J Marine Sci Res Dev. 2016 Apr;6(2):188. doi: 10.4172/2155-9910.1000188.

Mercury accumulation and the mercury-PCB-sex interaction in summer flounder

Charles P. Madenjian1, Olaf P. Jensen2, David P. Krabbenhoft3, John F. DeWild3, Jacob M. Ogorek3, and Anthony R. Vastano2

1US Geological Survey, Great Lakes Science Center, Ann Arbor, Michigan, USA

2Department of Marine and Coastal Sciences, Rutgers University, New Brunswick, New Jersey, USA

3US Geological Survey, Wisconsin Water Science Center, Middleton, Wisconsin, USA

 

Abstract

Patterns in the relative differences in contaminant concentrations between the sexes of mature fish may reveal important behavioral and physiological differences between the sexes. We determined whole-fish total mercury (Hg) concentrations in 23 female summer flounder (Paralichthys dentatus) and 27 male summer flounder from New Jersey coastal waters. To estimate the change in Hg concentration due to release of eggs at spawning, Hg concentration in the somatic tissue and ovaries of 5 of the 23 female summer flounder were also determined. To ascertain whether most of the Hg in the summer flounder was methylmercury (MeHg), whole-fish MeHg concentrations were determined in all 50 summer flounder. Whole-fish Hg concentrations averaged 113 ng/g for females and 111 ng/g for males. Thus, females were 2% higher in Hg concentration than males, on average, but the difference was not statistically significant. Based on Hg determinations in the somatic tissue and ovaries, we predicted that Hg concentration of females would increase by 3.6%, on average, immediately after spawning due to release of eggs. On average, 92% of the Hg in the summer flounder was MeHg. To determine whether the effect of sex on Hg concentration was significantly different from the effect of sex on polychlorinated biphenyl (PCB) concentration, we paired our Hg determinations with PCB determinations from a previous study, and applied regression analysis. Sex significantly interacted with contaminant type (Hg or PCBs), as males were 43% higher in PCB concentration than females, whereas females were 2% higher in Hg concentration than males. Males eliminating Hg from their bodies at a faster rate than females was a likely explanation for this discrepancy between the two contaminant types. Overall, the Hg and PCB concentrations in the summer flounder were relatively low, and therefore our findings also had implications for continued operation of the summer flounder fishery.

KEYWORDS: androgens; fish consumption advisories; Hg-elimination rates; mercury; methylmercury; PCBs; sex differences; summer flounder; testosterone

 

Supplement:

Mercury (Hg) and polychlorinated biphenyls (PCBs) are legacy contaminants found in fish. The predominant pathway of these contaminants into the fish’s body is via food consumption [1,2]. Correspondingly, both Hg and PCBs have been touted as reliable tracers of food consumption by fish [1,3]. Long-term elimination of PCBs from the fish’s body has been determined to be negligible [4,5]. In other words, PCB elimination proceeds so slowly, if at all, that changes in the amount of PCBs within the fish due to long-term elimination are not detectable. Long-term elimination of Hg from the fish’s body is measurable, although the elimination process is slow [1,4].

 

Because Hg and PCBs are considered reliable tracers of food consumption, we would expect that, for a given fish population, the ratio of PCB concentration in mature males to PCB concentration in mature females equals the ratio of Hg concentration in mature males to Hg concentration in mature females. However, this is not what we observe. Summary statistics for three species of freshwater fishes, namely lake trout (Salvelinus namaycush), burbot (Lota lota), and lake whitefish (Coregonus clupeaformis), as well as a marine species, namely summer flounder (Paralichthys dentatus), are displayed in Table 1. For all four species of these teleost fishes (modern bony fishes), the ratio of PCB concentration in males to PCB concentration in females exceeds the ratio of Hg concentration in males to Hg concentration in females.

 

Table 1. Estimates of the ratio of PCB concentration in males to PCB concentration in females and the ratio of Hg concentration in males to Hg concentration in females. Estimates taken from Madenjian et al. [4].

 

In addition, PCB concentration in males is greater than PCB concentration in females for all four fish species (Table 1). This sex difference in PCB concentrations has been attributed to males expending energy at a faster rate than females, due to males having greater swimming activity than females and to males having a higher resting metabolic rate than females [5]. A higher rate of energy expenditure leads to a higher rate of food consumption, which in turn leads to a higher rate of PCB accumulation.

 

The most likely explanation for the above-mentioned discrepancy between the PCB ratios and the Hg ratios is that males eliminate Hg at a substantially faster rate than females [4,5]. Medical researchers have shown that mature male laboratory mice (Mus musculus) eliminate Hg in their urine at a rate roughly three times higher than that for mature female mice. Further research has demonstrated that once mature male mice are castrated, their Hg-elimination rate is on par with that for mature females. Moreover, injecting mature female mice with testosterone results in an increase in their Hg-elimination rate such that it is equal to the Hg-elimination rate for mature males. In sum, this medical research has provided compelling evidence linking testosterone with enhancement of the Hg-elimination rate in male laboratory mice. The testosterone in laboratory mice has a chemical structure identical to the testosterone found in teleost fishes as well as higher vertebrates, including humans. Male teleost fishes also possess 11-ketotestosterone, an androgen unique to the teleost fishes and very similar in structure to that of testosterone. Madenjian et al. [4,5] proposed that testosterone and 11-ketotestosterone enhance Hg-elimination rate in male teleost fishes. This enhancement of Hg-elimination rate in males can account for the ratio of PCB concentration in males to PCB concentration in females exceeding the ratio of Hg concentration in males to Hg concentration in females.

 

We also note that the difference between the ratio of PCB concentration in males to PCB concentration in females and the ratio of Hg concentration in males to Hg concentration in females varies considerably between fish species (Table 1). For example, male lake trout are 22% higher in PCB concentration than female lake trout, while male lake trout are 8% higher in Hg concentration than female lake trout. In contrast, male burbot are 29% higher in PCB concentration than female burbot, while female burbot are 22% higher in Hg concentration than male burbot. Madenjian et al. [4,5] proposed that this interspecific variability in the difference between these two ratios can be attributed to the degree of enhancement of Hg-elimination rate in males varying from one species to another. This interspecific variability in the degree of enhancement of the Hg-elimination rate in males may be partly due to the level of androgens responsible for Hg-elimination rate enhancement (such as testosterone and 11-ketotestosterone) in males varying between species.

 

To illustrate the difference in Hg budgets between the sexes of teleost fishes, consider the summer flounder as an example. The predominant pathway of entry of Hg into the bodies of summer flounder is via food consumption (Figure 1). For a given size of summer flounder, the rate of intake of Hg via food consumption is greater for males than females, because males consume food at a higher rate than females due to a higher rate of energy expenditure. However, males eliminate Hg from their bodies at a faster rate than females, because Hg-elimination rate of males is enhanced by certain androgens. The net result is that Hg concentration in females is very similar to Hg concentration in males in summer flounder (Table 1; Figure 1). 

 

 

Figure 1. Illustration of the Hg budget for both male and female summer flounder.

 

References

[1] Trudel M, Rasmussen JB. 2001. Predicting mercury concentration in fish using mass balance models. Ecological Applications 11:517-529.

[2] Weininger D. 1978. Accumulation of PCBs by lake trout in Lake Michigan. Ph.D. dissertation, University of Wisconsin-Madison.

[3] Madenjian CP, CP, O’Connor DV, Nortrup DA. 2000. A new approach toward evaluation of fish bioenergetics models. Canadian Journal of Fisheries and Aquatic Sciences 57:1025-1032.

[4] Madenjian CP, Jensen OP, Krabbenhoft DP, DeWild JF, Ogorek JM, Vastano AR. 2016. Mercury accumulation and the mercury-PCB-sex interaction in summer flounder. Journal of Marine Science: Research & Development 6:188.

[5] Madenjian CP, Rediske RR, Krabbenhoft DP, Stapanian MA, Chernyak SM, O’Keefe JP. 2016. Sex differences in contaminant concentrations of fish: a synthesis. Biology of Sex Differences 7:42.

 

Acknowledgments

We thank Joshua Miller and Abram DaSilva for providing helpful comments to improve the manuscript. We also thank Taaja Tucker for preparing the scientific illustration.

 

Contact

Charles Madenjian

USGS Great Lakes Science Center

1451 Green Road

Ann Arbor, Michigan, USA

Phone: (734) 214-7259

E-mail: cmadenjian@usgs.gov