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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 Americaas 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, NormaGrier, Neva Hassanein, Jacob Kann, Maureen Kirk, Becky Long, Kay Rumsey, Glen Spain, and LauraWeiss.

We also value the following individuals and agencies who contributed photos and graphics that arereproduced here with permission: Nancy Allen of Corvallis Environmental Center, K. Born, AndyDuncan 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 supportingfoundations and individuals.

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

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Diminishing Returns: Salmon Decline and Pesticides

Diminishing Returns:Salmon Decline and Pesticides

By Richard D. Ewing, PhDFebruary 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 CoralGables in 1968. After conducting research at Oak Ridge National Laboratory and at OregonState 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 leftODFW to form Biotech Research and Consulting, Inc., a Corvallis-based consulting companythat specializes in hatchery operations and chemical analyses relating to fisheries. Dr. Ewinghas published widely in professsional journals and written many reports for the Oregon De-partment of Fish and Wildlife.

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Table of ContentsExecutive 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 ........................................................................... 52

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ExecutiveSummary

Pacific salmon are in serious trouble.The enormous runs of migratory salmon ofthe past have slowly diminished to thetrickle of adult spawning salmon thatpresently inhabit western rivers. Althoughsalmon recovery efforts are underway,scientists, policy makers, and interestgroups have thus far given insufficientattention to the role that pesticide contamina-tion of our watersheds may play in salmondecline. Accordingly, the purpose of Dimin-ishing Returns: Salmon Decline and Pesticides isto review scientific literature on the effects ofsublethal concentrations of pesticides onsalmonids (see full report for documenta-tion and references). The report placesspecial emphasis on how pesticides canalter the biology of fishes in subtle waysthat decrease their chances for reproductionand survival.

Dynamics of Pesticides in theEnvironment

Pesticides include a broad class ofchemical and biological agents that arepurposefully introduced into the environ-ment to kill or damage organisms, includ-ing insecticides, herbicides, and fungi-cides. Once applied, pesticides move intostreams and rivers throughout water-sheds and may pose problems far fromthe site of application. Movement oftenoccurs through the medium of water,thereby exposing all aquatic organismsduring this transport. Where water qual-ity monitoring has been done, a greatvariety of pesticides are typically found insalmon habitat. Federal and state agen-cies have established few criteria or stan-

dards for the protection of aquatic lifefrom short-term (acute) and long-term(chronic) exposure to pesticides.

Pesticides do not necessarily disappearwith time. They transform into other com-pounds that may be less toxic, of equaltoxicity, or of greater toxicity than theoriginal compound. The toxicity of thesebreakdown products is not well under-stood, and in general how they affectaquatic life has not been studied. All thewhile, fish and other aquatic organismsmust 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 knownas bioaccumulation, pesticides absorbedinto plant and animal tissues may becomeconcentrated and reach levels manytimes higher than those in surroundingwater.

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Fish Kills and Acute Toxicity ofPesticides to Salmon

Pesticides are capable of killing salmonand other aquatic life directly and within ashort period of time. For example, in 1996the herbicide acrolein was responsible forthe death of approximately 92,000 steel-head, 114 juvenile coho salmon, 19 residentrainbow trout, and thousands of nongamefish in Bear Creek, a tributary of the RogueRiver. Deaths of threatened and endan-gered species from accidental contamina-tion of waterways are of grave concern.The loss of each individual in a sensitivepopulation makes recovery efforts thatmuch more difficult. Fortunately, thesedeaths are relatively infrequent.

Behavioral Effects of Pesticidesat Sublethal Concentrations

In contrast to dramatic fish kills, theeffects of sublethal concentrations of pesti-cides are more subtle and go largely unseenand unregulated. Sublethal concentrationsof pesticides do not cause immediate death,but can interfere with the biology of theorganism in other ways and can ultimatelyimpact the survival of the species. Labora-tory studies show that sublethal concentra-tions of pesticides can affect many aspectsof salmon biology, including a number ofbehavioral effects:

• Long-term exposure to certainpesticides can increase stress in juvenile

salmonids and thereby render them moresusceptible to predation.

• Certain pesticides can alter swim-ming ability, which in turn can reduce theability to feed, to avoid predators, to defendterritories, and to maintain position in theriver system.

• Many pesticides interrupt schoolingbehavior, a critical tactic for avoiding pre-dation during salmon migration. Disrup-tion of schooling behavior is thought bysome researchers to be a classic method forexamining sublethal effects of pesticidesbecause the effect is so common.

• Several pesticides (and other pollut-ants) have been shown to cause fish to seeksuboptimal water temperatures, thus sub-jecting them to increased dangers of diseaseand predation.

• Some herbicides have been shownto inhibit normal migration to the sea,resulting in severe disruption of the lifecycle. There is a dearth of research lookingat this effect for common insecticides.

• Several studies suggest that certainpesticides 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 migrationpatterns to avoid polluted areas, resultingin delayed spawning.

Compromised Immune Systems

In addition to changes in behavior,exposure to relatively low concentrations of

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pesticides can disrupt the immune systemof salmon. Evidence for these effects insalmonids is not as extensive as for disrup-tion of behavior, but the data availablesuggest that pesticides can have seriousnegative impacts on the immune system.Such disruption results in the onset ofdisease and even death.

Endocrine Disruptors

Fish and other organisms are especiallyvulnerable to endocrine-disrupting effectsduring the early stages of development.Pesticides at low concentrations may act asmimics or blockers of sex hormones, caus-ing abnormal sexual development, femini-zation of males, abnormal sex ratios, andunusual mating behavior. The uniqueplasticity of sex differentiation in fish sug-gests that these animals may be very sus-ceptible to disruption of sexual characteris-tics by pollutants. Pesticides can also inter-fere with other hormonal processes, such asthyroid functioning and bone development.

Indirect Effects of Pesticides onSalmon

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

ceptibility to predation. These indirecteffects are subtle, but evidence suggeststhat in complex ecosystems indirect effectscan be even more important than directeffects.

Recommendations

From the evidence available at present,there is a plausible basis for consideringpesticides to be one of the causes of declin-ing salmon populations in the PacificNorthwest. Based on this review, we offerseveral policy recommendations and iden-tify areas for further research:

1. Address the impacts of pesticideson salmon when developing and imple-menting recovery plans for threatened andendangered species. To date, efforts torecover salmon have devoted insufficientattention to pesticides as a contributingfactor in salmon decline. We must act nowusing available information to formulatemanagement strategies that will minimizethe potential danger from sublethal concen-trations of pesticides.

2. Conduct ecoepidemiological stud-ies in critical salmonid habitat. Most ofthe effects of pesticides referred to in thisreport have been determined in experimen-tal laboratories. In the field, however,environmental conditions are not con-trolled, and many factors interact to confusethe determination of direct relationships.Ecoepidemiological investigations in theGreat Lakes have established the relation-ship between chlorinated hydrocarbons andthe decrease in lake trout populations. Anecoepidemiological approach for salmon inthe Pacific Northwest would be particularlyvaluable because it is designed to attributecausality to events occurring in real-worldsituations.

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3. Create comprehensive pesticidetracking systems in the Pacific Northwest.To better understand the relationship be-tween pesticides and salmon decline, wemust have accurate, site-specific data on thepatterns of pesticide use in the watershedsof the Northwest. State and provincialgovernments need to collect data on whichpesticides are used where, when, and inwhat amounts. Such data can then becombined with watershed-specific informa-tion on indicators of salmon health. (Cur-rently, California is the only state withPacific salmon habitat where such informa-tion is collected.) Pesticide use informationwill also enable efficient instream monitor-ing for pesticide contamination.

4. Establish instream monitoringprograms in critical salmon habitats. Asystematic monitoring program for pesti-cides and their breakdown products needsto be undertaken. Not all pesticides can betested for in all locations, but current testingis woefully inadequate for understandingthe role of pesticides in salmon decline. Inconjunction with pesticide use data, theseanalyses can be targeted to the compoundsof most concern. Such targeting can greatlyimprove the cost-effectiveness of monitoring.

5. Err on the side of caution whensetting water quality standards for pesti-cides. There are few established criteria forthe protection of aquatic life from pesti-cides. Moreover, evidence reviewed here

shows that sublethal effects on salmonidshave not been fully appreciated, that juve-nile salmonids succumb more easily totoxins in the water, that laboratory studiesdo not reflect the natural life cycle of thefish, and that little is known about howpesticides affect aquatic ecosystems. Thesefactors must be considered when settingstandards, and a precautionary approachmust be adopted.

6. Prevent pesticide contamination ofsalmonid habitat by reducing pesticideuse. Once contaminated, water is difficultif not impossible to clean up. Therefore,pest management approaches that do notdepend on pesticide use in agricultural andnon-agricultural settings should be encour-aged and further developed. There isample evidence that ecologically sound andeconomically viable methods can be suc-cessfully implemented. The adoption ofsuch alternatives can be encouragedthrough technical assistance, financialincentives and disincentives, demonstrationprograms, and information exchange op-portunities.

7. Adopt state and provincial pro-grams in the Pacific Northwest to phaseout pesticides that persist andbioaccumulate in the environment. Nu-merous pesticides, including some that areno longer used and many that are currentlyused, are known to persist in the environ-ment and to bioaccumulate in aquaticsystems. Washington State’s Department ofEcology is now considering a plan to endthe release of such toxins, including certainpesticides, into the environment. To ensuresalmon recovery, all state and provincialgovernments in the Pacific Northwestshould adopt similar programs.

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IntroductionSalmon are a keystone species for

Northwest ecosystems. Entire foodchainsbase their existence on the proliferation ofsalmon and trout that surge from the seainto streams and rivers, work their wayupstream to their natal spawning areas, laytheir eggs, and die, providing a source ofnutrients for the very organisms that laterfeed the salmon’s progeny.

Salmon andtrout make up thefamily Salmonidae, agroup of fish charac-terized by an adi-pose fin located nearthe tail. These fishrequire clean, coldfresh water for muchof their life history.Because such habitatis low in nutrients,salmon and many ofthe trout developed anadromy, a behaviorpattern in which the juveniles migrate tothe sea. In the sea, the juvenile fish use richocean productivity for feeding and growth,then return to the streams where they wereborn to lay their eggs.

Today, migratory salmon and trout arefighting for their survival. The enormousruns of migratory salmonids in the 1860shave slowly diminished to the trickle ofadult spawning salmon that presentlyinhabit western rivers. The causes for thedecline are many, some of which are welldocumented. Yet, in their recovery effortsfor threatened populations, scientists,policy makers, and interest groups havetended to overlook the role of pesticidesthat flow daily through salmon habitat,potentially changing the biology of the fish

in subtle ways that decrease their chancesfor 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 bufferstrips along streams). Insufficient attention,however, has been devoted to the use andpresence of pesticides in the watersheds andthe role this water quality degradation playsin salmon decline. Accordingly, the purposeof this report is to present information from

scientific literaturethat points to theunseen dangerposed by theexistence of pesti-cides in salmonidhabitats.

Pesticidesinclude a broadclass of chemicaland biologicalagents that are

purposefully applied to the environment tokill or damage organisms (National Re-search Council 1993). These agents areused in a wide range of occupations for avariety of purposes. Foresters use herbi-cides to keep broadleaf plants from compet-ing with conifer seedlings, and insecticidesto deal with numerous insect pests thatdamage forests. Farmers use insecticides toprotect their crops and keep insects awayfrom their livestock, and herbicides toremove unwanted weeds from fields andwaterways. State and local agencies useherbicides to remove brush from roadsides.Fishermen use defouling compounds liketributyltin to keep organisms from settlingon the hulls of their boats. The ordinaryhomeowner uses a wide variety of pesti-cides: herbicides on the lawn, insecticideson pets, and fungicides in house paint.

Rivers and streams have become greatconduits through which pesticides,either intact or as breakdown products,flow to the sea. Salmon now livethroughout their life cycle with theseresidues as part of their dailyenvironment.

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Chinook Salmon (ocean-rearing)• Distribution includes coast and Columbia Basin mainstem

rivers.• 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 the

spring, 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.

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 monthsover the summer before fall spawning.

• They spawn in concentrations on gravel bars in uppertributaries.

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 on

large 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 theymay not migrate at all.

• Those that do go to the ocean migrate out in the spring, stayonly a few months close to shore, then return in the fall.

• The ones that migrate may rear in fresh water for several

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. Thespawning age of cutthroats seems to vary over their distribu-tion area.

• Cutthroat prefer the smallest, highest tributaries in a basin.

Coho Salmon• Juveniles rear throughout watersheds and tend to live in pools

in 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 in

upper watersheds.• Most adults spawn when they are 3 years old.

Sockeye/Kokanee Salmon• There is both an ocean-going form (called sockeye), and a

resident 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 to

lakes. Kokanee are thriving in some lakes.

Steelhead• There are two subspecies of steelhead in Oregon. Each

also has a resident form. Coastal steelhead are closelyrelated to rainbow trout. Inland steelhead are closelyrelated to redband trout.

• Most juveniles rear in fresh water for 1 or 2 years and migrateto the ocean in the spring.

• Most steelhead spend 2 years in the ocean. Theirdistribution is poorly known but appears to be further off-shore than other salmon.

• Most inland steelhead return to fresh water in the summerwhile 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.

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Once applied, pesticides can moveaway from the point where they were used.As a result, rivers and streams have becomegreat conduits through which pesticides,either intact or as breakdown products,flow to the sea. Salmon now live through-out their life cycle with these residues aspart of their daily environment.

This report reviews our existingscientific knowledge of the effects of pesti-cides on salmonids, placing a special em-phasis on sublethal effects of pesticides.Sublethal effects are those that result fromexposure to a pesticide in an amount that isnot high enough to cause death, but candamage an organism in other ways, includ-ing physiological and behavioral changesthat can ultimately impact the survival ofthe species. These effects can occurthroughout the entire life history of salmo-nids, from hatching of eggs, entry ofjuveniles into the ocean, and return of

adults for spawning. With the data cur-rently available, it is possible to identify keyareas that need immediate attention.

The present report emphasizes researchperformed on salmonids. Most of thestudies included here, however, have beendone with rainbow trout, which are foundthroughout the United States, are relativelyeasy to grow, and provide a reasonablestandard for examining physiological andbehavioral changes. Fewer studies weredone with anadromous (seagoing) salmon.Where this research exists, the informationis emphasized. Studies from other speciesof fish are introduced when certain pointsneed to be made and information is notavailable from salmonid research.

The data suggest there is a plausiblebasis for considering pesticides as acausative factor in salmon populationdeclines.

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Dynamics ofPesticides in theEnvironment

Pesticides are Ubiquitous inWestern Watersheds

In 1991, the U. S. Congress providedfunds for the U. S. Geological Survey toconduct a National Water-Quality Assess-ment (NAWQA) on major river systems inthe United States. The study units chosenencompass sources of drinking water forabout 70 percent of the U. S. population. Inthe Northwest, study units included thePuget Sound and the central Columbia

River plateau of Washington, theWillamette River Basin of Oregon, theSacramento and San Joaquin River systemsof California, and the Snake River Basin ofIdaho. Table 1 presents the numbers ofpesticides detected in streams and thenumbers of pesticide detections that exceedcriteria for aquatic life.

A major problem with the interpreta-tion of the data presented in Table 1 is thatconcentrations of pesticides compatiblewith aquatic life are not well defined. TheU.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 the118 pesticides typically looked for in waterquality 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 # Pesticides # Exceeding # For WhichExamined Detected Aquatic Life Aquatic Life

Criteria1 CriteriaAre Available

_______________________________________________________________________________________________

Oregon Willamette Basin2 86 36 4 22Washington Puget Sound Basin3 NA 23 4 NA Central Columbia 84 45 5 18 River Plateau4

California San Joaquin Basin5 83 49 7 16Idaho 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 bythe Canadian Council of Resources and Environment Ministers.

2 Data from Anderson et al. (1997).3 Data from Bortleson and Davis (1997).4 Data from Wagner et al. (1996).

5 Data from Dubrovsky et al. (1998).6 Data from Clark et al. (1998).

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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 lifecriteria for only 6 insecticides (Larson et al.1997). EPA has not established any aquaticlife criteria for the herbicides and fungi-cides 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 wasbased on acute toxicity data but did nottake into account bioaccumulation, suble-thal effects, or synergistic effects.

The EPA and NAS/NAE criteria arecommonly used as indicators of the degreeof water pollution, but, as we shall see, maybe far higher than the levels at which dam-age to fish can occur.

From the NAWQA studies, one can seethat pesticide use is prevalent in our water-sheds, and the water in our river basinscontains dozens of pesticides. Exactly whathappens to the hundreds of tons of pesti-cides put on the land each year?

Pesticides Persist in theEnvironment and Degrade intoToxic Products

Most pesticides undergo chemicaltransformations after application (Day1991). The transformations may result fromeither physical processes, such as oxidationor photolysis, or biological metabolism bymicrobes. The breakdown products maybe less toxic, of equal toxicity, or more toxicthan the original compound. In manycases, the breakdown products of pesticidesare not completely understood and theirtoxicities 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 con-cluded that the pesticide has been clearedfrom the system. However, the breakdownproducts 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 shortlyafter application. However, experimentshave shown that glyphosate may persist inthe environment for as long as 3 years(Torstensson et al. 1989). Its metabolite,AMPA, may persist even longer (WorldHealth Organization 1994). Glyphosate is

Figure 1Number of pesticides with

aquatic life criteria.

(Based on 118 pesticides typically looked forin water quality studies)

Source: Larson et al. (1997)

Pesticideswith criteria

20(17%)

Pesticideswithout waterquality criteria

98(83%)

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typical of many pesticides in that its break-down is dependent upon the environmentalconditions in which it is used and that thetoxicity of its breakdown products is equalto or greater than the toxicity of glyphosateitself.

The rate at which a pesticide breaksdown varies widely, depending upon theconditions of application. Degradationdepends largely upon temperature. Pesti-cides such as glyphosate may oxidize in aslittle as 3 days in Texas or as long as a yearin Canada. Conditions that favor microor-ganisms also tend to promote pesticidedegradation (Barbash and Resek 1996),although in some cases, the presence of

humic material in the soil stabilizes thepesticide (Chapman et al. 1981; Barbash andResek 1996). Light and water are alsoimportant in the degradation of pesticides(Barbash and Resek 1996). Pesticides breakdown more quickly under bright sunshinethan under cloud cover. Breakdown occursmore quickly under moist conditions thanunder dry conditions. Oxygen concentra-tion is also important for metabolism ofpesticides. For example, pesticides areresistant to breakdown in the anoxic, highlyreducing muds of estuaries where there isan absence of oxygen (Barbash and Resek1996).

In short, the timing of degradation ofa pesticide is highly variable and depen-

dent upon environmental conditions.Pesticides may remain in the environmentmuch longer than expected or claimed,and the breakdown products may also betoxic 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 agostill appear in water quality surveys.One aspect of pesticide degradation isquite clear. Pesticides and their metabo-lites do not magically disappear from theenvironment.

Pesticides Move throughoutWatersheds

Water promotes the transport of pesti-cides from their site of application (seeFigure 2). Streams are often the recipients ofpesticide residues following rainfall. Butthe rapid downstream transport of chemi-cals by streams and rivers does not meanthat pesticides have no effects on a varietyof organisms living in the area of applica-tion. Pesticides in streams typically reachhigh levels for short periods of time afterapplication, then decrease to very low orundetectable levels. During the brief pe-riod of high concentration, damage to

Pesticides may remain in theenvironment much longer thanexpected or claimed, and thebreakdown products may also betoxic to organisms.

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Pesticide residues move readily into streams andrivers following rainfall.

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organisms in the stream may occur. Fishand wildlife at early stages of developmentare particularly vulnerable. Brief exposuresto toxic materials at early stages in develop-ment may arrest future development ofcomplete organ systems (Guillette et al.1995). During early development, thesexual characteristics of the animal areformed, the immune system developscompetence, and a variety of hormonesregulate the formation of bone structureand organ systems. Disruption of any ofthese complex systems at critical times canlead to permanent impairment.

Pesticides in streams are rapidly di-luted by riverflow so that soon after entryinto a stream they can be detected only atvery low levels or no longer be detected at

all. While the concentrations in streamsmay be relatively harmless during rain andhigh water flow, under certain conditionspesticides are concentrated rather thandiluted. Depending on the nature of thepesticide, they may attach to sedimentparticles, accumulate in the tissues of vari-ous organisms, or become buried in thesediment (Barbash and Resek 1996). Even-tually, all probably reach the sea, wherethey become a problem of relatively un-known magnitude. If pesticides are appliedin huge amounts each year for dozens ofyears, the dilution effect begins to disap-pear as the chemical concentrations increasein their particular final resting place. Thus,spraying of hillsides with a certain pesticidemay not affect the animals in the immediatevicinity but may have disastrous effects on

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

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other populations downstream from the siteof application.

Most pesticides reach the water boundto soil particles (Barbash and Resek 1996).Erosion, which in the United States is esti-mated to transport four billion tons of soil ayear intowaterways, is amajor contribu-tor of pesti-cides to riversand river beds.Thus, poorland-usepractices notonly contributebuildup of siltto the spawning areas in streams whichresults in suffocation of eggs. Erosion mayalso deliver pesticides to the rivers at a timewhen the fish, as embryos, are most sensi-tive to their deleterious effects.

Pesticide Concentrations CanBecome Magnified in Tissues

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

mulated in tissues of aquatic organisms,often becoming magnified thousands oftimes higher in the organism than in thesurrounding water. Usuallybiomagnification is a function of the fatsolubility of the pesticide (Norris et al.1991). Biomagnification is thus dependent

upon the metabolicstate of the ani-mal, such thatfatter animalstend to accumu-late more lipidsoluble pesticides.This reaches anextreme in thelipid-rich eggsand embryos.

Eggs of aquatic organisms usually haveenough fats in the form of yolk to meetearly energy requirements during develop-ment. Lipid soluble pesticides accumulaterapidly in these fat deposits and are noteasily removed. There they may competewith hormones provided maternally for useby the embryos (Bern 1990). The presenceof environmental contaminants in the yolkthat act as endocrine mimics thus may havea powerful influence on embryonicdevelopment.

Not only are pesticides taken up di-rectly from the environment, fishes can alsoabsorb them from food organisms. A studyof DDT accumulation in brook trout (Macekand Korn 1970) found that ten times moreof the available DDT and its metaboliteswere absorbed from food than from thewater. This can be magnified still further asthe pesticide travels through food chains.Metcalf et al. (1971) demonstrated thisbiomagnification effect convincingly withradioactive DDT in a model ecosystem. C14-DDT was applied to Sorghum as the sourcefor the pesticide. The Sorghum was then

Pesticides can be taken up from the waterand accumulated in tissues of aquatic organ-isms, often becoming magnified thousandsof times higher in the organism than in thesurrounding water.

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

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introduced into a system with severalcomponents that provided a food web.Sorghum was eaten by a salt marsh caterpil-lar. Excreta from the caterpillar was con-sumed by diatoms, which were subse-quently eaten by nine species of plankton.The plankton was eaten by mosquito larvaewhich were subsequently eaten by Gambu-sia, the mosquito fish. After one month,54% of the radioactivity was found in thefish, of which most was DDE, a breakdownproduct of DDT. The concentration of DDTwas 84,000 times greater in the fish than inthe water, while the concentration of DDEwas 110,000 times greater in the fish than inthe water. Biomagnification of concentra-

tions of DDT and its metabolites has beenwell established (Woodwell et al. 1967;Risebrough et al. 1967), which was a majorfactor leading to its removal from the pesti-cide market in the United States.

Modern pesticides are usually morewater soluble and do not accumulate inhigh concentrations in fat deposits. How-ever, they do show bioaccumulation (Table2). While these accumulations are not asdramatic as those of DDT, they show thatthe concentration of pesticide in the watermay not be relevant in determining whetherlevels of pesticide will cause biologicaleffects. These accumulations are usually

Table 2. Bioaccumulation of various pesticides, pesticideadditives, and pesticide contaminants in fishes.

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Pesticide Category Bioaccumulation Factor Species Reference______________________________________________________________________________________Carbaryl (Sevin) Insecticide 30 golden ide 1Chlordecone Insecticide 1100-2200 fathead minnow 2Chlorothalonil Fungicide 840 rainbow trout 3Chlorpyrifos (Dursban) Insecticide 1374 rainbow trout 4Cypermethrin Insecticide 700-1000 rainbow trout 5Diazinon Insecticide 60 carp 2Dichlobenil (Casoron) Herbicide 40 golden ide 1Fenvalerate Insecticide 40-200 salmon 6Flucythrinate Insecticide 3000-5000 fathead minnow 6Hexachlorobenzene Contaminant of chlorothalonil, 5500 rainbow trout 7

picloram, and pentachlorophenolNonyl phenol Surfactant 1300 stickleback 8Pentachlorophenol Insecticide 251-5370 rainbow trout 2Permethrin Insecticide 1700-3300 fathead minnow 6

73 Atlantic salmon 9Pentachlorophenol Fungicide 100 rainbow trout 102,3,7,8-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.

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.

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Without complete analysis of the pesti-cides and their breakdown products inaquatic organisms in a natural state, weare unable to determine the exact concen-trations to which they are subjected. Ifaquatic life has been exposed for longperiods of time, the concentrations withinthe tissues may be much higher than thatof the surrounding water.

measured in whole animals. Localizedconcentrations of pesticides at the cellularlevel may be extremely high, but this is anarea that has notbeen widely ex-plored.

Bioaccumulationandbiomagnificationproperties ofpesticides intissues representsa problem in ourassessment oftheir toxicity.Without completeanalysis of thepesticides and theirbreakdown products in aquatic organismsin a natural state, we are unable to deter-mine the exact concentrations to which they

are subjected. If aquatic life has been ex-posed for long periods of time, the concen-trations within the tissues may be much

higher than that ofthe surroundingwater. In addi-tion, exposure tomany types ofpesticides maylead to interac-tions betweenthem that in-crease theirtoxicity. Littlework has beendone on theinteractionsbetween differ-ent pesticides,

but available evidence suggests that theseinteractions can increase toxic effects(Koenig 1977; Cook et al. 1997).

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Fish Kills andAcute Toxicity ofPesticides

Pesticides are capable of killing salmo-nids and other aquatic organisms quickly.These short-term, acute toxicities to fishhave been studied extensively for mostchemicals used in forestry, agriculture,manufacturing, and the home. Much of thisinformation is provided by the chemicalmanufacturer in order to meet requirementsby the Environmental Protection Agencyand various state agencies.

Most of theseacute toxicity studiesreport lethal amountsas LC50s, the concentra-tions of chemicals thatkill 50% of the testanimals within 48 or 96hours, or LD50s, thedoses of chemicals inmilligrams per kilo-gram body weight ofthe test animal which kill 50% of the ani-mals within 48 or 96 hours. Organismsused for these tests range from algae tomice and rats. Rainbow trout are a com-mon subject, as are bluegills, fathead min-nows, mosquitofish (Gambusia), andzebrafish (Brachydanio rerio). A number ofLC50s for various fish are available in theliterature (e.g., Norris et al. 1991; Andersonet al. 1997) or on the internet (e.g.,http://ace.orst.edu/info/extoxnet/pips/ghindex.html). In the interest of space, theywill not be reproduced here.

Acute toxicity studies are usuallyperformed on subadult or adult fish. Fewof these studies have used eggs or fry, even

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 conge-ners of TCDD injected into eggs of laketrout were additive and effective at muchlower dosages than with juvenile fish. Ingeneral, embryonic stages are the mostsensitive to environmental pollutants(Guillette et al. 1995). This is an area ofresearch in western salmonids which hasbeen overlooked in the past and needsimmediate consideration.

When pesticides in water suppliesexceed their lethal concentrations, theresults are immediate. Large numbers offish are killed, and these are reported to a

variety of federaland state agen-cies. The spill iscleaned up whenpossible and theresponsible par-ties are fined. Anexample of thisregulatory actioncomes fromsouthern Oregon.

The Rogue River has received a number ofinadvertant spills of pesticides, particularlyacrolein, an herbicide used for removal ofaquatic vegetation. This herbicide is verytoxic to fish. Lorz et al. (1979) reported a1977 release of treated irrigation watercontaining Magnicide H, a gaseous form ofacrolein, into the Rogue River within 24hours of treatment instead of the recom-mended holding time of 6 days. A 10 milesection of the river was affected. ODFWofficials estimated that 238,000 fish werekilled, including 42,000 salmonids with anestimated value of $284,000.

On May 9, 1996, another large fish killoccurred in a four-mile stretch of Bear

The herbicide acrolein killed approxi-mately 92,000 steelhead, 114 juvenilecoho, 19 resident rainbow trout, andthousands of nongame fish in theRogue River Basin.

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Creek, a tributary of the Rogue River, Or-egon. A head gate was found open on anirrigation canal which had been treatedwith acrolein. The acrolein was used toremove aquaticvegetation that grewin the canal andinterfered with itsoperation. Approxi-mately 92,000 steel-head, 114 juvenilecoho salmon, 19resident rainbowtrout, and thousandsof nongame fish werekilled within a shortperiod of time afterexposure. Talent Irrigation District wasfined $356,000 for the loss of steelhead byOregon Department of Fish and Wildlife.They were also fined $50,000 by the OregonDepartment of Environmental Quality andan additional fine of $407 by the OregonDepartment of Agriculture for allowing the

Deaths of threatened and endangeredspecies from inadvertant contaminationof waterways are of grave concern be-cause the loss of each individual in asensitive population makes recoveryefforts that much more difficult.

pesticide to enter the stream (Evenson1998).

Deaths of threatened and endangeredspecies frominadvertant con-tamination ofwaterways are ofgrave concernbecause the loss ofeach individual ina sensitive popu-lation makesrecovery effortsthat much moredifficult. Fortu-nately, these

events are relatively infrequent. By con-trast, pesticide contamination at sublethallevels are probably an even greater dan-ger to salmonid populations because thecontamination is poorly regulated, themortalities go unseen, and the conse-quences are unknown.

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BehavioralEffects ofPesticides atSublethalConcentrations

Behavior of salmonids is specificallydirected at the continuance of the species.Each aspect of behavior has been highlyselected over the generations to contributeto survival. (See Figure 3.) Interruptions ofthese behavior patterns will thereforereduce survival and diminish populations.

Pesticides at sublethal concentrationshave been shown to disrupt many of thebehavior patterns of both juvenile and adultsalmonids and probably have deleteriousimpacts on their survival. Examples ofthese disruptions are presented below,although their impact on survival of fishpopulations is unknown at this time.

Pesticides Impair SwimmingPerformance

The ability to feed, to avoid predators,to defend territories, and to maintain posi-tion in the river system are all dependentupon the swimming ability of the fish. Adecrease in swimming performance reducesthe ability of the fish to survive and com-pete with others. Swimming performanceis commonly measured in swim tubeswhere the fish is forced to swim against agradually increasing current. The currentvelocity at which the fish loses its positionis referred to as critical swimming speed.The time of swimming at a particular veloc-ity before it loses its position is referred to

as swimming stamina. Both are used asindications of swimming performance.

Exposure to sublethal concentrations ofpesticides often causes a loss in swimmingperformance. The fungicide TCMTB, whichis used to prevent fungal staining of logs,causes deleterious effects on the swimmingability of salmonids. Chinook salmon andrainbow trout juveniles exposed to 5-20 ppbTCMTB for 48 hours, then removed to cleanwater for 12 hours, showed a dose-depen-

Figure 3Salmon life cycle.

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 returningto the stream where they were born to lay their eggs.

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dent reduction in critical swimming speeds(Nikl and Farrell 1993). A further studywith coho salmon at the same concentra-tions indicated that the reduction in criticalswimming speed was dependent on boththe concentration of TCMTB and the time ofexposure to the chemical (Nikl and Farrell1993). Damage to gill structure also in-creased with concentration and time ofexposure. The researchers speculated thatgill damage prevented respiratory exchangeand that the decrease in oxygen availabilitywas at least partially responsible for thedecrease in swimming speed.

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 theexposed fish was reduced 57% compared tocontrols. Paul and Simonin (1996) felt thatthis 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 hoursand found no change in swimmingstamina. However, they found that both aninsecticide formulation containingresmethrin and Scourge, a synergisedformulation with resmethrin and piperonylbutoxide, did affect swimming stamina.Brook trout that were held in solutions of3.2 ppb synergised and non-synergisedresmethrin for 6 hours had significantlyreduced stamina. Little et al. (1990) exam-ined behavior of rainbow trout exposed for96 hours to sublethal concentrations of fiveagricultural chemicals: carbaryl, chlordane,2,4-D amine, methyl parathion, and pen-tachlorophenol. All chemicals inhibitedspontaneous swimming activity and swim-ming stamina.

Rainbow trout exposed to tributyltinoxide, an anti-fouling agent used in boat

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

Half of juvenile Atlantic salmon sub-jected to 1 ppm of the insecticidefenitrothion for 15-16 hours lost the abilityto maintain territories for a period of sixdays after exposure (Symons 1973). Expo-sure of rainbow trout to 46 ppb of Vision, aglyphosate herbicide, for one month causedincreased aggressive behavior (Morgan andKiceniuk 1992). Rainbow trout exposed tothe synthetic pyrethroids, fenvalerate andpermethrin, tended to swim at the watersurface, 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 musclespasms and skeletal deformations. Bothpesticides are cholinesterase inhibitors andthe reactions were attributed to blocked

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

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neural transmission. Trout exposed to thechlorinated hydrocarbon, Kelthane(dicofol), became dark, lethargic, andshowed signs of respiratory distress, sug-gesting both respira-tory and neurotrans-mission problems(Holcombe et al.1982).

These experi-ments show thatpesticides at verylow concentrationscan interfere withswimming perfor-mance in salmonids and that these effectscan last for some time after exposure to thechemicals. The evidence comes from labo-ratory experiments and would be verydifficult to replicate in the field. If similareffects occurred in field situations, however,interference with swimming performancewould result in increased death frompredation.

Pesticides Can IncreasePredation on Juvenile Salmonids

The end result of any decrease inswimming ability will be an increase inpredation upon the juvenile salmonids. If ayoung salmonid is slowed in its escaperesponses by ion imbalances, metabolicproblems, or disease, it becomes prey for anumber of hungry predators. Its demise isnot immediately evident without sophisti-cated predator tests. Several studies havedemonstrated that pesticides can indeedincrease predation.

For example, Kruzinski and Birtwell(1994) found that juvenile coho salmonexposed to sublethal concentrations of thefungicide TCMTB showed fright and es-

cape responses similar to controls in asimulated estuarine environment. Afterfive days, however, TCMTB-treated fishhad been preferentially consumed by intro-

duced rockfish 5.5times more fre-quently thancontrols. In an-other study, after a24-hr exposure to1.0 ppmfenitrothion,Atlantic salmonparr were morevulnerable topredation by

brook trout than controls (Hatfield andAnderson 1972). Exposure to DDT had noeffect on the predation. Little et al. (1990)found that carbaryl and pentachlorophenolincreased vulnerability of rainbow trout topredation.

Predator avoidance tests with coho(Olla et al. 1992) and chinook salmon (Ollaet al. 1995) indicated that stresses causingincreased plasma cortisol levels resulted insusceptibility to predation, but that preda-tor avoidance in coho salmon returnedwithin 90 minutes (Olla et al. 1992) or 4hours (Olla et al. 1995). In chinook salmon,predator avoidance was recovered in 24hours after exposure to stress. While acutestresses seem to render the juveniles sus-ceptible to predation, the effects of chronicstresses from pesticide exposure are notwell known. Exposure of juvenile cohosalmon to sublethal levels of two triclopyrherbicides for four hours did not result insignificant changes in secondary stresseffects, such as respiration, plasma glucoseand lactate, and hematocrit (Janz et al.1991). No plasma cortisol levels weremeasured, but these usually correlate wellwith plasma glucose concentrations. How-ever, exposure to sublethal concentrations

These experiments show that pesti-cides at very low concentrations caninterfere with swimming performancein salmonids and that these effects canlast for some time after exposure tothe chemicals.

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of the butoxyethanol ester of 2,4-D causedenlargement of the interrenal gland, anindication that cortisol production wasincreased (McBride et al. 1981). If chronicexposure to pesticides does cause increasestress responses in salmonids, the studies ofOlla et al. (1992, 1995) suggest that preda-tion will be much greater in exposed fish.

Temperature Selection isChanged by Pesticides

Most organisms respond to the pres-ence of patho-gens throughtemperatureselection. Cold-blooded animalssuch as lizards orfish typicallyseek warmerenvironments toincrease meta-bolic repairwhen subjectedto toxicants orinfections. In salmonids, studies showed thatthe temperature selected depended on theconcentration of the pesticides to which thefish were exposed. Juvenile Atlantic salmonexposed to low doses of DDT selected lowertemperatures than controls (Ogilvie andAnderson 1965; Peterson 1973). At higherdoses of DDT, exposed fish selected highertemperatures than controls. This effect wasaccentuated in fish acclimated to warmtemperatures (170 C) compared to fish accli-mated to cool temperatures (80 C). Fishacclimated to 170 C and exposed to 10 ppb orhigher of DDT became hyperactive whenintroduced into cold water. Brook troutexposed to isomers of DDT and derivativesshowed similar changes in temperatureselection (Miller and Ogilvie 1975; Gardner1973). The alteration in temperature selection

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

These results suggest that salmonidsexposed to some pesticides select tem-peratures according to the concentrationof pesticide. At low concentrations, fish tryto lower their body temperature to minimize

the effects on physi-ological processes. Asthe concentrationincreases, they respondby seeking warmerwater to stimulatedetoxification. Theseeffects can last for aconsiderable time afterthe pesticide is re-moved, causing the fishto seek abnormal watertemperatures and thus

subjecting them to increased dangers ofdisease and predation.

Schooling Behavior is Reducedby Pesticides

Schooling behavior is a tactic to reducepredation. Predators are presented with alarge mass of fish from which it is difficultto focus on a single individual (Cushingand Harden-Jones 1968). Seaward migra-tion of juvenile salmonids is accompaniedby schooling responses, probably to reducelosses to the population during themigration.

Many pesticides disrupt schoolingbehavior. Drummond et al. (1986) found

Disruption of schooling behavior bymany pesticides suggests that thesecompounds may increase predationupon juvenile salmonids and lead topopulation losses that would be verydifficult to detect by conventionalfisheries techniques.

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that loss of schooling behavior in fatheadminnows was the most sensitive indicatorof stress for 133 of 139 organic chemicalstested, including a number of pesticides.Exposure to sublethal concentrations of thefungicide TCMTB interferes with schoolingbehavior in chinook salmon (Kruzinski andBirtwell 1994). Exposure to methoxyclorcaused a progressive increase in inter-fishdistance in brook trout (Kruzinski 1972).Holcombe et al. (1982) found that schoolingbehavior was disrupted in fathead min-nows exposed to sublethal concentrationsof Kelthane, Dursban, disulfoton,fenvalerate, and permethrin.

Disruption of schooling behavior bymany pesticides suggests that these com-pounds may increase predation uponjuvenile salmonids and lead to populationlosses that would be very difficult to detectby conventional fisheries techniques. Theprevalence of this effect by organic chemi-cals (Drummond et al. 1986) suggests thatthis sublethal effect may be more wide-spread than we might suspect.

Pesticides Can Interfere WithSeaward Migration

Juvenile salmon rearing in streamsreach a stage where their color changesfrom brown to silver. This is the stage ofparr-smolt transformation where a varietyof morphological, physiological, and behav-ioral changes occur. In addition to thesilvery color, the smolts lose their territorialbehavior, begin to school, and to migratedownstream 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 seawardmigration have not been extensively stud-

ied because of the difficulty of measure-ment of migration tendency. Lorz et al.(1979) studied the effects of three herbicideson seaward migration in coho salmon.Diquat at concentrations from 0.5 ppm to3.0 ppm inhibited seaward migration in adose-dependent manner. Dinoseb inhibitedmigration only at the high (but sublethal)concentrations of 40 and 60 ppm. Tordon101 (a mixture of picloram and 2,4-D)caused a slight inhibition of migration atthe highest levels studied (1.2 and 1.8 ppm),but the results were not significantly differ-ent from controls. Although the herbicideswere not lethal to the fish at the concentra-tions used, the levels were very high (ppm)compared to other concentrations of pesti-cides (ppb) described in this section. Thismay be due to the low toxicity of mostherbicides, compared to other classes ofpesticides. More work on seaward migra-tion should be done with other pesticides,especially the organochlorine and organo-phosphate insecticides commonly found inwestern streams.

Pesticides Interfere withSeawater Adaptation

The end result of seaward migration isthe entry of juvenile salmon into an estuary

Estuaries are a critical transition zone wheresalmon adapt to saltwater.

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and the tranformation of the fish’s osmo-regulatory mechanisms from a fresh waterto a saltwater environment. These osmo-regulatory processes permit the fish tomaintain required water and ion concentra-tions in various organ systems. The stressesinvolved with this transition can be sur-mised from the large mortality (usuallyabout 90% or greater for hatchery smolts)which results from seawater entry (Pearcy1992). Death can result from several causes.The juvenile fish may simply not make thetransition to seawater and die from osmo-regulatory problems. The juvenile fish maybe slowed by the osmotic stresses and beeaten by birds or predatory fish. The im-mune system of the fish may be compro-mised by the os-motic stresses,permitting theonset of diseaseand subsequentpredation by pis-civorous birds orfish.

Most salmo-nids spend a period of transition in theestuary where they seek the salinities theyprefer. Many utilize the less saline estua-rine surface water which stratifies overdeeper more saline water (Iwata et al. 1982;Birtwell and Kruzinski 1989).

Few studies have looked at the salinitypreference of fish exposed to sublethallevels of pesticides. One would expect thatthe stress from pesticide exposure mightcause the fish to select salinities compa-rable to that of their blood to relieve theextra burden of osmotic stress. Cohosalmon in the stratified salinity tank set upby Kruzinski and Birtwell (1994) sought thefreshwater wedge if they were previouslyexposed to TCMTB. Mosquitofish, how-ever, sought a higher salinity if exposed to

DDT (Hansen 1972). No change in salinitypreference was induced by malathion(Hansen 1972).

In a study on the effects of herbicideson juvenile coho salmon, three of the thir-teen herbicides studied, Amitrole-T, diquat,and paraquat, caused dose-dependentmortality in seawater tests (Lorz et al. 1979).An interesting phenomenon occurred infish exposed to Tordon 101 (a mixture of2,4-D and picloram). In December, fishwere tested at eight different concentra-tions. The two lowest concentrations, 0.25and 0.5 ppm, caused increased mortalities,while at higher concentrations up to 20ppm all fish survived. When this was

repeated in March,fish exposed to 20ppm Tordon 101 alldied in seawater. Theresearchers could notexplain the unex-pected mortalities atthe low concentra-tions but suggestedthat pre-smolted coho

salmon in December were less sensitive toenvironmental pesticides than those insmolted condition in March (Lorz et al.1979). Mitchell et al. (1987) found that a 10-day exposure to 2.78 ppm of the herbicideRoundup (a glyphosate formulation) didnot affect seawater adaptation or growth.

Because the transition from fresh waterto seawater is a critical period in the sur-vival of the juvenile salmon, one wouldexpect pesticides to have some of theirgreatest effects at this stage. However,studies showing relationships betweenpesticides and osmoregulatory problemsleading to mortality in salmonids are few.Most of the studies that have been donehave focused on marine species or euryha-line species which do not undergo the

Because the transition from fresh waterto seawater is a critical period in thesurvival of the juvenile salmon, onewould expect pesticides to have some oftheir greatest effects at this stage.

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

Pollutants Affect Adult Returns

The result of interference with lifehistory mechanisms of the juveniles shouldbe the decrease in numbers of returningadults. Because the sublethal effects ofpesticides on fish survival have not beenfully appreciated, there are few studies thathave correlated the return of adult salmonwith the extent of pesticide use in the riverbasin. In New Brunswick, however, re-searchers have found that decreased returnsof Atlantic salmon have been correlatedwith the use of pesticides in the area. Spe-cific concern has focused on the compoundsknown as nonyl phenols, which are usednot only as wetting agents in pesticides, butalso in the production of paper, textiles, andpetroleum products. Nonyl phenols arethought to act both by endocrine disruptionand by interference with the normal adap-tation of salmon smolts to seawater. While

the evidence is convincing that the salmonruns have been affected by spraying, theexperimental evidence has not yet beenpublished in the scientific literature. Apaper describing these effects has beensubmitted for publication (Fairchild 1999).

Migration patterns and timing of adultsalmon may be altered by pollutants as theyre-enter fresh water during their spawningruns. Elson et al. (1972) showed thatradiotagged Atlantic salmon entering theunpolluted Tabusintac estuary in NewBrunswick moved quickly up the estuaryand into the river system. In contrast,salmon entering the Miramichi estuary, aheavily industrialized estuary, spent timeswimming back and forth in an attempt toavoid heavily polluted water. They werenever found in a channel on the northwestside of Beaubears Island, where a marsh atthe lower end of the island served as areservoir for effluent from a wood-preser-vative plant. This effluent seeped into theriver at high tides. Salmon clung to thecleanest side of the river as they swamupstream past the industrial area. Clearly,the fish were slowed in their spawningmigration as they searched for the cleanestparts of the river.

Respiration of adult coho salmon wasexamined as they attempted to pass apolluted 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 passagetimes, or swam through the polluted areas,resulting in an oxygen debt and decreasedenergy reserves. Decreased energy re-serves could result in smaller eggs andinsufficient energy for passage into up-stream spawning areas.

An adult chinook salmon that is ready to spawn.

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In summary, these studies on thedisruption of behavior of salmonids bypesticides suggest that the presence ofpesticides can have profound effects on thesurvival of the juveniles. Every aspect oftheir biology can be affected. The studiesreported here consider mainly the freshwa-ter 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 the

estuary is the amphipod Corophium, whichspends the day buried in sediments whichmay be the final repository for many of thepesticides applied far upstream. It is likelythat the amphipods accumulate pesticidesand transfer them to the salmonids wheneaten. Few studies have documented thebehavior of juvenile salmonids once theyreach the estuary. Even fewer have exam-ined the effect of pollutants and pesticideson their behavior and survival.

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CompromisedImmune Systems

Fish in polluted waters are subject tomore frequent and more severe outbreaksof disease because many synthetic chemi-cals tend to suppress the immune system(Moller 1985;Repetto andBaliga 1996).Immune systemsprotect fish fromserious diseasescaused by exter-nal bacteria,parasites, andviruses. Thecomplexities ofthese systems are regulated and coordi-nated by a variety of compounds that actsimilar to hormones but that do not quite fitinto the classical definition (Bern 1990).Most texts on molecular endocrinologyinclude interleukins, cytokines, epithelialgrowth factors, and other compounds thatinfluence the immune system as hormones(Bolander, 1994). These immunohormonescan be compromised in various ways byenvironmental pollutants (Anderson 1996;Repetto and Baliga 1996).

Although considerable work has beendone 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 mam-mals, 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). Inrainbow trout, a gradual increase in im-mune competence occurs during early

growth, with non-specific immunity devel-oping first, followed by cell-mediated andthen humoral immunity. Full humoralimmunity, the ability to produce circulatingantibodies, develops at about 1 g in size.

A number of natural and anthropo-genic factors suppress the function of theimmune system. Stresses from habitat

changes, poor waterquality, lack of food,and pollutants allresult inimmunosupressionand an increase indisease (Pickering1993).

Information onimmunosuppression

in salmonids due to pesticides is scanty,although other fish have received more

Fish in polluted waters are subject tomore frequent and more severe out-breaks of disease because many syn-thetic chemicals tend to suppress theimmune system.

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attention (Anderson 1996; Iwama andNakanishi 1996). The insecticide endrinreduced the activities of phagocytes andantibody producing cells in rainbow trout(Bennett and Wolke 1987). Organotincompounds caused immune suppression inrainbow trout (O’Halloran et al. 1998).Although tributyltin is considered moretoxic to fish than its breakdown product,dibutyltin, the latter was the more potentimmunotoxin. Phenol and the PCBArochlor 1254 were found to reduce anti-body producing cells in rainbow trout(Anderson et al. 1984) and coho salmon(Cleland et al. 1989). TCDD caused mitoge-nic suppression in rainbow trout(Spitsbergen et al. 1986) and increasedsusceptibility to infectious hematopoeticnecrosis virus (Spitsbergen et al. 1988).

The timing of exposure to pollutantsmay be an important factor for the health ofthe immune system in anadromous salmo-nids. Maule et al. (1987) found that im-

mune suppression occurred to a greaterextent during smolting of coho salmon.This may be due to the higher levels of thestress hormone, cortisol, found duringsmolting in salmonids (Specker and Schreck1982; Thorpe et al. 1987). Cortisol isknown to suppress the immune system ofsalmonids (Maule et al. 1987; Pickeringand Pottinger 1989; Maule and Schreck1990). It is likely that the effects of expo-sure to immunosuppressant chemicalsduring the period of seaward migrationmay be compounded by the high levels ofplasma cortisol in the fish at that time.Many pesticides cause some degree ofimmunosuppression in mammalian sys-tems (Repetto and Baliga 1996). It seemslikely that similar effects may be found inthe fish immune systems. Before thenecessary research provides answers, itseems prudent to err on the side of cau-tion and assume that similar immunosup-pression by pesticides can be found insalmonids.

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EndocrineDisruptors

In the late 70s, researchers MikeHowell and Ann Black found that theirseine hauls from a small coastal stream inthe panhandle of Florida containedmosquitofish with a strange characteristic.They were all males (Howell et al. 1980).On further inspection, another oddity wasnoted. Many of the apparently male fishhad a gravid spot on their gonopodium,which normally indicates a female withinternally developing young. Furtheranalysis in the laboratory indicated thatmany of the apparent males were in factmasculinized females. A few months later,a second population of masculinized fe-males was discovered in the FenhollowayRiver of coastal Florida (Bortone and Davis1994), a stream approximately 300 kilome-ters east of the first stream. This collectionincluded not only mosquito fish but alsothe least killifish and the sailfin molly. Inboth streams, the masculinized femaleswere found downstream of paper mills.Some component of the effluent from papermills caused the females to acquire mascu-line traits.

This research was one of many studiesconducted over the past twenty years thatindicated that certain synthetic chemicals,including many pesticides, can alter thesexual endocrine (or hormone) system ofwildlife (Colborn and Clement 1992). Theeffects of these pseudo-hormones can varyconsiderably. In the above example, femalefish became masculinized. Other pollutantsact as artificial female sex hormones orestrogens. In still others, sexual expressionis not affected. Instead, the chemicalsinterfere with bone formation during earlydevelopment and result in stunted or mal-

formed adults. As scientists gain greaterinsights into the complex workings ofendocrine systems, they have come toappreciate the delicate balance of hormonesneeded to direct the early development ofan embryo and the profound effects thatendocrine mimics may produce.

Endocrine systems in an organismcontrol production of hormones, which inturn control many of its functions. Anendocrine system is a complex network ofpositive effectors and feedback loops that

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

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carry messages from one part of the body toanother to keep the body functioning prop-erly. Initial input to the system comes fromthe environment in the form of tempera-ture, light, or other sensory stimuli. Thesestimuli are recognized and integrated in thebrain. Through anumber of pathways,brain centers controlthe synthesis of pri-mary hormones in thepituitary, a small budof nerves and tissuesat the base of thebrain. In the reproduc-tive cycle, the pituitary produces gonadot-ropins which act on the gonads to producesteroid hormones: androgens predominat-ing for males and estrogens predominatingfor females. Steroids and other hormonestravel through the blood to seek specificreceptors in the cytoplasm of responsivecells. Each sex contains both male andfemale receptors in its cells so that therelative concentration of androgens andestrogens are the determining factor forsexual differentiation. When the steroidbinds to the receptor protein, the steroid-receptor complex finds its way to thenucleus where it binds to DNA response

elements to stimulate or regulate the pro-duction of steroid specific proteins.

In such a complex system, pesticidesand their derivatives can interact at manylevels in the brain-pituitary-target organ

axis with avariety ofeffects. Theseeffects canmanifest them-selves throughbehavioral,reproductive,immunologi-

cal, or physiological changes (Bern 1990).Our knowledge of the hormonal relation-ships to many of these functions is not wellenough defined at present to exactly deter-mine what effects pollutants may have onthese functions. However, our knowledgeof the female endocrine system and theeffects of pesticides on its function hasgrown rapidly in recent years, and numer-ous studies have defined some of the un-wanted effects.

Pesticides Can Mimic Estrogens

The sex of fishes can be determinedrelatively late in development. For ex-ample, applications of testosterone duringthe egg and fry stages of salmonids canconvert the young fish completely to malesor 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 chinooksalmon, Piferrer et al. (1994) suggested thataromatase, an enzyme that converts andro-gens to estrogens, acts as a regulatoryswitch for the process of sex differentiation.They showed that a treatment of youngsalmon with an aromatase inhibitor for only

Certain pesticides and pollutants canmimic the effects of estrogens, causingfeminization of male animals.

During early development, fish are especiallyvulnerable to pesticides that can mimic naturalhormones.

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two hours could transform genetic femalesinto functional males. These transexualmales had testes indistinguishable fromnormal males, underwent all stages ofsperm maturation, and were later used tofertilize females to produce all femaleoffspring. Concentrations of androgensand estrogens circulating through the bloodprovide a stimulus for induction of levels ofaromatase activity (Callard and Callard1987). With a system of sex differentiationin fishes that is labile (i.e., likely to change),the potential for major impacts from estro-gen mimics may be quite large.

Certain pesticides and pollutants canmimic the effects of estrogens, causingfeminization of male animals. Actions ofpesticides that result in feminization in fishare thought to occur in three ways:

1) Estrogen mimics compete withestradiol, the female sex hormone, for itsreceptor protein. The complex that isformed enters the nucleus, binds the DNAresponse elements, and stimulates theresponses expected from normal female sexhormones. This has little effect in femalesbut stimulates inappropriate responses inmales, which have only very low concentra-tions of circulating estrogens. The result isfeminization of the males.

2) Antiandrogenic compounds com-pete with androgens, or male sex hor-mones, for the androgen receptor protein.Once bound, the complex enters thenucleus but is not able to bind to DNAresponse elements. Consequently, noandrogenic 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

mechanisms in the brain. The interferenceresults in an upset of the regulatory mecha-nisms that distinguish males from femalesand sends the wrong messages to the pitu-itary. The result may be the release ofgonadotropins that stimulate feminizationof the juvenile fish.

The best known examples of feminiza-tion by competition of pesticides for estro-gen receptors have occurred with alligatorsin the Southeast (Guillette et al. 1995), seagulls (Fry and Toone 1981) and Caspianterns (Fox 1992). Increasing numbers ofchemicals are found to have estrogenicactivity in fish (Jobling and Sumpter 1993;Jobling et al. 1995). Unknown chemicalcontaminants from sewage effluents havebeen shown to produce estrogenic re-sponses in male carp (Folmar et al. 1996).DDT and its long-lived breakdown product,o,p’-DDE, have been shown to bind estro-gen receptors to provide weakly estrogenicresponses, whereas p,p’-DDE does not bindestrogen receptors except at high concentra-tions (Donohoe and Curtis 1996). p,p’-DDE

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

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has a higher affinity for androgen receptors(Kelce et al. 1995),suggesting thatthe binding maybe nonspecific fora number ofsteroid receptors.Lindane,chlordecone(Donohoe andCurtis 1996; Thomasand Khan 1997), alkylphenols (Jobling et al.1995; White et al. 1994), endosulfan, dield-rin, and toxaphene (McLachlan 1993; Sotoet al. 1994) have all been shown to provideestrogenic responses in fish and otherorganisms through binding to estrogenreceptors.

Most of these pesticides bind onlyweakly to the estro-

gen receptor. Forexample, thebinding of theinsecticidesendosulfan,dieldrin, tox-aphene, andchlordane to theestrogen receptor

was very weak: less than 1/10,000 that ofthe natural binding compound, estradiol(McLachlan,1993; Soto et al. 1994). For thisreason, these compounds were thought fora long time to produce few environmentaleffects. However, environmental com-pounds in combination may act together

Environmental compounds in combina-tion may act together with the estrogenreceptors to provide responses fargreater than that of single compounds.

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

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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.

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Notes: Lines above the bars represent standard errors. * indicates that the increase in number of

cells is significantly greater than unexposed cells. Proliferation of breast cancer cells is a standard

test for estrogenic effects.

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with the estrogen receptors to provideresponses far greater than that of singlecompounds (see Figure 4).

Feminization of males may also bebrought about by antiandrogenic com-pounds. Vinclozolin, a fungicide usedwidely for grapes, ornamental plants, snappeas, and turfgrass (Kelce et 1994), causesfeminization of males. The fungicide bindsto androgen receptors and enters thenucleus, but blocks normal androgenicresponses. The vinclozolin-androgenreceptor complex cannot recognize theappropriate DNAresponse elementsto stimulate pro-duction of essentialmale proteins(Wong et al. 1995).DDE, the persis-tent break-downproduct of DDT,also binds toandrogen receptorswith similar results (Kelce et al. 1995).Antiandrogenic responses in fish are notwell understood at present. Part of thisdifficulty is the problem of demonstratingandrogen binding activity in fish tissues(Monosson et al 1997). The relationship ofthe active androgen in fish, 11-

ketotestosterone, to receptors for test-osterone in the nucleus is not clear(Pasmanik and Callard 1985; Callard andCallard 1987), although a receptor for 11-ketotestosterone in the ovaries of cohosalmon has been reported (Fitzpatrick etal. 1994).

The third category of hormonal disrup-tion which may result in feminization byenvironmental pollutants arises from theinterference with regulatory functions inthe brain and pituitary. This interferencecan affect neurotransmitter functions,

sensory systems,control of serumhormone levels andtherefore hormonalfeedback. Weknow little aboutthe role of pesti-cides in this area,although there isample informationthat shows that

brain function is a necessary part of pro-viding the correct hormones for sexualdifferentiation. 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 gonadotro-pins. Arochlor 1254 has been shown tocause decreases in serotonin and dopaminelevels in the brains of fish (Kahn andThomas 1996), due either to increaseddegradation or decreased synthesis of theneurotransmitters. Many insecticides arecholinesterase inhibitors, that is, theyinterfere with the normal breakdown ofacetylcholine, a neurotransmitter, byblocking the enzyme cholinesterase. Thisresults in a longer lifespan for acetylcho-line and a disruption of normal neuralfunction.

The peculiar lability of sex differentiationin fishes suggests that endocrine-dis-rupting chemicals in the environmentmay profoundly alter the sex ratios andbreeding capabilities of our native fish.

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The peculiar lability of sex differentia-tion in fishes (Chan and Yeung 1983) sug-gests that endocrine-disrupting chemicalsin the environment may profoundly alterthe sex ratios and breeding capabilities ofour native fish. This field is still young andeffects on fish population are largely un-known. With the development of moresophisticated methods for detection ofpseudo-estrogens and pseudo-androgens inthe environment, we should have a betterunderstanding of the effects of chemicalsthat find their way into our watersheds.

Pesticides May Have OtherEndocrine Effects

Although disruption of sex steroidfunction has received the most attention, itis not the only type of endocrine disruptionthat may result from exposure to environ-mental chemicals. Brucker-Davis (1998)listed over 90 synthetic chemicals thataffected function of the thyroid gland.Thyroid hormones are thought to influenceseasonal adaptations, reproduction, migra-tion, and growth of fish. Hypothyroidismresulting in the formation of goiters wasshown in coho and chinook salmon rearingin the Great Lakes and was related to envi-ronmental 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 inthe kidney, but increased thyroxine in thepharyngeal thyroid. Peripheral conversionof thyroxine to the active hormone, tri-iodothyronine, was suppressed with bothcompounds.

Skeletal deformities have long beenrecognized as an effect of environmental

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

pollution and have been suggested as anexcellent 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

impact on fish populations that we expect.

Bone formation and structure reliesupon the mobilization and handling ofcalcium ions, which are controlled by avariety of hormones, including growthhormone, calcitonin, parathyroid hormone,and stanniocalcin (Davis 1997). These arein turn controlled by the brain-pituitaryaxis described earlier and subject to similarfeedback mechanisms to regulate theirsynthesis and concentration. Unfortu-nately, calcium regulation mechanisms havenot received the study that reproductivehormones have and consequently we knowlittle about specific mechanisms underlyingskeletal defects. Evidence that links envi-ronmental pesticides to skeletal abnormali-ties, however, is widespread.

In the early 1970s, fish biologists study-ing members of the drum family in JamesRiver, Virginia, found that a large numberof specimens had shortened vertebralcolumns compared to similar species in thenearby York River. With the help of toxi-cologists, they found that a manufacturing

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facility for chlordecone, a widely-usedinsecticide, had been releasing largeamounts of the compound into the JamesRiver. The stunted fish contained highchlordecone levels (Davis 1997). Exposureto chlordecone interfered with calciumdeposition into bone and produced scoliosisand compression of the vertebrae (Couch etal. 1977). After 1976, when manufacture ofchlordecone had stopped, the frequency ofvertebral abnormalities decreased.

Wells and Cowan (1982) reporteddysplasia in Atlantic salmon parr after asimulated spill oftrifluralin, a pre-emergent herbicide,in the Eden River ofScotland. The fishwere exposed to theherbicide for lessthan 1 day. Parrdeveloped scolioticvertebral abnormalities that caused them toappear stumpy. Laboratory tests showedthat exposure to trifluralin resulted inhyperosteosis, a proliferation of the bonetissue (Couch et al. 1979). This was accom-panied by fusion of vertebrae, persistenceof osteoblasts, abnormal vertebral pro-cesses, and, strangely, the presence of noto-chord tissue in the vertebral canal. Clearly,the mechanisms of bone formation hadbeen severely disrupted.

A number of other environmentalpollutants, including chlorinated hydrocar-bons (toxaphene, DDT), organophosphatepesticides (malathion, parathion, demeton),crude oil, and heavy metals (Bengtsson1979), have been implicated in bone abnor-malities in fishes. In most of these studies,

researchers feel that the damage is done inthe egg or early fry stages, possibly byeffects on neuromuscular interactionsduring early development.

Recent studies on squawfish in theWillamette River have shown elevatednumbers of abnormalities in bone forma-tion, especially in the Newberg Pool (RM 26to RM 60) (Altman et al. 1997). In theNewberg Pool, skeletal deformities rangedfrom 22.6 to 52.0 percent. No specific causefor the deformities has been identified, buta variety of factors including high tempera-

tures, low dis-solved oxygen,pesticides, PCBs,and effluents frompulp mills, papermills, and oresmelters have beensuggested. Analy-ses by the U. S.

Geological Survey showed the presence ofheavy metals (Altman et al. 1997), orga-nochlorine pesticides, organophosphatepesticides, and even trifluralin in theWillamette River and its tributaries(Anderson et al. 1997). Although noskeletal abnormalities were found insalmonids in the watershed, the wide-spread occurrence of pesticides inWillamette River and the presence ofskeletal abnormalities in squawfishshould stimulate research on the potentialendocrine-disrupting effects of the mostcommon contaminants, such as atrazine,simazine, metolachor, and diuron. At theleast, such abnormalities in the fish popu-lations should provide a warning for thepresence of endocrine disruptors in ourwatersheds.

Trifluralin, a pesticide found in theWillamette River, has been shown tocause bone abnormalities in Atlanticsalmon.

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Indirect Effectsof Pesticides onSalmon

Pesticides can indirectly affect fish byinterfering with their food supply or alter-ing the aquatic habitat, even when theconcentrations are too low to affect the fishdirectly. Such indirect effects may greatlyreduce the abundance of food organismswhich in turn reduces the growth andprobable survival of the fish.

Excellent examples of indirect effects ofpesticides on salmonids were documentedin the attempts to control spruce budwormin the forests of northeastern U. S. andCanada (Muirhead-Thomson 1987). In themid 1970s, permethrin, a synthetic pyre-throid, was introduced to kill the sprucebudworm. The insecticide was lethal toinsects and moderately toxic to fish. Experi-mental sprayings of permethrin at 13 differ-ent streams be-tween 1976 and1980 did not resultin moralities innative fish(Kingsbury andKreutzweiser1987). Blockingseines set at thebottom of thesprayed areaswere never found to contain dead fish.Minnows and juvenile Atlantic salmonheld in live cages in the sprayed areashowed no mortality attributed to thespraying regimes.

The same could not be said for theaquatic larvae in the streams, however(Kreutzweiser and Kingsbury 1987). Huge

numbers of poisoned nymphs were founddrifting downstream after spraying. Com-parisons with pre-spray drift samplesshowed that the numbers of dead nymphsincreased as much as 6000 times afterspraying. This massive mortality wasfollowed by a feeding frenzy among thesalmonids. Atlantic salmon increased thenumber of nymphs in their stomachs by 2-4

fold. Brook troutfed even morevoraciously, increas-ing their stomachcontents by as muchas 10-fold.

The poisonedinsects seem to haveno apparent directeffects on the salmo-

nids, which fed as long as the driftinglarvae were available. With time, however,the diets of the salmonids, especially thebrook trout, changed considerably. Withfew of the normal food components ofstonefly and mayfly nymphs and caddislarvae left in the streams, the trout changedto a diet of primarily Dipteran (fly) larvaeand terrestrial insects.

Pesticides can indirectly affect fish byinterfering with their food supply oraltering the aquatic habitat, even whenthe concentrations are too low to affectthe fish directly.

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Densities of Atlantic salmon and brooktrout were followed for a year after spray-ing. One month after spraying, the densityof Atlantic salmon rearing in the area ofhighest application had decreased substan-tially. Brook trout populations did notshow as great a decrease. It was felt thatthe reduced density of the Atlantic salmonwas due to migration from the area inresponse to a reduced food supply.

Insect larvae and crustaceans are verysensitive to many types of pesticides, reduc-ing the availability of these organisms tofish as prey (Macek et al. 1976; Brown 1978;Muirhead-Thomson 1987). Experimentalspraying of ponds with carbaryl to simulateoverspraying for spruce budworm controlresulted in massive mortality of aquaticinvertebrates (Muirhead-Thomson 1987).Some species of amphipods were not foundfor three years after the spray event (Gibbset al. 1984). Walker (1964) found no fishmortality after application of 2-6 ppm ofatrazine, a common herbicide, to ponds butinsect larvae were killed immediately.

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

In experimental treatments of replicateponds with atrazine, deNoyelles et al.(1989) found that phytoplankton andaquatic plants were reduced by as much as95% at the higher concentrations. Zoop-lankton did not seem to be directly affected.However, several months later, zooplank-ton populations also were reduced(deNoyelles et al. 1982). In the same studyon atrazine, Dewey (1986) reported a de-crease in the number of nonpredatory

insects, while the predatory insect popula-tion was unaffected. She suggested that thedecrease in nonpredatory insects was dueto a reduction of algae and plants used asfood and a reduction of water plants usedas habitat for the insects. Further study ofthe fish populations indicated that thereproduction of bluegills was greatly re-duced, probably from a lack of food. Thestomach contents of the bluegills in thetreated ponds were significantly lower thanthose in the control ponds (Kettle et al.1987). Populations of young bluegills werefurther reduced by the lack of aquaticvegetation in which to hide. Without theaquatic vegetation, the young were preyedupon 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 effectson salmonid populations, although it seemslikely that they would be subject to popula-tion dynamic forces similar to those demon-

The integrity of aquatic ecosystems is essential forhealthy salmon populations.

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strated with bluegills. Interference withgrowth of salmonids, however, has deleteri-ous effects on smolting (Ewing et al. 1980),immune function (Tatner 1996), predation(Parker 1971),seaward migration(Wedemeyer et al.1980), and seawateradaptation (Folmarand Dickhoff 1980;Mahnken et al.1982).

In addition to interference with theirfood supply, pesticides may also affect thehabitat of the fish. Increased predation onsmall fish may occur when water plants arekilled by herbicides in the aquatic environ-ment (Lorz et al. 1979; Kettle et al. 1987).Adverse water temperatures may resultfrom the removal of riparian vegetation byherbicides (Norris et al. 1991). Fish mayavoid contaminated areas with a conse-quent reduction in availability and suitabil-ity of feeding and spawning areas

(Beitinger 1990; Birge et al. 1993). Brown(1978) found that application of the herbi-cide paraquat caused death and decomposi-tion of aquatic plants which in turn lowered

the oxygen contentof the water enoughto kill trout.

These resultsand others of simi-lar nature (Brown1978; Muirhead-

Thomson 1987) indicate that disruption ofthe food chains in aquatic ecosystems canhave relatively long-lasting effects on fishpopulations. In complex ecosystems,indirect effects can be more importantthan direct effects (Lampert et al. 1989)and non-target organisms may be betterindicators of ecosystem health than theorganisms of interest. Management ofpesticide applications for protection ofaquatic habitats is obviously much morecomplex than promoting the use of LC50sfor setting application limits.

Increased predation on small fish mayoccur when water plants are killed byherbicides in the aquatic environment.

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ConclusionsSalmonids require coordinated re-

sponses to environmental stimuli andinternal physiological reactions for healthydevelopment, territorial defense, smolting,seaward migration, and adaptation toseawater. Interruptions of this interplaymay cause inappropriate physiologicalresponses that have deleterious effects onsurvival of the salmon. As we have shownhere, sublethal concentrations of pesticidescan cause such interruptions and therefore

result in harmful changes in physiologyand behavior. The wide array of effects thathave been demonstrated is cause for con-cern (Table 3).

The magnitude of the problem frompesticides is difficult to assess because ofthe lack of monitoring programs for the useand distribution of pesticides. Yet, wherewater quality monitoring has been done,pesticides are usually detected. A recentreport commissioned by the Oregon Legis-lature (Botkin et al. 1995:104) concludedthat fertilizers and pesticides were detri-

Table 3. Sublethal effects of selected pesticides found in theWillamette River Basin Study by USGS.1

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Herbicides InsecticidesAtrazine Simazine Malathion Chlorpyrifos Carbaryl

____________________________________________________________________________________________________________Negative Effects on:

Food Supply +2 +3 +4 +5

Growth +2 +6 +7 +8

Reproductive success +2 +9 +10

Bone Abnormality +11 +12 +13

Endocrine Disruptor +14 +13,14

Immune System +15

Behavior +16 +17,18 +12,17 +12

Schooling +19

Predator Avoidance +20 +18

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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.

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mental to salmon: “With such large appli-cations of pesticides and fertilizers, someportion is sure to make its way into nearbystreams, especially since most agriculturalland lies in close proximity to streams andrivers. Since little monitoring is done to detectthe presence of pesticides and fertilizers instreams, the levels of exposure by fish to chemi-cals are largely unknown (authors’ empha-sis).”

Certain facts about pesticides in theenvironment are known and reviewedbriefly here:

• Pesticides are typically found in greatvariety in salmonid habitats.

• Pesticides break down into productsthat may be less toxic, of equal toxicity, orof greater toxicity than the original com-pounds.

• Fish and other aquatic organismsmust continue to cope daily with a varietyof pesticides or breakdown products whichwere used years ago but remain in aquaticenvironments.

• Pesticides move in streams and riversthroughout the watersheds and may poseproblems far from the site of application.

• In a process known asbioaccumulation, pesticides absorbed intoplant and animal tissues may becomeconcentrated and reach levels many timeshigher than the concentrations in the sur-rounding 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

sensitive population thwarts our efforts torecover wild salmonids.

In contrast to these dramatic fish kills,sublethal concentrations of pesticides aremore subtle and their effects are largelyunseen. From laboratory experimentation,researchers have found that sublethalconcentrations of pesticides can affect manyaspects of salmonid biology, includingswimming performance, predator avoid-ance, temperature selection, schoolingbehavior, seaward migration, immunity todisease, reproduction, and food supply.Specifically, the literature reviewed hereshows that:

• A variety of pesticides impairswimming performance which can reducesuch critical behaviors as the ability to feed,to avoid predators, to defend territories,and to maintain position in the river sys-tem.

• Chronic exposure to certain pesti-cides can increase stress in juvenile salmo-nids and thereby render them more suscep-tible to predation.

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• Several pesticides have been shownto cause fish to seek abnormal water tem-peratures, thus subjecting them to in-creased dangers of disease and predation.

• Many pesticides interrupt normalschooling behavior of salmon, a critical tacticfor avoiding predation during migration.

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

• Several studies suggest that certainpesticides can impair salmonids’ ability totransition from fresh water to sea water;

however there is a need for further researchin this area, placing particular emphasis onthe critical period of transition that takesplace in the estuary.

• As with other pollutants, pesticidesmay interrupt the spawning migrations ofadult salmon by interfering with the timingof migration and by draining energyreserves.

• Pesticides can suppress the normalfunctioning of the immune system, result-ing in a higher incidence of disease.

• Certain pesticides can act as hormonemimics or blockers, causing abnormalsexual development, feminization of males,abnormal sex ratios, and abnormal matingbehavior.

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

• Fishes and other organisms areespecially vulnerable to endocrine-disrupt-ing effects during the embryonic and earlydevelopment stages of life.

• Pesticides can indirectly affect salmo-nids by altering the aquatic habitat andfood supply for salmonids.

Pesticides can affect salmon biology at many stagesin their development.

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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 newapproach to appreciate the dangers pesticides pose for salmonids may be necessary. Onemethod that has proved useful to establish the relationship between chlorinated hydrocarbonconcentrations 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 particu-lar 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 centralhypothesis 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 laketrout. 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 eggsimproved significantly as concentrations of PCBs, DDT, and oxychlordane declined. Thesecond criterion is that there must be a strong correlation between exposure to the hypotheti-cal agent and the disease. In a study of egg and fry survival at different locations, the extentof 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. Compari-son of different species at the same time, the same species at different times, and the samespecies at different locations established that reproductive impairment correlated with PCBexposure. 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 thehypothesis 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, whichis 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 relation-ships between environmental contaminants and population survival in real-world settingswhere a host of factors come into play. Restrictions on the use and dumping of organochlo-rine compounds into the Great Lakes resulted in partial restoration of the lake trout popula-tions.

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RecommendationsFrom the evidence available at present,

it can be concluded that there is a plausiblebasis for considering pesticides as onecausative factor in the decrease of salmonpopulations. Based on this review, we offerseveral policy recommendations andidentify areas for further research:

1. Address the impacts of pesticideson salmon when developing and imple-menting recovery plans for threatenedand endangered species. As federal, state,provinicial, and local agencies work torecover salmon in the Pacific Northwest,all factors contributing to the declineshould be addressed. To date, pesticideshave been overlooked as a factor deservingattention in our recovery efforts. Al-though there is a need for more informa-tion on the effects of pesticide use insalmon habitats, our salmon runs may beextinct by the time lengthy and laboriousstudies using strict scientific methods arecomplete. Thus, we must act now usingavailable information to formulate man-agement strategies that will minimize thepotential danger from sublethal concen-trations of pesticides.

2. Conduct ecoepidemiological stud-ies in critical salmonid habitat. Most ofthe effects of pesticides referred to in thisreport have been determined in experimen-tal laboratories. In the field, however,environmental conditions are not con-trolled, and many factors interact to con-fuse the determination of direct relation-ships. An ecoepidemiological approach(see inset opposite page) would be particu-larly valuable because it is designed toattribute causality to events occurring inreal-world situations. This approachrequires data which are not currently being

collected. In particular, ecoepidemiologicalstudies at the watershed level requirespecific pesticide use information in orderto establish correlations between salmondecline 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 datacan then be combined with watershed-specific information on a host of physi-ological and behavioral indicators ofsalmon health. (Currently, California isthe only state with salmon habitat wheresuch information is collected.) Pesticideuse information will also enable efficientinstream monitoring for pesticidecontamination.

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We must act now to protect salmon from pesticides.

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4. Establish instream monitoringprograms in critical salmon habitats. Asystematic monitoring program for pesti-cides and their breakdown products needsto be undertaken. Clearly, not all pesticidescan be tested for in all locations, but currenttesting is woefully inadequate for under-standing the role of pesticides in salmondecline. In conjunction with pesticide useinformation, these analyses can be targetedto the compounds of most concern. Suchtargeting can greatly improve the cost-effectiveness of monitoring.

5. Err on the side of caution whensetting water quality standards for pesti-cides. As discussed in this report, there arefew established criteria for the protection ofaquatic life from pesticides. Moreover,evidence reviewed here shows that suble-thal effects on salmonids have not beenfully appreciated, that juvenile salmonidssuccumb more easily to toxins in the water,that laboratory studies do not reflect thenatural life cycle of the fish, and that little isknown about how pesticides affect aquaticecosystems. These factors must be consid-ered when setting standards, and a precau-tionary approach must be adopted. Muchcan be gained by emphasizing how toeliminate the introduction of these toxicsubstances into the watersheds that com-prise critical salmonid habitat.

6. Prevent pesticide contamination ofsalmonid habitat by reducing pesticideuse. Once contaminated, water is difficultif not impossible to clean up. Therefore,pest management approaches that do notdepend on pesticide use in agricultural andnon-agricultural settings should be encour-aged and further developed. There isample evidence that ecologically sound andeconomically viable methods can be suc-cessfully implemented. The adoption ofsuch alternatives can be encouragedthrough technical assistance, financialincentives and disincentives, demonstrationprograms, and information exchange op-portunities.

7. Adopt state and provincial pro-grams in the Pacific Northwest to phaseout pesticides that persist andbioaccumulate in the environment.Numerous pesticides, including some thatare no longer used and many that arecurrently used, are known to persist inthe environment and to bioaccumulate inaquatic systems. Washington State’sDepartment of Ecology is now consider-ing a plan to end the release of suchtoxins, including certain pesticides, intothe environment. To ensure salmon re-covery, all state and provincial govern-ments in the Pacific Northwest shouldadopt similar programs.

45


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Glossary, Abbreviationsand Scientific Names2,4-D — 2,4-dichlorophenoxyacetic acid. Aherbicide that mimics natural planthormones.

DDT — dichlorodiphenyltrichloroethane.An insecticide widely used in the past butnow illegal in the United States.

DDE — dichlorodiphenylethane. A long-lived breakdown product of DDT.

Eulachon — Thaleichthys pacificus

Euryhaline — the ability to tolerate wideranges of salinity. Euryhaline fish are oftenfound in estuaries where the salinities canrange from fresh water to seawater.

Gonopodium — front rays of the anal fin oflivebearing fish (Family Poeciliidae) areelongated to form an organ that assists ininternal fertilization.

IHN virus — infectious hematopoeticnecrosis virus, a major cause of mortalitiesin Columbia basin salmonids

Lamprey, Pacific — Lampetra tridentata

Minnow, fathead — Pimophales promelas

Mosquitofish — Gambusia sp.

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

Ppb — parts per billion; a concentration ofpesticide equal to one gram of the com-pound 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 compounddissolved in a million grams of water. Equiva-

lent to milligrams per liter (mg/L).

Pesticide — anthropogenic chemicals usedfor control of target organisms. These in-clude insecticides, herbicides, fungicides,and other biocides.

Redd — a depression dug in the streambedgravel in which salmonids lay their eggs.

Salmon, Atlantic — Salmo salar

Salmon, chinook — Oncorhynchustshawytscha

Salmon, coho — Oncorhynchus kisutch

Salmon, sockeye — Oncorhynchus nerka

Shad, American — Alosa sapidissima

Smolt — a juvenile salmonid characterizedby a uniform silvery color. Fish at this stageundergo a number of physiologicalchanges, lose their ability to hold territories,tend to school, and begin migration towardthe sea.

Steelhead — Oncorhynchus mykiss, a migra-tory form of rainbow trout

Surfactant — a chemical added to formula-tions of pesticides to reduce surface tensionand cause wetting by the pesticide solution.

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

TCMTB — 2-(thiocyanomethythio)-benzothiazole, an antisapstain fungicideused on timber to be exported.

Trout, brook — Salvelinus fontinalis

Trout, brown — Salmo trutta

Trout, cutthroat — Oncorhynchus clarki

Trout, lake — Salvelinus naymaycush

Trout, rainbow — Oncorhynchus mykiss

For more information…

Northwest Coalition for Alternatives to PesticidesP.O. Box 1393

Eugene, OR 97440-1393(541) 344-5044; fax (541) 344-6923

www.efn.org/~ncap

Oregon Environmental Council520 SW 6th Ave., Suite 940

Portland, OR 97204(503) 222-1963; fax (503) 222-1405

www.orcouncil.org

OSPIRG Foundation1536 SE 11th Ave.

Portland, OR 97214(503) 231-4181; fax (503) 231-4007

www.pirg.org/ospirg

Institute for Fisheries ResourcesPO Box 11170

Eugene, OR 97440-3370(541) 689-2000; fax (541) 689-2500

www.pond.net/~fish1ifr

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