Diminishing Returns:

Salmon Decline andPesticides

A publication of theOregon Pesticide Education Network (OPEN)■ Oregon Environmental Council■ Northwest Coalition for Alternatives to Pesticides■ OSPIRG Foundation■ Institute for Fisheries Resources

We gratefully acknowledge the support of:■ The Pew Charitable Trusts■ The Bullitt Foundation■ Turner Foundation■ The Tides Center■ Rockefeller Family Fund
■ True North Foundation■ The Educational Foundation of America
as well as numerous individuals who have supported the work of theOregon Pesticide Education Network.

We sincerely appreciate the special contributions that the following individuals made to this report:
Jeff Allen, Lev Anderson, Robie Honeyman-Colvin, Caroline Cox, Georgia Ewing, Lita Furby, Norma
Grier, Neva Hassanein, Jacob Kann, Maureen Kirk, Becky Long, Kay Rumsey, Glen Spain, and Laura
Weiss.
We also value the following individuals and agencies who contributed photos and graphics that are
reproduced here with permission: Nancy Allen of Corvallis Environmental Center, K. Born, Andy
Duncan and Lynn Ketchum of OSU Extension and Experiment Station Communications, Institute forFisheries Resources, Kathryn Kostow, Tom and Pat Leeson, Oregon Dept. of Environmental Quality,
Oregon Dept. of Fish and Wildlife, Public Interest GRFX, Oregon Sea Grant, Ana Soto, Steve Stoneof National Marine Fisheries Service, and the US Fish and Wildlife Service.
The opinions expressed in this report do not necessarily reflect the views of the supporting
foundations and individuals.

Copies of this report can be found at:
http://www.pond.net/~fish1ifr/salpest.pdf

Diminishing Returns: Salmon Decline and Pesticides

Diminishing Returns:
Salmon Decline and Pesticides

TOM AND PAT LEESON

By Richard D. Ewing, PhD
February 1999

About the Author:
Richard D. Ewing is a native Oregonian who graduated from Reed College in 1962, andreceived his Ph.D. in cellular and molecular biology from the University of Miami at Coral
Gables in 1968. After conducting research at Oak Ridge National Laboratory and at Oregon
State University, Dr. Ewing joined the research team at the Oregon Department of Fish andWildlife where he worked as a physiologist and hatchery specialist from 1975-1992. He left
ODFW to form Biotech Research and Consulting, Inc., a Corvallis-based consulting company
that specializes in hatchery operations and chemical analyses relating to fisheries. Dr. Ewing
has published widely in professsional journals and written many reports for the Oregon Department of Fish and Wildlife.
1Diminishing Returns: Salmon Decline and Pesticides

Table of Contents
Executive Summary.......................................................................................................................... 3
Introduction ....................................................................................................................................... 7
Dynamics of Pesticides in the Environment ............................................................................... 10
Pesticides are Ubiquitous in the Western Watersheds ............................................... 10
Pesticides Persist in the Environment and Degrade into Toxic Products ................ 11
Pesticides Move throughout Watersheds ..................................................................... 12
Pesticide Concentrations Can Become Magnified in Tissues .................................... 14
Fish Kills and Acute Toxicity of Pesticides.................................................................................. 17
Behavioral Effects of Pesticides at Sublethal Concentrations................................................... 19
Pesticides Impair Swimming Performance .................................................................. 19
Pesticides Can Increase Predation on Juvenile Salmonids ........................................ 21
Temperature Selection is Changed by Pesticides ........................................................ 22
Schooling Behavior is Reduced by Pesticides ............................................................. 22
Pesticides Can Interfere with Seaward Migration ...................................................... 23
Pesticides Interfere with Seawater Adaptation ........................................................... 23
Pollutants Affect Adult Returns .................................................................................... 25
Compromised Immune Systems .................................................................................................. 27
Endocrine Disruptors ..................................................................................................................... 29
Pesticides Can Mimic Estrogens .................................................................................... 30
Pesticides May Have Other Endocrine Effects ............................................................ 34
Indirect Effects of Pesticides on Salmon ...................................................................................... 36
Conclusions ..................................................................................................................................... 39
Recommendations .......................................................................................................................... 43
References ........................................................................................................................................ 45
Glossary, Abbreviations and Scientific Names ........................................................................... 522

Diminishing Returns: Salmon Decline and Pesticides

Executive
Summary
Pacific salmon are in serious trouble.
The enormous runs of migratory salmon of
the past have slowly diminished to thetrickle of adult spawning salmon that
presently inhabit western rivers. Althoughsalmon recovery efforts are underway,
scientists, policy makers, and interest
groups have thus far given insufficientattention to the role that pesticide contamination of our watersheds may play in salmon
decline. Accordingly, the purpose of Diminishing Returns: Salmon Decline and Pesticides isto review scientific literature on the effects ofsublethal concentrations of pesticides on
salmonids (see full report for documentation and references). The report places
special emphasis on how pesticides canalter the biology of fishes in subtle waysthat decrease their chances for reproduction
and survival.

Dynamics of Pesticides in theEnvironment
Pesticides include a broad class ofchemical and biological agents that are
purposefully introduced into the environment to kill or damage organisms, including insecticides, herbicides, and fungicides. Once applied, pesticides move into
streams and rivers throughout watersheds and may pose problems far fromthe site of application. Movement often
occurs through the medium of water,
thereby exposing all aquatic organisms
during this transport. Where water quality monitoring has been done, a great
variety of pesticides are typically found insalmon habitat. Federal and state agencies have established few criteria or stan-dards for the protection of aquatic life
from short-term (acute) and long-term(chronic) exposure to pesticides.
Pesticides do not necessarily disappear
with time. They transform into other compounds that may be less toxic, of equal
toxicity, or of greater toxicity than theoriginal compound. The toxicity of thesebreakdown products is not well understood, and in general how they affectaquatic life has not been studied. All thewhile, fish and other aquatic organisms
must continue to cope daily with pesticides(and their breakdown products), some ofwhich are no longer used but remain inwatersheds.
Although pesticides are diluted bytransport in rivers and streams, a numberof mechanisms concentrate the chemicals,
often to toxic levels. In a process known
as bioaccumulation, pesticides absorbed
into plant and animal tissues may become
concentrated and reach levels manytimes higher than those in surrounding
water.
3

Diminishing Returns: Salmon Decline and Pesticides

salmonids and thereby render them more
susceptible to predation.

Fish Kills and Acute Toxicity ofPesticides to Salmon
Pesticides are capable of killing salmon
and other aquatic life directly and within ashort period of time. For example, in 1996
the herbicide acrolein was responsible forthe death of approximately 92,000 steelhead, 114 juvenile coho salmon, 19 resident
rainbow trout, and thousands of nongame
fish in Bear Creek, a tributary of the Rogue
River. Deaths of threatened and endangered species from accidental contamination of waterways are of grave concern.
The loss of each individual in a sensitive
population makes recovery efforts thatmuch more difficult. Fortunately, these
deaths are relatively infrequent.

Behavioral Effects of Pesticides
at Sublethal Concentrations
In contrast to dramatic fish kills, theeffects of sublethal concentrations of pesticides are more subtle and go largely unseen
and unregulated. Sublethal concentrationsof pesticides do not cause immediate death,but can interfere with the biology of theorganism in other ways and can ultimately
impact the survival of the species. Laboratory studies show that sublethal concentrations of pesticides can affect many aspectsof salmon biology, including a number ofbehavioral effects:• Long-term exposure to certain
pesticides can increase stress in juvenile
4• Certain pesticides can alter swimming ability, which in turn can reduce theability to feed, to avoid predators, to defend
territories, and to maintain position in theriver system.
• Many pesticides interrupt schoolingbehavior, a critical tactic for avoiding predation during salmon migration. Disruption of schooling behavior is thought bysome researchers to be a classic method for
examining sublethal effects of pesticides
because the effect is so common.
• Several pesticides (and other pollutants) have been shown to cause fish to seek
suboptimal water temperatures, thus subjecting them to increased dangers of disease
and predation.
• Some herbicides have been shownto inhibit normal migration to the sea,
resulting in severe disruption of the life
cycle. There is a dearth of research looking
at this effect for common insecticides.
• Several studies suggest that certain
pesticides can impair salmonid’s ability totransition from freshwater to seawater.
There is a need for further research in thisarea, placing particular emphasis on thecritical period of transition that takes placein the estuary.
• Adult salmon adjust their migration
patterns to avoid polluted areas, resulting
in delayed spawning.

Compromised Immune Systems
In addition to changes in behavior,
exposure to relatively low concentrations ofDiminishing Returns: Salmon Decline and Pesticides

pesticides can disrupt the immune systemof salmon. Evidence for these effects insalmonids is not as extensive as for disruption of behavior, but the data available
suggest that pesticides can have serious
negative impacts on the immune system.
Such disruption results in the onset of
disease and even death.

Endocrine Disruptors
Fish and other organisms are especiallyvulnerable to endocrine-disrupting effects
during the early stages of development.
Pesticides at low concentrations may act as
mimics or blockers of sex hormones, causing abnormal sexual development, feminization of males, abnormal sex ratios, andunusual mating behavior. The uniqueplasticity of sex differentiation in fish suggests that these animals may be very susceptible to disruption of sexual characteristics by pollutants. Pesticides can also interfere with other hormonal processes, such as
thyroid functioning and bone development.

Indirect Effects of Pesticides on
SalmonPesticides can indirectly affect fish byinterfering with their food supply or altering the aquatic habitat, even when theconcentrations are too low to affect the fishdirectly. Such indirect effects greatly reduce
the abundance of food organisms which inturn reduces the growth and probability ofsurvival of the fish. In addition, removal of
aquatic vegetation can decrease habitat
suitability and increase the salmon’s sus-

ceptibility to predation. These indirect
effects are subtle, but evidence suggeststhat in complex ecosystems indirect effects
can be even more important than direct
effects.

Recommendations
From the evidence available at present,
there is a plausible basis for considering
pesticides to be one of the causes of declining salmon populations in the PacificNorthwest. Based on this review, we offer
several policy recommendations and identify areas for further research:
1. Address the impacts of pesticides
on salmon when developing and implementing recovery plans for threatened andendangered species. To date, efforts torecover salmon have devoted insufficientattention to pesticides as a contributing
factor in salmon decline. We must act now
using available information to formulate
management strategies that will minimize
the potential danger from sublethal concentrations of pesticides.
2. Conduct ecoepidemiological studies in critical salmonid habitat. Most of
the effects of pesticides referred to in thisreport have been determined in experimental laboratories. In the field, however,environmental conditions are not controlled, and many factors interact to confuse
the determination of direct relationships.
Ecoepidemiological investigations in the
Great Lakes have established the relationship between chlorinated hydrocarbons andthe decrease in lake trout populations. An
ecoepidemiological approach for salmon in
the Pacific Northwest would be particularly
valuable because it is designed to attributecausality to events occurring in real-world
situations.
5Diminishing Returns: Salmon Decline and Pesticides

3. Create comprehensive pesticidetracking systems in the Pacific Northwest.
To better understand the relationship between pesticides and salmon decline, wemust have accurate, site-specific data on thepatterns of pesticide use in the watershedsof the Northwest. State and provincial
governments need to collect data on which
pesticides are used where, when, and inwhat amounts. Such data can then be
combined with watershed-specific information on indicators of salmon health. (Currently, California is the only state withPacific salmon habitat where such information is collected.) Pesticide use information
will also enable efficient instream monitoring for pesticide contamination.

4. Establish instream monitoring
programs in critical salmon habitats. A
systematic monitoring program for pesticides and their breakdown products needs
to be undertaken. Not all pesticides can betested for in all locations, but current testing
is woefully inadequate for understanding
the role of pesticides in salmon decline. In
conjunction with pesticide use data, theseanalyses can be targeted to the compoundsof most concern. Such targeting can greatly
improve the cost-effectiveness of monitoring.
5. Err on the side of caution whensetting water quality standards for pesticides. There are few established criteria forthe protection of aquatic life from pesticides. Moreover, evidence reviewed here

6shows that sublethal effects on salmonids
have not been fully appreciated, that juvenile salmonids succumb more easily totoxins in the water, that laboratory studies
do not reflect the natural life cycle of thefish, and that little is known about how
pesticides affect aquatic ecosystems. These
factors must be considered when setting
standards, and a precautionary approach
must be adopted.
6. Prevent pesticide contamination of
salmonid habitat by reducing pesticideuse. Once contaminated, water is difficult
if not impossible to clean up. Therefore,
pest management approaches that do notdepend on pesticide use in agricultural andnon-agricultural settings should be encouraged and further developed. There is
ample evidence that ecologically sound andeconomically viable methods can be successfully implemented. The adoption ofsuch alternatives can be encouraged
through technical assistance, financial
incentives and disincentives, demonstration
programs, and information exchange opportunities.
7. Adopt state and provincial programs in the Pacific Northwest to phaseout pesticides that persist andbioaccumulate in the environment. Numerous pesticides, including some that are
no longer used and many that are currently
used, are known to persist in the environment and to bioaccumulate in aquatic
systems. Washington State’s Department of
Ecology is now considering a plan to end
the release of such toxins, including certain
pesticides, into the environment. To ensuresalmon recovery, all state and provincial
governments in the Pacific Northwest
should adopt similar programs.

Diminishing Returns: Salmon Decline and Pesticides

Introduction

in subtle ways that decrease their chances
for survival and reproduction.

A great deal of work is being done tocatalog and restore the physical aspects ofNorthwest streams (e.g., restoring riparianvegetation and gravel beds, planting buffer
strips along streams). Insufficient attention,
however, has been devoted to the use andpresence of pesticides in the watersheds andthe role this water quality degradation plays
in salmon decline. Accordingly, the purposeof this report is to present information fromscientific literature
Salmon andthat points to thetrout make up theunseen danger
family Salmonidae, aRivers and streams have become great
posed by thegroup of fish characconduits through which pesticides,
existence of pestiterized by an adieither intact or as breakdown products,
cides in salmonidpose fin located nearflow to the sea. Salmon now live
habitats.
the tail. These fish
throughout
their
life
cycle
with
these
require clean, cold
Pesticides
residues as part of their daily
fresh water for muchinclude a broadof their life history.
environment.
class of chemical
Because such habitatand biologicalis low in nutrients,
agents that aresalmon and many of
purposefully applied to the environment to
the trout developed anadromy, a behavior
kill or damage organisms (National Repattern in which the juveniles migrate tosearch Council 1993). These agents are
the sea. In the sea, the juvenile fish use richused in a wide range of occupations for aocean productivity for feeding and growth,variety of purposes. Foresters use herbithen return to the streams where they werecides to keep broadleaf plants from competborn to lay their eggs.
ing with conifer seedlings, and insecticides
to deal with numerous insect pests that
Today, migratory salmon and trout aredamage forests. Farmers use insecticides tofighting for their survival. The enormous
protect their crops and keep insects awayruns of migratory salmonids in the 1860s
from their livestock, and herbicides tohave slowly diminished to the trickle ofremove unwanted weeds from fields andadult spawning salmon that presently
waterways. State and local agencies use
inhabit western rivers. The causes for the
herbicides to remove brush from roadsides.
decline are many, some of which are wellFishermen use defouling compounds likedocumented. Yet, in their recovery efforts
tributyltin to keep organisms from settlingfor threatened populations, scientists,on the hulls of their boats. The ordinary
policy makers, and interest groups havehomeowner uses a wide variety of pestitended to overlook the role of pesticides
cides: herbicides on the lawn, insecticides
that flow daily through salmon habitat,on pets, and fungicides in house paint.
potentially changing the biology of the fish
Salmon are a keystone species forNorthwest ecosystems. Entire foodchainsbase their existence on the proliferation of
salmon and trout that surge from the sea
into streams and rivers, work their way
upstream to their natal spawning areas, lay
their eggs, and die, providing a source ofnutrients for the very organisms that later
feed the salmon’s progeny.

7

Diminishing Returns: Salmon Decline and Pesticides

Oregon’s ocean-going salmon
years before going to the ocean.
• They spawn in the winter and early spring, using small
pockets of gravel. They may spawn more than once. The
spawning age of cutthroats seems to vary over their distribution area.
• Cutthroat prefer the smallest, highest tributaries in a basin.

Chinook Salmon (ocean-rearing)

Chinook (stream-rearing)• In Oregon, they are only in upper Columbia Basin tributaries.
• Juveniles migrate to the ocean as 1-year-olds, in the spring.
• Little is known about the ocean distribution of Oregon’s
stream-rearing chinook.
• Adults return to fresh water in the spring, when 3 to 5 years
old, and require deep, cool pools to hold for several months
over the summer before fall spawning.
• They spawn in concentrations on gravel bars in upper
tributaries.

Chum Salmon• Shortest freshwater residence of all salmon. Adults stay
only about a week prior to spawning; juveniles migrate tothe ocean hours after hatching.
• Juveniles rear briefly in estuaries.
• Most Oregon chums migrate to the Gulf of Alaska for ocean
rearing.
• Adults spawn at 3 to 5 years of age.
• Spawning occurs in lower mainstems, concentrated onlarge gravel bars.
• Adults are unable to pass even minor barriers.

Coastal Cutthroat• Some coastal cutthroats migrate to the ocean. But others
may migrate only to the estuary or river mainstems, or they
may not migrate at all.
• Those that do go to the ocean migrate out in the spring, stay
only a few months close to shore, then return in the fall.
• The ones that migrate may rear in fresh water for several

8

Coho Salmon• Juveniles rear throughout watersheds and tend to live in poolsin the summer.
• Juveniles migrate to the ocean at 1 year, in the spring.
• Most Oregon coho rear just off our coast.
• Adults return to fresh water in the fall and spawn in late fall
and winter.
• Adults tend to spawn in concentrations on gravel bars inupper watersheds.
• Most adults spawn when they are 3 years old.

Sockeye/Kokanee Salmon• There is both an ocean-going form (called sockeye), and aresident form (called kokanee).
• Juveniles rear in a lake, spending 1 to 2 years in fresh
water before migrating to the ocean in the spring.
• Columbia Basin sockeye migrate to the Gulf of Alaska for
ocean rearing.
• Adults typically spend 2 years in the ocean.
• Loss of Oregon sockeye resulted from blocked access tolakes. Kokanee are thriving in some lakes.

Steelhead• There are two subspecies of steelhead in Oregon. Eachalso has a resident form. Coastal steelhead are closely
related to rainbow trout. Inland steelhead are closely
related to redband trout.
• Most juveniles rear in fresh water for 1 or 2 years and migrate
to the ocean in the spring.
• Most steelhead spend 2 years in the ocean. Their
distribution is poorly known but appears to be further offshore than other salmon.
• Most inland steelhead return to fresh water in the summer
while most (but not all) coastal steelhead return in thewinter.
• Summer-run steelhead require cold, deep pools where theyhold until spawning. All steelhead spawn in the winter andmay spawn more than once.

ILLUSTRATION AND INFORMATION COURTESY: KATHRYN KOSTOW, OREGON DEPARTMENT OF FISH AND WILDLIFE• Distribution includes coast and Columbia Basin mainstemrivers.
• Juveniles migrate to the ocean the first fall after they hatch,rearing briefly in estuaries.
• They rear over a broad ocean area, ranging from northern
California to the Gulf of Alaska.
• Adults, typically 3 to 5 years old, return to fresh water in thespring, summer or fall.
• Spring and summer migrants prefer deep, cool pools where
they hold several months before fall spawning.
• Adults spawn in large concentrations on mainstem gravel
bars; may use both upper and lower mainstems.

Diminishing Returns: Salmon Decline and Pesticides

Once applied, pesticides can moveaway from the point where they were used.
As a result, rivers and streams have become
great conduits through which pesticides,
either intact or as breakdown products,
flow to the sea. Salmon now live throughout their life cycle with these residues aspart of their daily environment.
This report reviews our existingscientific knowledge of the effects of pesticides on salmonids, placing a special emphasis on sublethal effects of pesticides.
Sublethal effects are those that result fromexposure to a pesticide in an amount that is
not high enough to cause death, but candamage an organism in other ways, including physiological and behavioral changes
that can ultimately impact the survival of
the species. These effects can occur
throughout the entire life history of salmonids, from hatching of eggs, entry ofjuveniles into the ocean, and return ofadults for spawning. With the data currently available, it is possible to identify key
areas that need immediate attention.
The present report emphasizes research
performed on salmonids. Most of thestudies included here, however, have been
done with rainbow trout, which are foundthroughout the United States, are relatively
easy to grow, and provide a reasonable
standard for examining physiological andbehavioral changes. Fewer studies weredone with anadromous (seagoing) salmon.
Where this research exists, the information
is emphasized. Studies from other speciesof fish are introduced when certain points
need to be made and information is notavailable from salmonid research.
The data suggest there is a plausible
basis for considering pesticides as a
causative factor in salmon population
declines.

9

Diminishing Returns: Salmon Decline and Pesticides

Dynamics ofPesticides in theEnvironment
Pesticides are Ubiquitous in
Western Watersheds
In 1991, the U. S. Congress provided
funds for the U. S. Geological Survey toconduct a National Water-Quality Assessment (NAWQA) on major river systems in
the United States. The study units chosen
encompass sources of drinking water for
about 70 percent of the U. S. population. In
the Northwest, study units included the
Puget Sound and the central ColumbiaRiver plateau of Washington, theWillamette River Basin of Oregon, theSacramento and San Joaquin River systemsof California, and the Snake River Basin of
Idaho. Table 1 presents the numbers ofpesticides detected in streams and thenumbers of pesticide detections that exceed
criteria for aquatic life.
A major problem with the interpretation of the data presented in Table 1 is thatconcentrations of pesticides compatible
with aquatic life are not well defined. The
U.S. Environmental Protection Agency(EPA) has identified aquatic life criteria forthe protection of aquatic organisms fromshort-term (acute) or long-term (chronic)
exposure for very few pesticides. Of the
118 pesticides typically looked for in water
quality studies, only 20 (17%) have been

Table 1. Pesticide detections in the western United States asmeasured by the U. S. Geological Survey NAWQA program.
State, region# Pesticides
Examined# Pesticides
Detected# Exceeding
Aquatic Life
Criteria1# For Which
Aquatic Life
Criteria
Are Available_______________________________________________________________________________________________

OregonWillamette Basin2
86
36
4
22
Washington
Puget Sound Basin3
NA
23
4
NA
Central Columbia
84
45
5
18
River Plateau4
California
San Joaquin Basin5
83
49
7
16
Idaho
Snake River Basin6
80
36
2
17
______________________________________________________________________________________
NA, not available.
1

Aquatic life criteria set by the National Academy of Sciences and National Academy of Engineering or by
the Canadian Council of Resources and Environment Ministers.
2
Data from Anderson et al. (1997).
5
3
Data from Dubrovsky et al. (1998).
Data from Bortleson and Davis (1997).
6
4
Data from Clark et al. (1998).
Data from Wagner et al. (1996).

10

Diminishing Returns: Salmon Decline and Pesticides

assigned aquatic life criteria (Larson et al.
1997). Of the 96 herbicides, 55 insecticides,and 30 fungicides that currently have thehighest agricultural use in the UnitedStates, EPA has established aquatic life
criteria for only 6 insecticides (Larson et al.
1997). EPA has not established any aquatic
life criteria for the herbicides and fungicides most commonly used today.
The National Academy of Sciences(NAS) and National Academy of Engineers(NAE) set aquatic life criteria for a numberof commonly used pesticides in 1973, butthese are outdated. Their derivation was
based on acute toxicity data but did nottake into account bioaccumulation, sublethal effects, or synergistic effects.

Figure 1
Number of pesticides withaquatic life criteria.

Pesticides
with criteria
20
(17%)

Pesticides
without water
quality criteria
98
(83%)

(Based on 118 pesticides typically looked forin water quality studies)
Source: Larson et al. (1997)

The EPA and NAS/NAE criteria arecommonly used as indicators of the degreeof water pollution, but, as we shall see, may
be far higher than the levels at which damage to fish can occur.
From the NAWQA studies, one can seethat pesticide use is prevalent in our watersheds, and the water in our river basinscontains dozens of pesticides. Exactly what
happens to the hundreds of tons of pesticides put on the land each year?

Pesticides Persist in theEnvironment and Degrade into
Toxic Products
Most pesticides undergo chemicaltransformations after application (Day1991). The transformations may result fromeither physical processes, such as oxidationor photolysis, or biological metabolism by
microbes. The breakdown products may
be less toxic, of equal toxicity, or more toxic
than the original compound. In manycases, the breakdown products of pesticides
are not completely understood and their
toxicities to aquatic life have not beenstudied. In surveys of pesticides in streams,
the parent compound is typically lookedfor. When it is not found, it may be concluded that the pesticide has been cleared
from the system. However, the breakdown
products may still be present and constitutea danger to the organisms living there.
For example, Roundup, or glyphosate,has been publicized as an environmentallyfriendly herbicide that breaks down shortly
after application. However, experiments
have shown that glyphosate may persist in
the environment for as long as 3 years(Torstensson et al. 1989). Its metabolite,
AMPA, may persist even longer (World
Health Organization 1994). Glyphosate is
11

Diminishing Returns: Salmon Decline and Pesticides

The rate at which a pesticide breaks
down varies widely, depending upon theconditions of application. Degradation
depends largely upon temperature. Pesticides such as glyphosate may oxidize in as
little as 3 days in Texas or as long as a year
in Canada. Conditions that favor microorganisms also tend to promote pesticidedegradation (Barbash and Resek 1996),
although in some cases, the presence ofPesticides may remain in theenvironment much longer than
expected or claimed, and thebreakdown products may also be
toxic to organisms.

humic material in the soil stabilizes thepesticide (Chapman et al. 1981; Barbash andResek 1996). Light and water are also
important in the degradation of pesticides(Barbash and Resek 1996). Pesticides break
down more quickly under bright sunshine
than under cloud cover. Breakdown occurs
more quickly under moist conditions thanunder dry conditions. Oxygen concentration is also important for metabolism of
pesticides. For example, pesticides areresistant to breakdown in the anoxic, highly
reducing muds of estuaries where there isan absence of oxygen (Barbash and Resek
1996).
In short, the timing of degradation ofa pesticide is highly variable and depen12

dent upon environmental conditions.
Pesticides may remain in the environment
much longer than expected or claimed,
and the breakdown products may also be
toxic to organisms. Fish and aquaticorganisms must cope daily with a varietyof pesticides or metabolites that may havebeen used years before. Many of thepesticides which were banned long ago
still appear in water quality surveys.
One aspect of pesticide degradation isquite clear. Pesticides and their metabolites do not magically disappear from theenvironment.

Pesticides Move throughout
Watersheds
Water promotes the transport of pesticides from their site of application (seeFigure 2). Streams are often the recipients ofpesticide residues following rainfall. But
the rapid downstream transport of chemicals by streams and rivers does not meanthat pesticides have no effects on a varietyof organisms living in the area of application. Pesticides in streams typically reachhigh levels for short periods of time after
application, then decrease to very low orundetectable levels. During the brief period of high concentration, damage to

NEVA HASSANEIN

typical of many pesticides in that its breakdown is dependent upon the environmental
conditions in which it is used and that the
toxicity of its breakdown products is equal
to or greater than the toxicity of glyphosate
itself.

Pesticide residues move readily into streams andrivers following rainfall.

Diminishing Returns: Salmon Decline and Pesticides

Figure 2. Routes through which pesticides move in the water cycle.

organisms in the stream may occur. Fishand wildlife at early stages of development
are particularly vulnerable. Brief exposures
to toxic materials at early stages in development may arrest future development ofcomplete organ systems (Guillette et al.
1995). During early development, thesexual characteristics of the animal areformed, the immune system develops
competence, and a variety of hormones
regulate the formation of bone structure
and organ systems. Disruption of any ofthese complex systems at critical times canlead to permanent impairment.
Pesticides in streams are rapidly diluted by riverflow so that soon after entry
into a stream they can be detected only atvery low levels or no longer be detected atall. While the concentrations in streams
may be relatively harmless during rain andhigh water flow, under certain conditions
pesticides are concentrated rather thandiluted. Depending on the nature of thepesticide, they may attach to sedimentparticles, accumulate in the tissues of various organisms, or become buried in thesediment (Barbash and Resek 1996). Eventually, all probably reach the sea, where
they become a problem of relatively unknown magnitude. If pesticides are appliedin huge amounts each year for dozens ofyears, the dilution effect begins to disappear as the chemical concentrations increasein their particular final resting place. Thus,
spraying of hillsides with a certain pesticide
may not affect the animals in the immediate
vicinity but may have disastrous effects on
13

Diminishing Returns: Salmon Decline and Pesticides

other populations downstream from the siteof application.

mulated in tissues of aquatic organisms,
often becoming magnified thousands oftimes higher in the organism than in the
Most pesticides reach the water boundsurrounding water. Usually
to soil particles (Barbash and Resek 1996).
biomagnification is a function of the fat
Erosion, which in the United States is estisolubility of the pesticide (Norris et al.
mated to transport four billion tons of soil a1991). Biomagnification is thus dependent
year into
upon the metabolic
waterways, is astate of the animajor contribumal, such that
tor of pestifatter animals
Pesticides can be taken up from the water
cides to rivers
tend to accumuand accumulated in tissues of aquatic organand river beds.
late more lipid
isms, often becoming magnified thousands
Thus, poor
soluble pesticides.
of times higher in the organism than in theland-use
This reaches ansurrounding water.
practices not
extreme in the
only contributebuildup of silt
to the spawning areas in streams which
results in suffocation of eggs. Erosion may
also deliver pesticides to the rivers at a time
when the fish, as embryos, are most sensitive to their deleterious effects.

lipid-rich eggs
and embryos.
Eggs of aquatic organisms usually haveenough fats in the form of yolk to meet
early energy requirements during development. Lipid soluble pesticides accumulate
rapidly in these fat deposits and are noteasily removed. There they may competewith hormones provided maternally for use
by the embryos (Bern 1990). The presenceof environmental contaminants in the yolkthat act as endocrine mimics thus may havea powerful influence on embryonicdevelopment.

Pesticide Concentrations Can
Become Magnified in Tissues

CORVALLIS ENVIRONMENTAL CENTER

Under certain circumstances, pesticides
can be taken up from the water and accu-

Erosion, which in the United States is estimated totransport four billion tons of soil a year into
waterways, is a major contributor of pesticides torivers and river beds.

14

Not only are pesticides taken up directly from the environment, fishes can also
absorb them from food organisms. A studyof DDT accumulation in brook trout (Macek
and Korn 1970) found that ten times moreof the available DDT and its metabolites
were absorbed from food than from thewater. This can be magnified still further as
the pesticide travels through food chains.
Metcalf et al. (1971) demonstrated thisbiomagnification effect convincingly withradioactive DDT in a model ecosystem. C14DDT was applied to Sorghum as the source
for the pesticide. The Sorghum was thenDiminishing Returns: Salmon Decline and Pesticides

Table 2. Bioaccumulation of various pesticides, pesticide
additives, and pesticide contaminants in fishes.
____________________________________________________________________
Pesticide
Category
Bioaccumulation Factor
Species
Reference______________________________________________________________________________________
Carbaryl (Sevin)Insecticide30
golden ide
1
Chlordecone
Insecticide
1100-2200
fathead minnow
2
Chlorothalonil
Fungicide840
rainbow trout
3
Chlorpyrifos (Dursban) Insecticide
1374
rainbow trout
4
Cypermethrin
Insecticide
700-1000
rainbow trout
5
DiazinonInsecticide
60
carp
2
Dichlobenil (Casoron)
Herbicide40
golden ide
1
Fenvalerate
Insecticide
40-200salmon6
Flucythrinate
Insecticide
3000-5000
fathead minnow
6
Hexachlorobenzene
Contaminant of chlorothalonil,
5500
rainbow trout
7
picloram, and pentachlorophenol
Nonyl phenol
Surfactant
1300
stickleback
8
Pentachlorophenol
Insecticide251-5370
rainbow trout
2
Permethrin
Insecticide
1700-3300
fathead minnow
6
73
Atlantic salmon
9
Pentachlorophenol
Fungicide100
rainbow trout
10
2,3,7,8-TCCD
Contaminant of Dacthal, and 2,4-D
28,000
rainbow trout
11______________________________________________________________________
1. Freitag et al. 1985.
2. Howard 1991.
3. World Health Organization 1996.
4. Racka 1993.
5. Hill 1985.
6. Smith and Stratton 1986.

introduced into a system with several
components that provided a food web.
Sorghum was eaten by a salt marsh caterpillar. Excreta from the caterpillar was consumed by diatoms, which were subsequently eaten by nine species of plankton.
The plankton was eaten by mosquito larvae
which were subsequently eaten by Gambusia, the mosquito fish. After one month,
54% of the radioactivity was found in thefish, of which most was DDE, a breakdown
product of DDT. The concentration of DDT
was 84,000 times greater in the fish than in
the water, while the concentration of DDE
was 110,000 times greater in the fish than in
the water. Biomagnification of concentra-

7. Veith et al. 1979.
8. Ahei et al. 1993.
9. McLeese et al. 1980.
10. Hattula et al. 1981.
11. Mehrle et al. 1987.

tions of DDT and its metabolites has been
well established (Woodwell et al. 1967;
Risebrough et al. 1967), which was a major
factor leading to its removal from the pesticide market in the United States.
Modern pesticides are usually morewater soluble and do not accumulate inhigh concentrations in fat deposits. However, they do show bioaccumulation (Table2). While these accumulations are not as
dramatic as those of DDT, they show thatthe concentration of pesticide in the water
may not be relevant in determining whether
levels of pesticide will cause biologicaleffects. These accumulations are usually15

Diminishing Returns: Salmon Decline and Pesticides

measured in whole animals. Localized
are subjected. If aquatic life has been exconcentrations of pesticides at the cellular
posed for long periods of time, the concenlevel may be extremely high, but this is antrations within the tissues may be mucharea that has nothigher than that ofbeen widely exthe surrounding
plored.
water. In addition, exposure to
Without complete analysis of the pestiBioaccumulation
many types ofcides and their breakdown products inandpesticides may
aquatic organisms in a natural state, webiomagnification
lead to interacare unable to determine the exact concenproperties oftions between
trations
to
which
they
are
subjected.
If
pesticides inthem that inaquatic life has been exposed for longtissues represents
crease theirperiods of time, the concentrations withina problem in our
toxicity. Little
assessment ofwork has been
the tissues may be much higher than that
their toxicity.
done on theof the surrounding water.
Without complete
interactions
analysis of the
between differpesticides and theirent pesticides,
breakdown products in aquatic organisms
but available evidence suggests that thesein a natural state, we are unable to deterinteractions can increase toxic effects
mine the exact concentrations to which they
(Koenig 1977; Cook et al. 1997).

16

Diminishing Returns: Salmon Decline and Pesticides

Fish Kills andAcute Toxicity ofPesticides
Pesticides are capable of killing salmonids and other aquatic organisms quickly.
These short-term, acute toxicities to fish
have been studied extensively for mostchemicals used in forestry, agriculture,
manufacturing, and the home. Much of thisinformation is provided by the chemical
manufacturer in order to meet requirements
by the Environmental Protection Agency
and various state agencies.

though studies from the Great Lakes haveshown that exposure during this stage oflife can lead to profound results. Cook etal. (1997) found that the toxicities of congeners of TCDD injected into eggs of lake
trout were additive and effective at much
lower dosages than with juvenile fish. In
general, embryonic stages are the mostsensitive to environmental pollutants(Guillette et al. 1995). This is an area of
research in western salmonids which has
been overlooked in the past and needs
immediate consideration.

When pesticides in water supplies
exceed their lethal concentrations, theresults are immediate. Large numbers offish are killed, and these are reported to avariety of federal
Most of theseand state agenacute toxicity studies
cies. The spill isreport lethal amounts
The herbicide acrolein killed approxicleaned up whenas LC50s, the concentra- mately 92,000 steelhead, 114 juvenile
possible and thetions of chemicals that
coho, 19 resident rainbow trout, andresponsible parkill 50% of the test
thousandsofnongamefishintheties are fined. An
animals within 48 or 96
Rogue
River
Basin.
example of thishours, or LD50s, theregulatory action
doses of chemicals incomes frommilligrams per kilosouthern Oregon.
gram body weight of
The Rogue River has received a number of
the test animal which kill 50% of the aniinadvertant spills of pesticides, particularly
mals within 48 or 96 hours. Organisms
acrolein, an herbicide used for removal of
used for these tests range from algae toaquatic vegetation. This herbicide is very
mice and rats. Rainbow trout are a comtoxic to fish. Lorz et al. (1979) reported a
mon subject, as are bluegills, fathead min1977 release of treated irrigation water
nows, mosquitofish (Gambusia), andcontaining Magnicide H, a gaseous form ofzebrafish (Brachydanio rerio). A number ofacrolein, into the Rogue River within 24
LC50s for various fish are available in thehours of treatment instead of the recomliterature (e.g., Norris et al. 1991; Anderson
mended holding time of 6 days. A 10 mile
et al. 1997) or on the internet (e.g.,http://
section of the river was affected. ODFW
ace.orst.edu/info/extoxnet/pips/
officials estimated that 238,000 fish wereghindex.html). In the interest of space, they
killed, including 42,000 salmonids with anwill not be reproduced here.
estimated value of $284,000.
Acute toxicity studies are usually
On May 9, 1996, another large fish kill
performed on subadult or adult fish. Few
occurred in a four-mile stretch of Bearof these studies have used eggs or fry, even17

Diminishing Returns: Salmon Decline and Pesticides

pesticide to enter the stream (Evenson
Creek, a tributary of the Rogue River, Or1998).
egon. A head gate was found open on an
irrigation canal which had been treatedDeaths of threatened and endangeredwith acrolein. The acrolein was used to
species fromremove aquatic
inadvertant convegetation that grew
tamination ofin the canal andDeathsofthreatenedandendangeredwaterways are ofinterfered with its
grave concern
species from inadvertant contamination
operation. Approxibecause the loss ofmately 92,000 steelof waterways are of grave concern beeach individual inhead, 114 juvenile
cause the loss of each individual in aa sensitive popucoho salmon, 19
sensitive population makes recovery
lation makes
resident rainbow
efforts that much more difficult.
recovery efforts
trout, and thousandsthat much moreof nongame fish weredifficult. Fortukilled within a shortnately, these
period of time after
events are relatively infrequent. By conexposure. Talent Irrigation District was
trast, pesticide contamination at sublethal
fined $356,000 for the loss of steelhead bylevels are probably an even greater danOregon Department of Fish and Wildlife.
ger to salmonid populations because the
They were also fined $50,000 by the Oregoncontamination is poorly regulated, theDepartment of Environmental Quality andmortalities go unseen, and the consean additional fine of $407 by the Oregon
quences are unknown.
Department of Agriculture for allowing the18

Diminishing Returns: Salmon Decline and Pesticides

Behavioral
Effects ofPesticides atSublethal
Concentrations

Figure 3
Salmon life cycle.

Behavior of salmonids is specificallydirected at the continuance of the species.
Each aspect of behavior has been highly
selected over the generations to contributeto survival. (See Figure 3.) Interruptions ofthese behavior patterns will therefore
reduce survival and diminish populations.
Pesticides at sublethal concentrations
have been shown to disrupt many of the
behavior patterns of both juvenile and adultsalmonids and probably have deleterious
impacts on their survival. Examples ofthese disruptions are presented below,
although their impact on survival of fish
populations is unknown at this time.

Pesticides Impair Swimming
Performance
The ability to feed, to avoid predators,
to defend territories, and to maintain position in the river system are all dependent
upon the swimming ability of the fish. A
decrease in swimming performance reduces
the ability of the fish to survive and compete with others. Swimming performanceis commonly measured in swim tubes
where the fish is forced to swim against a
gradually increasing current. The current
velocity at which the fish loses its position
is referred to as critical swimming speed.
The time of swimming at a particular velocity before it loses its position is referred to

Salmon and many trout have developed anadromy, abehavior pattern in which juveniles migrate to the sea.
In the sea, juvenile fish feed and grow before returning
to the stream where they were born to lay their eggs.

as swimming stamina. Both are used asindications of swimming performance.
Exposure to sublethal concentrations ofpesticides often causes a loss in swimming
performance. The fungicide TCMTB, which
is used to prevent fungal staining of logs,
causes deleterious effects on the swimming
ability of salmonids. Chinook salmon andrainbow trout juveniles exposed to 5-20 ppb
TCMTB for 48 hours, then removed to cleanwater for 12 hours, showed a dose-depen19

Diminishing Returns: Salmon Decline and Pesticides

Colquhoun et al. (1984) tested theswimming stamina of brown trout exposedto the insecticide naled for 24 hours at aconcentration of 84 ppb. The stamina of the
exposed fish was reduced 57% compared tocontrols. Paul and Simonin (1996) felt that
this exposure time was unrealistic whencompared to the actual exposure times fromaerial application of pesticides overstreams. They held brook trout in watercontaining 23 and 46 ppb naled for 6 hours
and found no change in swimmingstamina. However, they found that both an
insecticide formulation containing
resmethrin and Scourge, a synergised
formulation with resmethrin and piperonyl
butoxide, did affect swimming stamina.
Brook trout that were held in solutions of
3.2 ppb synergised and non-synergised
resmethrin for 6 hours had significantly
reduced stamina. Little et al. (1990) examined behavior of rainbow trout exposed for
96 hours to sublethal concentrations of fiveagricultural chemicals: carbaryl, chlordane,
2,4-D amine, methyl parathion, and pentachlorophenol. All chemicals inhibited
spontaneous swimming activity and swimming stamina.
Rainbow trout exposed to tributyltinoxide, an anti-fouling agent used in boat
20

paint, lost their ability to orient themselvesin a current (Chliamovitch and Kuhn 1977).
Rainbow trout exposed to Aqua-Kleen, 2,4D butoxyethanol ester, also lost orientation
to currents with increasing concentrations(Dodson and Mayfield 1979a). At nearlethal concentrations, the orientation became variable. The most evident behavior
change was a lethargy that increased withgreater concentrations of the herbicide.

CORVALLIS ENVIRONMENTAL CENTER

dent reduction in critical swimming speeds(Nikl and Farrell 1993). A further study
with coho salmon at the same concentrations indicated that the reduction in criticalswimming speed was dependent on boththe concentration of TCMTB and the time of
exposure to the chemical (Nikl and Farrell1993). Damage to gill structure also increased with concentration and time of
exposure. The researchers speculated thatgill damage prevented respiratory exchange
and that the decrease in oxygen availability
was at least partially responsible for thedecrease in swimming speed.

Studies show that low concentrations of certain
pesticides impair the swimming performance ofrainbow trout.

Half of juvenile Atlantic salmon subjected to 1 ppm of the insecticide
fenitrothion for 15-16 hours lost the ability
to maintain territories for a period of six
days after exposure (Symons 1973). Exposure of rainbow trout to 46 ppb of Vision, aglyphosate herbicide, for one month caused
increased aggressive behavior (Morgan andKiceniuk 1992). Rainbow trout exposed tothe synthetic pyrethroids, fenvalerate andpermethrin, tended to swim at the water
surface, coughed repeatedly (attempting toclear the gill surface) and increased gillmovements, suggesting respiratory distress(Holcombe et al. 1982). Those exposed tothe organophosphate pesticides, Dursban(chlorpyrifos) and disulfoton, becamedarker and showed indications of muscle
spasms and skeletal deformations. Bothpesticides are cholinesterase inhibitors andthe reactions were attributed to blockedDiminishing Returns: Salmon Decline and Pesticides

cape responses similar to controls in aneural transmission. Trout exposed to thechlorinated hydrocarbon, Kelthane
simulated estuarine environment. After
five days, however, TCMTB-treated fish
(dicofol), became dark, lethargic, andhad been preferentially consumed by introshowed signs of respiratory distress, suggesting both respiraduced rockfish 5.5
times more fretory and neurotransThese experiments show that pestimission problems
quently than
cides
at
very
low
concentrations
can(Holcombe et al.
controls. In another study, after a1982).
interfere with swimming performance
24-hr exposure toin salmonids and that these effects canThese experi1.0 ppm
last for some time after exposure toments show that
fenitrothion,
the chemicals.
pesticides at very
Atlantic salmon
low concentrations
parr were more
can interfere withvulnerable toswimming perforpredation bymance in salmonids and that these effects
brook trout than controls (Hatfield andcan last for some time after exposure to theAnderson 1972). Exposure to DDT had nochemicals. The evidence comes from laboeffect on the predation. Little et al. (1990)
ratory experiments and would be very
found that carbaryl and pentachlorophenol
difficult to replicate in the field. If similar
increased vulnerability of rainbow trout toeffects occurred in field situations, however,predation.
interference with swimming performance
would result in increased death from
Predator avoidance tests with coho
predation.
(Olla et al. 1992) and chinook salmon (Ollaet al. 1995) indicated that stresses causing
increased plasma cortisol levels resulted in
Pesticides Can Increase
susceptibility to predation, but that predaPredation on Juvenile Salmonids
tor avoidance in coho salmon returned
within 90 minutes (Olla et al. 1992) or 4
The end result of any decrease inhours (Olla et al. 1995). In chinook salmon,
swimming ability will be an increase in
predator avoidance was recovered in 24
predation upon the juvenile salmonids. If ahours after exposure to stress. While acuteyoung salmonid is slowed in its escapestresses seem to render the juveniles susresponses by ion imbalances, metabolic
ceptible to predation, the effects of chronic
problems, or disease, it becomes prey for astresses from pesticide exposure are notnumber of hungry predators. Its demise iswell known. Exposure of juvenile coho
not immediately evident without sophistisalmon to sublethal levels of two triclopyr
cated predator tests. Several studies haveherbicides for four hours did not result in
demonstrated that pesticides can indeed
significant changes in secondary stressincrease predation.
effects, such as respiration, plasma glucose
and lactate, and hematocrit (Janz et al.
For example, Kruzinski and Birtwell1991). No plasma cortisol levels were(1994) found that juvenile coho salmon
measured, but these usually correlate well
exposed to sublethal concentrations of thewith plasma glucose concentrations. Howfungicide TCMTB showed fright and esever, exposure to sublethal concentrations
21

Diminishing Returns: Salmon Decline and Pesticidesof the butoxyethanol ester of 2,4-D caused
enlargement of the interrenal gland, an
indication that cortisol production wasincreased (McBride et al. 1981). If chronic
exposure to pesticides does cause increasestress responses in salmonids, the studies ofOlla et al. (1992, 1995) suggest that predation will be much greater in exposed fish.

by subyearling Atlantic salmon exposed tosublethal concentrations of DDT persisted forat least a month after the fish were transferred
to clean water (Ogilvie and Miller 1976).
Exposure to the organochlorine insecticide
aldrin at a concentration of 100-150 ppb also
caused Atlantic salmon juveniles to selectlower water temperatures (Peterson 1973).

These results suggest that salmonids
exposed to some pesticides select temperatures according to the concentrationof pesticide. At low concentrations, fish try
Most organisms respond to the presto lower their body temperature to minimize
ence of pathothe effects on physigens throughological processes. As
temperature
the concentration
Disruption of schooling behavior by
selection. Coldincreases, they respondmany pesticides suggests that theseblooded animals
by seeking warmer
compounds may increase predationsuch as lizards orwater to stimulate
upon juvenile salmonids and lead tofish typicallydetoxification. These
population
losses
that
would
be
very
seek warmer
effects can last for adifficult to detect by conventional
environments toconsiderable time after
increase metathe pesticide is refisheries techniques.
bolic repair
moved, causing the fish
when subjected
to seek abnormal water
to toxicants or
temperatures and thus
infections. In salmonids, studies showed that
subjecting them to increased dangers of
the temperature selected depended on the
disease and predation.
concentration of the pesticides to which thefish were exposed. Juvenile Atlantic salmon
Schooling Behavior is Reduced
exposed to low doses of DDT selected lower
by Pesticides
temperatures than controls (Ogilvie andAnderson 1965; Peterson 1973). At higher
Schooling behavior is a tactic to reduce
doses of DDT, exposed fish selected higher
predation. Predators are presented with atemperatures than controls. This effect waslarge mass of fish from which it is difficult
accentuated in fish acclimated to warm0
to focus on a single individual (Cushingtemperatures (17 C) compared to fish acclimated to cool temperatures (80 C). Fishand Harden-Jones 1968). Seaward migra0
acclimated to 17 C and exposed to 10 ppb ortion of juvenile salmonids is accompanied
higher of DDT became hyperactive whenby schooling responses, probably to reduce
introduced into cold water. Brook trout
losses to the population during theexposed to isomers of DDT and derivatives
migration.
showed similar changes in temperature
selection (Miller and Ogilvie 1975; Gardner
Many pesticides disrupt schooling1973). The alteration in temperature selection
behavior. Drummond et al. (1986) foundTemperature Selection is
Changed by Pesticides

22that loss of schooling behavior in fatheadminnows was the most sensitive indicatorof stress for 133 of 139 organic chemicals
tested, including a number of pesticides.
Exposure to sublethal concentrations of thefungicide TCMTB interferes with schoolingbehavior in chinook salmon (Kruzinski andBirtwell 1994). Exposure to methoxyclor
caused a progressive increase in inter-fishdistance in brook trout (Kruzinski 1972).
Holcombe et al. (1982) found that schoolingbehavior was disrupted in fathead minnows exposed to sublethal concentrationsof Kelthane, Dursban, disulfoton,
fenvalerate, and permethrin.
Disruption of schooling behavior bymany pesticides suggests that these compounds may increase predation uponjuvenile salmonids and lead to population
losses that would be very difficult to detectby conventional fisheries techniques. The
prevalence of this effect by organic chemicals (Drummond et al. 1986) suggests that
this sublethal effect may be more widespread than we might suspect.

Pesticides Can Interfere With
Seaward Migration
Juvenile salmon rearing in streams
reach a stage where their color changes
from brown to silver. This is the stage ofparr-smolt transformation where a variety
of morphological, physiological, and behavioral changes occur. In addition to thesilvery color, the smolts lose their territorial
behavior, begin to school, and to migrate
downstream to the sea. The mechanisms ofthis process have been widely debated andhave been the subject of many local andinternational workshops.
The effects of pesticides on seaward
migration have not been extensively stud-

INSTITUTE FOR FISHERIES RESOURCES

Diminishing Returns: Salmon Decline and Pesticides

Estuaries are a critical transition zone where
salmon adapt to saltwater.

ied because of the difficulty of measurement of migration tendency. Lorz et al.
(1979) studied the effects of three herbicides
on seaward migration in coho salmon.
Diquat at concentrations from 0.5 ppm to
3.0 ppm inhibited seaward migration in adose-dependent manner. Dinoseb inhibited
migration only at the high (but sublethal)concentrations of 40 and 60 ppm. Tordon
101 (a mixture of picloram and 2,4-D)
caused a slight inhibition of migration at
the highest levels studied (1.2 and 1.8 ppm),
but the results were not significantly different from controls. Although the herbicides
were not lethal to the fish at the concentrations used, the levels were very high (ppm)compared to other concentrations of pesticides (ppb) described in this section. Thismay be due to the low toxicity of mostherbicides, compared to other classes ofpesticides. More work on seaward migration should be done with other pesticides,
especially the organochlorine and organophosphate insecticides commonly found inwestern streams.

Pesticides Interfere with
Seawater Adaptation
The end result of seaward migration isthe entry of juvenile salmon into an estuary
23

Diminishing Returns: Salmon Decline and Pesticides

and the tranformation of the fish’s osmoDDT (Hansen 1972). No change in salinity
regulatory mechanisms from a fresh water
preference was induced by malathion
to a saltwater environment. These osmo(Hansen 1972).
regulatory processes permit the fish to
maintain required water and ion concentraIn a study on the effects of herbicides
tions in various organ systems. The stresses
on juvenile coho salmon, three of the thirinvolved with this transition can be surteen herbicides studied, Amitrole-T, diquat,
mised from the large mortality (usuallyand paraquat, caused dose-dependent
about 90% or greater for hatchery smolts)
mortality in seawater tests (Lorz et al. 1979).
which results from seawater entry (Pearcy
An interesting phenomenon occurred in1992). Death can result from several causes.
fish exposed to Tordon 101 (a mixture of
The juvenile fish may simply not make the2,4-D and picloram). In December, fishtransition to seawater and die from osmowere tested at eight different concentraregulatory problems. The juvenile fish may
tions. The two lowest concentrations, 0.25
be slowed by the osmotic stresses and be
and 0.5 ppm, caused increased mortalities,
eaten by birds or predatory fish. The imwhile at higher concentrations up to 20
mune system of the fish may be comproppm all fish survived. When this was
mised by the osrepeated in March,
motic stresses,
fish exposed to 20
Becausethetransition
from
fresh
water
permitting the
ppm Tordon 101 all
to seawater is a critical period in theonset of disease
died in seawater. The
and subsequent
researchers could notsurvival of the juvenile salmon, one
predation by pisexplain the unexwould expect pesticides to have some ofcivorous birds orpected mortalities attheir greatest effects at this stage.
fish.
the low concentrations but suggested
Most salmothat pre-smolted coho
nids spend a period of transition in thesalmon in December were less sensitive toestuary where they seek the salinities theyenvironmental pesticides than those in
prefer. Many utilize the less saline estuasmolted condition in March (Lorz et al.
rine surface water which stratifies over1979). Mitchell et al. (1987) found that a 10deeper more saline water (Iwata et al. 1982;
day exposure to 2.78 ppm of the herbicide
Birtwell and Kruzinski 1989).
Roundup (a glyphosate formulation) did
not affect seawater adaptation or growth.
Few studies have looked at the salinity
preference of fish exposed to sublethal
Because the transition from fresh waterlevels of pesticides. One would expect thatto seawater is a critical period in the surthe stress from pesticide exposure mightvival of the juvenile salmon, one would
cause the fish to select salinities compaexpect pesticides to have some of theirrable to that of their blood to relieve thegreatest effects at this stage. However,extra burden of osmotic stress. Cohostudies showing relationships between
salmon in the stratified salinity tank set up
pesticides and osmoregulatory problems
by Kruzinski and Birtwell (1994) sought theleading to mortality in salmonids are few.
freshwater wedge if they were previously
Most of the studies that have been done
exposed to TCMTB. Mosquitofish, howhave focused on marine species or euryhaever, sought a higher salinity if exposed toline species which do not undergo the24Diminishing Returns: Salmon Decline and Pesticides

radical transformation of osmoregulation
experienced by salmonids and otheranadromous species. Studies on the effectsof pesticides, especially organochlorine andorganophosphate pesticides, on salmonids
are needed in this area.

OREGON SEA GRANT

the evidence is convincing that the salmon
runs have been affected by spraying, theexperimental evidence has not yet been
published in the scientific literature. A
paper describing these effects has been
submitted for publication (Fairchild 1999).

An adult chinook salmon that is ready to spawn.

Pollutants Affect Adult Returns
The result of interference with life
history mechanisms of the juveniles shouldbe the decrease in numbers of returning
adults. Because the sublethal effects ofpesticides on fish survival have not been
fully appreciated, there are few studies thathave correlated the return of adult salmon
with the extent of pesticide use in the river
basin. In New Brunswick, however, researchers have found that decreased returnsof Atlantic salmon have been correlatedwith the use of pesticides in the area. Specific concern has focused on the compounds
known as nonyl phenols, which are used
not only as wetting agents in pesticides, butalso in the production of paper, textiles, andpetroleum products. Nonyl phenols arethought to act both by endocrine disruption
and by interference with the normal adaptation of salmon smolts to seawater. While

Migration patterns and timing of adultsalmon may be altered by pollutants as theyre-enter fresh water during their spawning
runs. Elson et al. (1972) showed thatradiotagged Atlantic salmon entering theunpolluted Tabusintac estuary in New
Brunswick moved quickly up the estuary
and into the river system. In contrast,
salmon entering the Miramichi estuary, aheavily industrialized estuary, spent time
swimming back and forth in an attempt to
avoid heavily polluted water. They were
never found in a channel on the northwestside of Beaubears Island, where a marsh at
the lower end of the island served as areservoir for effluent from a wood-preservative plant. This effluent seeped into theriver at high tides. Salmon clung to thecleanest side of the river as they swam
upstream past the industrial area. Clearly,
the fish were slowed in their spawningmigration as they searched for the cleanest
parts of the river.
Respiration of adult coho salmon was
examined as they attempted to pass a
polluted estuary within the city limits ofSeattle, Washington (Smith et al. 1972).
They found that respiration decreased andblood lactate increased during swimmingin the polluted area. They suggested thatthe salmon either avoided the areas ofpollution, resulting in delayed passage
times, or swam through the polluted areas,
resulting in an oxygen debt and decreased
energy reserves. Decreased energy reserves could result in smaller eggs andinsufficient energy for passage into upstream spawning areas.
25

Diminishing Returns: Salmon Decline and Pesticides

In summary, these studies on the
disruption of behavior of salmonids bypesticides suggest that the presence ofpesticides can have profound effects on thesurvival of the juveniles. Every aspect of
their biology can be affected. The studies
reported here consider mainly the freshwater portion of the salmonid life history.
Exposure to pesticides continues in theestuaries and in the sea. For example, amajor food source for juvenile salmon in the26

estuary is the amphipod Corophium, which
spends the day buried in sediments which
may be the final repository for many of thepesticides applied far upstream. It is likelythat the amphipods accumulate pesticides
and transfer them to the salmonids wheneaten. Few studies have documented the
behavior of juvenile salmonids once theyreach the estuary. Even fewer have examined the effect of pollutants and pesticides
on their behavior and survival.

Diminishing Returns: Salmon Decline and Pesticides

Compromised
Immune Systems

growth, with non-specific immunity developing first, followed by cell-mediated andthen humoral immunity. Full humoral
immunity, the ability to produce circulating
antibodies, develops at about 1 g in size.

Fish in polluted waters are subject to
A number of natural and anthropomore frequent and more severe outbreaks
genic factors suppress the function of theof disease because many synthetic chemiimmune system. Stresses from habitat
cals tend to suppress the immune systemchanges, poor water(Moller 1985;
quality, lack of food,
Repetto andand pollutants all
Baliga 1996).
Fishinpollutedwatersaresubject
toresult in
Immune systems
morefrequentandmoresevereoutimmunosupression
protect fish fromand an increase in
breaksofdiseasebecausemany
synserious diseases
disease (Pickering
caused by exterthetic chemicals tend to suppress the1993).
nal bacteria,
immune system.
parasites, andInformation onviruses. The
immunosuppression
complexities ofinsalmonidsduetopesticides
is scanty,
these systems are regulated and coordialthough other fish have received morenated by a variety of compounds that act
similar to hormones but that do not quite fit
into the classical definition (Bern 1990).
Most texts on molecular endocrinology
include interleukins, cytokines, epithelial
growth factors, and other compounds that
influence the immune system as hormones(Bolander, 1994). These immunohormones
can be compromised in various ways byenvironmental pollutants (Anderson 1996;
Repetto and Baliga 1996).

CORVALLIS ENVIRONMENTAL CENTER

Although considerable work has been
done on the immune system of fish, ourunderstanding is still far from that we havegained about the intricacies of the humanand rat immune mechanisms. As in mammals, fish have both cellular and humoral(antibody) responses to foreign agents, andexert both the B cell and T cell responses tothese stimuli. It is generally agreed thatsize rather than age of fish determines theimmunological maturity (Tatner 1996). In
rainbow trout, a gradual increase in immune competence occurs during early27

Diminishing Returns: Salmon Decline and Pesticides

attention (Anderson 1996; Iwama andNakanishi 1996). The insecticide endrin
reduced the activities of phagocytes andantibody producing cells in rainbow trout(Bennett and Wolke 1987). Organotin
compounds caused immune suppression in
rainbow trout (O’Halloran et al. 1998).
Although tributyltin is considered more
toxic to fish than its breakdown product,
dibutyltin, the latter was the more potent
immunotoxin. Phenol and the PCB
Arochlor 1254 were found to reduce antibody producing cells in rainbow trout(Anderson et al. 1984) and coho salmon(Cleland et al. 1989). TCDD caused mitogenic suppression in rainbow trout(Spitsbergen et al. 1986) and increased
susceptibility to infectious hematopoetic
necrosis virus (Spitsbergen et al. 1988).
The timing of exposure to pollutants
may be an important factor for the health of
the immune system in anadromous salmonids. Maule et al. (1987) found that im-

28

mune suppression occurred to a greater
extent during smolting of coho salmon.
This may be due to the higher levels of thestress hormone, cortisol, found duringsmolting in salmonids (Specker and Schreck
1982; Thorpe et al. 1987). Cortisol isknown to suppress the immune system of
salmonids (Maule et al. 1987; Pickeringand Pottinger 1989; Maule and Schreck1990). It is likely that the effects of exposure to immunosuppressant chemicals
during the period of seaward migration
may be compounded by the high levels ofplasma cortisol in the fish at that time.
Many pesticides cause some degree of
immunosuppression in mammalian systems (Repetto and Baliga 1996). It seems
likely that similar effects may be found in
the fish immune systems. Before thenecessary research provides answers, it
seems prudent to err on the side of caution and assume that similar immunosuppression by pesticides can be found insalmonids.

Diminishing Returns: Salmon Decline and Pesticides

In the late 70s, researchers Mike
Howell and Ann Black found that theirseine hauls from a small coastal stream in
the panhandle of Florida contained
mosquitofish with a strange characteristic.
They were all males (Howell et al. 1980).
On further inspection, another oddity was
noted. Many of the apparently male fish
had a gravid spot on their gonopodium,
which normally indicates a female withinternally developing young. Further
analysis in the laboratory indicated thatmany of the apparent males were in fact
masculinized females. A few months later,a second population of masculinized females was discovered in the Fenholloway
River of coastal Florida (Bortone and Davis
1994), a stream approximately 300 kilometers east of the first stream. This collection
included not only mosquito fish but also
the least killifish and the sailfin molly. In
both streams, the masculinized females
were found downstream of paper mills.
Some component of the effluent from paper
mills caused the females to acquire masculine traits.
This research was one of many studies
conducted over the past twenty years thatindicated that certain synthetic chemicals,
including many pesticides, can alter thesexual endocrine (or hormone) system of
wildlife (Colborn and Clement 1992). The
effects of these pseudo-hormones can varyconsiderably. In the above example, female
fish became masculinized. Other pollutants
act as artificial female sex hormones or
estrogens. In still others, sexual expression
is not affected. Instead, the chemicals
interfere with bone formation during early
development and result in stunted or mal-

Endocrine-disrupting chemicals can interferewith normal functioning of the body’s hormone
system in a variety of ways. By mimicking or
blocking hormones, the synthetic chemicals
disrupt normal cellular communication, alteringor preventing the appropriate biologicalresponse. Some endocrine disruptors can alsointerfere with chemical messengers involved
with the immune system, hormone synthesis,
neurotransmitters, and growth processes.

formed adults. As scientists gain greater
insights into the complex workings of
endocrine systems, they have come toappreciate the delicate balance of hormones
needed to direct the early development ofan embryo and the profound effects that
endocrine mimics may produce.
Endocrine systems in an organism
control production of hormones, which inturn control many of its functions. An
endocrine system is a complex network of
positive effectors and feedback loops that
29

K. BORN

Endocrine
Disruptors

Diminishing Returns: Salmon Decline and Pesticides

OREGON DEPT. OF FISH AND WILDLIFE

carry messages from one part of the body toelements to stimulate or regulate the proanother to keep the body functioning propduction of steroid specific proteins.
erly. Initial input to the system comes fromthe environment in the form of temperaIn such a complex system, pesticides
ture, light, or other sensory stimuli. Theseand their derivatives can interact at many
stimuli are recognized and integrated in thelevels in the brain-pituitary-target organ
brain. Through aaxis with anumber of pathways,
variety ofbrain centers control
effects. These
Certain pesticides and pollutants can
the synthesis of prieffects can
mimic the effects of estrogens, causing
mary hormones in the
manifest thempituitary, a small bud
feminization of male animals.
selves throughof nerves and tissues
behavioral,at the base of the
reproductive,
brain. In the reproducimmunologitive cycle, the pituitary produces gonadotcal, or physiological changes (Bern 1990).
ropins which act on the gonads to produce
Our knowledge of the hormonal relationsteroid hormones: androgens predominatships to many of these functions is not welling for males and estrogens predominating
enough defined at present to exactly deterfor females. Steroids and other hormones
mine what effects pollutants may have on
travel through the blood to seek specificthese functions. However, our knowledge
receptors in the cytoplasm of responsiveof the female endocrine system and thecells. Each sex contains both male andeffects of pesticides on its function has
female receptors in its cells so that thegrown rapidly in recent years, and numerrelative concentration of androgens andous studies have defined some of the unestrogens are the determining factor forwanted effects.
sexual differentiation. When the steroid
binds to the receptor protein, the steroidPesticides Can Mimic Estrogens
receptor complex finds its way to the
nucleus where it binds to DNA response
The sex of fishes can be determined
relatively late in development. For example, applications of testosterone during
the egg and fry stages of salmonids canconvert the young fish completely to males
or cause them to become sterile, dependingon the concentration. Applications ofestradiol, the female sex hormone, cancause production of 100% female salmon(Hunter and Donaldson 1983). In chinook
salmon, Piferrer et al. (1994) suggested that
aromatase, an enzyme that converts androgens to estrogens, acts as a regulatory
switch for the process of sex differentiation.
During early development, fish are especiallyvulnerable to pesticides that can mimic natural
They showed that a treatment of young
hormones.
salmon with an aromatase inhibitor for only
30

Diminishing Returns: Salmon Decline and Pesticides

Certain pesticides and pollutants can
mimic the effects of estrogens, causing
feminization of male animals. Actions ofpesticides that result in feminization in fish
are thought to occur in three ways:
1) Estrogen mimics compete with
estradiol, the female sex hormone, for its
receptor protein. The complex that isformed enters the nucleus, binds the DNA
response elements, and stimulates the
responses expected from normal female sex
hormones. This has little effect in females
but stimulates inappropriate responses inmales, which have only very low concentrations of circulating estrogens. The result isfeminization of the males.
2) Antiandrogenic compounds compete with androgens, or male sex hormones, for the androgen receptor protein.
Once bound, the complex enters thenucleus but is not able to bind to DNA
response elements. Consequently, no
androgenic response is stimulated. In theabsence of an androgenic response, the fishassumes that it is a female and the result isfeminization.
3) Compounds may interfere withneurotransmitters or signal transduction

OREGON DEPT. OF FISH AND WILDLIFE

two hours could transform genetic females
into functional males. These transexual
males had testes indistinguishable fromnormal males, underwent all stages ofsperm maturation, and were later used tofertilize females to produce all female
offspring. Concentrations of androgens
and estrogens circulating through the blood
provide a stimulus for induction of levels ofaromatase activity (Callard and Callard
1987). With a system of sex differentiationin fishes that is labile (i.e., likely to change),
the potential for major impacts from estrogen mimics may be quite large.

Pesticide exposure at the fry stage can cause
feminization of male fish or even sterility.

mechanisms in the brain. The interference
results in an upset of the regulatory mechanisms that distinguish males from females
and sends the wrong messages to the pituitary. The result may be the release of
gonadotropins that stimulate feminizationof the juvenile fish.
The best known examples of feminization by competition of pesticides for estrogen receptors have occurred with alligatorsin the Southeast (Guillette et al. 1995), sea
gulls (Fry and Toone 1981) and Caspianterns (Fox 1992). Increasing numbers ofchemicals are found to have estrogenic
activity in fish (Jobling and Sumpter 1993;
Jobling et al. 1995). Unknown chemical
contaminants from sewage effluents havebeen shown to produce estrogenic responses in male carp (Folmar et al. 1996).
DDT and its long-lived breakdown product,o,p’-DDE, have been shown to bind estrogen receptors to provide weakly estrogenic
responses, whereas p,p’-DDE does not bind
estrogen receptors except at high concentrations (Donohoe and Curtis 1996). p,p’-DDE
31

Diminishing Returns: Salmon Decline and Pesticides

has a higher affinity for androgen receptors
Most of these pesticides bind only
(Kelce et al. 1995),
weakly to the estrosuggesting thatgen receptor. For
the binding may
example, theEnvironmental compounds in combinabe nonspecific forbinding of the
tion
may
act
togetherwiththeestrogena number of
insecticides
receptors to provide responses far
steroid receptors.
endosulfan,
greater than that of single compounds.
Lindane,dieldrin, toxchlordecone
aphene, and(Donohoe andchlordane to theCurtis 1996; Thomas
estrogen receptor
and Khan 1997), alkylphenols (Jobling et al.
was very weak: less than 1/10,000 that of
1995; White et al. 1994), endosulfan, dieldthe natural binding compound, estradiol
rin, and toxaphene (McLachlan 1993; Soto
(McLachlan,1993; Soto et al. 1994). For thiset al. 1994) have all been shown to provide
reason, these compounds were thought for
estrogenic responses in fish and othera long time to produce few environmentalorganisms through binding to estrogeneffects. However, environmental comreceptors.
pounds in combination may act together*

METHOXYCHLOR

DDE

DDD

PCB

DDT

PCB

DIELDRIN

TOXAPHENEENDOSULFAN A

100

COMBINATION OF 10 CHEMICALS200

ENDOSULFAN B

Increase in number of breast cancer cells(in thousands)

Figure 4. Combinations of chemicals have a greater estrogenic
effect on organisms than single chemicals.

0
Unexposed(control)Exposed to single chemicals
at low concentrations (1µM)

Notes: Lines above the bars represent standard errors. * indicates that the increase in number ofcells is significantly greater than unexposed cells. Proliferation of breast cancer cells is a standard
test for estrogenic effects.

Exposed to a
combination ofchemicals at low
concentrations

Source: Soto, A. M., K. L. Chung, and C. Sonnenschein. 1994. The pesticides endosulfan, toxaphene, anddieldrin have estrogenic effects on human estrogen-sensitive cells. Environ. Health Perspect. 102:380-383.

32

Diminishing Returns: Salmon Decline and Pesticides

with the estrogen receptors to provide
responses far greater than that of single
compounds (see Figure 4).

ketotestosterone, to receptors for testosterone in the nucleus is not clear(Pasmanik and Callard 1985; Callard andCallard 1987), although a receptor for 11ketotestosterone in the ovaries of coho
salmon has been reported (Fitzpatrick et
al. 1994).

Feminization of males may also bebrought about by antiandrogenic compounds. Vinclozolin, a fungicide usedwidely for grapes, ornamental plants, snap
peas, and turfgrass (Kelce et 1994), causes
The third category of hormonal disrupfeminization of males. The fungicide binds
tion which may result in feminization by
to androgen receptors and enters theenvironmental pollutants arises from thenucleus, but blocks normal androgenic
interference with regulatory functions in
responses. The vinclozolin-androgenthe brain and pituitary. This interference
receptor complex cannot recognize thecan affect neurotransmitter functions,appropriate DNA
sensory systems,
response elements
control of serum
to stimulate prohormone levels and
The peculiar lability of sex differentiation
duction of essential
therefore hormonalin fishes suggests that endocrine-dismale proteins
feedback. We
rupting chemicals in the environment(Wong et al. 1995).
know little about
may profoundly alter the sex ratios and
DDE, the persisthe role of pestibreeding capabilities of our native fish.
tent break-downcides in this area,

CORVALLIS ENVIRONMENTAL CENTER

product of DDT,
also binds toandrogen receptors
with similar results (Kelce et al. 1995).
Antiandrogenic responses in fish are notwell understood at present. Part of thisdifficulty is the problem of demonstrating
androgen binding activity in fish tissues(Monosson et al 1997). The relationship of
the active androgen in fish, 11-although there is
ample informationthat shows thatbrain function is a necessary part of providing the correct hormones for sexual
differentiation. Serotonin has been shownto cause release of gonadotropins from thepituitary in croakers (Khan and Thomas1992) and goldfish (Somoza et al. 1988) socompounds that interfere with serotoninlevels may affect the release of gonadotropins. Arochlor 1254 has been shown tocause decreases in serotonin and dopaminelevels in the brains of fish (Kahn andThomas 1996), due either to increased
degradation or decreased synthesis of theneurotransmitters. Many insecticides arecholinesterase inhibitors, that is, theyinterfere with the normal breakdown ofacetylcholine, a neurotransmitter, byblocking the enzyme cholinesterase. This
results in a longer lifespan for acetylcholine and a disruption of normal neuralfunction.
33

Diminishing Returns: Salmon Decline and Pesticides

Pesticides May Have Other
Endocrine Effects
Although disruption of sex steroid
function has received the most attention, it
is not the only type of endocrine disruptionthat may result from exposure to environmental chemicals. Brucker-Davis (1998)
listed over 90 synthetic chemicals that
affected function of the thyroid gland.
Thyroid hormones are thought to influence
seasonal adaptations, reproduction, migration, and growth of fish. Hypothyroidism
resulting in the formation of goiters wasshown in coho and chinook salmon rearing
in the Great Lakes and was related to environmental contaminants in the lakes(Moccia et al. 1977; Moccia et al. 1981).
Thyroid impairment has been shown in thecatfish Clarias batrachus after exposure tocarbaryl (Sinha et al. 1991) and malathion(Sinha et al. 1992). Both malathion andcarbaryl suppressed levels of thyroxine in
the kidney, but increased thyroxine in thepharyngeal thyroid. Peripheral conversionof thyroxine to the active hormone, triiodothyronine, was suppressed with bothcompounds.
Skeletal deformities have long beenrecognized as an effect of environmental
34

pollution and have been suggested as an
excellent indicator of the extent of pollution(Bengtsson 1979). A comparison of reportsof skeletal damage from old and newsources has given rise to the suspicion thatwater pollution may be having a larger

OREGON DEPT. OF
ENVIRONMENTAL QUALITY

The peculiar lability of sex differentiation in fishes (Chan and Yeung 1983) suggests that endocrine-disrupting chemicals
in the environment may profoundly alter
the sex ratios and breeding capabilities of
our native fish. This field is still young andeffects on fish population are largely unknown. With the development of moresophisticated methods for detection ofpseudo-estrogens and pseudo-androgens in
the environment, we should have a better
understanding of the effects of chemicals
that find their way into our watersheds.

Squawfish from the Newberg pool in the WillametteRiver have a high incidence of skeletal deformities.

impact on fish populations that we expect.
Bone formation and structure relies
upon the mobilization and handling of
calcium ions, which are controlled by avariety of hormones, including growth
hormone, calcitonin, parathyroid hormone,and stanniocalcin (Davis 1997). These arein turn controlled by the brain-pituitary
axis described earlier and subject to similar
feedback mechanisms to regulate theirsynthesis and concentration. Unfortunately, calcium regulation mechanisms have
not received the study that reproductive
hormones have and consequently we know
little about specific mechanisms underlying
skeletal defects. Evidence that links environmental pesticides to skeletal abnormalities, however, is widespread.
In the early 1970s, fish biologists studying members of the drum family in JamesRiver, Virginia, found that a large numberof specimens had shortened vertebral
columns compared to similar species in the
nearby York River. With the help of toxicologists, they found that a manufacturingDiminishing Returns: Salmon Decline and Pesticides

facility for chlordecone, a widely-used
insecticide, had been releasing large
amounts of the compound into the JamesRiver. The stunted fish contained highchlordecone levels (Davis 1997). Exposure
to chlordecone interfered with calcium
deposition into bone and produced scoliosis
and compression of the vertebrae (Couch etal. 1977). After 1976, when manufacture ofchlordecone had stopped, the frequency ofvertebral abnormalities decreased.

researchers feel that the damage is done in
the egg or early fry stages, possibly byeffects on neuromuscular interactions
during early development.

Recent studies on squawfish in the
Willamette River have shown elevatednumbers of abnormalities in bone formation, especially in the Newberg Pool (RM 26
to RM 60) (Altman et al. 1997). In the
Newberg Pool, skeletal deformities ranged
from 22.6 to 52.0 percent. No specific cause
Wells and Cowan (1982) reported
for the deformities has been identified, but
dysplasia in Atlantic salmon parr after aa variety of factors including high temperasimulated spill oftures, low distrifluralin, a presolved oxygen,emergent herbicide,pesticides, PCBs,
Trifluralin, a pesticide found in thein the Eden River ofand effluents from
Willamette River, has been shown to
Scotland. The fish
pulp mills, paper
cause
bone
abnormalities
inAtlantic
were exposed to themills, and ore
salmon.
herbicide for lesssmelters have beenthan 1 day. Parrsuggested. Analydeveloped scoliotic
ses by the U. S.
vertebral abnormalities that caused them toGeological Survey showed the presence ofappear stumpy. Laboratory tests showed
heavy metals (Altman et al. 1997), orgathat exposure to trifluralin resulted innochlorine pesticides, organophosphate
hyperosteosis, a proliferation of the bone
pesticides, and even trifluralin in thetissue (Couch et al. 1979). This was accomWillamette River and its tributaries
panied by fusion of vertebrae, persistence(Anderson et al. 1997). Although noof osteoblasts, abnormal vertebral proskeletal abnormalities were found incesses, and, strangely, the presence of notosalmonids in the watershed, the widechord tissue in the vertebral canal. Clearly,
spread occurrence of pesticides in
the mechanisms of bone formation had
Willamette River and the presence ofbeen severely disrupted.
skeletal abnormalities in squawfish
should stimulate research on the potential
A number of other environmental
endocrine-disrupting effects of the mostpollutants, including chlorinated hydrocarcommon contaminants, such as atrazine,bons (toxaphene, DDT), organophosphatesimazine, metolachor, and diuron. At thepesticides (malathion, parathion, demeton),
least, such abnormalities in the fish popucrude oil, and heavy metals (Bengtsson
lations should provide a warning for the1979), have been implicated in bone abnorpresence of endocrine disruptors in our
malities in fishes. In most of these studies,watersheds.

35

Diminishing Returns: Salmon Decline and Pesticides

Pesticides can indirectly affect fish byinterfering with their food supply or altering the aquatic habitat, even when theconcentrations are too low to affect the fishdirectly. Such indirect effects may greatly
reduce the abundance of food organisms
which in turn reduces the growth andprobable survival of the fish.
Excellent examples of indirect effects ofnumbers of poisoned nymphs were foundpesticides on salmonids were documented
drifting downstream after spraying. Comin the attempts to control spruce budworm
parisons with pre-spray drift samples
in the forests of northeastern U. S. andshowed that the numbers of dead nymphs
Canada (Muirhead-Thomson 1987). In theincreased as much as 6000 times aftermid 1970s, permethrin, a synthetic pyrespraying. This massive mortality wasthroid, was introduced to kill the spruce
followed by a feeding frenzy among the
budworm. The insecticide was lethal tosalmonids. Atlantic salmon increased theinsects and moderately toxic to fish. Experinumber of nymphs in their stomachs by 2-4
mental sprayings of permethrin at 13 differfold. Brook trout
ent streams befed even more
tween 1976 andvoraciously, increas1980 did not result
Pesticides can indirectly affect fish bying their stomach
in moralities ininterfering with their food supply orcontents by as much
native fishalteringtheaquatic
habitat,even
when
as 10-fold.
(Kingsbury andtheconcentrations
are
too
low
to
affectKreutzweiser
The poisoned
the fish directly.
1987). Blocking
insectsseem to haveseines set at the
no apparent directbottom of theeffects on the salmosprayed areas
nids, which fed as long as the drifting
were never found to contain dead fish.
larvae were available. With time, however,
Minnows and juvenile Atlantic salmon
the diets of the salmonids, especially theheld in live cages in the sprayed area
brook trout, changed considerably. With
showed no mortality attributed to thefew of the normal food components ofspraying regimes.
stonefly and mayfly nymphs and caddis
larvae left in the streams, the trout changed
The same could not be said for theto a diet of primarily Dipteran (fly) larvae
aquatic larvae in the streams, however
and terrestrial insects.
(Kreutzweiser and Kingsbury 1987). Huge
36

LYNN KETCHUM, OREGON STATE UNIVERSITY

Indirect Effects
of Pesticides on
SalmonDiminishing Returns: Salmon Decline and Pesticides

Densities of Atlantic salmon and brooktrout were followed for a year after spraying. One month after spraying, the densityof Atlantic salmon rearing in the area ofhighest application had decreased substantially. Brook trout populations did notshow as great a decrease. It was felt thatthe reduced density of the Atlantic salmon
was due to migration from the area in
response to a reduced food supply.
Insect larvae and crustaceans are very
sensitive to many types of pesticides, reducing the availability of these organisms tofish as prey (Macek et al. 1976; Brown 1978;
Muirhead-Thomson 1987). Experimental
spraying of ponds with carbaryl to simulate
overspraying for spruce budworm control
resulted in massive mortality of aquatic
invertebrates (Muirhead-Thomson 1987).
Some species of amphipods were not found
for three years after the spray event (Gibbs
et al. 1984). Walker (1964) found no fishmortality after application of 2-6 ppm ofatrazine, a common herbicide, to ponds but
insect larvae were killed immediately.

insects, while the predatory insect population was unaffected. She suggested that thedecrease in nonpredatory insects was due
to a reduction of algae and plants used asfood and a reduction of water plants used
as habitat for the insects. Further study ofthe fish populations indicated that the
reproduction of bluegills was greatly reduced, probably from a lack of food. The
stomach contents of the bluegills in thetreated ponds were significantly lower thanthose in the control ponds (Kettle et al.
1987). Populations of young bluegills were
further reduced by the lack of aquaticvegetation in which to hide. Without theaquatic vegetation, the young were preyed
upon by the adult bluegills (Kettle et al. 1987).
At present, we have no information onwhether deleterious effects of pesticides toalgae (Stadnyk et al. 1971; Brown 1978;
Bester 1995) or diatoms (Menzel et al. 1970;
Brown 1978) may have trickle-down effects
on salmonid populations, although it seems
likely that they would be subject to population dynamic forces similar to those demon-

In experimental treatments of replicate
ponds with atrazine, deNoyelles et al.
(1989) found that phytoplankton andaquatic plants were reduced by as much as
95% at the higher concentrations. Zooplankton did not seem to be directly affected.
However, several months later, zooplankton populations also were reduced(deNoyelles et al. 1982). In the same study
on atrazine, Dewey (1986) reported a decrease in the number of nonpredatory

NEVA HASSANEIN

Pesticides may also indirectly affectprey species. Aquatic herbicides kill algaeand diatoms on which aquatic insect larvae
feed, thereby reducing the number ofaquatic insects and decreasing growth andsurvival of fish feeding on the insects(Brown 1978).

The integrity of aquatic ecosystems is essential for
healthy salmon populations.

37

Diminishing Returns: Salmon Decline and Pesticides(Beitinger 1990; Birge et al. 1993). Brown
strated with bluegills. Interference with
(1978) found that application of the herbigrowth of salmonids, however, has deletericide paraquat caused death and decomposious effects on smolting (Ewing et al. 1980),
tion of aquatic plants which in turn lowered
immune function (Tatner 1996), predation
the oxygen content(Parker 1971),
of the water enoughseaward migration
to kill trout.
(Wedemeyer et al.
Increased predation on small fish may
1980), and seawater
occur when water plants are killed by
These results
adaptation (Folmar
herbicides
intheaquatic
environment.
and others of simiand Dickhoff 1980;
lar nature (Brown
Mahnken et al.
1978; Muirhead1982).
Thomson 1987) indicate that disruption of
the food chains in aquatic ecosystems can
In addition to interference with their
have relatively long-lasting effects on fish
food supply, pesticides may also affect the
populations. In complex ecosystems,
habitat of the fish. Increased predation on
indirect effects can be more important
small fish may occur when water plants arethan direct effects (Lampert et al. 1989)
killed by herbicides in the aquatic environand non-target organisms may be better
ment (Lorz et al. 1979; Kettle et al. 1987).
indicators of ecosystem health than theAdverse water temperatures may resultorganisms of interest. Management offrom the removal of riparian vegetation bypesticide applications for protection ofherbicides (Norris et al. 1991). Fish may
aquatic habitats is obviously much more
avoid contaminated areas with a consecomplex than promoting the use of LC50s
quent reduction in availability and suitabilfor setting application limits.
ity of feeding and spawning areas

38

Diminishing Returns: Salmon Decline and Pesticides

Conclusions
Salmonids require coordinated responses to environmental stimuli andinternal physiological reactions for healthy
development, territorial defense, smolting,seaward migration, and adaptation toseawater. Interruptions of this interplay
may cause inappropriate physiologicalresponses that have deleterious effects on
survival of the salmon. As we have shown
here, sublethal concentrations of pesticides
can cause such interruptions and therefore

result in harmful changes in physiology
and behavior. The wide array of effects thathave been demonstrated is cause for concern (Table 3).
The magnitude of the problem frompesticides is difficult to assess because of
the lack of monitoring programs for the use
and distribution of pesticides. Yet, wherewater quality monitoring has been done,
pesticides are usually detected. A recent
report commissioned by the Oregon Legislature (Botkin et al. 1995:104) concluded
that fertilizers and pesticides were detri-

Table 3. Sublethal effects of selected pesticides found in the
Willamette River Basin Study by USGS.1__________________________________________________________________________________________________________
Herbicides
Insecticides
Atrazine
Simazine
Malathion
Chlorpyrifos
Carbaryl____________________________________________________________________________________________________________
Negative Effects on:
Food Supply
GrowthReproductive success
Bone Abnormality
Endocrine Disruptor
Immune System
Behavior
Schooling
Predator Avoidance

+2
+2
+2

+3
+6

+16
+20

+11
+14
+15
+17,18

+4
+7
+9
+12

+5
+8
+10
+13
+13,14+12,17

+12
+19

+18

____________________________________________________________________________________________________________________
Plus indicates a detectable response from sublethal concentrations of pesticide. Blanks indicate thatstudies were not found analyzing these effects. Superscripts are references.
1. Anderson et al. 1997.
2. Macek et al. 1976.
3. Naqvi and Hawkins 1989.
4. Washino et al. 1972.
5. Burdick et al. 1960.
6. Hermanutz 1978.
7. Brazner and Kline. 1990.
8. Arunachalam and Palanichamy 1982.
9. Jarvinen et al. 1983.
10. Carlson 1971.

11. Weis, P. and J. S. Weis. 1976.
12. Holcombe et al. 1982.
13. Weis, J. S. and P. Weis. 1976.
14. Bruckner-Davis 1998.
15. Plumb and Areechon. 1990.
16. Dodson and Mayfield. 1979b.
17. Hansen 1969.
18. Hansen 1972.
19. Weis, P. and J. S. Weis. 1974.
20. Lorz et al. 1979.

39

Diminishing Returns: Salmon Decline and Pesticides

mental to salmon: “With such large applications of pesticides and fertilizers, some
portion is sure to make its way into nearby
streams, especially since most agriculturalland lies in close proximity to streams andrivers. Since little monitoring is done to detect
the presence of pesticides and fertilizers instreams, the levels of exposure by fish to chemicals are largely unknown (authors’ emphasis).”Certain facts about pesticides in theenvironment are known and reviewed
briefly here:• Pesticides are typically found in great
variety in salmonid habitats.
• Pesticides break down into productsthat may be less toxic, of equal toxicity, orof greater toxicity than the original compounds.
• Fish and other aquatic organisms
must continue to cope daily with a varietyof pesticides or breakdown products whichwere used years ago but remain in aquatic
environments.

sensitive population thwarts our efforts torecover wild salmonids.
In contrast to these dramatic fish kills,
sublethal concentrations of pesticides are
more subtle and their effects are largely
unseen. From laboratory experimentation,
researchers have found that sublethal
concentrations of pesticides can affect many
aspects of salmonid biology, including
swimming performance, predator avoidance, temperature selection, schoolingbehavior, seaward migration, immunity todisease, reproduction, and food supply.
Specifically, the literature reviewed here
shows that:• A variety of pesticides impair
swimming performance which can reducesuch critical behaviors as the ability to feed,
to avoid predators, to defend territories,
and to maintain position in the river system.
• Chronic exposure to certain pesticides can increase stress in juvenile salmonids and thereby render them more susceptible to predation.

• In a process known asbioaccumulation, pesticides absorbed intoplant and animal tissues may become
concentrated and reach levels many times
higher than the concentrations in the surrounding water.
The levels of pesticides encountered instreams and rivers have occasionallyreached lethal concentrations for salmonids,
as evidenced by the major fish kills thathave occurred in the Rogue River Basin andelsewhere. Loss of each individual in a
40

OREGON DEPT. OF FISH AND WILDLIFE• Pesticides move in streams and rivers
throughout the watersheds and may pose
problems far from the site of application.

Diminishing Returns: Salmon Decline and Pesticides

OREGON DEPT. OF FISH AND WILDLIFE

however there is a need for further researchin this area, placing particular emphasis on
the critical period of transition that takes
place in the estuary.
• As with other pollutants, pesticides
may interrupt the spawning migrations ofadult salmon by interfering with the timingof migration and by draining energy
reserves.

Pesticides can affect salmon biology at many stages
in their development.

• Pesticides can suppress the normal
functioning of the immune system, resulting in a higher incidence of disease.

• Several pesticides have been shownto cause fish to seek abnormal water temperatures, thus subjecting them to increased dangers of disease and predation.

• Certain pesticides can act as hormone
mimics or blockers, causing abnormal
sexual development, feminization of males,
abnormal sex ratios, and abnormal mating
behavior.

• Many pesticides interrupt normal
schooling behavior of salmon, a critical tactic
for avoiding predation during migration.

• Pesticides can interfere with otherhormonal processes, such as normal thyroid
functioning and bone development.

• Several herbicides have been shownto inhibit normal seawater migration patterns; however, there is a dearth of researchlooking at this effect for common insecticides.

• Fishes and other organisms areespecially vulnerable to endocrine-disrupting effects during the embryonic and early
development stages of life.

• Several studies suggest that certain
pesticides can impair salmonids’ ability totransition from fresh water to sea water;• Pesticides can indirectly affect salmonids by altering the aquatic habitat andfood supply for salmonids.

41

Diminishing Returns: Salmon Decline and Pesticides

The Ecoepidemiological Approach
An extensive literature on the effects of synthetic chemicals on survival, physiology andreproduction of fishes is available (Murty 1986). The literature is disparate, however, andlargely fails to attribute causality to events occurring in particular aquatic ecosystems. A new
approach to appreciate the dangers pesticides pose for salmonids may be necessary. One
method that has proved useful to establish the relationship between chlorinated hydrocarbon
concentrations and the decrease in lake trout populations in the Great Lakes is the applicationof principles borrowed from epidemiology (Mac and Edsall 1991).
Epidemiology is the medical science used to determine the causes of disease in a particular population when many confounding factors are present simultaneously. The subdisciplineused for examining environmental health hazards to wildlife populations is calledecoepidemiology (Morgenstern and Thomas 1993). In epidemiology, researchers form acentral hypothesis about the cause of an outbreak of a disease. The validity of the central
hypothesis is then tested by five criteria, as illustrated by Mac and Edsall’s (1991) study of theGreat Lakes’ trout.
The hypothesis in Mac and Edsall’s study was that large concentrations of chlorinatedhydrocarbons were responsible for the reduced reproductive success in populations of lake
trout. The first criterion is that the problem must be temporally related to the appearance ofthe causative agent. In the Great Lakes, during the period 1975 to 1988, survival of trout eggs
improved significantly as concentrations of PCBs, DDT, and oxychlordane declined. The
second criterion is that there must be a strong correlation between exposure to the hypothetical agent and the disease. In a study of egg and fry survival at different locations, the extent
of egg and fry loss was directly proportional to the concentration of PCBs in the water and infemale fish at each location. Thirdly, the causative agent must be shown to induce the disease.
Tests done in various laboratories established that PCBs could decrease egg and fry survival.
Fourth, the observed cause-effect relationship must be shown in repeated studies. Comparison of different species at the same time, the same species at different times, and the same
species at different locations established that reproductive impairment correlated with PCB
exposure. Finally, there must be a biological plausibility of the relationship between thecausative agent and the symtoms. Laboratory studies of tissue histology, exposure to otherchlorinated hydrocarbons, and studies of enzyme induction were all consistent with the
hypothesis that PCBs and chlorinated hydrocarbons were impairing egg and fry survival.
The authors concluded that their hypothesis was strongly supported, although they pointout that “much of this evidence is circumstantial with little definitive proof of causality, which
is why the epidemiological approach is used” (Mac and Edsall 1991). In other words, thestrength of the ecoepidemiological approach is that it involves trying to understand relationships between environmental contaminants and population survival in real-world settings
where a host of factors come into play. Restrictions on the use and dumping of organochlorine compounds into the Great Lakes resulted in partial restoration of the lake trout populations.

42

Diminishing Returns: Salmon Decline and Pesticides

Recommendations

1. Address the impacts of pesticides
on salmon when developing and implementing recovery plans for threatened
and endangered species. As federal, state,provinicial, and local agencies work torecover salmon in the Pacific Northwest,
all factors contributing to the decline
should be addressed. To date, pesticides
have been overlooked as a factor deserving
attention in our recovery efforts. Although there is a need for more information on the effects of pesticide use insalmon habitats, our salmon runs may be
extinct by the time lengthy and laborious
studies using strict scientific methods arecomplete. Thus, we must act now using
available information to formulate management strategies that will minimize thepotential danger from sublethal concentrations of pesticides.
2. Conduct ecoepidemiological studies in critical salmonid habitat. Most of
the effects of pesticides referred to in thisreport have been determined in experimental laboratories. In the field, however,environmental conditions are not controlled, and many factors interact to confuse the determination of direct relationships. An ecoepidemiological approach(see inset opposite page) would be particularly valuable because it is designed toattribute causality to events occurring inreal-world situations. This approachrequires data which are not currently being

INSTITUTE FOR FISHERIES RESOURCES

From the evidence available at present,
it can be concluded that there is a plausible
basis for considering pesticides as one
causative factor in the decrease of salmon
populations. Based on this review, we offer
several policy recommendations andidentify areas for further research:

We must act now to protect salmon from pesticides.

collected. In particular, ecoepidemiologicalstudies at the watershed level require
specific pesticide use information in orderto establish correlations between salmon
decline and pesticide use.
3. Create comprehensive pesticidetracking systems in the Pacific Northwest.
To better understand the relationshipbetween pesticides and salmon decline,
we must have accurate, site-specific dataon the patterns of pesticide use in thewatersheds of the Northwest. State andprovincial governments need to collectdata on which pesticides are used where,
when, and in what amounts. Such data
can then be combined with watershedspecific information on a host of physiological and behavioral indicators of
salmon health. (Currently, California is
the only state with salmon habitat wheresuch information is collected.) Pesticide
use information will also enable efficient
instream monitoring for pesticidecontamination.
43

Diminishing Returns: Salmon Decline and Pesticides

4. Establish instream monitoring
programs in critical salmon habitats. A
systematic monitoring program for pesticides and their breakdown products needs
to be undertaken. Clearly, not all pesticides
can be tested for in all locations, but current
testing is woefully inadequate for understanding the role of pesticides in salmon
decline. In conjunction with pesticide use
information, these analyses can be targetedto the compounds of most concern. Suchtargeting can greatly improve the costeffectiveness of monitoring.
5. Err on the side of caution whensetting water quality standards for pesticides. As discussed in this report, there arefew established criteria for the protection of
aquatic life from pesticides. Moreover,evidence reviewed here shows that sublethal effects on salmonids have not been
fully appreciated, that juvenile salmonids
succumb more easily to toxins in the water,that laboratory studies do not reflect thenatural life cycle of the fish, and that little is
known about how pesticides affect aquatic
ecosystems. These factors must be considered when setting standards, and a precautionary approach must be adopted. Muchcan be gained by emphasizing how toeliminate the introduction of these toxic
substances into the watersheds that comprise critical salmonid habitat.

44

6. Prevent pesticide contamination of
salmonid habitat by reducing pesticideuse. Once contaminated, water is difficult
if not impossible to clean up. Therefore,
pest management approaches that do notdepend on pesticide use in agricultural andnon-agricultural settings should be encouraged and further developed. There is
ample evidence that ecologically sound andeconomically viable methods can be successfully implemented. The adoption ofsuch alternatives can be encouraged
through technical assistance, financial
incentives and disincentives, demonstration
programs, and information exchange opportunities.
7. Adopt state and provincial programs in the Pacific Northwest to phaseout pesticides that persist andbioaccumulate in the environment.
Numerous pesticides, including some thatare no longer used and many that are
currently used, are known to persist in
the environment and to bioaccumulate inaquatic systems. Washington State’s
Department of Ecology is now considering a plan to end the release of suchtoxins, including certain pesticides, into
the environment. To ensure salmon recovery, all state and provincial governments in the Pacific Northwest should
adopt similar programs.

Diminishing Returns: Salmon Decline and Pesticides

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Diminishing Returns: Salmon Decline and Pesticides

Glossary, Abbreviations
and Scientific Names
2,4-D — 2,4-dichlorophenoxyacetic acid. A
herbicide that mimics natural plant
hormones.
DDT — dichlorodiphenyltrichloroethane.
An insecticide widely used in the past but
now illegal in the United States.

lent to milligrams per liter (mg/L).
Pesticide — anthropogenic chemicals used
for control of target organisms. These include insecticides, herbicides, fungicides,
and other biocides.
Redd — a depression dug in the streambed
gravel in which salmonids lay their eggs.
Salmon, Atlantic — Salmo salar

DDE — dichlorodiphenylethane. A longlived breakdown product of DDT.

Salmon, chinook — Oncorhynchus
tshawytscha

Eulachon — Thaleichthys pacificus

Salmon, coho — Oncorhynchus kisutch

Euryhaline — the ability to tolerate wide
ranges of salinity. Euryhaline fish are often
found in estuaries where the salinities canrange from fresh water to seawater.

Salmon, sockeye — Oncorhynchus nerka

Gonopodium — front rays of the anal fin of
livebearing fish (Family Poeciliidae) areelongated to form an organ that assists ininternal fertilization.
IHN virus — infectious hematopoetic
necrosis virus, a major cause of mortalities
in Columbia basin salmonids
Lamprey, Pacific — Lampetra tridentata

Shad, American — Alosa sapidissima
Smolt — a juvenile salmonid characterized
by a uniform silvery color. Fish at this stage
undergo a number of physiologicalchanges, lose their ability to hold territories,
tend to school, and begin migration toward
the sea.
Steelhead — Oncorhynchus mykiss, a migratory form of rainbow trout

Minnow, fathead — Pimophales promelas

Surfactant — a chemical added to formulations of pesticides to reduce surface tension
and cause wetting by the pesticide solution.

Mosquitofish — Gambusia sp.

TCDD — 2,3,7,8-tetrachlorodibenzo-dioxin

Parr — a juvenile salmonid characterized
by vertical bars, or parr marks, along its
sides. Fish at this stage are brownish incolor and hold territories in the stream.

TCMTB — 2-(thiocyanomethythio)benzothiazole, an antisapstain fungicide
used on timber to be exported.
Trout, brook — Salvelinus fontinalis

Ppb — parts per billion; a concentration ofpesticide equal to one gram of the compound dissolved in a billion grams of water.
Equivalent to micrograms per liter (µg/L).
Ppm — parts per million; a concentration ofpesticide equal to one gram of the compound
dissolved in a million grams of water. Equiva52

Trout, brown — Salmo trutta
Trout, cutthroat — Oncorhynchus clarki
Trout, lake — Salvelinus naymaycush
Trout, rainbow — Oncorhynchus mykiss

For more information…
Northwest Coalition for Alternatives to Pesticides
P.O. Box 1393
Eugene, OR 97440-1393(541) 344-5044; fax (541) 344-6923
www.efn.org/~ncap
Oregon Environmental Council
520 SW 6th Ave., Suite 940
Portland, OR 97204(503) 222-1963; fax (503) 222-1405
www.orcouncil.org
OSPIRG Foundation
1536 SE 11th Ave.
Portland, OR 97214(503) 231-4181; fax (503) 231-4007
www.pirg.org/ospirg
Institute for Fisheries Resources
PO Box 11170
Eugene, OR 97440-3370(541) 689-2000; fax (541) 689-2500
www.pond.net/~fish1ifr