Thomas H. Suchanek

Carbon Dioxide Exchange Between an Old-growth Forest and the Atmosphere

Eddy-covariance and biometeorological methods show significant net annual carbon uptake in an old-growth Douglas-fir forest in southwestern Washington, USA. These results contrast with previous assumptions that old-growth forest ecosystems are in carbon equilibrium. The basis for differences between conventional biomass-based carbon sequestration estimates and the biometeorologic estimates are discussed. Annual net ecosystem exchange was comparable to younger ecosystems at the same latitude, as quantified in the AmeriFlux program. Net ecosystem carbon uptake was significantly correlated with photosynthetically active radiation and air temperature, as well as soil moisture and precipitation. Optimum ecosystem photosynthesis occurred at relatively cool temperatures (5°–10°C). Understory and soil carbon exchange always represented a source of carbon to the atmosphere, with a strong seasonal cycle in source strength. Understory and soil carbon exchange showed a Q10 temperature dependence and represented a substantial portion of the ecosystem carbon budget. The period of main carbon uptake and the period of soil and ecosystem respiration are out of phase, however, and driven by different climatic boundary conditions. The period of strongest ecosystem carbon uptake coincides with the lowest observed values of soil and ecosystem respiration. Despite the substantial contribution of soil, the overall strength of the photosynthetic sink resulted in the net annual uptake. The net uptake estimates here included two correction methods, one for advection and the other for low levels of turbulence.

Net Ecosystem Exchanges of Carbon, Water, and Energy in Young and Old-growth Douglas-Fir Forests

To be able to estimate the cumulative carbon budget at broader scales, it is essential to understand net ecosystem exchanges (NEE) of carbon and water in various ages and types of ecosystems. Using eddy-covariance (EC) in Douglas-fir dominated forests in the Wind River Valley, Washington, USA, we measured NEE of carbon, water, and energy from July through September in a 40-year-old stand (40YR) in 1998, a 20-year-old stand (20YR) in 1999, and a 450-year-old stand (450YR) during both years. All three stands were net carbon sinks during the dry, warm summers, with mean net daily accumulation of –0.30 g C m−2 d−1, –2.76 g C m−2 d−1, and –0.38 g C m−2 d−1, respectively, in the 20YR, 40YR, and 450YR (average of 1998, 1999) stands; but for individual years, the 450YR stand was a carbon source in 1998 (0.51 g C m−2 d−1) and a sink in 1999 (–1.26 g C m−2 d−1). The interannual differences for the summer months were apparent for cumulative carbon exchange at the 450YR stand, which had 46.9 g C m−2 loss in 1998 and 115.9 g C m−2 gain in 1999. As predicted, the 40YR stand assimilated the most carbon and lost the least amount of water to the atmosphere through evapotranspiration.

MERCURY TROPHIC TRANSFER IN A EUTROPHIC LAKE: THE IMPORTANCE OF HABITAT‐SPECIFIC FORAGING

Mercury (Hg) trophic transfer and bioaccumulation in fish from a mine-impacted, eutrophic lake were examined in relation to foraging habitat, trophic position, and size. Diet analysis indicated that there were clear ontogenetic shifts in foraging habitats and trophic position. Pelagic diet decreased and benthic diet increased with increasing fish length in bluegill, black crappie, inland silverside, and largemouth bass, whereas there was no shift for prickly sculpin or threadfin shad. Stable carbon isotope values (delta13C) were inversely related to the proportion of pelagic prey items in the diet, but there was no clear relationship with benthic foraging. There were distinct differences between pelagic and benthic prey basal delta13C values, with a range of approximately -28 per thousand in pelagic zooplankton to approximately -20 per thousand in benthic caddisflies. Profundal prey such as chironomid larvae had intermediate delta13C values of approximately -24 per thousand, reflecting the influence of pelagic detrital subsidies and suppressing the propagation of the benthic carbon isotope signal up the food chain. Fish total mercury (TotHg) concentrations varied with habitat-specific foraging, trophic position, and size; however, the relationships differed among species and ages. When controlling for the effects of species, length, and trophic position, TotHg and delta13C were positively correlated, indicating that Hg trophic transfer is linked to benthic foraging. When examined on a species-specific basis, TotHg was positively correlated with delta13C only for bluegill, largemouth bass, and threadfin shad. However, diet-based multiple regression analyses suggested that TotHg also increased with benthic foraging for inland silverside and black crappie. In both species, benthic prey items were dominated by chironomid larvae, explaining the discrepancy with delta13C. These results illustrate the importance of foraging habitat to Hg bioaccumulation and indicate that pelagic carbon can strongly subsidize the basal energy sources of benthic organisms.

CHANGES IN FISH DIETS AND FOOD WEB MERCURY BIOACCUMULATION INDUCED BY AN INVASIVE PLANKTIVOROUS FISH

The invasion, boom, collapse, and reestablishment of a population of the planktivorous threadfin shad in Clear Lake, California, USA, were documented over a 20-year period, as were the effects of changing shad populations on diet and mercury (Hg) bioaccumulation in nearshore fishes. Threadfin shad competitively displaced other planktivorous fish in the lake, such as inland silversides, young-of-year (YOY) largemouth bass, and YOY bluegill, by reducing zooplankton abundance. As a result, all three species shifted from a diet that was dominated by zooplankton to one that was almost entirely zoobenthos. Stable carbon isotopes corroborated this pattern with each species becoming enriched in delta13C, which is elevated in benthic vs. pelagic organisms. Concomitant with these changes, Hg concentrations increased by approximately 50% in all three species. In contrast, obligate benthivores such as prickly sculpin showed no relationship between diet or delta13C and the presence of threadfin shad, suggesting that effects of the shad were not strongly linked to the benthic fish community. There were also no changes in Hg concentrations of prickly sculpin. The temporary extirpation of threadfin shad from the lake resulted in zooplankton densities, foraging patterns, isotope ratios, and Hg concentrations in pelagic fishes returning to pre-shad values. These results indicate that even transient perturbations of the structure of freshwater food webs can result in significant alterations in the bioaccumulation of Hg and that food webs in lakes can be highly resilient.

REDISTRIBUTION OF MERCURY FROM CONTAMINATED LAKE SEDIMENTS OF CLEAR LAKE, CALIFORNIA

Mining operations conducted at the Sulphur Bank Mercury Mine at Clear Lake, California, from 1872–1957, together with acid mine drainage since abandonment, deposited ca. 100 metric tons of mercury (Hg) in the sediments of Clear Lake. In 1992 Hg in surficial sediments (up to 183 mg kg-1 total Hg and 15.9 μg kg-1 methyl Hg) exhibited a classic point source distribution with maximum concentrations adjacent to the mine. However, the ratio of methyl:total Hg in sediments increased with distance from the mine, suggesting either differential transport of methyl Hg or a non-linear relationship between sediment inorganic Hg concentrations and methylation. Water exhibited an even more gradual decline in total Hg concentrations with distance from the mine, in both unfiltered bottom water (max. ca. 70 ng L-1) and filtered surface water (max. ca. 7 ng L-1). In comparison with other studies, Clear Lake exhibits high total Hg in sediment and water, yet relatively low methyl Hg concentrations. Our findings indicate a non-linearity between total and methyl Hg concentrations in sediments. The ratio of methyl:inorganic Hg is approximately 2 orders of magnitude higher in the water column than in the sediments, making the methyl fraction much more available for down-gradient transport away from the mine. Particulate Hg comprises ca. 33–94% of the total Hg and ca. 25–78% of the methyl Hg in the water column. Geothermal springs do not appear to represent a significant source of Hg to Clear Lake. The present pattern of Hg distribution in Clear Lake shows that water column transport plays some role in the lake-wide contamination of methyl Hg, but high methylation at relatively low inorganic Hg concentrations cannot be ruled out. No quantitative estimate of the area of sediments requiring remediation is possible from these descriptive data alone.

THE BASIS FOR ECOTOXICOLOGICAL CONCERN IN AQUATIC ECOSYSTEMS CONTAMINATED BY HISTORICAL MERCURY MINING

The Coast Range of California is one of five global regions that dominated historical production of mercury (Hg) until declining demand led to the economic collapse of the Hg-mining industry in the United States. Calcines, waste rock, and contaminated alluvium from inactive mine sites can release Hg (including methylmercury, MeHg) to the environment for decades to centuries after mining has ceased. Soils, water, and sediment near mines often contain high concentrations of total Hg (TotHg), and an understanding of the biogeochemical transformations, transport, and bioaccumulation of this toxic metal is needed to assess effects of these contaminated environments on humans and wildlife. We briefly review the environmental behavior and effects of Hg, providing a prelude to the subsequent papers in this Special Issue. Clear Lake is a northern California lake contaminated by wastes from the abandoned Sulphur Bank Mercury Mine, a U.S. Environmental Protection Agency Superfund Site. The primary toxicological problem with Hg in aquatic ecosystems is biotic exposure to MeHg, a highly toxic compound that readily bioaccumulates. Processes that affect the abundance of MeHg (including methylation and demethylation) strongly affect its concentration in all trophic levels of aquatic food webs. MeHg can biomagnify to high concentrations in aquatic food webs, and consumption of fish is the primary pathway for human exposure. Fish consumption advisories have been issued for many North American waters, including Clear Lake and other mine-impacted waters in California, as a means of decreasing MeHg exposure. Concerns about MeHg exposure in humans focus largely on developmental neurotoxicity to the fetus and children. Aquatic food webs are also an important pathway for MeHg exposure of wildlife, which can accumulate high, sometimes harmful, concentrations. In birds, wild mammals, and humans, MeHg readily passes to the developing egg, embryo, or fetus, life stages that are much more sensitive than the adult. The papers in this issue examine the origin, transport, transformations, bioaccumulation, and trophic transfer of Hg in Clear Lake, assess its potential effects on biota and humans, and provide information relevant to remediation of mine-impacted aquatic ecosystems.

THE LEGACY OF MERCURY CYCLING FROM MINING SOURCES IN AN AQUATIC ECOSYSTEM: FROM ORE TO ORGANISM

Clear Lake is the site of an abandoned mercury (Hg) mine (active intermittently from 1873 to 1957), now a U.S. Environmental Protection Agency Superfund Site. Mining activities, including bulldozing waste rock and tailings into the lake, resulted in approximately 100 Mg of Hg entering the lakes ecosystem. This series of papers represents the culmination of approximately 15 years of Hg-related studies on this ecosystem, following Hg from the ore body to the highest trophic levels. A series of physical, chemical, biological, and limnological studies elucidate how ongoing Hg loading to the lake is influenced by acid mine drainage and how wind-driven currents and baroclinic circulation patterns redistribute Hg throughout the lake. Methylmercury (MeHg) production in this system is controlled by both sulfate-reducing bacteria as well as newly identified iron-reducing bacteria. Sediment cores (dated with dichlorodiphenyldichlorethane [DDD], 210pb, and 14C) to approximately 250 cm depth (representing up to approximately 3000 years before present) elucidate a record of total Hg (TotHg) loading to the lake from natural sources and mining and demonstrate how MeHg remains stable at depth within the sediment column for decades to millenia. Core data also identify other stresses that have influenced the Clear Lake Basin especially over the past 150 years. Although Clear Lake is one of the most Hg-contaminated lakes in the world, biota do not exhibit MeHg concentrations as high as would be predicted based on the gross level of Hg loading. We compare Clear Lakes TotHg and MeHg concentrations with other sites worldwide and suggest several hypotheses to explain why this discrepancy exists. Based on our data, together with state and federal water and sediment quality criteria, we predict potential resulting environmental and human health effects and provide data that can assist remediation efforts.

IS CLEAR LAKE METHYLMERCURY DISTRIBUTION DECOUPLED FROM BULK MERCURY LOADING

Clear Lake is the site of the abandoned Sulphur Bank Mercury Mine, active periodically from 1873 to 1957, resulting in approximately 100 Mg of mercury (Hg) being deposited into the lakes ecosystem. Concentrations of total (primarily inorganic) Hg (TotHg) in Clear Lake are some of the highest reported worldwide for sediments (up to 4.4 x 10(5) ng/g [ppb dry mass]) and water (up to 4 x 10(-1) microg/L [= ppb]). However, the ratio of methylmercury (MeHg) to TotHg at Clear Lake indicates that the methylation process is mostly decoupled from bulk inorganic Hg loading, with Hg in lower trophic level biota significantly less than anticipated compared with other Hg-contaminated sites worldwide. This may be due to several factors, including: (1) reduced bioavailability of Hg derived from the mine (i.e., cinnabar, metacinnabar, and corderoite), (2) the alkaline nature of the lake water, (3) the shallow depth of the lake, which prevents stratification and subsequent methylation in a stratified hypolimnion, and (4) possible dilution of MeHg by a highly productive system. However, while bulk inorganic Hg loading to the lake may not contribute significantly to the bioaccumulation of Hg, acid mine drainage (AMD) from the mine likely promotes Hg methylation by sulfate-reducing and iron-reducing bacteria, making AMD a vehicle for the production of highly bioavailable Hg. If Clear Lake were deeper, less productive, or less alkaline, biota would likely contain much more MeHg than they do presently. Comparisons of MeHg:TotHg ratios in sediments, water, and biota from sites worldwide suggest that the highest production of MeHg may be found at sites influenced by chloralkali plants, followed by sites influenced by gold and silver mines, with the lowest production of MeHg observed at cinnabar and metacinnabar Hg mines. These data also suggest that the total maximum daily load (TMDL) process for Hg at Clear Lake, as currently implemented to reduce contamination in fishes for the protection of wildlife and humans, may be flawed because the metric used to implement Hg load reduction (i.e., TotHg) is not directly proportional to the critical form of Hg that is being bioaccumulated (i.e., MeHg).

Monitoring Inter-Annual Variability Reveals Sources Of Mercury Contamination In Clear Lake, California

Mercury (Hg) in the aquatic ecosystem of Clear Lake has been documented since the 1970s when fishes were found to have elevated levels of toxic methyl mercury (meHg). Mining practices at the Sulphur Bank Mercury Mine (active intermittently from 1872–1957) along the shoreline of Clear Lake included the bulldozing of waste rock and overburden ore into the shallow nearshore regions of the lake and the creation of steeply sloped piles of waste rock at the waters edge. This process, plus erosion of the waste rock piles, resulted in the accumulation of an estimated 100 metric tons of Hg in Clear Lake. A monitoring program to assess Hg in Clear Lake was established in 1992, and conducted continuously from 1994. Drought conditions in California had persisted for ca. 6 yrs prior to 1992, when the U.S. Environmental Protection Agency (USEPA) remediated the steeply sloped eroding waste rock piles, which appeared to reduce sediment Hg concentrations significantly. In April 1995, a white flocculent material was observed in Clear Lake adjacent to the mine and has been observed every year since, leading to the discovery of ongoing acid mine drainage (AMD), low pH fluids high in Hg and extremely high in sulfate. AMD is now believed to be the most likely cause of elevated meHg in Clear Lake. The discovery of this source of meHg production in Clear Lake, which will significantly influence remedial options, was only made possible by implementation of a diligent monitoring program.

MINE-DERIVED MERCURY: EFFECTS ON LOWER TROPHIC SPECIES IN CLEAR LAKE, CALIFORNIA

Considerable ecological research on mercury (Hg) has focused on higher trophic level species (e.g., fishes and birds), but less on lower trophic species. Clear Lake, site of the abandoned Sulphur Bank Mercury Mine, provides a unique opportunity to study a system influenced by mine-derived Hg. An exponentially decreasing gradient of total Hg (TotHg) away from the mine allowed us to evaluate Hg bioaccumulation in planktonic and benthic invertebrates and evaluate population- and community-level parameters that might be influenced by Hg. Studies from 1992-1998 demonstrated that TotHg in lower trophic species typically decreased exponentially away from the mine, similar to trends observed in water and sediments. However, a significant amount of invertebrate TotHg (approximately 60% for sediment-dwelling chironomid insect larvae) likely derives from Hg-laden particles in their guts. Spatially, whole-body methylmercury (MeHg) did not typically exhibit a significant decrease with increasing distance from the mine. Temporally, TotHg concentrations in plankton and chironomids did not exhibit any short-term (seasonal or annual) or long-term (multiyear) trends. Methylmercury, however, was elevated during late summer/fall in both plankton and chironomids, but it exhibited no long-term increase or decrease during this study. Although data from a 50-yr monitoring program for benthic chaoborid and chironomid larvae documented significant population fluctuations, they did not demonstrate population-level trends with respect to Hg concentrations. Littoral invertebrates also exhibited no detectable population- or community-level trends associated with the steep Hg gradient. Although sediment TotHg concentrations (1-1200 mg/kg dry mass) exceed sediment quality guidelines by up to 7000 times, it is notable that no population- or community-level effects were detected for benthic and planktonic taxa. In comparison with other sites worldwide, Clear Lakes lower trophic species typically have significantly higher TotHg concentrations, but comparable or lower MeHg concentrations, which may be responsible for the discrepancy between highly elevated TotHg concentrations and the general lack of observed population- or community-level effects. These data suggest that MeHg, as well as TotHg, should be used when establishing sediment quality guidelines. In addition, site-specific criteria should be established using the observed relationship between MeHg and observed ecological responses.