Combined effects of pulp and paper effluent, dehydroabietic acid, and hypoxia on swimming performance, metabolism, and hematology of rainbow trout

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Abstract

Experiments were conducted to examine the effects of a thermomechanical (TMP)/bleached kraft pulp and paper mill effluent (BKME), dehydroabietic acid (DHAA), hypoxia, and combinations of hypoxia and effluent on juvenile rainbow trout. In the first two experiments, trout were exposed for 4 weeks to 0%, 10%, 30%, and 70% TMP/BKME or 0, 35, 110, and 250 μg L−1 DHAA, respectively. Endpoints of those dose–response studies included critical swimming speed, oxygen consumption, and hematology. Reduced swimming performance was found for fish exposed to 70% TMP/BKME. Moderate increases in mean cell hemoglobin concentration at 70% TMP/BKME and blood glucose at 30% and 70% TMP/BKME were also seen. The opposite trend for glucose was found for DHAA-exposed fish, where a slight decrease in glucose was seen at 110 and 250 μg L−1 DHAA. The third experiment examined the effects of 15% v/v TMP/BKME exposure at 2.5 and 5.0 mg L−1 dissolved oxygen (DO) for 4 weeks. This experiment found no effect of low DO on swimming ability. An interactive effect between DO and effluent exposure was seen only on hematocrit, where effluent caused an increase in hematocrit at 5 mg L−1 and a decrease at 2.5 mg L−1 DO. Effluent exposure in this experiment resulted in a greater number of smaller red blood cells. The current study demonstrated physiological effects in rainbow trout exposed to varying concentrations (15–70% v/v) of a TMP/BKME and no substantial effects of DHAA exposure. With the exception of the reduced swimming performance in fish exposed to TMP/BKME, the observed effects are considered relatively small in magnitude but are occurring at concentrations of effluent that occur in the receiving environment.

Introduction

Early studies on pulp and paper mill effluents (ME) reported numerous effects on basic fish physiology, including reduced growth and food conversion in sockeye salmon (Oncorhynchus nerka) and pinfish (Lagodon rhomboides) (Webb and Brett, 1972; Stoner and Livingston, 1978), altered respiration and ventilation in coho salmon (Oncorhynchus kisutch), rainbow trout (Oncorhynchus mykiss), and pinfish (Walden et al., 1970; Stoner and Livingston, 1978), and modest increases in oxygen consumption in rainbow trout (Oikari et al., 1985). Other studies have revealed effects on swimming performance, such as reduced maximal swimming ability in juvenile sockeye and coho salmon (Brett, 1964; Howard, 1975) and impaired ability of perch (Perca fluviatilis) to maintain position in a rotary-flow apparatus (Lehtinen and Oikari, 1980). In addition to the direct effects of pulp and paper effluents on fish physiology, the potential influence of hypoxia, indirectly caused by effluents, is of concern to the health of aquatic organisms.

The high biochemical oxygen demand and nutrient levels associated with pulp and paper effluents has often resulted in low concentrations of dissolved oxygen (DO) in the receiving environment (Colodey and Wells, 1992; Chambers et al., 1997; Lowell and Culp, 1999). Due to the improvements in effluent treatment throughout the world, this situation is far less common than it was in previous decades, but it does still occur. Despite concerns about hypoxia downstream of pulp and paper mills in New Zealand (Dell et al., 1996), effluent–hypoxia interactions in fish have received only limited scientific scrutiny (Landman et al., 2004). Increased pulp mill effluent toxicity under hypoxic conditions has previously been demonstrated in fish (Alderdice and Brett, 1957; Hicks and DeWitt, 1971; Graves et al., 1981). However, since these early North American studies were performed with relatively untreated and toxic effluents, the findings can no longer be extrapolated to present day conditions. As modern, well-treated effluents are generally not acutely lethal, the impact of hypoxia on the acute lethality of effluents is no longer a relevant question. However, the converse question of what influence pulp and paper mill effluents may have on the sensitivity of fish to hypoxia remains an untested issue. Well-treated effluents still contain organic compounds, such as resin acids, which are known to influence fish respiration (Nikinmaa and Oikari, 1982), and there are reasonable grounds to hypothesize that interactions between pulp and paper effluent and hypoxia could occur.

Resin acids are natural compounds found mostly in pine species. The effects of resin acids on fish have been studied since their abundance in effluents and significance as contributors to fish toxicity was realized (Leach and Thakore, 1975). Notable effects of one abundant resin acid, dehydroabietic acid (DHAA), on the liver and blood have been observed (Oikari et al., 1983; Mattsoff and Oikari, 1987; Bogdanova and Nikinmaa, 1998; Nikinmaa et al., 1999), with recent studies elucidating effects and mechanisms relating to disruption of cellular energetics (Rissanen et al., 2003). There is some evidence to suggest that acute exposures to certain effluent components, such as tetrachloroguaiacol, may result in reduced swimming performance in rainbow trout (Johansen et al., 1994). However, Kennedy et al. (1995) showed that exposure to chlorinated DHAAs had no significant effect on swimming performance of rainbow trout.

Examinations of a New Zealand pulp and paper effluent have demonstrated the potential to influence reproductive physiology (van den Heuvel and Ellis, 2002) and oxygen consumption (Landman et al., 2004) in rainbow trout and secondary sexual characteristics in mosquitofish (Gambusia affinis) (Ellis et al., 2003). However, to date there has been no attempt to determine the effect of the same pulp and paper effluent on swimming performance nor that of exposures combined with hypoxia. Therefore, the aim of this study was to determine how exposures of intermediate duration (4 weeks) to a modern pulp and paper mill effluent, hypoxia, and simultaneous effluent and hypoxia might influence the blood physiology, metabolic rate, and swimming performance of rainbow trout. In contrast to mill effluent experiments, this study also examined the effects of DHAA exposure. The intention here was to determine whether the pattern of response to DHAA, as one of the most prominent effluent constituents, was similar to that to effluent.

Section snippets

Mill effluent and resin acid

Effluent was collected from the Tasman Mill, Kawerau, New Zealand. The mill is an integrated thermomechanical (TMP)/bleached kraft (BK) pulp and paper mill. Mill furnish is primarily softwood (Pinus radiata) with some Eucalyptus spp. pulping. Effluent from the TMP waste stream of the TMP/BK mill is pretreated in a moving-bed bioreactor prior to being combined with the remainder of effluent streams within the mill. Combined effluent is settled in a primary treatment pond, followed by secondary

Water chemistry

Extractives analysis of the TMP/BKME used in experiments 1 and 3 (Table 1) demonstrates the variability that may occur in effluent chemistry from a complex operation such as a pulp and paper mill. A 5-year average resin acid concentration for this effluent was found to be approximately 1000 μg L−1 (van den Heuvel et al., 2004). Thus, effluent used for experiment 3 was very typical when the resin acid concentration was compared to the long-term average. Although effluent used for experiment 1 was

Discussion

The experiments conducted demonstrated that exposure to a modern pulp mill effluent alone at moderate to high concentrations can influence the swimming ability of rainbow trout. This impact could not be measured with resting oxygen consumption as an endpoint. An interactive effect was observed on hematocrit, which shows some potential for cumulative effluent–hypoxia effects on certain blood parameters and the ability to carry oxygen. The overall results suggest that exposure to combinations of

Conclusions

The current study has demonstrated physiological effects in rainbow trout exposed to a wide range of nominal pulp mill effluent concentrations but no substantial effects of DHAA exposure. Although the effect of effluent on swimming performance found in this study was modest, this observation may still be significant as swimming ability in fish is often critical to survival. Despite observable effects at effluent concentrations within the realm of those occurring in the receiving environment,

Acknowledgments

The authors thank Environment Bay of Plenty, Department of Conservation, Norske-Skog/Carter Holt Harvey Tasman Mill, and Carter Holt Harvey Consumer Brands for funding this research. All fish manipulations were done in accordance with the Scion Research Code of Ethical Conduct for the handling of animals and the New Zealand Animal Welfare Act (1999).

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