Reproductive Effects in Birds Exposed toPesticides and Industrial ChemicalsD. Michael FryDepartment of Avian Sciences, University of California, Davis, California

Environmental contamination by agricultural chemicals and industrial waste disposal results in adverse effects on reproduction of exposed birds. Thediversity of pollutants results in physiological effects at several levels, including direct effects on breeding adults as well as developmental effects onembryos. The effects on embryos include mortality or reduced hatchability, failure of chicks to thrive (wasting syndrome), and teratological effectsproducing skeletal abnormalities and impaired differentiation of the reproductive and nervous systems through mechanisms of hormonal mimickingof estrogens. The range of chemical effects on adult birds covers acute mortality, sublethal stress, reduced fertility, suppression of egg formation,eggshell thinning, and impaired incubation and chick rearing behaviors. The types of pollutants shown to cause reproductive effects includeorganochlorine pesticides and industrial pollutants, organophosphate pesticides, petroleum hydrocarbons, heavy metals, and in a fewer number ofreports, herbicides, and fungicides. o,p'-DDT, polychlorinated biphenyls (PCBs), and mixtures of organochlorines have been identified asenvironmental estrogens affecting populations of gulls breeding in polluted "hot spots" in southern California, the Great Lakes, and Puget Sound.Estrogenic organochlorines represent an important class of toxicants to birds because differentiation of the avian reproductive system is estrogendependent. - Environ Health Perspect 103(Suppl 7):165-171 (1995)

Key words: environmental estrogens, pollution, PCB, DDT, development

Introduction

Wild birds are very conspicuous in thelandscape. Injuries to populations of birdsfrom environmental pollutants and pesti-cides are obvious indicators of environmen-tal damage. Rachel Carson's Silent Spring(1) identified the urban use of pesticides(primarily DDT) as the cause of a notice-able decline of birds singing in the eastern

United States and also the cause of mass

songbird mortalities. While direct exposure

to DDT is not highly toxic to birds, heavyand repetitive use of the pesticide is. DDTwas used aggressively to kill the beedes thatspread Dutch Elm disease; this resulted inthe bioaccumulation of DDE in nontargetspecies of earthworms. The levels were highenough that robins and other songbirdswhich ingested the earthworms received

This paper was presented at the Symposium onEstrogens in the Environment, III: Global HealthImplications held 9-11 January 1994 in Washington,DC. Manuscript received: March 15,1995; manuscriptaccepted: April 4,1995.

Address correspondence to Dr. D.M. Fry,Department of Avian Sciences, University of California,Davis, Davis, CA 95616. Telephone: (916) 752-1201.Fax: (916) 752-0753. E-mail: DMFRY@UCDAVIS.EDU

Abbreviations used: DDT, dichlorodiphenyl-trichloroethane; DDD, dichlorodiphenyidichloro-ethane; PCBs, polychlorinated biphenyls; HCH,hexachlorocyclohexane; HCB, hexachlorobenzene;PGC, primordial germ cells; AFP, a-fetoprotein; DES,diethylstilbestrol; GLEMEDS, Great Lakes embryomortality, edema, and deformity syndrome; PAHs,polyaromatic hydrocarbons.

lethal doses of the pesticide, resulting inlarge losses of urban birds.

Contemporaneous with DDT use tocontrol Dutch elm disease, DDD (a DDTanalog) was used to control gnats in ClearLake, California (2,3); this resulted in thefirst well-documented ecological magnifi-cation of an organochlorine in inverte-brates, fish, and birds. Nesting westerngrebes exhibited breeding failure after thefirst applications of DDD to the lake in1949 and significant adult mortality aftertreatment in 1954. Eggshell thinning andembryo mortality were evident in nestinggrebes through 1971, 14 years after the lastDDD treatment.

Silent Spring emphasized mortality ofbirds due to biomagnification of organo-chlorines and eggshell thinning by DDTmetabolites as primary causes of reproduc-tive impairment. Subsequent research hasalso identified other pesticides and indus-trial chemicals that cause mortality andreproductive impairment, which affectsboth embryos and adult birds. The effectson embryos include mortality or reducedhatchability, failure of chicks to thrive(wasting syndrome), and teratologicaleffects that produce skeletal abnormalitiesand impaired differentiation of the repro-ductive and nervous systems throughmechanisms of hormonal mimicking ofestrogens. The range of chemical effects onadult birds covers acute mortality, sub-lethal stress, reduced fertility, suppressionof egg formation, eggshell thinning, and

impaired incubation and chick rearingbehaviors (4). The types of pollutantsshown to cause reproductive effects includeorganochlorine pesticides and industrialpollutants, organophosphate pesticides,petroleum hydrocarbons, heavy metals,and in a fewer number of reports, herbi-cides, and fungicides.

Background StudiesThe urban and agricultural use of DDTand other organochlorine pesticidesresulted in localized high-residue levels insoils and plants; runoff resulted insignificant aquatic residues in estuaries,resulting in bioaccumulation by fish andpredatory birds. For example, reproductivefailure of grebes (3), ospreys (5), peregrinefalcons (6,7), and bald eagles (8,9) wascaused primarily by urban and agriculturalinsect control measures. Point source pol-lution from manufacturing plants wasresponsible for reproductive failure ofcormorants and pelicans in southernCalifornia (10-13). Breeding failures andhigh organochlorine levels in aquatic birdsnesting in the Great Lakes implicatedDDE, polychlorinated biphenyls (PCBs),dioxins, and dibenzofurans (14-16).

Eggshell thinning and breeding failureof raptors and seabirds (11,14,17,18) weredocumented with DDT and its metabolites(19). DDT, however, was not the onlypesticide or pollutant to affect reproduc-tion in birds. Other persistent organochlo-rine pesticides with documented effects

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included dieldrin, endrin, aldrin, mirex,kepone, chlordane, toxaphene, hexa-chlorobenzene, and lindane (20). Most ofthe organochlorines contributed only in aminor way compared to DDT and dield-rin, and most were banned from use in theUnited States in the early 1970s. Manycontinue to be used in Asia, Africa, andSouth America (21,22).

In estuaries, the environmental buildupof industrial chemicals such as PCBs anddioxins also occurred during the 1950s and1960s. Documented exposures to birds,especially in the Great Lakes (23), LongIsland Sound (24), Puget Sound (25,26),and San Francisco and San Diego Bays(27,28), were correlated with declines inpopulations of fish-eating birds. In thesecases, the causative agent(s) was difficult topinpoint because several organochlorinesand heavy metals (copper, mercury, sele-nium, tributyl tin) were often found incomplex mixtures.

Organochlorine CompoundsOrganochlorine compounds includePCBs, dioxins, dibenzofurans, and manypersistent pesticides including DDT,kepone, cyclodiene pesticides (dieldrin,aldrin, and endrin), lindane (HCH), andhexachlorobiphenyl (HCB), toxaphene,and chlordane. Most of the persistentorganochlorine pesticides have beenremoved from the market in Europe andNorth America, but many are still in usein Africa, Asia, and South America.Endosulfan, methoxychlor, and dicofolremain in use in the United States becausetheir persistence and potential for bioaccu-mulation is lower. PCBs, dibenzodioxins,and dibenzofurans became environmentalpollutants only through industrial wastedisposal, waste incineration, or as contami-nants in the herbicides 2,4-D and 2,4,5-T.PCB disposal is now largely a historicalproblem rather than a continuing inputinto the environment. Incinerators andkraft-process paper pulp bleaching mills arestill sources of dibenzodioxins and diben-zofurans, but the discharge of dioxins isbeing reduced by conversion of pulp millsto nonchlorine bleaching processes (29).

Most dasses of organochlorines are rep-resented by many congeners (75 dibenzo-dioxins, 135 dibenzofurans, and 209PCBs), and complex mixtures of theseorganochlorines are typically foundtogether in environmental samples (sedi-ments, tissue, or egg residues). The acutetoxicity of individual congeners varies overseveral orders of magnitude, with the

2,3,7,8-chlorinated dioxins and coplanarPCBs being the most toxic (30,31).

At Scotch Bonnet Island in LakeOntario and on Santa Barbara Island insouthern California, observed abnormalbehaviors of breeding gulls were associatedwith organochlorine pollutants (32,33),leading to the hypothesis that o,p'-DDT,mirex, and some PCBs are estrogenicat environmental concentrations andresponsible for hormonal disruptions ofbreeding birds and abnormalities in theiroffspring (34,35).

Field and laboratory data gathered overthe past two decades indicated that themechanisms of action of organochlorinepollutants on reproduction in birds arequite diverse. The field observations andthe effects seen in birds have been very use-ful in predicting effects in other wildlifespecies, such as mink, snapping turtles, oralligators (36-38). Hormone-disruptingeffects are a result of organochlorines mim-icking the action of estrogens; the xenobi-otic hormone disruptions are complex, andeffects in birds and mammals may be quitedissimilar because steroid hormone controlof reproductive system differentiation byestrogens and androgens is different inmammals and birds. An understanding ofthe control of differentiation of the repro-ductive tracts in mammals and birds is nec-essary to understand differences inxenobiotic estrogen effects in these twoclasses of vertebrates.

Sexual Differentiation ofBirds and MammalsIn both birds and mammals, sex determi-nation and control of differentiation arelinked to the heterogametic sex. In mam-mals the heterogametic sex is the male,with a XY sex chromosome complement(female XX), while in birds the female isthe heterogametic sex (ZW, with malebeing ZZ). In birds and mammals, thehomogametic sex is the "default" sex, i.e.,the phenotype into which the embryo willdevelop in the absence of the sex-specifichormones and other compounds that causesex differentiation. In mammals the defaultsex is female, and without expression ofspecific gene products initiated by genes onthe Y chromosome, the embryo will differ-entiate into a phenotypic female. In birds,the default sex is male (ZZ); phenotypicdifferentiation of the embryo into a malewill occur unless specific female gene prod-ucts are translated and estradiol is synthe-sized, causing differentiation of the gonadinto an ovary.

In both birds and mammals, the initialorganization of the gonad is similar, withan indifferent gonad developing as a geni-tal ridge protruding into the dorsal bodycavity cranial to the kidneys. In mammals,expression of the testicular organizer genelocated on the Y chromosome induces con-densation of cells into the presumptiveseminiferous tubules (39). Primordial germcells (PGC), which originate as extraem-bryonic cells in the yolk sac of both birdsand mammals, migrate into the indifferentgonads at mid-gestation. In mammals, thePGC become localized in the default loca-tion of the ovarian cortex or, under theinfluence of testosterone, the PGC migrateinto the seminiferous tubules and becomethe primary spermatogonia.

In birds, the PGC migrate into thedefault location of the seminiferous tubulesin males (40). Development of the ovarianarchitecture occurs when estradiol is syn-thesized by the gonad, causing localizationof the PGC in the cortex of the left ovaryrather than in the presumptive seminiferoustubules. Estradiol additionally causes regres-sion of the right gonad and suppression ofthe synthesis of a glycoprotein, Mullerianregression factor, which, in the absence ofestrogen, causes regression of the develop-ing oviducts in males. Estradiol is respon-sible for retention of the left Mullerianduct and for its differentiation into thefunctional left oviduct and shell gland.

Because of the differences in steroidhormonal control of sexual differentiationin birds and mammals, xenobiotic estro-gens have different effects on birds andmammals during embryonic development.In male birds, the primary differentiationof the testes will be altered by estrogensthat stimulate PGC to become localized inthe cortex of the gonad in addition to thenormal development of seminiferoustubules and localization of the normalPGC within the medulla of the gonad. Thenumber of PGC that become localized inthe cortex is estrogen dose dependent, withlow doses resulting in only a few PGClocalized in the cortex and large doses'resulting in a layer of cortical PGC similarto the cortex of an ovary (35). The corticalPGC differentiate into primordial folliclesby entering into meiotic prophase, typicalof ovarian PGC. The seminiferous tubulesare retained with a reduced number ofPGC in the gonadal medulla of estrogen-treated males; they provide histological evi-dence of the male genetic sex of theembryo, even in embryos exposed to highlevels of estradiol in which the gross shape

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of the gonad is converted to the ovarianform. Estrogen exposure to female embryosdoes not cause alteration of the structure ofthe ovary in birds, but does result inoviduct changes.

Differentiation of the accessory sexualducts is altered by estrogen exposure in adose-dependent fashion. In male gulls andin chickens, the left oviduct may beretained in males at hatching, in additionto the retention of the vasa deferentia(40,41). The right oviduct is frequentlyretained as a small edematous vestigialtubule, not usually more than 5 to 6 mmin length. In females, the left oviduct is notgrossly altered, but an abnormally largeright oviduct may be retained. Functionalchanges in the left oviduct and shell glandmay occur when female chicks reachadulthood, as exposed birds lay eggs withdefective, thin, or soft shells (42).

In mammals, the effect of exogenousestrogen exposure is qualitatively differentthan in birds because testosterone controlsthe differentiation of the gonads. Estrogenis normally present in the fetal circulationfrom maternal sources but is sequestered byax-fetoprotein (AFP), which has a highestrogen binding affinity and protects thefetal tissues from estrogen exposure (39). Itwould be expected, therefore, that andro-gen analogs would have much more of aneffect on primary sexual differentiation inmammals, in contrast to the estrogen effectsin birds.

In mammals, the dose dependency andeffects of exogenous estrogens may bespecies specific because of the large speciesvariation in circulating maternal estrogensand circulating levels of AFP, which bindestrogens, reducing or preventing estrogenbinding to fetal tissue receptors. Xenobioticestrogens are made up of many chemicalforms, however, and may not bind withequal affinity to the estrogen receptor andAFP, possibly resulting in circulating levelsof xenobiotic estrogens that exceed thebinding capacity ofAFP in the fetal circula-tion. Estrogens do not control differentia-tion of the primary sexual apparatus inmammals, but they do have modifyingeffects on the uterus and brain, as has beendemonstrated with human fetal exposure toDES (43).

Reproductive Effects ofXenobiotic Estrogenson Bird EmbryosTo date the only xenobiotic estrogens thathave been identified to have effects onavian differentiation have been lipophilic

organochlorines, which bioaccumulate andare deposited into the yolk of eggs. Severalorganochlorine compounds have beenidentified as weak estrogens or precursorsof estrogens produced by liver hydroxyla-tion (44-46). Organochlorine pesticidesidentified as estrogenic include kepone,o,p'-DDT, methoxychlor, endosulfan, anddicofol (34,46-48).

o,p'-DDT or methoxychlor injectioninto gull eggs mimics the action of estro-gens or DES (41) and results in abnormali-ties of both male and female embryos.Males are feminized, with primordial germcells becoming localized in the cortex ofthe gonad as well as in the seminiferoustubules. In gulls, the amount of ovarian-type cortical tissue is dose dependent, as isthe retention of the left and right oviduct(35). In females, the right oviduct may beonly partially regressed. The qualitativeeffects of o,p'-DDT or methoxychlor weresimilar to estradiol treatment, with estra-diol being more than 100-fold more potentthan o,p'-DDT.

Estrogen receptor binding studies witho,p'-DDT, methoxychlor, or their hydroxy-lated metabolites (47) indicate that thebinding affinity of the parent pesticide islow, but a hydroxylated metabolite mayhave a binding affinity very similar to estra-diol. Significant hormonal activity can beproduced when only a fraction of the par-ent pesticide is metabolized. The extent oforganochlorine pollutant metabolism isdependent upon liver enzyme induction,and liver mixed-function oxidases becomeinducible by several classes of organochlo-rines midway through embryonic develop-ment (49). Avian embryos are particularlyat risk from metabolite activation becausethe metabolite products are not excretedfrom the egg but remain in the blood circu-lation throughout incubation. The normalnitrogenous metabolic wastes are seques-tered in the allantois as a semisolid slurry ofurates, and water-soluble metabolites ofxenobiotics will remain in the circulation.

Hydroxylated PCB congeners also havebeen identified as estrogenic (50,51), witha large variation in potency between hy-droxylated metabolites. In experimentalstudies the enzymatic hydroxylation can bemanipulated by the dosing regimen, withsmall initial doses of PCBs causing theinduction of liver microsomal enzymes andsubsequent larger doses being rapidlyhydroxylated to active estrogens (52).Most of the hydroxylated metabolitesformed are more water soluble than theparent congeners, and most were thought

to be excreted in the urine of mammals(53). However, retention of 13 hydroxy-lated PCB metabolites at high levels hasrecently been shown in humans, rats, andseals (54), indicating both that hydroxyla-tion is a widespread metabolic pathwayand that hydroxylated metabolites may beretained in the circulation or fat.

Other Classes ofXenobiotic EstrogensAlkyl phenols, widely used as wettingagents, surfactants, and industrial chemicaladditives, are also estrogenic (55) and havebeen demonstrated to have adverse effectson fish downstream of municipal waste-water discharges. In response to alkyl phe-nol exposure, male fish are reported tosynthesize vitellogenin, an estrogenic pro-tein synthesis by the liver and normallyexpressed only in females. No studies todate have implicated alkyl phenols as beingestrogenic in birds.

Many plants synthesize isoflavanoidphytoestrogens, which may have eitherestrogenic agonist or antiestrogenic effectson estrogen receptor binding (56). Mostdo not have significant effects on avianreproduction but may be used as chemicalcues to modify reproduction. Variations inlevels of isoflavanoids in clover and otherlegumes have been implicated in affectingreproduction in wild quail (57).

The extent to which animals are at riskfrom estrogenic xenobiotics is difficult toestimate. Animals have been exposed tophytoestrogens for many generations andhave apparently developed metabolicpathways to adjust to this exposure fromnatural sources. Most hydroxylatedmetabolites of organochlorines are weakestrogens, they are unlikely to be bioaccu-mulated because of their water solubility,and they will be excreted in the urine ofadult animals before reaching concentra-tions high enough to adversely affect adultreproductive function. Embryonic animals,however, are sensitive to permanent devel-opmental effects of estrogens, and the riskof exposure to hydroxylated organochlo-rines is largely unknown. The binding con-stants for organochlorines to AFP may bevery different from binding constants forsteroidal estrogens, and exposure of thefetus will be a complex function of mater-nal or fetal liver hydroxylation, estrogenreceptor binding, AFP sequestration, andmaternal urinary excretion. The exposurerisk for avian embryos is also very differentfrom that of mammals. The embryonicliver is capable of responding to induction

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by organochlorines, as mixed-function oxi-dases are active in the last half of incuba-tion (49). If hydroxylated metabolites withestrogenic activity are produced, they willremain in the embryonic circulationthroughout embryonic developmentbecause water is recycled within the egg asnitrogenous wastes are sequestered as semi-solid urates in the allantois. Avian embryosare also at higher risk than mammalianembryos because the phenotypic determi-nation of sex is estrogen dependent. Theopportunity for embryonic exposure tomuch higher concentrations of xenobioticestrogens is also a factor because thelipophilic organochlorines are selectivelydeposited in the high lipid yolk of eggs,especially in raptors and fish-eating birds.The combination of food chain exposureand estrogen dependence of sexual differ-entiation is almost certainly responsible forthe field observations of estrogenic effectsin birds. To date, only colonial fish-eatingbirds breeding in "hot spots" of contami-nation have been reported with estrogenicdevelopmental defects.

The likelihood that gulls in the wildwere suffering population effects of estrog-enization of males was tested by Fry andcoworkers (34,35); experiments demon-strated that levels ofDDT found in eggs insouthern California caused feminization ofmale embryos. They postulated that thetemporal and geographical localization offemale-female pairing, supernormalclutches of eggs in gull nests, and sex ratioskew of breeding gulls was due to reducednumbers of male breeders at the colony.These effects were due to feminization ofembryos and either chemical neutering ofthe hatched chicks or differential survivalof chicks.

In this review, only direct effects of pol-lutants on the reproductive system havebeen examined. Developmental effects onbehavior also occur with in ovo exposure ofestrogens, which have the potential to alterthe structure and function of the centralnervous system. The complex topic ofestrogen control of brain differentiationand behavior has been recently addressedby Adkins-Regan et al. (58).

Other Effects of Pollutants onAvian Embryos and ChicksEgg-borne pollutants and direct applica-tion of pollutants to eggs have been docu-mented to cause mortality, reducedhatchability, terata, and reduced survival ofchicks hatched from eggs. In addition toorganochlorines as causative agents, heavy

metals, petroleum hydrocarbons, and pesti-cides have been identified. Adverse effectson survival and hatchability of eggs aredocumented with bioaccumulation ofdioxins (59,60) and selenium (61), both ofwhich are pollutants more toxic to embryosthan to adults and which bioaccumulateinto yolk to concentrations that becometoxic to embryos. Sublethal effects pro-duced by these compounds include subcu-taneous and cardiac edema and terata ofthe beak, axial skeleton, and heart. Severalsites within the Great Lakes that are pol-luted with PCBs and other organochlorineshave produced abnormalities in embryosand chicks of bald eagles, cormorants,gulls, and terns. The consistent pattern ofedema, beak malformations, cardiacedema, and skeletal malformations hasbeen termed GLEMEDS (Great Lakesembryo mortality, edema, and deformitysyndrome); the syndrome correlates withdioxin toxic equivalents, which are primar-ily a result of bioaccumulation of coplanarPCB congeners (PCB 126, 169, and 77being the most toxic congeners). Seleniumcontamination through bioaccumulationfrom food-chain magnification of agricul-tural drainwater metals in high seleniumsoils in several low rainfall regions has beenresponsible for deformities of waterfowl andshorebirds in the Kesterson Wildlife Refuge,California (61), and in Nevada (62).

Direct application of toxicants at highconcentrations to wild bird eggs probablyoccurs rarely in the wild, but it may occurthrough transfer of contaminants such asspilled petroleum oil from the plumage ofcontaminated incubating birds or fromdirect application of agricultural chemicalsto eggs in nests adjacent to agriculture.Hoffman (63) has reviewed this data andsummarized the toxicity and teratogenicityof products applied directly to eggs.Mortality and reduced hatchability of eggswere caused by petroleum oils [the mosttoxic components are the polyaromatichydrocarbons (PAHs)], organophosphateinsecticides, some herbicides (paraquat,trifluralin, prometon, and others) andfungicides (maneb). Dose dependency ofmany of the products has not been estab-lished for direct application toxicitybecause the solvent vehicle is an importantdeterminant of toxicant penetrationthrough the eggshell and, therefore, forexposure determination. Most of the prod-ucts tested were also teratogenic at sub-lethal levels. The PAH fractions ofpetroleum oils produced liver necrosis,edema of heart, and enlargement of the

spleen (64-66). Refined oils and crank-case oils studied by several workersreviewed by Hoffman (63) were also toxicand teratogenic, with PAHs and metalcontaminants being most toxic. Organo-phosphate insecticides caused axial skele-ton malformations (scoliosis and lordosis),edema, and stunted growth. The toxicitywas compared with application rates, andrelative risk for the organophosphatestested was highest for malathion, withdecreasing risk for dimethoate, diazinon,parathion, and acephate. Carbamate insec-ticides did not cause terata at expectedenvironmental exposure concentrations,and of nine fungicides tested only manebcaused malformations (63).

Reproductive Effectsin Adult BirdsMortality of birds is not a specific repro-ductive effect, but on a population level,reproduction is impaired due to decreasednumbers of breeding birds and decreasedfitness of remaining adults. Sublethal expo-sures may adversely affect reproductionthrough nonspecific morbidity or increasedstress, which results in cessation of lay,interruption of incubation, or reduced careof chicks. Petroleum oil exposure to breed-ing birds, either by exposure of theplumage or by ingestion of oil, causesincreased stress with elevated circulatingcorticosterone and apparent feedbackdown regulation of reproduction at thepituitary level (67-69). Oil exposure willcause cessation of egg yolk formation (70),which results in reduced lay or abandon-ment of breeding. Laboratory exposurestudies have been reviewed by Albers(71,72), demonstrating considerable vari-ability in sensitivity to hydrocarboninduced hemolytic anemia (73-75) andinduction of liver mixed-function oxidases(76)-effects that appear to contribute toincreased stress and reduced breeding suc-cess. Field studies (77) have shown thatexposure to 0.1- to 2.0-ml weathered crudeoil is sufficient to prevent or impair eggformation and egg laying, incubation, andstability of the pair bond. Trivelpiece et al.(69) showed that field exposure of adultstorm-petrels during the chick-rearingperiod caused reduced foraging and fooddelivery by adults, which resulted indecreased growth or death of chicks.

The best documented and notoriouseffect of environmental pollutants on birdsis eggshell thinning caused by DDE; thisresults in crushed eggs and breeding failureof many sensitive raptorial and fish-eating

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birds (10,17,18). Eggshell thinning iscorrelated with DDE inhibition of shellgland calcium ATPase (78,79), and thespecies most susceptible to eggshell thin-ning appear to have reduced ability tometabolize organochlorines (80). Whetherthe increased sensitivity to eggshell thin-ning is related to differences in liver metab-olism of organochlorines is unknown.

Organochlorine pollutants and organo-phosphate pesticides may also influence thebreeding bahavior of exposed birds. Herringgulls breeding on Scotch Bonnet Island,Lake Ontario, showed decreased incubationattentiveness and decreased defense of terri-tories correlated with a mix of organochlo-rines (32,81). Incubation and chick-rearing

behavior impairment has also been corre-lated with organochlorine exposure to ringdoves (82) and merlins (83). Parathion hasbeen correlated with altered incubationbehavior in experimentally exposed mallardsand laughing gulls (84,85).

The effects of pollutants on reproduc-tion are mediated at many different physio-logical levels. The diversity and extent ofeffects have been impossible to predictbecause many of the biochemical mecha-nisms of the side effects of agriculturalchemicals are unrelated to the specificmechanisms of action of the designed use.The unexpected side effects, such aseggshell thinning by DDE or estrogeniceffects of op'-DDT, could not be predicted

before initial use of the compounds, andthe bioaccumulation and ecologicalmagnification consequences were notanticipated. The positive value of monitor-ing wild bird populations has been demon-strated with the observations of ecologicalinjury that have occurred with misuse ofpesticides and irresponsible pollutant dis-posal. The adverse effects of chemicals onwildlife have been signals for revision oflaws and implementation of new regula-tions to prevent adverse effects on humanpopulations, but only through continuedwildlife monitoring will new, unexpectedside effects of chemicals in the environmentbe observed and corrected.

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