Elsevier

Science of The Total Environment

Volume 431, 1 August 2012, Pages 348-356
Science of The Total Environment

Cumulative impacts of urban runoff and municipal wastewater effluents on wild freshwater mussels (Lasmigona costata)

https://doi.org/10.1016/j.scitotenv.2012.05.061Get rights and content

Abstract

Aquatic biota living in urban watersheds, are chronically exposed to a complex mixture of contaminants from various sources, including municipal wastewater effluents and road runoff. This study examined the general condition, immune function and contaminant load of wild freshwater mussels collected from a large urbanized river over three consecutive field seasons. Four study sites along the Grand River (ON) were selected to represent an incremental contaminant exposure, such that mussels collected from the final downstream site were exposed to the cumulative inputs from 11 municipal wastewater treatment plants and road runoff from four cities. Wild mussels collected downstream of the urban area had significantly lower (p < 0.05) condition factor and did not live as long (significantly reduced mean age) as the mussels collected upstream of the cities. There appears to be a trend of increasing proportions of gravid females at the downstream sites, but whether this trend indicates feminization of the mussel population or is simply an artifact of sampling effort is unclear. An examination of hemocyte phagocytosis revealed a pattern of increasing immune activity at the downstream sites, but only in one of the years sampled. The significant and cumulative increase in Cu, Pb, Zn, Al, Cr, and Ni in the gills of downstream mussels indicates that metals are bioavailable in this ecosystem and that tissue concentrations increase with multiple urban inputs. While the complex nature of the exposure prevents identification of the cause(s) of the observed effects, some contaminants such as ammonia and chloride reach levels known to be toxic to freshwater mussels at the downstream sites. These results indicate that chronic exposure to multiple contaminants negatively impacts mussel health and longevity and corroborates previous assumptions that waterborne contaminants contributed to the decline of the freshwater mussel populations in this watershed.

Highlights

► Wild freshwater mussels were collected from an urbanized river. ► Mussels living downstream of cites had reduced condition factor and mean age. ► Metal concentrations in mussel gills increased with multiple urban inputs. ► Ammonia and chloride at the downstream sites reach levels toxic to mussels. ► Chronic exposure to a complex contaminant mixture negatively impacted mussels.

Introduction

Non-point source contaminants from urban and agricultural runoff as well as specific inputs from industry and municipal treatment plants can negatively impact aquatic ecosystem health. Contaminant induced impairments in wild aquatic animals have been observed across all levels of biological complexity, ranging from sub-cellular alterations in enzymes and proteins (Couillard et al., 1995, Munkittrick et al., 1994, Gillis et al., 2006, Gagné et al., 2011) to ecosystem level impacts of reduced population size and species diversity (Kidd et al., 2007, Collins and Russell, 2008, Brown et al., 2011). Although there are many, one of the key contributors to poor water quality in urban water bodies is the effluent from municipal wastewater treatment plants. Municipal wastewater effluents (MWWE) contain complex mixtures of domestic, municipal and industrial origins (Bennie, 1999, Metcalfe et al., 2003, Servos et al., 2003, Servos et al., 2005, Metcalfe et al., 2010, Holeton et al., 2011). In addition, wastewater treatment plants release organic material which can result in eutrophication and reduced dissolved oxygen levels (Chambers et al., 1997, Cooke, 2006). Impacts of MWWE exposure range from feminization of male fish (Jobling et al., 2002, Tetreault et al., 2011) to impaired immune function in mussels (Blaise et al., 2002). In addition to the inputs from municipal wastewater treatment plants, urban watersheds receive a mixture of chemicals from road runoff. Urban runoff can transport metals (e.g. zinc, lead and copper), road salt, and polycyclic aromatic hydrocarbons (PAH) from roads to nearby water bodies. Negative impacts have been associated with the influx of contaminants from road runoff including alterations in amphibian community structure in chloride impacted roadside ponds (Collins and Russell, 2008) and benthic invertebrate toxicity in metal and PAH impacted sediments in storm-water ponds (Grapentine et al., 2008).

The Grand River in southern Ontario is an example of a river with diverse anthropogenic inputs. While most of the watershed drains agricultural and forested lands, 5% of the land use is urban (Cooke, 2006). In fact, the Grand River watershed receives inputs from 30 municipal treatment plants (Anderson, M. Grand River Conservation Authority, Personal communication, 2011) and runoff from roads connecting a population of nearly 1 million people (GPS Group, 2010). Water quality indices classify the upstream water quality as good but conditions deteriorate downstream as the river flows through urban areas (Cooke, 2006). Long-term water quality data (Ontario Provincial Water Quality Monitoring Network) demonstrate that the levels of numerous contaminants (metals, chloride) and nutrients (phosphorus, nitrate, ammonia) increase moving downstream through the study area (Table 1, Table 2), often reaching levels that exceed Water Quality Guidelines (Cooke, 2006). In addition, dissolved oxygen levels can fall below the (Ontario) Water Quality Guideline in areas downstream of MWWE release points (Cooke, 2006). While recent studies in the Grand River watershed have demonstrated the negative impacts of poor water quality on fish (Tetreault et al., 2011, Brown et al., 2011), the impact on other biota including freshwater mussels remains unknown.

The Grand River watershed has historically supported a diverse and abundant population of freshwater mussels (Metcalfe-Smith et al., 2000). In fact of over 60% of Canadian freshwater mussel species are found there. Although historic records indicate that 34 species have, at one time (records dating to 1885), been found in the watershed (Metcalfe-Smith et al., 2000), recent surveys found that mussel diversity has declined. Specifically, Kidd (1973) found 17 mussel species and Metcalfe-Smith et al. (2000) reported 25 species. Kidd (1973) reported fewer species in the lower reaches of the river (downstream of the cities of Kitchener–Waterloo and Cambridge) and suggested that the decrease in mussel diversity was due to a range of factors including pollution, siltation and the presence of dams that prevented the movement of host fish. Nearly 30 years later, Metcalfe-Smith et al. (2000) found that mussel populations in the lower stretch of the river had begun to recover but stated that ‘the growing pressures of urbanization and agriculture may slow, stop, or even the reverse hard-won gains’. In addition to concerns surrounding negative pressures on freshwater mussels in general, is the unknown impact contaminants have on the nine federally endangered mussel species in this watershed (Department of Fisheries and Oceans, 2010). Indeed nearly 70% of the freshwater mussels species in North America are either endangered, threatened or in decline, and environmental pollution is considered to be one of the contributing factors (Williams et al., 1993, Neves et al., 1997, Strayer et al., 2004, Lydeard et al., 2004). Even though the decrease in mussel diversity in the Grand River watershed correlates to human population growth and the increase in anthropogenic activities in the area, the effect of the urban derived contaminants on mussel health had not been examined.

This study examined wild freshwater mussels chronically exposed to a complex mixture of contaminants in an urban river. Over a period of three field seasons, adult Lasmigona costata were collected from areas both upstream and downstream of a large urban area such that the furthest downstream site was downstream of 11 municipal wastewater treatment plants and a population of nearly 1 million people. Endpoints from various levels of biological organization were examined. Tissue metal concentrations in the mussel's gills were quantified to confirm exposure, and to determine whether the bioavailable contaminant load increases with incremental urban inputs. Since both individual metals (e.g. cadmium, Sheir and Handy, 2010) and municipal effluents (Blaise et al., 2002) have been shown to induce changes in bivalve immune function, hemocyte phagocytosis, one of the key components of the mussel's immune system (Cheng, 1981), was assessed to determine if the complex exposure affects immune defenses. In addition, as the cumulative effects of chronic contaminant exposure can eventually become evident and cause impairment at the whole organism level, condition factor, gonadal somatic index, mussel age, and reproductive status were assessed in the chronically exposed mussels.

Section snippets

Study area

The Grand River watershed covers an area of 6965 km² in southern Ontario, Canada. Four study sites were selected, spanning approximately 50 km of the river, and both rural and urban areas (Fig. 1, Table 3). The furthest upstream site at West Mountrose (Site 1) is referred to as the upstream or reference site because it is located upstream of the twin cities of Kitchener–Waterloo, although there are actually two small tertiary municipal wastewater treatment plants upstream of this site (Fig. 1).

Mussel collections

Although this study did not aim to quantify the size of the L. costata population at the study sites, it should be noted that the time taken to reach the quota of 25 adult mussels was noticeably longer at the furthest downstream site compared to all other sites. It took approximately 8 h to collect 25 mussels at Site 1, whereas 20 h was required at Site 4. Sites 2 and 3 required 10 and 12 h for the collection, respectively.

Age and condition factor

The results for the combined multi-year data sets for mussel age and

Mussel collections

While this study did not quantify the four mussel populations sampled, the large (> 2 fold) difference in the length of time required to collect the targeted number of adult mussels at the different sites was striking and suggests that the population of L. costata at Site 4 was smaller than the upstream population (Site 1). While this collection information is somewhat anecdotal, it could be considered as evidence of a population level impact in wild mussels downstream of urban areas. Goudreau

Conclusions

Wild freshwater mussels living downstream of a large urban area had lower condition factor, showed some evidence of stimulated immune response and did not live as long as mussels collected upstream of the cities. In addition, the incremental increase in metals in the mussel's gills indicates that metals are bioavailable and increase with multiple urban inputs. Although water quality at the downstream site is impaired, and the levels of at least two contaminants (ammonia and chloride) reach

Acknowledgments

The author would like to thank R McInnis, T Hooey, S Higgins, S Craig, S Turner, E Choy, A Machado, L Nogueira, and M Jorge for their contributions to laboratory and field components of this project, A Bartlett for instrument time, as well as many (C Blaise, F Gagne, S Trottier, M Douville and S Trepanier) at Environment Canada's Center St. Lawrence for providing guidance on the hemocyte assays. This project was funded by Environment Canada.

References (57)

  • J.L. Metcalfe-Smith et al.

    Changes in the biodiversity of freshwater mussels in the Canadian waters of the lower Great Lakes drainage basin over 10 the past 140 years

    J Great Lakes Res

    (1998)
  • M.R. Servos et al.

    Distribution of estrogens, 17 beta-estradiol and estrone, in Canadian municipal wastewater treatment plants

    Sci Total Environ

    (2005)
  • G.R. Tetreault et al.

    Intersex and reproductive impairment of wild fish exposed to multiple municipal wastewater discharges

    Aquat Toxicol

    (2011)
  • T. Augspurger et al.

    Water quality guidance for the protection of freshwater mussels (Unionidae) from ammonia exposure

    Environ Toxicol Chem

    (2003)
  • D. Bennie

    Review of the environmental occurrence of alkylphenols and alkylphenol ethoxylates

    Water Qual Res J Can

    (1999)
  • C. Blaise et al.

    Immunocompetence of bivalve hemocytes as evaluated by a minituarized phagocytosis assay

    Environ Toxicol

    (2002)
  • U. Borgmann et al.

    Relationship between chronic toxicity and bioaccumulation of cadmium in Hyalella azteca

    Can J Fish Aquat Sci

    (1991)
  • P.A. Chambers et al.

    Impacts of municipal wastewater effluents on Canadian waters: a review

    Water Qual Res J Can

    (1997)
  • T.C. Cheng

    Bivalves

  • H.A. Clarke

    The Tribe Alasmidontini (Unionidae; Anodontinae), Part II: Lasmigona and Simpsonaias

    Smithson Contrib Zool

    (1985)
  • S.J. Collins et al.

    Toxicity of road salt to Nova Scotia amphibians

    Environ Pollut

    (2008)
  • Committee on the Status of Endangered Wildlife in Canada

    Canadian species at risk

    Available at Committee on the Status of Endangered Wildlife in Canada

    (2007)
  • S. Cooke

    Water quality in the Grand River: a summary of current conditions (2000–2004) and long term trends

  • Y. Couillard et al.

    Field transplantation of a freshwater bivalve, Pyganodon grandis, across a metal contamination gradient. II. Metallothionein response to Cd and Zn exposure, evidence for cytotoxicity, and links to effects at higher levels of biological organization

    Can J Fish Aquat Sci

    (1995)
  • M.-N. Croteau et al.

    Trophic transfer of metals along freshwater food webs: evidence of Cd biomagnification in nature

    Limno Oceanogr

    (2005)
  • Department of Fisheries and Oceans

    Distribution maps for mussel and fish species at risk

  • J. Dumas et al.

    The internal distribution of nickel and thallium in two freshwater invertebrates and its relevance to trophic transfer

    Environ Sci Tech

    (2008)
  • W.J. Fleming et al.

    Freshwater mussel die-off attributed to anticholinesterase poisoning

    Environ Toxicol Chem

    (1995)
  • Cited by (54)

    View all citing articles on Scopus
    View full text