Detection of reproductive impacts of effluents from pulp and paper mills: Shifts in issues and potential causes

Early research in the late 1980s initiated considerable debate about the causes of reproductive effects observed in fish near pulp and paper mill outfalls and linkages with the effluents discharged. This research into the effect of pulp and paper mill effluents on aquatic ecosystems had a major impact on environmental remediation efforts of the industry, led to the development of a standardized, national environmental effects monitoring program in Canada, and resulted in changes to regulations in Canada and many other jurisdictions internationally. Many of the papers dealing with this important environmental issue were published in Environmental Toxicology and Chemistry and include several papers on the “Top 100” list. Although the mechanisms resulting in population-level changes in fish at these sites are now better understood, the specific causal chemicals and processes remain elusive 1. In the mid-1980s, the Environment Cellulose project in Sweden suggested that pulp mill effluents could cause impacts on aquatic ecosystems, including impacts on fish at very low dilutions in the receiving environment 2, 3. These observations focused international attention and debate on pulp mill effluents, and an international review panel was formed to review the findings and uncertainties 4. It was argued by some at the time that the impacts were unique to Norssundet and would not be expected at other mill sites in Sweden or other parts of the globe (e.g., North America). In the late 1980s a number of similar studies were initiated at pulp mill sites in Canada. Our studies were initially focused on Jackfish Bay in Lake Superior, which received effluent from a bleached kraft mill located in Terrace Bay, Ontario, Canada. The bay received no other effluents and had no permanent human residents. Relative to reference sites in Lake Superior, white sucker (Catostomus commersoni) exposed to the effluent in Jackfish Bay were shown to have lower levels of circulating reproductive steroid hormones, smaller gonad sizes, and less obvious secondary sex characteristics, concomitant with mixed function oxygenase induction 5, 6. These observations expanded the Swedish findings of the potential effects of pulp mill effluents at low concentrations to include a potential mechanism for the reproductive disturbances, that is, the depression in hormone levels 7, 8. Our initial results in Canada therefore supported the Swedish reports and prompted a series of studies to understand the responses and make linkages to causes at Jackfish Bay that continue to this day 9. We now have almost 25 years of data from this site and comparable reference areas. Our initial results became public as both Canada and the United States were considering revisions to their national effluent regulations for pulp and paper mills. Until the late 1980s, little attention was paid to pulp and paper mill effluents. Environmental regulations developed in the early 1970s were focused on habitat alterations, eutrophication, and toxicity concerns 10. During the mid- to late 1980s, polychlorinated dioxins and furans were detected in effluents 11 as a by-product of chlorine bleaching 12, and dioxin contamination rapidly became an international concern. At this time environmental activists and regulators were generally focused on chlorine bleaching and the possible impacts of persistent chlorinated organic material on ecosystems 13. A worldwide public campaign against the use of molecular chlorine in bleaching pulp developed 14 despite the lack of clear evidence linking chlorinated compounds to effects in fish 15. The initial studies at Jackfish Bay in 1988 5 and 1989 6 were completed prior to the construction of a large aerated stabilization lagoon (secondary treatment), which came online in October 1989. Collections of spawning fish the following spring (May 1990) showed that impacts remained in the population despite the implementation of secondary treatment 16. This was not considered surprising at the time as reproductive effects were being attributed to chemicals such as polychlorinated dioxins, which had long half-lives in fish and the environment 17. Much of science progresses through serendipity, although we like to think of it as good design. In August 1990 we initiated fish collections in Jackfish Bay that were designed to determine the spatial extent of the effects so that we could establish a baseline for watching the future recovery of the system as exposure to persistent chlorinated compounds was reduced over time. When we returned to sample additional fish in September 1990, the effluent flow was much reduced because, unbeknownst to us, the mill was going through an annual maintenance shutdown. We decided to sample the fish anyway, assuming that with the expected long half-life of the “responsible” chemicals, our sampling and interpretation would not be affected. Much to our surprise, the resulting analyses found no evidence of mixed function oxygenase (MFO) induction, relative to very high induction in the fish sampling collected only a few weeks earlier. These results, reporting the fast recovery in MFO activity and suggesting that the responsible chemicals were probably not long-lived and likely associated with chemicals that could survive secondary waste treatment 16, received considerable international interest. These new findings indicated that there would still be the potential for receiving environmental effects after mills modernized their waste-treatment systems even though they complied with the proposed new federal regulations still under development in Canada. These concerns were supported by studies being conducted at other mills in Canada that had installed secondary treatment 18 and minimized the use of molecular chlorine 19. The discovery of subtle reproductive effects due to exposure to “nonlethal” pulp mill effluent challenged a number of Canadian regulatory assumptions. It had long been assumed that effluents, which were not acutely toxic at 100% concentration, would not show chronic toxicity after receiving significant environmental dilution. The discovery of subtle reproductive impacts at low-level exposures to “nontoxic effluents” associated with chemicals that appeared to be water-soluble and that survived secondary treatment meant that it was possible for chemicals that were not persistent, did not appreciably biomagnify, and were not toxic in existing regulatory bioassays to have significant reproductive effects that could exist for large distances downstream of outfalls, approaching 100 km 18. These findings at pulp and paper mill sites were being reported as the issue of endocrine-disrupting substances was emerging. For example, the highly influential work of Colborn et al. 20 received considerable attention and increased the concerns that existing regulatory tools and techniques needed to be reexamined. Within Canada and globally there was intense public pressure to eliminate chlorine use in bleaching pulp 14, and several Canadian provinces brought in “zero AOX” regulations (adsorbable organic halides). Under the Canadian Environmental Protection Act, “effluents from pulp mills using bleaching” were declared “toxic,” which then required risk-management action 21, but additional information was required to show that regulation of chlorine would actually alleviate the impacts of concern. In addition, the Canadian federal regulations under the Fisheries Act were being revised to address effluent quality limits required to protect the environment. Despite the global pressure to regulate molecular chlorine, it was still unknown if or how chlorinated contaminants might have a role in causing the kinds of effects being observed. As a result, in the fall of 1991, we selected 10 large pulp mills in Ontario, Canada, to determine whether we would see similar effects on fish as we had reported previously at Jackfish Bay. The results of these studies showed that similar impacts were observed even at mills that did not use chlorine 22. In addition, the effects were not predicted by chronic bioassays often applied to pulp mill effluents 23 and were not predicted by tissue dioxin levels 24, 25. Although the identification of the specific responsible chemicals has proven much more elusive than originally anticipated 26, the studies led to regulators questioning the direct linkage between the biological impacts of pulp mill effluents and persistent chlorinated organic contaminants. By this time, the Canadian pulp and paper regulatory package was well into its development and it was well known that the regulatory package would need to deal with dioxins. It was also known that dealing with the issue of dioxins and with the need for secondary waste effluent treatment would not guarantee that the environmental effects would disappear. The widespread debate about how common these effects would be and whether the regulatory package would truly eliminate environmental concerns such as those seen in Jackfish Bay contributed to the development of the methods for the Environmental Effects Monitoring (EEM) program and the inclusion of a requirement to conduct EEM studies in the pulp and paper regulatory package under the Fisheries Act 27. The objective of the EEM regulation was to direct an industry-funded monitoring program to provide the information to the government to determine what proportion of receiving environments were still associated with environmental effects when they were in compliance with the new regulation. After several cycles of this monitoring program, it was demonstrated that the pattern of responses reported at Jackfish Bay was consistent with the typical or average response seen at most Canadian pulp mills 28. There was intense public debate about the existence of the reproductive responses associated with exposure to some pulp mill effluents for almost 15 years. The research included in the “Top 100” papers had an impact on the regulatory approach in Canada by showing that compounds other than persistent organochlorines were contributing to impacts and that proposed regulations would not necessarily remove reproductive impacts in fish. This led to the implementation of a national monitoring program (EEM) and considerable investment by the Canadian pulp and paper industry to improve their effluent quality. These studies also influenced the structure of monitoring programs at pulp mill sites in New Zealand, Scandinavia, the United States, and South America. Impacts of the results are still seen internationally, and a recent long-term monitoring program developed for a new pulp mill in Uruguay utilized the Canadian EEM framework through a Finnish consulting company for a World Bank project 29. This work has had a far-reaching impact on the development of regulations and subsequent monitoring that has resulted in considerable improvement in the environment, and the results remain one of the best-documented cases of endocrine disruption associated with chemicals discharged into the environment. The current situation with the pulp and paper industry and the potential impacts are of interest to understand the breadth of the issue today. A Web of Science search in January 2013 found more than 325 papers published on pulp mill effluent since January 2010, with authors from more than 40 countries; 160 of the papers fall under the category of “environmental sciences ecology,” and more than half of the papers come from India, Canada, the United States, and China. A similar search from January 1985 to 1988 found 37 papers, with 70% of the authors from Sweden, Finland, Canada, and Denmark. The identities of the compounds responsible for the reproductive impacts are still not confirmed and remain an area of interest. The economic situation in North America, combined with the expansion of the pulp and paper situation in South America, has led to the closure of a large number of Canadian mills and the switch in processing to new technologies and new products. In some countries, cellulose industries are moving quickly toward biorefinery capacities, and the potential impacts of these new effluents are unknown. The closed facilities also offer opportunities to study ecosystem recovery after the cessation of effluent release. As well, the expansion of cellulose industries in South America and Asia offers a wealth of opportunities for study in new ecosystems and for examination of the potential impacts of modern processing and treatment technologies. Most of this work was conducted while all three authors were employed by the federal government of Canada. The authors have no conflicts of interest to declare. Table S1 (49 KB PDF). Additional Supporting Information may be found in the online version of this article. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.

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