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The ability of environmental contaminants to affect reproductive and developmental processes in fish and wildlife species has long been known. An increasingly persuasive body of evidence indicates that many of these chemicals may be causing such effects through interference and disruption of normal endocrine function. Field observations have correlated abnormal sex organ morphology, unusual sex hormone levels and ratios, and altered physiological and biochemical processes with exposure to environmental contaminants. These developmental end points are under the control of the endocrine system, lending support to the hypothesis that environmental contaminants may disrupt endocrine function.
Environmental contaminants that can affect the endocrine system in animals, which controls important functions through communication of glands, hormones and cellular receptors, are known as endocrine disrupting compounds (EDCs). Many EDCs are associated with developmental, reproductive and other health problems in fish and wildlife, both in the field and the laboratory. In the past decade, efforts in this line of research have increased significantly in North America, Europe and Japan.
The Biological Resources Division (BRD) of the U.S. Geological Survey is engaged in a number of research projects dealing with endocrine disrupting chemicals. The Contaminant Biology Program in BRD has a wide diversity of innovative research projects dealing with EDCs to support science needs of Bureaus in the Department of Interior. Specific information about these projects are detailed below in five categories of research:
1) Chemistry
2) Reproduction
3) Stress
4) Immunology
Dr. Carl Orazio, Columbia Environmental Research Center, Columbia MO
(http://www.cerc.cr.usgs.gov/Brnch_Webs/EChem/index.htm)
Summary of Research: The Environmental Chemistry Branch conducts research to determine the presence, concentration, bioavailability, fate and distribution of endocrine disrupting chemicals (EDCs) in the environment. Our analytical chemistry research facility is equipped with a full range of instrumentation: liquid chromatography (LC), gas chromatography (GC), mass spectrometry (MS), LC/MS, high resolution MS, LC-ICP/MS, GC/MS. This allows discovery and measurement of an array of EDCs. We develop new cleanup and instrumental methods for identification of EDCs; conduct toxicity-directed class fractionation of organic and metal/metalloid chemicals; use passive devices for polar and non-polar EDCs; develop multidimensional methods of analysis to discover new EDCs within complex mixtures. It is fair to say that we can conduct analysis and fate research on nearly all commonly listed EDCs: Persistent Organohalogens including dioxins and furans, PBBs, hexachlorobenzene, octachlorostryrene, and pentachlorophenol. Pesticides: 2,4,5-T, 2,4-D, alachlor, aldicarb, atrazine, beta-HCH, carbaryl, chlordane, gamma-cyhalothrin, cis-nonachlor, cypermethrin, , DDT, DDT metabolites, dicofol, dieldrin, endosulfan, esfenvalerate, ethylparathion, fenvalerate, heptachlorepoxide, heptachlor, kepone, lindane, methoxychlor, mirex, oxychlordane, permethrin, synthetic pyrethroids, toxaphene, trans-nonachlor, and trifluralin. We can set up to conduct environmental chemical analysis of the remainder of commonly listed EDC pesticides. Our program includes research and analysis of phthalates, arsenic, cadmium, lead, and mercury, other metals and heavy metals. We have published our findings of drug estrogens, birth control pills in river waters. And we have published at study showing bisphenol A, a potent estrogenic endocrine disruptor, leaches into water from polycarbonate cages that are commonly used to house animals for estrogenic endocrine disruption studies.
Objectives of current work: 1. Expand our use of the polar organic chemical sampler (POCIS) in combination with the yeast estrogen screening assay (YES) to detect estrogenic activity in aquatic systems. 2. Continue our thyroid disrupting polybrominated diphenyl ether flame retardants (PBDEs) research: a) use our recently developed definitive GC/HRMS methods for analysis of PBDE congeners; b) complete a study on environmental sources of PBDEs; c) publish study on bioconcentration of PBDEs in various organisms/tissues; d. continue study of indoor air PBDE contamination in US and Russia 5. Continue collaboration with research managers to determine trophic transfer studies of various organochlorine EDCs. 6. Use semipermeable membrane device (SPMD) investigations to determine biological exposure to EDCs in air and aquatic ecosystems. 7. Set up for analysis of atrazine waters from aquatic organism study. 8. Develop our ability to detect pharmaceuticals in rivers using POCIS and LC/MS. 9. Finish our project that is tracking snowmobile engine exhaust in national parks, 10. Continue our role in assessing pathway of exposure for natural resources caused by dioxins, furans, PCBs, pesticides, metals. 11. Set up method for tracking penta-nonylphenols in Florida municipal effluent. 12. Continue to identify interferences in analysis of EDCs at environmentally relevant concentrations. 13. Develop cleanup methods of analysis of EDCs in diverse matrices: high lipid biological tissues, organic-rich sediments, POCIS, SPMDs. 14. Develop LC/MS methods for polar EDCs. 15. Development of methods for the LC-ICP/MS chemical speciation of organomercury and organoselenium compounds 16. Complete research related to food chain accumulation of mercury in California fish for human health consumption assessment. 17. Conduct study to determine environmental distribution of heavy metals in pore waters and sediments from mining areas within Mark Twain National Forest.
Dr. Tim Gross, Florida Integrated Science Center, Gainesville FL
(http://cars.er.usgs.gov/Environmental_Contaminants/environmental_contaminants.html
)
Summary of Research: The FISC contaminants (ecotoxicology) program at Gainesville Florida has a series of ongoing projects that focus on "endocrine disruption". These efforts include: 1) An evaluation of the endocrine disrupting effects of organo-chlorine pesticides in American alligators (Alligator mississippiensis) and fish, as well as potential interactions with other environmental stressors or factors, 2) An assessment of endocrine active components in papermill effluents in fish, 3) the development of models to assess effects of endocrine active compounds in complex mixtures using fish, invertebrates and alligators as models, 4) An evaluation of mercury as a non-receptor mediated endocrine disruptor in fish and freshwater mussels, 5) an evaluation and identification of "endocrine disrupting" chemicals associated with exposure to wastewater reuse or discharge and effects in fish, 6) An evaluation of atrazine as an endocrine active agent in fish, reptiles and amphibians, and 7) An evaluation of bioaccumulation of "endocrine active agents" in fish and birds and the interactions with or influence of soil components and reclamation processes. These efforts utilize paired field and laboratory studies, as well as an evaluation of mechanisms of action and effects from the molecular to the organism level of function.
Objectives of current work: The primary objectives of the FISC-ecotoxioclogy program efforts in "endocrine disruption" is to identify chemical contaminants that may exert "endocrine disrupting" effects in aquatic species either by direct receptor mediated action or by other indirect modes of disruption on endocrine function. In addition, a primary objective is the elucidation of adverse effects associated with exposure to "endocrine disrupting" contaminants and the potential for subsequent population, community and impacts on reproductive endpoint function.
Dr. Robert Grove, Forest and Range Ecosystem Science Center
(http://fresc.usgs.gov/sitemap.html)
Summary of Research: Our recent research has focused on river otters and environmental contaminants in the Pacific Northwest. Our preliminary work pointed to possible reproductive organ hypoplasia in young male river otters (Lutra canadensis) . An in depth study was instituted to determine whether the preliminary data was real or not. At this time, we still do not have an answer, though colleagues from B.C. Canada have observed similar findings in mink. Further data analyses of the otter data we collected from Oregon and Washington is needed before any conclusions can be drawn. Hopefully, reports will be available by fall of this year. We do, however, have a good data set on reference concentrations of contaminants (OCs, PCBs, dioxons, furans) for juvenile, yearling, and adult male river otters form Oregon and Washington. We have also been looking at other contaminants of interest (i.e. organotins, perfluorooctanesulfonates).
Objectives of Current Work: To finish data analyses, thesis writing, and publications.
Dr. Miguel Mora, Brazos Bend, TX Field Station
(http://www.cerc.cr.usgs.gov/FRS_Webs/Brazos1/index.htm )
Summary of Research: Research is currently underway to evaluate the potential effects of endocrine disrupting substances and other contaminants on birds from the Rio Grande using cliff (Hirundo pyrrhonota) and cave swallows (H. fulva) as indicator species.
Objectives of current work: The objectives of this study are: 1) to determine the relationship between hormone levels and concentrations of contaminants in bird tissues; 2) to examine potential DNA damage in blood cells using flow cytometry; 3) to measure P450 aromatase activity in gonads of adults and chicks as possible indicators of exposure and effects of contaminants on sex ratio; 4) to determine exposure and effects of anticholinesterase pesticides by measuring brain cholinesterase activity; and 5) to use stable isotopes for elucidating potential sources of contaminants in wintering and breeding areas.
Ms. Jessica Noggle, Florida Integrated Science Center
(http://cars.er.usgs.gov/Environmental_Contaminants/environmental_contaminants.html)
Objectives of current work: • To determine utility of mosquitofish for pulp & paper mill effluent exposure screening and testing. • To evaluate potential impacts of pulp & paper mill effluent on reproduction in mosquitofish Summary of Research: Female Gambusia hollbrooki, or eastern mosquitofish, respond to pulp & paper mill effluent exposure by developing male-like secondary sex characteristics. Specifically, the female anal fin elongates into a structure resembling a maturing male's gonopodium, or copulatory structure. A popular hypothesis explaining this phenomenon involves water-borne exposure to androgens derived from bacterially-degraded plant sterols, one of the many chemical constituents in pulp & paper mill effluents. In light of this hypothesis, sex steroids (estradiol and testosterone) have been examined in addition to anal fin morphology in female Gambusia, and as a final stage of this research reproductive success of females was evaluated. Anal fin elongation in females varied with mill and through time with mill process improvements. Indeed, at the primary effluent-receiving stream under study anal fin elongation is no longer observed, nor has it been induced under controlled exposure to whole effluent dilutions. The discharging mill has implemented major process changes in accordance with EPA's 2001 cluster rules, and further process changes are slated in the next two years. Sex steroids, measured by RIA as whole body tissue concentrations, initially were biased towards testosterone in effluent-exposed females, supporting the androgen hypothesis. However, further analysis indicates potential influence of gonad stage on hormone levels, complicating interpretation. Finally, initial evaluation of reproductive success (age-sex population structure, brood size & stage, and fry production) reveals reproduction is not impaired by effluent exposure, and may actually be increased via a longer reproductive season. This conclusion places female anal fin elongation as a marker of exposure, as opposed to a marker of adverse effect. Further, this conclusion leads to concerns of Gambusia's role in fish communities within effluent-receiving streams.
Dr. Diana Papoulias, Columbia Environmental Research Center, Columbia MO
(http://www.cerc.cr.usgs.gov/About/bchem_brnch.htm )
Summary of Research: My research interests include understanding the effects of endocrine disrupting chemicals on fish reproduction. Most recently, I have studied the effects of chemicals on sexual differentiation and development and established a fish model using the dr-R strain of Japanese medaka (Oryzias latipes) for testing chemicals for their potential to induce feminization or masculinization. I am also evaluating endocrine and histological biomarkers of fishes from contaminated sites for exposure to and effects of endocrine disruptors as part of general fish health assessments in order to direct resource management and research efforts.
Objectives of current work: Current work involves investigating the effects of atrazine on endocrine and functional aspects of fish reproduction. These preliminary lab studies using environmentally relevant concentrations with several species of fish are precursors to planned mesocosm studies.
Dr. Don Tillitt, Columbia Environmental Research Center, Columbia MO
(http://www.cerc.cr.usgs.gov/About/bchem_brnch.htm)
Summary of Research: Our interests in endocrine disruption are focused on effects on fish reproduction and development. We have developed and applied both laboratory and field models to evaluate endocrine disruption and reproductive performance in fish. Our studies generally have endpoints at the biochemical, physiological, histological, and organismal levels of biological organization, with the intent of developing linkages and biomarkers. We have a major effort on-going with atrazine focused on biomarkers and population effects in the environment. We are developing a study plan to begin investigations on the effects of mercury on gene expression and reproduction in fish. We oversee field monitoring efforts of the BEST Large Rivers Program for fish health monitoring. Additionally, we collaborate with numerous scientists on projects related to fish reproduction and development.
Objectives of current work: Develop tools and models for fish reproduction and development. Apply those tools and models to natural resource issues.
Dr. Alec G. Maule, Western Fisheries Research Center, Columbia River
Research Lab, Cook, WA
(http://wfrc.usgs.gov/labs/columbia.htm)
Summary of Research: Anadromous Arctic charr (Salvelinus alpinus) feed primarily while in the ocean—doubling their body mass in 6 to 8 weeks. During the remainder of the year, in freshwater, charr mobilize lipids as their main energy source. In an ecologically relevant lab experiment, we orally contaminated charr (0, 1, 10, 100 mg Aroclor 1254 kg-1 body mass) and fasted them for five months; other fish (0, 100 mg Aroclor 1254 kg-1 body mass) were fed. In subsequent performance tests, PCB-treated, fasted fish (1) had lower resting plasma cortisol titers and disrupted stress responses, (2) impaired osmoregulatory capacity, and reduced growth and survival in saltwater, and (3) impaired immune responses and reduced disease resistance. All of these physiological functions are regulated by glucocorticoid hormones. We also found that, while the capacity of interrenal cells to secrete cortisol was not impacted, the amounts of glucocorticoid receptors, hsp70 and hsp90 in the brain were reduced in PCB-treated fish Our results suggest that PCBs disrupt glucocorticoid responsiveness of neuronal cells involved in the negative feedback regulation of circulating cortisol levels.
Objectives of current work: To test these lab findings in the wild--i.e., Bear Island, Norway where one lake has charr with high PCBs (and other OCs) and another in which fish have very low PCBs. We'll combine performance measures (stress and immune responses) and gene (next 3-yrs). Followed by examination of reproductive and F-1 generation effects (following 3 to 5 yrs).
Dr. Steve McCormick, Leetown Science Center, Conte Anadromous Fish Research Center, Turners Falls, MA (http://www.lsc.usgs.gov/CAFLindex.asp )
Summary of Research: Endocrine disruption of smolting and ion regulation in Anadromous fish.
Atlantic salmon (Salmo salar) in Maine have recently been listed as an endangered species, yet the reason for this decline is unknown. Contaminants and their impact on the parr-smolt transformation have been suggested to be involved in the decline in Atlantic salmon populations in Maine and the limited success of restoration efforts in southern New England. While there is increasing knowledge on the sublethal impacts of contaminants on reproductive processes in fish, there is very little scientific information on the impacts of contaminants on other hormone driven developmental events such as the parr-smolt transformation. The studies outlined here will determine whether contaminants can act as endocrine disruptors of smolting and the freshwater-seawater transition in anadromous fish. Objectives of this project are the following:
1. Investigate the developmental effects of the environmental contaminants nonylphenol (NP), polychlorinated biphenyls (A1254), hexazinone, atrazine, and acid/aluminum on Atlantic salmon (Salmo salar) by integrating physiological and behavioral indices. These studies will attempt to answer the following principle objectives: A. To determine the capacity of contaminants to act as endocrine disruptors of the parr-smolt transformation by adversely affecting salinity preference and tolerance of smolts following exposure at different developmental stages. B. To determine how contaminant exposure affects smolt capacity to cope with stressful events (e.g., swimming fatigue, dam passage, and capture or handling) C. To investigate the mechanisms by which contaminant exposure affects seawater survival.
2. Monitor physiological changes in wild and hatchery-reared Atlantic salmon juveniles during the parr-smolt transformation and ocean entry to determine if smolting is being compromised by exposure to contaminants.
3. Develop non-lethal methods for determining whether Atlantic salmon have been exposed to contaminants (gene expression and levels of CYP1A, CYP19 and CYP2C; gill levels of aluminum).
Objectives of current work: Determine whether contaminants are disrupting seawater tolerance of Atlantic salmon and whether this is responsible for declines in salmon populations.
Dr. Vicky Blazer, Leetown Science Center, Leetown, WA
(http://www.lsc.usgs.gov/FHBindex.asp)
Summary of Research: Research to date at the Leetown Fish Health laboratory has primarily been directed toward providing histological assessment of fish gonads (and other tissues) for a variety of projects including the BEST monitoring program, NAWQA studies, Chesapeake Bay and Lake Erie fish health studies. In addition, for a number of these studies we have measured reproductive hormones, thyroid hormones and cortisol and are determining the interaction of hormones/potential endocrine disruption and disease resistance/immune function. Immune system indicators include histopathological analyses, function of macrophages, lymphocytes and cytotoxic cells, serum factors and actual disease prevalence.
Objectives of current work: Research includes development and validation of histologic biomarkers for reproductive health of fishes, understanding the significance of various findings (intersex, arrested gonadal development, thyroid follicle hyperplasia, proliferation of interrenal tissue) to the overall health of individual fish and how that relates to population effects. Since the endocrine system relates almost all aspects of growth, reproduction and development, we are also attempting to tie these studies in with growth and immune function..
Dr. Gary Fellers, Western Ecological Research Center, Point Reyes Field
Station
(http://www.werc.usgs.gov/pt-reyes/index.html )
Summary of Research: For the last 12 years, my research has centered around issues of declining amphibians. Initially, the primary effort was to determine whether amphibians were declining in the California. My field crews and I have now visited over 6,000 sites In California and there is a clear pattern of loss, primarily in the Sierra Nevada mountains. Increasingly, I have focused my research on determining caused of these declines. While such things as introduced fish and disease (chytrid fungus) are likely playing a role, the most compelling evidence is suggests that various contaminants used on agricultural crops in the Central Valley are the most likely cause of amphibian declines.
Objectives of current work: I am now collaborating with several scientists to evaluate the impact of contaminants on amphibians in both the field and the lab. While some pilot work was done on endocrine disruptors in amphibians (Rana aurora and Hyla regilla), no clear conclusions have been reached.
Dr. Jill Jenkins, National Wetlands Research Center, Lafayette, LA
(http://www.nwrc.usgs.gov/about/web/jenkins.htm)
Summary of Research: The research with which I am involved concerns assessing the effects in animals of environmental stressors, including contaminants. Reproductive biomarker endpoints have been particularly useful with several studies and interface well and complement immunological and enzyme assays. These data have been useful with NAWQA projects. Particular focus is often on the males of any species, and the following assays and methodologies include:
1. Genomic damage in sperm cells or blood cells: (DNA integrity, where strand breaks or cytogenetic properties can be assessed using flow cytometry [FCM], comet assay, and sperm chromatin structure assay. Alterations in germ cells could result in heritable genetic changes.) 2. Sperm count, or numbers of cells per mg testis (FCM and hemocytometer). 3. Sperm viability and mitochondrial function (FCM) 4. Sperm morphology (microscopic image analysis) 5. GSI 6. Histopathology
Dr. Reynaldo Patiño, Texas Cooperative Fish & Wildlife Research Unit,
Lubbock, Texas
(https://coopunits.org/Units/TX_FW)
Summary of Research: One of the research themes of interest to the Texas Cooperative Fish & Wildlife Research Unit is Aquatic Ecotoxicology. We are specifically interested in the development of tools to assess, as well as in research that addresses, the effects of endocrine-disrupting compounds on the health and reproduction of the aquatic vertebrate fauna with a major emphasis on fishes and some attention to amphibians. Recently completed projects include (1) the identification, isolation and characterization of the estrogen receptors and estrogen-binding proteins of channel catfish (Ictalurus punctatus), and an assessment of their interaction with environmental estrogenic compounds; and (2) an assessment of the health and reproductive status of common carp (Cyprinus carpio) in contaminated areas of Lake Mead, Nevada. Current work aims to continue earlier research, but we have also initiated new research efforts focusing on environmental contaminants that affect the thyroid system and on the development of sensitive biomarkers to monitor the effects of these contaminants on animal development and reproduction. Other new efforts focus on new contaminants for which little information about their biological effects is presently available. Our work consists of independent efforts as well as collaborative research with universities and other USGS science centers.
Objectives of current work: To (1) develop sensitive markers of exposure and response to thyroid-disrupting contaminants (e.g., perchlorate, chlorate) in fishes; (2) determine the effects of thyroid-disrupting contaminants on fish development and reproduction; and (3) determine the lethal toxicity and sublethal reproductive effects of RDX in fishes.
Dr. Carl B. Schreck, Oregon Cooperative Fish and Wildlife Research Unit
(https://coopunits.org/Units/OR_FW)
Summary of Research: For several decades our laboratory has been examining the effects of environmental contaminants, acting as endocrine disrupting chemicals (EDCs), on various aspects of fish performance measures mediated via the endocrine system. We have projects that have addressed the mechanisms of action of these compounds as well as consequences of exposure in both the field and the laboratory. Our specific interests lie in ultimate impacts on reproduction, immunology and development (including early development of the immune system and smoltification). We have also developed molecular techniques to examine effects of stressors. We collaborate with molecular biologists, toxicologists, analytical chemists, immunologists and pathologists amongst others as co- PIs of our projects.
Objectives of current work: Our overall goal is to provide an understanding of the effects of EDCs, in both wild and laboratory held fish, with developmental, reproductive and immune dysfunction. Current objectives include 1) ascertaining effects of EDCs on reproduction and immune function of white sturgeon (Acipenser transmontanus), 2) determining effects of EDCs on innate and acquired immunity of salmon, 3) ascertaining the possibility of airborne EDC effects on fishes in seven western national parks and 4) development of clean technologies for aquaculture effluents.
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