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Fish Stocking as an Overlooked Driver of Methylmercury Cycling and Exposure in Aquatic Ecosystems Sophia V. Hansson*,† and Michael S. Bank‡,§ †
Department of Bioscience − Arctic Research Centre, Aarhus University, Frederiksborgvej 399, Roskilde DK-4000, Denmark Department of Contaminants and Biohazards, Institute of Marine Research, Bergen, Norway § Department of Environmental Conservation, University of Massachusetts Amherst, 160 Holdsworth Way, Amherst, Massachusetts 01003, United States identify and discuss the role of fish introductions as an overlooked driver of methylmercury cycling and exposure in aquatic ecosystems (Figure 1). Farmed fish are often raised on a high-energy diet, with feed often originating from marine ecosystems that potentially leads to elevated concentrations of contaminants.5 When fish later are introduced or “stocked” into natural freshwater ecosystems they can be considered a humanly induced biovector with the potential to transport beneficial nutrients and harmful contaminants, such as MeHg, that then can be incorporated into the food web in the “new ecosystem”. Stocking lakes with non-indigenous or farm-reared predators, such as trout species, is a worldwide activity that has occurred at broad spatiotemporal scales and, with the exception of Antartica, non-native fish can currently be found in lakes and watersheds on all continents.6 Compared with the first estimates made nearly three decades ago the number of non-native species introduced worldwide has now more than doubled. In Europe alone, a yearly average of 132 million juvenile trout is produced for stocking purposes and millions of fish are annually introduced to freshwater ecosystems through sport fish management programs, rendering major economic and recreational benefits. However, the act of stocking fish to freshwater nvironmental contaminants, such as mercury (Hg) are ecosystems (Figure 1) may also cause several adverse effects. In often found in remote environments1 and management of a recent study, Hansson et al.7 used a suite of isotopic this ubiquitous pollutant, is of great interest to policymakers. signatures (i.e., 15N, 13C, 86−87Sr, and 199−204Hg) to show that Mercury pollution and specifically its more toxic form, introduction of farmed brown trout (Salmo trutta fario) to three methylmercury (MeHg), is of considerable global and societal high-altitude Pyrenean lakes, also led to an introduction and importance given Hg’s potential for long-range transport, transfer of marine Hg and MeHg to freshwater ecosystems.7 efficient bioaccumulation, and human exposure. Although Specifically, the marine derived Hg-isotopic signal could be atmospheric deposition is often a primary source of Hg seen up to five years after the initial fish introduction,7 clearly pollution, migrating biota can also act as biovectors by indicating a strong link between fish stocking and MeHg transporting contaminants across ecosystems. For example, exposure dynamics in freshwater ecosystems. migrating salmon that return to remote freshwater ecosystems, Further, fish stocking can lead to an extension of the natural can transfer MeHg from marine to terrestrial environments, food web by adding an additional trophic position to the introducing up to 1 kg of MeHg per year.2 Additionally, the ecosystem4 leading to either increased or decreased THg in export of Hg from freshwater environments back to the ocean resident top predators depending on the resident food web via juvenile salmon constitutes 3−30% of the total imported structure and prey−predator interaction.8 For example, historic Hg, providing clear evidence that biota act as a significant Hgfish stocking of non-native smallmouth bass (Micropterus pollution biovector.3 This movement of biomass has enormous dolomieu) at Acadia National Park, ME (USA), has created potential to alter exposure regimes and biogeochemical cycles an additional trophic position to the Hodgdon pond ecosystem in the surface waters to which they are introduced, yet despite as well as other waterbodies where bass are stocked. Here, these the obvious consequences of non-native fish introductions on 4 introduced bass bioaccumulated abnormally high levels of Hg ecosystems, the overall effects on the MeHg biogeochemical (maximum 3.86 ppm wet wt., and mean = 1.72 ppm wet wt.9) cycle remains poorly understood. Previous studies on biovector transport have largely focused on the natural migration of birds or fish, thus overlooking the humanly induced biovector Received: May 3, 2018 transports from aquaculture to natural watersheds. Here we ‡
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© XXXX American Chemical Society
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DOI: 10.1021/acs.est.8b01299 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
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Environmental Science & Technology
Figure 1. Conceptual image of the mercury cycle and the role of biota as biovectors of mercury fate and transport. Note that arrows and artwork are not to scale and are for descriptive purposes only.
independent, and that aquatic ecosystems can be bioengineered to either enhance or limit exposure to methylmercury, is of paramount importance to further understand the global mercury cycle. As we move forward as a scientific community addressing the problems related to MeHg fate, sources, effects and exposure will require a greater understanding of the importance and role of fish stocking on these processes. In light of the worldwide increasing trend of stocking, and the prioritized international interest in Hg as a global pollutant via the United Nations Minamata Convention on Mercury, it is clear that the contamination aspect related to fish introductions must be considered within sustainable fisheries management strategies and that stocking, with important exposure effects for both humans and piscivorous wildlife, has generally been overlooked as a driver of MeHg cycling in aquatic ecosystems.
resulting in a massive increase in exposure to humans and wildlife within a Class I Airshed, national park protected area. In contrast, fish introductions can also result in low Hg exposure regimes as was shown by Levengood et al.10 who reported extremely low levels of Hg in bighead carp (Hypophthalmichthys nobilis) and silver carp (Hypophthalmichthys molitrix) sampled from the Illinois River, IL (USA), which is hydrologically connected to the Great Lakes ecosystem. Fish stocking can also increase population density levels leading to reduced growth and biomass, which in turn leads to a higher trophic transfer rate of MeHg.11 This becomes even more important when considering that >85% of the Hg found in fish is in the highly neurotoxic and bioavailable form of MeHg.12 Since farmed fish are often raised on feed of marine origin stocking would also likely lead to an addition of MeHg5 that can remain in the altered watershed several years after introduction,7 creating a pollution exposure regime that is far more substantial than if the stocking had never occurred. Furthermore, stocking may also lead to a large introduction of biomass with the ability to alter ecological and geochemical processes. Carcasses from fish will contribute nutrients and organic carbon to aquatic ecosystems, which can stimulate primary production, heterotrophic activities and secondary production, but also exert controls over within lake MeHg cycling.13 Sarica et al.13 reported that leeches, that fed on fish carcasses, rapidly reached 5 times higher internal Hgconcentrations, and assumed the same Hg-isotopic signature of the fish carcass, within only 14 days. On average, 16% of the MeHg was transferred to scavengers and 3% to nearby biofilm, thus transferring the MeHg to other trophic levels in the lake.13 Studies have also shown that fish stocking may lead to a selective predation of pigmented invertebrates, which in turn may suppress key mechanisms of invertebrate photo reduction from UV.14 Such consequences and subsequent effects becomes imminent when fish stocking occurs in high-altitude environments which are already exposed to stronger UV radiation,15 a key function in the methylation process of Hg.16 Therefore, the consequences of stocking in clear, naturally fishless mountain lakes may exert a synergistic impact on biodiversity and ecosystem scale processes. In conclusion, collectively, the effects of fish stocking on biodiversity, ecosystem process and Hg and MeHg cycles should be considered substantial. Moreover, the concept that fisheries management and contaminant cycling are not
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AUTHOR INFORMATION
Corresponding Author
*Phone: +45 8715 86 77; e-mail:
[email protected]. ORCID
Sophia V. Hansson: 0000-0001-5874-0720 Notes
The authors declare no competing financial interest.
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REFERENCES
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DOI: 10.1021/acs.est.8b01299 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
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DOI: 10.1021/acs.est.8b01299 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
