Lake Trout Ecosystems in a Changing Environment - Chapter 9 ppsx

Kidd Department of Fisheries and Oceans, Freshwater Institute Contents Introduction Mercury concentrations in lake trout populations in small Boreal lakes Factors affecting mercury conce

chapter nine

Mercury contamination

of lake trout ecosystems

R.A (Drew) Bodaly

Department of Fisheries and Oceans, Freshwater Institute

Karen A Kidd

Department of Fisheries and Oceans, Freshwater Institute

Contents

Introduction

Mercury concentrations in lake trout populations in small Boreal lakes

Factors affecting mercury concentrations in lake trout

Management of mercury exposure from consumption of lake trout

Effects of mercury on fish

Possible future trends

Summary

References

Introduction

Mercury is a widespread contaminant in freshwater fish and is currently causing great concern because of its potential impact on the health of humans and wildlife Most mercury (Hg) in fish flesh is present as methyl mercury (MeHg) (Bloom, 1992) This organic form

of mercury is a powerful neurotoxin and in large doses causes motor, sensory, and devel-opmental problems in humans and other vertebrate animals (Clarkson, 1992) Because of the concerns over human health impacts, Canadian provincial and federal agencies mon-itor Hg concentrations in fish from lakes with important fisheries and in commercial shipments If total Hg (both methyl mercury and inorganic Hg) concentrations exceed the

commercial sales are restricted Though high concentrations of persistent pesticides have occasionally been the cause, mercury is by far the most common reason for fish consump-tion advisories in North American freshwaters (e.g., Quebec Ministère de l’Environnement

et de la Faune, 1995; United States Environmental Protection Agency, 1998; Ontario Min-istry of the Environment, 2003) For example, in Ontario 95% of fish consumption

advisories in lakes were related to mercury, and consumption advisories for this contam-inant applied to 1206 of the 1595 lakes tested (Ontario Ministry of the Environment, 2003)

In the United States in 1997 mercury accounted for 78% of the fish consumption advisories

in freshwaters (United States Environmental Protection Agency, 1998) Present-day expo-sure of humans to MeHg results almost wholly from the consumption of fish (Clarkson, 1992)

Lake trout (Salvelinus namaycush) frequently have high concentrations of mercury

because of their position at the top of food chains and because the Boreal lakes that they inhabit often have conditions favorable for mercury bioaccumulation As a result, most lake trout populations in Boreal lakes have fish consumption advisories In this chapter

we review current knowledge concerning Hg in lake trout populations in the southern Shield lakes of Ontario, Quebec, Minnesota, and New York

Factors affecting Hg in freshwater fish are outlined, with discussion of the reasons why lake trout are frequently highly contaminated with Hg Emphasis is on lakes that do not receive direct anthropogenic discharges of Hg but rather receive their Hg from atmo-spheric sources and local weathering of the earth’s crust Examples of Hg in lake trout populations are given, especially to demonstrate how Hg varies with size and trophic position of the fish and with the food-web structure of the lake Approaches to managing mercury contamination in freshwater systems are outlined, including sampling needed to determine existing levels and advisory systems to advise the public of recommended consumption limits Finally, some speculation is made about future trends of Hg in lake trout populations

Mercury concentrations in lake trout populations in small Boreal lakes

Mercury concentrations in lake trout in Boreal lakes are frequently high, and most popu-lations of lake trout have at least some fish with Hg concentrations greater than the

(excluding the Great Lakes) contain lake trout with Hg concentrations greater than the Canadian limit, and therefore consumption advisories exist for this species (Ontario Min-istry of the Environment, 2003) In Quebec, 80 of 105 lake trout populations (76%) that have been sampled had consumption advisories (Quebec Ministère de l’Environnement

et de la Faune, 1995) Braune et al (1999) noted that mercury in lake trout from northern Canadian lakes usually exceeds consumption guidelines Fish consumption advisories exist for lake trout in all regions that have been sampled, demonstrating that mercury is

a widespread problem for this species and its consumers

Large differences in Hg concentrations are observed in fish from lakes in close prox-imity to one another Within a region, mean Hg concentrations in predatory fish vary fivefold or more, even after standardization of these data for fish size and/or age For example, in northern Quebec lakes standardized concentrations of Hg varied about five-fold in lake trout (Schetagne and Verdon, 1999), and predatory fish in six lakes in north-western Ontario varied three- to fourfold (Bodaly et al., 1993) Similarly, mean Hg (stan-dardized for fish size) in lake trout in almost 100 lakes from all regions of Ontario varied

Haines (1997) also found mean Hg concentrations in lake trout from 120 randomly chosen

dem-onstrate that Hg concentrations in lake trout populations can vary considerably within a limited geographic area

Despite the high variability in lake trout Hg concentrations within regions, some geographic trends remain evident In southern Ontario, 74% of lakes have Hg in lake trout

only 58% of lakes have Hg in lake trout greater than 0.5 µg g and only 8% have Hg in

to Ontario, mercury concentrations in lake trout from Quebec are lower in southern regions (Outaouais and Fleuve Saint-Laurent: 26 of 46 populations tested with recommended consumption limits less than four meals per month) than in the more remote northern areas (Lac Saint-Jean and Gaspésie–Côte-Nord: 22 of 26 lake trout populations with restricted consumption; La Grande Rivière and Grande Rivière de la Baleine: 32 of 33 populations; excluding reservoirs) (Quebec Ministère de l’Environnement et de la Faune, 1995) The underlying causes of these trends are not yet understood but may be related

to differences in geologic or atmospheric sources of Hg

Factors affecting mercury concentrations in lake trout

With the exception of lakes that have received direct discharges of Hg (e.g., the English-Wabigoon river system in northwestern Ontario; Parks and Hamilton, 1987), most Hg entering freshwater systems today is probably atmospheric in origin This mercury orig-inates from natural sources (such as geologic weathering, volcanic eruptions, and ocean degassing) and from anthropogenic sources (such as burning of coal, oil, and municipal wastes and industrial processes) Atmospheric concentrations of mercury in the northern hemisphere have increased since industrial times, and between one-half and three-fourths

of the Hg in the atmosphere is anthropogenic in origin (Swain et al., 1992) This atmo-spherically derived Hg is mainly in inorganic forms and enters lakes directly and indirectly via watershed runoff Atmospheric deposition of Hg to temperate and Arctic lakes is now

atmospheric deposition rates have caused increases in concentrations of Hg in freshwater fish, including lake trout, is unclear but some evidence suggests this (Kelly et al., 1975; Johnson, 1987; Swain and Helwig, 1989; Rolfhus and Fitzgerald, 1995)

Climate and rates of atmospheric deposition of Hg to lakes and their watersheds are similar within a given region and therefore cannot explain lake-to-lake differences in Hg concentrations in fish The high variability in mercury levels in lake trout populations within regions must therefore be related to the physical, chemical, and biological charac-teristics of lakes and their watersheds The lake-specific characcharac-teristics that are believed

to affect Hg concentrations in freshwater fish include the rate of supply of inorganic Hg and methyl mercury to lakes and their watersheds, the trophic position and growth rates

of different fish species, and the physical and chemical characteristics of lakes and their watersheds The relatively high concentrations of Hg in lake trout in Boreal lakes are probably mainly the result of the trophic position of lake trout in freshwater systems, the relatively large size and age of many individual lake trout, and the chemical conditions

of Boreal lakes that tend to promote high Hg concentrations in fish

Almost all of the Hg in fish muscle is MeHg (Bloom, 1992; Lasorsa and Allen-Gil, 1995; Hammerschmidt et al., 1999), and this is the form of mercury that is accumulated

in aquatic food webs Lakes and their biota receive MeHg from three sources: precipitation, runoff from the surrounding watershed, and in-lake methylation of inorganic mercury (Rudd, 1995) Inputs of MeHg from precipitation are not sufficient to account for Hg in fish in the Boreal lakes of North America, and in-lake production of MeHg by methylation

of inorganic mercury is thought to be a significant source of mercury to food chains and fish (Rudd, 1995)

MeHg production and its bioavailability are affected by chemical factors, and many

of the conditions known to favor Hg methylation are observed in the Boreal lakes that support lake trout populations For example, low pH and high dissolved organic carbon (DOC) concentrations are common in Boreal lakes, and these factors tend to be associated

with high Hg in fish in lakes (McMurtry et al., 1989; Wiener et al., 1990; Driscoll et al., 1994) The significant relationship between DOC and Hg in fish may be, at least in part,

a result of the inputs of DOC-associated MeHg from wetlands in a lake’s catchment (St Louis et al., 1994)

The physical characteristics of lakes also affect Hg bioaccumulation in lake trout and other fish species A study of six lakes in the Canadian Shield in northwestern Ontario that varied in their surface area from 89 to 35,000 ha but were similar in other chemical and physical characteristics revealed that lake size exerted a strong influence on Hg concentrations in fish (Bodaly et al., 1993) Concentrations of mercury in yearling yellow

smallest lake that was studied and decreased in a regular pattern with lake size (Figure 9.1) These differences in mercury concentrations between the smaller and larger study lakes were also seen in predatory and planktivorous species The methylation of mercury by microorganisms is a temperature-dependent process The cooler epilimnetic temperatures

in large lakes decrease mercury methylation rates and subsequent inputs of mercury to the food web (Figure 9.1) (Bodaly et al., 1993) In contrast, McMurtry et al (1989) observed that Hg in lake trout was positively related to lake area in a study where the ratio of catchment to lake area was not kept constant as in Bodaly et al (1993) Lakes with pro-portionately larger catchment areas will have greater inputs of mercury from drainage basin runoff and, most likely, higher mercury concentrations in the fish from these systems Other studies have demonstrated that the watershed size in relation to the lake size is important in determining Hg concentrations in fish in Boreal lakes (Suns and Hitchin, 1990; Evans, 1986)

Fish obtain most of their mercury from their food and only a small proportion directly from the water via uptake across the gills (Hall et al., 1997; Rodgers, 1994; Harris and Snodgrass, 1993) Therefore, Hg in fish is influenced strongly by Hg concentrations in

Figure 9.1 Mean mercury concentrations in axial muscle of yearling yellow perch from six lakes in northwestern Ontario Vertical bars are mercury concentrations (with 95% confidence intervals and number of fish), and points are mean epilimnetic water temperatures (June–August, 1986–1989) Lakes are arranged in order of smallest (Green, 89 ha) to largest (Trout, 35,000 ha) From Bodaly

et al., 1993, Canadian Journal of Fisheries and Aquatic Sciences 50: 980–987

their diet (Borgmann and Whittle, 1992; Harris and Snodgrass, 1993; Harris and Bodaly, 1998) Top predators such as lake trout contain the highest concentrations of mercury in part because they tend to feed on prey with high mercury concentrations The MeHg they are accumulating is successively concentrated from the base of the food web because it is much more efficiently absorbed and accumulated (Mason et al., 1996) and excreted more slowly (Trudel and Rasmussen, 1997) by organisms than the inorganic forms of Hg Concentrations of MeHg increase from prey to predator, and high-trophic-level organisms tend to have the greatest concentrations of mercury in their tissues (Kidd et al., 1995; Cabana et al., 1994) As an example, in Lake Michigan mean dry weight concentrations

of MeHg increase through the pelagic food web from 0.01 in zooplankton to 0.21 in the

increases are seen in Boreal lake food chains

In recent studies of mercury accumulation through food webs, the trophic position of fish and invertebrates has been characterized using tissue ratios of stable nitrogen isotopes

consumers, from primary consumers to secondary consumers, and so on up through the food web by an average of 3 to 5 parts per thousand (per mil; Peterson and Fry, 1989) This enrichment in the heavy isotope provides a continuous relative measure of an organism’s trophic positioning within the food web and also reflects dietary habits over a period of months to years (Hesslein et al., 1993) Kidd et al (1995) used stable nitrogen isotope ratios

in fish muscle to quantify the trophic transfer of mercury through several food webs in northwestern Ontario They found a highly significant relationship between muscle con-centrations of Hg and the trophic position of fish (as quantified by stable nitrogen isotope

for mercury and other persistent pollutants in other freshwater and marine food webs

from the differences in the slope of this relationship that the accumulation of Hg through food webs varies considerably from lake to lake; such variation may be related to varying efficiencies of carbon transfer in these systems

The length of the underlying food chain also significantly affects the concentration of

Hg in top predators such as lake trout Such effects were unequivocally demonstrated by Cabana et al (1994) and Cabana and Rasmussen (1994) They categorized temperate lakes into three classes based on the length of the pelagic food chain leading up to the top predator lake trout using the presence or absence of important prey species: Class 1 lakes had the shortest food chains with no mysids (a zooplanktivorous crustacean) or pelagic prey fishes

(rainbow smelt [Osmerus mordax], lake cisco [Coregonus artedi], lake whitefish [Coregonus

clupeaformis], alewife [Alosa pseudoharengus], and others); Class 2 lakes had an intermediate

food chain length because of the presence of pelagic prey fishes; Class 3 lakes had the longest food chains because of the presence of both pelagic prey fishes and mysids They found that the concentrations of mercury in lake trout increased 3.6-fold from the Class 1

to Class 3 lakes and were significantly related to the stable nitrogen isotope ratios in this species It is likely that manipulations (both intended and accidental) of freshwater food webs will influence the concentrations of Hg in top predators Vander Zanden and Ras-mussen (1996) observed that Hg concentrations in lake trout were considerably higher in lakes that had introduced populations of smelt They hypothesized that this was the result

of increased food chain lengths in the systems that had introductions of this exotic species Concentrations of Hg in fish are also affected by the amount of its diet that it uses for growth relative to metabolism The MeHg present in a fish’s diet is efficiently absorbed and retained in its tissues; the excretion rates of MeHg are slow compared to that of Hg and are slower in older than in younger fish (Trudel and Rasmussen, 1997) Young, immature fish use a large proportion of their dietary carbon intake for growth and

generally have low Hg concentrations in their tissues This is often termed growth dilution, and although the MeHg is not “diluted,” it results in concentrations in fast-growing, immature predators that can be similar to that of their prey Larger, mature fish tend to

be slow growing, and these fish use most of their ingested carbon for metabolism and reproduction (not growth) while retaining most of the ingested mercury These fish there-fore tend to have higher concentrations of this contaminant (Harris and Snodgrass, 1993; Rodgers, 1994; Harris and Bodaly, 1998), although Stafford and Haines (2001) did not find

a relationship between growth rate and mercury in a lake trout population As predatory fish grow, they tend to eat larger prey items with higher concentrations of contaminants,

between Hg concentrations and fish size is commonly seen in temperate and Boreal lakes (e.g., Wiener et al., 1990)

Management of mercury exposure from consumption of lake trout

The primary objective of provincial and federal agencies in Canada for managing mercury

in lake trout populations is to reduce health risks to humans Fish are collected from lakes,

Figure 9.2 Relations between total mercury (µg.g wet weight) and standardized δ N (per mil) of fish muscle from seven species from the Northwestern Ontario Lake Size Series (Kidd et al., 1995,

Water, Air, and Soil Pollution 80: 1011–1015.) [The δ15N of the obligate benthivore, white sucker, generally increased with decreasing lake size, likely as a result of differences in in-lake cycling or sources of nitrogen For this reason, δ15N of all fish were standardized to the mean δ15N of white sucker using the following formula: δ15Nfish − δ15Nwhite sucker + 6.8 (to account for the fact that suckers are secondary consumers and that δ15N increases an average of 3.4 per mil with each trophic level)]

and the concentrations of mercury in axial muscle from individual fish are determined Muscle tissue is typically analyzed for mercury because it is the main tissue consumed

by people The relation between mercury concentrations and fish size is then determined, and mercury concentrations are presented in relation to fish size in terms of the recom-mended human consumption limit for each species sampled (Ontario Ministry of the Environment, 1997; Quebec Ministère de l’Environnement et de la Faune, 1995) Advice

on the sizes of fish fit for consumption is delivered to the public through booklets for anglers and signs posted on lake shores, and through the dissemination of information to communities In aboriginal communities, fish are often an important and significant part

of the diet For this reason advice on the species, sizes, and quantities of fish that are safe

to eat is based on consumption information specific to these communities (Health and Welfare Canada, 1984)

Safe consumption limits are based on recommendations from Health and Welfare

Health and Welfare Canada, 1984) Health Canada is currently recommending that Hg

weight/day

Sampling lakes to determine Hg concentrations in fish and its risk to human consum-ers is relatively straightforward From each lake, at least 20 fish of each species likely to

be caught and consumed by people should be obtained Ideally, this sample should include

a wide range of fish lengths and weights to ensure that analyses are conducted on all sizes

of fish likely to be consumed This eliminates the need for extrapolation of mercury concentrations to fish sizes not sampled and ensures a statistically reliable relationship between Hg and fish size for each species To compare the concentrations of Hg in fishes across lakes, statistical methods are generally used to standardize Hg for differences in size and age Several techniques have been used including regressions and transforma-tions, alternative techniques such as multivariate analysis of univariate and bivariate statistics (Somers and Jackson, 1993), or polynomial regressions with indicator variables (Tremblay et al., 1998) As noted above, this information is often used by governmental agencies to advise sport fishers of recommended fish consumption limits for various water bodies (e.g., Ontario Ministry of the Environment, 1997)

Figure 9.3 Relationship between Hg concentrations and fish length in lake trout from three lakes in

northwestern Ontario Data from Fudge et al., 1994 Canadian Data Report of Fisheries and Aquatic

Sciences 921.

Effects of mercury on fish

Although the main emphasis of research and management of mercury in freshwater fish populations has been placed on the human health implications, high MeHg concentrations may be affecting the fish themselves There has been little research to date on the effects

of Hg on fish at environmentally realistic concentrations or on possible effects on fish-eating wildlife (Wiener and Spry, 1996) However, there is some evidence that MeHg may impair reproduction in freshwater predators For example, Friedmann et al (1996) found

walleyes affected their growth and gonadal development Latif et al (2001) examined the effect of MeHg in water, also at realistic concentrations, on walleye egg development and found significant reductions in egg survival at higher MeHg concentrations Also, fathead minnows consuming food with elevated MeHg concentrations were found to show reduced spawning success (Hammerschmidt et al., 2002) The toxicologic significance of MeHg to fish is an important area for future research

Possible future trends

Future trends in Hg levels in freshwater fish generally and lake trout specifically are difficult to forecast because many factors influence Hg concentrations in these organisms There is some recent evidence that rates of atmospheric deposition of Hg in the northern hemisphere have recently begun to decrease (Engstrom and Swain, 1996) Some studies suggest that mercury concentrations in fish are related to rates of atmospheric deposition (Kelly et al., 1975; Swain and Helwig, 1989; Rolfhus and Fitzgerald, 1995) For this reason, reductions in atmospheric transport and deposition of Hg may lead to general decreases

of this contaminant in lake trout populations

Climate warming may have significant effects on Hg concentrations in fish in Boreal lakes by affecting rates of mercury methylation and the supply of MeHg to food chains

As noted above, Bodaly et al (1993) found significant relationships between epilimnetic temperatures and Hg in fish in Boreal lakes Climate warming may produce warmer and/or deeper epilimnia in the Boreal zone Because mercury methylation probably takes place mainly in epilimnetic sediments and is known to be temperature dependent, climatic warming could increase rates of methylation On the other hand, lower inputs of DOC to Boreal lakes with decreased precipitation and runoff (Schindler and Gunn, this volume) could in turn reduce the supply of MeHg to lakes from their watersheds

The acidification of lakes by atmospheric deposition of pollutants may be increasing

Hg concentrations in lake trout in small Boreal lakes Experimental lake acidification was observed to increase Hg in fish (Wiener et al., 1990) and Hg in fish in lakes has often been observed to be negatively related to pH (e.g., McMurtry et al., 1989) Also, Hg methylation

is stimulated by sulfate addition (Gilmour et al., 1992), and atmospheric sulfate deposition

declined substantially in recent years, with an approximate 40% decline in total North America emissions since 1980 (Jeffries et al., 2003)

The recent introduction and the spread of rainbow smelt into freshwater systems may also increase Hg concentrations in lake trout (Franzin et al., 1994; Cabana and Rasmussen, 1994; Futter, 1994) Because the presence of smelt is believed to increase the length of the food chain, lake trout from lakes with smelt tend to have higher Hg when compared to the same species from lakes without smelt (Vander Zanden and Rasmussen, 1996; Akielaszak and Haines, 1981)

Intensive fishing tends to decrease Hg in freshwater fish, at least temporarily (Verta, 1990) Exploitation will tend to decrease fish densities, increase growth rates, and decrease the mean age of the population, all of which will tend to decrease Hg in lake trout populations Therefore, the presence of sport and commercial and subsistence fisheries on lake trout lakes may reduce Hg concentrations, at least on a size-adjusted basis

Summary

Mercury is present in all freshwater fish Lake trout, because of their piscivorous nature, are particularly susceptible to accumulating high concentrations of this contaminant Most lake trout populations surveyed have mean concentrations of mercury greater than the

of variation among lakes even within a given region Mercury enters freshwater systems primarily from atmospheric deposition and is converted to MeHg, the form that is effi-ciently bioaccumulated through food webs Factors affecting mercury concentrations in lake trout include the length of the food chain, the size and age of individual fish, and physical and chemical characteristics of lakes and their watersheds It is difficult to predict future contaminant trends in predatory fish, including lake trout, in Boreal lakes Declines

in atmospheric deposition, increased fishing pressure, and a reduced supply of DOC to lakes from their watersheds may reduce mercury concentrations in lake trout On the other hand, the spread of rainbow smelt populations into lakes and climate warming might increase the concentrations of mercury in lake trout and the risk to humans and fish-eating wildlife At present, it is not possible to predict how these opposing factors will affect the concentrations of a widespread contaminant in freshwater fish

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