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944 The Toxicology of Fishes
of PMEs high in fiber and BOD resulted in habitat degradation (e.g., smothering of spawning beds due
to fiber deposition, reduced oxygen concentration in the water column) and acute lethality to fish in
receiving waters (Folke, 1996; McLeay and Associates, 1987; Owens, 1996). In response to these effects,
regulators established “end-of-pipe” effluent quality limits for BOD and total suspended solids (TSS),
an indication of the fiber concentration in effluents (Folke, 1996; Owens, 1991). Final effluents could
also not be acutely lethal. The pulp and paper industry in North America and Scandinavia responded to
observations of environmental impact and regulatory concern by significantly improving effluent quality
with better process and spill control and installation of effluent treatment (Smook, 1994; Folke, 1996).
In the 1970s and early 1980s, the focus shifted to identification of the chemicals responsible for acute
toxicity of PMEs (Folke, 1996; Owens, 1991, 1996). A landmark paper in this regard was that of Leach
and Thakore (1975), who identified resin acids as primary contributors to acute effluent toxicity to fish.
This led to increased attention to resin and fatty acids and chlorinated phenolics (Holmbom and Lehtinen,
1980; Kringstad and Lindström, 1984; Owens, 1991). In addition, the discovery of persistent chlorinated
organic compounds (dioxin and furan congeners) bioaccumulating in aquatic biota led to regulations
restricting their discharge in whole (adsorbable organic halide) or in part (dioxins and furans) (Folke,
1996; Servos et al., 1994).
During the 1980s and 1990s, process modifications largely focused on changing the type or volume
of bleaching chemicals used to reduce the formation and discharge of chlorinated organic compounds
(Kovacs et al., 2003; Oikari and Holmbom, 1996; Owens, 1996; Servos, 1996; Strömberg et al., 1996).
Prior to the discovery of these compounds, elemental chlorine was the dominant bleaching agent. To
reduce the discharge of organochlorines, elemental chlorine-free technologies were developed where
elemental chlorine was replaced wholly, or in part, by chlorine dioxide. Totally chlorine-free bleaching
technologies have also been developed where bleaching is conducted using oxygen, ozone, or hydrogen
peroxide. The concentration of organochlorines also decreased due to reduced volumes of chemicals
used in the bleach plant. Improved delignification of the pulp prior to the bleach plant reduced the
amount of fiber entering the plant, which in turn, reduced the volume of bleaching chemicals required
to achieve desired pulp brightness (NCASI, 1989).
Changes in mill process and effluent treatment during the 1980s and 1990s improved effluent quality
and shifted the assessment of effects from measurements of lethal toxicity to the potential of effluents
to cause more subtle, sublethal effects such as reduced growth and reproduction (Folke, 1996). Interest
was also focused on the potential for physiological indicators to identify pulp mill effects in fish at early
stages of effect diagnoses. Induction of liver detoxification enzymes (mixed-function oxygenases
[MFOs]), for example, received much attention as a physiological indicator of exposure of fish to PME
(Hodson, 1996; Martel et al., 1994, 1995; Munkittrick et al., 1992a,b, 1994; Oikari and Holmbom, 1996;
Soimasuo et al., 1998a,b).
Long-term field studies in Sweden, Finland, and Canada recorded the changes in effects measured
through periods of mill modernization. The receiving waters of a BKPM at Norrsundet, Sweden, on the
coast of the Bothnian Sea, have been a site of extensive field investigations examining effluent effects
on the survival, reproduction, physiology, biochemistry, histopathology, and morphology of perch (Perca
fluviatilis) (Andersson et al., 1988; Södergren, 1989). In the 1980s, typical effects measured in the
exposed fish included fin erosion, reduced gonad weight, delayed sexual maturation, impaired fry
production, liver enlargement, induction of liver detoxification enzymes, affected carbohydrate metab-
olism, disturbed ion balance, stimulated red blood cell production, and a weakened immune system
(Andersson et al., 1988; Larsson et al., 1988; Sandström et al., 1988). After significant improvements
in mill process and effluent treatment, studies in 1993 indicated many of the biochemical and physio-
logical effects in perch had either disappeared or were significantly reduced (Ericson and Larsson, 2000;
Larsson et al., 2003). Delayed sexual maturity, smaller perch embryos, altered sex ratios, genotoxic
effects (i.e., DNA adducts), and slight responses in liver detoxification enzymes, however, continue to
be reported (Sandström, 1995; Ericson and Larsson, 2000; Larsson et al., 2000; Larsson and Forlin 2002;
Larsson et al., 2003; Sandstrom and Neuman, 2003).
Since 1991, an intensive Finnish case study has been conducted at southern Lake Saimaa, in connection
with major technological changes in the pulp and paper industry (Karels and Oikari, 2000). Perch (Perca
fluviatilis) and roach (Rutilus rutilus) living in the lake are exposed to effluents from three pulp and