specific regulations (NSSP 1997); for

example, harvesting shellfish is forbidden within one mile of any out-fall from a sewage

treatment plant. This is because of public health concerns associated with toxicants

(heavy metals, PCBs, polycyclic aromatic hydrocarbons, etc.) released in industrial and

residential waste, and because many human pathogens (including viruses and bacteria)

are associated with treated human sewage. Shellfish sanitation is not adversely affected

by nutrients (carbon, nitrogen or phosphorus).

Viruses are generally taxa-specific, and viruses pathogenic to fish, such as infectious

pancreatic necrosis (IPN), viral hemorrhagic septicemia (VHS), and infectious

hematopoietic necrosis (IHN) have no documented effect on human beings. However,

fecal coliform (FC) bacteria persist in sediments high in total organic carbon (TOC) for

varying periods. These bacteria are specific to warm-blooded animals (mammals and

birds) and are not a normal part of the microflora found in fish intestines. However,

mammals and birds are strongly attracted to fish farms increasing the potential for

increased fecal coliform levels in the sediments near salmon farms. There is no potential

for an increase in fecal coliform bacteria associated with cultured fish.

NSSP defines water quality standards for shellfish growing areas and has a methodology

for assessing and classifying shellfish harvest grounds. Approved growing areas must

have a most probable number or geometric mean (FC MPN) of <14 FC/100 ml, with not
46

more than 10% of the samples exceeding an MPN of 43/100 ml in a 5-tube decimal

dilution test (APHA, 1992).

Brooks (2000a) analyzed 33 water samples from the vicinity of an operating salmon farm

during every quarter of the year. The MPN for all stations was less than the NSSP

requirements for an Approved Shellfish Harvest Classification (14 FC/100 ml), and all

stations met NSSP requirements. He also examined shellfish tissues for FC bacteria.

NSSP has established an allowable upper limit of 230 FC/100 g of tissue for product

entering interstate (or international) commerce. Average clam tissue levels at the closest

station located 200 m from the farm were 130 FC/100 g tissue. At 500 m the average

level dropped to 50 FC/100 g, and at the reference station it was 20 FC/100 g. All of the

shellfish samples tested met the NSSP requirement for shellfish tissues in commerce. In

summary, he observed slightly more FC bacteria in water and shellfish tissues at stations

closest to the farm perimeter. The sources of observed bacteria were not determined, but

potential sources include farm workers themselves and, more probably, the birds and

mammals which congregate around salmon farms. Water and shellfish tissues were

consistently of high quality and met all bacteriological requirements imposed by NSSP.

4.3.2 Farm wastes

Ellis (1996) postulated that waste feed and feces might enhance populations of a variety

of ubiquitous marine bacteria pathogenic to humans. There is no direct evidence in the

scientific literature that salmon farm wastes enhance pathogenic marine bacteria. In an

extensive review of the epidemiological records for shellfish in the waters of Washington

State spanning 20 years, Brooks (1993 unpubl. data, Aquatic Environmental Sciences,

Port Townsend, WA 98368) did not find one documented case of Vibrio vulnificusinduced disease. This, he concluded, was because thermophilic bacteria, like V.

vulnificus, required a high water temperatures in addition to a rich source of organic

material to thrive. Elevated ambient water temperatures would likely be a requirement of

most bacteria that are pathogenic to homoeothermal humans. Bacteria which flourish in

warm-blooded animals are unlikely to proliferate in cold Pacific Northwest waters under

salmon farms. Also, as salmon are poikilotherms, FC and other disease-causing bacteria

which flourish in warm-blooded animals would not likely multiply in the gut of salmon,

whose intestinal flora is determined primarily by ambient bacterial concentrations. He

concluded there was no basis for assuming the feces of caged salmon would contain more

than ambient concentrations of those bacteria pathogenic to humans.

In another comparison of microbial levels in the tissues of farmed and wild salmon,

Calderwood et al. (1988) examined the kidney, liver, spleen, heart, and muscle tissues for

the presence of viruses and 16 bacterial species, including several later hypothesized as

risks by Ellis (1996). They compared 68 adult wild steelhead trout at Robertson Creek

and 50 wild adult coho from Chehalis, Washington with cultured chinook salmon from

Sechelt and Sooke Basin in British Columbia. Their results were as follows:

(a) V. vulnificus, a potentially serious human pathogen in immune-compromised

individuals, was not detected in the cultured fish. However, 44% of wild fish returning to

Chehalis were positive for this bacterium. Other vibrio species, including the potential
47

human pathogen, V. parahaemolyticus, were not found in the farmed salmon, but were

found with a prevalence of 9 and 44% in the wild fish.

(b) Acinetobacter calcoaceticus var. anitratus, which is a common bacterium

found in water and soil, and has been associated with pneumonia, meningitis, and

septicemia in humans, was observed with an average prevalence of 14% in cultured fish,

and five times higher (76%) in wild fish.

(c) Aeromonas hydrophila was observed in over half of the wild fish from both

Robertson Creek and Chehalis. Both A. hydrophila and A. salmonicida are common fish

pathogens (Roberts 1978) but neither was isolated from tissues of cultured chinook

salmon.

This early work by Caldewood et al. (1988) suggests that wild fish are far more likely to

be a source of disease-causing bacteria than farmed fish. Their data do not support any

hypothesis that environmental conditions on farms with healthy chinook salmon are

enhancing populations of pathogenic bacteria.

Furthermore, in their search for human diseases epidemiologists most frequently examine

the population having the greatest exposure to the suspected etiologic agent. On salmon

farms, the populations most exposed to the fish are the farm workers and processors. If

farms are a significant source of human pathogens, then farm workers and fish processors

should show some history of such diseases. There are no epidemiological records, which

show evidence of any infectious outbreaks of disease.

Collectively, an understanding of productive environments and fish and human

physiology, and the lack of supporting epidemiological evidence, show that salmon farms

in the Pacific Northwest are unlikely to increase any risk to human health from marine

bacteria. Because of differences in its physical and chemical composition fish farm

wastes do not disperse over large areas. They remain localized where they are

metabolized by naturally occurring marine bacteria and opportunistic invertebrates.

There is no evidence that salmon farms create conditions leading to a proliferation of

pathogenic bacteria. Furthermore, from a perspective of human health there appears to

be no basis for suggesting fish farm wastes are comparable with human sewage from

either large cites or even small towns.

4.4 The Effects of Therapeutic Compounds

The majority of therapeutic compounds used at salmon farms are for the control of sea

lice. Sea lice, particularly Caligus elongatus, Lepeophtheirus salmonis, and Ergasilus

labracis, have caused extensive losses of fish, particularly at farms in the northeastern

Atlantic. They have not presented significant problems to producers in the Pacific

Northwest, and salmon produced in Washington have not been treated for lice for the last

15 years (A. Mogster, Northwest Seafarms, personal communication). Both ivermectin

and emamectin have been used infrequently to control sea lice in BC.

Costello (1993) and Roth et al. (1993) describe the physical, chemical, and biological

methods used to control sea lice on fish farms in other areas. Current practices rely
48

primarily on the administration of chemo-therapeutic compounds in food or as a bath.

The following treatments have been authorized for use.

(i) Ivermectin

Ivermectin (22, 23-dihydroavermectin B1) has been used widely in agriculture for many

years to control parasites, and was reported by Smith et al. (1993), and Johnson and

Margolis (1993) to be effective in controlling sea lice on caged salmon. It is

administered as a coating on feed at a rate of 0.025 mg ivermectin/kg of fish at 10oC

twice per week for 4 weeks. The dose is increased by 10% for every 1oC decrease in

ambient temperature. In Scotland the maximum number of weekly treatments is three per

year (SEPA 2000).

Ivermectin is a broad-spectrum biocide which has low water solubility and a moderately

high affinity for binding to particles. The compound is reported by SEPA (1998a) to

concentrate in Mytilus edulis by a relatively low factor of 752. Grant and Briggs (1998a)

stated that it did not appear to accumulate or concentrate in the food chain.

Dissolved concentrations of ivermectin are lethal to a number of marine organisms,

ranging from a 96 hr LC50 of 0.022 μg ivermectin/L for Mysidopsis bahia (Davies et al.

1997) to >10,000 μg/L for nematodes (Grant and Briggs 1998b). Most of the 96 hr LC50

values are less than 1000 μg/L. Collier and Pinn (1998) and Grant and Briggs (1998b)

have shown that crustaceans and polychaetes are more susceptible to ivermectin than

mollusks. Annual studies in Scotland by ERT Ltd. did not detect ivermectin in the water

column (detection limit = 0.5 μg/L) at a Scottish farm undergoing treatment (ERT 1997,

and ERT 1998).

Burridge and Haya (1993) found that ivermectin-coated waste feed affected non-target

species, such as the shrimp (Crangon septemspinosa) at concentrations of 8.5 μg

ivermectin/g food. Ivermectin toxicity was demonstrated in laboratory sediments at

concentrations ranging from a 10 day LC50 of 23 μg ivermectin/kg dry sediment for

Arenicola marina by Thain et al. (1997), and to 180 μg/kg for Asterias rubens by Davies

et al. (1998). Black et al. (1997) documented significant mortality of polychaetes at

ivermectin accumulations >81 μg ivermectin/m2. This is equivalent to a concentration of

approximately 25 μg/kg if the ivermectin is mixed into the top 2-cm of sediments having

a density of 1.6 g/cm3. Of particular interest was the adverse effect on the organic carbon

tolerant opportunist C. capitata, whose abundance was significantly reduced at

ivermectin concentrations above the calculated value of 25 μg/kg. The paper by Black et

al. (1997) did not discuss the increased chemical and biological remediation times that

might result from a significant reduction in the abundance of C. capitata.

The fate of ivermectin not absorbed by Atlantic salmon appears to be sedimentation

followed by slow degradation. Collier and Pinn (1998) noted that the breakdown of

ivermectin in marine sediments was dependent on light and temperature. Davies et al.

(1998) determined a half-life of ivermectin in marine sediments to be >100 days under

the tested conditions.
49

ERT (1997 and 1998) detected ivermectin at concentrations ranging from 5–11 μg/kg

(wet sediment weight) in only 3 of 54 sediment samples at a farm undergoing treatment.

Ivermictin was also detected in sediment traps deployed on the perimeter of farms

undergoing treatment at 42 g/kg. Ivermectin was detected in 2 of 108 mussel samples at

concentrations of 5 and <5 μg/kg collected from caged mussels deployed around farms

undergoing treatment. The active ingredient was not detected in wild shrimp (Nephrops

norvegicus) collected in the vicinity of the treated farm. According to a report by the

Canadian Department of Fisheries and Ocean (DFO), ivermectin (with a detection limit

of 1 to 2 μg/kg) was not found in American lobsters (Homarus americanus) around

salmon farms (DFO 1996); however, the same document noted detection of ivermectin in

sediments at distances up to 50 m from a farm in the Bay of Fundy where the compound

was used. Concentrations varied between 13.7 and 17.3 μg/kg dry sediment at distances

<10 m from the farm perimeter. Traces (between 2 and 6 μg/g) of ivermectin were

detected at distances up to 100 m from the farm.

These results suggest that ivermectin is most likely to be detected in sediments and not in

the water column. DFO has set a predicted no-effect sediment concentration (PNEC) of

1.8 μg ivermectin/kg dry sediment. Empirical evidence has demonstrated sediment

concentrations exceeding this value to 50 m from the perimeter of one farm, but not

beyond. In general, significant sediment concentrations of ivermectin have not been

observed at distances beyond 10–20 m. The half-life of sedimented ivermectin is

approximately three months (DFO 1996). Permission to use ivermectin on farms in

Scotland has been withdrawn by the Scottish Environmental Protection Agency (SEPA).

(ii) Emamectin benzoate

SEPA reviewed the proposed use in Scotland of the pharmaceutical emamectin benzoate

under the proprietary name ®Slice (SEPA 1999a). Emamectin has low water solubility

and is expected to accumulate in sediments. However, based on laboratory bioassays

SEPA stated that emamectin was about ten times less toxic than ivermectin, at least for

the genus Crangon. However, SEPA noted that the PNEC level of 0.763 μg

emamectin/kg wet sediment was lower than the PNEC of 1.8 μg ivermectin/kg proposed

by DFO (DFO 1996). Field studies failed to detect emamectin in water, and maximum

observed sediment concentrations were just above the level of quantification (1.0 μg/kg

wet weight). The sediment half-life of emamectin was 175 days. No adverse effects on

infaunal communities were observed following treatment with emamectin benzoate.

SEPA used the deposition model (DEPOMOD) to suggest that the ratio of the predicted

environmental concentration (PEC) to the PNEC was low, and there was little risk that

treatment would pose a threat to sediment-dwelling organisms, even in the worst-case

scenario tested. Currently ®Slice is in use in Chile, Ireland, and Norway, and has been

approved in Scotland by SEPA in January 2000 (SEPA 2000) but to-date no permits have

been issued.

(iii) Calicide

Calicide (teflubenzuron) has been licensed by SEPA for the control of sea lice in

Scotland (SEPA 2000), and is being licensed in Canada, Chile, Ireland, and Norway.

This therapeutic compound is administered as a 2-g/kg coating on feed. It is a chitinase
50

inhibitor effective against juvenile sea lice on salmon at a dose of 10 mg/kg-day-1 for

seven consecutive days. It has reduced effectiveness after lice become adults and stop

molting.

SEPA (1999b) noted that calicide had a long half-life of 115 days in sediments, and could

be detected at distances up to 1,000 m downstream from farms being treated. However,

no adverse effects were detected in benthic communities (including crustaceans) and

SEPA concluded that any residual teflubenzuron was not bio-available. Calicide inhibits

the production of chitinase and therefore is not toxic to phyla other than the Crustacea.

For teflubenzuron, SEPA (1999b) permitted an allowable sea-water quality standard of

6.0 ng/L for the annual average, and a maximum allowable concentration of 30 ng/L. In

Scotland there is an 'allowable effects area' of 100 m from salmon farms. A sediment

quality standard of 2.0 μg calicide/kg dry sediment in a 5-cm deep core has been

established outside this area. Sediment concentrations at all distances within 25 m of a

treated farm must be maintained at less than 10 mg calicide/kg dry sediment (5 cm core).

Calicide is approved only for interrupting the life cycle of sea lice. It is not approved for

treating adult lice infestations. Its use is based on computer-modeling of specific sites

and it is not approved for general use. Predicted sediment and water column

concentrations of the active ingredient must be lower than the water and sediment quality

standards described above.

(iv) Cypermethrin

®Cypermethrin (dichlorvos) is a pesticide being used in investigative programs, and

under some form of temporary registration in Canada, Ireland, Norway, UK, and US. It

is administered in a 5 μg/L bath for 60 minutes within a confined and covered area.

Dichlorvos is toxic to crustaceans, with a LC50 of 0.006 μg/L and a no-observed-effect

concentration (NOEC) of 0.003 μg/L for Mysidopsis bahia. It is adsorbed by sediments

where it degrades with a half-life of 35 days in high TVS sediments and 80 days in low

TVS environments. It has a 10-day NOEC of 1000 μg/kg in Arenicola, and 64 μg/kg in

amphipods of the genus Corophium. Concentrations greater than about 10 ng/L are

acutely toxic to some crustaceans, and modeling suggests that this value can be exceeded

in the immediate vicinity of pens being treated with this product. SEPA (1998b)

concluded that toxic effects to non-target species could occur within a few hundred

meters of a treated farm and that these effects might last for several hours.

High mortality of shrimp and lobsters has been observed when they are exposed to a bath

of dichlorvos, but the effect has not been observed outside net-pens. Field trials have

observed peak water concentrations of 187 ng/L 25 m downstream from salmon net-pens

following removal of the tarpaulin covers.

Based on an absence of demonstrated deleterious effects on non-target animals, SEPA

(1998b) recommended authorization of ®Excis (containing dichlorvos) for a 2-year

period initially. Individual permits are issued by SEPA. Modeling must predict that the
51

proposed treatment will not result in exceeding a 3-hr environmental quality standard of

16 ng/L in the dispersing plume following removal of the covers. Post-treatment

monitoring is required.

(v) Azamethiphos

Azamethiphos (or ®Salmosan) is a pesticide administered in a bath at 0.1 mg/L. The

active ingredient degrades with a half-life of approximately 11 days at neutral pH. Larval

lobsters were the most sensitive organism tested with a 96 hr-LC50 of 0.52 μg/L and a noobserved-effect level (NOEL) of 0.156 μg/L. A toxicity threshold to lobster larvae was

estimated by SEPA (1997) at 0.078 μg/L. Azamethiphos is very water-soluble and is not

expected to accumulate in sediments. Compared with dichlorvos, azamethiphos is

considered more toxic to crustaceans. SEPA (1997) restricted its use in aquatic

environments where modeling predicted that:

• 3 h after treatment the mean residual concentrations in the dispersion zone will not

exceed 160 ng/L.

• 24 h after treatment the mean residual concentrations in the receiving water will

nowhere exceed 80 ng/L.

• 3 days after treatment the residual concentrations in the receiving water will nowhere

exceed 5 ng/L.

Post-application monitoring was required by SEPA to ensure compliance.

The control of sea lice is important to the health of farmed salmon and to reduce the

potential for salmon farms to act as vectors for the infestation of wild stocks of salmon

and sea trout. A review of the available treatments suggests that great care must be

exercised in the use of these therapeutic compounds. They are all non-specific, at least

within the Class Crustacea, and several are broad-spectrum biocides with potential to

affect many phyla adversely. However, field studies have not found significant

widespread adverse effects to either pelagic or benthic resources associated with the

authorized use of these pharmaceuticals or pesticides.

4.5 Farm Sediments

4.5.1 Monitoring environmental effects on sediments

Infaunal community analysis, as demonstrated by Pearson and Rosenberg (1978),

Mahnken (1993), and Brooks (2000a), is ultimately the most direct and sensitive

methodology for assessing the biological response to organic loading from salmon

farming. However, benthic communities are not stable, as shown by Mills (1969) and

Eagle (1975), and their structure is influenced by many natural processes unrelated to

human influence. These processes include seasonal factors (Crisp 1964, Arntz and

Rumohr 1982, and Brooks 2000a) and physicochemical factors (Striplin Environmental

Associates 1996). Skalski and McKenzie (1982) pointed out that this variability typically

requires large numbers of samples to achieve reasonable test powers.

The international Joint Group of Experts on the Scientific Aspects of Marine

Environmental Protection (GESAMP) noted that the taxonomy required in support of

infaunal analysis was expensive and time consuming (GESAMP 1996). This cost, when
52

coupled with high internal variability, detracted from infaunal analysis as a routine

method for evaluating environmental effects as part of regulatory programs. Therefore

physicochemical endpoints, including TVS, TOC, redox potential (Eh) and total sediment

sulfides (S=) were being used increasingly as rapid and inexpensive surrogates for

assessing biological response. GESAMP (1996) concluded that the visually determined

depth of the reduction-oxidation discontinuity was of low value because it was semiquantitative. They did not consider emerging physicochemical endpoints, such as sulfide

analysis using ion specific probes (Wildish, et al. 1999), or TVS (Hargrave et al. 1995,

Brooks 2000e and 2000f).

Brooks (2000c and 2000e) discussed the relative merits of TVS, TOC, S=, and Eh for

evaluating the environmental response to salmon farms. He noted that organic carbon,

whether measured as TOC or TVS, had only a moderate correlation with biological

effects, particularly infauna. He hypothesized that sediment carbon comes in many forms

including woody debris, which is refractory to microbial catabolism resulting in low

BOD. Drift macroalgae and eelgrass form an intermediate class of sediment carbon

broken down within a few months to one year. Fish feces on the other hand was very

labile and created high BOD, more frequently leading to anaerobic conditions than

woody debris or macroalgae. Therefore 15% TVS may not exceed the assimilative

capacity of the sediment if it was in the form of woody debris, whereas 15% TVS

associated with salmon farm waste in the same sediment would be more likely to create

anaerobic conditions with significant biological effects. It was recognized that when

finely divided woody debris exceeded the assimilative capacity the effect could last for

centuries as the wood deteriorated very slowly. Salmon farm waste, on the other hand,

because it was catabolized very quickly had rather ephemeral effects lasting from months

to two or three years in extreme cases.

Redox potential (Eh) was identified by GESAMP (1996) and Wildish et al. (1999) as a

valuable endpoint for evaluating sediment chemistry near salmon farms because it is

rapid, low cost, and permits extensive spatial surveys. Brooks (2000f) found low

sediment redox (20.68 + 22.29 mV) and low sulfide concentrations (29.83 + 11.59

μmoles) in the same samples from reference stations located in areas with greater than

80–90% silts and clays comprising the sediment grain size distribution. He noted low Eh

and high sulfide concentrations in sediments were not always well correlated, and that

low Eh could be the result of physical processes, especially in fine-grained sediments.

This limited its usefulness in evaluating the effects of carbon input from salmon farms.

Wang and Chapman (1999) described the response of laboratory bioassay test animals to

sediment sulfides. However, despite attempts by Brown et al. (1987), Henderson and

Ross (1995), and Hargrave et al. (1997), the literature does not provide a good

quantitative description of the response of natural infaunal communities to sediment

sulfide concentrations or redox potential.

In summary, benthic infaunal and epifaunal analysis appears to be the most sensitive

indicator of environmental health in sediments around salmon farms. However, benthic

communities are not stable across environments and depend on the physical environment,
53

including water depths, current speeds, sediment grain size distribution, and the

availability of organic carbon (Striplin Environmental Associates 1996). In addition

benthic communities vary by season, as influenced by food input and water temperature,

etc. (Arntz and Rumohr 1982).

4.5.2 Biological changes in the water column and sediments

The environmental changes associated with salmon farms are superimposed on natural

changes. These potential effects have been examined in numerous studies during the last

two decades. Despite significant site-specific variability there is a consistent thread

binding this literature.

(i) Water column changes

Possible changes in the water column associated with the intensive culture of fish could

be associated with intoxication due to hydrogen sulfide and ammonia production in

underlying sediments, decreases in dissolved oxygen associated with salmon respiration

and/or the oxidation of sedimented waste, and eutrophication associated with nitrogen

released across gill epithelia and in urine and feces. The magnitude and consequences of

environmental changes associated with these factors is dependent on environmental

parameters such as water depth, current speeds, background nutrient availability, salinity,

rainfall, wind, etc., which in aggregate constitute the local environment.

(ii) Nitrogen and phosphorous loading to the water column

Marine environments along the west coast of North America are especially productive

because cold, upwelling, nutrient rich water replaces surface waters driven offshore by

prevailing northwesterly winds. In addition, the relatively high geographic latitude of BC

and Washington results in reduced light penetration in water compared with more

southerly latitudes. Lastly, moisture laden onshore winds create significant cloud cover

throughout much of the year. These factors combine to limit light availability

significantly in most temperate marine environments, except during summer months.

Furthermore, it should be noted that in most marine environments, nitrogen is the limiting

nutrient and not phosphorus. The remainder of this review will focus on nitrogen inputs.

In the Pacific Northwest, wind-driven vertical-mixing drives a significant proportion of

the phytoplankton crop below the compensation depth where cell respiration equals

photosynthesis and where they no longer multiply. Where water freely circulates, flood

tides replenish nutrients from water upwelling offshore. When coupled with the

atmospheric and geographical factors that reduce light availability, the result is that

primary productivity in the Pacific Northwest is generally light limited, not nutrient

limited. This is especially true during winter months. In other words, there is insufficient

light to use the nutrients already available in the water column. Adding more nutrients in

a light limited system does not increase plant growth.

There are sheltered, poorly flushed, shallow embayments where salinity and temperature

induced stratification results in a stable water column that allows phytoplankton to

remain above the compensation depth. When these conditions occur in the spring or

summer, significant blooms can occur following several days or weeks of clear sunny
54

weather. These blooms eventually wane because winds increase vertical mixing; cloud

cover reduces the available light; or nutrients are depleted in the surface water. In this

last situation, nutrient input from a salmon farm could further stimulate plant growth,

exacerbating the problem. In addition, shallow bays having significant freshwater input

and minimal flushing, are not considered good sites for net-pen grow-out operations.

However, they might be deemed appropriate as smolt introduction sites.

The last point to consider in this general discussion is that nitrogenous compounds are

released from fish farms into currents that generally average greater than 4 to 12 cm-sec-1

and acoustic Doppler current meter studies at British Columbia salmon farms have

revealed net transport speeds of 1.0 to 5.0 cm-sec-1. At temperatures of 10–15oC, it takes

one to two days for an algal cell to divide, even if all of its photosynthetic needs are met

(Brooks 2000g). An algal bloom may result in cell densities increasing from a few

thousand cells per ml to perhaps a million. That requires eight or nine cell generations,

which requires a minimum of 8–16 days. In open bodies of water, moving with a net

speed of even 2 cm-sec-1, a phytoplankton population would move 14 km from the

location at which nutrients were added during creation of a bloom. Recall that the barely

significant increases in nitrogen observed 6 m downstream from farms in Puget Sound

were generally not detectable at 30 m downstream. Therefore it appears reasonable to

conclude that, within a single algal cell division (one to two days), the water passing

through the farm would have traveled at least 1.7 km. It is difficult to conclude that the

nutrient additions from the farm, generally undetectable at 30 m downstream would have

any effect at all on primary production even if the water body was nutrient limited.

Pease (1977), Rensel (1988 and 1989), and Parametrix Inc., (Parametrix 1990)

documented small increases in dissolved nitrogen within and on the perimeter of salmon

farms. However, all of these authors agreed that the quantity of dissolved nitrogen added

by even several farms would have no measurable effect on phytoplankton production.

Gowen et al. (1988) studied a Scottish loch with very restricted water exchange to the

open sea and a large salmon farm. The authors concluded that the farm had no

measurable effect on phytoplankton density.

Weston (1986) conducted a quantitative assessment of the effects of five hypothetical

farms located in a small embayment with poor flushing. His analysis suggested that the

nitrogen added by five farms could not be expected to adversely affect the phytoplankton

abundance in the embayment. He did address the issue of nutrient sensitive embayments

and recommended that these areas should be identified and carefully managed.

Banse et al. (1990), Parsons et al. (1990), Pridmore and Rutherford (1992), Taylor

(1993), and Taylor and Horner (1994) all examined phytoplankton production and

blooms of noxious phytoplankton in the Pacific Northwest. They concluded that nitrogen

levels and phytoplankton production at salmon farms were determined by ambient

conditions. Furthermore, they found that salmon farms had little or no effect on ambient

levels of either nutrients or phytoplankton density.
55

The literature is consistent with the previous general discussion and strongly supports a

thesis that, with the exception of a few shallow, very poorly flushed embayments, the

potential for net-pen enhancement of phytoplankton populations is remote, or nonexistent. Based on similar arguments and ten years of monitoring dissolved nutrients at

salmon farms, Washington State eliminated any requirement for water column

monitoring in compliance with NPDES permits issued to all salmon farms in 1996.

4.5.3 Hydrogen sulfide gas production in sediments

When the assimilative capacity of the benthos is exceeded, oxygen is depleted and sulfurreducing bacteria continue to degrade organic carbon. During the process either

ammonia or hydrogen sulfide gas may be produced. These gases, particularly the latter,

are highly toxic and can significantly compromise infauna. They are not unique to fish

farms and other sources of anthropogenic carbon, and are frequently found in natural

environments where organic debris (leaves, macroalgae, eel-grass, etc.) accumulates.

Hydrogen sulfide is the cause of the 'rotten egg' smell emitted from many pristine

estuarine sediments at levels >2 μg/L (EPA 1986).

Hargrave et al. (1997) examined a suite of physicochemical parameters under 11 salmon

farms and 11 reference stations located >50 m from net-pens in the Western Isles region

of the Bay of Fundy on the east coast of Canada. Sediment concentrations of hydrogen

sulfide were found to be significantly different (P = 0.00001) under net-pens when

compared with reference sediments. Total sulfide concentrations in surface sediments at

all cage sites were >180 μM while values at all but one reference location were <200 μM.

They noted sulfide concentrations >2000 μM were indicative of high organic loading

under some net-pens and were generally associated with negative Eh potentials.

Ammonia and hydrogen sulfide are lighter than water and when significant quantities of

these gases accumulate in sediments, they can escape and rise to the surface (outgassing). As the bubbles rise the soluble H2S is dissolved in the water column.

Samuelsen et al. (1988) analyzed gas released from sediments underlying poorly flushed

salmon farms. They found that 98% of the gas was CH4 and CO2. Less than 1.9% of the

gas at the sediment-water interface was sulfide (S=). Furthermore they found that, after

rising 3 m in the water column, the S= was reduced to 0.05% of the total gas. The

resulting concentration would be 1.54 x 10-6 g S= /(58.9 ml x 1.025 g/ml) or 25.5 μg S= /L

seawater (25 ppb). Water quality standards are based on the undissociated sulfide (H2S)

which is ca. 10% of S= at pH = 8.4. Applying this factor predicts an undissociated H2S

level of 2.55 in the 0.5 cm diameter column through which the gas bubble passes. This is

approximately equal to the 2 μg/L chronic water quality criteria established by the EPA

(1986) for freshwater and marine environments. In reality oxidation, diffusion, and

mechanical mixing significantly reduce concentrations further by a factor of 100 or more.

Samuelsen et al. (1988) found that the fraction of the less soluble CH4 did not appreciably

change during transit of the bubbles through the water column. The low concentration of

H2S in the bubbles at the sediment-water interface, and the low water concentrations

predicted during ascent, suggests that very large gas emissions would be required before

sufficient H2S could be dissolved in the water column to create toxic conditions.
56

4.5.4 Dissolved oxygen

Weston (1986) reviewed the effects of salmon culture on ambient dissolved oxygen

levels and concluded that farms could decrease these levels by 0.3 ppm. Brooks (1991,

1992, 1993a, 1994a, 1994b, 1995a, and 1995b) observed decreases of as much as 2 ppm

in water passing through a large, poorly flushed farm in Puget Sound. Significant

reductions in dissolved oxygen (DO) were not observed by Brooks (1994a and 1994b) at

farms in well-flushed passages. In no case were DO levels within 6 m of the downstream

farm perimeter depressed below 6 ppm, a minimum level for optimum culture of

salmonids. Winsby et al. (1996) reported a range of results from the literature. However,

his discussion in general suggested that depressed oxygen levels are associated with the

water column immediately overlying anaerobic sediments. Cross (1993) concluded that

salmon farms in BC have minimal effects on ambient DO levels.

Depressed oxygen levels (3 to 6 ppm) are infrequently encountered at salmon farms

along the Pacific coast. These depressions result from the upwelling of cold, nutrient rich

but oxygen deficient water to the surface. Conditions favoring depressed DO are most

frequently encountered in the Pacific Northwest during the summer and fall when

northwest trade winds increase oceanic upwelling. Deep fjords, like Hood Canal in

Washington State, can also experience depressed concentrations of DO when winds bring

anoxic water to the surface from deep stagnant pools. Feeding is suspended and

compressors used to increase DO when these naturally occurring masses of water with

low DO levels flow into salmon farms. This phenomenon is imposed on the farm, not

caused by the farm. However, the frequency of occurrence of these oxygen deficient

water masses should be assessed in siting a farm. In addition, it could be considered

good management on the part of operators to measure DO in bottom water under their

farms in an attempt to predict periods of depressed surface oxygen.

In summary, based on the literature it appears that net-pens create only minor depressions

in surface water DO concentrations. When sediments under a farm become anaerobic the

overlying water to a depth of perhaps a meter may experience some reduction in DO.

This is most likely to occur under farms with very poor circulation (<3 to 5 cm-sec-1

maximum current speeds).

4.5.5 Changes in the local fish community

Salmon farms are known to function as fish aggregating devices. The structures attract

numerous fish species, which frequently take up residence between the containment and

predator nets. There are no published reports as yet which document this community of

aquatic animals, and its abundance. Brooks (1994b and 1995b), at a well-flushed net-pen

site in Washington identified pile perch (Rhacochilus vacca), shiner perch (Cymatogaster

aggregata), herring (Clupea pallasi), lingcod (Ophiodon elongatus), bay pipefish

(Syngnathus leptorhynchus) and several species of sole (Pleuronichthys spp.) all in

abundance. At another site nearby, located over a sandy bottom, sea cucumbers

(Parastichopus californicus) and geoducks (Panopea abrupta) had proliferated. All of

these populations are closely associated with the farm (within 30 m). It should be added

that one of these facilities is located in shallow water (15–18 m MLLW) and fast currents
57

(115 cm-sec-1). The second facility is located in a moderately well flushed environment

with maximum currents of 30 cm-sec-1 and water depths of 22–30 m MLLW.

4.5.6 Physicochemical changes in the sediment near salmon farms

The chemical and biological effects associated with fish farms have been documented

and reviewed by Pease (1977), Braaten et al. (1983), Earll et al. (1984), Ervik et al.

(1985), Ackefors (1986), Weston (1986), Aure et al. (1988), Rosenthal et al. (1988 and

1995), Weston and Gowen (1988), Hansen et al. (1990), Parametrix (1990), Gowen et al.

(1991), Johannessen et al. 1994, Winsby (1996), Mazzola et al. (1999) and Morrisey et al.

(2000). It is possible to model rates of organic loading from net-pen operations described

by Weston and Gowen (1988), Findlay (1992), Einen et al. (1995), Silvert and Sowles

(1996), and Ervik et al. (1997). The fate and transport of those wastes is a far more

complex problem. However, the effects of farm wastes on the benthos in a variety of

environments have been well documented. Brooks (1992, 1993a, 1994a, 1994b, 1995a,

and 1995b) studied sediment chemistry (redox, TOC, nitrogen, and sediment grain size)

and benthic infaunal response at two farms which represented two very different

environments in Puget Sound, Washington. In terms of negative environmental effects

associated with intensive net-pen fish culture, organic loading to the sediments is most

significant. Goyette and Brooks (1999) observed statistically significant changes in the

composition of the benthic infaunal community in Sooke Basin, BC associated with small

natural changes in sediment organic carbon content of <1% change across the 500-m

study area. In general, the literature suggests a lack of appreciation of the sensitivity of

the benthos to small additions of organic carbon, particularly labile forms like fish feces.

Hargrave et al. (1995) documented sediment total sulfide concentrations under salmon

farms in the Bay of Fundy that were <6,600 μmoles S=. In contrast, Brooks (2000c and

2000f) observed significantly higher sediment sulfide concentrations (<16,000 μmoles)

on the perimeter of salmon farms in Canada BC, and Wildish (1999) reported sediment

concentrations up to 36,000 μmoles S= in Bay of Fundy sediments under operating farms.

4.5.7 Biological effects

The biological response of infauna to the sediment physicochemical changes occurring as

a result of organic loading from salmon farms has been assessed by Hargrave (1994),

Henderson and Ross (1995), and Hargrave et al. (1997). The toxicity of sulfide to

infauna is documented for a few species (Bagarinao 1993; Wang and Chapman 1999),

but despite the efforts of Henderson and Ross (1995), quantitative relationships between

infauna and physicochemical endpoints (S=, Eh, TVS) remain elusive. Brooks (2000a)

observed a significant enhancement in infauna during the early stages of production and

at the end of the fallow period. However, at the peak biomass there was a significant

reduction in the number of invertebrates observed at downstream stations located

between 20 m and about 70 m from the farm perimeter. Near-field invertebrate numbers

were supplemented by allochthonous input from the fouling community on farm nets. In

addition, a significant portion of the invertebrate community associated with near-field

sediments during periods of high organic farm input were the TOC tolerant species C.

capitata and Ophryotrocha cf. vivipara.
58

Species richness, the number of species observed in biological samples, is frequently a

more sensitive indicator of environmental stress than abundance. Brooks (2000a)

observed significant reductions (<2.0 standard deviations below the mean) in the number

of taxa within 45 m of the farm during peak production. It did not appear that significant

effects extended beyond 75 m during this production period. Biological remediation

began as soon as harvest was initiated in April of 1997 and was essentially complete

within four months of fallow. A slight enhancement in taxa richness was evident five

months following the completion of harvest.

Polychaete abundance was enhanced as sediment organic carbon built up at the beginning

of the production cycle. Abundance declined within 80 m of the farm perimeter during

peak biomass when farm waste exceeded the assimilative capacity of the sediments,

which became anaerobic. Polychaete abundance began increasing again during the

winter of 1996–1997, approximately six months after harvest began. Polychaetes

proliferated with the improving benthic conditions and exceeded reference abundance

during the last 6 months of the study. The enhanced area extended from the farm

perimeter to a distance of at least 75 m during the October 1997 evaluation.

Brooks (2000a) found that crustaceans were adversely affected at near-field stations

earlier (and therefore possibly in association with smaller increases in sediment organic

carbon) than polychaetes. A steady increase in the number of crustacean taxa was

observed as soon as the fish biomass began decreasing during harvest. The salmon farm

had little effect on the overall abundance of crustaceans. In part that was because the

benthos in the immediate vicinity of the farm was supplemented by allochthonous input

from the net-pens, such as the amphipods Metacaprella kennerlyi and Jassa falcata.

Arthropods were supplemented by mobile crustaceans, such as the megalope of Cancer

magister which were very abundant in the vicinity of the farm during June 1996.

Brooks (2000a) found that mollusks were an abundant and diverse part of the infaunal

invertebrate community in reference sediments from the study area. Statistically

significant decreases in the numbers of mollusks were not observed in this study.

However, the number of molluskan taxa was significantly reduced at all farm stations

during the production cycle. An increase in the number of molluskan taxa was evident at

the end of the study, but the number of taxa observed within 50–75 m from the net-pen

perimeter had not recovered to reference conditions.

Brooks (2001) has determined the biological response to varying concentrations of

sediment TVS, sulfides, and Eh as a function of farm production, overlying currents, and

sediment grain size distribution. Preliminary results indicated that reference sulfide

concentrations were generally low (10–100 μmoles) but could be as high as 250–300

μmoles. Reductions in the number of taxa from >20 species to 12–14 species, with

significantly increased abundance and biomass of infauna, were noted with sulfide

concentrations in the range of 300–2,000 μmoles. Sediments containing >2000

micromoles S= had a reduced infaunal community dominated by C. capitata, and those

containing greater than 6,000 μmoles were generally sparse. His findings were consistent
59

with the reports of Wildish (1999), Poole et al. (1978), and Pearson and Rosenberg

(1978), which are tabulated below.

Endpoint Classification Reference

Microbial Normal Oxic Hypoxic Anoxic Poole et al. 1978

Macrofaunal Normal Transitory Polluted Grossly

polluted

Pearson and

Rosenberg 1978

Sulfides <300 300–1300 1300–6000 >6000 Wildish et al. 1999

4.5.8. Case histories describing benthic responses to salmon farming.

Brooks (1991a, 1992, 1993a, 1994a, and 1995a) evaluated a salmon farm located in a

poorly circulated bay with maximum current speeds of less than 8 to 10 cm-sec. This

farm is situated in deep water (30–33 m MLLW) over fine-grained substrates containing

820–50% silt and clay mixed with sand. The farm has produced as much as 863 mt of

Atlantic salmon in one year. TOC remained constant near the baseline mean of 1.067%

at all stations until 1990 when production increased. By 1990, TOC at the periphery of

the farm increased to 2.48% and remained within a range of 1.85 to 2.95 from 1990 until

1995 while significant quantities of salmon were being produced. This level of TOC in

sediments containing less than 50% fines (silt and clay) resulted in a significant change in

the benthic community.

Reductions in the infaunal community were generally restricted to distances less than

22*m, and in 1992 and 1993 a normal benthic community was observed at distances as

close as 6 m from the farm perimeter. The biomass of salmon on site during the period

immediately preceding the survey was significantly greater in 1995 (453,229 kg) than in

previous years (134,577 kg in 1994). The effects of this were seen in the increased TOC

at all far-field stations. Sediment organic carbon was very sensitive to farm operations

and highly correlated with management practices.

The number of infaunal species was determined at the same stations used to measure

TOC. The results indicated a reasonably homogeneous benthic community over the 60 m

sampling transect during the baseline survey. Infaunal diversity decreased at stations less

than 6 m from the perimeter of the farm very shortly after operations began in 1989.

Species diversity was variable at stations >15 m from the perimeter of the farm following

start-up. In general infaunal diversity exceeded baseline values at stations >30 m in all

years except 1989, which was probably due to a 1,250 m3 oil spill in the harbor several

months prior to the survey. In years following that accident, infaunal diversity at all

stations greater than 15 m from the farm perimeter were elevated above the 1987 baseline

value. However, the 15 m station suffered a significant decline in species during 1995

when production peaked.

Total invertebrate abundance was more sensitive than diversity to organic carbon input.

Except for the year of the oil spill, and 1995 when production peaked, infaunal

abundance was generally equal to or greater than baseline values at all stations greater

than or equal to 30 m from the perimeter of the farm. There was a consistent

amplification of abundance at the 60 m station in all years. Benthic impacts were

restricted to 15 m and less, except when production peaked. This reinforces the diversity
60

data and demonstrates that both abundance and diversity were sensitive to organic carbon

input. Over the history of this farm the distance at which adverse effects on benthic

community were observed varied between 6 m and 30 m downstream from the farm

perimeter. These effects were dependent on the biomass of fish being raised and the

resulting sediment concentrations of organic carbon.

Sediment organic carbon was reduced to less than baseline values between 30–60 m

downstream where there was a significant increase in the number of species (average of

106 species per station) and their abundance (9,367 animals per station, which was over

twice the baseline average of 4,552). No cause and effect relationship between this

amplification and the reduced TOC at stations 30 m and 60 m was investigated. Brooks

hypothesized that the increased infaunal biomass was consuming the missing TOC.

In contrast, Brooks (1994b and 1995b) documented sediment chemistry and infauna

downstream from a salmon farm located in a well-flushed passage with maximum current

speeds in excess of 125 cm-sec-1. The water was shallow (15–18 m MLLW) and the

bottom consists of large gravel, cobble and rock mixed with small amounts of sand, silt,

clay and broken shell. The site was used for final grow-out as part of a complex, which

produced approximately 3,000 mt of Atlantic salmon per year. Monitoring results

demonstrated the positive environmental effects associated with this farm, which had

been operating continuously for more than 10 years in the same location. A total of 3,953

infaunal organisms distributed in 116 species were observed at the 60 m control station in

1994. The abundance and diversity of benthic infauna was enhanced at all stations closer

to the farm with a maximum of 7,350 animals distributed in 173 species observed at the

30 m station. On the periphery of the farm 4,207 animals were observed, distributed in

142 species. Annelids dominated the infaunal community and the annelids C. capitata

(16%) and Prionospio steenstrupi (17%) were abundant in the immediate vicinity of the

farm. However, arthropods and surprisingly mollusks (Mysella tumida and Macoma

spp.) were well represented in these samples. The abundance and diversity of infaunal

organisms was positively correlated with sediment TOC, suggesting that organic carbon

was limiting the infaunal community throughout the area. Significant numbers of fish,

shrimp and other megafauna were observed during each annual survey at this site, which

appeared to function as an artificial reef. Three salmon farms located in close proximity

all shared the same characteristics. They appeared to attract megafaunal predators and to

enhance the infaunal and epifaunal communities.

4.6. Recovery and Remediation of Sediments

Chemical and biological recovery of sediments under salmon farms has been documented

by, inter alia, Ritz et al. (1989), Anderson (1992), Mahnken (1993), Brooks (1993b),

Brooks (2000a), Lu and Wu (1998), Karakassis et al. (1999) and Crema et al. (2000).

4.6.1 Chemical remediation

Brooks (2000a) defined chemical remediation as the reduction of accumulated organic

carbon with a concomitant decrease in hydrogen sulfide and an increase in sediment

oxygen concentrations under and adjacent to salmon farms to a level at which aerobic

organisms can recruit into the area. At the farm being studied sediment concentrations of
61

volatile solids declined rapidly as soon as harvest was started in June of 1996 and they

were close to control values when the harvest was completed in April of 1997. By the

end of the 10-month harvest, significant differences (α = 0.05) in TVS were not observed

between the mean for all reference area data and farm stations located at 5, 10, and 15 m

from the net-pen perimeter. Chemical remediation resulted in increased levels of oxygen

in sediment pore water and decreased levels of H2S and/or ammonia. H2S was evaluated

organoleptically. High levels of sediment H2S were evident to 20 m during peak

production. Moderate levels of H2S were observed as far as 37 m on the downstream

transect. H2S was detectable at low levels to distances less than 50 m from the net-pen

perimeter at the peak of production. It was moderately well correlated with other

physicochemical parameters (r = 0.68 to 0.69).

4.6.2 Biological remediation

Biological remediation was defined by Brooks (2000a) as the restructuring of the infaunal

community to include those taxa representing at least 1% of the total invertebrate

abundance observed at a local reference station. Recruitment of rare species (those

representing <1% of the reference area abundance) into the remediation area is not

considered necessary for biological remediation to be considered complete.

Brooks (2000a) observed the beginning of biological remediation during the harvest

period. Biological remediation appeared to be nearly complete 5 months following

harvest. Several infaunal series are apparent in his data. These were initially identified

using principal components analysis. The results are presented in Figure 1.

Farm inputs (fish biomass and 30-day feeding rate) associated in Group I were positively

correlated with several sediment physicochemical variables including percent fines, total

volatile solids and the presence of hydrogen sulfide. There was also a significant and

positive correlation between the opportunistic polychaetes C. capitata and O. vivipara,

and farm inputs.

Species identified in Group II were not strongly negatively correlated with farm inputs.

However these species all shared at least one of two characteristics. Larval shrimp

(LSHRIMP), and crab megalope larvae (BRACHMEG) are mobile organisms which live on

top of the sediments, enabling them to avoid the anaerobic conditions associated with

high organic loading. The amphipods, Jassa falcata (JASFAL) and Metacaprella

kennerlyi (METKEN), and barnacles in the Class Cirripedia (CIRRI), were found in great

abundance on the farm structure. Their presence on anaerobic sediments containing high

amounts of volatile solids probably represented an ephemeral benthic community derived

from the net-pen structure.
62

Figure 1. Output from a Varimax normalized principal components analysis of the

dominant infauna, farm inputs, and sediment physicochemical parameters. (From Brooks

2000a).

Key for Group II organisms

LSHRIMP – Larval shrimp

BRACHMEG – crab megalope larvae

JASFAL – the amphipod Jassa falcata

METKEN – the amphipod Metacaprella kennerlyi

CIRRI – barnacles in the Class Cirripedia

Factor Loadings, Factor 1 vs. Factor 2

Rotation: Varimax normalized

Extraction: Principal components

Factor 1

Factor 2

DATE

DISTANCE

AACUT

AMPHAR

CAPCAP

CHSETO

CIRRSP

D_PSEUDO

ETLONGA

EXOMOL

LEITPUG

LEPSQUA

LUMSP

LUMBIC LUMLUTI LUMSIM

LUMZON

MALDSP

MEDSP

MIROCUL

NEPHFER

NICLUMB

NOTCAL

PECTGRAN

PHYLCIT

PHYLMAD

PHYLMAC

PHYLSP

POLYNSP

OPHVIV

SPIBOM

SPISP

SYLELONG

SYLSP

TERRIB

THMULTI

UNIDANN

JASFAL

LSHRIMP

MEGASP

METKEN

CIRRI

BRACHMEG

AXSER

COOSUB

LUCANN

NUCTEN MYTUM

ALGAUS

BITSP

ODOSP

AMPHIO

NEMA

ABUND

DIVERS

SHANNON

PIELOU

MARGALEF

FINES

TVS

BIO_1000 FEED_100

H2S

RPD

-0.8

-0.6

-0.4

-0.2

0.0

0.2

0.4

0.6

0.8

-0.4 -0.2 0.0 0.2 0.4 0.6 0.8 1.0

Group I

Group IV

Group III

Group II
63

Group III organisms were early colonizers following chemical remediation. Organisms

in this group demonstrated a range of tolerance to sedimented organic carbon. Chemical

remediation occurred very quickly at this site and the order of recruitment into the area

was more likely a function of when the various taxa spawned than of sediment TVS

concentrations. Finally, the organisms in Group IV were strongly negatively correlated

with farm inputs. These organisms were least tolerant of sedimented carbon, or recruited

late in the year. It is also worthy of note that Shannon’s diversity index, Margalef’s

index, and infauna-diversity were more negatively correlated with farm inputs than any

of the individual taxa. These data suggested at least three invertebrate series, as follows:

Concentrations of organic carbon

High Medium Low

Capitella capitata Nematoda Lepidonotus squamatus

Ophryotrocha vivipara Mediomastus sp. Cooperella subdiaphana

Eteone longa Syllis elongata

Lumbrineris sp. Notocirrus californiensis

Other measures of biological integrity (Shannon’s diversity index and Margalef's index)

were also evaluated. Striplin Environmental Associates (1996) found that Shannon’s

index varied between 1.09 and 1.53 at Puget Sound reference stations where the percent

fines (silt and clay) was less than 20% and water depths were <45 m. Brooks (2000a)

found relatively high values of Shannon’s index (2.6 + 0.4) at the reference station.

These values suggest that the undisturbed infaunal community was diverse and evenly

distributed. Low values of Shannon’s index suggest a community dominated by a few

species. This condition was evident to 50 m and possibly as far as 100 m from the

perimeter of the net-pens on the down current transect during the peak of the production

period. Shannon’s index increased steadily following the initiation of harvest and an

enhancement of the invertebrate community was suggested by this index at the end of the

5-month fallow period.

Anderson (1992) aggregated the taxa identified in three replicate Ponar grab (0.05 m2)

samples at each station at fallow farms in Canada BC, and found H’ values varying from

0.108 to 1.465. The lowest values were found at stations with high TOC loading

dominated by C. capitata, Nephtys cornuta, and the gastropod Mitrella gouldi. The

higher values were generally associated with undisturbed reference stations. He used

principal components analysis (PCA) to observe that factors fallow time, biomass,

percent fines, total taxa richness and Shannon’s index (H’) were positively correlated

with each other and negatively correlated with TVS, coarse sand, gravel, and sulfide. He

concluded that high values of TVS and sulfide were indicative of unhealthy ecological

conditions. Anderson (1992) observed recovery times that varied between several

months at sites with low initial impact to an estimate of two years for severely impacted

sites during which physical, chemical and microbial processes acted on sediments to

make them hospitable to macrofaunal colonization. This refractory period was referred

to as chemical remediation by Brooks (2000a). Once macrofaunal colonization began

Anderson (1992) observed an increased rate of recovery.
64

In Washington State Brooks (1993b) found recovering sediments dominated by N.

cornuta, Glycera, and Lumbrineris, with few C. capitata in the vicinity of a fallow

salmon farm in Port Townsend Bay, Washington. He hypothesized that, following

cessation of production in October 1992, an initial period of chemical remediation was

followed by a proliferation of opportunistic C. capitata. As the organic load was

dispersed and catabolized by microbes, and the oxidation-reduction potential increased,

predatory polychaetes in the genera Nephtys, Glycera, and Lumbrineris flourished by

preying on the large standing crop of smaller prey species.

Mahnken (1993) studied the succession of invertebrates at a depositional environment in

Clam Bay, Puget Sound, for two years during a fallow period at a salmon farm and

observed two distinct 'stanzas' of biological recovery. The first was a three month period

of rapid recovery in abundance and species diversity followed by a 3–25-month period

when community recovery proceeded more slowly. Species which were numerically

dominant in samples from the reference station showed rapid colonization. Rare species

were slow to recruit to the area. He identified four successional series including:

• A pre-successional series comprised of species tolerant of sediments having high

TOC.

• A pioneering group of early colonizers containing several species of organic-tolerant

opportunists.

• An intermediate group of colonizers associated with reduced numbers of deposit

feeding opportunists.

• A group of late colonizers consisting of a group of more conservative and persistent

species.

A fifth group of rare species identified at the reference station were still absent from the

farm sediments at the end of the 20.5 month study. Mahnken (1993) observed that

succession was most clearly defined in the Order Polychaeta. At the Clam Bay site

biological recovery was initiated by C. capitata and followed in successive series

characterized in turn by Armandia brevis, Phyllodoce maculata, Pectinaria granulata,

Platynereis bicanaliculata, and finally by more generalist species like Leitoscoloplos

pugettensis. He concluded that the sequence was best described as a response to

changing organic content in the sediments, resulting from biogenic reworking by

changing guilds of benthic organisms.

Brooks (2000a) conducted an exhaustive study of a salmon farm in BC during production

and fallow periods over a period of two years. This was the first study documenting the

relationship between salmon farm biomass, fish feed inputs, and the physicochemical and

biological response of the benthos. The study design focused on quarterly samples

collected on the downstream transect from the net-pen perimeter to a distance of 75 m,

and at a local reference station located approximately 1,200 m from the farm. A

maximum Atlantic salmon biomass of 1,199 mt was raised at the farm under study. His

data clearly depicted the accumulation of volatile organic material under the farm and out

to distances of ca. 40 m from the net-pen perimeter during the peak of production. The

physicochemical data (TVS, TOC, hydrogen sulfide, zinc, and depth of the reductionoxidation potential (RPD) discontinuity) were well correlated and internally consistent.
65

Organic carbon accumulations (TOC or TVS) were sensitive indicators of biological

effects. The regression approach taken in the experimental design allowed for the threedimensional mapping of these parameters describing the spatial (as a function of distance

from the net-pen perimeter on the downstream transect) and temporal (as a function of

both season and production cycle) trends in the data.

In all of these cases chemical and biological recovery of the benthos occurred within

weeks or months at some sites, and within two to three years at others. These benthic

recoveries have occurred naturally with no need for intervention or mitigation.

4.6.3 The assimilative capacity of the local environment

Brooks (2000a) provided a methodology for estimating the assimilative capacity of

sediments adjacent to salmon farms. The upper 90th percentile TVS observed at the local

reference station was 3.4%. In Figure 2 this value is represented by the boundary

between dark green and light blue. Based on the assumption that the 90th percentile TVS

observed at the reference station represents the sediment assimilative capacity (SAC), this

analysis suggested that a maximum salmon biomass of ca. 170 mt could be raised at this

site without exceeding the SAC on the perimeter of the farm. That is 14% of the actual

farm production. A similar methodology could be applied to other physicochemical

benchmarks including sediment sulfides or Eh.

4.7 Managing the Environmental Effects Associated with Salmon Farms

4.7.1 Monitoring experiences

From 1987 until 1996 the Washington State DNR required monitoring of sediment

chemistry (carbon, nitrogen, redox and sediment grain size), water chemistry (dissolved

oxygen, pH, nitrate, nitrite, total ammonia and unionized ammonia), and the benthic

community (quantitative infaunal surveys and qualitative scuba surveys) as a condition in

ALLs for salmon farms. That monitoring experience provided an extensive database

upon which to evaluate the effectiveness of each measured parameter in predicting

environmental effects. Several lessons were learned from those studies, as follows:

(a) Sediment grain size and water depth were primary factors determining the

structure of an undisturbed infaunal community.

(b) Absent any anthropogenic inputs, i.e., in reference areas, the TOC content of

undisturbed sediments was significantly correlated with the proportion fines (silt and

clay) contained in superficial sediments (<2 cm depth). Depositional areas associated

with slow current speeds and gyres accumulate both fine sediments and particulate

organic materials at higher rates than high-energy areas.

(c) The redox potential and health of the infaunal community associated with a

particular sediment grain size distribution appears well correlated with the level of TOC

in the sediments (Striplin Environmental Associates 1996, Goyette and Brooks 1999).

This is evident in Figure 3, which depicts the relationship between infaunal abundance,

diversity, redox potential, and percent TOC. Note that the significant depressions in

infaunal diversity and abundance observed at distances of zero and 6 m from the

perimeter of the net-pens was associated with TOC levels averaging 2.8% and an RPD
66

Figure 2. Surface contour plot describing the relationship between salmon biomass (kg),

distance from the farm perimeter on the downcurrent transect in meters, and TOC

expressed as a proportion of dry sediment weight.

z=0.021-0*x+5.859e-8*y+2.25e-6*x*x-6.028e-10*x*y-1.415e-14*y*y

Distance from netpen perimeter in meters

Biomass of salmon in kilograms

 0

 60000

 120000

 180000

 240000

 300000

 360000

 420000

 480000

 540000

 600000

 660000

 720000

 780000

 840000

 900000

 960000

1020000

1080000

0 10 20 30 40 50 60 70 80 90 100 110 120 130 140 150 160 170 180 190 200

 0.011

 0.016

 0.021

 0.026

 0.031

 0.036

 0.041

 0.046

 0.051

 0.056

Sediment TVS (Proportion dry weight)

Upper 90th percentile TOC at the local reference station

Maximum salmon biomass not exceeding

the upper 90th percentile TOC observed

at the local reference station at a distance

of 30 meters from the netpen perimeter.

Approximate salmon biomass not exceeding 

the sediment's assimilative capacity.
67

that was very close to the sediment surface. These sediments smelled strongly of

hydrogen sulfide. Beyond 6 m the TOC declined rapidly to 1.8% and the depth of the

RPD increased to approximately 1.0 cm. Conditions remained constant to 24 m from the

farm perimeter where TOC slowly declined to background levels of ca. 1.25%. Infaunal

samples were not collected at all TOC stations during this study. However, sediments

were depauperate from the perimeter of the farm to 6 m downstream. The abundance and

diversity of infauna slowly increased between 6 and 30 m downstream but remained

depressed to a distance of 30 m from the net-pen perimeter. A normal community was

observed in samples collected 60 m downstream from the perimeter of this farm.

0

100

200

300

400

500

600

700

0

102030405060708090

100110120130140150160170180190200

Distance from farm perimeter (feet)

Infaunal Abundance/10 and Diversity

0.00

1.00

2.00

3.00

4.00

5.00

6.00

Total Organic Carbon (%) and RPD (cm)

Diversity

Abundance

12/95 TOC

12/95 RPD

Figure 3. Relationship between percent total organic carbon, depth of the reductionoxidation potential discontinuity (cm), Washington State TOC triggers, and abundance

and diversity of infaunal organisms at a major salmon farm located in a deep (33 m

MLLW) bay where maximum currents speeds were less than 10 cm-sec-1.
68

Based on these monitoring reports, it appears that TOC can be used as a screening tool to

evaluate benthic health indirectly. This is not unlike the use of bioassays as a screening

tool in evaluating the effects of toxic industrial and municipal effluents in fine-grained

sediments. The use of TOC (or TVS) as a screening tool has the advantage of being fast.

Analyses can be completed in a few days, whereas infaunal community analysis takes

months. In addition, the lower cost of TOC/TVS analysis allows more frequent

monitoring. When combined, these factors allow TOC/TVS to be used as a real-time

parameter useful to farm managers.

Sediment total sulfides and oxidation-reduction potential measured with ion specific

probes immediately following sample collection are emerging as more biologically

relevant physicochemical endpoints in ongoing studies in BC. The results of these

studies will be available in May 2001.

(d) Invertebrate community analysis has been a traditional and direct way of

evaluating the effects of organic loading (see Pearson and Rosenberg 1978, Lunz and

Kendall 1982, Weston 1990, Brooks 1993 and 1993b, Henderson and Ross 1995, Brooks

1994a, 1994b, 1995a, and 1995b). In Washington State invertebrate infaunal community

analysis is used as a primary endpoint for evaluating benthic sediment quality (WAC

173–204–320).

(e) Salmon farms located in well-flushed (>50 to 100 cm-sec-1) environments

frequently increase both the abundance and taxa richness of infaunal communities, even

at high levels of salmon production (Brooks 1994b and 1995b).

(f) Salmon farms located in poorly flushed (<10 cm-sec-1) environments can result

in the deposition of significant amounts of carbon to the benthos – even when located in

water as deep as 30 m MLLW. Adverse effects are generally restricted to an area within

15–22 m from the perimeter of farms located in these poorly circulated environments.

Increases in both the level of TOC and the distance at which adverse effects are observed

are sensitive to farm management practices (Brooks 1994a). However, in these poorly

flushed environments the negative effects can be managed so that they remain within 33–

100 m of the farm perimeter, even during intensive production of fish.

(g) Indicator invertebrate taxa have been identified at several of the farms studied

in the ALL Program of DNR. These indicator taxa and groups of taxa appear temporally

consistent but are specific to different environments (Brooks 1995a and 1995b). Other

authors (Weston 1990, Tsutsumi et al. 1991, Mahnken 1993, and Henderson and Ross

1995) have identified similar suites of indicator species in response to organic loading.

4.7.2 Management by modeling salmon farm wastes

There is significant interest in modeling salmon farm waste as a management tool for

regulatory agencies. Some of these models are qualitative (Sowles et al. 1994) and others

attempt to quantify the dispersal and accumulation of particulate organic matter in

sediments (Fox 1990, Gowen et al. 1994, and Silvert 1994b). It appears that the more

basic the model inputs, the more room there is for error. Silvert (1994a) used a simple

carbon budget to model salmon farm waste and concluded that 40% of the feed was not

consumed by the fish. There is no evidence in the literature substantiating feed loss rates

this high. None of these models has been tested to compare predictions with observed

carbon deposition rates or sediment physicochemical responses to salmon farm waste.
69

Findlay and Watling (1994) modeled sediment organic carbon decay rates and developed

nonlinear regression equations relating oxygen delivery (mmoles/m2-hr) and maximum

oxidizable organic matter (grams carbon/m2-day) to sediments as a function of current

speed (cm/sec). They concluded that the maximum carbon flux not exceeding the

assimilative capacity of the sediment is highly dependent on the minimum 2-hour average

bottom current speed.

Silvert and Sowles (1996) developed several algorithms considered useful in modeling

the environmental response to salmon farming. They concluded that models exist which

can help to assess impacts and make reasonable management decisions, but this is not

substantiated in the existing literature.

These models provide some insight into the environmental response to salmon farm

waste. However, they are not adequate for making reasonable quantitative predictions

regarding the degree or spatial extent of salmon farm waste.

4.7.3 Risk management through NPDES permit standards

In 1996 Washington State developed sediment management standards for marine netpens (WAC 173–204). The Washington State rule is based on the following

assumptions:

(a) Salmon farming provides significant benefit to the State and its people.

(b) The negative benthic effects associated with net-pen operations in poorly

flushed environments will remediate naturally following cessation of operation or

initiation of a fallow period.

(c) The spatial extent of these effects can be managed. The sediment rule for netpens authorizes a sediment impact zone (SIZ) extending 33 m from the perimeter of the

farm structure. This distance was chosen because it corresponds to the SIZ provided for

other industrial discharges. From a biological point of view, it would seem more

appropriate to develop site specific SIZs which reflect the biological productivity of the

site’s benthos and the presence of adjacent valuable resources. In that context, SIZ

widths could extend considerably further from the perimeter of a farm, perhaps to a

distance of 100 m or more.

(d) TOC can be used as a screening tool in evaluating the health of the benthos.

TOC 'triggers' have been defined as a function of the proportion of silt and clay in the

sediment matrix. TOC triggers used to screen sediments for adverse biological effects at

salmon farms in Washington State are tabulated below. If sediments located 33 m from

the perimeter of the net-pen structures at salmon farms exceed these trigger values, then

an evaluation of the health of the infaunal community is required.

Proportion (%) silt-clay

in the sediments

TOC trigger (%)

0 – 20 0.5

20 – 50 1.7

50 – 80 3.2

80 – 100 2.6
70

(e) Biennial monitoring of sediment TOC is required at seven stations at each

permitted farm. Four of these stations are located at a distance of 30 m from the

perimeter on each side of the farm. Three replicate sediment samples are collected at

each station. No further monitoring is required if sediment TOC is not statistically

elevated (t-test) above the TOC trigger corresponding to the observed percent fines at

each 30 m station. If the measured TOC is significantly higher than the corresponding

trigger, then repeat sampling is required in the summer of the next year together with the

collection of five benthic infaunal samples at each station failing the TOC trigger, and at

a suitable control. Benthic infaunal analysis is required for any station at which elevated

TOC is observed during the second round of sampling.

(f) Each farm is required to manage its production such that there are no

significant negative effects on benthic resources beyond the boundary of this 33-m SIZ.

WAC 173–204 states that biological resources in sediments are considered adversely

impacted if the mean numbers of crustaceans, mollusks or polychaetes in the test

sediment at the boundary of the SIZ are reduced to significantly less than 50% of the

number of animals belonging to the same taxa living in an undisturbed reference

sediment. Evaluation is based on a one tailed t-test at α = 0.05 for five replicate 0.1 m2

samples. It should be pointed out that populations of benthic organisms are frequently

found in patchy distributions with many animals of the same species confined in groups

separated from each other. Infauna are seldom found regularly distributed in sediments.

For that reason, if three samples were collected from the same general area, the individual

samples would likely contain very different numbers of any one of these taxa. The

reason that the rule relies on a 50% reduction in the number of any taxa is not that it is

acceptable to kill 50% of the crustaceans, mollusks, or polychaetes outside the boundary

of the sediment impact zone, but to acknowledge that the collection of a reasonable

number of random samples may produce two means which vary by as much as 50%, even

though the sediments are not impacted at all, or share the same level of impact.

(g) Benthic conditions at each of the four orthogonal 30 m SIZ stations must be

photographically documented every two years and whenever sediment samples cannot be

collected and analyzed in conformance with the requirements stipulated in the Puget

Sound estuary protocols (PSEP 1986).

(h) Well-managed salmon farms recognize the benefits of vaccination and BMPs

in controlling disease. While not examined in this review, records of antibiotic use in

Washington indicated a sharp decline at permitted farms between 1992 and 1996.

Similarly, Kontali (1996) reported that the use of vaccines in Norway had resulted in

reductions in the use of antibiotics from a high of 592 mg/kg salmon produced in 1987 to

5, 9 and 3 mg/kg in 1994, 1995, and 1996, respectively.

Based on the current low use, Washington regulations (WAC 173–204–412) do not

require routine monitoring for bacterial resistance at marine net-pet sites. All farms are

required to maintain an operational log that specifies the date and nature of application of

all disease control chemicals used. In addition, farms are required annually to report the

amount of each therapeutic used on each farm.

Based on the absence of adverse effects observed during 10 years of monitoring the water

column adjacent to salmon farms in Washington State, the WDOE eliminated all
71

requirements for nutrient and dissolved oxygen monitoring in the water column from the

NPDES permits.

This approach by the State of Washington regulatory agencies is appealing for several

reasons:

• It recognizes the value of net-pen culture while requiring that any negative impacts be

restricted to the immediate vicinity of the farm

• It invokes a realistically achievable performance standard that can (must) be met

through proper management practices

• It is a relatively inexpensive approach as long as TOC levels at the boundary of the

SIZ remain below trigger levels. This provides a real incentive to maintain carbon

levels below specified triggers

• The immediate endpoint (TOC) can be measured quickly and is useful as a real time

management tool

• The performance standard encourages future siting in environments that either have

fine grained sediments that support high TOC levels, or in high current areas where

TOC will not accumulate

On the other hand there have been some problems in implementing the State's NPDES

permit system. For example, sediment samples collected from coarse bottoms cannot be

analyzed for TOC because the matrix must be ground to a fine consistency. Sediments

from erosion environments are generally composed of coarse gravel and cobble.

Opponents of aquaculture have argued that the WDOE biological performance standard

defined in WAC 173–204–320 (3)(c) is inappropriate because it allows for up to a 50%

reduction in the abundance of arthropods, mollusks, or annelids, and because it does not

include some measure of species richness (PCHB Nos. 96–257 through 96–268). This

criterion applies to all discharges in the State of Washington and not just to salmon farms.

Application of the criterion requires analysis of these major taxa in five 0.1 m2 infaunal

samples. A one-tailed t-test is then applied with α = 0.05. Alpha is the probability of

finding an effect when it does not exist (the probability of making a Type I error or of

rejecting the null hypothesis when it should not be rejected). That means that

approximately 1 in 20 tests will indicate a statistically significant difference in the means

of the populations when in fact the populations are identical. Brooks (2001, unpubl. data,

Aquatic Environmental Sciences, Port Townsend, WA 98368) has tested this hypothesis

using a Monte Carlo approach for analyzing benthic data from reference sites at two

farms located in Puget Sound. He found that the null hypothesis was in fact rejected in

22% of the analyses on samples collected from the same reference station. Obviously,

absent the allowable error of 50% incorporated in the WDOE rule, the criterion would be

too conservative.

The consequences to the permittee of failing the benthic biological criteria are significant,

requiring reductions in the number of fish raised, or the amount of food provided, or

actually fallowing the farm for a period. That is a significant penalty when there is a half
72

chance that failure is simply a matter of chance with α = 0.05. There are at least three

ways to address this issue:

(a) The value of α could be decreased to 1% or 0.5%. When α = 0.1%, there is

only a one in 100 probability of obtaining a false positive (Type I error). That would

require a larger difference between the mean number of animals in any of the taxa

observed at the reference site and the SIZ boundary – in other words it would not provide

any more protection for the environment,

(b) The DOE has defined an allowable error term of 50%,

(c) The number of endpoints at each station could in increased by evaluating both

the abundance and the number of species observed in each of the major taxa. This would

provide six endpoints (abundance and richness of arthropods, mollusks and annelids) for

evaluation. By requiring failure of two of these endpoints before considering the station

failed, the probability of a false positive would be decreased to 0.05 x 0.05 = 0.0025.

4.7.4 Risk management practices in British Columbia

Following the exhaustive review of the scientific literature by EAO (EAO 1997), the

Provincial Government of Canada BC has been developing a performance-based waste

management policy (WMP) to insure that adverse benthic effects associated with salmon

farming are managed. The following are essential elements likely to emerge.

(a) Only single year-classes of fish will be grown at BC salmon farms. The

purpose of this restriction, as practiced also in Norway and Chile since the mid-1990s, is

to reduce the potential for disease transfer between year-classes and to provide for a

fallow period between production cycles sufficient to insure that sediments chemically

remediate to within 30 m of the farm perimeter prior to restocking.

(b) Prior to restocking a new year-class, the farm must remain fallow until the

level of volatile residue in sediments at a distance of 33 m from the net-pen complex

perimeter returns to baseline or local reference station values. The length of fallow is not

specified, but farm management must certify to the Ministry of Environment that this

condition has been met before restocking fish.

(c) At no time will adverse benthic effects be allowed at distances >100 m from

the perimeter of the net-pens. This performance standard will be evaluated annually

during the months of August through November. This distance is under review and will

likely be set by the BC Government during 2001.

(d) Based on the problems encountered with the analysis of TOC in Washington

State, BC is using TVS as a primary screening tool. TVS (as a percent of dry sediment

weight) must not statistically exceed (one-tailed t-test, α = 0.05, N = 3) the upper 90th

percentile value observed at a local reference station. Samples are collected for this

analysis at a distance of either 30 m (for the pre-stocking certification) or 100 m (for the

annual monitoring) from the midpoint on each of the sides of the net-pen’s perimeter.

These points are referred to as the 'inner' and 'outer' sediment impact zones (ISIZ and

OSIZ). If no local reference station is available, then farm samples will be compared

against TVS triggers which represent the upper 90th percentile of historical TVS levels

observed at reference stations throughout BC.

(e) Hargrave et al. (1997) examined the biological and physicochemical attributes

at 11 salmon farm and 11 reference stations in the Western Isles region of the Bay of

Fundy on the east coast of Canada. They found that organic carbon, sediment sulfides,
73

and redox potential were effective endpoints for evaluating the benthic effects associated

with salmon farming. The results of this study have been incorporated in the WMP by

requiring quantitative evaluation of sediments for total sulfides (S=) and oxidationreduction potential (ORP). Protocols developed by Hargrave et al. (1995) were adopted

for these analyses. Specific performance standards for sulfides and Eh will be developed

pending the outcome of a series of focused studies designed to determine the biological

response to varying concentrations of these endpoints.

Stations failing the screening tests will probably be evaluated against the biologicallybased performance standard which states that, 'Adverse Sediment Biological Effects will

be evaluated by comparing abundance and diversity (number of species) in the Class

Crustacea, Class Polychaeta and the Phylum Mollusca at farm sample stations defined in

the performance standards with the abundance and diversity of the same taxa found at a

local reference station. This test will establish six endpoints for evaluation (abundance

and diversity in each of three major taxa). These differences shall be evaluated using a

one-tailed t-test with a probability of observing an effect when one does not exist of five

percent (a = 0.05). Because one in twenty of these tests are expected to produce a false

positive (indicates an adverse effect when one does not exist), this performance standard

defines adverse biological effects when two or more of the six endpoints are statistically

decreased compared to levels observed at a local reference station. This procedure will

still result in one false positive in 400 tests.

This biological standard will be determined by comparing the three major taxa, observed

in five 0.1 m2 grab samples at each farm station with the abundance and diversity of

these taxa observed at a local reference station sharing similar depth and sediment grain

size characteristics. This may require more than one local reference station per farm.

Identification of all taxa in this evaluation will be to the level of species, or the lowest

practical level. Ammann et al. (1997) used the results from 28 previous studies to

examine the Taxonomic Sufficiency of various levels of biological organization to

determine adverse impacts in aquatic environments. They found that for 89% of the

experiments evaluated, phyla counts were as sensitive as any of the metrics evaluated.

Community metrics (Shannon-Weiner’s, Simpson’s, and Brillouin’s diversity and

evenness and richness) were never found to be more sensitive than count data. Amman et

al. (1997), and the citations included therein, support British Columbia’s choice of major

taxa (Phylum Molluska, Class Crustacea and Class Polychaeta) as appropriate metrics

in developing their regulatory policy. The identification of organisms to species will

allow for future analysis using a variety of additional metrics.

Farms with stations failing the Sediment Biological Effects Standard will be required to

develop a remediation plan that brings the farm back into compliance.'

The BC Provincial Government has stated a desire to establish a final performance based

salmon farm management program in the fall of 2001. In addition, the DFO, which has

the responsibility to enforce the Fisheries Act is participating at the technical level in

developing the BC program.
74

5. ATLANTIC SALMON AND THE LOCAL ECOSYSTEMS

The fifth chapter is very specific to the pros and cons of salmon species in the

local ecosystem of the Northwest (Puget Sound). It has seven identified subsets.

The first subsection reviews the issue of the introduction of Atlantic salmon into

the Pacific ecosystem and the potential interactions. Specific sections review

possible hybridization between Atlantic and Pacific salmon, the genetic dilution

and alteration of the gene pool, the colonization of the aquatic environment by

Atlantic salmon, and finally the interactions of wild salmon and genetically

altered transgenics. The second subsection concerns epidemics and transmission

of waterborne disease, and reviews the potential for cultured Atlantic salmon, an

exotic species, to introduce new diseases into the local ecosystem. There are nine

specific items, from the diseases which might be involved, to potential

interactions, and current policies for disease control. The third subsection

concerns the potential ecological impacts in the Pacific Northwest, specifically

the interaction with Pacific salmon and predation. The following sections review

the effects of artificial propagation practices in the region in general, the impacts

of the introduction of non-indigenous species, and a comparison of escapes or

releases of propagated Atlantic and Pacific salmon. The last section examines the

NMFS Biological Status Reviews of west coast Pacific salmon stocks.

5.1 General Issues of Artificial Propagation of Salmonids

Ellis (1996) and Alverson and Ruggerone (1997) comment that the artificial propagation

of salmon and trout in the Pacific Northwest had come under increasing scrutiny in recent

years. This was due to the recognition that hatchery cultured salmon and trout may have

the potential to adversely impact natural populations. Although the weight of attention

has been focused on the extremely large complex of federal, state, tribal, and cooperative

hatcheries in Alaska and the western States, concerns about the potential adverse impacts

of private trout and salmon culture in Washington have also been expressed.

Concerns about genetic interactions, the transmission of disease, and ecological

interactions are most commonly voiced. The secondary source for this unpublished study

is Gross (1997), who stated that Atlantic salmon had the potential for hybridization with

Pacific salmon. Quinn (1997) stated that it was possible that the 369,000 Atlantic salmon

which escaped into Puget Sound in 1997 would produce 10 million healthy smolts in

local rivers. The Alaska Department of Fish and Game (ADF&G) has expressed concern

that escaped Atlantic salmon from west coast salmon farms will compete with wild

salmon and spread diseases and parasites for which Pacific salmon have little resistance

(ADF&G 1999). For example, a letter sent to Alaska Senator Stevens (April 25, 1997),

by a constituent, read, in part, 'The continued introduction of Atlantic salmon to the

marine habitat of British Columbia and Washington State will inevitably have negative

biological impacts. These will include displacement, hybridization, and the introduction

of alien....disease.' (Gilbertsen 1997).
75

5.2 Genetic Interactions of Artificially-Propagated Pacific and Atlantic Salmon

A major concern with artificial propagation in general and farming of Pacific salmonids

and Atlantic salmon in particular are the potential genetic effects of inadvertent escapees

on the native salmonids. For the salmon farming industry in BC, where both Pacific and

Atlantic salmon are extensively farmed, the BCSAR study listed four major areas of

concern (EAO 1997):

• Hybridization between Atlantic and Pacific salmon

• Genetic dilution and alteration of the wild salmonid gene pool

• Colonization by Atlantic salmon

• Interactions between wild salmon and genetically altered transgenics

These concerns are both geographically and species specific. For the Puget Sound, the

primary concern is with Atlantic salmon, as Pacific salmon, with rare exception, are not

cultured by private enterprises.

5.2.1 Hybridization

No genetic interactions between Atlantic and wild Pacific salmon have been reported in

the Pacific Northwest. Similarly, under controlled and protected laboratory conditions

where survival of hybrid offspring should be optimized, viable hybrids between Atlantic

and Pacific salmonid species are difficult to produce. Refstie and Gjedrem (1975),

Sutterlin et al. (1977), and Blanc and Chevassus (1979, 1982) found that crosses between

Atlantic salmon and rainbow trout failed to produce any viable progeny. A similar lack

of vitality was observed in pairings of Atlantic salmon and coho salmon (Chevassus

1979) and Atlantic salmon and pink salmon (Loginova and Krasnoperova 1982). Gray et

al. (1993) attempted to produce diploid and triploid hybrids by crossing Atlantic salmon

with chum and coho salmon, and rainbow trout. All embryos died in early developmental

stages, leading to the conclusion that hybridization of Atlantic salmon with Pacific

salmon species was unlikely to happen.

The secondary source of these two unpublished BC studies by Alverson and Ruggerone

(1997) have provided more data regarding the relative genetic compatibility between

Atlantic and Pacific salmon (R. Devlin, DFO Canada, reported in Alverson and

Ruggerone 1997). In the first, using a small number of eggs, Atlantic salmon produced

no viable hybrids with coho, chum, chinook, sockeye salmon, and rainbow trout. In the

same experiment, each species of Pacific salmon readily produced hybrids with between

two and five other Pacific salmon species, and confirmed previous observations in this

genus by, inter alia, Foerster (1935), and Seeb et al. (1988). These results were cited as

evidence of 'rampant hybridization potential' in hearings before the Washington State

PCHB (96–257–266, and 97–110, 1998). However, the Board found the statement not

supported by the study, and there was no reasonable potential for hybridization between

escaped Atlantic salmon and native Pacific salmon in Puget Sound based on current

knowledge and behavior (PCHB 1998).

In the second study using a much larger number of eggs, viable hybrids to hatch

involving rainbow and steelhead trout, coho, chum, chinook, and pink salmon were

produced. Approximately 6.1% of the steelhead x Atlantic salmon, and 0.01% of the
76

pink salmon x Atlantic salmon hybrids survived to the hatching stage. The inter-specific

crosses between Oncorhynchus species produced hybrids with survivals to hatch ranging

from 10–90% in 15 of the 42 crosses. Despite these high survivals to hatch among the

Pacific salmon hybrids, compared with the fractional survival to hatch observed between

an Atlantic salmon x pink salmon cross, no concerns over the introduction of hatchery

stocks of Pacific salmonids into natural habitats were addressed to the PCHB.

The 'successful' Atlantic x steelhead hybrids were carefully controlled experiments in

vitro, and actual Atlantic/steelhead hybridization would probably not happen under

natural conditions in Washington State. The Atlantic salmon stocks used in Washington

have finished spawning by the end of November (W. Waknitz, NMFS, unpublished data),

and wild steelhead in western Washington spawn between mid-March and mid-June

(Freymond and Foley 1985). Therefore, there is virtually no opportunity for Atlantic

salmon to spawn with local wild, native steelhead outside the laboratory.

While viable hybrids between Atlantic salmon and the Pacific salmonid species have

been difficult to produce in the laboratory and do not occur under natural conditions,

hybrids between Atlantic salmon and a sympatric species, the brown trout are relatively

successful. Viable Atlantic salmon x brown trout hybrids have been produced in the

laboratory by, inter alia, Suzuki and Fukuda (1971), Refstie and Gjedrem (1975), Blanc

and Chevassus (1982), and Gray et al. (1993).

Successful hybridization under natural conditions has been reported for Europe where

brown trout are native, and also in North America where the brown trout has been

introduced (Verspoor and Hammar 1991). The frequency of natural hybridization in

Europe and North America ranges from 0.1 to 13.2% of juveniles in river systems

(Jordan and Verspoor 1993) and appears to be increasing relative to pre-aquaculture

levels (Hindar et al. 1998). McGowan and Davidson (1992) cite the breakdown in prereproductive isolating mechanisms (abundance of mature Atlantic parr) as the principal

mechanism for natural hybridization. Hindar et al. (1998) reported that although a

disproportionate number of hybrids were the product of matings involving Atlantic

salmon females, there was no evidence that escaped farmed Atlantic salmon females

produced more hybrids than wild females. Youngson et al. (1993), on the other hand,

had previously reported that escaped female in western and northern Scotland rivers

hybridized with brown trout more frequently. Wilkins et al. (1993) found that male

hybrids were fertile and when back-crossed with female Atlantic salmon produced about

1% diploid progeny. Galbreath and Thorgaard (1995) reported that back-crosses between

male diploid, male triploid, and female diploid Atlantic salmon x brown trout hybrids and

both parental species produced either non-viable or sterile progeny.

No natural hybrids between Atlantic salmon and Pacific salmonids have been reported in

Europe. This is despite the fact that introduced rainbow/steelhead trout, brook trout, coho

salmon, and pink salmon have all established naturalized populations within the native

range of Atlantic salmon throughout the European continent (MacCrimmon and

Campbell 1969, MacCrimmon 1971, Berg 1977, and Lever 1996). Similarly, no hybrids

between Atlantic salmon and brown trout, rainbow trout or brook trout have been
77

reported in South America or New Zealand, even though all four of these species are not

native to those locations (MacCrimmon 1971, Lever 1996).

The propensity of Atlantic salmon to produce successful hybrids with brown trout and

not with the Pacific salmonids may be related to the phylogenetic distances that exist

between the two groups. Neave (1958) postulated that the putative ancestors of the

Salmo group migrated to the Pacific 600,000 to 1,000,000 years ago, were subsequently

isolated by land bridges, and evolved to the ancestral Oncorhynchid form. The ancestral

Oncorhynchid form subsequently developed to form the separate Oncorhynchus species

(Simon 1963). McKay et al. (1996), based on DNA sequence analysis of growth

hormone type-2 and mitochondrial NADH dehydrogenase subunit 3 gene, estimated that,

at a minimum, the major divergence between the genus Salmo and the genus

Oncorhynchus occurred 18 million years ago, while speciation within the genus

Oncorhynchus began about 10 million years ago. Benfey et al. (1989) also noted that the

evolutionary differences between the Pacific and Atlantic salmonids were reflected by

immunologically detectable forms of vitellogenin.

Attesting to their phylogenetic similarity, interspecific hybrids within the Oncorhynchids

are relatively successful. Foerster (1935) was among the first to report successful hybrids

between controlled mating of sockeye, chum, pink and chinook salmon. Since then,

limited occurrences of natural hybrids have been reported among anadromous salmonids.

Bartley et al. (1990) reported on natural hybridization between chinook and coho salmon

in a northern California river, and Rosenfield (1998) reported a natural pink x chinook

hybrid from the St. Mary’s River in Michigan. On the other hand, hybridization between

introduced rainbow trout and native cutthroat trout appears to be almost ubiquitous

throughout the interior part of western North America, and has been enormously

detrimental to the latter species according to Gresswell (1988) and Behnke (1992).

5.2.2 Genetic dilution and alteration of the wild salmonid gene pool

Adverse genetic and ecological effects due to releases or escapes of artificiallypropagated Atlantic salmon from public hatcheries and private net-pens on wild Atlantic

salmon populations in Norway, Scotland, Ireland, and the Canadian Maritimes have been

reported. For wild Atlantic salmon these include a reduction in their genetic adaptability

and capacity to evolve as a result of interbreeding with artificially-propagated fish, and

direct competition for food and space (Einum and Fleming 1997, Gross 1998).

Such adverse effects only happened in those locations because both the cultured and wild

fish were Atlantic salmon. Escaped Atlantic salmon on the west coast of North America

do not have congeneric wild individuals with which to interact. In the Pacific Northwest

region, the release of hatchery Pacific salmon has the greater potential to produce impacts

on native Pacific salmon which are analogous to those found between cultured and wild

Atlantic salmon in Europe and eastern North America.

Adverse genetic and/or ecological interactions on local wild salmon populations from

artificially-propagated Pacific salmon have been well documented by Weitkamp et al.

(1995), Busby et al. (1996), Hard et al. (1996), EAO (1997), Gustafson et al. (1997),
78

Johnson et al. (1997), Myers et al. (1998), and Johnson et al. (1999). No detrimental

effects related to Atlantic salmon have been reported in western North America.

Compared with the evidence in the literature of genetic alterations of Pacific salmonid

populations as a consequence of salmonid enhancement and supplementation programs in

the Pacific Northwest, there is little or no evidence in the literature of adverse impacts

associated with escaped Atlantic salmon in the region.

5.2.3 Colonization by Atlantic salmon

In the past century there have been numerous attempts in the US and elsewhere to

establish Atlantic salmon outside their native range. These attempts involve at least 34

different States, including Washington, Oregon, and California. None of these efforts

was successful. MacCrimmon and Gots (1979) subsequently reported that no

reproduction by Atlantic salmon was observed in the waters of these States, and twenty

years later this was reconfirmed by Dill and Cordone (1997) and Alverson and

Ruggerone (1997).

It also appears difficult to reintroduce Atlantic salmon to their native rivers. In the last

100 years, Atlantic salmon populations in New England have declined precipitously,

despite the large-scale introduction of locally derived hatchery fish (Moring et al. 1995).

The Penobscot strain of Atlantic salmon (which is used in net-pen farms in Puget Sound)

is now under consideration for listing under the US Endangered Species Act 1974

(USDOI/USDOC 1995).

Between 1905 and 1934 the government of BC released 7.5 million juvenile Atlantic

salmon into local waters, primarily on the east coast of Vancouver Island and the lower

Fraser River in Canada (MacCrimmon and Gotts 1979; Alverson and Ruggerone 1997).

These releases were not successful in establishing Atlantic salmon populations in the

Province, although some natural reproduction may have occurred according to Carl et al.

(1959). Emery (1985) noted that even in historic Atlantic salmon habitat, such as the

lower Great Lakes, attempts to re-establish Atlantic salmon populations have not been

successful, although Brown (1975) had earlier stated that introduced Pacific salmonids

had succeeded in establishing self-reproducing populations in that area.

Lever (1996) noted that, worldwide, no self-sustaining populations of anadromous

Atlantic salmon have been established outside the natural range of this species, although

a landlocked population appears to have become established in the mountains of New

Zealand. Reproduction by Atlantic salmon was also observed subsequent to introduction

in Chile and Australia, but these transfers also failed to create self-sustaining populations.

The failure of early introductions of Atlantic salmon to produce self-sustaining

populations could have been due to the rather primitive hatchery methods used in the

early 1900s. However, the same primitive methods that failed to establish Atlantic

salmon anywhere in North America proved to be remarkably successful in establishing

European brown trout, brook trout, and rainbow trout almost everywhere in the earliest

days of fish culture, usually on the first attempt. With these particular salmonids, the
79

success or failure of introduction appears to be associated with attributes inherent to the

species, not from the hatchery methods employed. Atlantic salmon are virtually the only

non-native salmonid not successfully introduced to Washington, with the exception of

Arctic char and Masu salmon (Wydoski and Whitney 1979).

The initial transfer of Atlantic salmon to Washington occurred in 1904, according to

MacCrimmon and Gots (1979), and Coleman and Rasch (1981) noted that attempts to

introduce runs of this species continued until about 1980. Occasional releases of Atlantic

salmon into high mountain lakes have since been made. Sea-run and landlocked strains

were used, but neither life-history form succeeded in establishing self-perpetuating

populations. Attempts to establish Atlantic salmon in Canada BC took place during this

period, with similar results, although successful spawning may have occurred in the

Cowichan River, Canada as specimens thought to have resulted from the planting of

Atlantic salmon were taken until May 1926, according to Dymond (1932), Carl et al.

(1959), and Hart (1973). The DFO has been carrying out a long term monitoring study

on the catches and sightings of individuals and to see is self-sustaining populations are

becoming established but without results (Thomson and Candy 1998). Recently Volpe et

al. (2000) reported that Atlantic salmon had successfully produced offspring in BC.

Several Atlantic salmon farmers in Washington rear juveniles in the Chehalis River basin

prior to transfer to seawater in Puget Sound. Since the mid-1980s escaped Atlantic

salmon smolts have been captured in traps designed to monitor the outmigration of

juvenile Pacific salmon (Seiler et al. 1995). However, as of 1998, no returning adult

Atlantic salmon have been encountered at adult salmon traps on several tributaries of the

Chehalis River system, or been caught in tribal gillnet fisheries, which capture about 10%

of all upstream migrants in the main stem of the Chehalis River (D. Seiler, WDFW,

personal communication).

The risk of anadromous Atlantic salmon establishing self-perpetuating populations

anywhere outside of their home range is extremely remote, given that substantial and

repeated efforts over the last hundred years have not produced a successful selfreproducing population anywhere in the world. In the Pacific Northwest Atlantic salmon

introductions also have not succeeded in producing self-sustaining populations, even

though a few naturally produced juveniles may have been observed from time to time,

according to Dill and Cordone (1997).

5.2.4 Interactions of wild salmon and transgenic fish

As with other agricultural sectors, there is considerable interest within the fish farming

sector to improve growth or survival of fish or shellfish through genomic manipulations.

In recent years the role of transgenics (descendants of genetically engineered parents

whereby introduced DNA has been incorporated and inherited) in traditional farming has

been a controversial topic.

The potential exists that transgenic fish, should they escape from fish farms, may

reproduce successfully with wild or other transgenic fish and produce offspring which

may eventually adapt to their local environments. This is a topic which will receive
80

considerable debate in the years to come. There is no evidence in the literature that

transgenic fish have been raised or are currently being raised in Puget Sound waters, and

there are no plans to raise them in the future.

5.3 Epidemics and the Transmission of Waterborne Disease

5.3.1 The origin and disease status of Atlantic salmon stocks in Puget Sound

In 1971 scientists from the NMFS Northwest Fisheries Science Center began testing the

feasibility of rearing New England stocks of Atlantic salmon in seawater net-pens in

Puget Sound to provide 3.5 million eyed eggs annually for restoring depleted runs in

southern New England (Mighell 1981, Harrell et al. 1984). Between 1971 and 1983

NMFS received eggs from many North American stocks, including the Grand Cascapedia

River in Quebec (via Oregon State), and the Penobscot, Union, St. John, and Connecticut

rivers in the USA.

All Atlantic salmon eggs sent to the NMFS Manchester Research Station were examined

according to the code of federal regulations (Regulation 50 CFR) and certified by federal

pathologists to be free of bacterial and viral pathogens prior to transfer from New

England to Washington. However, few eggs were ever sent back to New England due to

the reluctance of east coast fisheries managers to accept eggs from Atlantic salmon which

had been grown in waters inhabited by Pacific salmon. A panel of New England state

and federal fisheries officials met at Newton Corner, Massachusetts in March, 1984 and

determined that raising Atlantic salmon in Puget Sound had rendered the eggs unfit for

transfer back to the east coast because the risk of introducing Pacific salmon diseases to

New England Atlantic salmon populations was too great.

As a result of this decision, millions of Atlantic salmon eggs originally meant for New

England restoration programs were available for distribution to salmon farmers in

Washington. These eggs proved to be a boon to the local industry as, by this time, it was

clear from work in Norway and Scotland, that Atlantic salmon were superior to Pacific

salmon in all aspects of culture, including survival to hatching, growth rate in fresh and

sea water, and, contrary to east coast opinion, resistance to infectious diseases (Mighell

1981, Waknitz 1981).

5.3.2 Disease of salmonids

Freshwater salmonid diseases observed in Pacific salmon hatcheries in the Pacific

Northwest include furunculosis, bacterial gill disease, bacterial kidney disease, botulism,

enteric redmouth disease, cold water disease, columnaris, infectious hematopoietic

necrosis, infectious pancreatic necrosis, viral hemorrhagic septicemia, erythrocytic

inclusion body syndrome, and a large number of parasitic infections, such as

gyrodactylus, nanophyetus, costia, trichodina, ceratomyxosis, proliferative kidney

disease, whirling disease, and ichthyophonis. All these diseases are described in works

by, inter alia, Wood (1979), Leitritz and (1980), Foott and Walker (1992), and Kent and

Poppe (1998).
81

The frequency of occurrence of these pathogens in hatcheries appears to vary

geographically. For example, between 1988 and 1992, a greater percentage of hatcheries

in Alaska tested positive for infectious hematopoietic necrosis, viral hemorrhagic

septicemia, furunculosis, and ceratomyxosis than hatcheries located elsewhere in the

western States, whereas the same hatcheries in Alaska tested positive at the lowest rate

for several other salmonid pathogens (PNWFHPC 1993) (Table 1).

In the Pacific Northwest, hatchery diseases associated with freshwater organism can also

occur in natural sea water environments after salmon are released from hatcheries or

transferred to net-pens for further rearing. Some pathogens, such as V. anguillarum and

various parasites, are unique to the marine environment and are normally encountered by

wild and hatchery-reared salmonids only after they leave rivers for the sea (Wood 1979,

Harrell et al. 1985 and 1986, Kent and Poppe 1998). Salmonid diseases observed in

salmon and trout reared in public and private net-pens in sea water in the Pacific

Northwest include; vibriosis, furunculosis, bacterial kidney disease, enteric redmouth

disease, myxobacterial disease, infectious hematopoietic necrosis, infectious pancreatic

necrosis, viral hemorrhagic septicemia, erythrocytic inclusion body syndrome, rosette

agent, and a large number of parasitic infections. Kent and Poppe (1998) listed and

described infections currently observed in salmonids in marine waters.

Like other animals, salmon can carry pathogen organisms without themselves being

infected. For example, numerous bacterial species were observed in tissues of chinook

salmon which had returned from the ocean to a hatchery in the lower Columbia River

Basin, although the fish displayed no clinical signs of disease. Some bacteria observed

were Listeria sp., Aeromonas hydrophila, Enterobacter agglomerans, E. cloacae,

Staphylococcus aureus, Pseudomonas sp., Pasteurella sp., V. parahaemolyticus, V.

extorquens, V. fluvialis, Hafnia alvei, and Serratia liquefaciens (Sauter et al. 1987).

Several of these organisms found in hatchery salmon are known to be infectious for

humans but it does not infer they pose any risk.
82

Table 1. Facilities (%) testing positive for various salmonid pathogens (July 1988–June

1993). (Data from PNWFHPC 1993)

State or

Agency

IHN IPN VHS EIBS BKD FUR ERM CWD PKD MC CS ICH

AK 47.3 0.0 1.2 0.0 75.2 42.5 10.9 27.5 NS NS 50.0 0.0

CA 24.2 0.0 0.0 0.0 31.2 2.2 23.0 19.4 27.9 12.0 12.8 56.3

ID 20.2 8.7 0.0 15.5 48.4 1.8 12.3 23.6 4.3 15.6 20.4 20.7

MT 0.0 0.0 0.0 0.0 5.6 2.5 0.8 4.2 7.7 0.0 0.0 0.0

OR 18.1 0.3 0.0 24.6 53.1 35.9 17.8 84.8 0.0 2.9 33.3 26.2

WA 11.5 0.7 0.1 34.2 52.6 20.1 17.0 60.3 3.5 0.0 11.9 24.4

USFWS 37.5 1.0 0.0 27.2 84.9 23.7 20.0 34.9 0.0 0.6 30.6 24.0

NWIFC 2.9 0.0 0.6 NS 51.5 14.0 18.1 39.9 56.3 0.0 0.0 15.0

Average 20.2 1.3 0.2 14.5 50.3 17.8 15.0 36.8 12.5 4.4 18.8 20.8

NS = Not surveyed

Key:

(a) Viral Diseases

IHN Infectious hematopoietic necrosis

IPN Infectious pancreatic necrosis

VHS Viral hemorrhagic septicemia

EIBS Erythrocytic inclusion body syndrome

(b) Bacterial Diseases

BKD Bacterial kidney disease

FUR Furunculosis

ERM Enteric redmouth disease

CWD Coldwater disease

(c) Parasites

PKD Proliferative kidney disease

MC Whirling disease

CS Ceratomyxa

ICH Ichthyopthirius
83

5.3.3 Infectious disease therapy

Fish diseases and subsequent antibiotic therapy have been normal occurrences at state,

federal, and tribal Pacific salmon hatcheries since the 1940s (WDF 1950, PNWFHPC

1993). For example, an examination of the disease histories of Puget Sound area Pacific

salmon hatcheries (data from 45 hatcheries) during the 1980s showed that on average

each hatchery commonly experienced disease outbreaks from about 4 different

pathogenic organisms during this period, frequently on an annual basis (PNWFHPC

1988a–d).

Cumulatively, salmon hatcheries in the Pacific Northwest (Alaska, Washington, Oregon,

and Idaho), including those located in Puget Sound, experience hundreds of disease

outbreaks every year, according to Wood (1979) and PNWFHPC (1988a–d). For

example, Michak and Rodgers (1989) reported that, between 1983 and 1986, the WDFW

Cowlitz Hatchery experienced Costia sp. infections on 11 different occasions, bacterial

hemorrhagic septicemia 4 times, cold water disease 9 times, bacterial kidney disease 8

times, and furunculosis once. Disease outbreaks have been observed in hatchery salmon

reared in saltwater in Washington since the first attempts at seawater rearing in the 1950s

(WDF 1954, PNWFHPC 1998). However, the occurrence of fish diseases and their

treatment with chemotherapeutics at public hatcheries has not been show to have

deleterious effects on wild salmonids.

Diseases in public trout and salmon hatcheries (Table 1) are normally treated with a

variety of antibiotics and chemical baths including, inter alia, oxytetracycline, ®Romet30, formalin, iodophores (Wood 1979; PNWFHPC 1988a–d, 1998). Drug therapy in

federal, state, and tribal hatcheries in Washington State is conducted in line with FDA

guidelines (K. Amos, WDFW, personal communication). Antibiotic-resistant strains of

bacterial fish pathogens have been observed in Pacific salmon hatcheries in the Pacific

Northwest for over 40 years (WDF 1954, Wood 1979, PNWFHPC 1993), but no adverse

impacts on wild salmonids have been reported as a result of drug use or the occasional

development of antibiotic-resistant bacteria.

Schnick (1992) reported that only three therapeutants (formalin, oxytetracycline, and

®Romet-30) and one anesthetic (MS-222) were currently approved by the federal

government for use with food fish in public and private artificial propagation facilities.

However, the use of antibiotics in the US is far more restrictive than in other countries.

For example, Weston (1996) stated that 26 different antibacterials were approved for use

in Japan. This compares currently with three in Canada, according to EAO (1997) and

two in the US (Schnick 1992).

Given that Pacific salmon hatcheries rear thousands of metric tons of fish each year, the

amount of antibiotics used to treat bacterial salmon diseases is not insignificant,

amounting to hundreds of tons of medicated feed each year. Michak et al. (1990) stated

that WDF hatcheries located in the Columbia River Basin used about 200 mt of feed

containing antibiotics. Since WDF (now WDFW) hatcheries in the Columbia River

Basin represented only about 25% of the number of all salmon and trout hatcheries (albeit

many of the largest facilities are in the Columbia River Basin) in Washington State at that
84

time (Myers et al. 1998), it is reasonable to estimate that the total amount of medicated

feed used by the public hatchery system in the State was about 450 mt in 1990.

However, no adverse impacts to wild salmonids have been reported as a result.

Actual or estimated annual amounts of medicated feed used in private fish culture of

Atlantic salmon in seawater and rainbow trout in freshwater are not available at this time

for the USA. However, the amount of drugs used elsewhere in salmon farming has

greatly declined, mostly as a result of improved husbandry practices, including

development of effective vaccines. EAO (1997) noted that salmon farmers in Norway

used 48.7 mt of antibacterial drugs in 1987, and the figure had fallen to 6 mt by 1993. In

1998 it was only 679 kg (Intrafish 2000). During the same ten year period, the

production of salmon increased from 50,000 mt to 400,000 mt, and the quality of product

was considerably improved (ODIN 2001). A similar pattern of reduced drug use has

occurred in BC. With few salmon farms in Washington the annual use of antibiotics in

the net-pen farms will be minimal.

5.3.4 Disease interactions between wild and propagated salmonids

Documented examples of pathogen transmission between wild and artificially-propagated

fish are not common, yet have been known to occur (Brackett 1991). For example, the

planting of infected Atlantic salmon smolts from Norwegian federal salmon hatcheries

into rivers in Norway was responsible for the introduction of the freshwater parasite

Gyrodactylus salaris, which caused the extirpation of Atlantic salmon in many river

systems (Johnsen and Jensen 1986, 1988). The salmonid viral pathogen IHN (infectious

hematopoietic necrosis) was introduced to Japan from a shipment of infected sockeye

salmon eggs from a hatchery in Alaska and subsequently caused epizootic mortality in

Japanese chum salmon and in two species of landlocked salmon which occur only in

Japan (McDaniel et al. 1994). In these two cases, the indigenous salmonids in Norway

and Japan were exposed to novel pathogens to which they had little or no immunity. In

Washington the pathogens found in cultured salmonids are identical to those known to

occur in wild salmon (Amos and Appleby 1999).

PSGA (2000) and Carrel (1998) assert that local Atlantic salmon stocks are more likely to

carry pathogens than hatchery stocks of Pacific salmon, but this is not supported the

scientific literature. Salmonids, including Atlantic salmon, can only carry diseases to

which they have been exposed. The New England Atlantic salmon stocks used by

Washington growers were certified by federal pathologists to be pathogen-free prior to

shipment from east coast hatcheries between 1980 and 1986, inclusive, and have been

reared exclusively in the Pacific Northwest for many generations. Their diseases, if any,

would be no different than the diseases found in nearby Pacific salmon hatcheries. In

addition, Washington regulations require that all broodstocks of hatchery salmon,

including Atlantic salmon broodstocks, are examined for pathogens each year (WAC

220–77; RCW 75.58). Non-indigenous salmon diseases transmitted into the Pacific

Northwest by North American stocks of Atlantic salmon have not been reported.

Pacific salmonids do not seem to be put to any increased risk of pathogen transmission

when exposed to water in which Atlantic salmon have been reared. For example, Rocky
85

Ford Creek near Ephrata, in eastern Washington, is considered one of the premier trout

streams in the State but its entire flow consists of effluent from an Atlantic salmon

hatchery (J. Parsons, Troutlodge Inc., personal communication). There are no reports of

diseased trout in this stream in either the scientific literature or in 'gray' literature.

There is no evidence to suggest that hatchery-reared Atlantic salmon have introduced or

spread non-indigenous pathogens to native fishes in Washington. With Pacific salmon,

Griffiths (1983) observed that outbreaks of serious contagious diseases were normally

associated with the intensive culture of fish in a hatchery environment. There are no

recorded observations to suggest this would be any different for artificially-propagated

Atlantic salmon or rainbow trout.

5.3.5 The scale of artificial propagation

Based solely on the enormous number of hatchery-reared salmonids released into rivers

and lakes in the Pacific Northwest, the potential for transmission of disease to wild stocks

from hatchery-reared Pacific salmon and trout greatly exceeds that of accidentallyescaped farmed Atlantic salmon and rainbow trout in Washington State. This is because

escaped Atlantic salmon and rainbow trout constitute an insignificant percentage of all

artificially-propagated salmon which end up in natural waters in the area. However, the

millions of Pacific salmon which enter the marine waters of Washington each year have

not been shown to impose adverse impacts on wild salmonids. Carrel (1998) described

escaped Atlantic salmon as 'smart bombs, delivering disease right into the bedrooms of

wild salmon' in the Pacific Northwest, but this is not supported in the scientific literature.

Because Atlantic salmon are propagated in only a few facilities in the Pacific Northwest,

compared with the several hundred federal, state, tribal, and cooperative hatcheries

rearing Pacific salmon and trout, the primary difference in the disease incidence between

artificially-propagated Atlantic and Pacific salmon is one of scale. Mahnken et al. (1998)

reported that, since 1980, the number of Pacific salmon released from west coast

hatcheries was about two billion fish annually. This number is 4 or 5 orders of

magnitude larger than the number of Atlantic salmon which may have escaped from netpens since 1980 (Table 2).

Table 2. Number (in millions) of salmon released or escaped by species and location

along the west coast of North America, 1980–1995 (Data from NRC 1995 and 1996;

Thomson and McKinell 1993–1997; Mahnken et al. 1998; Thomson and Candy 1998).

State or Region Atlantic Sockeye Chum Steelhead Pink Coho Chinook

Alaska 0 978 3,885 2 8,610 193 98

Canada BC ~0.4 3,930 2,870 17 533 300 721

Pacific Northwest ~0.6 52 1,081 359 21 726 4,320

Total ~1.0 4,960 7,836 377 9,164 2,219 5,139

Total (%) 0.0003 16.7 26.4 1.2 30.9 7.5 17.3

Comparing only the number of Pacific salmon released from salt-water net-pens, then the

magnitude and geographic distribution of these artificially-propagated Pacific salmon is

still much greater than the number and magnitude of Atlantic salmon reared in farms.
86

For example, NRC (1995, 1996) reported that coho salmon were released annually from

18 different marine net-pen sites, chinook salmon from 13 different sites, and chum

salmon from 10 different sites in Puget Sound between Olympia and Bellingham. The

annual release from these marine sites between 1980 and 1992 averaged about 10 million

fish. These fish had sometimes been exposed to various salmonid pathogens while in

seawater, including bacterial kidney disease, vibriosis, and furunculosis. Infections in

these fish were often treated with antibiotics prior to their release (PNWFHPC 1988a–d),

yet no adverse impacts on wild salmonids have been reported as a result.

5.3.6 Disease control policies in Washington and the USA

In Washington all public and private growers of salmon, including Atlantic salmon

hatchery operators, are required to adhere to strict disease control polices which regulate

all phases of fish culture, from egg take to harvest and/or release (NWIFC/WDFW 1991;

NWIFC/WDFW1998). Each year at spawning time, adult salmon at public and private

hatcheries must be sampled for viral, bacterial, and parasitic organisms. If any of several

reportable organisms are detected in fish at a hatchery, or have been detected within the

past five years, transfer of eggs or fish from that facility is prohibited.

The movement of fish and eggs across state or international borders is regulated by the

USFWS under Title 50 of the CFR, which has stipulations and controls in accord with

State regulations (Regulation 50 CFR, Part 16.13). For the case in point, all Atlantic

salmon stocks distributed to local growers by NMFS were federally certified by federal

pathologists before transfer from New England, and have been annually certified since

then under Washington guidelines and procedures.

Most of the cumulative body of information pertaining to salmon farming developed in

the last several decades has already been integrated into the regulatory processes of

Washington State. This scientific information has been incorporated into State

regulations relating to farm fish escapes, antibiotic residues in sediments, accumulation

of organic wastes on the seabed, importation of non-native and non-local species, and

disease management. These and other important regulations and documents pertaining to

private salmon farming include:

• Final programmatic EIS for fish culture in floating net-pens (WDF 1990)

• Recommended interim guidelines for the management of salmon net-pen culture in

Puget Sound (WDOE 1986)

• Environmental effects of floating mariculture in Puget Sound (Weston 1986)

• Environment fate and effects of aquacultural antibacterials in Puget Sound (Weston et

al. 1994)

• Disease control policies of Washington (NWIFC/WDF 1991)

• Disease control policies of the United States (USFWS 1984)

• Fish health manual of the Washington Department of Fish and Wildlife (WDFW

1996)
87

5.4 Potential Ecological Impacts of Atlantic Salmon in the Pacific Northwest

In areas where Atlantic salmon are indigenous, such as Scandinavia, Great Britain, and

eastern North America, adverse genetic and ecological impacts for natural populations of

Atlantic salmon have been reported by, inter alia, Gibson 1977; Gross 1998; Hearn and

Kynard 1986; Jones and Stanfield 1993; Beall et al. 1989; Heggberget et al. 1993,

following programmed releases or escapes of artificially-propagated Atlantic salmon

from public hatcheries and private net-pens. The impacts included reduction in genetic

adaptation and capacity to evolve in wild Atlantic salmon resulting from interbreeding

with artificially-propagated Atlantic salmon, and competition for food and space between

wild and hatchery stocks of Atlantic salmon.

These adverse effects occurred because both the artificially-propagated and wild

salmonid species were Atlantic salmon. Escaped Atlantic salmon on the Pacific coast of

North America do not have congeneric wild individuals with which to interact. In the

Pacific Northwest region it is the introduction of hatchery stocks of Pacific salmon which

have the potential to produce impacts on native Pacific salmon comparable to those found

between propagated and wild Atlantic salmon in Europe and eastern North America.

Adverse genetic and/or ecological interactions on local wild salmon populations resulting

from plants of artificially-propagated Pacific salmonids have been well documented in

the Pacific Northwest in papers by Nickelson et al. (1986), Behnke (1992), Kostow

(1995), Campton and Johnston (1985), WDFW et al. (1993), and Leider et al. (1997). A

series of papers by Thomson and McKinnell (1993, 1994, 1995, 1996, and 1997),

Thomson and Candy (1998), and Amos and Appleby (1999) have reported no detrimental

effects in the region which can be related to deliberate or accidental Atlantic salmon

introductions.

5.4.1 Social interactions between Pacific and Atlantic salmon

Gibson (1981) reported that, from laboratory studies in New England, introduced Pacific

steelhead juveniles were more aggressive than Atlantic salmon. In turn Atlantic salmon

fry appeared to be more aggressive than coho salmon fry when introduced into open

pools, although it was recognized that open pools are not the preferred habitat of coho

salmon fry. Beall et al. (1989) in a similar experiment reported that the survival of

Atlantic salmon was reduced in the presence of older coho salmon fry.

In trials of inter-specific combative behavior in New England, Hearn and Kynard (1986)

observed that rainbow trout juveniles initiated three to four times more aggressive

encounters than did Atlantic salmon, and concluded that it would take very large numbers

of Atlantic salmon juveniles to displace or even disrupt native species. Jones and

Stanfield (1993), in a study conducted in a Lake Ontario tributary once inhabited by

Atlantic salmon, reported that their attempts to reintroduce hatchery strains of Atlantic

salmon were significantly impaired in the presence of naturalized Pacific salmon

juveniles, compared with reintroduction in stream sections where Pacific salmon

juveniles had been removed.
88

5.4.2 Predation by Atlantic salmon

In a study on farmed fish in Canada BC by Black et al. (1992) stomach analyses revealed

that <1% of farmed salmon in net-pens (in this case coho and chinook salmon) contained

the remains of fish. Since 1992 scientists of the Canadian federal government have

examined the stomach contents of escaped Atlantic salmon recovered in the open waters

of BC. Fish remains of any sort were rarely observed, and no confirmed salmonid

remains were reported (see Thomson and McKinnell 1993, 1994, 1995, 1996, 1997;

Thomson and Candy 1998). This confirms earlier work by Tynan (1981) who examined

the stomachs of 93 coho salmon captured after release from a net-pen near Squaxin

Island, in South Puget Sound, and reported that only three stomachs contained fish

remains, which were identified as smelt.

At the NMFS Manchester Research Station in Puget Sound many species of forage fish

have been observed seeking refuge from predators in net-pens containing large Atlantic

salmon. Among the species observed are known prey of salmonids, such as herring,

smelt, candlefish, shiner perch, and tube snouts. These prey species enter the net-pens

voluntarily and then grow too large to exit. A report by Alverson and Ruggerone (1997)

noted that many thousands of these small fish had been observed in Atlantic salmon netpens, and had to be removed by hand.

Buckley (1999) showed that cannibalism and predation on other salmonids by chinook

salmon when feeding was uncommon in Puget Sound waters. It is difficult to imagine

that escaped Atlantic salmon, conditioned to a diet of artificial feed pellets and trained to

be fed by humans, could have greater predation impacts on juvenile native salmonids

than the low impact observed with free-swimming Puget Sound chinook salmon.

In the Cowichan River in Canada BC, non-native brown trout became established soon

after its first introduction in 1932. Idyll (1942) observed that native salmon and trout,

and their eggs, were a significant dietary component of newly-established Cowichan

River brown trout, and were the primary food item of large brown trout. Recent

evaluations by Wightman et al. (1998) of steelhead populations on the east coast of

Vancouver Island showed that the Cowichan River was one of only two rivers (out of 27

evaluated) with a relatively healthy steelhead population. Therefore the successful

colonization of the Cowichan River by a highly piscivorous species such as the brown

trout has apparently had no adverse impact on steelhead abundance for more than 60

years, whereas concurrent attempts to establish Atlantic salmon in the Cowichan River

basin were failures.

5.5 Potential Impacts of Propagated Pacific Salmon

Adverse genetic and ecological effects from artificially-propagated Pacific salmon have

been documented by, inter alia, Weitkamp et al. (1995), Busby et al. (1996), Hard et al.

(1996), Gustafson et al. (1997), Johnson et al. (1997), Myers et al. (1998), and Johnson et

al. (1999) in a number of coast-wide status reviews of Pacific salmonids. These status

reviews were conducted by NMFS in fulfillment of their responsibilities under ESA. The

reviews contained information from the scientific literature which documented known
89

adverse ecological impacts sometimes associated with the artificial propagation and

release of Pacific salmon. In recent years, west coast management agencies have

eliminated many of the policies which contributed to these adverse effects. However,

examining some of the known adverse impacts of Pacific salmon hatchery programs

which have not been observed to be a result of Atlantic salmon hatchery programs on the

west coast offers an effective demonstration that the ecological and genetic risks

associated with Atlantic salmon farming are small in the waters of Puget Sound. The

following paragraphs provide a brief review by species of adverse effects of artificial

propagation which occurred under the old Pacific salmon hatchery policies.

(i) Steelhead trout

Hatchery stocks of steelhead have been widely distributed. Few native steelhead stocks

exist in the contiguous US which have not had some influence from hatchery operations.

For example, Busby et al. (1996) cite the summer steelhead program at the Nimbus

Hatchery in Central Valley, California was established with fish from a distant coastal

tributary hatchery which was itself earlier established with Lower Columbia River

summer steelhead.

Howell et al. (1985) reported that over 90% of the 'wild' steelhead spawning in the

Cowlitz River originated in a hatchery, and some of these fish exhibited genetic

characteristics of Puget Sound steelhead due to previous transfers of Puget Sound stock

to the Cowlitz Hatchery.

Chilcote (1997) reported that, since 1980, the percentage of non-native stray hatchery

steelhead (from upper Columbia River and Snake River hatcheries) spawning in the

Deschutes River had increased to over 70% of the run, while the percentage of native,

wild steelhead spawning in the Deschutes River decreased to less than 15%. Phelps et al.

(1997) postulated that introductions of non-native steelhead stocks in Washington,

primarily Chambers Creek winter steelhead and Wells and Skamania summer steelhead,

may have changed the genetic characteristics of some populations sufficiently so that the

original genetic relationships between stocks may have been obscured. Finally, Leider et

al. (1987) concluded that the genetic fitness of the wild Kalama River population had

been compromised by maladaptive gene flow from excess hatchery escapement. By

comparison, no documented adverse effects on steelhead have been reported to result

from escapes of Atlantic salmon in Washington or elsewhere.

(ii) Chinook salmon

About 2 billion hatchery chinook salmon have been released into Puget Sound since

1953, with the stock from the Green River Hatchery being the dominant stock as far back

as 1907. Concerns that this strategy may erode genetic diversity was raised by Myers et

al. (1998). As recently as 1995, 20 hatcheries and 10 marine net-pen sites throughout

Puget Sound regularly released Green River-stock chinook salmon. Busack and Marshall

(1995) reported that the extensive use of this stock had an undoubted impact on amongstock diversity within the South Puget Sound, Hood Canal, and Snohomish summer/fall

genetic diversity unit (GDU), and may also have impacted GDUs elsewhere in Puget

Sound and the Strait of Juan de Fuca.
90

Rogue River chinook salmon were recently released on the Oregon side of the Lower

Columbia River to produce a south-migrating stock to avoid interception in commercial

fisheries in Canada BC and Southeast Alaska. However, chinook salmon exhibiting

Rogue River fall chinook salmon genetic markers were subsequently observed by

Marshall (1997) in several lower Columbia River tributaries, and were estimated to

comprise about 13% of the Lower Columbia River naturally-produced chinook salmon

sampled in 1995. Marshall et al. (1995) had earlier stated that most of the naturallyspawning spring chinook salmon in Lower Columbia River tributaries were hatchery

strays. Adverse impacts resulting from the introduction of artificially-propagated fish

into native populations of chinook salmon were identified as a primary concern by the

NMFS Biological Review Team during the recent review of the status of west coast

chinook salmon populations (Myers et al. 1998). There is no documented evidence of

adverse effects on chinook salmon resulting from escaped Atlantic salmon in Washington

or elsewhere.

(iii) Chum salmon

Johnson et al. (1997) reported that five hatchery stocks and several wild populations of

chum salmon outside the Hood Canal, but which received eggs from Hood Canal

hatcheries for several years, exhibited genetic frequencies more similar to those in Hood

Canal hatchery populations than to populations in nearby streams not receiving Hood

Canal hatchery stocks. Their analyses of gene frequency patterns were consistent with

the hypothesis that egg transfers between hatcheries and out-plantings of Hood Canal

stock fry had genetically influenced the receiving populations. According to Phelps et al.

(1995) such transfers were terminated because of the potential jeopardy to wild gene

pools through interbreeding. However, there is no documented evidence of adverse

effects on chum salmon resulting from escaped Atlantic salmon in Washington or

elsewhere.

(iv) Coho salmon

Weitkamp et al. (1995) noted that the NMFS Biological Review Team was unable to

identify any remaining natural populations of coho salmon in the lower Columbia River

below Bonneville Dam, due in large part to persistent and extensive hatchery programs.

A recent survey by NRC (1999) of coho salmon spawning habitat in the lower Columbia

River estimated that about 97% of recovered spawned-out carcasses originated from

hatchery releases. Hatchery fish were observed in high percentages in streams up to 45

miles from the nearest hatchery. In many streams, wild, native coho salmon were not

observed at all. In an earlier similar survey by NRC (1997) in Hood Canal, over 50% of

all spawning coho in streams within a 10-mile radius of a net-pen release site were fish

released from the net-pen as juveniles 18 months earlier.

Kostow (1995) stated that hatchery programs in Oregon may have contributed to the

decline of wild coho salmon by supporting harvest rates in mixed-stock fisheries which

were excessive for sustained wild fish production, and by reducing the fitness of wild

populations through interbreeding of hatchery and wild fish. Furthermore, they may have

reduced survival of wild coho salmon juveniles in Oregon through increased competition
91

for food in streams and estuaries, through attraction of predators during mass migrations,

and through initiation of disease problems.

Weitkamp et al. (1995) also reported that artificial propagation of coho salmon had

appeared to have substantial impact on native coho salmon populations to the point where

it was difficult for the NMFS Review Team to identify self-sustaining native stocks in

Puget Sound, as over half the returning spawners originated in hatcheries. Spawn-timing

had been advanced by selective breeding so that most hatcheries met their quotas for eggs

by early November, and fish arriving at the hatchery with the later run (which would be

coincidental with the spawn-time of the wild or native fish) were not propagated. As a

result of such practices, according to Flagg et al. (1995), segments of hatchery coho

salmon populations which historically returned as late as January through March have

disappeared from many river systems, resulting in a significant loss of life history

diversity. Again, for comparison, there is no documented evidence of adverse effects on

coho salmon resulting from escaped Atlantic salmon.

(v) Trouts

Long-term introductions of rainbow trout into western streams originally inhabited only

by cutthroat trout have resulted in widespread extinctions of native cutthroat trout

through introgressive hybridization, according to Leary et al. (1995). They noted that

hybridization between introduced brook trout and bull trout is widespread in the western

USA, and usually produces sterile hybrids. Behnke (1992) noted that introduced brown

trout had commonly replaced interior subspecies of cutthroat trout in large streams

throughout the same region, and introduced brook trout were the most common trout to

be found in many small streams.

The situation regarding attempts to establish Atlantic salmon populations in the West is

much different. In summary, MacCrimmon and Gots (1979) described frequent attempts

and failures to introduce Atlantic salmon to the western States, many of which occurred

in the same river systems and at the same time as the introductions noted above. Since

then no recent introductions, accidental or not, have succeeded and, most importantly, no

known adverse impacts on indigenous species by Atlantic salmon have been reported in

the literature.

5.6 Adverse Impacts of Non-indigenous Fish Introductions

As many as 50 species of non-native fish are successfully established in the western US

(Table 3). The Atlantic salmon is not one of those listed. Some adverse impacts

associated with the establishment of these species are discussed below. None of these

negative impacts has been associated with the artificial propagation of Atlantic salmon in

the Pacific Northwest.
92

Table 3. Status of non-native fish introductions in the Pacific Northwest vis-à-vis their

behavior relative to Pacific salmonids (Data after Behnke 1992, Lever 1996, ODFW

1999, WDFW 1999, Dill and Cordone 1997)

Non-Native Species

Naturalized

in

Washington

Naturalized

in

Oregon

Naturalized

in

California

Predator Competitor Hybridize

Atlantic salmon

Non-native rainbow X X X X X X

Non-native cutthroat X X X X X X

Lahotan cutthroat X X

Westslope cutthroat X X X X

Brown trout X X X X X X

Brook trout X X X X X X

Lake trout X X X X X

American shad X X X X

Threadfin shad X

Lake whitefish X

Arctic grayling X X

Grass pickerel X X

Northern pike X X X

Striped bass X X X

White bass X

Common carp X X X X

Grass carp X X

Tench X X

Brown bullhead X X X X X

Black bullhead X X X X X

Yellow bullhead X X X X X

Flathead catfish X X X X

Blue catfish X X X

Channel catfish X X X X X

White catfish X X X X

Largemouth bass X X X X X

Smallmouth bass X X X X X

Warmouth bass X X X X X

Rock bass X X X

Redeye bass X

Northern spotted bass X

Alabama spotted bass X

Black crappie X X X X X

White crappie X X X X X

Green sunfish X X X X X

Bluegill X X X X X

Pumpkinseed X X X X X

Redear sunfish X

Bigscale logperch X

Yellow perch X X X X X

Walleye X X X X X
93

ODFW/NMFS (1998) documented that many introduced non-native species were

harmful to native salmon. For example, walleye, bass, perch, sunfish, brown trout, and

brook trout, among others, are all now well-established in Northwest waters and are wellknown predators and/or competitors of native salmon and trout. Beamesderfer and Nigro

(1988) and Beamesderfer and Ward (1994) estimated that walleye and smallmouth bass

introduced into the John Day Reservoir of the Columbia River consumed an average of

400,000 and 230,000 juvenile salmonids, respectively, each year.

Daily et al. (1999 in prep.) reported that juvenile salmonids from seven ESUs currently

listed as threatened or endangered under ESA must migrate through the John Day

Reservoir; and in some coastal lakes in Oregon the summer rearing of coho salmon fry no

longer occurred due to predation by introduced largemouth bass. Seiler (WDFW,

personal communication) has observed that introduced bass eat out-migrating salmon,

including juvenile chinook salmon, as they pass through the Lake Washington Ship Canal

in Seattle, WA. There is no documented literature which shows that Atlantic salmon in

western states prey on juvenile native salmonids.

In 1997 and 1999, in response to the escape of some net-pen Atlantic salmon, WDFW

suspended fishing regulations concerning size and bag limits for these fish. Licensed

anglers fishing in open management zones were permitted to keep all Atlantic salmon

they could catch, of whatever size (WDFW 1997c, 1999). Suspension of fishing

regulations for an introduced, non-native species in waters inhabited by native salmonids

at some period of their life cycle is an appropriate management which WDFW has used

before. For example, freshwater angling regulations for non-native brook trout in

Washington were recently relaxed to increase harvest of this species, and regulations for

non-native shad, perch, crappie, and carp have long-since been dismissed entirely.

Catch limits and close seasons for non-native salmonids in Washington (such as brown

trout, golden trout, lake trout, landlocked Atlantic salmon, California-strain rainbow

trout, and grayling) have given these species many of the same protections given to

native salmonids. Furthermore, several non-native species known to prey on salmonid

juveniles (such as smallmouth and largemouth bass, walleye, and channel catfish) are

currently managed for sustained natural reproduction through regulations which limit the

take of large individuals which have the greatest reproductive potential (WDFW 2001).

From a review of the literature, Atlantic salmon have far less potential for adverse

impacts than all the non-native species noted above. Therefore, to decrease unnecessary

adverse impacts on listed native salmonids by non-indigenous fish, it would not be an

inconsistent strategy for states in the Pacific Northwest to suspend regulations for the

harvest of all non-indigenous fish by licensed anglers.
94

5.7 A Perspective of Salmon Culture in Northwest Waters

Most of the concerns for the negative impacts of Atlantic salmon on native salmon in the

Pacific Northwest are hypothetical. They are associated with the belief that artificiallypropagated fish are bigger, stronger, and more vigorous that wild fish. Although this

opinion has been generally disproved in a multitude of studies, many studies and reviews,

among them WDFW et al. (1993) and the NMFS Status Reviews, have shown that

adverse impacts from hatchery stocks of Pacific salmon are likely to occur if and when

hatchery fish comprise a large portion of the total population. Therefore, it is instructive

to compare the numbers of artificially-propagated Pacific salmon released each with the

number of Atlantic salmon estimated to escape each year to give a perspective as to

where and when the greatest risks actually occur, and to what degree, keeping in mind

recent changes in hatcheries strategies in the Pacific Northwest which will likely reduce

the impact of hatchery fish on wild fish.

Mahnken et al. (1998) reported that several billion Pacific salmon were released from

freshwater hatcheries and marine net-pens in North America each year (see Table 2).

Although Washington, Oregon, Idaho, and California had more salmon hatcheries, the

total number of fish released in the contiguous States of the Pacific Northwest was

dwarfed by the vast number of hatchery salmon released in Alaska each year. McNair

(1997, 1998, and 1999) documented the annual release of about 1.4 billion hatchery

salmon into natural rearing areas since 1996.

Pacific salmon have been released from hatcheries with the understanding that they must

compete for food and habitat in common with native wild salmon to survive. Until

recently the capacity of the ocean pastures were thought to be limitless. Recent

investigations by Heard (1998), Cooney and Broduer (1998), and Beamish et al. (2000)

show that food availability in the ocean fluctuated over time and might be limiting

salmon abundance. Bisbal and McConnah (1998) proposed fishery managers planning

to release vast numbers of fish from hatcheries should take these fluctuations into

account. Compared with the great numbers of Pacific salmonids released each year into

the marine ecosystems, there is no evidence in the literature that the few Atlantic salmon

which escape pose any competitive threat to native Pacific salmon for forage or habitat.

The majority of Atlantic salmon escapes have occurred in Puget Sound. However, the

number of escapees is extremely low compared with the number of Pacific salmon

deliberately introduced into the ecosystem. NRC (1995, 1996) documented that the total

number of cultured chinook. coho, and chum salmon released into Puget Sound

tributaries by various fisheries agencies between 1980 and 1992 exceeded 2.2 billion in

number. Although data are not yet available through the year 2000, it is predictably over

3 billion. For comparative purposes, if the total number of Atlantic salmon which

escaped into Puget Sound since 1980 was represented on a histogram by a bar one inch

high, the total number of Pacific salmon released into Puget Sound and its river basins

since 1980 would be a bar about 250 feet high. Comparison with the 13.5 billion

hatchery fish released into Alaskan waters since 1990, using annual data published by
95

ADF&G between 1991 and 2000, is even more dramatic, and would require a bar almost

one quarter of a mile high.

The adverse ecological and genetic interactions associated with abundant releases of

hatchery-reared Pacific salmon are well-documented and present a more serious risk for

native salmonids. There is no evidence in the literature which associates adverse impacts

with the escape of Atlantic salmon in the Pacific Northwest, or that they even pose a

serious threat.

NRC (1995) reported that over 240 million small, non-migratory, hatchery coho salmon

were released into Puget Sound tributaries between 1980 and 1992, which averaged about

18 million annually. FPC (1999) since reported that the number of unsmolted coho

salmon was reduced by over half, due to the previously mentioned changes in hatchery

strategies. Nonetheless, these artificially-propagated fish have to survive by competing

for natural food and rearing space with native salmon for about 18 months. Using typical

wild coho salmon life history data (ODFW 1982), such as egg-to-fingerling survival

levels of 10% and a fecundity of 4000 eggs per female, it would take every year about

92,000 mature, successful Atlantic salmon spawners (1:1 female:male ratio) to produce

enough fry to equal the numbers of artificially-propagated non-migrant coho salmon

planted in Puget Sound rivers every year.

Applying the same calculations on a more local scale, FPC (1999) reported that about

7,500,000 coho salmon fry of hatchery origin were planted in the Green River between

1993 and 1996. To produce an equal number of Atlantic salmon juveniles, it would be

necessary for over 9,000 mature Atlantic salmon adults to escape and spawn successfully

in the Green River each year. However, Thomson and Candy (1998) recaptured fewer

than 20 mature Atlantic salmon in all Washington rivers systems during 1997, although

some were not surveyed completely. BMPs for net-pen salmon farming continue to

stress the importance of preventing escapes (BCSFA 1999), but any potential adverse

impacts associated with escaped Atlantic salmon cannot begin to approach the potential

impacts of fish released from Pacific salmon hatchery programs, even when recent

changes in hatchery strategies are considered

Volpe et al. (2000) recovered less than 100 naturally-spawned juvenile Atlantic salmon

during counts of salmon juveniles in the Tsitika River in Canada BC. Noakes (1999)

noted more than 10,000 juvenile Pacific salmonids were observed in this river in the

same survey. The juvenile Atlantic salmon made up approximately 1% of the juvenile

salmonids in the river and presented no competition to native salmonids for food or

rearing space. No naturally-produced Atlantic salmon have been observed in Washington

rivers to-date, although surveys have not been as vigorous as those in Canada.

The success of a hatchery or net-pen facility, as well as the degree to which hatchery fish

potentially impact wild fish, is largely determined by how well fish survive in the wild

after release. Some hatchery programs are very successful at producing fish for harvest.

Johnson et al. (1997) noted that hatcheries in Alaska, through extremely successful earlyrearing strategies, produced prodigious numbers of adult chum and pink salmon, two
96

species which normally have juvenile to adult survival rates of <0.5%. The Hidden Falls

Hatchery in Southeast Alaska has consistently experienced survivals of 3 –8% with chum

salmon (Bachen 1994), resulting in this single facility producing more than 22% of all the

chum salmon, wild and hatchery, caught in the fisheries of southeast Alaska (Johnson et

al. 1997). McNair (1998) reported that 93.6% of all pink salmon caught in Prince

William Sound in 1997 were artificially propagated, and that for all salmon harvested in

common property fisheries throughout Alaska that year, 22% of the coho salmon, 30% of

the pink salmon, and 65% of the chum salmon originated in hatcheries. Overall, she

reported that hatcheries contributed 26% of all salmon harvested in Alaska in 1997. In

2000, McNair (2001) reported that 34% of the total salmon catch in Alaska was produced

in Alaskan hatcheries. Additional contributions to Alaska’s commercial harvest from

hatcheries in British Columbia, Washington, Oregon, and Idaho were not include in this

analysis. In Washington, WDFW (2000) estimated that hatcheries provide about 75% of

all coho and chinook salmon harvested, as well as 88% of all steelhead harvested. As

west coast hatcheries put enough artificially-propagated salmon into the natural

environments to produce a significant proportion of the harvest in Alaska, and the

overwhelming proportion of fish harvested in Washington, it is not possible that the

relatively inconsequential competition for natural resources from present levels of

escaped Atlantic salmon could even be evaluated.

Given that it is necessary for millions of hatchery Pacific salmon to compete successfully

with wild salmon in natural environments to survive and contribute to the economies of

Alaska and Washington, expressions of concern by ADF&G (1999) regarding

competition for food from relatively small numbers of escaped Atlantic salmon appear

misdirected. A review of the literature reveals that the potential for artificiallypropagated Pacific salmon released from public hatcheries to pose adverse impacts with

wild Pacific salmon through competition for food is far greater than the potential for

competition posed by escaped Atlantic salmon.

5.8 NMFS Biological Status Reviews of West Coast Pacific Salmon Stocks

Since 1991 14 Biological Status Reviews have been published by NMFS as part of the its

federal obligation under ESA. These Reviews are individual scientific studies of the

current status of all anadromous salmonid populations on the west coast of the USA.

These are generally regarded as the most complete scientific reviews of their kind ever

published. They form the basis for NMFS actions concerning ESA listing

determinations, as well as the scientific basis for NMFS testimony for litigation and

courtroom challenges to proposed and implemented listings under ESA.

In these Reviews, experienced federal scientists have identified many factors which have

adverse effects on the Pacific salmonids of the west coast. The potential biological

impacts of cultured salmon have continuously been identified as a primary factor (see

Hard et al. 1992, and Waples 1991). Atlantic salmon farms have not been identified as

the cause of adverse effects in any of the 14 Reviews conducted to-date, which cover 58

separate ESUs for Pacific salmon species, or factors in the decline of west coast

populations of chinook salmon or steelhead (NMFS 1996, 1998).
97

6. POST SCRIPT

In 1996 a group of organizations brought suit before the PCHB in the State of

Washington against WDOE, WDFW, and salmon farmers in the State. The suit (PCHB

Nos. 96–257 through 96–268) challenged the issuance of NPDES permits to the salmon

farmers. The basis of the suit by the appellants was a series of allegations regarding

conflict with other resources and unacceptable environmental risks associated with the

culture of Atlantic salmon, the effects of waste on the water column and benthos, and

damage to other resources, including fish and shellfish.

Following months of testimony by experts, on May 27, 1997 the PCHB denied partial

summary judgement to the appellants because of a genuine issue of material fact as to

whether escaped Atlantic salmon 'shall cause or tend to cause pollution' under State law,

and whether they constitute 'a man-made change to the biological integrity of State water'

under federal law (PCHB 1997). The PCHB found that, 'the Permittees’ facilities do not

create unresolved conflicts with alternative uses of Puget Sound resources as

contemplated by RCW 43.32C.030(2)(e). The existence of commercial salmon farms as

permitted uses does not preclude other beneficial uses in Puget Sound, such as shellfish

harvesting, commercial or sport fishing, navigation or recreational boating. Likewise,

the existence of the salmon farms does not operate to the exclusion of available

resources, such as native salmon runs, sediment and water quality, or marine mammals.

In short, salmon farming in Puget Sound does not present the citizens of the State of

Washington with an “either/or” choice with respect to other beneficial uses and

important resources.'

The Board issued its Final Order on the matter on November 30, 1998 (PCHB 1998) and

found: ' no evidence that Permittees’ facilities have impacts that effectively exclude other

beneficial uses of available resources of Puget Sound. The escapement of Atlantic

salmon from Permittees’ facilities absent large regular releases in the future does not

pose an unacceptable risk to native Pacific salmon in terms of competition, predation,

disease transmission, hybridization or colonization.' This decision by the PCHB was not

substantially different from that of the authors of the British Columbia Salmon

Aquaculture Review (EAO 1997) which concluded that salmon aquaculture, as currently

practiced in BC, did not pose unacceptable risks to the environment. The PCHB finding

in favor of the ‘performance standard’ on which the NPDES permit system in

Washington State is based also supports the decision by the BC government to work

towards similar standards.

Organic and inorganic loading of the benthos, the transport, fate and biological effects of

pharmaceuticals, and dissolved nutrient effects on phytoplankton are important public

concerns which have long been recognized and studied. Responsible publications by

Weston (1986), Parametrix Inc. (Parametrix 1990), Winsby et al. (1996), and the BC

government (EAO 1997) have reviewed all these issues in depth, and in the context of the

environment of the Pacific Northwest.
98

7. REFERENCES

Foreword

BCSFA (British Columbia Salmon Farmers Association). 1999. Code of practice. British Columbia

Salmon Farmers Association, 1200 West Pender Street, Vancouver, BC V6E 2S9, 13 p.

DOC (US Department of Commerce). 1999. US Department of Commerce Aquaculture Policy, August 10,

1999. Silver Spring, MD.

EAO (Environmental Assessment Office, Canada BC). 1997. British Columbia salmon aquaculture

review. Environmental Assessment Office, Government of British Columbia, 836 Yates Street,

Victoria, BC V8V 1X4.

FEAP (Federation of European Aquaculture Producers). 2000. A code of conduct for European

aquaculture. Federation of European Aquaculture Producers, 12 p.

SSFA (Shetland Salmon Farmers Association). 2000. Code of best practice for Shetland salmon farming.

Shetland Marine Aquaculture Consultation Agency, Port Arthur House, Scalloway, Shetland ZE1

0UN, 26 p.

Chapter 1.

JSA (Joint Subcommittee on Aquaculture). 1999. Aquaculture 2000: National Aquaculture Development

Plan of 2000. Working Draft, October 1 1999. National Science and Technology Council,

Washington DC.

USDA (US Department of Agriculture). 1999. Census of aquaculture, 1998. Volume 3, Special studies pt.

3, 1997 Census of Agriculture. US Department of Agriculture, National Agricultural Statistics

Service, Washington DC.

WRAC (Western Regional Aquaculture Center). 1999. Western regional aquaculture industry situation

and outlook report. Volume 5 (through 1997), Western Regional Aquaculture Center, School of

Fisheries Box 357980, Univ. Washington, Seattle, WA 98195-7980.

Chapter 2.

Alpine Appraisers. 1988. Effect of fish farms on surrounding property values. In Fish culture in floating

net-pens; Technical Appendix K, Final programmatic environmental impact statement,

Washington Department of Fisheries, 1990, Olympia, WA.

Amos K.H., and A. Appleby. (1999) Atlantic salmon in Washington State: a fish management

perspective. Washington Department of Fish and Wildlife, Olympia, WA. Internet document

www.wa.gov:80/wdfw/fish/atlantic/summary.htm.

BCSFA (British Columbia Salmon Farmers Association). 1999. Industry facts and figures. Internet

document http://www.salmonfarmers.org

Cardwell, R.D., M.I. Carr, and E.W. Sanborn. 1980. Water quality and flushing of five Puget Sound

marinas. Technical Report 56, Washington Department of Fisheries, Olympia,

77 p.
99

Cardwell, R.D., and R.R. Koons. 1981. Biological considerations for the siting and design of marinas and

affiliated structures in Puget Sound. Technical Report 60, Washington Department of Fisheries,

Olympia, WA, 31 p.

Clark Jr., R.C., J.S. Finlay, and G.G. Gibson. 1974. Acute effects of outboard motor effluent on two

marine shellfish. Env. Sci. and Technol. 8(12)1009–1014.

Crutchfield, J.A. 1989. Economic aspects of salmon aquaculture. Northwest Environmental Journal,

5:37–52.

Dicks M.R., R. McHugh, and W. Webb. 1996. Economy-wide impacts of US aquaculture.

P-946, Oklahoma Agricultural Experiment Station, Oklahoma State University, OK.

Didier, A.J. Jr. 1998. Estimates of salmon harvests in washington, Oregon, California, and Isaho, 1993–

1998. (NPAFC Doc. 437) 13p. Pacific States Marine Fisheries Commission, 45 SE 82nd,

Gladstone, OR.

Drinkwin J., and T.W.Ransom. 1999. Puget Sound Action Team's local liaisons: advocating for the Sound

at local government level, p412. In Coastal Zone 99, Abstracts. Urban Harbors Institute,

Massachusetts, Boston, MA.

DOC (US Department of Commerce). 1998. Fisheries of the United States, 1997. Current Fishery

Statistics No. 9700. National Marine Fisheries Service, Fisheries Statistics and Economics

Division, Silver Spring, MD.

Elston, R. 1997. Pathways and management of marine non-indigenous species in the shared waters of

British Columbia and Washington. Final Report to the Puget Sound Water Quality Authority, US

Environmental Protection Agency, and the Department of Fisheries and Oceans Canada. Internet

document http://www.wa.gov/puget_sound/shared/nis.html.

Eriksson, T., and L..O. Eriksson. 1993. The status of wild and hatchery propagated salmon stocks after 40

years of hatchery releases in the Baltic rivers. Fisheries Research 18:147–159.

Forster, J. 1995. Cost trends in farmed salmon. Report to the Alaska Department of Commerce and

Economic Development, Juneau, AK.

Garrod, G.D., and K.G. Willis. 1992. Valuing goods characteristics: an application of the hedonic price

method to environmental attributes. J. Environ. Manage. 34:59–76.

Gausen, D. and V. Moen. 1991. Large-scale escapes of farmed Atnatic salmon (Salmo salar) into

Norwegian rivers threaten natural populations. Can. J. Fish. Aquat. Sci. 48:426–428.

Goodwin, R.F., and T.J. Farrell. 1991. Washington state marine directory. WASHU–D–91–002, Univ.

Washington Sea Grant Program, Seattle, WA.

ICOR (Washington State Interagency Committee for Outdoor Recreation). 2000. Motorized boat

launches. Internet document http://www.wa.gov/iac/boating.html.

Henriksson, S-H. Effects of fish farming on natural Baltic fish communities, p 85–104. In

T. Mäkinen (ed.), Marine Aquaculture and Environment. Nordic Council of Ministers,

Copenhagen.

HIE (Highlands and Islands Enterprise). 1999. The economic impact of Scottish salmon farming.

Highlands and Islands Enterprises, Bridge House, Bridge Street, Inverness IV1 1QR, 125 p.
100

Inveen, D. 1987. The aquaculture industry in Washington State; an economic overview. Washington

State Department of Trade and Economic Development, Olympia, WA.

Jonsson, B., N. Jonsson, and L.P. Hansen. 1991. Differences in life history and migratory behaviour

between wild and hatchery-reared Atlantic salmon in nature. Aquaculture 98:69–78.

Kitsap County. 2000a. Kitsap County population. Internet document

http://www.wa.gov/esd/lmea/pubs/profiles/kitspop.htm.

Kitsap County. 2000b. Kitsap County industries, employment, and wages. Internet document

http://www.wa.gov/esd/lmea/pubs/profiles/kitsiew.htm

Lura, H., and H. Saegrov. 1991. Documentation of successful spawning of escaped farmed female

Atlantic salmon, Salmo salar, in Norwegian rivers. Aquaculture 98:151–159.

Lura, H., B.T. Barlaup, and H. Saegrov. 1993. Spawning behaviour of a farmed escaped female Atlantic

salmon (Salar salar). J. Fish Biol. 42:311–313.

McKinnell, S., A.J. Thompson, E.A. Black, B.L Wing, C.M. Guthrie III, J.F. Koerner, and J.H. Helle.

1997. Atlantic salmon in the North Pacific. Aquacult. Res. 28:145–157.

Milliken, A.S., and V. Lee. 1990. Pollution impacts from recreational boating: a bibliography and

summary review. RIU–G–90–002, University of Rhode Island Sea Grant Program, Narragansett,

RI, 26 p.

Moring, J.R. 1989. Documentation of unaccounted-for losses of chinook salmon from saltwater cages.

Prog. Fish. Cult. 51:173–176.

NMFS (National Marine Fisheries Service). 1995. Status review of coho salmon from Washington,

Oregon, and California. US Dep. Commer., NOAA Tech. Memo. NMFS–NWFSC–24, 258 p.

NMFS (National Marine Fisheries Service). 1996. Status review of West Coast steelhead from

Washington, Idaho, Oregon, and California. US Dep. Commer., NOAA Tech. Memo. NMFS–

NWFSC–27, 261 p.

NMFS (National Marine Fisheries Service). 1997a. Status review of chum salmon from Washington,

Oregon, and California. US Dep. Commer., NOAA Tech. Memo. NMFS–NWFSC–32, 280 p.

NMFS (National Marine Fisheries Service). 1997b. Impacts of California sea lions and Pacific harbor

seals on salmonids and on the coastal ecosystems of Washington, Oregon, and California. US

Dep. Commer., NOAA Tech. Memo. NMFS–NWFSC–28, 172 p.

NMFS (National Marine Fisheries Service). 1998. Status review of chinook salmon from Washington,

Idaho, Oregon, and California. US Dep. Commer., NOAA Tech. Memo. NMFS–NWFSC–35, 443 p.

Northern Aquaculture. 2000. Net results: northern aquaculture statistics 1999 – the year in review. Report

by Price Waterhouse Coopers. Northern Aquaculture 6(7).

NWIFC (Northwest Indian Fisheries Commission. 2000. Future brood document. Internet document

http://www.nwifc.wa.gov/00fbd/fpspens.trt.

ODFW (Oregon Department of Fish and Wildlife). 2000. The facts about Oregon's hatcheries. Internet

document http://www.dfw.state.or.us

OSU (Oregon State University). 2000. Net-pen salmon. Internet document

http://forums.library.orst.edu/forums
101

Pacific Fishing. 2001. 2000 Washington salmon landings and average price, p. 58. March issue.

Parsons, G.R. 1991. Effect of coastal land-use restrictions on housing prices; a repeat sale analysis. J.

Env. Econ. Manage. 22:25–37.

PSWQAT (Puget Sound Water Quality Action Team). 2000. Puget Sound's health 2000. Internet

document http://www.wa.gov/puget_sound/pshealth2000/index.html.

PSWQAT (Puget Sound Water Quality Action Team). 2001. Marinas and recreational boating. Internet

document http://www.wa.gov/puget_sound/Programs/Marinas.htm.

Radtke, H. 2000. The changing nature of salmon economics in the Columbia Basin. Report to the

Northwest Power Planning Council. The Research Group, Yachats, OR.

Rensel, J.E., R.P. Harris, and T.J. Tynan. 1988. Fishery contribution and spawning escapement of coho

salmon reared in net-pens in southern Puget Sound, Washington. North American J. Fish.

Manage. 8:359–366.

SOAEFD (Scottish Office, Agriculture Environment and Fisheries Department). 1997. Scottish fish

farms: annual production surveys, 1992–1997. Report by the Marine Laboratory, Aberdeen.

Stokes, R.L. 1988. The economics of salmon farming. In Fish culture in floating net-pens; Technical

Appendix E, Final programmatic environmental impact statement, Washington Department of

Fisheries, 1990, Olympia, WA.

USDA (US Department of Agriculture). 1999. Census of aquaculture, 1998. Volume 3, Special studies pt.

3, 1997 Census of Agriculture. US Department of Agriculture, National Agricultural Statistics

Service, Washington DC.

USDA (US Department of Agriculture). 2001. Aquaculture outlook. Economic Research Service, US

Department of Agriculture, March issue.

Washington Sea Grant Program. 2001. Fisheries. Internet document

http://www.wsg.washington.edu/outreach/mas/fisheries.html.

WDF (Washington State Department of Fisheries). 1990. The economics of salmon farming. In Fish

culture in floating net-pens. Washington Department of Fisheries, 1990, Olympia, WA.

WDFW (Washington State Department of Fish and Wildlife). 1994. Commercial salmon and recreational

salmon harvest levels, 1978–1993. Washington Department of Fish and Wildlife, Olympia, WA.

WDFW (Washington State Department of Fish and Wildlife). 1997a. WDFW News Release, December

23, 1997. Internet document: http://www.wa.gov/wdfw/do/dec97/dec2327a.htm.

WDFW (Washington State Department of Fish and Wildlife). 1997b. 1996-1997 Annual Report:

Department Statistics. Internet document: http://www.wa.gov/wdfw/anualrpt/97rpt-8.htm.

WDFW (Washington State Department of Fish and Wildlife). 2000. WDFW Hatcheries program:

statistics. Internet document http://www.wa.gov.wdfw/hat/hat-stat.htm.

WDL (Washington State Department of Licensing). 1997. Registered recreational boats, 1984–1996.

Washington Department of Licensing, Olympia, WA.

WDNR (Washington State Department of Natural Resources). 1999. Potential offshore finfish aquaculture

in the State of Washington. Aquatic Resources Division, Department of Natural Resources,

Olympia, WA.
102

WDNR (Washington State Department of Natural Resources). 2000a. Our changing nature: fish

hatcheries. Internet document http://www.wa.gov/dnr/ocn/pg63.html.

WDNR (Washington State Department of Natural Resources). 2000b. Aquatic resources policy

implementation manual. State of Washington, DNR Aquatic Resources Division, Olympia, WA.

WDNR (Washington State Department of Natural Resources). 2001. Aquatic lands lease data. State of

Washington, DNR Aquatic Resources Division, Olympia, WA.

Weston D.P. 1986. The environmental effects of floating mariculture in Puget Sound. Report prepared for

the Washington Department of Fisheries and department of Ecology, School of Oceanography,

Univ. Washington, Seattle, WA.

Wing, B.L., M.M. Masuda, C.M. Guthrie III, and J.H. Helle. 1998. Some size relationships and genetic

variability of Atlantic salmon (Salmo salar) escapees captured in Alaska fisheries, 1990–95. US

Dep. Commer., NOAA Tech. Memo. NMFS–AFSC–96, 32 p.

WRAC (Western Regional Aquaculture Center). 1999. Western regional aquaculture industry situation

and outlook report. Volume 5 (through 1997), Western Regional Aquaculture Center, Seattle,

WA.

Young et al. (1998). Report on current practices and benefits of finfish aquaculture in Maine. State

Department of Marine Resources, Augusta, ME.

Zook, B. 1999. Recreational and economic importance of introduced fishes in Washington. In ODFW and

NMFS, Management implications of co-occurring native and introduced fishes. NMFS, Portland,

OR. Internet document http://www.nwr.noaa.gov/nnative/proceed/final.pdf.

Chapter 3.

Angot V., and P. Brasseur. 1993. European farmed Atlantic salmon ( Salmo salar L.) are safe from

aniskid larvae. Aquaculture 118:339–344.

Baeverfjord, G., and A. Krogdahl. 1996. Development and regression of soybean meal induced enteritis in

Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. J.

Fish Dis. 19:375–387.

Baker, I.J., I.I. Solar, and E.M. Donaldson. 1988. Masculinization of chinook salmon (Oncorhynchus

tshawytscha) by immersion treatments using 17-ß-methyltestosterone around the time of hatching.

Aquaculture 72:359–367.

Bristow, G.A., and B. Berland. 1991. The effect of long term, low level Eubothrium sp. (cestoda:

pseudophyllides) infection on growth in farmed salmon (Salmo salar l.). Aquaculture

98:325–330.

Cappon, C.J. 1983. Content and chemical form of mercury and selenium in Lake Ontario salmon and

trout. J. Great Lakes Res. 10(4):429–434.

Cleland, G.B., J.F. Leatherland, and R.A. Sonstegard. 1987. Toxic effects in C57BI/6 and DBA/2 mice

following consumption of halogenated aromatic hydrocarbon-contaminated great lakes coho

salmon (Oncorhynchus kisutch Walbum). Env. Health Per. 75:153–157.

Cleland, G.B., P.J. Mc Elroy, and R.A. Sonstegard. 1989. Immunomodulation in C57BI/6 mice following

consumption of halogenated aromatic hydrocarbon-contaminated coho salmon (Oncorhynchus

kisutch) from Lake Ontario. J. Toxicol. Env. Health 17(2):405–420.
103

CFOI (Census of Fatal Occupational Injuries). 1999. Bureau of Labor statistical census of fatal

occupational injuries.

Dabrowski, K., P. Poczyczynski, G. Koeck, and B. Berger. 1989. Effect of partially or totally replacing

fish meal protein by soybean meal protein on growth, food utilization and proteolytic enzyme

activities in rainbow trout (Salmo gardneri). New in vivo test for exocrine pancreatic secretion.

Aquaculture 77:29–49.

Daly, H.B., D.R. Hertzler, and D.M. Sargent. 1989. Ingestion of environmentally contaminated Lake

Ontario salmon by laboratory rats increases avoidance of unpredictable aversive non-reward and

mild electric shock. Behav. Neurosci. 103(6):1356–1365.

Deardorff T.L., and M.L. Kent. 1989. Prevalence of larval Anisakis simplex in pen-reared and wild-caught

salmon (Salmonidae) from Puget Sound. J. Wildl. Dis. 25:416–419.

Drudi, D. 1998. Fishing for a living is dangerous work. Compensation and Working Conditions, Summer

issue, p. 3–7.

FAO (Food and Agriculture Organization). 1995. Code of conduct for responsible fisheries. Rome, Italy,

41 p.

FAO (Food and Agriculture Organization). 1997. Technical guidelines for responsible fisheries: No. 5,

Aquaculture development. Rome, Italy, 40 p.

Fong, G.W., and G.L. Brooks. 1989. Regulation of chemicals for aquaculture use. Food Tech. 43:88–93.

Gale, P., C. Young, G. Stanfield, and D. Oakes. 1998. Development of a risk assessment for BSE in the

aquatic environment. J. App. Micro. 84(4):467–477.

Green, B.W., and D.R. Teichert-Coddington. 2000. Human food safety and environmental assessment of

the use of 17-ß-methyltestosterone to produce male tilapia in the United States. J. World

Aquacult. Soc. 31(3):337–357.

Greenlees, K.J. 1997. Laboratory studies for the approval of aquaculture drugs. Prog. Fish. Cult.

59:141–148.

Hammond, B.G., J.L. Vinci, G.F. Hartnell, M.W. Naylor, C.D. Knight, E.H. Robinson, R.L. Fuchs, and

S.R. Padgette. 1996. The feeding value of soybeans fed to rats, chickens, catfish, and dairy cattle

is not altered by genetic incorporation of glyphosate tolerance.

J. Nutr. 126(3):717–727.

Haard, N.F. 1992. Control of chemical composition and food quality attributes of cultured fish. Food Res.

Int. 25:289–307.

Hung, Silas S.O., C.Y. Cho, and S.J. Slinger. 1981 Effect of oxidized fish oil, DL-α-tocopheryl acetate

and ethoxyquin supplementation on the vitamin e nutrition of rainbow trout (Salmo gairdneri) fed

practical diets. J. Nutr. 111:648–657.

Jensen, G.L., and K.J. Greenlees. 1997. Public health issues in aquaculture. Rev. Sci. Tech. Off. Int. Epiz

16(2):641–651.

JSA (Joint Subcommittee on Aquaculture). 1994. Guide to drug, vaccine, and pesticide use in aquaculture.

Texas Agricultural Extension Service, Texas A&M University, College Station.
104

Milliken, A.S., and V. Lee. 1990. Pollution impacts from recreational boating: a bibliography and

summary review. RIU–G–90–002, University of Rhode Island Sea Grant Program, Narragansett,

RI, 26 p.

Nettleton, J.C. 1990. Comparing nutrients in wild and farmed fish. Aquacult. Mag. Jan/Feb:34–41.

Nettleton, J.C., and J. Exler. 1992. Nutrients in wild and farmed fish and shellfish. J. Food Sci.

57(2):257–260.

Ostrowski, A.C., and D.L. Garling, Jr. 1986. Dietary androgen-estrogen combinations in growth

promotion in fingerling rainbow trout. Prog. Fish. Cult. 48:268–272.

Otwell, W.S. 1989. Regulatory status of aquacultured products. Food Tech. 43:103–105.

Piferreri, F., and E.M. Donaldson. 1989. Gonadal differentiation in coho salmon (Oncorhynchus kisutch)

after a single treatment with androgen or estrogen at different stages during ontogenesis.

Aquaculture 77(2–3):251–262.

Refstie, S., O.J. Korsoen, T. Storebakken, G. Baeverford, I. Lein, and A.J. Roem. 2000. Differing

nutritional responses to dietary soybean meal in rainbow trout (Oncorhynchus mykiss), and

Atlantic salmon (Salmo salar). Aquaculture 190:49–63.

Roderick, G.E., and T.C. Cheng. 1989. Parasites: occurrence and significance in marine aquaculture.

Food Tech. 43:98–102.

Sanz, A., A.E. Morales, M. De La Higuera, and G. Cardenate. 1994. Sunflower meal compared with

soybean meal as partial substitutes for fish meal in rainbow trout (Oncorhynchus mykiss) diets:

protein and energy utilization. Aquaculture 128:287–300.

Sargent, J.R. 1995. (n-3) polyunsaturated fatty acids and farmed fish. PJ Barnes & Associates, p. 67–94.

SCAN (Scientific Committee on Animal Nutrition). 2000. Opinion on the dioxin contamination of

feeding-stuffs and their contribution to the contamination of food of animal origin. European

Commission Health and Consumer Protection Directorate General. 105 p.

Seegal, R.F. 1999. Are PCBs the major neurotoxicant in Great Lakes salmon? Env. Res. 80(2):38–45.

Sniezko, S.F. 1957. Use of antibiotics in the diet of salmonid fishes. Prog. Fish. Cult. p. 84–84.

Sniezko, S.F., and E.M. Wood. 1954. The effect of some sulfonamides on the growth of brook trout,

brown trout, and rainbow trout. Trans. Am. Fish. Soc. 84:86–92.

Stoffregen, D.A., B.R. Paul, and J.G. Babish. 1996. Antibacterial chemotherapeutants for finfish

aquaculture: a synopsis of laboratory and field efficacy and safety studies. J. Aquat. Anim. Health

8(3):181–202.

Svensson, B.G., A. Nilsson, M. Hansson, C. Rappe, B. Aakesson, and S. Skerfving. 1991. Exposure of

dioxins and dibenzofurans through the consumption of fish. New Eng. J. Med. 324(1):8–12.

Sylvia, G., M.T. Morrissey, T. Graham, and S. Garcia. 1995. Organoleptic qualities of farmed and wild

salmon. J. Aquat. Food Prod. Tech. 4(1):51–64.

USOFR (US Office of the Federal Register). 1995a. Evidence to establish safety and effectiveness. Code

of Federal Regulations. Title 21 Part 514.1(B)8. US Government Printing Office, Washington,

DC.
105

USOFR (US Office of the Federal Register). 1995b. Good laboratory practice for nonclinical laboratory

studies. Code of Federal Regulations. Title 21, Part 58. US Government Printing Office,

Washington, DC.

USOFR (US Office of the Federal Register). 1995c. Astaxanthin. Code of Federal Regulations. Title 21,

Part 73.35. US Government Printing Office, Washington, DC.

Van Leeuwen, F.X.R., and M.M. Younes. 2000. Consultation on assessment of the health risk of dioxins:

reevaluation of the tolerable daily intake (TDI): Executive summary. Food Additives and

Contaminants. Volume 17(4)223–240.

Wagner, E.D. 1954. The effects of antibiotics and arsanilic acid on the growth of rainbow trout

fingerlings. Prog. Fish. Cult. 16(1):36–38.

Ward, D.R. 1989. Microbiology of aquaculture products. Food Tech. 43:82–87.

Wessells, C.R., and D. Holland. 1998. Predicting consumer choices for farmed and wild salmon.

Aquacult. Econ. Manage. 2(2):49–59.

WHO (World Health Organization). 1999. Food safety issues associated with products from aquaculture:

report of joint FAO/NACO/WHO study group. WHO Technical Report Series 883, 46 p.

Yu, T.C., R.O. Sinnhuber, and J.D. Hendricks. 1979. Effect of steroid hormones on the growth of juvenile

coho salmon (Oncorhynchus kisutch). Aquaculture 16(4):351–359.

Chapter 4.

Ackefors, H. 1986. The impact on the environment by cage farming in open water. J. Aquacult. Trop.

1:25–33.

Ackefors, H., and M. Enell. 1990. Discharge of nutrients from Swedish fish farming to adjacent sea areas.

Ambio 19(1)28–35.

Ackefors, H., and M. Enell. 1994. The release of nutrients and organic matter from aquaculture systems in

Nordic countries. J. Appl. Ichthyol. 10(4):225–241.

Ammann, L.P., W.T. Waller, J.H. Kennedy, K.L. Dickson, and F.L. Mayer. 1997. Power, sample size and

taxonomic sufficiency for measures of impact in aquatic systems. Environ. Toxicol. Chem.

16(11):2421–2431.

Anderson, E. 1992. Benthic recovery following salmon farming: study site selection and initial surveys.

Report to the Water Quality Branch, Ministry of Environment, Lands and Parks, Province of

British Columbia, 170 p.

Anderson, S. 1998. Dietary supplementation of salmon diets with zinc: alternative sources and their

effects on the environment. Report prepared by Steward Anderson, Aquaculture Industry

Coordinator, Hoffmann La-Roche Ltd., 9 p.

APHA (American Public Health Association). 1992. Standard methods for the examination of water and

wastewater. 18th Edition, APHA/WEF/AWWA, 1992.

Arntz, W.E., and H. Rumohr. 1982. An experimental study of macrobenthic colonization and succession,

and the importance of seasonal variation in temperate latitudes. J. Exp. Mar. Biol. Ecol. 64:17–45.

Aure, J., A.S. Ervik, P.J. Johannesen and T. Ordemann. 1988. The environmental effects of seawater fish

farms. Fisken Havet ISSN 0071–5638 (English abstract).
106

Bagarinao, T.U. 1993. Sulfide as a toxicant in aquatic habitats. SEAFDEC-ASIAN-Aquacult. 15(3):2–4.

Banse, K., R. Horner and J. Postel. 1990. Fish farms innocent. Seattle Post Intelligencer, August 4, 1990.

Beveridge, M.C.M, M.J. Phillips, and R. M. Clarke. 1991. A quantitative and qualitative assessment of

wastes from aquatic animal production, p. 506–533. In D. Brune and J.R. Tomasso (eds.),

Aquaculture and Water Quality. Advances in World Aquaculture, World Aquaculture Society,

Baton Rouge, LA.

Black, K.D., S. Fleming, S.D. Nickell, and P.M.F. Pereira. 1997. The effects of ivermectin, used to control

sea lice on caged farmed salmonids, on infaunal polychaetes. ICES J. Mar. Sci. 54:276–279.

Braaten, B., J. Aure, A. Ervik, and E. Boge. 1983. Pollution problems in Norwegian fish farming. ICES

C.M.1983/F:26.

Brett, J.R., and C.A. Zala. 1975. Daily pattern of nitrogen excretion and oxygen consumption of sockeye

salmon (Oncorhynchus nerka) under controlled conditions. J. Fish. Res. Board Can.

32(12)2479–2486.

Brooks, K.M. 1991. Environmental sampling at Sea Farm Washington Inc., net-pen facility II in Port

Angeles Harbor, WA during 1991. Produced for the Washington Department of Natural

Resources, Olympia, WA, 16 p.

Brooks, K.M. 1992. Environmental sampling at the Sea Farm Washington Inc., net-pen facility II in Port

Angeles Harbor, WA during 1992. Produced for the Washington Department of Natural

Resources, Olympia, WA, 7 p.

Brooks, K.M. 1993a. Environmental sampling at Sea Farm Washington Inc., net-pen facility II in Port

Angeles Harbor, WA during 1993. Produced for the Washington Department of Natural

Resources, Olympia, WA, 18 p.

Brooks, K.M. 1993b. Environmental sampling at Paradise Bay Salmon Farm located in Port Townsend

Bay, WA January 1993 following abandonment of the site. Produced for the Washington State

Department of Natural Resources, Olympia, WA.

Brooks, K.M. 1994a. Environmental sampling at Sea Farm Washington, Inc., net-pen facility II in Port

Angeles Harbor, Washington during 1994. Produced for the Washington Department of Natural

Resources, Olympia, WA, 18 p.

Brooks, K.M. 1994b. Environmental sampling at Global AquaUSA Inc., saltwater II salmon farm located

in Rich Passage, WA 1994. Prepared for Global Aqua USA Inc., 600 Ericksen Avenue N.E.,

Suite 370, Bainbridge Island, WA. 98110, 20 p.

Brooks, K.M. 1995a. Environmental sampling at Sea Farm Washington Inc., net-pen facility II in Port

Angeles Harbor, WA during 1995. Produced for the Washington Department of Natural

Resources, Olympia, WA, 20 p.

Brooks, K.M. 1995b. Environmental sampling at Global Aqua USA Inc., saltwater II salmon farm located

in Rich Passage, WA 1994. Prepared for Global Aqua –USA Inc., 600 Ericksen Avenue, N.E.,

Suite 370, Bainbridge Island, WA 98110, 20 p.

Brooks, K.M. 2000a. Salmon farm benthic and shellfish effects study 1996 – 1997. Aquatic

Environmental Sciences, 644 Old Eaglemount Road, Port Townsend, WA 98368, 117 p.
107

Brooks, K.M. 2000b. Sediment concentrations of zinc near salmon farms in British Columbia, Canada

during the period June through August 2000. BC Salmon Farmers Association, 1200 West Pender

Street, Vancouver, BC V6E 2S9, 12 p.

Brooks, K.M. 2000c. Database report to the Ministry of Environment describing sediment

physicochemical response to salmon farming in British Columbia, 1996 through April 2000. BC

Salmon Farmers Association, 1200 West Pender Street, Vancouver, BC V6E 2S9, 41 p.

Brooks, K.M. 2000d. Determination of copper loss rates from Flexgard XITM treated nets in marine

environments and evaluation of the resulting environmental risks. Report to the Ministry of

Environment for the BC Salmon Farmers Association, 1200 West Pender Street, Vancouver, BC

V6E 2S9, 24 p.

Brooks, K.M. 2000e. Sediment concentrations of sulfides and total volatile solids near salmon farms in

British Columbia, Canada during the period June through August 2000, and recommendations for

additional sampling. Report to the Ministry of Environment prepared for the BC Salmon Farmers

Association, 1200 West Pender Street, Vancouver, BC V6E 2S9, 16 p.

Brooks, K.M. 2000f. Results of the June 2000 interim salmon farm monitoring at Stolt Sea Farm, Inc.

salmon aquaculture tenures located in British Columbia. Submitted to the Ministry of

Environment for Stolt Sea Farm, Inc., 1261 Redwood Street, Campbell River, BC V9W 3K7.

Brooks, K.M. 2000g. Literature review and model evaluation describing the environmental effects and

carrying capacity associated with the intensive culture of mussels (Mytilus edulis

galloprovincialis). Technical appendix to an Environmental Impact Statement produced for

Taylor Resources, Southeast 130 Lynch Road, Shelton, WA 98584.

Brooks, K. 2001. Evaluation of the relationship between salmon farm biomass, organic inputs to

sediments, physico-chemical changes associated with the inputs, and the infaunal response - with

emphasis on total sediment sulfides, total volatile solids, and oxygen reduction potential as

surrogate end-points for biological monitoring. Report to the Technical Advisory Group, B.C.

Ministry of the Environment, 183p. (Available from B.C. Ministry of the Environment, 2080-A

Labieux Road, Nanaimo, B.C. Canada V9T 6J9).

Brown, J.R., R.J. Gowen, and D.S. McLusky. 1987. The effect of salmon farming on the benthos of a

Scottish sea loch. J. Exp. Mar. Biol. Ecol. 109:39–51.

Burridge, L.E. and K. Haya. 1993. The lethality of ivermectin, a potential agent for treatment of salmonids

against sea lice, to the shrimp Crangon septemspinosa. Aquaculture 117:9–14.

Calderwood, V., W. Kusser, and S.G. Newman. 1988. Types and prevalence of diseases in farmed and

wild salmon at the time of slaughter. Unpublished study prepared for Dr. Brad Hicks, British

Columbia Ministry of Agriculture, Farms and Fisheries, 21 p.

Chow, K.W., and W.R. Schell. 1978. The minerals. In Fish Feed Technology. A series of lectures

presented at the FAO/UNDP training course in fish feed technology held at the College of

Fisheries, University of Washington, Seattle, Washington, 9 October–15 December, 1978. FAO

Publication ADCP/REP/80/11.

Collier, L.M., and E.H. Pinn. 1998. An assessment of the acute impact of the sea lice treatment ivermectin

on a benthic community. J. Exp. Mar. Bio. Ecol. 230:131–147.

Costello, M.J. 1993. Review of methods to control sea lice (Caligidae: Crustacea) infestations on salmon

(Salmo salar) farms. In G.A. Boxshall, and D. Defaye (eds.), Pathogens of Wild and Farmed Fish:

Sea Lice. Ellis Horwood, Chichester.
108

Crema, R., D. Prevedelli, A. Valentini, and A. Castelli. 2000. Recovery of the macrozoobenthic

community of the Comacchio lagoon system (northern Adriatic Sea). Ophelia 52(2):143–152.

Crisp, D.J. 1964. The effects of the severe ice winter of 1962–63 on marine life in Britain.

J. Anim. Ecol. 33:165–210.

Cross, S.F. 1990. Benthic impacts of salmon farming in British Columbia. Summary Report (Volume I)

prepared for the Ministry of Environment, Water Management Branch, 765 Broughton St.

Victoria, BC, 78 p.

Cross, S.F. 1993. Oceanographic characteristics of net-cage culture sites considered optimal for

minimizing environmental impacts in coastal British Columbia. Prepared for the Ministry of

Agriculture, Fisheries and Food, Courtenay, Canada BC. Prepared by Aquametrix Research Ltd.,

Sidney, BC, 86 p.

Davies, I.M., J.G. McHenery, and G.H. Rae. 1997. Environmental risk from dissolved ivermectin to

marine organisms. Aquaculture 158:263–275.

Davies, I.M., P.A. Gillibrand, J.G. McHenery, and G.H. Rae. 1998. Environmental risk of ivermectin to

sediment dwelling organisms. Aquaculture 163:29–46.

DFO (Department of Fisheries and Oceans, Canada). 1996. Monitoring of sea lice treatment chemicals in

southwestern New Brunswick. DFO Science High Priority Project. Project Code 9019. Project

leaders: W. Watson-Wright and B. Chang. DFO St. Andrews Biological Station, New Brunswick

Canada.

Di Toro, D.M., J.D. Mahony, D.J. Hansen, K.J. Scott, A.R. Carlson, and G.T. Ankley. 1992. Acid volatile

sulfide predicts the acute toxicity of cadmium and nickel in sediments. Environ. Sci. Technol.

26:96–101.

Eagle, R.A. 1975. Natural fluctuations in a soft bottom community. J. Mar. Biol. Assoc. UK

55:865–878.

Earll, R.C., G. James, C. Lumb, and R. Pagett. 1984. A report on the effects of fish farming on the marine

ecology of the Western Isles. Report to the Nature Conservancy Council. Contract MF3/11/9.

Marine Biological Consultants Ltd.

Einen, O., I. Holmefjord, T. Asgard, and C. Talbot. 1995. Auditing nutrient discharges from fish farms:

theoretical and practical considerations. Aquaculture Res. 26:701–713.

Ellis, D. 1996. Net loss; the salmon netcage industry in British Columbia. A report to the David Suzuki

Foundation, Suite 219, 2211 West Fourth Avenue, Vancouver, BC V6K 4S2, 146 p.

Enell, M. and Lof, J. 1983. Environmental impact of aquaculture: sedimentation and nutrient loadings

from fish cage culture farming. Vatten. 39:346–375.

Enell, M., and H. Ackefors. 1992. Development of Nordic salmonid production in aquaculture and

nutrient discharges into adjacent sea areas. Aquaculture Europe. 16:6–11.

EAO (Environmental Assessment Office, Canada BC). 1997. British Columbia salmon aquaculture

review. Environmental Assessment Office, Government of British Columbia, 836 Yates Street,

Victoria, BC V8V 1X4.

EPA (US Environmental Protection Agency). 1986. Quality criteria for water – 1986. EPA

440/5–86–001. US Environmental Protection Agency, Office of Water, Regulations and

Standards.
109

EPA (US Environmental Protection Agency). 1994. Briefing report to the EPA science advisory board on

the EqP approach to predicting metal bio-availability in sediment and the derivation of sediment

quality criteria for metals. EPA 822/D–94/002.

EPA (US Environmental Protection Agency). 1995. Ambient water quality criteria – saltwater copper

addendum. US Environmental Protection Agency, Office of Water, Office of Science and

Technology, Washington, DC.

ERT (ERT Ltd.). 1997. Ivermectin field trials: impact on benthic assemblages, incorporating additional

data. Report to the Scottish Salmon Growers Association. ERT Ltd., Edinburgh, Scotland. ERT

97/029.

ERT (ERT Ltd.). 1998. Ivermectin field trials: impact on benthic assemblages. Report to the Scottish

Salmon Growers Association. ERT Ltd., Edinburgh, Scotland. ERT 97/223.

Ervik, A., P. Johannessen, and J. Aure. 1985. Environmental effects of marine Norwegian fish farms.

ICES C.M. 1985 F:37.

Ervik, A., P. K. Hansen, J. Aure, A. Stigebrandt, P. Johannessen, and T. Jahnsen. 1997. Regulating the

local environmental impact of intensive marine fish farming. I. The concept of the MOM system.

Aquaculture 158:85–94.

Findlay, R.H. 1992. The effects of salmon net-pen aquaculture on the benthic microbial and macrofaunal

community: model verification. University of Maine Center for Marine Studies, Sea Grant

College Program. Unpublished project summary.

Findlay, R.H., and L. Watling. 1994. Toward a process level model to predict the effects of salmon netpen aquaculture on the benthos, p.47–77. In B.T. Hargrave (ed.), Modeling Benthic Impacts of

Organic Enrichment from Marine Aquaculture. Can. Tech. Rep. Fish. Aquat. Sci. 1949, 125 p.

Folke, C., N. Kautsky, and M. Troell. 1994. The costs of eutrophication from salmon farming:

implications for policy. J. Env. Man. 40:173–182.

Fox, W.P. 1990. Modeling of particulate deposition under salmon net-pens. In Final Programmatic

Environmental Impact Statement: Fish Culture in Floating Net-Pens (Technical Appendices).

Washington State Department of Fisheries, 115 General Administration Building, Olympia, WA

98504.

GESAMP (Joint Group of Expert on Scientific Aspects of Marine Environmental Protection). 1996.

Monitoring the ecological effects of coastal aquaculture wastes. GESAMP Reports and Studies

No. 57, FAO, Rome, 38 p.

Gormican, S.J. 1989. Water circulation, dissolved oxygen, and ammonia concentrations in fish net-cages.

M.Sc. Thesis. Univ. British Columbia, Vancouver BC.

Gowen, R.J., and N.B. Bradbury. 1987. The ecological impact of salmonid farming in coastal waters: a

review. Oceanogr. Mar. Biol. Annu. Rev. 25:563–575.

Gowen, R.J., D. Smyth, and W. Silvert. 1994. Modelling the spatial distribution and loading of organic

fish farm waste to the seabed, p.19–39. In B.T. Hargrave (ed.), Modeling Benthic Impacts of

Organic Enrichment From Marine Aquaculture. Can. Tech. Rep. Fish. Aquat. Sci. 1949.

Gowen, R.J., D.P. Weston, and A. Ervik. 1991. Aquaculture and the benthic environment: a review,

p.187–205. In C.B. Cowey and C.Y. Cho (eds.), Nutritional Strategies and Aquacultural Waste.

Fish Nutrition Research Laboratory, Department of Nutritional Sciences, Univ. Guelph, Ontario,

Canada.
110

Gowen, R.J., J. Brown, N. Bradbury, and D.S. McLusky. 1988. Investigation into benthic enrichment,

hypernutrification and eutrophication associated with mariculture in Scottish coastal waters

(1984–1988). Report by the Department of Biological Sciences, Univ. Stirling, Scotland.

Goyette, D., and K.M. Brooks. 1999. Creosote evaluation. Phase II, Sooke Basin study: baseline to 535

days post-construction, 1995–1996. Commercial Chemicals Division, Environment Canada,

Pacific and Yukon Region, 568 p.

Grant, A., and A.D. Briggs. 1998a. Use of ivermectin in marine fish farms: some concerns. Mar. Pol.

Bull. 36(8):566–568.

Grant, A., and A.D. Briggs. 1998b. Toxicity of ivermectin to estuarine and marine invertebrates. Mar.

Pol. Bull. 36(7):540–541.

Hansen, P.K., K. Pittman, and A. Ervik. 1990. Effects of organic waste from marine fish farms on the sea

bottom beneath the cages. ICES C.M. 1990/F:34, 9 p.

Hargrave, B.T. 1994. A benthic enrichment index, p.79–91. In B.T. Hargrave (ed.), Modeling Benthic

Impacts of Organic Enrichment from Marine Aquaculture. Can. Tech. Rep. Fish. Aquat. Sci.

1949.

Hargrave, B.T., G.A. Phillips, L.I. Doucette, M.J. White, T.G. Milligan, D.J. Wildish, and R.E. Cranston.

1995. Biogeochemical observations to assess benthic impacts of organic enrichment from marine

aquaculture in the Western Isles region of the Bay of Fundy, 1994. Can. Tech. Rep. Fish. Aquat.

Sci. 2062, 159 p.

Hargrave, B.T., G.A. Phillips, L.I. Doucette, M.J. White, T.G. Milligan, D.J. Wildish, and R.E. Cranston.

1997. Assessing benthic impacts of organic enrichment from marine aquaculture. Water, Air and

Soil Pollution, 99:641–650.

Henderson, A.R., and D.J. Ross. 1995. Use of macrobenthic infaunal communities in the monitoring and

control of the impact of marine cage fish farming. Aquaculture Research. 26:659–678.

Johannessen, P.J., H.B. Botnen, and O.F. Tvedten. 1994. Macrobenthos: before, during and after a fish

farm. Aquacult. Fish. Manage. 25:55–66.

Johnsen, F., and A. Wandsvik. 1991. The impact of high energy diets on pollution control in the fish

farming industry, p.51–62. In C.B. Cowey and C.Y. Cho (eds.), Nutritional Strategies and

Aquaculture Waste. Proc. 1st International Symposium on Nutritional Strategies in Management

of Aquaculture Waste. Univ. Guelph, Ontario, Canada.

Johnsen, R.I., O. Grahl-Nelson, and B.T. Lunestad. 1993. Environmental distribution of organic waste

from a marine fish farm. Aquaculture 118:229–244.

Johnson, S.C., and L. Margolis. 1993. Efficacy of ivermectin for control of the salmon louse

Lepeophtheirus salmonis on Atlantic salmon. Dis. Aquat. Org. 17:101–105.

Kadowaki, S., T. Kasedo, T. Nakazono. Y. Yamashita, and H. Hirata. 1980. The relation between

sediment flux and fish feeding in coastal culture farms. Mem. Fac. Fish. Kagoshima Univ.

29:217–224.

Karakassis, I., E. Hatziyanni, M. Tsapakis, and W. Plaiti. 1999. Benthic recovery following cessation of

fish farming: a series of successes and catastrophes. Marine Ecology Progress Series

184:205–218.
111

Kontali. 1996. Introduction of new vaccines in the production of salmon – analysis of the consequences.

Knotali analyses. Industriv. 18, 6500 Kr..sund Norway, 25 p.

Levings, C.D. 1997. Waste discharge, p.WD1–47. In British Columbia Salmon Aquaculture Review,

Environmental Assessment Office, Vancouver BC.

Lewis, A.G., and A. Metaxas. 1991. Concentrations of total dissolved copper in and near a copper-treated

salmon net-pen. Aquaculture 99:269–276.

Long, E.R., D.D. MacDonald, S.L. Smith, and F.D. Calder. 1995. Incidence of adverse biological effects

within ranges of chemical concentrations in marine and estuarine sediments. Environmental

Management 19(1):81–97.

Lu, L., and R.S.S. Wu. 1998. Recolonization and succession of marine macrobenthos in organic-enriched

sediment deposited from fish farms. Environ. Pollution 101:241–251.

Lunz, J.D., and D.R. Kendall. 1982. Benthic resources assessment technique: A method for quantifying

the effects of benthic community changes on fish resources. Oceans 1021–1027.

MacDonald, D.D. 1994. Approach to the assessment of sediment quality in Florida coastal waters.

Florida Department of Environmental Protection, Tallahassee, FL.

Mahnken, C.V.W. 1993. Benthic faunal recovery and succession after removal of a marine fish farm.

Doctoral dissertation submitted to the Univ. Washington, Seattle, WA, 290 p.

Mayer, I., and E. McLean. 1995. Bioengineering and biotechnological strategies for reduced waste

aquaculture. Water Science and Technology 31:85–102.

Mazzola, A., S. Mirto and R. Danovaro. 1999. Initial fish-farm impact on meiofaunal assemblages in

coastal sediments of the western Mediterranean. Mar. Pollution Bull. 38(12):1126–1133.

Meijer, L.E., and Y. Avnimelech. 1999. On the use of micro-electrodes in fish pond sediments. Aquacult.

Eng. 21(2):71–83.

Merican, Z.O., and M.J. Phillips. 1985. Solid waste production from rainbow trout (Salmo gairdneri

Richardson) cage culture. Aquacult. Fish. Manag. 1:55–69.

Mills, E.L. 1969. The community concept in marine zoology, with comments on continua and instability

in some communities: a review. J. Fish. Res. Board Can. 26:1415–1428.

Morrisey, D.J., M.M. Gibbs, S.E. Pickmere, and R.G. Cole. 2000. Predicting impacts and recovery of

marine-farm sites in Stewart Island, New Zealand, from the Findlay-Watling model. Aquaculture

185(3–4):257–271.

NSSP (National Shellfish Sanitation Program). 1997. Manual of operations, I Sanitation of Shellfish

Growing Areas. US Department of Health and Human Services, Public Health Service, Food and

Drug Administration. Washington, DC 20204.

Parametrix. 1990. Final programmatic environmental impact statement fish culture in floating net-pens.

Prepared by Parametrix Inc., for Washington State Department of Fisheries, 115 General

Administration Building, Olympia, WA 98504, 161 p.

Parsons, T.R., B.E. Rokeby, C.M. Lalli, and C.D. Levings. 1990. Experiments on the effect of salmon

farm wastes on plankton ecology. Bull. Plankton Soc. Japan. 37:49–57.
112

Pearson, T.H. 1986. Disposal of sewage in dispersive and non-dispersive areas: contrasting case histories

in British coastal waters, p.577–595. In G. Kullenberg (ed.), The Role of the Oceans as a Waste

Disposal Option. D. Reidel Publishing Company, Dordrecht, The Netherlands.

Pearson, T.H., and R. Rosenberg. 1978. Macrobenthic succession in relation to organic enrichment and

pollution of the marine environment. Oceanogr. Mar. Biol. Annu. Rev. 16:229–311.

Pease, B.G. 1977. The effect of organic enrichment from a salmon mariculture facility on the water

quality and benthic community of Henderson Inlet, Washington. Ph.D. Thesis, Univ. Washington,

Seattle, 145 p.

Persson, G. 1988. Relationship between feed, productivity and pollution in the farming of large rainbow

trout (Salmo gairdneri). National Swedish Environmental Protection Board Report No. 3534.

Peterson, L.K., J.M. D’Auria, B.A. McKeown, K. Moore, and M. Shum. 1991. Copper levels in the muscle

and liver tissue of farmed chinook salmon, Oncorhynchus tshawytscha. Aquaculture 99:105–115.

Poole, N.J., D.J. Wildish, and D.D. Kristmanson. 1978. The effects of the pulp and paper industry on the

aquatic environment. CRC Crit. Rev. Environ. Control 8:153–195.

Pridmore, R.D., and J.C. Rutherford. 1992. Modeling phytoplankton abundance in a small-enclosed bay

used for salmon farming. Aquacult. Fish. Manage. 23:525–542.

PSEP (Puget Sound Estuary Protocols). 1986. Recommended protocols for measuring selected

environmental variables in Puget Sound. Puget Sound Water Quality Authority, P.O. Box 40900,

Olympia, WA 98504-0900.

Rensel, J.E. 1988. Environmental sampling at the American Aqua foods net-pen site near Lone Tree Point

in north Skagit Bay. Prepared by Rensel Associates, Seattle, WA, Pacific Aqua Foods, Vancouver

BC, and Washington Department of Natural Resources, 7 p.

Rensel, J.E. 1989. Phytoplankton and nutrient studies near salmon net-pens at Squaxin Island, WA. In,

Technical appendices to the final programmatic environmental impact statement, fish culture in

floating net-pens. Prepared for the Washington Department of Fisheries, Olympia, WA, 33 p.

Ritz, D., M.E. Lewis, and M. Shen. 1989. Response to organic enrichment of infaunal macrobenthic

communities under salmonid sea cages. Mar. Biol. (NY) 103:211–214.

Roberts, R.J. 1978. Fish Pathology. Bailliere Tindall, University Press, Aberdeen, Great Britain, 318 p.

Rosenthal, H., D.J. Scarratt, and M. McInerney-Northcott. 1995. Aquaculture and the environment,

p.451–500. In A.D. Boghen (ed.), Cold-water aquaculture in Atlantic Canada. 2nd Edition. Ins.

Can. Tech. Dev. Reg.

Rosenthal, H.D., D. Weston, R. Gowen, and E. Black. 1988. Environmental impact of mariculture.

Cooperative research report. ICES:154.

Roth, M., R.H. Richards, and C. Sommerville. 1993. Current practices in the chemotherapeutic control of

sea lice infestations in aquaculture: a review. J. Fish. Dis. 16:1–26.

Samuelsen, O.B., A. Ervik, and E. Solheim. 1988. A qualitative and quantitative analysis of the sediment

gas and diethylether extract of the sediment from salmon farms. Aquaculture 74:277–285.

SEPA (Scottish Environment Protection Agency). 1997. Cage fish farms: sea lice treatment chemicals risk

assessment of azamethiphos. SEPA Policy No. 17.
113

SEPA (Scottish Environment Protection Agency). 1998a. Ivermectin: a review of the laboratory and field

data available to SEPA. (Source unknown).

SEPA (Scottish Environment Protection Agency). 1998b. The use of cypermethrin in marine cage fish

farming risk assessment, EQS, and recommendations. SEPA Policy No. 30.

SEPA (Scottish Environment Protection Agency). 1999a. Emamectin benzoate use in marine fish farming.

SEPA, Fish Farm Advisory Group, SEPA Report 66/99.

SEPA (Scottish Environment Protection Agency). 1999b. Calicide (teflubenzuron): authorization for use

as an in-feed sea lice treatment in marine cage salmon farms. Risk assessment, EQS, and

recommendations. SEPA Policy No. 29.

SEPA. (Scottish Environment Protection Agency). 2000. Regulation and monitoring of marine cage fish

farming in Scotland: a manual of procedures. Internet document

http://www.sepa.org.uk/publications/fishfarmmanual.htm.

Silvert, W. 1994a. Modeling benthic deposition and impacts of organic matter loading, p.1–30. In B.T.

Hargrave (ed.), Modeling Benthic Impacts of Organic Enrichment From Marine Aquaculture.

Can. Tech. Rep. Fish. Aquat. Sci. 1949.

Silvert, W. 1994b. Simulation models of finfish farms. J. Appl. Ichthyol. 10:349–352.

Silvert, W., and J.W. Sowles. 1996. Modeling environmental impacts of marine finfish aquaculture. J.

Appl. Ichthyol. 12:75–81.

Skalski, J.R., and D.H. McKenzie. 1982. A design for aquatic monitoring programs. J. Environ. Manag.

14:237–251.

Smith, P.R., M. Moloney, A. McElligott, S. Clarke, R. Palmer, J. O’Kelly, and F. O’Brien. 1993. The

efficiency of oral ivermectin in the control of sea lice infestations of farmed Atlantic salmon. In

G.A. Boxshall and D. Defaye (eds.), Pathogens of Wild and Farmed Fish – Sea Lice. Shorewood

Publishing, New York, NY.

Sowles, J.W., L. Churchill, and W. Silvert. 1994. The effect of benthic carbon loading on the degradation

of bottom conditions under farm sites, p.31–79. In B.T. Hargrave (ed.), Modeling Benthic

Impacts of Organic Enrichment From Marine Aquaculture. Can. Tech. Rep. Fish. Aquat. Sci.

1949.

Stanley, S.O., J. Leetley, D. Miller, and T.H. Pearson. 1980. Chemical changes in the sediments of Loch

Eil arising from the input of cellulose fiber, p.409–418. In J. Albaiges (ed.), Analytical

Techniques in Environmental Chemistry. Pergamon Press, Oxford.

Striplin Environmental Associates, Inc. 1996. Development of reference value ranges for benthic infauna

assessment endpoints in Puget Sound. Final Report prepared for the Washington State

Department of Ecology, Sediment Management Unit, 45 p.

Sutherland, T.F., A.J. Martin, and C.D. Levings. 2000. The characterization of suspended particulate

matter surrounding a salmonid net-pen in the Broughton Archipelago, British Columbia.

Department of Fisheries and Oceans, West Vancouver Laboratory, 4160 Marine Drive, West

Vancouver, BC V7V 1N6, 15 p.

Taylor, F.J.R. 1993. Current problems with harmful phytoplankton blooms in British Columbia waters,

p.699–703. In T.J. Smayda and Y. Shimizu (eds.), Toxic Phytoplankton Blooms in the Sea.

Elsevier Science Publishers, Amsterdam.
114

Taylor, F.J.R., and R. Horner. 1994. Red tides and other problems with harmful algal blooms in Pacific

Northwest coastal waters, p.175–186. In R.C.H. Wilson, R.J. Beamish, Aitkens, and J. Bell (eds.),

Review of the marine environment and biota of Strait of Georgia, Puget Sound, and Juan de Fuca

Strait. Can. Tech. Rep. Fish. Aquat. Sci. 1948.

Taylor, L.A., P.M. Chapman, R.A. Miller and R.V. Pym. 1998. The effects of untreated municipal sewage

discharge to the marine environment off Victoria, BC Canada. Water quality international 1998.

IAWQ 19th Biennial International Conference; 21–26 June, 1998, Vancouver, Canada.

Thain, J.E., I.M. Davies, G.H. Rae, and Y.T. Allen. 1997. Acute toxicity of ivermectin to the lugworm

Arenicola marina. Aquaculture 159:47–52.

Tsutsumi, H., T. Kikuchi, M. Tanaka, T. Higashi, K. Imasaka, and M. Miyazaki. 1991. Benthic faunal

succession in a cove organically polluted by fish farming. Mar. Poll. Bull. 23:233–238.

WAC (Washington Administrative Code). 1991. Sediment management standards. Chapter 173–204,

State of Washington Administrative Code, WAC 173–204, 61 p.

Wang, F., and P.M. Chapman. 1999. Biological implications of sulfide in sediment: a review focusing on

sediment toxicity. Env. Tox. Chem. 18(11):2526–2532.

Warrer-Hansen, I. 1982. Evaluation of matter discharged from trout farming in Denmark,

p.57–63. In J.S. Alabaster (ed.), Workshop of Fish-farm Effluents, Silkeborg, Denmark, 26–28

May 1981. EIFAC Tech. Pap. 41.

Weston, D. 1986. The environmental effects of floating mariculture in Puget Sound. Report prepared for

the Washington State Department of Fisheries and the Washington State Department of Ecology,

148 p.

Weston, D.P. 1990. Quantitative examination of macrobenthic community changes along an organic

enrichment gradient. Mar. Ecol. Prog. Ser. 61:233–244.

Weston, D.P., and R. J. Gowen. 1988. Assessment and prediction of the effects of salmon net-pen culture

on the benthic environment. Final Programmatic Environmental Impact Statement, Fish Culture

in Floating Net-Pens, prepared for the Washington State Department of Fisheries Olympia, WA,

62 p.

Wildish, D.J., H.M. Akagi, N. Hamilton, and B.T. Hargrave. 1999. A recommended method for

monitoring sediments to detect organic enrichment from mariculture in the Bay of Fundy. Can.

Tech. Rep. Fish. Aquat. Sci. No. 2286.

Winsby, M., B. Sander, D. Archibald, M. Daykin, P. Nix, F.J.R. Taylor, and D. Munday. 1996. The

environmental effects of salmon netcage culture in British Columbia. Prepared for the Ministry of

Environment, Lands and Parks, Environmental Protection Department, Industrial

Waste/Hazardous Contaminants Branch, 1106 – 1175 Douglas Street, Victoria, BC, 214 p.

Chapter 5.

ADF&G (Alaska Department of Fish and Game). 1999. Alaska expresses concern over Atlantic salmon.

Imported species poses threat to wild salmon stocks. Press release, 1 March, 1999, Alaska

Department of Fish & Game, Anchorage, AK.

Alverson, D.L., and G.T. Ruggerone. 1997. Escaped farm salmon: environmental and ecological concerns.

In British Columbia Salmon Aquaculture Review, Environmental Assessment Office, Vancouver

BC. Discussion paper, Part B, Volume 3, August 1997. Internet document

http://www.eao.gov.bc.ca.
115

Amos K.H., and A. Appleby. (1999) Atlantic salmon in Washington State: a fish management

perspective. Washington Department of Fish and Wildlife, Olympia, WA. Internet document

www.wa.gov:80/wdfw/fish/atlantic/summary.htm

Bachen, B. 1994. The impacts of success: a case history of Hidden Falls hatchery, p. 46–56. Northeast Pacific

Pink and Chum Salmon Workshop, Feb. 24–26, 1993, Juneau, AK.

Bartley, D.M., G.A.E. Gall, and B. Bentley. 1990. Biochemical detection of natural and artificial

hybridization of chinook and coho salmon in northern California. Tran. Am. Fish. Soc.

119:431–437.

Beall, E., M. Heland, and C. Marty. 1989. Interspecific relationships between emerging Atlantic salmon,

Salmon salar, and coho salmon, Oncorhynchus kisutch, juveniles. J. Fish. Biol. 35(A):285–293.

Beamesderfer, R.C., and A.A. Nigro. 1988. Predation by resident fish on juvenile salmonids in a mainstem

Columbia reservoir: III. Abundance and distribution of northern squawfish, walleye, and smallmouth

bass, p. 211–248. In B.E. Rieman (ed.), Predation by Resident Fish on Juvenile Salmonids in John

Day Reservoir, 1983–1986, Vol. 1, Final Research Report, US Dept. Energy, Portland, OR.

Beamesderfer, R.C., D.L. Ward. 1994. Review of the status, biology, and alternatives for management of

smallmouth bass in John Day Reservoir. Ore. Dept. Fish and Wildl. Info. Rep. 94–4.

Beamish, R., D. Noakes, G. Mcfarlane, W. Pinnix, R.Sweeting, and J. King. 2000. Trends in coho marine

survival in relation to the regime concept. Fish. Ocean. 9:114–119.

Behnke, R. 1992. Native trout of western North America. Amer. Fish. Soc., Monograph 6. Bethesda, MD,

275 p.

Benfey, T.J., E.M. Donaldson, and T.G. Owen. 1989. An homologous radioimmunoassay for coho salmon

(Oncorhynchus kisutch) vitellogenin, with general applicability to other Pacific salmonids.

Berg, M. 1977. Pink salmon, Oncorhynchus gorbuscha (Walbaum) in Norway. Rep. Instit. Freshwater

Res. 56:12–17.

Bisbal, G.A., and W.E. McConnaha. 1998. Consideration of ocean conditions in the management of salmon.

Can. J. Fish. Aquat. Sci. 55:2178–2186.

Black, E.A., D.J. Gillis, D.E. Hay, C.W. Haegele, and C.D. Levings. 1992. Predation by caged salmon in

British Columbia. Bull. Aquacult. Assoc. Can. 92:58–60.

Blanc, J.M., and B. Chevassus. 1979. Hybridization in salmonids: results and perspectives. Aquaculture

17:113–128.

Blanc, J.M., and B. Chevassus. 1982. Interspecific hybridization of salmonid fish. II. Survival and growth

up to the 4th month after hatching in F1 generation hybrids. Aquaculture 29:383–387.

Brackett, J. 1991. Potential disease interactions of wild and farmed fish. Bull. Aquacult. Assoc. Can.

91–3:79–80.

BCSFA (British Columbia Salmon Farmers Association). 1999. Code of practice. British Columbia

Salmon Farmers Association, 1200 West Pender Street, Vancouver, BC V6E 2S9, 13 p.

Brown, T.L. 1975. The 1973 salmonid run: New York’s Salmon River sport fishery, angler activity, and

economic impact. New York Sea Grant Publication, NYSSGP–RS–75–024, 29 p.
116

Buckley, R.M. 1999. Incidence of cannibalism and intra-genetic predation by chinook salmon (Oncorhynchus

tshawytscha) in Puget Sound, Washington. Washington Department of Fish and Wildlife, Resource

Assessment Division Reptort, RAD 99–04, 22 p.

Busack, C., and A.R. Marshall. 1995. Defining genetic diversity units in Washington salmonids. Washington

Department of Fish and Wildlife, Technical Report, RAD 95–02, 19 p.

Busby, P.J., T.C. Wainwright, G.J. Bryant, L.J. Lierheimer, R.S. Waples, F.W. Waknitz, and I.V. Lagomarsino.

(1996). Status review of west coast steelhead from Washington, Idaho, Oregon and California.

NOAA Tech. Memo. NMFS–NWFSC–27, 261 p.

Carl, G.C., W.A. Clemens, and C.C. Lindsey. 1959. The freshwater fishes of British Columbia. British

Columbia Province Museum Handbook 5, 192 p.

Carrel, C. 1998. Killer salmon. Seattle Weekly, Sept. 17–23, 1998.

Campton, D.E., and J.M. Johnston. 1985. Electrophoretic evidence for a genetic admixture of native and

nonnative rainbow trout in the Yakima River, Washington. Trans. Am. Fish. Soc. 114:782–793.

CFR (Code of Federal Regulations). No date. Title 50 Regulations. Internet document

http://www.access.gpo.gov/su_docs.

Chilcote, M.W. 1997. Conservation status of steelhead in Oregon. Draft report, August 1997, Oregon

Department of Fish and Wildlife, Portland, OR, 109 p.

Coleman, P., and T. Rasch. 1981. A detailed listing of the liberations of salmon into the open waters of the

State of Washington during 1980. Washington Department of Fisheries, Progress Report 132, 360 p.

Cooney, R.T., R.D. Brodeur. 1998. Carrying capacity and North Pacific salmon production: stockenhancement implications. Bull. Mar, Sci, 62:443–464.

Daily, K., T. Shrader, R. Temple, and B. Hooton. 1999. Introduced fishes management strategies. Oregon

Department of Fish and Wildlife. Internet document

http://www.dfw.state.or.us/ODFWhtml/publicreview.pdf.

Dill, W.A., and A.J. Cordone. 1997. History and status of introduced fishes in California, 1871–1996. Calif.

Dep. Fish Game Fish Bull. 178, 411 p.

Dymond, J.R. 1932. The trout and other game fishes of British Columbia. Biological Board of Canada,

Ottawa, 51 p.

EAO (Environmental Assessment Office, Canada BC). 1997. British Columbia salmon aquaculture

review. Environmental Assessment Office, Government of British Columbia, 836 Yates Street,

Victoria, BC V8V 1X4.

Einum, S., and I.A. Fleming. 1997. Genetic divergence and interactions in the wild among native, farmed

and hybrid Atlantic salmon. J. Fish Biol. 50(3):634–651.

Ellis, D. 1996. Net Loss. The salmon netcage industry in British Columbia. Report to the David Suzuki

Foundation, Suite 219, 2211 West Fourth Avenue, Vancouver, BC V6K 4S2, 196 p.

Emery, L. 1985. Review of fish species introduced in the Great Lakes, 1819–1974. Great Lakes Fisheries

Commission Technical Report 45, 16 p.

Foerster, R.E. 1935. Interspecific cross-breeding of Pacific salmon. Trans. Royal Soc. Can. Series 3, 29,

Section 5:21–33.
117

Foott, J.S., and R.L. Walker. 1992. Disease survey of Trinity River salmonid smolt populations. Report

by the US Fish and Wildlife Service to the California-Nevada Fish Health Center, Anderson, CA,

40 p.

FPC (Fish Passage Center). 1999. Current and historic mark release information, 1985–present. Fish Passage

Center, Portland, OR. Internet document http://www.fpc.org/Hatchery/MarkRel.htm.

Flagg, T.A., F.W. Waknitz, D.J. Maynard, G.B. Milner, and C.V.W. Mahnken. 1995. The effect of hatcheries

on native coho salmon populations in the Lower Columbia River. Amer. Fish. Soc. Symp.

15:366–375.

Freymond, B., and S. Foley. 1985. Wild steelhead: spawning escapement estimates for Boldt Case area rivers.

Washington Department of Game, Project AFS 127–1, 204 p.

Galbreath, P.F., and G.H. Thorgaard. 1995. Sexual maturation and fertility of diploid and triploid Atlantic

salmon x brown trout hybrids. Aquaculture 137:299–311.

Gibson, R.J. 1981. Behavioral interactions between coho salmon, Atlantic salmon, brook trout and steelhead

trout at the juvenile fluvial stages. Can. Tech. Rept. Fish. Aquat. Sci. 1029.

Gilbertsen, N. 1997. Letter to Senator Ted Stevens, US Senator, Alaska, April 25, 1997.

Gray A.K., M.A. Evans, and G.H. Thorgaard. 1993. Viability and development of diploid and triploid

salmonid hybrids. Aquaculture 122:125–142.

Griffiths, R.H. 1983. Stocking practices and disease control, p 87–88. In F.P. Meyer and J.W. Warren (eds.),

A Guide to Integrated Fish Health Management in the Great Lakes Basin. Great Lakes Fisheries

Commission Special Publication 83–2.

Gross, M. 1997. Testimony before the Pollution Control Hearing Board of Washington, Dec. 16, 1997,

MEC/WEC v. Ecology, PCHB Nos. 96–257 through 96–266 and 97–110.

Gross, M. 1998. One species with two biologies: Atlantic salmon (Salmo salar) in the wild and in

aquaculture. Can. J. Fish. Aquat. Sci. 55(suppl 1):131–144.

Gustafson, R.G., T.C. Wainwright, R.G. Kope, K.Neely, F.W. Waknitz, L.T. Parker, and R.S. Waples. Status

review of sockeye salmon in Washington and Oregon. NOAA Tech. Memo. NMFS–NWFSC–33,

282 p.

Hard, J.J., R.P. Jones, Jr., M.R. Delarm, and R.S. Waples. 1992. Pacific salmon and artificial propagation

under the Endangered Species Act. NOAA Tech. Memo. NMFS–NWFSC–2, 56 p.

Hard, J.J., R.G. Kope, W.S. Grant, F.W. Waknitz, L.T. Parker, and R.S. Waples. 1996. Status review of pink

salmon from Washington, Oregon and California. NOAA Tech. Memo. NMFS–NWFSC–25, 131 p.

Harrell, L.W., R.A. Elston, T.M. Scott, and M.T. Wilkinson. 1986. A significant new systemic disease of

net-pen reared chinook salmon (Oncorhynchus tshawytscha) brood stock. Aquaculture

55:249–262.

Harrell, L.W., T.A. Flagg, T.M. Scott, and W.F. Waknitz. 1985. Snake River fall chinook salmon broodstock program. Annual Report, 1984. Coastal Zone and Estuarine Studies Division, NWAFC,

NMFS, Seattle, WA.

Harrell, L.W., C.V.W. Mahnken, T.A. Flagg, E.F. Prentice, W.F. Waknitz, J.L. Mighell, and A.J. Novotny.

1984. Status of the NMFS/USFWS Atlantic salmon brood-stock program (summer 1984).

Coastal Zone and Estuarine Studies Division, NWAFC, NMFS, Seattle, WA.
118

Hart, J.L. 1973. Pacific fishes of Canada. Fish. Res. Board Can. Bull. 180, 740 p.

Heard, W.R. 1998. Do hatchery salmon affect the North Pacific Ocean ecosystem? North Pacific

Anadromous Fisheries Commission Bulletin 1:405–411.

Hearn, W.E., and B.E. Kynard. 1986. Habitat utilization and behavioral interaction of juvenile Atlantic salmon

(Salmo salar) and rainbow trout (S. gairndneri) in tributaries of the White River of Vermont. Can. J.

Fish. Aquat .Sci. 43:1988–1998.

Heggberget, T.G., F. Oekland, and O. Ugedal. 1993. Distribution and migratory behavior of wild and

farmed Atlantic salmon (Salmo salar) during return migration. Aquaculture 118:73–83.

Hindar, K., A. Ferguson, A. Youngson, and R. Poole. 1998. Hybridization between escaped farmed

Atlantic salmon and brown trout: frequency, distribution, behavioural mechanisms, and effects on

fitness, p.134–137. In K.G. Barthel, H. Barth, M. Bohle-Carbonell, C. Fragakis, E. Lipiatou, P.

Martin, G. Ollier, and M. Weydent (eds.), Third European Marine Science and Technology

Conference. Lisbon 23–27 May 1998. Project Synopses Vol. 5, Fisheries and Aquaculture.

Howell, P., K. Jones, D. Scarnecchia, L. LaVoy, W. Kendra, and D. Ortmann. 1985. Stock assessment of

Columbia River anadromous salmonids. II, Steelhead stock summaries, stock transfer guidelines –

information needs. US Department of Energy, Bonneville Power Administration, Project No. 83–335,

1032 p.

Idyll, C. 1942. Food of rainbow, cutthroat, and brown trout in the Cowichan River system, BC. J. Fish.

Res. Board Can. 5:448–458.

Intrafish. 2000. Salmon farming and the environment: of drugs and chemicals. Industry Report No. 2/00.

Internet document http://www.intrafishservices.com.

Johnsen, B.O., and A.J. Jensen. 1986. Infestations of Atlantic salmon, Salmo salar, by Gyrodactylus

salaris in Norwegian rivers. J. Fish Biol. 29:233–241.

Johnsen, B.O., and A.J. Jensen. 1988. Introduction and establishment of Gyrodactylus salaris Malmberg,

1957, on Atlantic salmon. Salmo salar L., fry and parr in the river Vefsna, northern Norway. J.

Fish Dis. 11:35–45.

Johnson, O.W., W.S. Grant, R.G. Kope, K. Neely, F.W. Waknitz, and R.S. Waples. 1997. Status review of

chum salmon from Washington, Oregon and California. NOAA Tech. Memo. NMFS–NWFSC–32,

280 p.

Johnson, O.W., M.H. Ruckelshaus, W.S. Grant, F.W. Waknitz, A.M. Garrett, G.J. Bryant, K. Neely, J.J. Hard,

and R.S. Waples. 1999. Status review of coastal cutthroat trout from Washington, Oregon and

California. NOAA Tech. Memo. NMFS–NWFSC–37, 292 p.

Jones, M.L., and L.W. Stanfield. 1993. Effects of exotic juveniles salmonines on growth and survival of

juvenile Atlantic salmon (Salmo salar) in a Lake Ontario tributary, p71–79. In J. Gibson and R.E.

Cutting (eds.), Production of Juvenile Atlantic salmon, Salmo salar, in Natural Waters. Can. Spec.

Publ. Fish. Aquat. Sci. 118.

Jordan, W.C., and E. Verspoor. 1993. Incidence of natural hybrids between Atlantic salmon, Salmo salar

L. and brown trout, Salmo trutta L, in Britain. Aquacult. Fish. Manag. 24:373–377.

Kent, M.L., and T.T. Poppe. 1998. Diseases of seawater net-pen-reared salmonid fishes. Pacific

Biological Station, Dept. Fish and Oceans, Nanaimo, BC, 138 p.
119

Kostow, K. 1995. Biennial report on the status of wild fish in Oregon. Oregon Department of Fish and

Wildlife, Salem, OR, 217 p.

Leary, R.F., F.W. Allendorf, and G.K. Sage. 1995. Hybridization and introgression between introduced and

native fish. Amer. Fish. Soc. Symp. 15:91–101.

Lever, C. 1996. Naturalized fishes of the world. Academic Press, New York, 408 p.

Leider, S., J. Loch, and P. Hulett. 1987. Studies of hatchery and wild steelhead in the Lower Columbia

Region. Washington Department of Fish and Wildlife, Fisheries Management Division Progress

Report. 87–8, 130 p.

Leitritz, E., and R.C. Lewis. 1980. Trout and salmon culture hatchery methods. Cal. Fish Bull. 164.

Univ. California Division of Agriculture and Natural Resources, Oakland, CA, 197 p.

Loginova, G.A., and S.V. Krasnoperova. 1982. An attempt at crossbreeding Atlantic salmon and pink salmon

(preliminary report). Aquaculture 27:329–337.

MacCrimmon, H.R. 1971. World distribution of the rainbow trout (Salmo gairdneri). J. Fish. Res. Board

Can. 28:663–704.

MacCrimmon, H.R., and S. Campbell. 1969. World distribution of the brook trout (Salvelinus fontinalis).

J. Fish. Res. Board Can. 26:1699–1725.

MacCrimmon, H.R., and B.L. Gots. 1979. World distribution of Atlantic salmon, Salmo salar. J. Fish. Res.

Board Can. 36:423–457.

Mahnken, C.V.W., G. T. Ruggerone, F.W. Waknitz, and T. Flagg. 1998. A historical perspective on salmonid

production from Pacific rim hatcheries. North Pacific Anadromous Fisheries Commission Bulletin

1:38–53.

Marshall, A. 1997. Genetic analysis of Abernathy Creek juvenile chinook, investigation of natural

reproduction by Rogue River stock hatchery-origin chinook. Washington Department of Fish and

Wildlife, Fish Management Division Progress Report, 8 p.

Marshall, A.R., C. Smith, R. Brix, W. Dammers, J. Hymer, and L. LaVoy. 1995. Genetic diversity units and

major ancestral lineages for chinook salmon in Washington, p C1–C55. In C. Busack and J. B.

Shaklee (eds.), Genetic Diversity Units and Major Ancestral Lineages of Salmonid Fishes in

Washington. Washington Department of Fisheries Management Program, Resource Assessment

Division Technical Report, No. RAD 95–02.

McDaniel, T.R., K.M. Pratt, T.R. Meyers, T.D. Ellison, J.E. Follet, and J.A. Burke. 1994. Alaska sockeye

salmon culture manual. Special Fisheries Report No. 6, Alaska Department of Fish and Game,

Juneau, AK, 39 p.

McGowan, C.,and W.S. Davidson. 1992. Unidirectional natural hybridization between brown trout (Salmo

trutta) and Atlantic salmon (S. salar) in Newfoundland. Can. J. Fish. Aquat. Sci. 49(9):1953–

1958.

McKay, S., R.H. Devlin, and M.J. Smith. 1996. Phylogeny of Pacific salmon and trout based on growth

hormone type-2 and mitochondrial NADH dehydrogenase subunit 3 DNA sequences. Can. J. Fish

Aquat. Sci. 53:1165–1176.

McNair, M. 1997. Alaska salmon enhancement program 1996: annual report. Regional Information Report

5J97–09, Alaska Department of Fish and Game, Juneau, AK, 48 p.
120

McNair, M. 1998. Alaska salmon enhancement program 1997: annual report. Regional Information Report

5J98–03, Alaska Department of Fish and Game, Juneau, AK, 36 p.

McNair, M. 1999. Alaska salmon enhancement program 1998: annual report. Regional Information Report

5J99–02, Alaska Department of Fish and Game, Juneau, AK, 35 p.

McNair, M. 2001. Alaska salmon enhancement program 2000: annual report. Regional Information Report

5J01–01, Alaska Department of Fish and Game, Juneau, AK, 35 p.

Michak, P, and B. Rogers. 1989. Augmented fish health monitoring: Annual Report of the Bonneville

Power Administration, US Department of Energy, Portland, OR, 172 p.

Michak, P, E. Wood, B. Rogers, and K. Amos. 1990. Augmented fish health monitoring. Annual Report

of the US Department of Energy, 27 p.

Mighell, J.L. 1981. Culture of Atlantic salmon, Salmo salar, in Puget Sound. Mar. Fish. Bull. 43(2):1–8.

Moring, J.R., J. Marancik, and F. Griffiths. 1995. Changes in stocking strategies for Atlantic salmon

restoration and rehabilitation in Maine, 1871–1993. Amer. Fish. Soc. 15:38–46.

Myers, J., R.G. Kope, G.J. Bryant, D.Teel, L.J. Lierheimer, T.C. Wainwright, W.S. Grant, F.W. Waknitz,

K. Neely, S.T. Lindley, and R.S. Waples. 1998. Status review of chinook salmon from

Washington, Idaho, Oregon, and California. US Dep. Commer., NOAA Tech. Memo.

NMFS–NWFSC–35, 443 p.

Neave, F. 1958. The origin and speciation of Oncorhynchus. Trans. Royal Soc. Can. LII (III): 25–39.

Nickelson, T.E., M.F. Solazzi, and S.L. Johnson. 1986. Use of hatchery coho salmon (Oncorhynchus

kisutch) presmolts to rebuild wild populations in Oregon coastal streams. Can. J. Fish. Aquat. Sci.

43:2443–2449.

NMFS/USFWS (National Marine Fisheries Service)/US Fish and Wildlife Service). 1984. Memorandum

of a meeting at USFWS Regional Office, Newton Corner, MA., 23 March, 1984. Provided by J.

Cookson, NMFS, Woods Hole, MA, 1 p.

Noakes, D.J. 1999. Deposition before the Washington Pollution Control Hearings Board, January 14, 1999,

Olympia, WA.

NRC (Natural Resources Consultants). 1995 and 1996. Artificial propagation of anadromous Pacific

salmonids, 1950 to present. Contract reports to the US Department of Commerce, NOAA, NMFS.

Including electronic databases.

NRC (Natural Resources Consultants). 1997. Straying of coho salmon from hatcheries and net-pens to streams

in Hood Canal and Grays Harbor, Washington, during 1995. Natural Resources Consultants, Seattle,

WA, 75 p.

NRC (Natural Resources Consultants). 1999. Abundance and stock origin of coho salmon on spawning

grounds of Lower Columbia River tributaries. Prepared for Pacific States Marine Fisheries

Commission, Portland, OR, 54 p.

NWIFC/WDF (Northwest Indian Fisheries Commission/Washington Department of Fisheries). 1991.

Salmonid disease control policy of the fisheries co-managers of Washington State. NWIFC/WDF,

Olympia, WA.
121

NWIFC/WDFW (Northwest Indian Fisheries Commission/Washington Department of Fish and Wildlife)

1998. Salmonid disease control policy of the fisheries co-managers of Washington State.

NWIFC/WDFW, Olympia, WA, 22 p.

ODFW (Oregon Department of Fish and Wildlife). 1982. Comprehensive plan for production and

management of Oregon’s anadromous salmon and trout: II Coho salmon plan considerations. Oregon

Department of Fish and Wildlife, Anadromous Fish Section, Portland, OR.

ODFW.NMFS (Oregon Department of Fish and Wildlife/National Marine Fisheries Service). 1998.

Management implications of co-occurring native and introduced species. Proceedings of the

Workshop, October 27–28, Portland, OR.

ODIN (Official Documentation and Information from Norway). 2001. Research knowhow in Norway:

priority areas – marine research. Internet document http://odin.dep.no/kuf/engelsk/pub...081–

120043/index-hov001-b-f-a.html.

PCHB (Pollution Control Hearing Board of Washington). 1997. First Order on Summary Judgement,

PCHB No. 96–257 et seq., NPDES Permit Appeals, May 29, 1997, 22 p.

PCHB (Pollution Control Hearing Board of Washington). 1998. Final Findings of Fact, Conclusions of

Law and Order, PCHB No. 96–257 et seq., NPDES Permit Appeals, November 30, 1998, 46 p.

Phelps, S.R., S.A. Leider, P.L. Hulett, B.M. Baker, and T.Johnson. 1997. Genetic analysis of Washington

steelhead: preliminary report incorporating 36 new collections from 1995 and 1996. Washington

Department of Fish and Wildlife, Fish Management Division Progress Report, 29 p.

Phelps, S., J. Uehara, D. Hendrick, J. Hymer, A. Blakley, and R. Brix. 1995. Genetic diversity units and major

ancestral lineages for chum salmon in Washington, p. C1–C55. In C. Busack and J.B. Shaklee (eds.),

Genetic Diversity Units and Major Ancestral Lineages of Salmonid Fishes in Washington.

Washington Department of Fish and Wildlife, Fish Management Program, Resource Assessment

Division Technical Report No. RAD 95–02.

PNWFHPC (Pacific Northwest Fish Health Protection Committee). 1988a. Report on current disease

status and historical occurrence of important disease problems from hatcheries operated by tribes

that make up the Northwest Indian Fisheries Commission. Olympia, WA, 18 p.

PNWFHPC (Pacific Northwest Fish Health Protection Committee). 1988b. Report on current disease

status and historical occurrence of important disease problems in US Fish and Wildlife Service

hatcheries. Olympia, WA, 16 p.

PNWFHPC (Pacific Northwest Fish Health Protection Committee). 1988c. Report on current disease

status and historical occurrence of important disease problems in Washington Department of

Wildlife hatcheries. Olympia, WA, 21 p.

PNWFHPC (Pacific Northwest Fish Health Protection Committee). 1988d. Report on current disease

status and historical occurrence of important disease problems in Washington Department of

Fisheries hatcheries. Olympia, WA, 17 p.

PNWFHPC (Pacific Northwest Fish Health Protection Committee). 1993. Fish health status reports 1988–

1992. Pacific Northwest Fish Health Protection Committee Meeting at Twin Falls, ID, September

28–29, 1993.

PNWFHPC (Pacific Northwest Fish Health Protection Committee). 1998. Fish health status reports 1998.

Pacific Northwest Fish Health Protection Committee Meeting at Las Vegas, NV, February 18–19

1998.
122

PSGA (Puget Sound Gillnetters Association). 2000. Warning – wear gloves to handle Atlantic salmon.

Internet document http://www.nwefish.com/.

Quinn, T. 1997. Testimony before the Pollution Control Hearing Board of Washington, Dec. 16, 1997,

MEC/WEC v. Ecology, PCHB Nos. 96–257 through 96–266 and 97–110.

Refstie, T. and T. Gjedrem. 1975. Hybrids between salmonidae species. Hatchability and growth rate in

the freshwater period. Aquaculture 6:333–342.

Rosenfield, J.A. 1998. Detection of natural hybridization between pink salmon (Oncorhynchus gorbuscha)

and chinook salmon (Oncorhynchus tshawytscha) in the Laurentian Great Lakes using meristic,

morphological, and color evidence. Copeia 3:706–714.

Sauter, R.W, C. Williams, E.A. Meyer, B. Celnik, J.L. Banks, and D.A. Leith. 1987. A study of bacteria

present within unfertilized salmon eggs at the time of spawning and their possible relation to early

lifestage disease. J. Fish Dis. 10 (3):193–203.

Schnick, R. A. 1992. Registration status report for fishery compounds. Fisheries 17(6):12–13.

Seeb, J.E., G.H. Thorgaard, and F.M. Utter. 1988. Survival and allozyme expression in diploid and

triploid hybrids between chum, chinook, and coho salmon. Aquaculture, 72:31–48.

Seiler, D., P. Hannraty, S. Neuheisher, P. Topping, M. Ackley, and L. Kishamoto. 1995. Wild salmon

production and survival evaluation, Oct. 1993–Sept. 1994. Annual Performance Report, Washington

Department of Fish and Wildlife, Olympia, WA.

Simon, R.C. 1963. Chromosome morphology and species evolution in the five North American species of

Pacific salmon. J. Morphol. 112:77–97.

Sutterlin, A.M., L.R. MacFarlane, and P. Harmon. 1977. Growth and salinity tolerance in hybrids within

Salmo sp. and Salvelinus sp. Aquaculture 12:41–52.

Suzuki, R. and Y. Fukuda. 1971. Survival potential of F1 hybrids among salmonid fishes. Bull.

Freshwater Fish. Res. Lab. (Tokyo) 21(1)69–83.

Thomson, A.J.L., and J.R. Candy. 1998. Summary of reported Atlantic salmon (Salmo salar) catches and

sightings in British Columbia and adjacent waters in 1997. Can Man. Rept. Fish. Aquat. Sci. 2467, 39 p.

Thomson, A.J.L., and S. McKinnell. 1993. Summary of reported Atlantic salmon (Salmo salar) catches and

sightings in British Columbia and adjacent waters in 1992. Can Man. Rept. Fish. Aquat. Sci. 2215, 15 p.

Thomson, A.J.L., and S. McKinnell. 1994. Summary of reported Atlantic salmon (Salmo salar) catches and

sightings in British Columbia and adjacent waters in 1993. Can Man. Rept. Fish. Aquat. Sci. 2246, 35 p.

Thomson, A.J.L., and S. McKinnell. 1995. Summary of reported Atlantic salmon (Salmo salar) catches and

sightings in British Columbia and adjacent waters in 1994. Can Man. Rept. Fish. Aquat. Sci. 2304, 33 p.

Thomson, A.J.L., and S. McKinnell. 1996. Summary of reported Atlantic salmon (Salmo salar) catches and

sightings in British Columbia and adjacent waters in 1995. Can Man. Rept. Fish. Aquat. Sci. 2357, 29 p.

Thomson, A.J.L., and S. McKinnell. 1997. Summary of reported Atlantic salmon (Salmo salar) catches and

sightings in British Columbia and adjacent waters in 1996. Can Man. Rept. Fish. Aquat. Sci. 2407, 37 p.

Tynan, T. 1981. Squaxin seafarm coho outmigration stomach content analysis. Squaxin Tribal Fisheries

Technical Report, Squaxin Island Tribe, Olympia, WA, 7 p.
123

US DOI/DOC (US Departments of Interior/Department of Commerce). 1995. Draft status review for

anadromous Atlantic salmon in the United States. US Department of the Interior, Washington DC

and the US Department of Commerce, Silver Spring, MD, 131 p.

USFWS (US Fish and Wildlife Service). 1984. Fish health protection policy (Title 50), US Fish and

Wildlife Service, Department of Interior, Washington DC.

Verspoor, E. 1988. Reduced genetic variability in first generation hatchery populations of Atlantic salmon

(Salmo salar). Can. J. Fish Aquat. Sci. 45:1686–1690.

Verspoor, E., and J. Hammar. 1991. Introgressive hybridization in fishes: the biochemical evidence. J.

Fish Biol. 39(A):309–334.

Volpe, J.P., E.B.Taylor, D.W. Rimmer, and B.W. Glickman. 2000. Evidence of natural reproduction of

aquaculture-escaped Atlantic salmon in a coastal British Columbia river. Conserv. Biol.14:899–903.

Waknitz, F. W. 1981. Broodstock programs at Manchester Fisheries Laboratory, p.31–33. In T. Nosho (ed.),

Salmonid Broodstock Maturation. Washington Sea Grant Publication WSG–WO 80–1.

Waples, R.S. 1991. Pacific salmon, Oncorhynchus spp., and the definition of "species" under the Endangered

Species Act. Mar. Fish. Rev. 53(3):11–22.

WDOE (Washington Department of Ecology). 1986. Recommended interim guidelines for the

management of salmon net-pen culture in Puget Sound. Department of Ecology, Olympia, WA.

WDF (Washington Department of Fisheries). 1950. Annual Report for 1949. Seattle, WA.

WDF (Washington Department of Fisheries). 1953. Annual Report for 1951. Seattle, WA.

WDF (Washington Department of Fisheries). 1954. Annual Report for 1953. Seattle, WA.

WDF (Washington Department of Fisheries). 1990. Final programmatic environmental impact statement

for fish culture in floating net-pens. Washington Department of Fisheries, Olympia, WA, 161 p.

WDFW (Washington Department of Fish and Wildlife). 1993. Atlantic salmon: a fish management

perspective. Internet document www:wa.gov/wdfw/fish/atlantic/toc.htm.

WDFW (Washington Department of Fish and Wildlife). 1996. Fish health manual. Fish Health Division,

Washington Department of Fish and Wildlife, Olympia, WA, 69 p.

WDFW (Washington Department of Fish and Wildlife). 1997c. Escaped Atlantic salmon provide fishing

opportunity. WDFW News Release, July 21, 1997. Internet document

http://www:wa.gov/wdfw/do/jul97/atlantic.htm.

WDFW (Washington Department of Fish and Wildlife). 1999. Atlantic salmon escape. WDFW News

Release, June 15, 1999. Internet document www:wa.gov/wdfw/do/jun99/jun1599a.htm.

WDFW (Washington State Department of Fish and Wildlife). 2000. WDFW Hatcheries program:

statistics. Internet document http://www.wa.gov.wdfw/hat/hat-stat.htm.

WDFW (Washington Department of Fish and Wildlife). 2001. Fishing and shell-fishing rules. Internet

document www:wa.gov/wdfw/fish/regs/fishregs.htm.
124

WDF/WDW/WWTIT (Washington Department of Fisheries/Washington Department of Wildlife/Western

Washington Treaty Indian Tribes). 1993. Washington State salmon and steelhead stock

inventory, 1992. Washington Department of Fish and Wildlife 212 p. (Available from

Washington Department of Fish and Wildlife, P.O. Box 43151, Olympia, WA 98504).

Weitkamp, L., T.C. Wainwright, G.J. Bryant, G.B. Milner, D.J. Teel, R.G. Kope, and R.S. Waples. 1995.

Status review of coho salmon from Washington, Oregon, and California. NOAA Tech. Memo.

NMFS–NWFSC–24, 258 p.

Weston, D.P. 1986. The environmental effects of floating mariculture in Puget Sound. Univ. Washington

School of Oceanography Report 87(16), 148 p.

Weston, D.P. 1996. Environmental considerations in the use of antibacterial drugs in aquaculture. In D.P.

Baird, M. Beveridge, L. Kelly, and J. Muir (eds.), Aquaculture and Water Resource Management.

Blackwell Science Publications, Oxford.

Weston, D.P., D.G. Capone, R.P. Herwig, and J.T. Staley. 1994. The environmental fate and effects of

aquacultural antibacterials in Puget Sound. NOAA Grant Publication

No. NA26FD0109–01, 19 p.

Wightman, J.C., B.R. Ward, R.A. Ptolemy, and F.N. Axford. 1998. A recovery plan for east coast

Vancouver Island steelhead trout. Ministry of Environment, Lands and Parks, Nanaimo, BC., 132 p.

Wilkins, N.P., H.P. Courtney, and A. Curatolo. 1993. Recombinant genotypes in back-crosses of male

Atlantic salmon x brown trout hybrids to female Atlantic salmon. J. Fish Biol. 43(3):393–399.

Wood, J.W. 1979. Diseases of Pacific salmon, their prevention and treatment (Third edition). Washington

Department of Fisheries, Hatchery Division Report, Olympia, 82 p.

Wydoski, R.S., and R.R. Whitney. 1979. Inland fishes of Washington. Univ. Washington Press, Seattle, WA,

220 p.

Youngson, A.F., J.H. Webb, C.E. Thompson, and D. Knox. 1993. Spawning of escaped farmed Atlantic

salmon (Salmo salar): hybridization of females with brown trout (Salmo trutta). Can. J. Fish.

Aquat. Sci. 50(9):1986–1990.

Post Script

EAO (Environmental Assessment Office, Canada BC). 1997. British Columbia salmon aquaculture

review. Environmental Assessment Office, Government of British Columbia, 836 Yates Street,

Victoria, BC V8V 1X4.

Parametrix. 1990. Final programmatic environmental impact statement fish culture in floating net-pens.

Prepared by Parametrix Inc., for Washington State Department of Fisheries, 115 General

Administration Building, Olympia, WA 98504, 161 p.

PCHB (Pollution Control Hearing Board of Washington). 1997. First Order on Summary Judgement,

PCHB No. 96–257 et seq., NPDES Permit Appeals, May 29, 1997, 22 p.

PCHB (Pollution Control Hearing Board of Washington). 1998. Final Findings of Fact, Conclusions of

Law and Order, PCHB No. 96–257 et seq., NPDES Permit Appeals, November 30, 1998, 46 p.

Weston, D.P. 1986. The environmental effects of floating mariculture in Puget Sound. Univ. Washington

School of Oceanography Report 87(16), 148 p.
125

Winsby, M., B. Sander, D. Archibald, M. Daykin, P. Nix, F.J.R. Taylor, and D. Munday. 1996. The

environmental effects of salmon netcage culture in British Columbia. Prepared for the Ministry of

Environment, Lands and Parks, Environmental Protection Department, Industrial

Waste/Hazardous Contaminants Branch, 1106–1175 Douglas Street, Victoria, BC, 214 p.