As indicated in the previous report (Solomon et al., 1993), effluents from some pulp and paper mills have yielded measurable responses by biota in receiving aquatic systems. Considerable information has been published on the effects of effluents from a variety of mills on many species and communities in receiving aquatic systems. However, synthesis of this information is often hampered due to inadequate characterization of the effluent (e.g., pulp source, pulping process, bleaching process, yield, and wastewater treatment are some factors that can greatly influence the presence or magnitude of effects and these factors are often not specified). Further, characteristics of the receiving aquatic system such as flow, volume, extant biota, substrate type and water quality are similarly often not specified. Regardless of these impediments to understanding underlying causes of responses, we are clearly left with some responses deserving consideration and even further study. As for the other sections of this report, this review concentrates on information produced since 1993.
Characterization of known or potential risks currently associated with pulp and paper mill effluents requires careful consideration of responses of receiving aquatic systems. Ecosystem, community, population, organismal and sub-organismal responses may be important endpoints or measurements in this characterization. Also crucial would be changes in these responses spatially and temporally as a function of changes in bleaching processes, wastewater treatment, or other factors that may alter exposures and concomitantly reduce risk in aquatic systems. Measurements of these effects have focused on important components of aquatic systems including fish, invertebrates, plants (algae) and suborganismal responses or biomarkers.
Since physiological responses are not typically linked with effects on growth, reproduction, or mortality of fish in receiving systems, this section focuses on organismal and population responses to pulp and paper mill effluents. Physiological or sub-organismal responses are considered in a subsequent section of this report. Although it is probably more a phenomenon than an effect, bioconcentration/bioaccumulation is also covered in this section.
Effects of pulp and paper mill effluent exposures on fish have been documented in both wild fish and in life cycle laboratory studies. Decreased reproductive performance in fish has been attributed to changes in maturation and fecundity (Hodson et al., 1992a; Gagnon et al., 1994a; 1994b; Sandström, 1994). Exposures to effluent from some bleached kraft mills have resulted an increased age to maturity, smaller gonads and lower fecundity with age in both males and females. Other observations included absence of secondary sex characteristics in males, and females failed to show an increase in egg size with age.
Some field observations of bleached kraft mill effluent effects have been confirmed by laboratory studies. Fathead minnows (Pimephales promelas) were exposed throughout their life cycle to secondary-treated bleached kraft mill effluent and responded with delayed sexual maturity, decreased egg production, depressed secondary sexual characteristics, and depressed hormone production. These observations were based on exposures of greater than 20% effluent (McMaster et al., 1996b; Robinson, 1994).
It is important to note that these reproductive responses of fish have not been observed at all pulp mill sites. Minimal changes in reproductive steroids of whitefish and suckers were observed in studies conducted in the effluent of a secondary-treated bleached kraft mill. Only mixed function oxygenase (MFO) induction was observed. In other studies of secondary-treated bleached kraft mill effluent are installation of chlorine dioxide substitution (Swanson et al., 1994; Kloepper-Sams, et al., 1994), MFO elevation was the only consistent response observed and numerous other physiological parameters were unresponsive.
Some recent reports have suggested that some previously unrecognized effects were caused by long term exposures to pulp and paper mill effluents. Smits et al.(l996a; 1996b) reported evidence of suboptimal immune function in mink (Mustela vison) associated with BKME exposure. In this study, mink were exposed via diet (fish from BKME receiving waters) as well as by ingestion of wastewater (25% BKME). This effect has not been field verified, however. Other researchers (e.g., Rao et al., 1994; Rao et al., 1995) have found some evidence of mutagenic and genotoxic potential of pulp mill effluent in laboratory tests while Metcalfe et al. (1995) reported some mutagenic activity of BK extracts but that BKME is not a potent liver carcinogen in fish. It is important to note that these are laboratory studies with unmeasured exposures and the environmental significance of the results need to be evaluated. In fact, a thorough histopathological study of fish exposed to BKME in situ revealed no incidence of cancers in fish (Deardorff et al., 1995).
A thorough study did not find any effects of mill effluents from a variety of sources on reproduction of Ceriodaphnia. Receiving waters from a variety of mills using diverse pulping processes and wastewater treatment tactics and discharging > 50,000 m3 day-1 of effluent were studied. The mills included in the study used chlorine/chlorine dioxide bleaching and an unbleached sulfite process which produced unbleached pulp. Cenodaphnia reproduction results (7-d survival and reproduction tests) correspond with the presence of secondary treatment. In all cases of mills with secondary treatment, Ceriodaphnia reproduction was enhanced relative to the corresponding reference water. This enhancement is commonly seen when ambient food (e.g., microbes) in the receiving water is increased.
In a laboratory study, Higashi et al. (1992) reported a high molecular weight component of bleached kraft mill effluent resembling Iignin decomposition products affected the sperm of an echinoderm, the purple sea urchin (Strongylocentrus purpuratus). Successful reproduction was apparently prohibited when the effluent material bound to the sperm and prevented recognition of chemical signals from the egg. This effect has not been documented in any field study, however.
Previous studies had illustrated that the effects of bleached kraft mill effluent on primary producers in receiving aquatic systems were limited to areas where light penetration sufficient to drive primary production was diminished. This usually constitutes a few meters of a mixing zone where receiving system flows are significant. Some recent reports suggested that chlorine-dioxin based bleaching processes could yield residual chlorate that could be toxic to certain algae in receiving systems. These effects should be most pronounced in systems with low ambient nitrogen concentrations (~ 10 mg NO3-N/L) since chlorate toxicity increases with decreased available nitrogen (Van Wijk and Hutchinson, in press). A recent review and research publication by Van Wijk and Hutchinson (in press) concluded that marine macro brown algae (e.g., Fucus sp.) are extremely sensitive to chlorate with adverse long-term effects at concentrations of 5-15 mg ClO3-/L at low ambient nitrogen concentrations and six month exposures. This is several orders of magnitude more sensitive than other algal species tested. In recent studies of Western Canadian rivers, growth rates and taxonomic composition of algae were not altered by exposures to chlorate up to 500 mg/L at 10 mg/L NO3-N (Perrin and Bothwell 1992). In most situations where chlorate would occur, available nitrogen should be protective of algae. To impart some perspective of risk to this situation, it is helpful to recognize that chlorate in effluents from ECF mills are non-detectable at mg/L concentrations. Therefore, a clear margin of safety is apparent, consonant with no quantifiable risk.
An issue that is currently unresolved regarding potential effects of new bleaching processes on primary producers is the toxicity of chelators to algae. Algae are relatively sensitive (EC50 = 10 µg/L) to some chelators which are resistant to secondary treatment (e.g., EDTA, DTPA). As new studies are conducted, this concern or question can be incorporated and the risk can be evaluated.
A variety of suborganismal, physiological or biomarker responses to pulp mill effluents have been measured in a number of tissues and cells. These tissues and cells have come from field-collected organisms as well as from organisms that have been exposed under carefully controlled conditions in mesocosmstmicrocosms or in laboratory exposures. Both responses indicative of exposure and responses indicative of effects have been measured. Presented below is a brief summary treatment of these data since 1994.
Enzyme induction has been used as a reliable measure of exposure. Mixed-function oxygenases (MFOs) are multi-enzyme complexes based on cytochrome P-450 that catalyze oxidation of various low molecular weight substrates. MFO is inducible by a variety of compounds that can bind to the Ah receptor. MFO activity is often determined from the rate of reaction of substrates with liver microsomes based on the reaction of EROD. Thus, EROD activity measurements are indicative of MFO induction and MFO induction is indicative of exposure to substances with the capacity to induce enzyme activity. The absence of significant MFO induction is good evidence of the absence of inducers at levels expected to cause adverse effects. However, significant MFO induction in exposed organisms is indicative of exposure and the potential for adverse effects if the inducers are identified and the strength of their interaction with the AhR is determined. Pulping liquors, both weak black liquor from kraft pulping and spent liquor from alcohol pulping, are potent MFO inducers. Products of resin acids are also potent MFO inducers. Historically, bleaching has also been a source of inducers. However, it is not clear that any portion of the pulp and paper process (species pulped, operation, bleaching etc.) has as great an effect on MFO induction as the efficacy of secondary treatment systems in reducing induction potential of effluents (Martel and Kovacs, 1996).
Other markers of exposure have included tissue levels of chlorophenolic compounds (Owens et al., 1994), recombinant receptor/reporter gene assays (Zacharewski et al., 1996) and P4501A protein antibodies (Owens and Lehtinen, 1996).
Several parameters have been used to predict reproductive responses of organisms in pulp and paper mill effluents. Levels of steroid hormones have considerable promise for prediction of impacts on sexual maturity and fecundity. Life cycle studies showed a good correlation between depressed circulatory steroid levels and altered secondary sexual characteristics with changes similar to those observed in wild fish (Robinson et al., in press). However, the mechanistic links between reproductive effects and a chemical cause are weak. Thus, no process modifications or effluent treatment strategy can be recommended to eliminate them. Plant sterol hormones such as ß-sitosterol can depress circulating steroid levels (Tana et al., 1994) and increased vitellogenin production.
Recent changes in process and wastewater treatment have led to dramatic decreases in TCDDs and TCDFs in fish in receiving systems (Swanson et al., 1996). This decline in TCDDs and TCDFs in fish tissue has been observed at a number of locations after the bleaching process was changed. In fact, Sonnenberg et al. (1994) suggested that much of the difference in bioaccumulated chlorinated substances between upstream and downstream fish was due to the fact that fish downstream from pulp mills are typically fatter (contain more lipids) than upstream fish and that the bleaching process may not be the most important source of organochlorines in fish downstream from pulp mills.
There are several obvious temporal trends in biological responses to pulp mill effluents. Clearly, these are related to alterations in exposure as a result of changes in process, raw material use, and effluent treatment. A general trend potentially influencing exposure has been rapid conversion to elemental-chlorine free (ECF) bleaching sequence during the past few years (Deardorff et al., 1995). This has led to notable decreases in lipophilic chlorinated substances (e.g., PCDD/PCDFs) in effluents. Further, recognition of the contribution of well-managed biological or secondary treatment systems to reduction in concentrations and effects of polychlorinated phenolic compounds has led to additional gains in terms of exposures. Consequently, fish tissue samples have shown dramatic declines in dioxin concentrations with concomitant lifting of consumption advisories.
In general, responses of communities and populations to improvements in waste treatment and pulping processes have been positive (Munkittrick et al., 1992; Axegård et al., 1993, Deardorff et al., 1995, Carey et al., 1996). In a few cases, there are still apparently issues to be resolved. In other cases, the improvements have had negligible effects since there were no impacts associated with the previous operating conditions (Deardorff et al., 1995). In other cases, the necessary process changes required are not known at present, but secondary wastewater treatment and 100% ClO2 substitution were not sufficient to alleviate reproductive responses in fish. Tight controls of process streams that can constitute sources of bioactive compounds including spills and black liquor losses as well as recovery of foul condensates may contribute to resolution of the few cases where effects are still observed (Axegård et al., 1993).
Any strategy employed to foster reductions in environmental risks should be evaluated on a holistic basis (e.g., life cycle analysis, risk assessment). For example, we do not need to trade an aquatic problem for an atmospheric one. Similarly, we do not need to spend exorbitant amounts of money correcting a "problem" that does not exist.
Before risk assessments of pulp mill effluent receiving waters are conducted it is crucial to understand the type of target ecosystem and the functional principles of the particular effluent receiving water body. For example, the functional mechanisms of rivers are different from those of lakes and coastal ecosystems. The functional characteristics of rivers are largely based on imported energy, whereas the functional characteristics of lakes and litoral costar systems are based on their own autotrophic capacity. Autotrophic capacity is, in turn, a function of nutrient input and light energy (latitude, Lehtinen et al., (1996). Receiving waters at different latitudes may therefore show profoundly different capacities to assimilate loads of antbropogenic substances. Such factors have rarely been taken into consideration in risk assessments. Autotrophic production in boreal regions, during which there is net oxygen evolution and carbon dioxide fixation, is restricted to a short period, 2-3 months in the year, whereas ecosystems in more equatorial latitudes may function autotrophically all year round. Such functional differences are likely to modify the effects of effluents. Therefore, risk assessments of pulp mill effluents should, in a case-by-case fashion, consider ecosystem function as a key property.
The effects of long-term exposure to pulp and paper mill effluents are deserving of continued evaluation because of their high volume introduction into receiving systems. This recommendation is made since our evaluation "tools" and "strategies" are constantly evolving and improving. However, any decisions made based upon this monitoring must be made with appropriate consideration of the ecological relevance of the data. Long-term and continuous exposure to effluents may cause changes in reproductive cycles, reduced or enhanced growth, changes in the age-structure of populations, or inhibit an organism's ability to cope with stress. However, all of these effects are not necessarily adverse unless they have been evaluated in the light of their environmental significance.
Any risk mitigation strategies employed should be evaluated on a holistic basis (e.g, life cycle analysis, risk assessment). For example, we do not need to trade an aquatic problem for an atmospheric one. Similarly, we do not need to utilize scarce resources correcting a "problem" that does not exist. The effects of long-term exposure to pulp and paper mill effluents are deserving of continued evaluation because of their high volume introduction into receiving systems. However, any decisions made based upon this monitoring must be made clear understanding of the ecological relevance of the data.