Correspondence/Rebuttal pubs.acs.org/est
Lack of Evidence for Lower Mercury Biomagnification by Biomass Dilution in More Productive Lakes: Comment on "Mercury Biomagnification through Food Webs Is Affected by Physical and Chemical Characteristics of Lakes"
M
DOC is not a good proxy of biomass as the study lakes are dystrophic (typically high DOC, unproductive). The relationship with biomagnification was significant for TN but not for TP. TP is usually a better correlate of plankton biomass than TN,5 certainly in lakes where the N/P ratio is as high as in these lakes (molar N/P = 39−71; Table S2 in ref 1). The authors collected samples only in lakes within a small range of trophic state5 (TP = 6−14 mg m−3; Table S2 in ref 1). Because of dystrophy, TP concentrations may actually overestimate trophic state in these lakes. In contrast, Kidd et al. (2012)6 sampled across a larger TP range (8−44 mg m−3), although still limited to oligotrophic lakes5 in terms of algal biomass (means 0.8−3.0 mg m−3chlorophyll a), and found a significant positive correlation between TP and biomagnification. The authors state that higher Hg biomagnification slopes in lower-nutrient and lower-TOC systems could be due to enhanced uptake of Hg by lower-trophic-level organisms, thereby driving up the intercepts of the regressions of log Hg versus δ15N. The authors add, contradictorily, that this does not explain the greater biomagnification of Hg in these food webs. Indeed, it would not, unless Hg concentrations in upper trophic level organisms would increase proportionally more than in lower-trophic-level organisms (scenario 4). Otherwise smaller, not higher slopes would result. However, although the authors are correct that intercepts of the regressions of log Hg versus δ15N are expected to be higher in lower-nutrient systems according to the biomass dilution hypothesis, the intercepts were not higher in these systems. Instead, intercepts increased with TOC (p < 0.01), TN (p < 0.05) and TP (not significant; Table S4; Figure S2 in ref 1). Moreover, correlations of TOC, TN, and TP with Hg concentrations in all sampled groups of lower-trophic-level organisms (Heptageniidae, Limnephilidae, and zooplankton) were positive (none significant; Table S4 in ref 1). This is probably the result of significant positive correlations between Hg in profundal water and TOC, TN, and TP concentrations (Table S41). These results refute the hypothesis that biomass dilution in more productive lakes results in lower biomagnification of Hg because the hypothesis predicts that the correlations of TOC, TN, and TP with Hg concentrations in lower-trophic-level organisms are negative. There is evidence for higher Hg in plankton4,7 and fish4,8 in oligotrophic lakes, but no study,1,4,7−9 to my knowledge, has shown the latter to increase more than the former with decreasing lake productivity. Therefore, no evidence exists that biomagnification is reduced by biomass dilution in more productive lakes. Growth dilution as an effect of food quality (low N/P ratio)9 may reduce biomagnification but evidence for a consistent link between productive lakes and high food
ercury (Hg) concentrations in upper trophic level organisms in lakes, such as fish, may be enhanced by various environmental conditions, including physical and chemical characteristics of lakes. 1−3 In part, high Hg concentrations in fish may result from enhanced biomagnification, the transfer of Hg through the food web. The Hg transfer through the food web is quantified by the regression of log Hg against the trophic level indicator δ15N measured in organisms, and biomagnification is defined as the slope of this regression. Clayden et al. (2013)1 suggest that biomagnification is enhanced in nutrient poor and unproductive lakes, while in more nutrient-rich and productive lakes biomass dilution of Hg in more plentiful organisms, as well as growth dilution, reduces biomagnification. However, no evidence has been presented, by the authors1 or elsewhere, for biomagnification decreasing with increasing biomass in lakes as an effect of biomass dilution. Conceptually, the biomagnification slope may increase by only five scenarios: (1) by decreased Hg concentrations in lower trophic level organisms without a change in Hg concentrations in upper trophic level organisms, (2) by increased Hg concentrations in upper trophic level organisms, without a change in Hg concentrations in lower trophic level organisms, (3) by decreased Hg concentrations in lower trophic level organisms combined with increased Hg concentrations in upper trophic level organisms, (4) by increased Hg concentrations in lower trophic level organisms, combined with a proportionally (i.e., as a percentage of the untransformed Hg) larger increase in Hg concentrations in upper trophic level organisms, or (5) by decreased Hg concentrations in lower trophic level organisms, combined with a proportionally smaller decrease in Hg concentrations in upper trophic level organisms. The concept of biomass dilution suggests that in less productive lakes with low plankton biomass mercury is more concentrated in lower trophic level organisms. Concurring with others,4 the authors expect that this scenario results in enhanced biomagnification in less productive lakes. This would suggest the fourth scenario. However, there was no evidence for a biomass dilution effect at low trophic levels.1 Hg concentrations in invertebrates (including zooplankton) did not decrease but increased with nutrient and TOC concentrations (not significant; Table S4, Figure 1 in ref 1). The authors did not collect data of plankton biomass or of chlorophyll a, a popular proxy of phytoplankton biomass, to distinguish productivity in lakes. Instead, they used several other proxies for lake productivity, including concentrations in the water column of total nitrogen (TN), total phosphorus (TP), and total organic carbon (TOC). Their relationships with biomagnification were negative (Table S4; Figure S2 in ref 1). However, most of TOC in the study lakes was dissolved organic carbon (DOC, 86−100%; Table S31) and not biomass. © 2014 American Chemical Society
Published: August 18, 2014 10524
dx.doi.org/10.1021/es405415c | Environ. Sci. Technol. 2014, 48, 10524−10525
Environmental Science & Technology
■
quality or high growth rates of individual fish is missing. Instead, in some productive lakes biomagnification appears enhanced as the intercept of the regression of log Hg against δ15N is reduced by lower Hg concentrations in lower-trophiclevel organisms as a result of biomass dilution. This was suggested by regressions of biomagnification slopes and intercepts against TP in other Canadian lakes.6 Furthermore, in more extreme eutrophic lakes biomagnification may be enhanced through factors affecting methyl-Hg production, such as low oxygen conditions in bottom water, causing higher Hg concentrations in fish, but not in plankton.10 Biomagnification regressions are needed across a larger range of lake productivity including eutrophic lakes, quantified by plankton biomass, to provide convincing evidence for an effect of lake productivity on biomagnification.
Correspondence/Rebuttal
NOTE ADDED AFTER ASAP PUBLICATION The title of this paper has been revised from the original posting of August 18, 2014. The correct version was posted August 21, 2014.
Piet Verburg*
■
National Institute of Water and Atmospheric Research (NIWA), PO Box 11-115 Gate 10 Silverdale Road, Hamilton 3251, New Zealand
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Phone: +64 7856 1787. Fax: +64 7856 0151. Notes
The authors declare no competing financial interest.
■
REFERENCES
(1) Clayden, M. G.; Kidd, K. A.; Wyn, B.; Kirk, J. L.; Muir, D. C. G.; O’Driscoll, N. J. Mercury Biomagnification through Food Webs Is Affected by Physical and Chemical Characteristics of Lakes. Environ. Sci. Technol. 2013, 47, 12047−12053, DOI: 10.1021/es4022975. (2) Driscoll, C. T.; Han, Y. J.; Chen, C. Y.; Evers, D. C.; Lambert, K. F.; Holsen, T. M.; Kamman, N. C.; Munson, R. K. Mercury Contamination in Forest and Freshwater Ecosystems in the Northeastern United States. Bioscience 2007, 57, 17−28. (3) Chen, C. Y.; Stemberger, R. S.; Kamman, N. C.; Mayes, B. M.; Folt, C. L. Patterns of Hg Bioaccumulation and Transfer in Aquatic Food Webs Across Multi-Lake Studies in the Northeast US. Ecotoxicology 2005, 14, 135−147. (4) Chen, C. Y.; Folt, C. High Plankton Densities Reduce Mercury Biomagnification. Environ. Sci. Technol. 2005, 39, 115−121. (5) Wetzel, R. G. Limnology, Lake and River Ecosystems, 3rd ed.; Academic Press: San Diego, CA, U.S.A, 2001. (6) Kidd, K. A.; Muir, D. C. G.; Evans, M. S.; Wang, X.; Whittle, M.; Swanson, H. K.; Johnston, T.; Guildford, S. Biomagnification of Mercury through Lake Trout (Salvelinus namaycush) Food Webs of Lakes with Different Physical, Chemical, and Biological Characteristics. Sci. Total Environ. 2012, 438, 135−143. (7) Pickardt, P. C.; Folt, C. L.; Chen, C. Y.; Klaue, B.; Blum, J. D. Algal Blooms Reduce the Uptake of Toxic Methylmercury in Freshwater Food Webs. Proc. Natl. Acad. Sci. U.S.A. 2002, 99, 4419−4423. (8) Essington, T. E.; Houser, J. N. The Effect of Whole-Lake Nutrient Enrichment on Mercury Concentration in Age-1 Yellow Perch. Trans. Am. Fish. Soc. 2003, 132, 57−68. (9) Karimi, R.; Chen, C. Y.; Pickhardt, P. C.; Fisher, N. S.; Folt, C. L. Stoichiometric Controls of Mercury Dilution by Growth. Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (18), 7477−7482. (10) Lithner, G.; Borg, H.; Ek, J.; Fröberg, E.; Holm, K.; Johansson, A.-M.; Kärrhage, P.; Rosén, G.; Söderström, M. The Turnover of Metals in a Eutrophic and an Oligotrophic Lake in Sweden. Ambio 2000, 29, 217−229. 10525
dx.doi.org/10.1021/es405415c | Environ. Sci. Technol. 2014, 48, 10524−10525