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. Author manuscript; available in PMC: 2016 Dec 1.
Published in final edited form as: Sci Total Environ. 2015 Aug 15;536:866–871. doi: 10.1016/j.scitotenv.2015.07.106

Ecotoxicoparasitology: Understanding mercury concentrations in gut contents, intestinal helminths and host tissues of Alaskan gray wolves (Canis lupus)

Ashley K McGrew a, Todd M O'Hara a,b, Craig A Stricker c, J Margaret Castellini b, Kimberlee B Beckmen d, Mo D Salman e, Lora R Ballweber a
PMCID: PMC4807146  NIHMSID: NIHMS716177  PMID: 26283618

Abstract

Some gastrointestinal helminths acquire nutrients from the lumen contents in which they live; thus, they may be exposed to non-essential elements, such as mercury (Hg), during feeding. The objectives of this study were: 1) determine the total mercury concentrations ([THg]) in Gray wolves (Canis lupus) and their parasites, and 2) use stable isotopes to evaluate the trophic relationships within the host. [THg] and stable isotopes (C and N) were determined for helminths, host tissues, and lumen contents from 88 wolves. Sixty-three wolves contained grossly visible helminths (71.5%). The prevalence of taeniids and ascarids was 63.6% (56/88) and 20.5% (18/88), respectively. Nine of these 63 wolves contained both taeniids and ascarids (14.3%). All ascarids were determined to be Toxascaris leonina. Taenia species present included T. krabbei and T. hydatigena. Within the GI tract, [THg] in the lumen contents of the proximal small intestine were significantly lower than in the distal small intestine. There was a significant positive association between hepatic and taeniid [THg]. Bioaccumulation factors (BAF) ranged from <1 to 22.9 in taeniids, and 1.1 to 12.3 in Toxascaris leonina. Taeniid and ascarid BAF were significantly higher than 1, suggesting that both groups are capable of THg accumulation in their wolf host. δ13C in taeniids was significantly lower than in host liver and skeletal muscle. [THg] in helminths and host tissues, in conjunction with stable isotope (C and N) values, provides insight into food-web dynamics of the host GI tract, and aids in elucidating ecotoxicoparasitologic relationships. Variation of [THg] throughout the GI tract, and between parasitic groups, underscores the need to further evaluate the effect(s) of feeding niche, and the nutritional needs of parasites, as they relate to toxicant exposure and distribution within the host.

1. Introduction

Mercury (Hg) is a non-essential element that exists in numerous chemical forms, occurring both naturally in the environment and as the result of human activities. Major anthropogenic sources include the burning of fossil fuels (especially coal), municipal waste incineration (Virtanen et al., 2007), and other point sources such as amalgam waste from dental clinics (Shraim et al., 2011). Emissions from geological sources (e.g. cinnabar), as well as emissions from forest fires and volcanoes, also contribute Hg to the environment. Hg is not only ubiquitous, but also environmentally persistent (Balshaw et al., 2007), and can have detrimental effects on the health of organisms. Methylmercury (MeHg) is the highly toxic form (Kruzikova et al., 2008; Virtanen et al., 2007), which includes monomethylmercury (MeHg+) and dimethylmercury. The MeHg+ form has been shown to bioaccumulate and/or biomagnify in food webs, and often reaches high concentrations in specific tissues of long-lived fish eating animals (Clarkson & Magos, 2006; Balshaw et al., 2007; Bridges & Zalups, 2010; Virtenan et al., 2007).

Historically, studies on food webs have rarely included parasites, partly due to the complex nature of host-parasite interactions (Gómez-Díaz & González-Solís, 2010). The term ecotoxicology has been applied to the field of study focused on the effects of toxic chemicals on biological organisms, at the population, community, ecosystem level (Moriarty, 1988); Ecotoxicoparasitology, however, relates to the interface of three disciplines, and is concerned with complex systems including parasites, their hosts, and the toxicants to which they are exposed.

Several gastrointestinal helminths feed on the intestinal contents of the hosts in which they live, thereby, putting them in direct competition with their host for nutrients (Coop & Kyriazakis, 1999). These parasites are exposed to the same dietary and elimination pathways (e.g. bile) of the host; thus, uptake of toxicants by the parasites likely occurs as a direct result of their feeding activities within the host's gastrointestinal (GI) tract. One previous study showed that GI helminths are capable of bioaccumulation and/or biomagnification of non-essential elements at concentrations that are orders of magnitude higher than those in host tissues (Sures et al., 1999). However, the process by which parasites acquire, concentrate, and/or biotransform non-essential elements, such as mercury (Hg), and their potential impact on host-toxicant dynamics, is not well understood.

One tool that may be used to explore aspects of host-parasite relationships and mercury exposure is stable isotope analysis. In many systems, C and N stable isotopes have been used in feeding ecology studies to determine food web length and structure (Gómez-Díaz & González-Solís, 2010), often facilitating assessment of consumer feeding habits (Daugherty & Briggs, 2007). Because parasites utilize various feeding strategies, it may be challenging to interpret trophic relationships using isolated approaches (Gómez-Díaz & González-Solís, 2010). Previously stable isotope and THg analysis have been used to provide insight into sources of Hg exposure in gray wolves (McGrew et al., 2014). Nitrogen signatures have also been shown to have a positive association with total mercury concentrations [THg] in arctic food webs (Atwell et al., 1998). The aim of this study was, therefore, to use stable isotope signatures (C and N) and [THg] together, to better understand the influence of the host-parasite relationship on [THg], and provide insight into the trophic relationships that exist within gray wolves from Alaska.

2. Materials and Methods

2.1 Sample Collection

Samples from gray wolves from across the state of Alaska were collected by the Alaska Department of Fish & Game, between 2006 and 2009, as part of ongoing studies. Previously, McGrew et al. (2014) measured C and N stable isotope signatures and [THg] from the liver, kidney, and skeletal muscle of this wolf population. In this work, the GI tracts, GI helminths, and host tissues were evaluated from a subset of these individuals, as well as other wolves from Alaska (n = 88). At necropsy, sex, and age class were determined, and tissues, including liver, skeletal muscle, and GI tracts (with lumen contents and parasites) were collected. Nine of 88 GI tracts were processed immediately, whereas the remaining GI tracts were transferred to the University of Alaska Fairbanks (UAF) and stored at -80 C until further processing could take place. Wolves were divided into two age classes, <12 months, and ≥12 months, based on previous studies (Gese et al., 1997; McGrew et al., 2014; Zarnke et al., 2004).

During processing, the large and small intestines were opened longitudinally using clean stainless steel instruments, and all grossly visible parasites were removed, rinsed with ultrapure water, and weighed. Due to freezing, only the ascarids were able to be enumerated. A limited number of representative ascarids were fixed in 10% formalin for morphologic identification; likewise, a single individual, terminal, taeniid proglottid was frozen for molecular identification (Obwaller et al., 2004). All remaining ascarids and taeniids were frozen for subsequent THg analysis, and C and N stable isotope (SI) analysis. Lumen contents and full-thickness sections of GI wall were collected from proximal small intestine (pSI), distal small intestine (dSI), and colon, and were weighed prior to freezing at -80 C. Determination of [THg] and stable isotopes was carried out for host tissues, lumen contents, and parasites.

2.2 Total mercury (THg) analysis

Host liver and skeletal muscle, are commonly sampled tissues in THg and SI studies due to their intrinsic properties and rate of cellular turnover. In this study, these tissues were thawed at room temperature, and sub-sampled (70-150 mg) using clean stainless steel forceps and scissors. Instruments were washed with ultrapure water and dried between each sample. Samples were analyzed with a direct mercury analyzer (DMA) using a Milestone DMA-80 instrument as described previously (Butala et al., 2006; McGrew et al., 2014; EPA 600-R-04-012). Groups of ascarids or taeniids from each host were freeze-dried, homogenized using a mortar and pestle, and analyzed for THg on a dry weight basis. Ascarids and taeniids were homogenized and analyzed separately in instances of mixed infection. The homogeneity ensured [THg] were representative of the parasite group(s) collected from each host. [THg] were not determined for taeniids from 6/56 wolves due to low biomass. While host tissue [THg] were determined on a wet weight (ww) basis, both ww and dry weight (dw) values are presented for comparative purposes. Dry weight [THg] was calculated as ww [THg]/(1 - fraction moisture content). Percent moisture was also used to calculate [THg] in parasites on a wet weight basis.

2.3 Stable isotope analysis

SI values (δ13C and δ15N) were determined as previously described (McGrew et al., 2014). Briefly, all tissues to be analyzed were freeze-dried and homogenized prior to analysis, which was carried out with continuous-flow isotope-ratio mass spectrometry using an elemental analyzer (Carlo Erba NC1500 or Thermo Flash 2000) interfaced to a mass spectrometer (Micromass Optima or Thermo-Finnigan Delta Plus XP). Isotope values are reported in delta (δ) notation:

δX=(Rsample/Rstandard)−1

where X represents 13C or 15N in parts per thousand (‰) deviation relative to a standard (monitoring) gas and Rsample and Rstandard represent the ratio of 13C/12C, or 15N/14N, for sample and standard, respectively. Analytical error was assessed by replicate measures of primary standards (<0.2‰ for all three isotopes across all analytical sequences) and quality control was assessed using several secondary standards, analyzed several times within individual analytical sequences (<0.3 ‰); accuracy was assessed using primary standards as unknowns, and was within 0.2‰ for both isotopes. Reproducibility of values was generally better than 0.2‰.

2.4 Helminth Identification

Prevalence was defined as the proportion of wolves infected with a given parasite, and intensity was defined as the number of individuals of a particular parasite species, in a given host (Bush et al., 1997). Ninety-five percent confidence intervals were determined using the Clopper-Pearson method (Newcombe, 1998).

Ascarids were identified based on morphological criteria (Anderson et al., 1974). Three of 15 wolves harbored only a single ascarid; thus, species identification could not be performed without adversely affecting [THg] and stable isotope determination. Taeniids were identified using molecular techniques. Individual proglottids were taken from the taeniiids of 54/56 wolves. Genomic DNA was isolated from individual proglottids using a commercially available kit, according to manufacturer's instructions (Qiagen, DNA Blood and Tissue Kit). Primers targeting a fragment of the NADH dehydrogenase subunit I (ND1) gene, based on the protocol of Obwaller et al. (2004), were used to amplify an approximately 471 bp product. Amplification products were purified (Qiagen, QIAquick Gel Extraction Kit) prior to direct sequencing (Proteomics and Metabolomics Facility, Colorado State University, Fort Collins, CO). Nucleotide sequence comparisons were made using the BLAST software available from the NCBI website. Five sequences were unreadable, therefore 49/54 of the proglottids were identified to species.

2.5 Statistical Analyses

Chi-square tests were used to evaluate potential associations between pairs of dichotomous variables: age class, sex, the presence of taeniids, and the presence of ascarids. A Bonferroni-Holm adjustment was used on the p-values to control the Family-Wise error rate for multiple comparisons.

[THg] in GI tracts were compared separately for dw and ww using a repeated measures one-way ANOVA with unstructured covariance. A log10 transformation of [THg] was used to the meet model assumptions of residual normality and homoscedasticity. Differences were estimated using least-squares means (Ostle, 1976) and 95% confidence intervals, with adjustments to p-values made using Tukey's Honest Significant Difference to control Family-Wise error.

Data from both taeniid species were combined and analyzed together based biologic similarities that exist between these two taeniid species within a given geographic region (e.g. dominant definitive and intermediate hosts, host specificity, distribution) (Samuel et al., 1971). Differences in [THg] between parasitic groups were analyzed for wolves harboring both taeniids and ascarids, as well as for hosts harboring only taeniids or ascarids. This was evaluated using the Welch's paired t-test, or the Wilcoxin rank sum test, respectively. Bioaccumulation factors (BAFs) were calculated by dividing the [THg] in either taeniids or ascarids by the [THg] in the lumen contents from where the parasites were derived. BAFs are defined as the ratio of a certain chemical or toxicant in an organism, to the concentration of that same chemical or toxicant in the food source or environment of that organism. To test whether BAF > 1, data were transformed prior to using a t-test of whether the mean BAF was greater than 1. A log-transformation of taeniid BAF data and an inverse transformation of ascarid BAF data (i.e. 1/ascarid BAF) were used to best approximate a normal distribution. A onesided Wilcoxon signed rank test was used to test whether the values were symmetric about 1. Linear regression analysis comparing [THg] in taeniids and host liver was carried out on 47 wolves using log10-transformed data. An ANOVA was conducted on the δ13C levels in the host tissues and taeniids. Comparisons with ascarids were not possible due to low sample numbers and/or biomass. R and SAS statistical software were used for the statistical analyses described. Statistical values in which p <0.05 were considered to be significant.

3. Results

3.1 Demographic data

Sex information was available for all 88 wolves, and estimated age class information was available for 85/88 individuals. Among wolves that were <12 months of age (n = 26), 13 were female and 13 were male; of wolves that were ≥12 months (n = 59), 30 were females and 29 were males. There was no significant association between the variables of age, sex, presence of ascarids and presence of taeniids; therefore, all data from all wolves were combined for subsequent analyses.

3.2 Prevalence, mean intensity, and biomass

Prevalence of GI macrohelminths was 63/88 (71.5%; 95% CI =61.0%, 80.7%). Taeniids were present in 56/88 (63.6%; 95% CI=52.7%, 73.6%) animals, and ascarids were present in 18/88 (20.5%; 95% CI=12.6%, 30.4%). Nine of 63 parasitized wolves contained both ascarids and taeniids (14.3%; 95% CI=6.7%, 25.4%). All ascarids were identified as Toxascaris leonina. Twenty of the 49 cestodes were identified as Taenia krabbei (40.8%; 95% CI=27.0%, 55.8%), and 29/49 were Taenia hydatigena (59.2%; 95% CI=44.2%, 73.0%). Mean intensity of ascarids was 27.1 (1 - 91), whereas mean intensity of taeniids could not be determined. Median ascarid biomass per animal was 1.2g (0.6g - 9.2g), and median taeniid biomass per animal was 10.5g (0.01g - 45.5g). There were no significant associations between ascarid mean intensity and [THg], or biomass of either parasite group and [THg].

3.3 [THg] in host tissues

Median (range) hepatic [THg] was 37.8 (5.7-2226.8) ppb ww. Median (range) [THg] in the lumen contents of the pSI, dSI, and colon were 5.0 (<1.0 – 64.0), 7.8 (1.2 – 57.9), and 22.0 (2.8 – 463.0) ppb ww, respectively. In proximal small intestine (pSI) lumen contents, [THg] were <1ppb in 2/88 samples. Median (range) [THg] in the wall of the pSI, distal small intestine (dSI), and colon were 4.1 (<1 – 177.8), 3.5 (<1 – 79.6), and 3.5 (<1 - 49.4) ppb, respectively. [THg] was <1 ppb in 9/81 pSI wall samples, 13/83 dSI wall samples, and 18/73 colon wall samples. [THg] in lumen contents differed significantly based on location along the GI tract for both ww and dw. Least-squares means for [THg] (log10) and 95% confidence intervals for the means show [THg] in pSI lumen contents were significantly lower than in dSI lumen contents (Table 1).

Table 1.

Least-squares means and estimated differences of log10 total mercury concentrations ([THg]) throughout the gastrointestinal tract. Means are given for (THg) as determined by wet weight and by dry weight.

[THg] by Section [THg] Mean ± 95% CI (log10)
Wet Dry
Proximal SI lumen 0.69 ± 0.091 1.14 ± 0.12
Distal SI Lumen 0.99 ± 0.09 1.40 ± 0.15
Colon Contents 1.35 ± 0.10 1.63 ± 0.27
Differences in [THg] [THg] Wet [THg] Dry
Mean ± 95% CI (log10) Mean ± 95% CI (log10)
pSI lumen – dSI lumen -0.30 ± 0.10a 0.27 ± 0.15a
pSI lumen – colon contents -0.66 ± 0.11a 0.49 ± 0.35a
dSI lumen – colon contents -0.36 ± 0.09a 0.22 ± 0.25a
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a

Estimated differences are significant (p ≤ 0.05); [THg] in GI tracts were compared separately for dw and ww using a repeated measures one-way ANOVA

3.4 [THg] in parasites and host liver

Mean [THg] in taeniids and in Toxascaris leonina were determined (Table 2). No significant differences in [THg] were noted between these two parasite groups. Hepatic [THg] in hosts infected with taeniids (n = 57) ranged from 5.70 to 2,226.83 ppb (ww). [THg] in taeniids from these hosts ranged from 0.31 to 107.34 ppb (ww). Regression analysis showed a highly significant positive association between taeniid and host hepatic [THg] (r2 = 0.38, slope = 0.696, p<0.0001) (Figure 1). The relationship between [THg] in ascarids and host hepatic tissue could not be analyzed due to sample size constraints.

Table 2.

Mean, median, and range of [THg] in parasites from Alaskan wolves (n), expressed in ppb, wet weight (ww); standard deviation of the mean is indicated in parentheses.

Parasite n Mean Median Range
Taeniids 52 18.7 (±24.4) 7.4 0.31-107.3
Ascarids 12 8.9 (±3.7) 4.4 0.4-14.87
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Figure 1.

Figure 1

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Total mercury concentrations ([THg]) in taeniids (log10) against [THg] in the host liver (log10). There was an association between [THg], shown by the blue regression line (r2 =0.38, p<0.0001). Age (shape) and sex (color) are included to illustrate the lack of influence of these variables.

3.5 [THg] in parasites relative to host lumen contents

BAF ranged from <1 to 22.9 in taeniids, and 1.1 to 12.3 in Toxascaris leonina (Table 3), and there was no significant difference between BAFs of taeniids and ascarids. Mean cestode BAF was found to be significantly higher than 1, as was mean nematode BAF. For both taeniids and ascarids, significantly more values were higher than one than were lower than one.

Table 3.

Mean and median bioaccumulation factors (BAFs) of parasites, in wolves carrying either taeniids or ascarids.

Parasite n Mean Median Range
Taeniids 35 3.1 1.8 0.3 - 22.9
Ascarids 10 2.6 1.5 1.1 - 12.3
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3.6 Stable isotope analysis

Stable isotope values (δ13C and δ15N) were measured in host tissues as well as in the taeniids and ascarids (Table 4). δ13C values in taeniids were significantly lower than host livers and skeletal muscle. The low number of ascarids on which isotope signatures were measured precluded statistical comparison between the two parasite groups, as well as between the ascarids and their host.

Table 4.

Nitrogen (δ15N) Carbon (δ13C) stable isotope values for ascarids, taeniids, and gray wolf tissues and GI lumen contents. Sample number is shown, as well as mean and median values (pSI = proximal small intestine (SI), dSI = distal SI). Values are expressed on a per mil basis.

δ15N δ13C
n Mean Median Range n Mean Median Range
Liver 72 7.0 6.9 5.7 to 8.6 73 -24.6 -24.6 -26.7 to -21.8
Muscle 42 6.1 5.9 4.9 to 8.8 43 -23.5 -23.4 -25.5 to -21.9
Taeniids 37 3.9 4.3 3.0 to 11.2 37 -25.5 -25.1 -28.0 to -22.8
Ascarids 3 5.0 4.7 4.4 to 6.0 3 -23.6 -23.6 -23.2 to -23.9
pSI wall 10 6 6.2 4.4 to 7.1 10 -23.8 -23.9 -25.2 to -22.3
dSI wall 10 7.1 7.1 5.9 to 8.2 10 -24.7 -24.0 -28.4 to -22.1
Colon wall 10 6.8 7.0 5.9 to 7.3 10 -24.7 -23.8 -29.2 to -22.1
pSI-lumen 4 6.4 6.4 5.9 to 6.8 4 -25.5 -25.5 -25.6 to -25.4
dSI-lumen 5 6.0 6.1 5.5 to 6.4 5 -24.8 -25.0 -25.4 to -23.5
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4. Discussion

While previous studies have explored isolated aspects of host-parasite relationships and C and N stable isotopes in mammals (Sinisalo et al., 2006), and stable isotopes have been extensively used in mammalian ecology (Crawford et al., 2008), studies integrating the use of stable isotopes and THg in order to examine the interface of the toxicant-parasite interactions and host feeding ecology in wolves have not been carried out. Furthermore, as few studies have explored [THg] and SI values in parasites, determining which species of parasites were present in these wolves was important, as it provides ecological and biological context for the [THg] and SI values obtained.

In this study, wolves were infected with Toxascaris leonina, Taenia krabbei, and Taenia hydatigena, all of which have been previously reported in this host species (Ćirović et al., 2015; Guerra et al., 2012; Lavikainen et al., 2011; Rausch, 1959; Segovia et al., 2001). Both prevalence and mean intensity of ascarids was higher in these wolves compared to wolves elsewhere (Abdybekova & Torgerson, 2012; Gori et al., 2015; Guberti et al., 1993; Popiolek et al., 2007; Stronen et al., 2011). The prevalence of these GI helminths was expected, given the dietary trends of these wolf populations, the transmission cycles of these parasites, and the presence of appropriate intermediate and/or paratenic hosts in this geographic region.

Within the host, [THg] in host lumen contents and GI wall were consistently low. However, trends were still evident, with concentrations increasing, moving aborally through the intestinal tract. Taeniids and ascarids commonly reside in the proximal small intestine of their definitive host, and appear to be inhabiting an ecological niche that is relatively lower in THg concentrations than elsewhere in the GI tract, as indicated in this study. Whether the [THg] in that particular area of the GI tract is lower due to the presence of the parasites is not known. Studies focused on understanding the mechanisms by which these parasites take up and/or excrete non-essential elements such as Hg, as well as whether inter- or intra-specific competition exists between parasite groups, are clearly needed. In these wolves, [THg] in the GI tract do not appear to be altering the typical site preferences of these parasites.

[THg] did not differ significantly between taeniids and ascarids, which was somewhat surprising, given that these parasite groups assimilate nutrients in different ways and utilize different feeding strategies (Hall, 1985; Halton, 1997). Taeniids do not possess a GI tract, and acquire host-derived nutrients directly across their tegument (Pappas, 1983). Whether certain cestode (taeniid) species are able to discriminate between different types of food sources remains unknown (Persson, 2007). Our results also suggest that some parasite groups may be more effective at THg bioaccumulation, relative to others, as evidenced by the greater variation of [THg] and BAFs seen in taeniids. The fact that [THg] in taeniids were associated with [THg] in the host liver suggests that [THg] in some groups of parasites may be reflective of trends seen at the level of the host. In the future, it would be worth exploring antemortem approaches to measuring [THg] in taeniid proglottids that have been passed into the environment.

BAFs in both parasite groups were significantly higher than 1 which signifies that THg is higher in the parasite than in the lumen contents in which it lives (i.e. source of nutrients). The possibility that parasites have the potential to affect host contaminant uptake and retention has been previously explored (Provencher, 2013; Robinson et al., 2010).

C and N stable isotope analysis is a valuable tool in understanding food-webs; however, their application in parasitology has only been explored on a limited basis. It is critical to recognize how parasitism differs from predation as a trophic strategy, and how parasites differ from each other when interpreting host-parasite-toxicant interactions in a complex system. We found that 15N was depleted in taeniids and ascarids relative to all wolf tissues and GI lumen contents. 15N depletion relative to host tissues has been previously reported for both nematodes and cestodes (Boag, 1998; Pinnegar et al., 2001; Xu et al., 2007) as well as in a number of studies on fish-host-parasite systems (Deudero et al., 2002; Iken et al., 2001, Pinnegar et al., 2001; Xu et al., 2007). To our knowledge, 15N depletion in parasites, relative to the host, has not been described in wolves, although it has been reported in non-mammalian speices (Robinson et al., 2010).

It has been noted previously that isotopic fractionation in parasites is not well understood (Boag et al., 1998; Neilson & Brown, 1999) and parasites have been shown to have both higher and lower isotope ratios (C & N) relative to their host (Boag 1998; Neilson & Brown, 1999; Deudero et al., 2002). It has also been suggested that, for parasites, which assimilate only specific host-derived biosubstrates, their isotopic composition will be based only on those particular nutrient components (Behrmann-Godel & Yohannes, 2013). In typical predator-prey relationships, 13C and 15N are enriched ∼1‰ and 0-6‰, respectively (Deniro & Epstein, 1978; Minagawa & Wada, 1984); however, the magnitude and direction of fractionation in parasites is thought to be affected by numerous factors, including feeding strategy, nutrient requirements, rate of feeding, rate of excretion, assimilation efficiency, feeding selectivity, and life stage (Behrmann-Godel & Yohannes, 2013; Deudero et al., 2002; Olive et al., 2003; Lafferty et al., 2008).

5. Conclusions

The results of this study suggest that parasites may potentially be playing a beneficial role, serving as a biological ‘sink’ for non-essential elements to which the host is exposed, which supports the findings of Sures (2008). It is plausible that parasites are also evolving mechanisms to survive and perpetuate their life cycle in the face of increasing exposure to toxicants and changing environmental stressors. For these reasons, further studies are needed to explore the dynamics of parasite populations within the host, and particularly, the effects of ecological niche on toxicant distribution and bioavailability within the host.

Highlights.

  • [THg] and stable isotopes together provide insight on host-parasite-Hg interactions

  • A significant positive association exists between host liver and taeniid [THg]

  • [THg] varies within the GI tract and may be influenced by the presence of parasites

  • [THg] is higher in ascarids & taeniids than in the lumen contents in the GI tract

Acknowledgments

The authors extend their sincere gratitude to personnel at the Alaska Department of Fish and Game (ADF&G), and those individuals who assisted in sample collection. The authors appreciate the assistance provided by personnel in the Wildlife Toxicology Laboratory (UAF) for review and discussion of techniques, assistance with shipping samples, as well as use of equipment. The project described was supported by Grant Number 5P20RR016466 from the National Center for Research Resources (NCRR), a component of the National Institutes of Health (NIH); its contents are solely the responsibility of the authors, and do not necessarily represent the official views of NCRR or NIH. Cayce Gulbransen and Matthew Emmons conducted the isotope analyses. The use of any trade, product, or firm names is for descriptive purposes only and does not imply endorsement by the U.S. government. The authors also thank Barb Andre for her statistical advice.

Footnotes

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