Investigating the link between pulp mill effluent and endocrine disruption: Attempts to explain the presence of intersex fish in the Wabigoon River, Ontario, Canada

Abstract

The ability of some pulp mill effluents (PME) to act as reproductive and endocrine disrupters in fish is well documented in the literature. However, changes are not always consistent with regard to species, gender, hormones, or reproductive effects. In the present study, the presence of the first intersexed fish that, to our knowledge, has been found in a Canadian river exposed to PME, is reported. A field survey of the Wabigoon River near Dryden, Ontario, in the fall of 2000 found intersexed walleye (Sander vitreus vitreus) with significantly altered hormone levels and reduced gonad size. The Wabigoon River receives discharge from a bleached kraft pulp and paper mill and a municipal wastewater (MWW) plant. It also has historical sediment contamination (wood fiber mats) contributing to extended periods of low dissolved oxygen under low flow, drought conditions. A mesocosm-based partial life cycle test exposing fathead minnows (Pimephales promelas) to reference water, 20% effluent volume to river volume (v/v), 40% (v/v), or 60% (v/v) PME as well as a field survey of the walleye in the Wabigoon River were conducted. The only change in our mesocosm exposure was a decrease in testosterone in males with increasing effluent concentration and vitellogenin induction in males exposed to 60% (v/v) effluent. These results did not reflect the magnitude of endocrine disruption seen in the wild fish survey. Several hypotheses that may explain these discrepancies are proposed. Specifically, evidence is offered from published studies indicating that either hypoxia or MWW, alone or in combination with PME, may explain the discrepancy between our field experiment and the wild fish survey. The present study illustrates the complexities of multistressor receiving environments and the need for the development of cumulative effects assessment approaches.

Phytoestrogens in the environment, I: Occurrence and exposure effects on fathead minnows

“…The present study indicates that genistein, daidzein, and formononetin are attenuated rapidly in the environment, and they are unlikely to cause widespread ecological harm in surface waters, except in the cases of female minnow egg production and larval survival. This points to a need for perhaps more treatment of anthropogenic phytoestrogen sources during critical developmental periods (e.g., larval development) and in locations where high concentrations of phytoestrogens are likely, such as industrial discharges or discharges from municipal wastewater treatment plants that receive waste from particular industries . Furthermore, effluent discharge sites often attract fish because of higher water temperatures and greater nutrient supplies, which may result in fish being exposed continuously to phytoestrogens at higher concentrations than can be expected below the mixing zone.…”

Intersex in the clam Scrobicularia plana (Da Costa): Widespread occurrence in English Channel estuaries and surrounding areas

“…However, the mechanistics of EDC impact in molluscs remains an area where more research effort is required. Besides exposure to STW effluents and generalised estuarine pollution, endocrine disruption in a range of species has been reported to be associated with agriculture (McCoy et al, 2008;Orton and Routledge, 2011); aquaculture (Ford et al, 2007); pharmaceutical manufacture (Sanchez et al, 2011); paper mill effluent (Pollock et al, 2010) and urbanisation (Schultz et al, 2013;Skelly et al, 2010). Given the very broad range of agricultural activities, industry, urbanisation and population density within the catchments bordering the Channel region; the superimposition of natural variables such as rainfall, run-off, hydrodynamic regimes and sediment dynamics; together with the wide range of potential causative chemicals, it is perhaps not surprising that such complex patterns of intersex in S. plana were apparent across the survey area.…”

“…been the case of some marine gastropod molluscs, whereby male characteristics (penis and vas deferens) were superimposed onto females in response to TBT exposure derived from antifouling paints which, in severe cases in some species resulted in sterility and population decline (Barroso et al, 2000;Bauer et al, 1995Bauer et al, , 1997Bryan et al, 1993Bryan et al, , 1986bBryan et al, , 1987Gibbs et al, 1991aGibbs et al, , 1987Gibbs et al, , 1988Gibbs et al, , 1991bOehlmann et al, 1998). The opposite response, feminisation of male individuals, has been most widely reported in freshwater fish exposed to EDCs derived from sewage treatment works and other sources (Hinck et al, 2009;Jobling et al, 1998;McGee et al, 2012;Pollock et al, 2010;Sanchez et al, 2011;Tetreault et al, 2011;Vajda et al, 2011). However, the physical manifestation of intersex (feminization) may take several forms including production of the egg-yolk precursor protein vitellogenin (Arukwe et al, 2000;Harries et al, 1997;Kime et al, 1999;Leonardi et al, 2010;Matozzo et al, 2008;Routledge et al, 1998); formation of female-like ducts (Jobling et al, 2002;Liney et al, 2005;Nolan et al, 2001); and the occurrence of oocytes in testicular tissue (ovotestis) (Bateman et al, 2004;Chesman and Langston, 2006;Langston et al, 2007;Liney et al, 2005;Matthiessen et al, 2002;Nadzialek et al, 2010;Stentiford and Feist, 2005;Stentiford et al, 2003).…”

“…In gonochoristic (dioecious) organisms, intersex is therefore defined as the abnormal condition of being intermediate between male and female sexes. In recent decades the phenomenon of intersex (measured by the manifestations described above) has been used as a biological indicator of the impact of endocrine disrupting chemicals (EDC) in aquatic environments (Bateman et al, 2004;Chesman and Langston, 2006;Ford et al, 2004Ford et al, , 2007Hashimoto et al, 2000;Jobling et al, 2002;Kirby et al, 2004;McGee et al, 2012;Moore and Stevenson, 1991;Nolan et al, 2001;Pollock et al, 2010;Stentiford and Feist, 2005). Arguably however, it is the simply determined endpoints, such as ovotestis or imposex, that are the most valuable and cost-effective to apply within large-scale assessments over a broad geographical area (Gibbs and Bryan, 1996;Gibbs et al, 1991aGibbs et al, , 1987Langston et al, 2007;Oehlmann et al, 1996).…”

Ratio of Mercury Concentration to PCB Concentration Varies with Sex of White Sucker (Catostomus commersonii)

“…As postulated by Madenjian et al [24,42], factors other than the GSI of males, along with the GSI of males, contribute to the relative difference in Hg-elimination rates between the sexes. Endocrine disruptors have been linked to reduced concentrations of androgens in male fish [43], and endocrine disruptors have also been linked to testicular tumors in mammals [44]. Hence, in theory, endocrine disruption could have contributed to the relatively modest difference in the two ratios for the Kewaunee River white suckers.…”