Spatial Distribution of Mercury and Organochlorine Contaminants in Great Lakes Sea Lamprey (Petromyzon marinus)

J. Great Lakes Res. 26(1):112–119 Internat. Assoc. Great Lakes Res., 2000

Spatial Distribution of Mercury and Organochlorine Contaminants in Great Lakes Sea Lamprey (Petromyzon marinus) D. Cameron MacEachen*, Ronald W. Russell, and D. Michael Whittle Great Lakes Laboratory for Fisheries and Aquatic Sciences Department of Fisheries and Oceans 867 Lakeshore Road Burlington, Ontario L7R 4A6 ABSTRACT. Adult sea lamprey (Petromyzon marinus) were collected during their spawning migration in streams entering each of the Great Lakes, except Lake Michigan. Skinless muscle tissue samples were analyzed for a range of organochlorine contaminants including p,p′-DDE, total PCB, toxaphene, and mercury. Concentrations of p,p′-DDE and PCBs were above the detection limit of 0.002 µg/g in all samples. Levels of total toxaphene in some individuals from Lake Superior were above recent Health Canada consumption advisory limits of 0.2 µg/g for fish. PCBs and ΣDDT concentrations in some lamprey tissue samples from the Lake Ontario basin exceeded limits for unrestricted human consumption. Mercury concentrations were highest in lamprey from the Lake Superior basin. Mercury levels were above the 0.5 µg/g Canada Health Protection Guideline for consumption in 75% of all the lamprey muscle tissue samples analyzed. Comparison of organic contaminant levels for lamprey muscle tissue samples and whole lake trout (Salvelinus namaycush) collected from the same lakes showed patterns of contaminant accumulation that were similar within each lake for both species. Mercury concentrations were up to 10 times higher in lamprey muscle tissue samples than whole lake trout sampled from the same lake. Lamprey display a differential ability to accumulate mercury versus organochlorines. By understanding these relationships for different classes of contaminants, it may be possible to utilize lamprey as a future alternate to lake trout as an indicator species to track spatial and temporal contaminant trends in the Great Lakes. INDEX WORDS:

Sea lamprey, PCB, toxaphene, DDE, mercury, bioaccumulation.

INTRODUCTION The expanding interest in both the domestic consumption and European export of sea lamprey (Petromyzon marinus) from the Great Lakes basin prompted initiation of a study to determine contaminant burdens in this segment of the aquatic ecosystem. A combination of decreased catches of lamprey and increased market prices in Portugal has led to investigations into the feasibility of Great Lakes sea lamprey importation and the development of marketability studies (Sales 1996a). Sea lamprey are parasitic organisms that feed on blood and tissues of specific fish species, such as salmonids, that may themselves be significantly

contaminated with environmental pollutants. The range and level of contamination of fish from the Great Lakes has been well established. The majority of these studies to date have focused on the top predatory fish species (Baumann and Whittle 1988, Borgmann and Whittle 1991, DeVault et al. 1996, Huestis et al. 1996). A few studies have described the contaminant levels in adult sea lamprey (Kaiser and Valdmanis 1978, Kaiser 1982). Renaud et al. (1995a, 1995b) analyzed fresh and preserved ammocoetes (larval lamprey) from the St. Lawrence River region for organochlorine pesticides (OCs) and total PCBs. Holmes and Youson (1996), and Renaud et al. (1998) have analyzed ammocoetes for trace metal concentrations. Considering that lamprey selectively parasitize the largest lake trout available (Swink 1991, Schneider et al. 1996) and

*Corresponding author. E-mail: [email protected]

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TABLE 1. Summary data (mean ± S.E.) for sea lamprey and silver lamprey muscle tissue samples. All contaminant data expressed as µg/g wet weight

N Length (mm) Weight (g) % Lipid Mercury Toxaphene p,p′-DDE Total PCB

Lake Ontario 19 434.6 (11.2) 181.6 (14.5) 5.0 (0.7) 1.35 (0.19) 0.15 (0.02) 0.36 (0.05) 1.30 (0.11)

Lake Erie 6 487.5 (14.1) 250.0 (30.1) 6.2 (1.4) 0.43 (0.15) 0.22 (0.12) 0.11 (0.05) 0.68 (0.06)

Sea Lamprey Lake Huron 16 433.8 (15.2) 182.3 (16.7) 4.6 (0.7) 0.79 (0.25) 0.30 (0.04) 0.15 (0.02) 0.53 (0.07)

that concentrations of PCBs, p,p′-DDE, and mercury increase with lake trout size and age (Niimi 1981, Borgmann and Whittle 1992, Huestis et al. 1996), lamprey have a great potential to bioaccumulate and biomagnify the many contaminants which have been detected in the Great Lakes ecosystem (International Joint Commission 1989). MATERIALS AND METHODS Fifty seven adult spawning-phase sea lamprey were captured during their spawning migration in rivers and streams flowing into Lakes Ontario, Erie, Huron, and Superior during May and June, 1997. Additionally, three native silver lamprey (Ichthyomyzon unicuspis) were collected from the open waters of the western basin of Lake Erie near Middle Sister Island (41°51′ N,82°91′ W). Lamprey were frozen immediately following collection and stored at –20°C until processing. In the laboratory, measurements of total length and weight were recorded (Table 1). Heads were removed and the individual lamprey were skinned, gutted, and the remaining muscle tissue was homogenized using a Hobart® meat grinder. Processing equipment and associated glassware were washed with distilled water and rinsed with distilled in glass (DIG) pesticide-grade hexane and acetone (Caledon Laboratories Georgetown, ON) prior to use. All tissue homogenates were placed in acetone and hexanerinsed flint glass jars and stored at –20°C for less than 6 weeks prior to analysis. Subsamples were retained for organic contaminant analysis, lipid content and mercury analysis. The collection protocol and analysis procedure for the lake trout values presented are described in Borgmann and Whittle (1991).

Lake Superior 16 435.3 (9.1) 194.2 (12.1) 5.2 (0.5) 2.28 (0.57) 1.22 (0.16) 0.06 (0.02) 0.32 (0.05)

Silver Lamprey Lake Erie 3 210.8 (7.9) 87.6 (9.1) 7.8 (0.3) NA NA 0.05 (0.02) 0.82 (0.15)

Sample Extraction and Cleanup Thawed lamprey tissue homogenates were mixed thoroughly prior to subsampling to recombine the tissues into a homogeneous mixture. Approximately 5 grams of sample was combined with 150 g of Na 2 SO 4 in a glass mortar and ground manually until homogeneity was achieved. This mixture was then transferred to a glass extraction column and eluted with 300 mL of dichloromethane (DCM). Bulk lipid removal was achieved via automated gel permeation chromatography. Further cleanup and separation were achieved using 3% deactivated silica gel columns. Samples were applied and the columns were eluted with 50 mL 1% DCM in hexane (Fraction A) followed by 70 mL DCM (Fraction B). Fraction A contains PCBs and p,p′DDE while Fraction B contains toxaphene. For mercury analysis, 1 gram of lamprey tissue was weighed out into a volumetric flask. The tissue was then dissolved in 15 mL of sulphuric acid. Organic and inorganic mercury compounds, if present, were decomposed using nitric acid, potassium permanganate, and potassium persulphate. Mercuric ions were reduced to the elemental state with stannous chloride. Instrumentation Organochlorine analyses were performed using a Varian 3600 gas chromatograph (GC) with dual electron capture detectors (ECD). Analysis of p,p′DDE required dual channel confirmation and an RTx-5 60 m × .25 mm × .25 mm column was used with an RTx-1701 60 m × .25 mm × .25 mm as the confirmation column. Samples were processed in batches of approximately 15 including OC, PCB, and toxaphene

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method spikes, duplicates, blanks, and reference materials. A description of the reference materials used is presented in Sergeant and Bolt (1997). All tissue samples and reference materials were spiked with a surrogate consisting of 2,4,5,6 tetrachloro-mxylene and decachlorobiphenyl (Supelco). Recoveries of the internally spiked standard ranged from 80% to 117% with a mean of 96%. Organochlorine compounds were quantified against an eight-point calibration curve, final results were corrected for recoveries and no blank corrections were performed. Total PCBs were quantified using a standard containing a 1:1:1 mixture of Aroclors 1242, 1254, and 1260 at a concentration of 500 pg/µL. Total toxaphene was quantified against a 500 pg/µL technical standard from Hercules Chemical. Twenty target peaks from the chromatogram were used in quantification. A detailed description of the extraction process and analytical method for total PCBs and OCs is presented in Huestis et al. (1995). The extraction, analysis, and quality assurance procedures for mercury are described in Environment Canada (1994). Briefly, for the determination of mercury concentrations, mercury vapor was removed from solution by aeration and total mercury was determined via cold vapor, flameless atomic absorption using a LDC Milton-Roy elemental mercury monitor. Quality assurance of the data incorporated the use of blanks, spikes, duplicates, and the National Research Council reference material DORM-1. The detection limit for total mercury is 0.01 mg/kg. Data Analysis All chemical data are expressed on a µg/g wet weight basis. Chemical concentration data used in analysis of variance were logarithmically transformed to control heteroscedasticity. A one-way multivariate analysis of variance (MANOVA) was selected as a statistical technique due to the multivariate nature of the data. The MANOVA was performed on the logarithmically transformed wet weight concentrations to determine inter-lake differences in organic contaminant concentrations in lamprey. Differences between cell means were tested by a Fisher’s Least Significant Difference (LSD) procedure (Wilkinson 1990). As mercury data were determined from a subset of the total number of samples collected, they were analyzed by a separate one-way analysis of variance (ANOVA) followed by a Fisher’s LSD test. Due to the small sample size, a Kruskal-Wallis non-para-

metric procedure was employed in lieu of ANOVA to compare differences in chemical accumulation in sea and silver lamprey collected from Lake Erie and it’s tributaries. RESULTS AND DISCUSSION As sea lamprey are highly mobile (Smith and Elliott 1953, Moore et al. 1974) and can travel large distances when attached to hosts, boats, or are free swimming (Dodge 1963), the site of capture does not necessarily represent the region in which contaminants were accumulated by the lamprey while feeding on their hosts. Therefore, lamprey integrate contaminant conditions throughout the lake in which they were captured. Additionally, sea lamprey select spawning streams based on several physical parameters and unlike salmonids do not solely rely on olfactory or “homing” cues (Morman et al. 1980). Only 7.5% of streams in the Great Lakes watershed have supported spawning sea lamprey since 1957 (Morman et al. 1980). For these reasons, it was determined that inter-site comparisons within individual lakes would not reveal useful patterns in contaminant accumulation in adult sea lamprey muscle tissue. The MANOVA performed on wet weight chemical concentrations revealed significant differences in chemical accumulation in sea lamprey between lakes for toxaphene, total PCB, and p,p′-DDE (Table 2). A Fisher LSD test showed significantly greater total PCB concentrations in Lake Ontario sea lamprey than in Lake Erie, Lake Huron, and Lake Superior lamprey (all p < 0.001, Fig. 1). Lake Superior sea lamprey accumulated significantly less total PCB than lamprey from Lakes Erie or Huron (p = 0.002 and p = 0.011 respectively, Fig. 1). Total PCB concentrations were similar in sea lamprey from Lake Erie and Lake Huron. Concentrations of p,p′ DDE in Lake Ontario sea lamprey were significantly greater than in lamprey from all other lakes (all p < 0.001, Fig. 1). Concentrations of p,p′-DDE were not significantly different in sea lamprey from Lakes Erie, Huron, and Superior. Sea lamprey from Lake Superior accumulated significantly greater toxaphene levels than lamprey from all other lakes (all p < 0.001, Fig. 1) and Lake Huron lamprey accumulated significantly more toxaphene than Lake Ontario lamprey (p = 0.034, Fig. 1). All other combinations were not significantly different with respect to toxaphene accumulation in sea lamprey. The relative distribution and abundance of the contaminants measured in lamprey across the lakes in

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TABLE 2. MANOVA table for inter-lake differences in organic contamiant accumulation in sea lamprey. Univariate F tests df MS F p 3 1.37 47.67 < 0.001 53 0.03 3 0.18 18.45 < 0.001 53 0.01 3 0.93 38.87 < 0.001 53 0.02

Effect SS Toxaphene 4.12 error 1.53 p,p′-DDE 0.55 error 0.53 Total PCB 2.79 error 1.27 Multivariate test Hotelling-Lawley trace = 10.94, F = 60.4, df = 9 , 149, p < 0.001

this study correlate with what has been observed in other studies (DeVault et al. 1995). Toxaphene concentrations varied greatly across the lakes with a high of 2.60 µg/g in one individual from Lake Superior to less than 0.03 µg/g in two lamprey from Lake Erie and one lamprey from Lake Ontario. These observations are similar to patterns of toxaphene accumulation seen in lake trout from each of the Great Lakes (Whittle et al. 1997). Total PCB concentrations in individual sea lamprey exhibited a wide range of concentrations across the four lakes studied (Fig. 1). Highest PCB values were observed in Lake Ontario sea lamprey (2.39 µg/g) and lowest in Lake Superior lamprey (0.136 µg/g). Concentrations of p,p′-DDE in individual sea lamprey were greatest in Lake Ontario (0.810 µg/g) and least in Lake Superior lamprey (0.008 µg/g). Comparisons of total PCB and p,p′-DDE concentrations between sea lamprey and silver lamprey captured in Lake Erie are presented in Figure 2. Non-parametric Kruskal-Wallis tests indicated that there were no significant differences in tissue concentrations for these chemicals between the two lamprey species. Silver lamprey are native to the Great Lakes and are known to parasitize a variety of fish species. Hosts specific to the silver lamprey include lake sturgeon (Acipenser fulvescens), longnose gar (Lepisosteus osseus), brown bullhead (Ameiurus nebulosus), and rock bass (Ambloplites rupestris) (Scott and Crossman 1979). Wounds on a variety of fish species recorded by fishermen on Lake Ontario indicated that lake trout are a preferred host of the sea lamprey (Christie and Kolenosky 1980). The similarities in chemical concentrations between these two species of lamprey

FIG. 1. Contaminant concentrations in muscle tissue samples of sea lamprey collected from the Great Lakes. Error bars represent ± one standard error.

are notable considering the differences in the species that they are known to parasitize. Mercury levels varied over a wide range in the four lakes. Seventy-five percent of the samples were above the 0.5 µg/g Canadian Health Guideline

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FIG. 2. Comparison of p,p’-DDE, and total PCB concentrations in Lake Erie sea and silver lamprey muscle tissue samples. Error bars represent ± one standard error.

for consumption. Fifty percent of samples analyzed are above the U.S. Food and Drug Administration edible portion action level for fish of 1.0 µg/g. The highest concentration was 4.46 µg/g in an individual muscle tissue sample from Lake Superior while the lowest reported value was 0.10 µg/g from Lake Erie. All correlation coefficients between mercury concentrations in sea lamprey and weight, percent lipid, and lakes were not significant. Lake Superior sea lamprey had the highest mean mercury concentrations in muscle, followed respectively by Lake Ontario, Lake Huron, and Lake Erie lamprey (Fig. 1). A one-way ANOVA on mercury concentrations in sea lamprey muscle tissue revealed significant differences between lamprey from different lakes (F [3, 24] = 4.35, p = 0.014). A Fisher least significant difference procedure indicated significantly greater mercury accumulation in Lake Superior sea lamprey than in Lake Huron (p = 0.01), Lake Superior and Lake Erie (p = 0.005), and Lake Ontario and Lake Erie (p = 0.046, Fig. 1). All other comparisons were not significantly different. Comparisons of mercury levels in whole lake trout and adult sea lamprey muscle tissue are found in Figure 3, where tissue concentrations of mercury in lamprey muscle tissue samples were as much as ten times higher than whole-fish lake trout concentrations from the same lake. Evans et al. (1972) observed a similar pattern of mercury accumulation in lamprey to that seen here, where mercury content in adult sea lamprey tissue muscle samples from Lake

FIG. 3. Comparison of selected contaminant concentrations in whole lake trout and adult sea lamprey muscle tissue samples. Lake trout data are from D. M. Whittle (personal communication). Error bars represent ± one standard error.

Superior averaged 3 to 4 times greater than concentrations found in their primary host fish species. Methylmercury has a higher affinity for protein than lipid and is more likely to be found in the muscle tissue than other metals (Hodson 1988, Mason

Mercury and Organochlorine Contaminants in Sea Lamprey et al. 1995). Methylmercury is the predominant form of mercury in fish tissue (Kamps et al. 1972, Bloom 1992) and readily accumulates in aquatic organisms. Once in a biological matrix, the methyl mercuric ion binds to protinaceous material in membranes (Spacie et al. 1995). This process favors accumulation in protein rich tissues versus lipid rich tissues. A study of the pharmacodynamics of methylmercury in rainbow trout after an intragastric dose demonstrated that of 20 tissues sampled, blood had the highest mercury concentration factor by weight (Giblin and Massaro 1973). A similar study by Ribeyre and Boudou (1984), using direct contamination of rainbow trout with methylmercury via the surrounding water, resulted in elevated mercury accumulation in the blood. While high levels of mercury (> 1 µg/g) have been reported in lamprey ammocoetes from streams in the St. Lawrence region (Renauld et al. 1998) it is unlikely that the concentrations seen in adults in this study are strictly a vestige of the potentially lengthy (3 to 17 yr) in-stream ammocoete larval stage of sea lamprey. In fact, it has been suggested that the levels of some metals in the larvae may be the result of maternal transfer to the eggs (Holmes and Youson 1996). However, given the potential size dilution factor between the ammocoete stage (< 15 cm, < 5 g) and the spawning phase adults analyzed here (31 to 57 cm, ⋅ 59.5 to 382.1 g), it is unlikely that there is a substantial contribution to mercury levels from ammocoetes to adults. Given the affinity for protein of methylmercury, it is probable that adult lamprey ingest a disproportionate amount of mercury via the blood compared to chlorinated organic contaminants which accumulate largely in the lipid tissues (Stow et al. 1997) resulting in the high mercury concentrations in lamprey tissue. Sea lamprey primarily parasitize lake trout (Christie and Kolenosky 1980, Schneider et al. 1996), therefore a similar suite of chlorinated organic contaminants should be found in both lake trout and in sea lamprey. As chemical elimination rates are typically much lower than uptake rates in fish (Gobas et al. 1989) it is unlikely that adult lamprey can metabolize or depurate (while between hosts) a substantial amount of the contaminants accumulated from their hosts. Due to the small size of the ammocoete larvae compared to the adult, chlorinated contaminants accumulated during the larval phase should present a negligible contribution to the adult body burden (Kaiser 1982). The similarities in contaminant distribution between lamprey

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and lake trout from the same lake suggest that lamprey accumulate chlorinated contaminants as adults from their food source (Fig. 3). A comparison of contaminant burdens of ammocoete larvae, metamorphosing larvae, young adults, and spawning adults from the same stream would clarify the contribution of contaminants from each life stage to overall body burdens. Sea lamprey spend 12 to 20 months as parasiticphase adults, feeding primarily on the blood and body fluids of top predators. During the parasitic phase, sea lamprey accumulate contaminants from the blood and fluids of the hosts. Basic digestive physiology indicates that chemical concentrations in the blood of the host more closely reflect concentrations in recently consumed dietary items than the concentrations in the adipose tissue of the host (Hansen et al. 1976). The organic contaminants described in this study reside primarily in lipid storage tissues of organisms. Considering this, lamprey contaminant profiles should more closely reflect the profile of the diet of the host during the lampreyfeeding period. Lamprey exhibit a snapshot of the composition and relative abundance of the contaminants in the blood of the host during the time that the lamprey were feeding. Analyzing lamprey could allow one to capture more subtle temporal changes in contaminant levels than obtained from the host with their high background levels. Lamprey may prove to be an alternate to fish as an indicator of toxic chemical accumulation patterns in the Great Lakes. They are found in all the Great Lakes and can be captured as spawning run individuals or with their hosts and they readily accumulate contaminants. Further information on the dynamics of contaminant partitioning between the blood and viscera of fish after feeding could clarify the utility of lampreys as a surrogate species for routine temporaltrend contaminant surveillance. Contaminant concentrations in some Great Lakes sea lamprey muscle-tissue samples exceeded levels considered safe for human consumption for more than one contaminant. Some individuals from Lake Ontario exceed Canadian health protection guideline concentrations of 2.0 µg/g for PCBs. Other individuals from Lake Superior exceeded the present consumption advisory guidelines of 0.2 µg/g and 0.5 µg/g for both toxaphene and mercury, respectively. These levels indicate that lamprey from the lakes sampled in this study are not suitable fisheries products for export or local consumption. While cooking has been shown to reduce the levels of PCBs and DDT in fish (Skea et al. 1979, Moya et

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al. 1997, Salama et al. 1998), the cooking methods that resulted in a statistically significant decrease in these contaminants are not employed in traditional lamprey recipes (Sales 1996b). Mercury levels will also not be reduced by cooking; in fact the concentrations will be similar to or increased from the precooked concentrations (Morgan et al. 1997). Lamprey collected from each of the four Great Lakes surveyed consistently accumulated elevated levels of both organochlorine compounds and mercury. This clear ability to biomagnify mercury combined with the ubiquitous nature of lamprey in the Great Lakes basin indicates that this species may be an effective biomonitoring organism. In order to more fully evaluate the utility of sea lamprey as a tool for monitoring trends of toxic contaminants in the Great Lakes aquatic ecosystem, additional studies comparing lamprey contaminant burdens with several fish species must be carried out. ACKNOWLEDGMENTS The authors wish to acknowledge the Great Lakes Fishery Commission (D.V. Gillman) who provided funding for this study and staff of the DFO Sea Lamprey Control Centre, Sault Ste. Marie, Ontario (R. MacDonald, J. Tibbles) who completed the field sampling. Environment Canada’s National Laboratory for Environmental Testing (G. Paquette) provided the data on mercury levels in the sea lamprey samples while D.G. Haffner, University of Windsor, Great Lakes Institute for Environmental Research provided data on contaminant burdens in the silver lamprey. M. Malecki and C. Belanger provided technical support. REFERENCES Baumann, P.C., and Whittle, D.M. 1988. The status of selected organics in the Laurentian Great Lakes: an overview of DDT, PCBs, dioxins, furans and aromatic hydrocarbons. Aquat. Tox. 11:241–257. Bloom, N.S. 1992. On the chemical form of mercury in edible fish and marine invertebrate tissue. Can. J. Fish. Aquat. Sci. 49:1010–1017. Borgmann, U., and Whittle, D.M. 1991. Contaminant concentration trends in Lake Ontario lake trout (Salvelinus namaycush): 1977 to 1988. J. Great Lakes Res. 17:368–381. ——— , and Whittle, D.M. 1992. Bioenergetics and PCB, DDE and mercury dynamics in Lake Ontario lake trout (Salvelinus namaycush): a model based on surveillance data. Can. J. Fish. Aquat. Sci. 49:1086–1096. Christie, W.J., and Kolenosky, D.P. 1980. Parasitic

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