Ecosystem responses to climate change at a Low Arctic and a High Arctic long-term research site.

Long-term measurements of ecological effects of warming are often not statistically significant because of annual variability or signal noise. These are reduced in indicators that filter or reduce the noise around the signal and allow effects of climate warming to emerge. In this way, certain indicators act as medium pass filters integrating the signal over years-to-decades. In the Alaskan Arctic, the 25-year record of warming of air temperature revealed no significant trend, yet environmental and ecological changes prove that warming is affecting the ecosystem. The useful indicators are deep permafrost temperatures, vegetation and shrub biomass, satellite measures of canopy reflectance (NDVI), and chemical measures of soil weathering. In contrast, the 18-year record in the Greenland Arctic revealed an extremely high summer air-warming of 1.3 °C/decade; the cover of some plant species increased while the cover of others decreased. Useful indicators of change are NDVI and the active layer thickness.

Microbes in nature are limited by carbon and energy: the starving-survival lifestyle in soil and consequences for estimating microbial rates.

Understanding microbial transformations in soils is important for predicting future carbon sequestration and nutrient cycling. This review questions some methods of assessing one key microbial process, the uptake of labile organic compounds. First, soil microbes have a starving-survival life style of dormancy, arrested activity, and low activity. Yet they are very abundant and remain poised to completely take up all substrates that become available. As a result, dilution assays with the addition of labeled substrates cannot be used. When labeled substrates are transformed into (14)CO2, the first part of the biphasic release follows metabolic rules and is not affected by the environment. As a consequence, when identical amounts of isotopically substrates are added to soils from different climate zones, the same percentage of the substrate is respired and the same half-life of the respired (14)CO2 from the labeled substrate is estimated. Second, when soils are sampled by a variety of methods from taking 10 cm diameter cores to millimeter-scale dialysis chambers, amino acids (and other organic compounds) appear to be released by the severing of fine roots and mycorrhizal networks as well as from pressing or centrifuging treatments. As a result of disturbance as well as of natural root release, concentrations of individual amino acids of ~10 µM are measured. This contrasts with concentrations of a few nanomolar found in aquatic systems and raises questions about possible differences in the bacterial strategy between aquatic and soil ecosystems. The small size of the hyphae (2-10 µm diameter) and of the fine roots (0.2-2 mm diameter), make it very difficult to sample any volume of soil without introducing artifacts. Third, when micromolar amounts of labeled amino acids are added to soil, some of the isotope enters plant roots. This may be an artifact of the high micromolar concentrations applied.

Salt marsh sediment diversity: a test of the variability of the rare biosphere among environmental replicates.

Much of the phylogenetic diversity in microbial systems arises from rare taxa that comprise the long tail of taxon rank distribution curves. This vast diversity presents a challenge to testing hypotheses about the effects of perturbations on microbial community composition because variability of rare taxa among environmental replicates may be sufficiently large that it would require a prohibitive degree of sequencing to discern differences between samples. In this study we used pyrosequencing of 16S rRNA tags to examine the diversity and within-site variability of salt marsh sediment bacteria. Our goal was to determine whether pyrosequencing could produce similar patterns in community composition among replicate environmental samples from the same location. We hypothesized that repeated sampling from the same location would produce different snapshots of the rare community due to incomplete sequencing of the taxonomically rich rare biosphere. We demonstrate that the salt marsh sediments we sampled contain a remarkably diverse array of bacterial taxa and, in contrast to our hypothesis, repeated sampling from within the same site produces reliably similar patterns in bacterial community composition, even among rare organisms. These results demonstrate that deep sequencing of 16s tags is well suited to distinguish site-specific similarities and differences among rare taxa and is a valuable tool for hypothesis testing in microbial ecology.

Changes in tundra pond limnology: re-sampling Alaskan ponds after 40 years.

The arctic tundra ponds at the International Biological Program (IBP) site in Barrow, AK, were studied extensively in the 1970s; however, very little aquatic research has been conducted there for over three decades. Due to the rapid climate changes already occurring in northern Alaska, identifying any changes in the ponds' structure and function over the past 30-40 years can help identify any potential climate-related impacts. Current research on the IBP ponds has revealed significant changes in the physical, chemical, and biological characteristics of these ponds over time. These changes include increased water temperatures, increased water column nutrient concentrations, the presence of at least one new chironomid species, and increased macrophyte cover. However, we have also observed significant annual variation in many measured variables and caution that this variation must be taken into account when attempting to make statements about longer-term change. The Barrow IBP tundra ponds represent one of the very few locations in the Arctic where long-term data are available on freshwater ecosystem structure and function. Continued monitoring and protection of these invaluable sites is required to help understand the implications of climate change on freshwater ecosystems in the Arctic.

Multi-decadal changes in tundra environments and ecosystems: synthesis of the International Polar Year-Back to the Future project (IPY-BTF).

Understanding the responses of tundra systems to global change has global implications. Most tundra regions lack sustained environmental monitoring and one of the only ways to document multi-decadal change is to resample historic research sites. The International Polar Year (IPY) provided a unique opportunity for such research through the Back to the Future (BTF) project (IPY project #512). This article synthesizes the results from 13 papers within this Ambio Special Issue. Abiotic changes include glacial recession in the Altai Mountains, Russia; increased snow depth and hardness, permafrost warming, and increased growing season length in sub-arctic Sweden; drying of ponds in Greenland; increased nutrient availability in Alaskan tundra ponds, and warming at most locations studied. Biotic changes ranged from relatively minor plant community change at two sites in Greenland to moderate change in the Yukon, and to dramatic increases in shrub and tree density on Herschel Island, and in subarctic Sweden. The population of geese tripled at one site in northeast Greenland where biomass in non-grazed plots doubled. A model parameterized using results from a BTF study forecasts substantial declines in all snowbeds and increases in shrub tundra on Niwot Ridge, Colorado over the next century. In general, results support and provide improved capacities for validating experimental manipulation, remote sensing, and modeling studies.

Microbial community composition in sediments resists perturbation by nutrient enrichment.

Functional redundancy in bacterial communities is expected to allow microbial assemblages to survive perturbation by allowing continuity in function despite compositional changes in communities. Recent evidence suggests, however, that microbial communities change both composition and function as a result of disturbance. We present evidence for a third response: resistance. We examined microbial community response to perturbation caused by nutrient enrichment in salt marsh sediments using deep pyrosequencing of 16S rRNA and functional gene microarrays targeting the nirS gene. Composition of the microbial community, as demonstrated by both genes, was unaffected by significant variations in external nutrient supply in our sampling locations, despite demonstrable and diverse nutrient-induced changes in many aspects of marsh ecology. The lack of response to external forcing demonstrates a remarkable uncoupling between microbial composition and ecosystem-level biogeochemical processes and suggests that sediment microbial communities are able to resist some forms of perturbation.

Processing arctic eddy-flux data using a simple carbon-exchange model embedded in the ensemble Kalman filter.

Continuous time-series estimates of net ecosystem carbon exchange (NEE) are routinely made using eddy covariance techniques. Identifying and compensating for errors in the NEE time series can be automated using a signal processing filter like the ensemble Kalman filter (EnKF). The EnKF compares each measurement in the time series to a model prediction and updates the NEE estimate by weighting the measurement and model prediction relative to a specified measurement error estimate and an estimate of the model-prediction error that is continuously updated based on model predictions of earlier measurements in the time series. Because of the covariance among model variables, the EnKF can also update estimates of variables for which there is no direct measurement. The resulting estimates evolve through time, enabling the EnKF to be used to estimate dynamic variables like changes in leaf phenology. The evolving estimates can also serve as a means to test the embedded model and reconcile persistent deviations between observations and model predictions. We embedded a simple arctic NEE model into the EnKF and filtered data from an eddy covariance tower located in tussock tundra on the northern foothills of the Brooks Range in northern Alaska, USA. The model predicts NEE based only on leaf area, irradiance, and temperature and has been well corroborated for all the major vegetation types in the Low Arctic using chamber-based data. This is the first application of the model to eddy covariance data. We modified the EnKF by adding an adaptive noise estimator that provides a feedback between persistent model data deviations and the noise added to the ensemble of Monte Carlo simulations in the EnKF. We also ran the EnKF with both a specified leaf-area trajectory and with the EnKF sequentially recalibrating leaf-area estimates to compensate for persistent model-data deviations. When used together, adaptive noise estimation and sequential recalibration substantially improved filter performance, but it did not improve performance when used individually. The EnKF estimates of leaf area followed the expected springtime canopy phenology. However, there were also diel fluctuations in the leaf-area estimates; these are a clear indication of a model deficiency possibly related to vapor pressure effects on canopy conductance.

Salt marsh sediment bacteria: their distribution and response to external nutrient inputs.

A primary focus among microbial ecologists in recent years has been to understand controls on the distribution of microorganisms in various habitats. Much less attention has been paid to the way that environmental disturbance interacts with processes that regulate bacterial community composition. We determined how human disturbance affected the distribution and community structure of salt marsh sediment bacteria by using denaturing gradient gel electrophoresis of 16S rRNA in five different habitats in each of four salt marshes located in northeastern Massachusetts, USA. Two of the four marsh creeks were experimentally enriched 15 x above background by the addition of nitrogen and phosphorus fertilizers for two or more growing seasons. Our results indicate that extrinsic factors acting at broad scales do not influence the distribution of salt marsh sediment bacteria. Intrinsic factors, controlled by local-scale environmental heterogeneity, do play a role in structuring these sediment microbial communities, although nutrient enrichment did not have a consequential effect on the microbial community in most marsh habitats. Only in one habitat, a region of the marsh creek wall that is heavily colonized by filamentous algae, did we see any effect of fertilization on the microbial community structure. When similar habitats were compared among marshes, there was considerable convergence in the microbial community composition during the growing season. Environmental factors that correlated best with microbial community composition varied with habitat, suggesting that habitat-specific intrinsic forces are primarily responsible for maintaining microbial diversity in salt marsh sediments.

Mycorrhizal fungi supply nitrogen to host plants in Arctic tundra and boreal forests: 15N is the key signal.

Symbiotic fungi's role in providing nitrogen to host plants is well-studied in tundra at Toolik Lake, Alaska, but little-studied in the adjoining boreal forest ecosystem. Along a 570 km north-south transect from the Yukon River to the North Slope of Alaska, the 15N content was strongly reduced in ectomycorrhizal and ericoid mycorrhizal plants including Betula, Salix, Picea mariana (P. Mill.) B.S.P., Picea glauca Moench (Voss), and ericaceous plants. Compared with the 15N content of soil, the foliage of nonmycorrhizal plants (Carex and Eriophorum) was unchanged, whereas content of the ectomycorrhizal fungi was very much higher (e.g., Boletaceae, Leccinum and Cortinarius). It is hypothesized that similar processes operate in tundra and boreal forest, both nitrogen-limited ecosystems: (i) mycorrhizal fungi break down soil polymers and take up amino acids or other nitrogen compounds; (ii) mycorrhizal fungi fractionate against 15N during production of transfer compounds; (iii) host plants are accordingly depleted in 15N; and (iv) mycorrhizal fungi are enriched in 15N. Increased N availability for plant roots or decreased light availability to understory plants may have decreased N allocation to mycorrhizal partners and increased delta15N by 3-4 parts per million for southern populations of Vaccinium vitis-idaea L. and Salix. Fungal biomass, measured as ergosterol, correlated strongly with soil organic matter and attained amounts similar to those in temperate forest soils.

Biogeography of bacterioplankton in lakes and streams of an Arctic tundra catchment.

Bacterioplankton community composition was compared across 10 lakes and 14 streams within the catchment of Toolik Lake, a tundra lake in Arctic Alaska, during seven surveys conducted over three years using denaturing gradient gel electrophoresis (DGGE) of PCR-amplified rDNA. Bacterioplankton communities in streams draining tundra were very different than those in streams draining lakes. Communities in streams draining lakes were similar to communities in lakes. In a connected series of lakes and streams, the stream communities changed with distance from the upstream lake and with changes in water chemistry, suggesting inoculation and dilution with bacteria from soil waters or hyporheic zones. In the same system, lakes shared similar bacterioplankton communities (78% similar) that shifted gradually down the catchment. In contrast, unconnected lakes contained somewhat different communities (67% similar). We found evidence that dispersal influences bacterioplankton communities via advection and dilution (mass effects) in streams, and via inoculation and subsequent growth in lakes. The spatial pattern of bacterioplankton community composition was strongly influenced by interactions among soil water, stream, and lake environments. Our results reveal large differences in lake-specific and stream-specific bacterial community composition over restricted spatial scales (<10 km) and suggest that geographic distance and connectivity influence the distribution of bacterioplankton communities across a landscape.

15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra.

When soil nitrogen is in short supply, most terrestrial plants form symbioses with fungi (mycorrhizae): hyphae take up soil nitrogen, transport it into plant roots, and receive plant sugars in return. In ecosystems, the transfers within the pathway fractionate nitrogen isotopes so that the natural abundance of 15N in fungi differs from that in their host plants by as much as 12% per hundred. Here we present a new method to quantify carbon and nitrogen fluxes in the symbiosis based on the fractionation against 15N during transfer of nitrogen from fungi to plant roots. We tested this method, which is based on the mass balance of 15N, with data from arctic Alaska where the nitrogen cycle is well studied. Mycorrhizal fungi provided 61-86% of the nitrogen in plants; plants provided 8-17% of their photosynthetic carbon to the fungi for growth and respiration. This method of analysis avoids the disturbance of the soil-microbe-root relationship caused by collecting samples, mixing the soil, or changing substrate concentrations. This analytical technique also can be applied to other nitrogen-limited ecosystems, such as many temperate and boreal forests, to quantify the importance for terrestrial carbon and nitrogen cycling of nutrient transfers mediated by mycorrhizae at the plant-soil interface.

Climate impacts on arctic freshwater ecosystems and fisheries: background, rationale and approach of the Arctic Climate Impact Assessment (ACIA).

Changes in climate and ultraviolet radiation levels in the Arctic will have far-reaching impacts, affecting aquatic species at various trophic levels, the physical and chemical environment that makes up their habitat, and the processes that act on and within freshwater ecosystems. Interactions of climatic variables, such as temperature and precipitation, with freshwater ecosystems are highly complex and can propagate through the ecosystem in ways that are difficult to project. This is partly due to a poor understanding of arctic freshwater systems and their basic interrelationships with climate and other environmental variables, and partly due to a paucity of long-term freshwater monitoring sites and integrated hydro-ecological research programs in the Arctic. The papers in this special issue are an abstraction of the analyses performed by 25 international experts and their associated networks on Arctic freshwater hydrology and related aquatic ecosystems that was initially published by the Arctic Climate Impact Assessment (ACIA) in 2005 as "Chapter 8--Freshwater Ecosystems and Fisheries". The papers provide a broad overview of the general hydrological and ecological features of the various freshwater ecosystems in the Arctic, including descriptions of each ACIA region, followed by a review of historical changes in freshwater systems during the Holocene. This is followed by an assessment of the effects of climate change on broad-scale hydro-ecology; aquatic biota and ecosystem structure and function; and arctic fish and fisheries. Potential synergistic and cumulative effects are also discussed, as are the roles of ultraviolet radiation and contaminants. The nature and complexity of many of the effects are illustrated using case studies from around the circumpolar north, together with a discussion of important threshold responses (i.e., those that produce stepwise and/or nonlinear effects). The issue concludes with summary the key findings, a list of gaps in scientific understanding, and policy-related recommendations.

General features of the arctic relevant to climate change in freshwater ecosystems.

Large variations exist in the size, abundance and biota of the two principal categories of freshwater ecosystems, lotic (flowing water; e.g., rivers, streams, deltas and estuaries) and lentic (standing water; lakes, ponds and wetlands) found across the circumpolar Arctic. Arctic climate, many components of which exhibit strong variations along latitudinal gradients, directly affects a range of physical, chemical and biological processes in these aquatic systems. Furthermore, arctic climate creates additional indirect ecological effects through the control of terrestrial hydrologic systems and processes, particularly those associated with cryospheric components such as permafrost, freshwater ice and snow accumulation/ablation. The ecological structure and function of arctic freshwater systems are also controlled by external processes and conditions, particularly those in the headwaters of the major arctic rivers and in the adjacent marine environment. The movement of physical, chemical and biotic components through the interlinked lentic and lotic freshwater systems are major determinants of arctic freshwater ecology.

Historical changes in arctic freshwater ecosystems.

Various types of ecosystem-based climate proxies have been used to assess past arctic change. Although lotic records are relatively poor because of the constant reworking of riverine material, high-quality lentic data have been assembled back to the end of the Pleistocene and deglaciation of the circumpolar Arctic. In general, climatic variations in the Holocene, partly due to changes in the shrinking effect of glacier coverage, produced significant temporal and spatial variations in arctic hydrology and freshwater ecosystems. Of particular note were the vast expansions of northern peatlands during major protracted periods of wetting. More recent lake biota and sedimentiological data reflect the general warming trend that has occurred over the last one to two centuries and indicate major changes to freshwater characteristics such as ice-cover duration and thermal stratification. Such data provide an excellent baseline against which future effects of climate change can be both projected and measured.

Climate change effects on hydroecology of arctic freshwater ecosystems.

In general, the arctic freshwater-terrestrial system will warm more rapidly than the global average, particularly during the autumn and winter season. The decline or loss of many cryospheric components and a shift from a nival to an increasingly pluvial system will produce numerous physical effects on freshwater ecosystems. Of particular note will be reductions in the dominance of the spring freshet and changes in the intensity of river-ice breakup. Increased evaporation/evapotranspiration due to longer ice-free seasons, higher air/water temperatures and greater transpiring vegetation along with increase infiltration because of permafrost thaw will decrease surface water levels and coverage. Loss of ice and permafrost, increased water temperatures and vegetation shifts will alter water chemistry, the general result being an increase in lotic and lentic productivity. Changes in ice and water flow/levels will lead to regime-specific increases and decreases in habitat availability/quality across the circumpolar Arctic.

Climate change effects on aquatic biota, ecosystem structure and function.

Climate change is projected to cause significant alterations to aquatic biogeochemical processes, (including carbon dynamics), aquatic food web structure, dynamics and biodiversity, primary and secondary production; and, affect the range, distribution and habitat quality/quantity of aquatic mammals and waterfowl. Projected enhanced permafrost thawing is very likely to increase nutrient, sediment, and carbon loadings to aquatic systems, resulting in both positive and negative effects on freshwater chemistry. Nutrient and carbon enrichment will enhance nutrient cycling and productivity, and alter the generation and consumption of carbon-based trace gases. Consequently, the status of aquatic ecosystems as carbon sinks or sources is very likely to change. Climate change will also very likely affect the biodiversity of freshwater ecosystems across most of the Arctic. The magnitude, extent, and duration of the impacts and responses will be system- and location-dependent. Projected effects on aquatic mammals and waterfowl include altered migration routes and timing; a possible increase in the incidence of mortality and decreased growth and productivity from disease and/or parasites; and, probable changes in habitat suitability and timing of availability.

Effects of ultraviolet radiation and contaminant-related stressors on arctic freshwater ecosystems.

Climate change is likely to act as a multiple stressor, leading to cumulative and/or synergistic impacts on aquatic systems. Projected increases in temperature and corresponding alterations in precipitation regimes will enhance contaminant influxes to aquatic systems, and independently increase the susceptibility of aquatic organisms to contaminant exposure and effects. The consequences for the biota will in most cases be additive (cumulative) and multiplicative (synergistic). The overall result will be higher contaminant loads and biomagnification in aquatic ecosystems. Changes in stratospheric ozone and corresponding ultraviolet radiation regimes are also expected to produce cumulative and/or synergistic effects on aquatic ecosystem structure and function. Reduced ice cover is likely to have a much greater effect on underwater UV radiation exposure than the projected levels of stratospheric ozone depletion. A major increase in UV radiation levels will cause enhanced damage to organisms (biomolecular, cellular, and physiological damage, and alterations in species composition). Allocations of energy and resources by aquatic biota to UV radiation protection will increase, probably decreasing trophic-level productivity. Elemental fluxes will increase via photochemical pathways.

Molecular characterization of sulfate-reducing bacteria in a New England salt marsh.

Sulfate reduction, mediated by sulfate-reducing bacteria (SRB), is the dominant remineralization pathway in sediments of New England salt marshes. High sulfate reduction rates are associated with the rhizosphere of Spartina alterniflora when plants elongate aboveground. The growth process concurrently produces significant amounts of new rhizome material belowground and the plants leak dissolved organic compounds. This study investigated the diversity of SRB in a salt marsh over an annual growth cycle of S. alterniflora by exploring the diversity of a functional gene, dissimilatory sulfite reductase (dsrAB). Because the dsrAB gene is a key gene in the anaerobic sulfate-respiration pathway, it allows the identification of microorganisms responsible for sulfate reduction. Conserved dsrAB primers in polymerase chain reaction (PCR) generated full-length dsrAB amplicons for cloning and DNA sequence analysis. Nearly 80% of 380 clone sequences were similar to genes from Desulfosarcina and Desulfobacterium species within Desulfobacteraceae. This reinforces the hypothesis that complete oxidizers with high substrate versatility dominate the marsh. However, the phylotypes formed several clades that were distinct from cultured representatives, indicating a greater diversity of SRB than previously appreciated. Several dsrAB sequences were related to homologues from gram-positive, thermophilic and non-thermophilic Desulfotomaculum species. One dsrAB lineage formed a sister group to cultured members of the delta-proteobacterial group Syntrophobacteraceae. A deeply branching dsrAB lineage was not affiliated with genes from any cultured SRB. The sequence data from this study will allow for the design of probes or primers that can quantitatively assess the diverse range of sulfate reducers present in the environment.

High overall diversity and dominance of microdiverse relationships in salt marsh sulphate-reducing bacteria.

The biogeochemistry of North Atlantic salt marshes is characterized by the interplay between the marsh grass Spartina and sulphate-reducing bacteria (SRB), which mineralize the diverse carbon substrates provided by the plants. It was hypothesized that SRB populations display high diversity within the sediment as a result of the rich spatial and chemical structuring provided by Spartina roots. A 2000-member 16S rRNA gene library, prepared with delta-proteobacterial SRB-selective primers, was analysed for diversity patterns and phylogenetic relationships. Sequence clustering detected 348 16S rRNA sequence types (ribotypes) related to delta-proteobacterial SRB, and it was estimated that a total of 623 ribotypes were present in the library. Similarity clustering showed that approximately 46% of these sequences fell into groups with < 1% divergence; thus, microheterogeneity accounts for a large portion of the observable genetic diversity. Phylogenetic comparison revealed that sequences most frequently recovered were associated with the Desulfobacteriaceae and Desulfobulbaceae families. Sequences from the Desulfovibrionaceae family were also observed, but were infrequent. Over 80% of the delta-proteobacterial ribotypes clustered with cultured representatives of Desulfosarcina, Desulfococcus and Desulfobacterium genera, suggesting that complete oxidizers with high substrate versatility dominate. The large-scale approach demonstrates the co-existence of numerous SRB-like sequences and reveals an unexpected amount of microdiversity.