Final Report: Endocrine Disruption in Fish and Birds

EPA Grant Number: R825433C003
Subproject: this is subproject number 003 , established and managed by the Center Director under grant R825433
(EPA does not fund or establish subprojects; EPA awards and manages the overall grant for this center).

Center: EERC - Center for Ecological Health Research (Cal Davis)
Center Director: Rolston, Dennis E.
Title: Endocrine Disruption in Fish and Birds
Investigators: Fry, D. Michael , Hinton, David E. , Wilson, Barry W.
Institution: University of California - Davis
EPA Project Officer: Packard, Benjamin H
Project Period: October 1, 1996 through September 30, 2000
RFA: Exploratory Environmental Research Centers (1992) RFA Text |  Recipients Lists
Research Category: Center for Ecological Health Research , Targeted Research


The objectives of this research project were to: (1) evaluate the endocrine-disruptive effects of active pesticide ingredients (methoxychlor, dicofol, and octylphenol) on bird development using in vitro approaches and whole animal field studies; and (2) investigate the development of the central nervous system and reproductive tracts of embryos and newly hatched chicks exposed to endocrine-active xenobiotic compounds.

Summary/Accomplishments (Outputs/Outcomes):

In our in vitro studies, we dosed neonatal zebra finches and Japanese quail with estradiol benzoate, octylphenol, methoxychlor, and dicofol. We evaluated the developmental changes to reproductive behavior by testing birds when they became adults. Our studies with zebra finches demonstrated that the gonad and oviducts of hatchlings are sensitive to estrogens and may be sensitive to disruption at the same stages as the brain. Components of many pesticides and other environmental contaminants have estrogenic properties.

We used egg injections to dose Japanese quail for characterization of gonadal maturation and estrogenic changes during maturation. We examined the maturation of the testes in birds hatched from dosed eggs. Dosed male quail developed clusters of primary oocytes or a cortical ridge of oocytes, similar to the feminized testes of other species.

With cliff swallows, we conducted field studies to evaluate the ecosystem effects of pesticides and other endocrine disruptors in Yolo County. We developed methods of quantifying alkylphenols and alkylphenol ethoxylates in food samples of wild swallows and water samples taken from agricultural drains to evaluate the magnitude of estrogenic chemicals entering the watershed. We characterized the reproductive success of colonies of cliff swallows nesting in Yolo County and their exposure hazard from all pesticides, including endocrine disruptors. We measured the reproductive success of cliff swallows in 20 nests per colony by directly observing eggs and chicks two to three times per week. In 1999, we evaluated the exposure hazard from pesticides throughout the county by correlating data from pesticide use reports. In addition, we made significant progress in developing an immunoassay for the quantification of octyl- and nonylphenols. This immunoassay will be useful for monitoring alkylphenols in agricultural runoff and throughout the watershed in general.

A final objective of our project was to develop suitable markers for evaluating the effects of endocrine-disrupting compounds on insectivorous birds feeding on insects in agricultural fields and drains. Thus, we developed techniques that harness the altered sizes of song nuclei in birds, as a biomarker of exposure to estrogenic chemicals. Male birds have a song nucleus approximately three times the volume of females, which is sufficiently different from females to provide a good indicator of altered development following neonatal exposure to estrogenic chemicals.

The following activities were accomplished:

• We developed techniques that harness the altered size of song nuclei in birds as a biomarker of exposure to estrogenic chemicals in the field. Male birds have a song nucleus approximately three times the volume of females, which is sufficiently different from females to provide a good indicator of altered development in females following neonatal exposure to estrogenic chemicals. This biomarker can be used widely by investigators to assess the impacts of estrogenic chemicals on bird development.

• We established a zebra finch colony with very high productivity and fledging success at the University of Calfornia–Davis. More than 400 chicks were hatched in the first 8 months of 1998 from 30 breeding pairs. This colony continues to be utilized for studies by researchers.

• We detected significant histological abnormalities in zebra finches and Japanese quail exposed as embryos or hatchlings to estradiol and estrogenic xenobiotics. Exposure to estrogenic compounds caused the formation of feminized testes, but ovarian follicles in feminized testes degenerate and disappear by day 21 posthatch. The degeneration may be related to the hormonal changes occurring at adolescence. This information will provide a basis for further study on the longer term effects of feminization occurring in early life stages of birds.

• In zebra finches, we observed significant changes in adult reproductive behavior following neonatal dosing with environmentally relevant amounts of octylphenol and methoxychlor. Oral dosing of zebra finch chicks on days 5-11 after hatching with 3.8-380 µg/g body weight/ day E2B produced altered courtship and singing behaviors in both males and females, expressed when the birds became adults. Our findings implicate estrogenic chemicals in exerting a delayed, but definite, impact on bird reproductive behaviors. This information deserves careful consideration by environmental management and regulatory agencies.

• Neonatal exposure to estrogens caused demasculinization of male zebra finch behavior, including reduced interest in females, suppression of copulatory behavior, increased latency, and increased broodiness. Again, these data show that estrogenic chemicals can have a significant impact on the reproductive development of birds, and environmental management and regulatory agencies should take note.

• We found that dosed females become capable of singing after treatment with estrogen or octylphenol for 6 days after hatching. Because female zebra finches do not normally sing, these data indicate the powerful impacts of estrogenic chemicals on bird development.

• We devised a toxicity index for cliff swallow reproductive success to facilitate the comparison of field sites with diverse pesticide use. The total toxicity index was based on the LD50 of each pesticide artificially inseminated to bobwhite quail. It will be useful in determining levels of pesticides harmful to birds in various field sites, and both investigators and regulatory agencies will benefit.

• Agricultural chemical use in nesting areas showed positive trends with reduced hatching success, fledging success, reproductive success, and number of young fledged per active nest of cliff swallows. Environmental and agricultural regulatory agencies and policymakers can use this information to minimize pesticide impact on bird reproductive development.

• We currently are developing an immunoassay for the quantification of octyl- and nonylphenols. The assay, which uses conjugated haptens of tertiary octylphenol and technical nonylphenol, will be useful for investigators and managers monitoring alkylphenols in agricultural runoff and throughout the watershed in general.

Supplemental Keywords:

ecosystem, ecosystem protection, environmental exposure and risk, geographic area, international cooperation, water, terrestrial ecosystems, aquatic ecosystem, aquatic ecosystem restoration, aquatic ecosystems and estuarine research, biochemistry, ecological effects, ecological indicators, ecological monitoring, ecology and ecosystems, environmental chemistry, restoration, state, water and watershed, watershed, watershed development, watershed land use, watershed management, watershed modeling, watershed restoration, watershed sustainability, agricultural watershed, exploratory research environmental biology, California, CA, Clear Lake, Lake Tahoe, anthropogenic effects, aquatic habitat, biogeochemical cycling, ecological assessment, ecology assessment models, ecosystem monitoring, ecosystem response, ecosystem stress, environmental stress, environmental stress indicators, fish habitat, hydrologic modeling, hydrology, integrated watershed model, lake ecosystems, lakes, land use, nutrient dynamics, nutrient flux, water management options, water quality, wetlands., RFA, Health, Scientific Discipline, Water, Water & Watershed, Health Risk Assessment, Endocrine Disruptors - Environmental Exposure & Risk, endocrine disruptors, Biochemistry, Ecology and Ecosystems, Biology, Endocrine Disruptors - Human Health, Watersheds, pesticide exposure, avian development, fish, xenobiotic, Cliff Swallow, EDCs, endocrine disrupting chemicals, developmental biology, animal models, birds, pesticide runoff, reproductive processes, animal studies, Zebra Finches, ecological research

Relevant Websites: Exit

Progress and Final Reports:

Original Abstract
  • 1997
  • 1998
  • 1999

  • Main Center Abstract and Reports:

    R825433    EERC - Center for Ecological Health Research (Cal Davis)

    Subprojects under this Center: (EPA does not fund or establish subprojects; EPA awards and manages the overall grant for this center).
    R825433C001 Potential for Long-Term Degradation of Wetland Water Quality Due to Natural Discharge of Polluted Groundwater
    R825433C002 Sacramento River Watershed
    R825433C003 Endocrine Disruption in Fish and Birds
    R825433C004 Biomarkers of Exposure and Deleterious Effect: A Laboratory and Field Investigation
    R825433C005 Fish Developmental Toxicity/Recruitment
    R825433C006 Resolving Multiple Stressors by Biochemical Indicator Patterns and their Linkages to Adverse Effects on Benthic Invertebrate Patterns
    R825433C007 Environmental Chemistry of Bioavailability in Sediments and Water Column
    R825433C008 Reproduction of Birds and mammals in a terrestrial-aquatic interface
    R825433C009 Modeling Ecosystems Under Combined Stress
    R825433C010 Mercury Uptake by Fish
    R825433C011 Clear Lake Watershed
    R825433C012 The Role of Fishes as Transporters of Mercury
    R825433C013 Wetlands Restoration
    R825433C014 Wildlife Bioaccumulation and Effects
    R825433C015 Microbiology of Mercury Methylation in Sediments
    R825433C016 Hg and Fe Biogeochemistry
    R825433C017 Water Motions and Material Transport
    R825433C018 Economic Impacts of Multiple Stresses
    R825433C019 The History of Anthropogenic Effects
    R825433C020 Wetland Restoration
    R825433C021 Sierra Nevada Watershed Project
    R825433C022 Regional Transport of Air Pollutants and Exposure of Sierra Nevada Forests to Ozone
    R825433C023 Biomarkers of Ozone Damage to Sierra Nevada Vegetation
    R825433C024 Effects of Air Pollution on Water Quality: Emission of MTBE and Other Pollutants From Motorized Watercraft
    R825433C025 Regional Movement of Toxics
    R825433C026 Effect of Photochemical Reactions in Fog Drops and Aerosol Particles on the Fate of Atmospheric Chemicals in the Central Valley
    R825433C027 Source Load Modeling for Sediment in Mountainous Watersheds
    R825433C028 Stress of Increased Sediment Loading on Lake and Stream Function
    R825433C029 Watershed Response to Natural and Anthropogenic Stress: Lake Tahoe Nutrient Budget
    R825433C030 Mercury Distribution and Cycling in Sierra Nevada Waterbodies
    R825433C031 Pre-contact Forest Structure
    R825433C032 Identification and distribution of pest complexes in relation to late seral/old growth forest structure in the Lake Tahoe watershed
    R825433C033 Subalpine Marsh Plant Communities as Early Indicators of Ecosystem Stress
    R825433C034 Regional Hydrogeology and Contaminant Transport in a Sierra Nevada Ecosystem
    R825433C035 Border Rivers Watershed
    R825433C036 Toxicity Studies
    R825433C037 Watershed Assessment
    R825433C038 Microbiological Processes in Sediments
    R825433C039 Analytical and Biomarkers Core
    R825433C040 Organic Analysis
    R825433C041 Inorganic Analysis
    R825433C042 Immunoassay and Serum Markers
    R825433C043 Sensitive Biomarkers to Detect Biochemical Changes Indicating Multiple Stresses Including Chemically Induced Stresses
    R825433C044 Molecular, Cellular and Animal Biomarkers of Exposure and Effect
    R825433C045 Microbial Community Assays
    R825433C046 Cumulative and Integrative Biochemical Indicators
    R825433C047 Mercury and Iron Biogeochemistry
    R825433C048 Transport and Fate Core
    R825433C049 Role of Hydrogeologic Processes in Alpine Ecosystem Health
    R825433C050 Regional Hydrologic Modeling With Emphasis on Watershed-Scale Environmental Stresses
    R825433C051 Development of Pollutant Fate and Transport Models for Use in Terrestrial Ecosystem Exposure Assessment
    R825433C052 Pesticide Transport in Subsurface and Surface Water Systems
    R825433C053 Currents in Clear Lake
    R825433C054 Data Integration and Decision Support Core
    R825433C055 Spatial Patterns and Biodiversity
    R825433C056 Modeling Transport in Aquatic Systems
    R825433C057 Spatial and Temporal Trends in Water Quality
    R825433C058 Time Series Analysis and Modeling Ecological Risk
    R825433C059 WWW/Outreach
    R825433C060 Economic Effects of Multiple Stresses
    R825433C061 Effects of Nutrients on Algal Growth
    R825433C062 Nutrient Loading
    R825433C063 Subalpine Wetlands as Early Indicators of Ecosystem Stress
    R825433C064 Chlorinated Hydrocarbons
    R825433C065 Sierra Ozone Studies
    R825433C066 Assessment of Multiple Stresses on Soil Microbial Communities
    R825433C067 Terrestrial - Agriculture
    R825433C069 Molecular Epidemiology Core
    R825433C070 Serum Markers of Environmental Stress
    R825433C071 Development of Sensitive Biomarkers Based on Chemically Induced Changes in Expressions of Oncogenes
    R825433C072 Molecular Monitoring of Microbial Populations
    R825433C073 Aquatic - Rivers and Estuaries
    R825433C074 Border Rivers - Toxicity Studies