Introduction

Ecotoxicology emerged by the mid-twentieth century. In the 1950s, all developing countries were recovering from the Second World War. “Chemistry, a key to better living” was the popular slogan in that time of technical and economic development. As environmental considerations were then totally inexistent, setbacks appeared quickly with air and water pollution events!

Two major episodes of acid smog in London in 1950 and 1952 killed several thousands of Londoners from respiratory symptoms. The first oxidizing smogs were also observed in California, as a result of intensive car traffic producing nitrogen oxides in exhaust emissions, associated with sunny weather and no wind conditions.

Yet, on top of atmospheric events, chronic and insidious pollution of water actually triggered the discipline, after environmental disasters, and unexpected health problems had occurred worldwide. The ecosystem-wide contamination of Clear Lake in California and Minamata disease in Japan sounded the alarm on unequivocal insults to humans and biota caused by persistent pollutants.

Historical pollution events

The Clear lake event had a worldwide impact due to dramatic ecosystem damages produced in spite of a regulatory use of insecticides. Clear Lake is a touristic site in California and an aquatic area that was populated with thousands of magnificent fish-eating birds, the grebes (Aechmophorus occidentalis), in the late 1940s. Insects abounded in the area. In order to eradicate gnats (Chaoborus astictopus), non-biting insects, that were a nuisance to people enjoying leisure time by the lake, three controlled applications of the insecticide DDD (dichloro diphenyl dichloroethane), an analogue of DDT (dichloro diphenyl trichloroethane), were carried out from 1949 to mid-1950s. These resulted in an ecosystem-wide DDD contamination that decimated the grebe population within a few years owing to reproductive failure.

In order to understand the disaster, analyses of insecticide contamination were carried out in different parts of the ecosystem. Very low water concentrations were found as expected, but unexpectedly, concentrations of DDD residues were found to increase from water to phytoplankton and zooplankton, to microphagous fish, to predator fish, and ultimately to piscivorous grebes. The concentrations in grebe tissue lipids were more than one million times higher than in water (Hunt and Bischoff 1960).

Similar phenomena of species disappearance at the top of food webs were recorded in terrestrial ecosystems in North America and Europe: severe population declines in birds and in a number of raptor species were associated with the use of chlorinated insecticides and DDT in agriculture. Such concerns regarding the new agricultural practices and their impact on fauna justified the creation of the Monks Wood Experimental Station within the Nature Conservancy in England in 1962. The study of aquatic and terrestrial bird contamination by Moore and Walker (1964) showed that carnivorous terrestrial birds were the most contaminated by organochlorinated compounds compared to plant-eating birds. This underlined the role of food web transfer in disappearance of birds of prey and especially of the sparrow hawk, an emblematic species in England. Ratcliffe (1958, 1967) demonstrated that eggshell thinning in raptors coincided with the use of organochlorinated insecticides and accounted for the eggs being crushed during brooding. In Canada, Peakall (1970) carried out mechanistic studies on toxicity of DDT and one of its persistent metabolites, p,p’-DDE (dichloro diphenyl dichloroethylene).

The most impressive discovery was biomagnification in food chains! This phenomenon can be depicted/schematized by two pyramids, the biomass pyramid compared to the inverted pyramid of pollutant concentrations in species tissues (Fig. 1, left and right side, respectively). The figure clearly shows that residue concentrations increase when going up the food chain and reach very high levels at the top, in predators, such as fish-eating birds, birds of prey, or humans. This occurrence was typical of organochlorinated compounds and persistent pollutants, either organic or inorganic.

Fig. 1
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Schema of the biomagnification process considering biomass and contaminant tissue concentrations (persistent bioaccumulative pollutants) across various trophic levels

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Contamination of food chains by pesticides and the Clear Lake event was popularized in Rachel Carson’s book “Silent Spring” published in 1962. It had the effect of a bomb in the minds of Americans since it conveyed the idea that environmental contamination by pesticides was incriminated in wildlife effects, leading to a world without birds, while also implicated in the onset of human cancers.

In the same time period, Minamata disease raised concern of scientists and health institutions regarding the long-term fate and effects of persistent pollutants (Box 1). Almost 20 years had passed between identification of the first case of neurologic disorders in 1953 and elucidation of the causes of this illness that afflicted the adult and infant populations of Minamata (Harada 1978). The discovery by Jensen & Jernelov (1969) of mercury methylation in aquatic sediment by fungi finally closed two decades of inquiries. The low concentrations of methylmercury in Minamata river water were biomagnified as a result of its lipophilicity and persistency in the hydro-system and resulted in high uptake through food input to cats and humans, both being the top fish consumers in the aquatic trophic web.

Box 1 The Minamata disease

By mid of the 1950s, a neuropathy struck down the population in the area of Minamata, a town along the Minamata river flowing into Minamata Bay of an island at the Southwest Japanese archipelago. The disease was epidemic in 1955, but without any viral or microbial etiology identified. A congenital form of the disease was described in 1959 in infants, as a cerebral paralysis characterized with delayed neurodevelopment, mental retardation, and fatal issues in a quarter of the cases (OCDE 1974; Harada 1978). The origin of the mysterious illness was discovered when a link was established between an abnormal behavior of cats and neurologic disorders in humans. Both humans and cats ate the same food, fishes from the bay. Analyses revealed a methylmercury contamination. A nearby acetaldehyde plant that used mercury as catalyst was suspected to be the polluting source, but managers disclaimed any responsibility arguing that mercury could be released in the river with the plant effluents but not methylmercury. Knowledge stagnated there during 10 years, until Jensen and Jernelov (1969) demonstrated mercury methylation in aquatic sediment by fungi, finally closing two decades of inquiries. The low concentrations of methylmercury in the Minamata river sediment and the water were biomagnified as a result of its lipophilicity and persistency in the aquatic systems resulting in high food input in cats and humans, at the top of the aquatic trophic web, as described with DDD at Clear Lake. In 1971, Snyder described the placental and milk transfer of methylmercury responsible for congenital mercury poisoning, destroying the prevailing beliefs that placenta was a protecting barrier for the fetus. Since then, it is known that infants may be contaminated via placenta and milk transfer!

The same phenomenon of amplification of cadmium concentration from the Jinzu river water to rice and to humans was reported as a cause of the Itaï-Itaï disease at the same period in the Toyama Prefecture in Japan (WHO 1992).

Ecotoxicology: a new discipline launched by JM Jouany

The biomagnification process was the major lesson learned from these pollution events, while the endocrine effects of organochlorinated pesticides on reproduction were misunderstood. As a result, scientists hardly worked at developing experimental models to identify biomagnification properties of pollutants. Metcalf and his coworkers at the University of Illinois in Urbana-Champaign (USA) were the first to develop a laboratory “model ecosystem” for the evaluation of pesticide biodegradability and ecological magnification (Metcalf et al. 1971, 1975). The authors used radiolabeled compounds to study an eventual water contamination after pesticide application to crop plants; they evaluated pollutant transfer using a seven-element food chain including soil and aquatic species. Their research extended to the whole class of organochlorinated compounds, including PCBs (polychlorinated biphenyls) just discovered among aquatic pollutants worldwide.

At that time, scientists were speaking of “ecological effects” or “ecological magnification.”

The term “ecotoxicology” was introduced and written for the first time by Jean-Michel Jouany in 1971, in his article Ecologie et nuisances published in a French journal “Actualités Pharmaceutiques” (Jouany 1971) where he stated: “The study of the influence of nuisances on the relationship between an individual [species] and his [its] environment could simply be termed Ecotoxicology,” with “ nuisances “ defined as “harmful and inimical factors induced by humans” (translated from French). In this article, he analyzed “how the constant changes in the relationships between individuals and their environment were decisive in the evolution, the species stability and the unsustainable equilibrium which resulted.”

Hence, Jouany conceived a new discipline, he named “Ecotoxicology”, and understood as “Toxicology in an ecological perspective”, a multidisciplinary science, which aims at studying:

  • The deleterious effects of chemical, physical, and biological agents on living organisms

  • The interrelations within communities and their interaction with the environment

In 1971, Jean-Michel Jouany is a young professor of Toxicology and is leaving the University of Nancy to establish a new research field, Ecotoxicology, in the University of Metz in France (Fig. 2). This scientist is eloquent, enthusiastic, and innovative, permanently exchanging and expressing his flow of ideas and concepts in an open-minded spirit and of unequaled humor during his lectures! He had a multi-disciplined and inspiring career path before his appointment as Professor of toxicology at the University of Nancy. After obtaining his diploma as a Pharmaceutical Chemist, he completed a fellowship as an assistant of Professor Henri Laborit in the Laboratory of Eutonology in Paris, then a 2-year post-doctorate in neurochemistry in the USA, followed by a Ph.D. thesis in Toxicology. His academic career starts as Professor of Physiology in Paris and then as assistant of Professor René Truhaut at the faculty of Pharmacy. In 1969, he obtained the degree of senior teacher lecturer in toxicology at the French national examination, and finally he moved to Nancy and to Metz in 1972. He developed the laboratory of Ecotoxicology at the new faculty of ecology founded on the impulse of Professor Jean-Marie Pelt at the University of Metz. His first research with the two Ph.D. students he supervised dealt with the transfer of cadmium in aquatic systems. In contrast to the Metcalf model with a seven-element food chain, he conceived a simple aquatic model composed of three trophic levels, namely, microalgae, microcrustaceans, and fish, to evaluate biomagnification properties; the microalgae exposed to cadmium served as food to daphnids and the latter as food to fish in experiments of several weeks of exposure. Jouany and his coworkers published their results in 1977 in a French journal Annales des Falsifications et de l’Expertise Chimique (Jouany et al. 1977). The same year, in the same journal, he published another article in which he launched the basis of experimental aquatic ecotoxicology for chronic toxicity assessment, discussing the test species to focus on bacteria, microalgae, microcrustaceans, and fish and the endpoints to study in the long term. He stressed the need for measuring growth and reproduction to reflect potential toxicity on populations, as well as biochemical parameters and enzymatic activities as markers of energetic systems. Testing low environmentally relevant pollutant concentrations was also one of his recommendations. All these principles are the ones we apply today.

Fig. 2
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Jean-Michel Jouany

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Jouany and Truhaut relationships

Truhaut and Jouany were two eminent scientists, excellent speakers, and two outstanding personalities, but with “mandarin-like” ambiguous relationships.

Jean-Michel Jouany (1929–2018) was one of the assistants of René Truhaut, the famous toxicologist, from 1965 to 1968. He was 20 years younger than his supervisor. Jouany is inventive, enthusiastic, and persuasive, and he likes diffusing his ideas. Owing to, or because of, his working relationships and fruitful exchanges with Truhaut, Jouany convinced him to embrace environmental issues! Truhaut knows how to recognize a good idea, which he readily endorses! He will then “steal the limelight” at the occasion of a conference in Stockholm, SCOPE in 1969, without quoting his young mentor. SCOPE, Scientific Committee on Problems of the Environment, was established by ICSU, the International Council of Scientific Unions. Truhaut, invited at this 10th ICSU meeting, pronounced the term “Ecotoxicology” that he presented as a “new branch of Toxicology.” From this point on, he was considered as the “father of ecotoxicology.” In 1977, Truhaut published the article Ecotoxicology: Objectives, Principles and Perspectives in the first issue of the new journal Ecotoxicology & Environmental Safety (Truhaut 1977), an article developing his “anthropocentric view of ecotoxicology” which contrasted with the ecology-based concept of ecotoxicology put forward by Jouany. Truhaut was invited by EEC in 1984 to preside the Scientific Committee on Ecotoxicology and Toxicity of Chemicals. Given his international position with health authorities, he spread the term Ecotoxicology and took advantage of its benefits.

René Truhaut (1909–1994) was a well-known toxicologist, internationally renowned; he was a remarkable orator, learned man, and hard worker (Fig. 3). He had an outstanding contribution in toxicology, namely, in the development of chemical quality limits and permissible levels in workroom air (maximum acceptable concentrations, MAC, Helsinki 1957); in occupational exposure limits (OELs) and HB (human based) recommended OELs for metals, solvents, and pesticides (WHO, 1980–1982); and in threshold limit values (TLV). He was also at the origin of the concept of the “acceptable daily intake” (ADI) for pesticides (1956), then MRL (maximum residue limit), in FAO/WHO committees on food and food additives. He had also an eminent role in favoring mutual understanding between international experts from leading countries (USA, USSR). Truhaut received many awards from WHO, EEC, FAO, etc. during his career and appreciated honors. Every scientist acknowledged his scientific qualities as a toxicologist. His fame was such that it did not seem possible for any legitimate competitor to emerge.

Fig. 3
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René Truhaut

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Truhaut, the senior man, published solo (never with coauthors!) his article on (eco)toxicology expressing his anthropocentric view and had never supervised any ecotoxicological research. However, since he had taken the lead in first pronouncing the term “ecotoxicology,” he continued to be cited as its father by posterity. Jouany suffered from what can be called an usurpation of authorship, but he recognized Truhaut’s efficiency in promoting the term at large, in every political and scientific institution Truhaut worked for.

In contrast, Jouany included Truhaut as coauthor in most of his articles (i.e., Truhaut and Jouany 1977), as a form of respect to his past supervisor, a common practice at that time, and also as recognition for their working relationships. Exceptionally in his first article entitled Ecologie et Nuisances, where Jouany introduced his meaning of “Ecotoxicology,” as an emergence from ecology within an anthropogenic polluted world, did he publish as a single author.

The research activities of Jouany focused exclusively in the field of ecotoxicology as reflected by his articles at the national and international level, published in both French and English. In his entire career, he was deeply involved in regulations of chemicals and pesticides at the European level (DG XI and DGVI) and research in joint committees for prioritization of hazardous aquatic pollutants (Brorasmussen et al. 1994) and for risk assessment. In France, he held a leading position at the Ministry of Health, the Ministry of Environment, and the Ministry of Agriculture for all questions linked to risk of chemicals and pesticides, throughout his career. For two decades, he chaired the Committee on methods for ecotoxicity of chemicals at the Ministry of Environment and acted as vice chairman of a number of committees regarding pesticides and chemicals. He initiated the development of the SIRIS method (System of Integration of Risk with Interaction of Scores), an original mathematical scoring system for the estimation of environmental risk of pesticides (Jouany et al. 1983; Vaillant et al. 1995) and chemicals (Guerbet and Jouany 2002). He founded the SEFA, Société d’Ecotoxicologie Fondamentale et Appliquée, in 1983 with Roger Cabridenc and Pascal Deschamps as co-founders and with the support of the Ministry of the Environment. He co-organized and presided seven research symposia within the next 15 years. Jean-Michel Jouany (1929–2018) left us recently, and a fitting tribute was paid in France by SEFA, Societé d’Ecotoxicologie Fondamentale et Appliquée, and ISTA19, to this exceptional man who launched ecotoxicology.

If Truhaut is often/always cited as the “father of ecotoxicology,” he was rather its brilliant marketer while Jouany was its inventor.

The international mobilization in the 1970s

The 1960s decade contributed to an awareness of the negative side effects of chemicals used without knowledge of environmental fate and effects. The 1970s decade incited a strong international mobilization for prevention, regulation, and survey of pollutions. The US EPA (US Environmental Protection Agency) was created in 1970 and Environment Canada in 1971. This led to the ban of DDT and most organochlorinated insecticides in 1972 by the US EPA. The European Economic Community (EEC) followed with EEC Directive 79/117/CEE December 21, 1978, banning since 01/01/1981, phytosanitary products containing aldrin, dieldrin, chlordane, DDT, endrin, heptachlor, hexachlorobenzene, alkyl, and aryl mercurials. At the same time, EEC Directive 79/831/CEE amending the 6th Directive 67/548/CEE on classification and labeling of chemicals dealt with chemical regulation requiring a notification dossier for new chemical substances since September 18, 1981.

In parallel, WHO initiated an International Programme on Chemical Safety (IPCS) and the publication of the Environmental Health Criteria series. Unsurprisingly, the first issues published in 1976 were devoted to mercury (N°1) and PCBs (N°2) (WHO 1976a, 1976b, respectively). While PCBs had been used since 1929, they were only recognized in the 1960s as pollutants of aquatic systems worldwide, in chromatograms of environmental analyses, along with organochlorinated insecticides (Jensen 1966; WHO 1976b).

Unfortunately, the 1970s decade was obscured by the SEVESO accident that occurred on July 10, 1976 in the North of Italy. The release of “dioxin” in the atmosphere of the small Italian city by an industry producing phenoxychlorinated herbicides (2,4-D and 2,4,5-T) produced a trauma in Western Europe.

The so-called Seveso-Directive (Directive 82/501/EEC) was adopted to prevent and control accidents by hazardous chemicals. It was amended in 1996 and 2012 to integrate the lessons learned from later accidents and to take into account the increased rights for citizens to access information and justice. The Seveso disaster showed again that long-term toxicity can result from use of hazardous substances, able to impact environmental and human health. Research on dioxins and dioxin-like PCBs continued to dominate scientific research during the two next decades and beyond.

In parallel to regulations, research centers devoted to ecotoxicology or to the wider field of environmental and human health were developed in industrialized countries. Additionally, research centers for human toxicology enlarged their activities to include ecotoxicology, environmental and analytical chemistry, and the environment in general. In some cases, dedicated institutes were created to investigate specific concerns.

Conclusion

While many scientists, not cited here, contributed to the development of ecotoxicology, Jouany and Truhaut, as pioneers, played key roles in the emergence of the discipline. These two outstanding French personalities were associated with its authorship. Truhaut’s notoriety allowed him to spread ecotoxicology quite efficiently as he took advantage of his authoritarian key position at the highest levels of international health. Hence, his acknowledged paternity for a discipline he presented as a branch of toxicology was congruent with his repute. Jouany, the actual conceptor, had the national floor to express his vision of ecotoxicology. He never competed with Truhaut, whom he acknowledged as the indisputable authority in the international sphere, while suffering from his “mandarin-like” attitude. Jouany, an intelligent and wise humanist, considered that mutualism was a more logical path to success. However, he often underlined in his speeches that it was fair and right “to give credit where credit is due”! This historical story teaches us that “sharing ideas is fine, as long as source and authorship are safeguarded.” It also illustrates that to “publish or perish” continues to be an everlasting pursuit. Indeed, publishing in a national language has its merits. However, publishing at the international sphere is better, and doing both is ideal!

To readers of this article, let it be known that whenever you read, “Truhaut, the father of ecotoxicology,” do not forget that Jean-Michel Jouany came first in this Ecotoxicology saga and that “it is only right to acknowledge his merits.”