A restatement of the natural science evidence base on the effects of endocrine disrupting chemicals on wildlife.

Endocrine disrupting chemicals (EDCs) are substances that alter the function of the endocrine system and consequently cause adverse effects to humans or wildlife. The release of particular EDCs into the environment has been shown to negatively affect certain wildlife populations and has led to restrictions on the use of some EDCs. Current chemical regulations aim to balance the industrial, agricultural and/or pharmaceutical benefits of using these substances with their demonstrated or potential harm to human health or the environment. A summary is provided of the natural science evidence base informing the regulation of chemicals released into the environment that may have endocrine disrupting effects on wildlife. This summary is in a format (a 'restatement') intended to be policy-neutral and accessible to informed, but not expert, policy-makers and stakeholders.

Introduction

The endocrine system plays a critical role in almost all biological and physiological functions. Endocrine disrupting chemicals (EDCs) are substances (or mixtures of substances) that alter the function of the endocrine system and consequently are capable of causing adverse effects to humans or wildlife [1]. EDCs include compounds with important agricultural, industrial and pharmaceutical uses, which can become pollution problems through inadvertent human or wildlife exposure. Many different types of chemicals can be EDCs and, beyond their effects on the endocrine system, there is no single characteristic or property that they all share. Particular compounds may affect other biological processes in addition to their EDC effects. Some common natural substances may have endocrine effects (for example sugar and caffeine) but concern about EDCs in the environment chiefly focuses on synthetic chemicals that can sometimes be active at low or even very low concentrations. Though not unique to EDCs, the ability of some chemicals to be biologically active at very low concentrations raises particular regulatory issues. Timing of exposure is also critical, because EDCs may only have an effect at particular life-history stages. Many of the first EDCs to attract regulatory attention had long half-lives in the environment and became concentrated in certain species of wildlife, negatively affecting their population viability. More recently, and in addition, there has been concern about widely used substances that are active at relatively low concentrations and, though short-lived, are commonly found in the environment due, for example, to their continuous release in wastewater.

The aim of the project described here is to provide a ‘restatement’ of the natural science evidence base relevant to the design and implementation of EDC regulations to protect wildlife. We define wildlife as all non-domesticated animals, including amphibians, fish and invertebrates as well as birds, reptiles and mammals. Humans are also exposed to these chemicals when, for example, they use products containing EDCs or through contamination of food (for an introduction to EDCs and human toxicology see [1] or [2]). Toxicology studies for human health protection may anticipate issues for wildlife and vice versa.

Some of the most well-documented examples of wildlife population reductions caused by industrial and agricultural chemicals were due to the endocrine disrupting properties of those chemicals. The widespread use of the organochlorine insecticide DDT from the 1950s onwards was a major driver of declines in birds of prey because of reproductive failure due to eggshell thinning [3,4]. The use of polychlorinated biphenyls (PCBs) in electrical equipment and for other industrial purposes resulted in large quantities of these highly persistent chemicals entering the environment. They have become concentrated in the bodies of species at the top of ecological food webs, particularly in high-latitude regions of the Northern Hemisphere, and are linked to impaired reproduction [5,6]. Use of both types of compounds is now restricted worldwide. Not all the toxic effects of these chemicals are through endocrine disruption, but the association of EDCs with a number of classic cases of pollution affecting wildlife means that they attract particular attention from environmental protection agencies, and raise strong concerns for non-governmental organizations involved in environmental protection.

We have attempted to write this restatement in a succinct manner comprehensible to non-expert but informed readers while providing an entry into the technical literature. We have tried to be policy-neutral, though we realize that this can never be absolute. In a short summary of a very large subject it is impossible to survey all of the literature relevant to the environmental effects of the very many types of EDCs. While our review is inevitably selective, we have tried to emphasize what, in the judgement of the authors, are the generic issues of relevance to multiple EDCs.

Methods

This evidence summary was produced using a similar procedure to that used in previous restatements (e.g. [7,8]). The literature on EDCs and wildlife was reviewed and a first draft produced by a subset of the authors. At a workshop, all authors discussed and assessed the different evidence components in the light of the strength and quality of the available literature. Subsequently, using a restricted set of terms (see Appendix A, ¶ 3), each piece of evidence was assigned a code with our assessment of the nature of the evidence base.

A revised evidence summary was produced and further debated electronically to produce a consensus draft. The restatement was then sent to 28 stakeholders or stakeholder groups, including scientists involved in environmental pollution research, representatives of the pharmaceutical, water and chemical industries and non-governmental organizations concerned with environment and conservation, and UK government departments and statutory bodies responsible for environmental chemicals. We asked them to judge whether the literature had been fairly covered and that we had not inadvertently overlooked key evidence, and to review the evidence codes outlined above. We also asked the stakeholders to comment on whether the restatement achieved its aims of being policy-neutral and not a work of advocacy. The document was revised in the light of much helpful feedback. Though many groups were consulted, the project was conducted completely independently of any stakeholder and was funded by the Oxford Martin School (part of the University of Oxford).

Results

The summary of the natural science evidence base relevant to policy-making on EDCs and wildlife is given in Appendix A, with an annotated bibliography (which includes a glossary of technical terms) provided as electronic supplementary material.

Discussion

In this restatement, we have used the World Health Organization (WHO) definition (see Appendix A, ¶ 4) of an EDC. This is probably the most commonly employed, though not without issues. For example, as noted above, some substances cause adverse effects but at concentrations that would seldom, if ever, occur in the field. The WHO definition would include them in this category, but the many everyday chemicals involved are not typically considered EDCs.

Even if a chemical is shown to have endocrine disruptive activity on wildlife by the WHO definition, the chief issue for regulators is whether the substance causes harm at the population and ecological community levels. This is often challenging to determine as there are few or no baseline population data available for most species, and typically we have a poor understanding of how different factors affecting mortality and fecundity combine to influence population abundance and resilience.

If an adverse effect is observed in wildlife, determining its cause and identifying any association with a particular chemical compound can be extremely difficult. In almost all cases where an EDC (or mixture of EDCs) has caused adverse effects on wildlife, the connection with exposure to the EDC(s) has been established only after the wildlife population had declined. Improved prediction of which compounds may cause harm when released into the environment would be very helpful. One challenge is to understand how different EDCs combine to affect wildlife. At the moment the potential and actual effects of EDCs (and other chemicals) are generally evaluated on an individual basis, while wildlife populations are exposed to complex cocktails of compounds that can interact with each other [9].

Finally, we note a number of limitations of this study and discuss how it might be extended.

First, we are aware that in attempting to discuss EDCs as a category of chemicals we were unable to provide a detailed evidence summary of all the work relevant to every EDC, due to the numbers and varieties of substances involved. The rationale behind our approach was to discuss common issues relevant to many EDCs, as well as to learn lessons from particular types of chemicals that have been shown to be harmful to wildlife and have thus been banned or their use severely restricted. Restatements for specific EDCs in which the literature is more comprehensively surveyed could be produced if requested by policy-makers. Previous restatements on neonicotinoid insecticides [7,10] are examples of more targeted studies (involving pollutants that are not EDCs) where a greater coverage of the literature was possible.

The second limitation to our study is that we have focused only on the effects of EDCs on wildlife and not on humans. The reason for this is that the two issues are somewhat different. Society has a very low tolerance of harm done to individual humans, while for wildlife the impacts on populations are typically considered most important. Sources and pathways of exposure to humans and wildlife may also be different. Nevertheless, as we discuss in the restatement, the two topics are related, and bringing them together in the future in the context of the ‘One Health’ [11] agenda may be valuable.

Finally, the restatement focuses on the natural science evidence base relevant to the regulation of EDCs. Policy-makers seeking to shape regulatory regimes will also require evidence about the economic costs and benefits of different interventions, as well as their political and social acceptability. Performing economic cost-benefit analyses in this area is complicated because of the need to include not only the direct financial impact of regulation (or lack thereof) on industry, consumers and government, but also the direct and indirect economic consequences of the effects of EDCs on human health and the state of the environment. There are also other topics in the social sciences and humanities, including the history and political economy of regulating pollutants in the environment, where research may be valuable to policy-makers in understanding the desirability and acceptability of different modes of chemical regulation to society [12].