This article is part of the monograph “The Ecological Relevance of Chemically Induced Endocrine Disruption in Wildlife.

Jobling, S

Tyler, CR

Environmental Health Perspectives

English

PubMed

Brunel University Research Archive

Environmental Health Perspectives • VOLUME 114 | SUPPLEMENT 1 | April 2006 7MonographOver the last two decades, there has been increasing scientific concernand public debate regarding the adverse effects of chemical pollutants inthe environment that can interfere with the normal functioning of theendocrine system in wildlife and in humans (the so-called endocrine-dis-rupting chemicals, EDCs). These concerns have been fueled primarilyby reports of disrupted reproductive function and development in cer-tain wildlife—mammals, birds, fish, amphibians, and mollusks—and bythe increased incidence of certain diseases of the endocrine system inhumans. Investigators hypothesize that EDCs are the cause. Some of theadverse effects observed in wildlife species are strongly associated withexposure to chemicals that mimic or interfere with hormone function,particularly estrogen function, but in many cases, the causal linkbetween exposure to EDCs and endocrine disruption is unclear. Becauseof the diverse effects of EDCs on the thyroid, retinoid, androgen, estro-gen, and corticosteroid systems of a wide range of animals, it is impera-tive that research continues to address the extent of the risk posed byEDCs to wildlife. The ecological relevance of endocrine disruption inwildlife is, however, difficult to quantify, as there is limited understand-ing of how physiological changes affect the individual animal and howindividual responses affect population and community. Furthermore, amajor challenge faced by environmental biologists is the need to placeendocrine disruption into context with other environmental pressuresfaced by our wildlife populations, for example, global warming. In July 2004 an international workshop was convened at theUniversity of Exeter in the United Kingdom to provide a forum for thedissemination and discussion of the most recent data on the ecologicalrelevance of chemical-induced endocrine disruption in wildlife. Theworkshop was organized by the COMPRENDO Project (ComparativeResearch on Endocrine Disruption; COMPRENDO 2006).COMPRENDO is one of four projects [COMPRENDO, EDEN(Endocrine Disrupters: Exploring Novel Endpoints, Exposure, Low-Dose and Mixture-Effects in Humans, Aquatic Wildlife andLaboratory Animals), EURISKED (Multi-organic Risk Assessment ofSelected Endocrine Disrupters), FIRE (Risk Assessment ofBrominated Flame Retardants As Suspected Endocrine Disrupters forHuman and Wildlife Health)] that form the research laboratory core(comprising 60 laboratories) of the CREDO (Coordinating EuropeanEnvironmental and Human Research into Endocrine Disruption) clusterfor research, technological development, and demonstration activities inthe European Community (CREDO 2006). CREDO is funded by theEuropean Commission’s Fifth Framework Programme. One hundred-eighty delegates attended the meeting from 20 countries spanningEurope, the United States, Japan, India, and South Africa and represent-ing many stakeholders including academia, government agencies, indus-try, and nongovernment agencies. The meeting proceedings are availableon the World Wide Web (COMPRENDO 2004). This monograph contains a synthesis of papers presented at theExeter meeting and presents novel research data and new thoughts andapproaches on the ecological relevance of endocrine disruption inwildlife. The first article by Guillette (2006) discusses how the issue ofendocrine disruption has developed in complexity, as we now appreciatethat a plethora of chemicals are capable of altering hormonal functionthrough a wide range of mechanisms of action. Understanding the effectsof EDCs on wildlife populations requires carefully conducted field studiesspanning a number of years. Such studies are unfortunately few and farbetween. Exceptions to these limited studies are those on the effects oforganotin compounds on populations of marine mollusks and estrogenicdisruption in marine and freshwater fish living in the coastal and riverinewaters of the United Kingdom. The latest findings and hypotheses inthese studies are presented by Horiguchi et al. (2006), Hagger et al.(2006), Scott et al. (2006), Jobling et al. (2006), Hayes et al. (2006a),Veeramachaneni et al. (2006), and Hall et al. (2006). These case studiesillustrate some of the challenges encountered when establishingcause–effect relationships between chemical exposures and physiologicalfunction in diverse species. Hagger et al. (2006), in particular, considerthe associated genotoxic effects of endocrine-disrupting chemicals onmollusks, perhaps expanding the mechanisms by which EDCs induceharm in wildlife, while Jobling et al. (2006) and Hall et al. (2006) usemodeling approaches to delineate the relative risks posed by differentEDCs on wildlife populations and to identify likely causative agents.Hayes et al. (2006a) rise to the ultimate challenge and address the likeli-hood that EDCs are responsible for the widespread population declinesin amphibian populations worldwide. Veermachanei et al. (2006)describe testis and antler dysgenesis in Sitka deer on the remote KodiakIsland of Alaska and draw on this as further evidence to support theendocrine disruption hypothesis linking testicular dygenesis in men withreproductive dysfunction in other male wildlife. Finally, in this section onfield studies, Durhan et al. (2006) take the reader beyond the dogma sur-rounding estrogens in the environment and present powerful evidence forthe presence of androgenic contaminants in runoff from beef feedlot.The authors identify the causative agents as metabolites of the growthpromoter trenbolone acetate. Most laboratory studies on chemical effects have been conducted onsingle chemicals, but in the wild, animals are often exposed to complexmixtures that potentially have interactive effects. The next two articles arederived from field studies and provide evidence for interactive effects ofEDCs with other environmental factors. Edwards et al. (2006) examineinteractive effects of water quality on reproduction in mosquito fish, andJenssen (2006) discusses the potential for interaction of EDCs with cli-mate change in Arctic marine mammals and birds. The following twoarticles on mixture effects are laboratory-based studies. Liney et al. (2006)consider the integrative effects of estrogenic effluents from wastewatertreatment works on roach health (spanning sexual function, immunotox-icity, hepatotoxicity, and genotoxicity). Thorpe et al. (2006) assess theability of the model of concentration addition to predict the interactiveeffects of estrogenic chemicals in a complex mixture (wastewater treat-ment works effluent) and conclude that end-pipe analysis may be the pre-ferred approach for assessing the effects of these complex mixtures. Human toxicology studies focus on the protection of the individual,but studies in ecotoxicology wildlife protection are directed principallyThis article is part of the monograph “The Ecological Relevance of ChemicallyInduced Endocrine Disruption in Wildlife.”In addition to employment at Brunel University, S. Jobling is also employed byBeyond the Basics Ltd., an independent consultancy. C. Tyler declares he has nocompeting financial interest.Received 28 February 2005; accepted 1 November 2005.Introduction: The Ecological Relevance of Chemically Induced EndocrineDisruption in WildlifeSusan Jobling1 and Charles R. Tyler21Beyond The Basics Ltd, Burnham, Bucks, United Kingdom, and Institute for the Environment, Brunel University, Uxbridge, Middlesex,United Kingdom; 2Environmental and Molecular Fish Biology Group, The Hatherly Laboratories, School of Biological and ChemicalSciences, University of Exeter, Devon, United KingdomEnviron Health Perspect 114(suppl 1):7–8 (2006).doi:10.1289/ehp.8046 available via http://dx.doi.org/ [Online 17 April 2006]Introduction8 VOLUME 114 | SUPPLEMENT 1 | April 2006 • Environmental Health Perspectivesat the population level. Nevertheless, assessments of chemical effects inwildlife are conducted at the biochemical (biomarker), tissue, and indi-vidual organism levels. A wide range of end points for effects ofendocrine-active substances in wildlife species has been identified, buttheir ecological relevance is not yet fully understood. A major challengefor investigators conducting studies into endocrine disruption in wildlifeis to better harmonize laboratory-based studies on chemicals and the endpoints used with effects occurring in wildlife populations. Developing the theme that we should not be trapped by the dogmain research into endocrine disruption is set in the opening article byGuillette (2006). The authors of the next five articles discuss newapproaches in determining the ecological relevance of endocrinedisruption in wildlife. Schulte-Oehlmann et al. (2006) present theCOMPRENDO research program, detailing how comparative phylo-genic approaches can be used to develop our understanding of the effectsof antiandrogenic chemicals and also to determine commonalities inmechanisms between taxa. Japan is a world leader in the field of ecotoxi-cogenomics, and the article by Iguchi et al. (2006) reveals how molecu-lar approaches are helping to unravel the mechanisms of action of EDCsin a wide range of animals from Daphnia to mammals. This articleemphasizes the need to link molecular responses with cellular and tissuelevel responses to establish pathways of effects for EDCs. In the nextarticle, Hutchinson et al. (2006) provide insight into how we might bestuse biomarkers for endocrine disruption and emphasizes the need to usebiomarkers as “signposts” rather than “traffic lights” in assessing the riskof EDCs. Chemical testing guidelines for endocrine disruption includevery few species, thus limiting the investigator’s ability to assess the eco-logical relevance of contamination of the environment by EDCs. Anexception for research into antiandrogens in fish has been the develop-ment of the three-spined stickleback model; the latest research into theuse of this model is presented by Katsiadaki et al. (2006). Gurney et al.(2006) present a fresh view that relatively simple models can provide auseful framework within which to consider the expression of alteredindividual characteristics at the population level. The objective of suchconsideration, as Gurney et al. stated, is “to identify those individualchanges that are likely to be critical in the population context, so thatexperimental effort can be appropriately focused.” The effects of bisphenol A in mollusks and of the herbicide atrazineon frog populations in the United States have received much attentionand have caused considerable controversy. The articles by Oehlmannet al. (2006) and Hayes et al. (2006b) provide further evidence for effectsof these chemicals at concentrations in the submicrogram per liter range. A key question is “how do we assess the risk posed by EDCs, andindeed should our approach differ from that for any other group ofchemicals?” Here, it seems opinions differ in both the scientific and regu-latory communities. Two articles are included on this subject. In the first,Gross-Sorokin et al. (2006) describe the U.K. Environment Agency’sapproach for a management strategy for chemicals causing feminizationof fish in U.K. rivers. The U.K. Environment Agency recognizes thethreat posed by EDCs and is implementing policy changes to combatpossible effects on the U.K. freshwater fishery. Lyons (2006) continuesthis theme and marks the potential threat posed by EDCs and identifiessome required policy changes. In the final paper, Gee (2006), of theEuropean Environment Agency, argues that scientific methods need tobetter reflect the realities of multicausality, mixtures, timing of dose, andsystem dynamics that characterize the exposures and effects of EDCs.This improved science could provide a more robust basis for the widerand wise use of the precautionary principle in the assessment and man-agement of the threats posed by endocrine disruptors. Over the next decade, we must address major issues regarding theadverse effects of EDCs on wildlife. This will necessitate collaborationand cooperation on an international scale in order to identify populationslikely to be at risk. Furthermore, we must dedicate resources to addressthe critical knowledge gaps that exist. Finally, it is the personal view ofthe editors of this monograph that we must communicate the results ofour studies effectively so that the risks posed by EDCs are understoodand that policy decisions concerning the protection of wildlife speciesfrom the effects of endocrine disruptors are based on the best availablescientific knowledge.REFERENCESCOMPRENDO (Comparative Research on Endocrine Disrupters). 2004. Ecological Relevance ofChemically-Induced Endocrine Disruption in Wildlife. Available: http://www.comprendo-pro-ject.org/_files/AbstractsExeter2004.pdf [accessed 7 April 2006].COMPRENDO (Comparative Research on Endocrine Disrupters). 2006. Home Page. Available:http://www.comprendo-project.org/index2.html [accessed 7 April 2006].CREDO (Cluster of Reserch into Endocrine Disruption in Europe). 2006. Information on EuropeanResearch Projects into Endocrine Disruption. Available: http://www.credocluster.info/[accessed 7 April 2006).Durhan EJ, Lambright CS, Makynen EA, Lazorchak J, Hartig PC, Wilson VS, et al. 2006. Identificationof metabolites of trenbolone acetate in androgenic runoff from a beef feedlot. Environ HealthPerspect 114(suppl 1):65–68.Edwards TM, Miller HD, Guillette LJ Jr. 2006. Water quality influences reproduction in female mos-quitofish (Gambusia holbrooki) from eight Florida springs. Environ Health Perspect 114(suppl 1):69–75.Gee D. 2006. Late lessons from early warnings: toward realism and precaution with endocrine-dis-rupting substances. Environ Health Perspect 114(suppl 1):152–160.Guillette LJ Jr. 2006. Endocrine disrupting contaminants—beyond the dogma. Environ HealthPerspect 114(suppl 1):9–12.Gross-Sorokin MY, Roast SD, Brighty GC. 2006. Assessment of feminization of male fish in Englishrivers by the Environment Agency of England and Wales. Environ Health Perspect 114(suppl 1):147–151.Gurney WSC. 2006. Modeling the demographic effects of endocrine disruptors. Environ HealthPerspect 114(suppl 1):122–126.Hayes TB, Case P, Chui S, Chung D, Haeffele C, Haston K, et al. 2006a. Pesticide mixtures, endocrinedisruption, and amphibian declines: are we underestimating the impact? Environ HealthPerspect 114(suppl 1):40–50.Hayes TB, Stuart AA, Mendoza M, Collins A, Noriega N, Vonk A, et al. 2006b. Characterization ofatrazine-induced gonadal malformations in African clawed frogs (Xenopus laevis) and compar-isons with effects of an androgen antagonist (cyproterone acetate) and exogenous estrogen(17β-estradiol): support for the demasculinization/feminization hypothesis. Environ HealthPerspect 114(suppl 1):134–141.Hagger JA, Depledge MH, Oehlmann J, Jobling S, Galloway TS. 2006. Is there a causal associationbetween genotoxicity and the imposex effect? Environ Health Perspect 114(suppl 1): 20–26.Hall AJ, McConnell BJ, Rowles TK, Aguilar A, Borrell A, Schwacke L, et al. 2006. Individual-basedmodel framework to assess population consequences of polychlorinated biphenyl exposure inbottlenose dolphins. Environ Health Perspect 114(suppl 1):60–64.Horiguchi T, Kojima M, Hamada F, Kajikawa A, Shiraishi H, Morita M, et al. 2006. Impact of tributyltinand triphenyltin on ivory shell (Babylonia japonica) populations. Environ Health Perspect114(suppl 1):13–19.Hutchinson TH, Ankley GT, Segner H, TylerCR. 2006. Screening and testing for endocrine disruptionin fish—biomarkers as “signposts,” not “traffic lights,” in risk assessment. Environ HealthPerspect 114(suppl 1):106–114.Iguchi T, Watanabe H, Katsu Y. 2006. Application of ecotoxicogenomics for studying endocrine dis-ruption in vertebrates and invertebrates. Environ Health Perspect 114(suppl 1):101–105.Jenssen BM. 2006. Endocrine-disrupting chemicals and climate change: a worst-case combinationfor Arctic marine mammals and seabirds? Environ Health Perspect 114(suppl 1):76–80.Jobling S, Williams R, Johnson A, Taylor A, Gross-Sorokin M, Nolan M, et al. 2006. Predicted expo-sures to steroid estrogens in U.K. rivers correlate with widespread sexual disruption in wild fishpopulations. Environ Health Perspect 114(suppl 1):32–39.Katsiadaki I, Morris S, Squires C, Hurst MR, James JD, Scott AP. 2006. Use of the three-spined stick-leback (Gasterosteus aculeatus) as a sensitive in vivo test for detection of environmentalantiandrogens. Environ Health Perspect 114(suppl 1):115–121.Liney KE, Hagger JA, Tyler CR, Depledge MH, Galloway TS, Jobling S. 2006. Health effects in fish oflong-term exposure to effluents from wastewater treatment works. Environ Health Perspect114(suppl 1):81–89.Lyons G. 2006. Viewpoint: policy requirements for protecting wildlife from endocrine disruptors.Environ Health Perspect 114(suppl 1):142–146.Oehlmann J, Schulte-Oehlmann U, Bachmann J, Oetken M, Lutz I, Kloas W, et al. 2006. Bisphenol Ainduces superfeminization in the ramshorn snail Marisa cornuarietis (Gastropoda: Prosobranchia)at environmentally relevant concentrations. Environ Health Perspect 114(suppl 1): 127–133.Schulte-Oehlmann U, Albanis T, Allera A, Bachmann J, Berntsson P, Beresford N, et al. 2006.COMPRENDO: focus and approach. Environ Health Perspect 114(suppl 1):98–100.Scott AP, Katsiadaki I, Kirby MF, Thain J. 2006. Relationship between sex steroid and vitellogeninconcentrations in flounder (Platichthys flesus) sampled from an estuary contaminated withestrogenic endocrine-disrupting compounds. Environ Health Perspect 114(suppl 1):27–31.Thorpe KL, Gross-Sorokin M, Johnson I, Brighty G, Tyler CR. 2006. An assessment of the model ofconcentration addition for predicting the estrogenic activity of chemical mixtures in wastewatertreatment works effluents. Environ Health Perspect 114(suppl 1):90–97.Veeramachaneni DNR, Amann RP, Jacobson JP. 2006. Testis and antler dysgenesis in Sitka black-tailed deer on Kodiak Island, Alaska: sequela of environmental endocrine disruption? EnvironHealth Perspect 114(suppl 1):51–59.

An assessment of the model of concentration addition for predicting the estrogenic activity of chemical mixtures in wastewater treatment works efﬂuents. Environ Health Perspect 114(suppl 1):90–97.

Application of ecotoxicogenomics for studying endocrine disruption in vertebrates and invertebrates. Environ Health Perspect 114(suppl 1):101–105.

Assessment of feminization of male ﬁsh in English rivers by the Environment Agency of England and Wales. Environ Health Perspect 114(suppl 1):

Bisphenol A induces superfeminization in the ramshorn snail Marisa cornuarietis (Gastropoda: Prosobranchia) at environmentally relevant concentrations. Environ Health Perspect 114(suppl1):

COMPRENDO: focus and approach. Environ Health Perspect 114(suppl 1):98–100.

Endocrine disrupting contaminants—beyond the dogma. Environ Health Perspect

Endocrine-disrupting chemicals and climate change: a worst-case combination for Arctic marine mammals and seabirds? Environ Health Perspect 114(suppl 1):76–80.

Health effects in ﬁsh of long-term exposure to efﬂuents from wastewater treatment works. Environ Health Perspect 114(suppl 1):81–89.

Identiﬁcation of metabolites of trenbolone acetate in androgenic runoff from a beef feedlot. Environ Health Perspect 114(suppl 1):65–68.

Impact of tributyltin and triphenyltin on ivory shell (Babylonia japonica) populations. Environ Health Perspect 114(suppl 1):13–19.

Individual-based model framework to assess population consequences of polychlorinated biphenyl exposure in bottlenose dolphins. Environ Health Perspect 114(suppl 1):60–64.

Is there a causal association between genotoxicity and the imposex effect? Environ Health Perspect 114(suppl 1):

Late lessons from early warnings: toward realism and precaution with endocrine-disrupting substances. Environ Health Perspect 114(suppl 1):152–160.

Modeling the demographic effects of endocrine disruptors.

of Reserch into Endocrine Disruption in Europe).

Pesticide mixtures, endocrine disruption, and amphibian declines: are we underestimating the impact? Environ Health Perspect 114(suppl 1):40–50.

Predicted exposures to steroid estrogens in U.K. rivers correlate with widespread sexual disruption in wild ﬁsh populations. Environ Health Perspect 114(suppl 1):32–39.

Relationship between sex steroid and vitellogenin concentrations in ﬂounder (Platichthys ﬂesus) sampled from an estuary contaminated with estrogenic endocrine-disrupting compounds. Environ Health Perspect 114(suppl 1):27–31.

Research on Endocrine Disrupters).

Screening and testing for endocrine disruption in fish—biomarkers as “signposts,” not “traffic lights,” in risk assessment. Environ Health Perspect 114(suppl 1):106–114.

Testis and antler dysgenesis in Sitka blacktailed deer on Kodiak Island, Alaska: sequela of environmental endocrine disruption? Environ Health Perspect 114(suppl 1):51–59.

Use of the three-spined stickleback (Gasterosteus aculeatus) as a sensitive in vivo test for detection of environmental antiandrogens. Environ Health Perspect 114(suppl 1):115–121.

Viewpoint: policy requirements for protecting wildlife from endocrine disruptors. Environ Health Perspect 114(suppl 1):142–146.

Water quality inﬂuences reproduction in female mosquitoﬁsh (Gambusia holbrooki) from eight Florida springs.

Introduction: The ecological relevance of chemically induced endocrine disruption in wildlife

Susan Jobling

Charles R. Tyler

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Introduction: The Ecological Relevance of Chemically Induced Endocrine Disruption in Wildlife

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Introduction: The ecological relevance of chemically induced endocrine disruption in wildlife

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