Responses of white sucker (Catostomus commersoni) to 20 years of process and waste treatment changes at a bleached kraft pulp mill, and to mill shutdown
Introduction
There has been considerable interest in the effects of bleached kraft mill effluent on fish populations over the last 15 years (McMaster et al., 2003), primarily as a result of two long-term studies at Jackfish Bay (JFB), Canada and at Norrsundet, Sweden. In the mid 1980s bleached kraft mill effluent studies at Norrsundet showed that pulp mill effluent could cause impacts on growth and reproduction of fish at very low environmental concentrations (Södergren, 1989). Although studies at Norrsundet confirmed many of the earlier findings over the following decade (Sandström, 1994), the results were not initially accepted as it was believed that these results were unique and would not occur at mills in North America (reviewed in Munkittrick et al., 2003). While the first reports were being published in Sweden, a series of Canadian studies were initiated on a bleached kraft pulp mill at Jackfish Bay on Lake Superior that showed alterations in reproduction of fish exposed to the effluent (McMaster et al., 1991, Munkittrick et al., 1991). These alterations included delayed sexual maturity, and reductions in gonad size, expression of secondary sexual characteristics and circulating steroid hormone levels (McMaster et al., 1991, Munkittrick et al., 1991). The Jackfish Bay studies have continued over the past two decades as the mill implemented waste treatment and process changes (summarized in Table 1).
The early findings prompted work at a variety of sites in Canada (reviewed in Munkittrick, 2004). While follow-up studies in Canada confirmed similar impacts (smaller gonads and larger livers in exposed fish) at a variety of sites (Munkittrick et al., 1994), this was not the case with all sites examined and impacts appeared to be site-specific and affected by a number of potential modifying factors (Kovacs et al., 1997). Interest in pulp mill impacts on wild fish has promoted similar work in Sweden (Larsson and Förlin, 2002, Sandström, 1994, Sandström and Neuman, 2003) and Finland (Karel and Niemi, 2002, Lappivaara et al., 2002), and has expanded to the United States (Fentress et al., 2006, Orlando et al., 2007, Sepúlveda et al., 2003, Sepúlveda et al., 2004), New Zealand (van den Heuvel et al., 2006, van den Heuvel et al., 2007), Portugal (Maria et al., 2003, Santos et al., 2004), India (Al-Arabi et al., 2005) and Chile (Orrego et al., 2005a, Orrego et al., 2005b, Orrego et al., 2006).
The Canadian pulp and paper industry underwent a series of process changes and modernizations during the 1990s, and spent over $8 billion in improvements to reduce the release of chemical contaminants (FPAC, 2002, FPAC, 2007). Beginning in the early 1990s, pulping process changes were undertaken to reduce the potential for the formation of dioxins and furans, including the substitution of chlorine dioxide (ClO2) or other bleaching agents for elemental chlorine (Doonan et al., 2005). Waste treatment systems were installed at nearly all mills in Canada to reduce biological oxygen demand, suspended solids and the acute lethality of final effluents (Munkittrick et al., 1992b, Munkittrick et al., 1997). These changes resulted in significant improvements in effluent quality and toxicity for which they were targeted. While some studies have attempted to followed the temporal pattern of fish reproduction responses to these numerous improvements and changes (Kovacs et al., 1995, Kovacs et al., 1997, Martel et al., 1994, Munkittrick et al., 1992b, Munkittrick et al., 1997, Munkittrick et al., 2000, Sandström and Neuman, 2003), two primary obstacles have prevented the establishment of linkages between production changes and improvements in reproductive performance in native fish: (i) many mills performed multiple process changes simultaneously making it impossible to attribute specific changes to improvements (Hewitt et al., 2008), and (ii) there has not always been good communication on mill process change information between mill personnel and investigators. What is clear is that despite many improvements, subtle effects on fish reproduction have persisted at some sites (McMaster et al., 2006, Munkittrick et al., 1992b, Sandström and Neuman, 2003).
The early Canadian findings led to the development of a regulated, cyclical Environmental Effects Monitoring (EEM) program near Canadian pulp and paper dischargers (Walker et al., 2002). Cycle 2 (1996–2000) and Cycle 3 (2000–2003) EEM program results showed three response patterns downstream of mills across Canada: nutrient enrichment, nutrient limitation and metabolic disruption (Lowell et al., 2005). Across Canada the most consistent response pattern seen in fish in Cycles 2 and 3 of EEM was metabolic disruption (Lowell et al., 2005); this pattern is characterized by an increased condition factor and liver size and decreased gonad size in fish, the same pattern that was initially seen at Jackfish Bay (Lowell et al., 2003, Lowell et al., 2004, Lowell et al., 2005). While there is general acceptance in Canada that some mill effluents can impact the reproduction of fish, there is still some controversy about how widely applicable these results are (Kovacs et al., 1997, Kovacs et al., 2005), or whether modernized mills still show impacts (Flinders et al., 2009).
The current economic conditions, coupled with the expansion of low cost pulp producers in South America, have meant large-scale changes in the Canadian pulp and paper industry including outsourcing, reducing costs and merging of companies (Pikulik and Crotogino, 2002, Lynch, 2007). These changes have resulted in closure of a number of mills where significant past studies have taken place, including the mills at Smooth Rock Falls, ON (Munkittrick et al., 2000), and Miramichi, NB (Couillard et al., 1999, Couillard and Nellis, 1999, Courtenay et al., 1993). These economic conditions inevitably affected the Jackfish Bay mill.
The studies at Jackfish Bay have been maintained throughout the 1990s and to the present day. Much of the whole-organism data has not been previously published and this study synthesized the data from a wide variety of studies (Table 2) from 1988 to 2007 into a chronological study of the responses of fish populations to the installation of secondary treatment and several other process changes. The overall objective of this study was to determine if there were significant changes in the response of the wild white sucker (Catostomus commersoni) populations to changes in process and waste treatment that occurred at the mill. Sample collections for this study continued while the mill was temporarily shutdown (closure was from February to September 2006) and after the mill had been reopened for a period of 8 months.
Section snippets
Study site
The bleached kraft pulp mill located in Terrace Bay, ON, Canada discharges effluent into Blackbird Creek that enters Jackfish Bay, Lake Superior (Fig. 1); the effluent makes up to 65–95% of the volume of the small creek during the summer to winter periods and flows 15 km before reaching Lake Superior. Historically, the pulp mill produced approximately 1200 air-dried metric tons (ADMT) of pulp per day and the mill discharged about 120,000 m3 of effluent per day. Jackfish Bay (48°50′N; 86°58′W) is
Results
During the years of primary effluent treatment (1988 and 1989), pre-spawning effluent-exposed white sucker were significantly shorter, had higher condition factors, and were significantly older than reference fish during most sampling periods (Table 3, Table 4). Pre-spawning exposed fish were also lighter and had smaller relative gonad and liver sizes but no differences in fecundity (Table 5). In the early recrudescent period, white sucker were shorter, lighter, with smaller gonads but had
Discussion
This study has demonstrated that bleached kraft pulp mill effluent at Jackfish Bay has impacted female and male white sucker over the past 17 years, and neither secondary effluent treatment nor bleaching process changes over the years have improved the status of pre-spawning fish. These impacts have primarily been on gonads, livers and condition, with fecundity not affected by effluent exposure. Implementation of secondary treatment and conversion to ECF bleaching were associated with slight
Summary
Effluent-exposed white sucker from Jackfish Bay showed a response pattern of reduced gonad sizes and circulating sex steroid levels, increased liver size and condition, and older age and delayed maturity. Although differences were still evident after secondary treatment, liver size differences were reduced by more than 25% in males and 50% in females, gonad size differences by closer to 10%, and significantly reduced age differences between sites. Conversion to high levels of ECF bleaching
Acknowledgements
This study has been supported over the years by a wide variety of funding agencies, graduate students, and technicians. The current study benefited by funding from the Canada Research Chairs and NSERC Discovery grant program (KRM), Environment Canada (MEM and LMH) and the University of New Brunswick.
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