Metal Bioaccumulation by Estuarine Food Webs in New England, USA.

Evaluating the degree of metal exposure and bioaccumulation in estuarine organisms is important for understanding the fate of metals in estuarine food webs. We investigated the bioaccumulation of Hg, methylmercury (MeHg), Cd, Se, Pb, and As in common intertidal organisms across a watershed urbanization gradient of coastal marsh sites in New England to relate metal exposure and bioaccumulation in fauna to both chemical and ecological factors. In sediments, we measured metal and metalloid concentrations, total organic carbon (TOC) and SEM-AVS (Simultaneously extracted metal-acid volatile sulfides). In five different functional feeding groups of biota, we measured metal concentrations and delta 15N and delta 13C signatures. Concentrations of Hg and Se in biota for all sites were always greater than sediment concentrations whereas Pb in biota was always lower. There were positive relationships between biota Hg concentrations and sediment concentrations, and between biota MeHg concentrations and both pelagic feeding mode and trophic level. Bioavailability of all metals measured as SEM-AVS or Benthic-Sediment Accumulation Factor was lower in more contaminated sites, likely due to biogeochemical factors related to higher levels of sulfides and organic carbon in the sediments. Our study demonstrates that for most metals and metalloids, bioaccumulation is metal specific and not directly related to sediment concentrations or measures of bioavailability such as AVS-SEM.

Benthic and pelagic pathways of methylmercury bioaccumulation in estuarine food webs of the northeast United States.

Methylmercury (MeHg) is a contaminant of global concern that bioaccumulates and bioamagnifies in marine food webs. Lower trophic level fauna are important conduits of MeHg from sediment and water to estuarine and coastal fish harvested for human consumption. However, the sources and pathways of MeHg to these coastal fisheries are poorly known particularly the potential for transfer of MeHg from the sediment to biotic compartments. Across a broad gradient of human land impacts, we analyzed MeHg concentrations in food webs at ten estuarine sites in the Northeast US (from the Hackensack Meadowlands, NJ to the Gulf of Maine). MeHg concentrations in water column particulate material, but not in sediments, were predictive of MeHg concentrations in fish (killifish and Atlantic silversides). Moreover, MeHg concentrations were higher in pelagic fauna than in benthic-feeding fauna suggesting that MeHg delivery to the water column from methylation sites from within or outside of the estuary may be an important driver of MeHg bioaccumulation in estuarine pelagic food webs. In contrast, bulk sediment MeHg concentrations were only predictive of concentrations of MeHg in the infaunal worms. Our results across a broad gradient of sites demonstrate that the pathways of MeHg to lower trophic level estuarine organisms are distinctly different between benthic deposit feeders and forage fish. Thus, even in systems with contaminated sediments, transfer of MeHg into estuarine food webs maybe driven more by the efficiency of processes that determine MeHg input and bioavailability in the water column.

Do low-mercury terrestrial resources subsidize low-mercury growth of stream fish? Differences between species along a productivity gradient.

Low productivity in aquatic ecosystems is associated with reduced individual growth of fish and increased concentrations of methylmercury (MeHg) in fish and their prey. However, many stream-dwelling fish species can use terrestrially-derived food resources, potentially subsidizing growth at low-productivity sites, and, because terrestrial resources have lower MeHg concentrations than aquatic resources, preventing an increase in diet-borne MeHg accumulation. We used a large-scale field study to evaluate relationships among terrestrial subsidy use, growth, and MeHg concentrations in two stream-dwelling fish species across an in-stream productivity gradient. We sampled young-of-the-year brook trout (Salvelinus fontinalis) and Atlantic salmon (Salmo salar), potential competitors with similar foraging habits, from 20 study sites in streams in New Hampshire and Massachusetts that encompassed a wide range of aquatic prey biomass. Stable isotope analysis showed that brook trout used more terrestrial resources than Atlantic salmon. Over their first growing season, Atlantic salmon tended to grow larger than brook trout at sites with high aquatic prey biomass, but brook grew two-fold larger than Atlantic salmon at sites with low aquatic prey biomass. The MeHg concentrations of brook trout and Atlantic salmon were similar at sites with high aquatic prey biomass and the MeHg concentrations of both species increased at sites with low prey biomass and high MeHg in aquatic prey. However, brook trout had three-fold lower MeHg concentrations than Atlantic salmon at low-productivity, high-MeHg sites. These results suggest that differential use of terrestrial resource subsidies reversed the growth asymmetry between potential competitors across a productivity gradient and, for one species, moderated the effect of low in-stream productivity on MeHg accumulation.

Assessing element-specific patterns of bioaccumulation across New England lakes.

Little is known about differences among trace elements in patterns of bioaccumulation in freshwater food webs. Our goal was to identify patterns in bioaccumulation of different elements that are large and consistent enough to discern despite variation across lakes. We measured methylmercury (MeHg) and trace element (As, Cd, Hg, Pb, and Zn) concentrations in food web components of seven New England lakes on 3-5 dates per lake, and contrasted patterns of bioaccumulation across lakes, metals and seasons. In each lake, trace element concentrations were compared across trophic levels, including three size fractions of zooplankton, planktivorous fish, and piscivorous fish. The trophic position of each food web component was estimated from N isotope analysis. Trace element concentrations varied widely among taxa, lakes and sampling dates. Yet, we identified four consistent patterns of bioaccumulation that were consistent across lakes: (1) MeHg concentration increased (i.e., was biomagnified) and Pb concentration decreased (i.e., was biodiminished) with increased trophic position. (2) Zinc concentration (as with MeHg) was higher in fish than in zooplankton, but overall variation in Zn concentration (unlike MeHg) was low. (3) Arsenic and Cd concentrations (as with Pb) were lower in fish than in zooplankton, but (unlike Pb) were not significantly correlated with trophic position within zooplankton or fish groups. (4) Average summer concentrations of As, Pb, Hg, and MeHg in zooplankton significantly predicted their concentrations in either planktivorous or piscivorous fish. Our secondary goal was to review sampling approaches in forty-five published studies to determine the extent to which current sampling programs facilitate cross-lake and cross-study comparisons of bioaccumulation. We found that studies include different components of the food web and sample too infrequently to enable strong cross-lake and cross-study comparisons. We discuss sampling strategies that would improve our capacity to identify consistent patterns of bioaccumulation and drivers of elevated trace element concentrations under naturally high levels of variability.

Seasonal shift in the effect of predators on juvenile Atlantic salmon (Salmo salar) energetics.

Predator effects on prey populations are determined by the number of prey consumed and effects on the traits of surviving prey. Yet, effects of predators on prey traits are rarely evaluated in field studies. We measured the effects of predators on energetic traits (consumption and growth rates) of juvenile Atlantic salmon (Salmo salar) in a large-scale field study. Salmon fry were released at 18 sites that encompassed a wide range in abundance of predatory slimy sculpin (Cottus cognatus). We sampled salmon after 21 and 140 days to measure salmon growth and estimate consumption using a mass-balance model of methylmercury accumulation. Salmon population density was reduced fivefold at sites with abundant sculpin. Over the early season, salmon consumed less where sculpin were abundant, suggesting that reduced foraging under predation risk contributed to predator-caused mortality. In contrast, over the late season, salmon grew more where sculpin were abundant, suggesting that compensatory growth at reduced salmon population density moderated predator-caused mortality. Predator effects on prey energetics can drive variation in survival and growth, with important consequences for population dynamics.

Bioaccumulation syndrome: identifying factors that make some stream food webs prone to elevated mercury bioaccumulation.

Mercury is a ubiquitous contaminant in aquatic ecosystems, posing a significant health risk to humans and wildlife that eat fish. Mercury accumulates in aquatic food webs as methylmercury (MeHg), a particularly toxic and persistent organic mercury compound. While mercury in the environment originates largely from anthropogenic activities, MeHg accumulation in freshwater aquatic food webs is not a simple function of local or regional mercury pollution inputs. Studies show that even sites with similar mercury inputs can produce fish with mercury concentrations ranging over an order of magnitude. While much of the foundational work to identify the drivers of variation in mercury accumulation has focused on freshwater lakes, mercury contamination in stream ecosystems is emerging as an important research area. Here, we review recent research on mercury accumulation in stream-dwelling organisms. Taking a hierarchical approach, we identify a suite of characteristics of individual consumers, food webs, streams, watersheds, and regions that are consistently associated with elevated MeHg concentrations in stream fish. We delineate a conceptual, mechanistic basis for explaining the ecological processes that underlie this vulnerability to MeHg. Key factors, including suppressed individual growth of consumers, low rates of primary and secondary production, hydrologic connection to methylation sites (e.g., wetlands), heavily forested catchments, and acidification are frequently associated with increased MeHg concentrations in fish across both streams and lakes. Hence, we propose that these interacting factors define a syndrome of characteristics that drive high MeHg production and bioaccumulation rates across these freshwater aquatic ecosystems. Finally, based on an understanding of the ecological drivers of MeHg accumulation, we identify situations when anthropogenic effects and management practices could significantly exacerbate or ameliorate MeHg accumulation in stream fish.

Rapid, efficient growth reduces mercury concentrations in stream-dwelling Atlantic salmon.

Mercury (Hg) is a potent toxin that biomagnifies in aquatic food webs. Large fish generally have higher Hg concentrations than small fish of the same species. However, models predict that fish that grow large faster should have lower Hg concentrations than small, slow-growing fish due to somatic growth dilution (SGD). We examined the relationship between Hg concentrations and growth rate in fish using a large-scale field experiment. Atlantic salmon (Salmo salar) fry hatched under uniform initial conditions were released at eighteen sites in natural streams, collected after one growing season, and Hg concentration and growth measured. As expected for Hg accumulation from food, mercury concentrations in salmon tracked Hg concentrations in their prey. Nonetheless, large, fast-growing salmon had lower Hg concentrations than small, slow-growing salmon, consistent with SGD. While prey Hg concentration accounted for 59% of the explained variation in salmon Hg concentration across sites, salmon growth rate accounted for 38% of the explained variation independent of prey Hg concentration. A mass-balance Hg accumulation model shows that such SGD occurs when fast growth is associated with high growth efficiency. Fish growth is tremendously variable and sensitive to anthropogenic impacts, so SGD of Hg has important implications for fisheries management.

Reduced trace element concentrations in fast-growing juvenile Atlantic salmon in natural streams.

To assess the effect of rapid individual growth on trace element concentrations in fish, we measured concentrations of seven trace elements (As, Cd, Cs, Hg, Pb, Se, Zn) in stream-dwelling Atlantic salmon (Salmo salar) from 15 sites encompassing a 10-fold range in salmon growth. All salmon were hatched under uniform conditions, released into streams, and sampled approximately 120 days later for trace element analysis. For most elements, element concentrations in salmon tracked those in their prey. Fast-growing salmon had lower concentrations of all elements than slow growers, after accounting for prey concentrations. This pattern held for essential and nonessential elements, as well as elements that accumulate from food and those that can accumulate from water. At the sites with the fastest salmon growth, trace element concentrations in salmon were 37% (Cs) to 86% (Pb) lower than at sites where growth was suppressed. Given that concentrations were generally below levels harmful to salmon and that the pattern was consistent across all elements, we suggest that dilution of elements in larger biomass led to lower concentrations in fast-growing fish. Streams that foster rapid, efficient fish growth may produce fish with lower concentrations of elements potentially toxic for human and wildlife consumers.

Mercury bioavailability and bioaccumulation in estuarine food webs in the Gulf of Maine.

Marine food webs are important links between Hg in the environment and human exposure via consumption of fish. Estuaries contain sediment repositories of Hg and are also critical habitat for marine fish and shellfish species consumed by humans. MeHg biotransfers from sites of production in estuarine sediments to higher trophic levels via both benthic and pelagic pathways. In this study, we investigated the potential for Hg biotransfer to estuarine food webs across a Hg contamination gradient in the Gulf of Maine. Despite the variation in sediment Hg concentrations across sites (>100 fold), Hg concentrations in biota ranged by only 2-4 fold for each species across sites. Sediment contamination alone explained some variation in Hg and MeHg concentrations in biota across sites. However, biogeochemical and ecological factors also explained significant variation in Hg bioaccumulation across species. Contaminated sites had higher total organic carbon concentrations in sediments, which related to a decrease in Hg bioaccumulation (measured as biota-sediment concentration factors). Moreover, concentrations of MeHg were higher in pelagic-feeding than benthic-feeding fauna (determined from delta13C), indicating the importance of pelagic pathways in transferring MeHg. Lastly, the proportion of total Hg as MeHg increased with trophic level (measured as delta15N). These results reveal the importance of both biogeochemical and ecological factors in determining the bioavailability and trophic transfer of MeHg in estuarine food webs.

Predators reverse the direction of density dependence for juvenile salmon mortality.

The effect of predators on prey populations depends on how predator-caused mortality changes with prey population density. Predators can enforce density-dependent prey mortality and contribute to population stability, but only if they have a positive numerical or behavioral response to increased prey density. Otherwise, predator saturation can result in inversely density-dependent mortality, destabilizing prey populations and increasing extinction risk. Juvenile salmon and trout provide some of the clearest empirical examples of density-dependent mortality in animal populations. However, although juvenile salmon are very vulnerable to predators, the demographic effects of predators on juvenile salmon are unknown. We tested the interactive effects of predators and population density on the mortality of juvenile Atlantic salmon (Salmo salar) using controlled releases of salmon in natural streams. We introduced newly hatched juvenile salmon at three population density treatments in six study streams, half of which contained slimy sculpin (Cottus cognatus), a common generalist predator (18 release sites in total, repeated over two summers). Sculpin reversed the direction of density dependence for juvenile salmon mortality. Salmon mortality was density dependent in streams with no sculpin, but inversely density dependent in streams where sculpin were abundant. Such predator-mediated inverse density dependence is especially problematic for prey populations suppressed by other factors, thereby presenting a fundamental challenge to persistence of rare populations and restoration of extirpated populations.