Reflections about three influential Ambio articles impacting environmental biogeochemistry research and knowledge

Abstract

Reflections about three influential environmental contaminants papers published in Ambio are presented. The PCB Story by Jensen in (1972) had a very important influence on environmental chemistry. This is captured by way of comments and personal anecdotes. Wania’s and MacKay’s (1993) paper highlights the physical chemistry underlying transport of PCBs and organochlorine pesticides from temperate zone ecosystems to Polar Regions. Their paper exemplifies how principles of chemistry and environmental processes informed understanding the biogeochemical cycles of chemicals of environmental concern (CEC). Mergler et al.’s (2007) paper reviews knowledge of methyl mercury exposure and impacts in humans and served as an example of how to approach exposure and human health concerns for all CECs. All great progress. Then, the question: “How we missed for two decades the importance of plastics in the environment identified in a paper published the same year as The PCB Story? Are we missing yet another important environmental contaminant now?

Introduction

Hundreds if not thousands of chemicals of environmental concern (CEC) have been released to the environment by human activities, both novel synthesized chemicals not naturally present (e.g. PCBs) and natural chemicals extensively mobilized by human activities (e.g. mercury, lead, petroleum). Arne Jernelov in his commentary (Jernelöv 2021) has noted the importance of the three Ambio articles selected for exemplifying the significant contributions of the science published in Ambio to understanding the inputs, fates and effects of CEC. He has provided several key points and stimulated my memory. I will amplify on his informative observations with a few personal observations and thoughts.

I became aware of Rachel Carson’s Silent Spring (Carson 1962) during Ph.D. studies at the Graduate School of Oceanography, University of Rhode Island September 1968 to August 1971. Those were tumultuous days in the United States (as they are now in the USA and worldwide), with protests related to the Vietnam War and to issues of racism/diversity, equity and inclusion. Another important activity that caught the attention of many were environmental issues leading up to the first Earth Day April 22, 1970. Understanding the input, fates and effects of CEC became a topic of interest for several early career scientists. We pursued careers blending fundamental research and research focused on societal needs—the “Pasteur’s Quadrant” so identified by Stokes (1995). An unintended consequence of releasing CEC into the environment is the chemicals often became tracers of biogeochemical processes—how natural, biogenic chemicals of similar properties moved through the environment.

“The PCB Story” (Jensen 1972)

Jensen’s “The PCB Story” appeared in Ambio in August–September of 1972. It was a riveting story then and is still so now. The paper provided a full accounting of the discovery and confirmation of PCBs in the range of samples analyzed, including a figure illustrating confirmatory mass spectrum. There had been indications in the literature that a paper such as this was much needed because by 1972 there had been about 120 papers published concerning various aspects of PCBs (Erickson 1997).

There had been a short news report-like note in New Scientist by Sören Jensen (1966) about the identification of PCBs as several of the unidentified peaks and partially resolved peaks present in electron capture detector gas chromatograms of isolates of extracts of tissues prepared for analysis of DDT compounds (e.g. DDTs and DDEs). This was followed by a short note by Widmark (1967), Sören Jensen’s Professor at the Institute of Analytical Chemistry, University of Stockholm. Shortly after that several papers were published reporting PCBs in samples of birds, fish and other organisms. Examples among these papers are Holmes et al. (1967), Risebrough et al. (1968), Koeman et al. (1969) and Jensen et al. 1969. Veith and Lee (1970) emphasized the need for a “systematic analytical procedure for the quantitative and qualitative determinations of the components of chlorinated biphenyl mixtures”.

Reading the scientific literature of the 1960s it became clear that researchers studying nuclear weapons test fallout chemicals such as ¹³⁷Cesium and ^239/240Plutonium were finding widespread distributions over land and in the sea, especially in the northern hemisphere where most of the weapons tests had occurred. It did not take long for the connections to be made by several scientist that long-lived human mobilized or synthesized chemicals such as chlorinated pesticides and PCBs were making their way into the atmosphere and were being distributed globally, including to the deep oceans in a manner analogous to certain chemicals from nuclear weapons tests.

During postdoctoral research at Woods Hole Oceanographic Institution with Dr. Max Blumer, an organic geochemist and pioneer in oil pollution research, I participated in a U. S. National Science Foundation funded International Decade of Ocean Exploration (IDOE) project focused on assessing the distribution of trace metals, chlorinated pesticides and PCBs, and petroleum hydrocarbons in the oceans. My colleague at WHOI, George R. Harvey, had been studying chlorinated pesticides and PCBs in the oceans for two years prior to my arrival. I focused on petroleum hydrocarbons.

The IDOE project held a workshop May 25–26, 1972 Chaired by Professor Edward Goldberg of Scripps Institution of Oceanography. Not only our project co-researchers in the USA (among whom was Robert W. Risebrough), but numerous international colleagues were present. The group included Sören Jensen, who most likely had just finished submitting “The PCB Story” for Ambio to be published three months later. It was my only meeting with Sören Jensen and it was an honor and very educational as an early career scientist to meet Goldberg, Jensen, Risebrough, Claire Patterson (lead pollution in environment pioneer), George Woodwell (chlorinated pesticide effects) and other pioneers of modern environmental chemistry, especially as it applied to the marine environment. The short report from the Conference was compiled and produced over a few days by Ed Goldberg and assistants, printed (Goldberg 1972), and delivered to the first U.N. Conference on the Human Environment in Stockholm, Sweden June 5–16, 1972.

It was an exciting time for this focus of research. It was also a sobering time as we realized the potential implications for the future if something was not done to curtail the promiscuous release of such compounds. It had been known for at least two decades that exposure to PCBs and some other industrial organochlorines (e.g. chlorinated naphthalenes and chlorinated polychlorinated terphenyls) in the workplace could be harmful to human health. Furthermore, there had been accidental commercial PCBs formulation contamination of food consumed by people that caused illness (e.g. WHO 1976). Would there be problems if PCBs made their way through the food web back to human consumers and at what concentration in the food?

A local connection

I was fortunate to receive an appointment at WHOI, expanding my postdoctoral research. Manfred Ehrhardt, a visiting scientist in Max Blumer’s laboratory, was assessing the presence of polycyclic aromatic hydrocarbons (PAH) in surface muds from a sampling transect across nearby Buzzards Bay. He noted interference from chlorinated hydrocarbons in the mass spectrometric analysis of PAH (guided in part by Jensen’s Ambio paper) for the sample in the outer reaches of the harbor of New Bedford, Massachusetts. Max Blumer suggested that Manfred check with me about PCBs being present in such high concentrations since Max knew that I had been born and educated through high school in New Bedford. I was chagrined that my focus had been so much on the open ocean that I had forgotten, temporarily, that two of the larger PCBs containing capacitor manufacturing plants in the world were located on the shores of New Bedford Harbor, a short distance across Buzzards Bay.

George Harvey left WHOI for a position at the US NOAA laboratory in Miami, Florida pursuing other research. The chlorinated pesticide/PCBs biogeochemistry research at WHOI evolved to my laboratory. During a visit to Woods Hole, Bob Risebrough introduced me to Ian C. T. Nisbet who was at the Massachusetts Audubon Society. Nisbet had written the US EPA Criteria Document for PCBs (USEPA 1977).

My laboratory group became engaged in research, along with others, focused on PCB pollution in New Bedford Harbor. Soon Bruce Brownawell joined our laboratory as a graduate student in the MIT/WHOI Joint Program (co-advised by Professor Phillip. M. Gschwend at MIT and me) and earned his Ph. D. degree in 1986. Bruce brought graduate student enthusiasm and innovative thinking to our PCB research. This was the time period where our laboratory (and several others) adapted glass capillary gas chromatographic columns coupled to ⁶³ Ni electron capture detectors for analysis of PCBs. The separation of most 209 congeners of PCBs allowed greater understanding of the relationship between structural specificity of chlorobiphenyl congeners and biogeochemical processes (e.g. Brownawell and Farrington 1986; Gustafsson et al. 1997), selective metabolism (Dawe and Stegeman 1991) or microbial degradation- slow as it might be. It is one of numerous examples following on from Jensen’s pioneering research, of advances in analytical chemistry coupled with physical chemical, structural chemical, ocean science, biochemical, biological, and ecological knowledge yielding advances in overall knowledge with application to societal needs.

After several years of persistence, and more extensive assessment, the New Bedford Harbor area was designated a USEPA Superfund Site in 1982–1983 (e.g. Farrington et al. 1985).

Global fractionation and cold condensation of low volatility organochlorine compounds in polar regions (Wania and Mackay 1993)

Research and assessments from the field, in laboratory experiments, and theoretical considerations progressed for organochlorines (OCs) of environmental concern such as PCBs, DDTs, DDEs, and other organochlorine pesticides, e.g. polychlorinated camphenes (toxaphene), chlordane, hexachlorobenzene, and hexachlorocyclohexane. One focal example, as noted by Wania and Mackay (1993), was how the polar ecosystems (most were Arctic data) far removed from manufacture and use were being contaminated by these OC compounds, some of which were also making their way through the food web in concentrations that were of human health concern for indigenous peoples such as the Inuit. The Wania and MacKay paper is important for two main reasons: (1) they gathered together key environmental measurements, and (2) they noted how the different physical chemical parameters of these compounds such as vapor pressure interacted with temperature to explain volatilization from land and ocean surface, precipitation, re-volatilization, precipitation again—perhaps for several iterations. This process was what others, descriptively, had called the “grass hopper” effect or Jernelov likened to a “ping-pong” ball effect transporting the organochlorines from Temperate to Polar Regions.

Given the differences in key physical chemical parameters of the various OC molecules (e.g. volatility) these were processes that could result in significant changes in the relative concentrations of specific OCs when comparing samples taken at different latitudes. These findings were combined with earlier observations of the relative hydrophobic and lipophilic natures of the OCs, sorption–desorption phenomena involving water particulates and sediments as noted above, and a picture began to emerge of the entire biogeochemical cycles of OCs. Figure 1, provides a simplified diagram for the biogeochemical cycle for PCBs in a coastal ecosystem with PCB polluted sediments.

Fig. 1.

Schematic of a biogeochemical cycle of chemicals of environmental concern in the coastal ocean. The route back to humans is through the consumption of fish and shellfish depicted as pelagic fauna and benthic fauna

Soon this aspect of the field of research matured sufficiently that Schwartzenbach, Gschwend, and Imbodden wrote their influential and acclaimed text “Environmental Organic Chemistry” now in its 3rd edition (2016). This provides advanced undergraduates and graduate students (and others) with the fundamental knowledge of physical chemical properties, useful parameters, processes, and behavior of organic CEC in the aquatic environment.

Methylmercury exposure and health effects in humans: a worldwide concern (Mergler et al. 2007)

Jernelov’s reflection on this article provides a succinct and informative history of the issue of mercury and especially methyl mercury as an environmental contaminant and pollutant. I have not conducted research concerned with methyl mercury. However, I have followed the essential literature. Unlike the environmental problems with OCs, the methylmercury problems are those of human mobilization of a natural chemical that causes excess concentrations in certain locations and species above those found normally without human actions.

The Mergler et al. (2007) paper provides a summation “tour de force” of knowledge at that time. Most important is the careful explanation of the various factors that have to be taken into account when assessing the human health aspects of methylmercury and mercury. Many of these assessment approaches are applicable to human health concerns for a wide range of CEC.

Mergler et al. (2007) provide an insightful discussion of toxicokinetic and physiologic based pharmacokinetic models to estimate internal doses for methylmercury. Although not easy, coupling these models with the aforementioned biogeochemical models in the previous section above, provides a connection between inputs in space and time, movement through the environment, uptake by humans, and potential or probable adverse effects of various types.

THE PRESENT

We are responding to the legacy of several previously identified pollutants of long environmental half-lives—designated Persistent Organic Pollutants or POPs by various national and international organizations, e.g. the Stockholm Convention of on Persistent Organic Pollutants 2001. New chemicals of environmental concern (CEC) continue to be added to a list of such chemicals. Examples are polybrominated biphenyls (PPBs) and per- and polyflouroalkyl substances (PFAS).

We must remain vigilant. During the past two decades an increasing number of studies have been published (now a plethora of publications) concerning plastics, especially “micro- and nanoplastics”, in the environment. They are a problem in and of themselves. The small plastic particles and pellets also have surfaces that sorb POPs and related CEC (e.g. Takada and Karapanagioti 2019). The emerging problem of plastics in the oceans was documented by Carpenter and Smith (1972) in a reputable scientific journal, the same year as “The PCB Story”. Yet, the topic of small pieces of plastic in the environment garnered little further attention for decades. How did we (I include myself) miss conducting the requisite research during the 1970s and 1980s on this increasingly important problem? We should learn from this and search diligently for important environmental problems we may be missing as we focus on both legacy and emerging chemicals of environmental concern, and on human caused climate change.

John W. Farrington

served as Associate Director for Education and Dean of Woods Hole Oceanographic Institution (WHOI) from 1990 to 2002, and as Vice President for Academic Programs and Dean 2002–2005. Retiring in early 2006.

His career has involved successive appointments at WHOI from Postdoctoral Investigator (1971) to Senior Scientist (1982), including Director of the WHOI Coastal Research Center (1981–1987), and he was Michael P. Walsh Professor of Environmental Sciences at UMass-Boston (1988–1990). During August 2009 to November 2012 he assisted his undergraduate and M. S. degree alma mater as Interim Dean of the School of Marine Science and Technology (SMAST) and then Interim Provost, University of Massachusetts-Dartmouth and continues as an Adjunct Professor at SMAST. He served as President of the Ocean Sciences Section of the American Geophysical Union from July 1, 2008 to June 30, 2010.

His scholarly interests include marine organic geochemistry, biogeochemistry of organic pollutants (including oil spills and chronic petroleum releases to the marine environment), biochemistry of marine organisms, environmental quality issues, science education, and science-policy and science-religion interactions. John has participated in eighteen open ocean oceanographic cruises, eight as Chief Scientist, a research dive in DSRV Alvin, Dive 658, July, 1976, and numerous one-day coastal cruises. He has published one hundred and nineteen publications in refereed scientific journals, books and reports; forty-five publications related to education, policy, public information, or science- policy interactions; and twelve technical reports. He has been a member of advisory committees for several international, national, state and local agencies and organizations. He has testified several times before the United States Congress on matters pertaining to oceanic and coastal environmental quality issues.

His honors include the University of Rhode Island Alumni Association Award for Excellence in Research in 1998. “For leadership in promoting science and its use in sound decision-making,” the United States Geological Survey Ambassador for Science Award in April 2001 “For distinguished service to the environment and community,” the David B. Stone Award from the New England Aquarium September 2001, the Bostwick H. Ketchum Award from Woods Hole Oceanographic Institution October 2003 “in recognition of achievements in science, education, and policy concerning the input and fate of organic contaminant chemicals in the marine environment.” In November 2003, he received a life appointment as a National Associate of the U.S. National Academies, “in recognition of extraordinary service to the National Academies in its role as advisor to the Nation in matters of science, engineering, and health.”

He has been honored with establishment of the John W. Farrington Reference Collection in the Woods Hole Oceanographic Institution Student Center established September 24, 2005 by the MIT/WHOI Joint Program Graduate Students and Alumni. In October 2006 he was placed on the Graduate School of Oceanography, University of Rhode Island Dean’s List for Outstanding Professional Achievement. In July 2007, he delivered the Nanquiang Lecture at Xiamen University in Xiamen, China. In March 2009, he received Doctor Honoris Causa from The University of Concepcion for “highly commendable and innovative contributions to the development of knowledge in benefit of the University of Concepcion and of the national and regional Higher Education, also contributing significantly to international scientific collaboration, and to the development of understanding and solidarity among nations”. He received the Samuel P. Stone Alumni Award in Sciences from the College of Arts and Sciences, University of Massachusetts-Dartmouth 2009, was Elected Fellow of the American Association for the Advancement of Science in November 2009, and Fellow of the American Geophysical Union in 2015.