Lisa D. Kraemer

Differentiating between direct (physiological) and food-chain mediated (bioenergetic) effects on fish in metal-impacted lakes

The objectives of this field project were to test relationships between the physiological and population status of indigenous fish and (a) ecological factors (habitat quality, food resources), (b) toxicological factors (ambient and tissue metal concentrations), and (c) metal detoxification factors (metallothionein induction and subcellular metal partitioning). The sentinel species, yellow perch (YP: Perca flavescens), was collected from lakes with contrasting metal levels located on the Canadian Precambrian Shield, downwind and downstream from metal smelters. In lakes at the high end of our exposure gradient, metals (Cu, Ni, and especially Cd) accumulate in YP to concentrations well above background tissue values; increases in tissue Zn concentrations were much more modest, despite the existence of a very marked gradient in ambient [Zn]. Metal accumulation in YP is accompanied by metallothionein induction, but all evidence to date suggests that metal detoxification by metallothionein is incomplete. Indeed, direct effects of metal toxicity are detected at multiple levels of biological organization, from effects at the cellular level, to effects in organs and tissues, to individuals and populations, in a pattern linked to accumulated metal concentrations (i.e., along the contamination gradient). In addition to direct or physiological effects, we also documented indirect, food-web-mediated effects of metals on YP in the most contaminated lakes. The most common indication of such indirect effects on YP is severely stunted growth coupled with a high degree of zooplankton dependence throughout their life.

Subcellular Distribution of Cadmium and Nickel in Chronically Exposed Wild Fish: Inferences Regarding Metal Detoxification Strategies and Implications for Setting Water Quality Guidelines for Dissolved Metals

ABSTRACT The objective of this study was to investigate metal detoxification in chronically exposed juvenile yellow perch (YP: Perca flavescens) and to field test the commonly assumed threshold toxicity model. Fish were collected from lakes located along a cadmium (Cd) and nickel (Ni) concentration gradient. Ambient dissolved metal concentrations were measured to evaluate exposure and total hepatic metal concentrations were determined as a measure of metal bioaccumulation. Hepatic metal partitioning among potentially metal-sensitive fractions (heat-denatured proteins, organelles) and detoxified metal fractions (metallothionein) was determined after differential centrifugation of YP liver homogenates. Major proportions of hepatic Cd were found in the heat-stable cytosolic peptides and proteins fraction (HSP; including metallothioneins), whereas Ni was mainly found in the potentially metal-sensitive heat-denaturable proteins fraction (HDP). For these chronically exposed fish there was no threshold exposure concentration below which binding of Cd or Ni to the heat-denaturable protein fraction or the organelle fraction did not occur. Metal detoxification was clearly incomplete and P. flavescens was subject to some metal-related stress, as evidenced notably by endocrine perturbations. Similar subcellular partitioning results were obtained when juvenile yellow perch were transferred from a reference lake to a Cd-contaminated lake and Cd accumulation was followed over time; there was no accumulation threshold below which Cd binding to the putative metal-sensitive fractions (HDP and organelles) did not occur. The presence of Cd and Ni in these fractions, even for low exposure concentrations and low hepatic accumulation, contradicts the threshold toxicity model that underpins metal toxicology theory and that is implicitly used in setting water quality guidelines for metals. Chronically exposed YP appear to have settled for a tradeoff between the cost of turning on their detoxification apparatus at full capacity, to completely suppress metal binding to metal-sensitive sites, and the alternative cost of allowing some binding of inappropriate metals to metal-sensitive sites.

The potential impact of climate on human exposure to contaminants in the Arctic

Abstract Many northern indigenous populations are exposed to elevated concentrations of contaminants through traditional food and many of these contaminants come from regions exterior to the Arctic. Global contaminant pathways include the atmosphere, ocean currents, and river outflow, all of which are affected by climate. In addition to these pathways, precipitation, animal availability, UV radiation, cryosphere degradation and human industrial activities in the North are also affected by climate change. The processes governing contaminant behaviour in both the physical and biological environment are complex and therefore, in order to understand how climate change will affect the exposure of northern people to contaminants, we must have a better understanding of the processes that influence how contaminants behave in the Arctic environment. Furthermore, to predict changes in contaminant levels, we need to first have a good understanding of current contaminant levels in the Arctic environment, biota and human populations. For this reason, it is critical that both spatial and temporal trends in contaminant levels are monitored in the environment, biota and human populations from all the Arctic regions. (Int J Circumpolar Health 2005; 64(5):498–508)

Uranium bioaccumulation in a freshwater ecosystem: impact of feeding ecology.

The objectives of our study were: (1) to determine if there was significant uranium (U) bioaccumulation in a lake that had been historically affected by a U mine and (2) to use a combined approach of gut content examination and stable nitrogen and carbon isotope analysis to determine if U bioaccumulation in fish was linked to foodweb ecology. We collected three species of fish: smallmouth bass (Micropterus dolomieu), yellow perch (Perca flavescens) and bluegill (Lepomis macrochirus), in addition to several invertebrate species including freshwater bivalves (family: Sphaeriidae), dragonfly nymphs (order: Odonata), snails (class: Gastropoda) and zooplankton (family: Daphniidae). Results showed significant U bioaccumulation in the lake impacted by historical mining activities. Uranium accumulation was 2-3 orders of magnitude higher in invertebrates than in the fish species. Within fish, U was measured in operculum (bone), liver and muscle tissue and accumulation followed the order: operculum>liver>muscle. There was a negative relationship between stable nitrogen ratios ((15)N/(14)N) and U bioaccumulation, suggesting U biodilution in the foodweb. Uranium bioaccumulation in all three tissues (bone, liver, muscle) varied among fish species in a consistent manner and followed the order: bluegill>yellow perch>smallmouth bass. Collectively, gut content and stable isotope analysis suggests that invertebrate-consuming fish species (i.e. bluegill) have the highest U levels, while fish species that were mainly piscivores (i.e. smallmouth bass) have the lowest U levels. Our study highlights the importance of understanding the feeding ecology of fish when trying to predict U accumulation.

Influence of body size on Cu bioaccumulation in zebra mussels Dreissena polymorpha exposed to different sources of particle-associated Cu

Size of organisms is critical in controlling metal bioavailability and bioaccumulation, while mechanisms of size-related metal bioaccumulation are not fully understood. To investigate the influences of different sources of particle-associated Cu on body size-related Cu bioavailability and bioaccumulation, zebra mussels (Dreissena polymorpha) of different sizes were exposed to stable Cu isotope ((65)Cu) spiked algae (Chlorella vulgaris) or sediments in the laboratory and the Cu tissue concentration-size relationships were compared with that in unexposed mussels. Copper tissue concentrations decreased with mussel size (tissue or shell dry weight) in both unexposed and algal-exposed mussels with similar decreasing patterns, but were independent of size in sediment-exposed mussels. Furthermore, the relative contribution of Cu uptake from algae (65-91%) to Cu bioaccumulation is always higher than that from sediments (9-35%), possibly due to the higher bioavailability of algal-Cu. Therefore, the size-related ingestion of algae could be more important in influencing the size-related variations in Cu bioaccumulation. However, the relative contribution of sediment-Cu to Cu bioaccumulation increased with body size and thus sediment ingestion may also affect the size-related Cu variations in larger mussels (tissue weight >7.5mg). This study highlights the importance of considering exposure pathways in normalization of metal concentration variation when using bivalves as biomonitors.

Effects of aging on the digestive solubilization of Cu from sediments.

Solubilization of particulate Cu by different solutions, mimicking digestive fluids of deposit-feeders, was quantified in stable isotope (65)Cu-spiked sediments (with 3 days-2 months Cu-sediment contact time or aging). Copper solubilization generally decreased with prolonged aging. However, such decrease became less evident after 1 month and equilibrium of Cu in sediments could be reached after 2 months. Aging effects on Cu solubilization can be explained by the changes in Cu geochemical fractionation with aging: Cu generally transferred from more mobile phases (carbonate and Fe-Mn associated) to more refractory phases (organic associated and residual phase). Besides Cu geochemical fractionation, digestive fluid composition and different Cu solubilization pathways involved, as well as sedimentary organic content, could all affect the digestive solubilization of Cu and its change with aging. Our results emphasize the necessity of considering Cu aging in laboratory sediment toxicity experiments, and in risk assessment of Cu contaminated sediments.

Influence of contact time and sediment composition on the bioavailability of Cd in sediments.

Stable isotope (111)Cd was spiked into sediments of different organic content levels for 3 days to 2 months. Bioavailability of spiked Cd to deposit-feeders, assessed by in vitro Cd solubilization, generally decreased with contact time but became comparable with that of background Cd after 2 months. This could be explained by the gradual transfer of Cd from the more mobile geochemical phase (carbonate associated phase) to more refractory phases (Fe-Mn oxide associated phase, and organic associated phase) within 2 months. The sedimentary organic content had a weak effect on Cd solubilization, while the distribution of Cd in carbonate or Fe-Mn oxide associated phase could have a larger influence on the solubilization of sedimentary Cd and its change with contact time. The observations in this study emphasize the need to consider Cd sequestration over time in sediments of various compositions, which would be useful in risk assessment of contaminated sediments.

The impacts of ontogenetic dietary shifts in yellow perch (Perca flavescens) on Zn and Hg accumulation.

Yellow perch (Perca flavescens) undergo several ontogenetic dietary shifts, and consequently these fish feed at different trophic levels and rely on different carbon sources over their lifetime. Stable isotope ratios of nitrogen (δ(15)N) and carbon (δ(13)C) are powerful ecological tools that are used to provide a temporally integrated description of the feeding ecology of aquatic animals such as fish. The main objective of this study was to use stable isotopes of nitrogen and carbon to determine if dietary changes affected mercury (Hg) and zinc (Zn) accumulation in yellow perch ranging in size from approximately 5 cm to 27 cm. Results showed that Hg bioaccumulation generally increased with increasing trophic level in fish feeding at higher trophic levels, however, the relationship between Hg levels and δ(15)N was non-linear showing no relationship in small fish (less than 15 cm). In contrast, there was a negative, linear relationship between δ(15)N and Zn, suggesting that as perch fed at progressively higher trophic levels, less of Zn bioaccumulated. No relationship was observed between δ(13)C and metal levels in perch. Collectively, these results demonstrate a contrast in the behavior of Zn and Hg bioaccumulation in yellow perch as a function of trophic status.

Temporal and spatial variation in Hg accumulation in zebra mussels (Dreissena polymorpha): Possible influences of DOC and diet

Zebra mussels (Dreissena polymorpha) are filter feeders located near the base of the foodweb and these animals are able to utilize a variety of carbon sources that may also vary seasonally. We conducted both a spatial and a temporal study in order to test the hypotheses: (1) dissolved organic carbon (DOC) concentrations influence Hg accumulation in zebra mussels sampled from a series of lakes and (2) seasonal variations in diet influence Hg accumulation. In the spatial study, we found a significant negative relationship between Hg concentrations and DOC concentrations, suggesting an influence of DOC on Hg bioaccumulation. In the temporal study, we used stable isotope ratios of nitrogen (δ(15)N) and carbon (δ(13)C) as ecological tools to provide a temporally integrated description of the feeding ecology of zebra mussels. Both δ(15)N and δ(13)C varied seasonally in a similar manner: more depleted values occurred in the summer and more enriched values occurred in the fall. Mercury concentrations also varied significantly over the year, with highest concentrations occurring in the summer, followed by a progressive decrease in concentrations into the fall. The C/N ratio of zebra mussels also varied significantly over the year with the lowest values occurring mid-summer and then values increased in the fall and winter, suggesting that there was significant variation in lipid stores. These results indicate that in addition to any effect of seasonal dietary changes, seasonal variation in energy stores also appeared to be related to Hg levels in the zebra mussels. Collectively results from this study suggest that DOC concentrations, seasonal variation in diet and seasonal depletion of energy stores are all important variables to consider when understanding Hg accumulation in zebra mussels.