Paleo-ecotoxicology: What Can Lake Sediments Tell Us about Ecosystem Responses to Environmental Pollutants?

The development of effective risk reduction strategies for aquatic pollutants requires a comprehensive understanding of toxic impacts on ecosystems. Classical toxicological studies are effective for characterizing pollutant impacts on biota in a controlled, simplified environment. Nonetheless, it is well-acknowledged that predictions based on the results of these studies must be tested over the long-term in a natural ecosystem setting to account for increased complexity and multiple stressors. Paleolimnology (the study of lake sediment cores to reconstruct environmental change) can address many key knowledge gaps. When used as part of a weight-of-evidence framework with more traditional approaches in ecotoxicology, it can facilitate rapid advances in our understanding of the chronic effects of pollutants on ecosystems in an environmentally realistic, multistressor context. Paleolimnology played a central role in the Acid Rain debates, as it was instrumental in demonstrating industrial emissions caused acidification of lakes and associated ecosystem-wide impacts. "Resurrection Ecology" (hatching dormant resting eggs deposited in the past) records evolutionary responses of populations to chronic pollutant exposure. With recent technological advances (e.g., geochemistry, genomic approaches), combined with an emerging paleo-ecotoxicological framework that leverages strengths across multiple disciplines, paleolimnology will continue to provide valuable insights into the most pressing questions in ecotoxicology.

Multi-trophic level response to extreme metal contamination from gold mining in a subarctic lake.

Giant Mine, located in the city of Yellowknife (Northwest Territories, Canada), is a dramatic example of subarctic legacy contamination from mining activities, with remediation costs projected to exceed $1 billion. Operational between 1948 and 2004, gold extraction at Giant Mine released large quantities of arsenic and metals from the roasting of arsenopyrite ore. We examined the long-term ecological effects of roaster emissions on Pocket Lake, a small lake at the edge of the Giant Mine lease boundary, using a spectrum of palaeoenvironmental approaches. A dated sedimentary profile tracked striking increases (approx. 1700%) in arsenic concentrations coeval with the initiation of Giant Mine operations. Large increases in mercury, antimony and lead also occurred. Synchronous changes in biological indicator assemblages from multiple aquatic trophic levels, in both benthic and pelagic habitats, indicate dramatic ecological responses to extreme metal(loid) contamination. At the peak of contamination, all Cladocera, a keystone group of primary consumers, as well as all planktonic diatoms, were functionally lost from the sediment record. No biological recovery has been inferred, despite the fact that the bulk of metal(loid) emissions occurred more than 50 years ago, and the cessation of all ore-roasting activities in Yellowknife in 1999.

The jellification of north temperate lakes.

Calcium (Ca) concentrations are decreasing in softwater lakes across eastern North America and western Europe. Using long-term contemporary and palaeo-environmental field data, we show that this is precipitating a dramatic change in Canadian lakes: the replacement of previously dominant pelagic herbivores (Ca-rich Daphnia species) by Holopedium glacialis, a jelly-clad, Ca-poor competitor. In some lakes, this transformation is being facilitated by increases in macro-invertebrate predation, both from native (Chaoborus spp.) and introduced (Bythotrephes longimanus) zooplanktivores, to which Holopedium, with its jelly coat, is relatively invulnerable. Greater representation by Holopedium within cladoceran zooplankton communities will reduce nutrient transfer through food webs, given their lower phosphorus content relative to daphniids, and greater absolute abundances may pose long-term problems to water users. The dominance of jelly-clad zooplankton will likely persist while lakewater Ca levels remain low.

Anomalous rise in algal production linked to lakewater calcium decline through food web interactions.

Increased algal blooms are a threat to aquatic ecosystems worldwide, although the combined effects of multiple stressors make it difficult to determine the underlying causes. We explore whether changes in trophic interactions in response to declining calcium (Ca) concentrations, a water quality issue only recently recognized in Europe and North America, can be linked with unexplained bloom production. Using a palaeolimnological approach analysing the remains of Cladocera (herbivorous grazers) and visual reflectance spectroscopically inferred chlorophyll a from the sediments of a Nova Scotia (Canada) lake, we show that a keystone grazer, Daphnia, declined in the early 1990s and was replaced by a less effective grazer, Bosmina, while inferred chlorophyll a levels tripled at constant total phosphorus (TP) concentrations. The decline in Daphnia cannot be attributed to changes in pH, thermal stratification or predation, but instead is linked to declining lakewater [Ca]. The consistency in the timing of changes in Daphnia and inferred chlorophyll a suggests top-down control on algal production, providing, to our knowledge, the first evidence of a link between lakewater [Ca] decline and elevated algal production mediated through the effects of [Ca] decline on Daphnia. [Ca] decline has severe implications for whole-lake food webs, and presents yet another mechanism for potential increases in algal blooms.

Impacts on aquatic biota from salinization and metalloid contamination by gold mine tailings in sub-Arctic lakes.

Precious metal mining activities have left complex environmental legacies in lakes around the world, including some sites in climatically sensitive regions of the Canadian sub-Arctic. Here, we examined the long-term impacts of past regional gold mining activities on sub-Arctic lakes near Con Mine (Yellowknife, Northwest Territories) based on sediment core analysis (paleolimnology). In addition to receiving metal(loid)s from roaster stack emissions, the study lakes were also influenced by salt-rich mine drainage from Con Mine tailings. Water samples from these lakes had some of the highest concentrations for salinity-related variables (e.g. Ca2+, Cl-, Na+) and metal(loid)s (e.g. As, Cu, Ni, Sb) in the Yellowknife area. Furthermore, the presence of halophilic diatom (Bacillariophyceae) taxa (Achnanthes thermalis and Navicula incertata) in the recent sediments of Keg and Peg lakes suggest that the extreme saline conditions are strongly influencing the present biota, more than 10 years after the cessation of gold mining activities at Con Mine. The sedimentary metal(loid) profiles (e.g. As, Cu, Ni) of Kam Lake tracked the influence of regional gold mining activities, particularly those at Con Mine, while the algal assemblages recorded the biological responses to salinization and metal(loid) pollution (e.g. marked decreases in diatom species richness, Hill's N2 diversity, and chrysophyte cyst:diatom valve ratio). At Kam Lake, the algal assemblage changes in the post-mining era were indicative of climate-mediated changes to lake thermal properties (e.g. rise in planktonic diatoms), nutrient enrichment related to urbanization (e.g. increase in eutrophic Stephanodisucs taxa), and/or a combination of both stressors. The lack of biological recovery (i.e. return to pre-mining assemblages) is consistent with investigations of mine-impacted lakes in temperate regions where elevated contaminant levels and emerging stressors (e.g. climate warming, land-use changes) are influencing lake recovery.

Determining the effects of past gold mining using a sediment palaeotoxicity model.

Ore processing techniques used in Yellowknife's largest mining operation, Giant Mine, is responsible for the atmospheric release of approximately 20,000 t of particulate arsenic trioxide and other heavy metal(loids). This rapid deposition of heavy metal(loids) may have caused ecological disturbances to aquatic food webs. Here we use 210Pb and 137Cs dated lake sediment cores from 20 lakes within a 40 km radius of Yellowknife to examine the spatial-temporal distribution of arsenic, antimony and lead. Further, we model the toxicity of the sediment to aquatic biota pre-, during, and post-mining using palaeotoxicity modelling, enrichment factor assessment, and comparisons to national sediment quality guidelines. We found that metal(loid) profiles in sediment peaked during the height of mining operations. These peak metal(loid) concentrations were highest in lakes near the mine's roaster stack, and decreased with distance from the historic mine. Palaeotoxicity modelling of lake sediment archives indicate that there is no significant difference in the mean predicted toxicity of pre- and post-mining samples (p = 0.14), however mining activities in the region significantly increased the predicted toxicity of sediments to aquatic organisms during mining operations (p < 0.001). In the years since roasting processes ceased, the mean palaeotoxicity of all lakes has decreased significantly (p < 0.05), indicating a projected pattern of biological recovery. Importantly, some lakes remain at an elevated risk, indicating that aquatic ecosystems in Yellowknife may continue to have lingering effects on aquatic biota despite the closure of the mine two decades ago.

Identifying novel treeline biomarkers in lake sediments using an untargeted screening approach.

Paleolimnology uses sedimentary biomarkers as proxies to reconstruct long-term changes in environmental conditions from lake sediment cores. This work describes an untargeted metabolomics-based approach and uniquely applies it to the field of paleolimnology to identify novel sediment biomarkers to track long-term patterns in treeline dynamics. We identified new potential biomarkers across the Canadian northern Arctic, non-alpine, treeline using high-resolution accurate mass spectrometry, and pattern recognition analysis. This method was applied to 120 sediment core extracts from 14 boreal, 25 forest-tundra, and 21 tundra lakes to assess long-term fluctuations in treeline position. High resolution accurate mass spectrometry resolved many compounds from complex mixtures with low mass accuracy errors. This generated a large dataset that required metabolomics styled statistical analyses to identify potential biomarkers. In total, 29 potential biomarkers discriminated between boreal and tundra lakes. Tetrapyrrole-type phorbides and squalene derivatives dominated in boreal regions, while biohopane-type lipids were in the tundra regions. Tetrapyrroles were in both surface and subsurface sediments of boreal lakes indicating these compounds can survive long-term burial in sediments. At the ecozone level, tetrapyrroles were more abundant in boreal Taiga Shield, and Taiga Plains. Boreal plant extracts belonging to Pinaceae and Ericaceae also contained tetrapyrroles. Squalene derivatives demonstrated long-term preservation, but wider distribution than tetrapyrroles. Hopanoids were present in tundra and forest-tundra lake regions, specifically the Low Arctic and Taiga Shield, and were absent in all boreal lake sediments. Herein, we describe a method that can systematically identify new paleolimnological biomarkers. Novel biomarkers would facilitate multi-proxy paleolimnological studies and potentially lead to more accurate paleoenvironmental reconstructions.

Trends in historical mercury deposition inferred from lake sediment cores across a climate gradient in the Canadian High Arctic.

Recent climate change may be enhancing mercury fluxes to Arctic lake sediments, confounding the use of sediment cores to reconstruct histories of atmospheric deposition. Assessing the independent effects of climate warming on mercury sequestration is challenging due to temporal overlap between warming temperatures and increased long-range transport of atmospheric mercury following the Industrial Revolution. We address this challenge by examining mercury trends in short cores (the last several hundred years) from eight lakes centered on Cape Herschel (Canadian High Arctic) that span a gradient in microclimates, including two lakes that have not yet been significantly altered by climate warming due to continued ice cover. Previous research on subfossil diatoms and inferred primary production indicated the timing of limnological responses to climate warming, which, due to prevailing ice cover conditions, varied from ∼1850 to ∼1990 for lakes that have undergone changes. We show that climate warming may have enhanced mercury deposition to lake sediments in one lake (Moraine Pond), while another (West Lake) showed a strong signal of post-industrial mercury enrichment without any corresponding limnological changes associated with warming. Our results provide insights into the role of climate warming and organic carbon cycling as drivers of mercury deposition to Arctic lake sediments.

Comparative histories of polycyclic aromatic compound accumulation in lake sediments near petroleum operations in western Canada.

We examined the historical deposition of polycyclic aromatic compounds (PACs) recorded in radiometrically-dated lake sediment cores from a small, conventional oil and gas operation in the southern Northwest Territories (Cameron Hills), and placed these results in the context of previously published work from three other important regions of western Canada: (1) the Athabasca oil sands region in Alberta; (2) Cold Lake, Alberta; and (3) the Mackenzie Delta, NT. Sediment PAC records from the Cameron Hills showed no clear changes in either source or concentrations coincident with the timing of development in these regions. Changes were small in comparison to the clear increases in both parent and alkyl-substituted PACs in response to industrial development from the Athabasca region surface mining of oil sands, where parent PAC diagnostic ratios indicated a shift from pyrogenic sources (primarily wood and coal burning) in pre-development sediments to more petrogenically-sourced PACs in modern sediments. Cores near in-situ oil sand extraction operations showed only modest increases in PAC deposition. This work directly compares the history and trajectory of contamination in lake ecosystems in areas of western Canada impacted by the most common types of hydrocarbon extraction activities, and provides a context for assessing the environmental impacts of oil and gas development in the future.

Broad-scale lake expansion and flooding inundates essential wood bison habitat.

Understanding the interaction between the response of a complex ecosystem to climate change and the protection of vulnerable wildlife species is essential for conservation efforts. In the Northwest Territories (Canada), the recent movement of the Mackenzie wood bison herd (Bison bison athabascae) out of their designated territory has been postulated as a response to the loss of essential habitat following regional lake expansion. We show that the proportion of this landscape occupied by water doubled since 1986 and the timing of lake expansion corresponds to bison movements out of the Mackenzie Bison Sanctuary. Historical reconstructions using proxy data in dated sediment cores show that the scale of recent lake expansion is unmatched over at least the last several hundred years. We conclude that recent lake expansion represents a fundamental alteration of the structure and function of this ecosystem and its use by Mackenzie wood bison, in response to climate change.

In-situ bitumen extraction associated with increased petrogenic polycyclic aromatic compounds in lake sediments from the Cold Lake heavy oil fields (Alberta, Canada).

Most future growth in the Alberta bituminous sands will be based on thermal in-situ recovery technologies. To date, however, most attention on the environmental effects of bitumen recovery has focused on surface mining in the Athabasca region. Recent uncontrolled bitumen flow-to-surface incidents (FTS; appearance at the surface of bitumen emulsions from deep subsurface recovery zones) reported at the Cold Lake heavy oil fields highlight the need to better understand the potential role of in-situ extraction as a source of contaminants to landscapes and surface waters. We analyzed sediment cores from a lake located ∼2 km away from a recent bitumen FTS incident to provide a long-term perspective on the delivery of metals, polycyclic aromatic compounds (PACs), and polychlorinated biphenyls (PCBs) to surface freshwaters, and to assess whether the onset of local in-situ bitumen extraction can be linked to contaminant increases in nearby lakes. An increase in alkyl PACs coincided with the onset and expansion of commercial in-situ bitumen extraction, and multiple lines of evidence indicate a petrogenic source for recent alkyl PAC enrichment. However, no coincident increase in vanadium (enriched in bitumen) occurred that would suggest the source of petrogenic PAC enrichment is direct input of bituminous particles. Our results show that, similar to surface mining in the Athabasca region, activities associated with in-situ extraction can increase the burden of petrogenic PACs in nearby lakes, but many questions still remain regarding the exact sources and pathways of PACs into the environment. Given that more than 80% of Alberta's bitumen reserves can only be accessed using in-situ technologies, we recommend that this be made a research priority.

Assessing the contribution of combustion-derived contaminants to a remote subarctic environment from traffic on the Tibbitt to Contwoyto winter road (Northwest Territories, Canada).

Remote mining operations in Canada's Northwest Territories and Nunavut are supported by a 600 km winter road, which spans the transition from subarctic boreal forest in Yellowknife to low Arctic tundra. Each year, thousands of truckloads of fuel, large equipment, and other heavy loads are hauled up the winter road. We investigated whether diesel emissions from commercial truck traffic is a major source of metals and polycyclic aromatic compounds (PACs) to aquatic ecosystems along the winter road. In March 2014, at the end of the hauling season, we collected integrated snow samples, water, and sediment from nine lakes located along the winter road, as well as from six lakes located within the city of Yellowknife. Examination of PAC composition and diagnostic ratios in snow samples showed that wildfires are an important source of PACs to lakes along the winter road, while anthropogenic sources are more prevalent in snow from Yellowknife lakes. Concentrations of PACs, including those associated with diesel emissions, were variable in snow, water, and sediment across all sites. The highest concentrations of PACs in snow were reported in winter road lakes located in the subarctic boreal forest, where forest fires are common. No compositional differences were observed for PACs in sediment and water samples between Yellowknife and winter road lakes. We did not observe any evidence of metal contamination in snow collected along the winter road, and metal concentrations in snow from winter road sites were consistently lower than Yellowknife sites. Our results show that a high contribution of PACs from natural sources can obscure potential contributions from diesel traffic emissions along the winter road.

Exploratory hydrocarbon drilling impacts to Arctic lake ecosystems.

Recent attention regarding the impacts of oil and gas development and exploitation has focused on the unintentional release of hydrocarbons into the environment, whilst the potential negative effects of other possible avenues of environmental contamination are less well documented. In the hydrocarbon-rich and ecologically sensitive Mackenzie Delta region (NT, Canada), saline wastes associated with hydrocarbon exploration have typically been disposed of in drilling sumps (i.e., large pits excavated into the permafrost) that were believed to be a permanent containment solution. However, failure of permafrost as a waste containment medium may cause impacts to lakes in this sensitive environment. Here, we examine the effects of degrading drilling sumps on water quality by combining paleolimnological approaches with the analysis of an extensive present-day water chemistry dataset. This dataset includes lakes believed to have been impacted by saline drilling fluids leaching from drilling sumps, lakes with no visible disturbances, and lakes impacted by significant, naturally occurring permafrost thaw in the form of retrogressive thaw slumps. We show that lakes impacted by compromised drilling sumps have significantly elevated lakewater conductivity levels compared to control sites. Chloride levels are particularly elevated in sump-impacted lakes relative to all other lakes included in the survey. Paleolimnological analyses showed that invertebrate assemblages appear to have responded to the leaching of drilling wastes by a discernible increase in a taxon known to be tolerant of elevated conductivity coincident with the timing of sump construction. This suggests construction and abandonment techniques at, or soon after, sump establishment may result in impacts to downstream aquatic ecosystems. With hydrocarbon development in the north predicted to expand in the coming decades, the use of sumps must be examined in light of the threat of accelerated permafrost thaw, and the potential for these industrial wastes to impact sensitive Arctic ecosystems.