Shrub expansion in tundra ecosystems: dynamics, impacts and research priorities

Temperature limits both the reproduction and growth of shrub species in tundra ecosystems. Growing season temperatures are increasing in northern North America and northwestern Russia [12, 61, 62], and, concurrent with this, the conditions for recruitment and growth of shrub species are also likely changing. Observations of low pollen or seed viability in populations of alder (Alnus viridis subsp. fruticosa), dwarf birch (Betula glandulosa) and willows (Salix spp.) near their range limits suggest that temperature limitation of reproduction may determine the northern extent of many shrubs in the low Arctic [16, 50, 63]. Studies of age distributions of shrub species in tundra ecosystems indicate that recruitment has increased in recent years at sites in the western North American and European Arctic [16, 25, 27, 64]. However, there are currently few studies that link warming and new recruitment to shrub increase in tundra ecosystems.

Several recent studies have documented significant positive correlations between ring widths or shoot lengths and early and mid growing season temperatures for some of the most common tall [23, 25, 27, 34, 65] and dwarf [66–70] shrub species found in tundra ecosystems. In some studies, winter temperatures and snow have been found to correlate with growth in the following summer [27, 71–73]. Snow melt timing determines the length of the growing season and the snowpack provides protection from frost damage during the winter and spring [74–76]. These analyses suggest that warmer conditions are likely to promote shrub growth either directly by altering physiological processes or indirectly by enhancing soil microbial activities that supply nutrients for shrub uptake, as long as other factors are not limiting [77]. Also, increased summer temperatures are often accompanied by greater summer moisture deficits, which could offset the expected growth increase created by higher summer temperature alone, as has been observed in boreal trees [78].

Tundra disturbances caused by fire, permafrost degradation, stream channels, animal burrowing or trampling, or human activities create and maintain microsites where tall shrubs can establish and remain dominant for decades to centuries. Recent evidence indicates that many of these disturbances, such as fire [4, 79] and permafrost degradation [3, 80–84], are increasing in high-latitude ecosystems. Increased abundance and growth of tall shrubs on thaw slumps [17], drained lake basins [85], pingos [18], tundra fires [16], vehicle tracks [86] and drilling mud sumps [87] suggest that increases in natural and anthropogenic disturbance could be contributing to increased shrub abundance and distribution.

In the low Arctic, disturbances that expose mineral soils and deepen active layers show rapid changes in functional group abundance, and after several decades are typically dominated by tall shrubs [16, 17, 87, 88]. In the short-term, landscape and soil disturbances are likely to stimulate more rapid recruitment than warming alone [16, 17]. The rate of shrub expansion on recently burned tundra sites is twice as fast as on comparable undisturbed surfaces (Lantz et al unpubl. data). Caribou and other animal species can create disturbances by trampling ground cover [89], creating trails that erode soils resulting in either damaged biomass and reduced shrub cover or the provision of sites for the recruitment of shrub seedlings [90]. Soil disturbances could also be a precondition for shrubs to take advantage of improved climate conditions and increase in abundance across the landscape. In contrast, in some ecosystems, landscape disturbances can also reduce shrub abundance. Decreases in shrub cover were observed in northwestern Arctic Russia where willows failed to regenerate in vehicle tracks two decades after the initial disturbance, due to the development of a graminoid-dominated sward [91]. Landscape-scale fires have set back potential shrub increase in Australian alpine areas for 5–20 yr, except in burn scars where species are able to re-sprout [92]. In addition, permafrost degradation of ice-rich palsas in northeast Siberia has resulted in dieback of large Betula nana patches and a conversion to graminoid cover (figure 2). Thus, future disturbances and recovery after disturbance in tundra ecosystems could lead to both increases and decreases in shrub abundance.

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Herbivores can reduce the survival of shrubs and limit or reduce shrub patch expansion, as shown by enclosure and exclosure experiments [54, 93]. Animals such as sheep, reindeer, muskoxen, lemmings, ptarmigan, moose and hares have been shown to decrease tundra tree and shrub abundance and canopy structure in Scandinavia, Greenland and Alaska [54, 55, 93–96]. However, current knowledge of the influence of different herbivores on seedling recruitment is limited, and little is known about the influence of insect herbivory and seed predation.

The influence of herbivory on shrub abundance in tundra ecosystems will depend on the size and density of the herbivore populations, intensity of grazing, palatability of the shrub species, and plant and herbivore phenologies [95]. Wild herbivores can migrate over large areas and exhibit cyclic population dynamics; therefore the influence of herbivory on shrub populations will likely change over time and space [5]. Shrub abundance has been reduced by mammalian herbivores in low Arctic Greenland [93] and Norway [96], while no evidence of reduction in shrub expansion by mammalian herbivores was found on the Arctic coast of the Yukon [19].

In tundra ecosystems, the dominant herbivores can be either wild or domesticated. In Fennoscandia and Siberia, land use is dominated by extensive grazing by reindeer and sheep, and this has strongly influenced the abundance of woody species in tundra environments [23, 54, 96, 97]. In northern Scandinavia, herbivory by sheep or reindeer is thought to be the primary factor determining the elevational position of the treeline ecotone [94, 95, 98], and declined use of pastures has resulted in increases in shrubs in the Alps [28]. Herbivores can also influence seed production and seedbed size [89, 99], transport seeds [100] and fertilize soils, which can in turn alter recruitment, dispersal, growth and potential rates of shrub increase.

Tundra shrubs can significantly influence the exchange of energy among the atmosphere, vegetation and soils [101–103]. With an increasing canopy height and density, a higher fraction of the incoming shortwave radiation is absorbed by the canopy and less is reflected to the atmosphere and, therefore, albedo decreases [12, 104–106]. Lower spring and summer albedo has been observed over shrub versus shrub-free tundra in Arctic Alaska [12, 105], alpine areas of the Yukon Territory [102], upland tundra north of Inuvik, NWT (Lantz et al unpubl. data) and across the tundra biome [105]. Shrub expansion can therefore significantly alter the interaction of the atmosphere with vegetation, soil and permafrost through changes in energy fluxes.

Shrub canopies and snow cover interact to influence soil and permafrost temperatures. Tundra shrubs can significantly modify the accumulation, timing and physical characteristics of snow, thereby influencing the exchanges of energy and moisture between terrestrial ecosystems and the atmosphere [101–103]. In winter, snow cover protects plant buds and tissue from the effects of extreme cold [74, 75]. Shrubs trap snow, leading to localized increases in snowpack, and also reducing the thermal conductivity of the snowpack by preventing the formation of highly conductive wind-compacted snow layers [110]. As a consequence, winter soil temperatures can be up to 30 °C warmer than air temperatures under shrub canopies [108], whereas soil temperatures may be almost equal to air temperatures in adjacent shrub-free sites [25]. The effect of tall shrubs on snow trapping and albedo can also be moderated by shrubs bending and being buried in the snowpack under the weight of snow [102–104]. In spring, snow melt is first accelerated as a result of the lowered albedo around shrub branches that protrude above the snowpack, but subsequent shading by shrub canopies may promote longer duration snow patches [103, 107, 109]. In summer, shading under shrub canopies decreases soil temperatures [103] and active layer depths [107]. Removal of the Betula nana shrub canopy in experimental plots in Siberia resulted in greater active layer depths due the loss of soil shading, despite the increase in surface albedo accompanying shrub removal [107]. Near surface soil temperatures under shrub canopies were found to be ∼2 °C cooler in summer and ∼5 °C warmer in winter in an experimental canopy manipulation conducted in alpine tundra of the Kluane Region [25]. The results of these studies suggest that both the summer soil cooling effect of shading and the winter soil warming effect of snow trapping must be considered to determine the year-round effect of changes in shrub cover on soil temperatures and permafrost conditions.

Interactions between the abiotic and biotic influences of shrub canopies can alter tundra nutrient cycling. Fertilization experiments show that vascular plant productivity is nutrient limited in tundra ecosystems, as demonstrated by an increase in shrub biomass after nitrogen and phosphorus fertilization [6, 9, 111, 112]. Increases in canopy cover and height of shrub species can increase litter inputs to soils [113], nitrogen mineralization rates [114] and the amount of carbon stored in above and below ground biomass [9]. Although deciduous shrub species produce more litter than other tundra species, this litter is relatively recalcitrant; thus, increases in shrubs could reduce overall decomposition rates in tundra soils [113]. In winter, snow trapped by shrub canopies insulates soils and has been hypothesized to increase decomposition and nutrient release [108]. Experimental manipulations demonstrate that greater snow depth and warmer winter soils under shrub canopies can increase litter decomposition [115] and nitrogen cycling [114, 116–119]. Recent work at Toolik Lake, Alaska showed a positive effect of winter snow addition on summer, but not winter, nitrogen mineralization rates [120]; however, there have not been experimental tests of the influence of summer canopy shading on nutrient cycling and decomposition rates. Carbon dioxide and methane fluxes are likely also altered by shrub canopies. Differences in growing season carbon dioxide effluxes were not explained by the presence of a half-meter-tall willow canopy in alpine tundra in the Kluane region, Yukon Territory [25]. However, increased evapotranspiration from greater shrub biomass could dry soils, and has been suggested to reduce methane emissions and increase carbon dioxide fluxes in areas with expanding shrub cover [121]. This same mechanism of soil drying from increased evapotranspiration when combined with the greater fuel load in shrub tundra could result in increased frequency and intensity of tundra fires with increases in shrubs [48].

Increases in shrub abundance could have negative effects on tundra species richness, through the loss of shade-intolerant species under shrub canopies [122]. At tundra sites in northwestern Fennoscandia and the Yamal Peninsula in Russia, the species richness of vegetation declined with increasing shrub height and cover [122]. The richness of herbaceous species decreased significantly over 20 yr with increasing dwarf shrub cover on an Arctic mountainside in northern Sweden [123]. Fewer species and lower biomass of tundra plants, excluding tall shrub canopies, were found in shrub versus adjacent shrub-free plots in alpine tundra of the Kluane Region in the Yukon Territory [25]. The loss of particular species or functional groups may have implications for tundra food webs and ecosystem services. Lichens have been shown to decline with increases in shrub cover [8, 124, 125]. As important forage species, lichen decline could negatively impact caribou and reindeer populations, and thus influence hunting or herding activities. Increased shrub cover could also reduce moss biomass, which is an important soil insulator. Thus, the loss of the moss layer may alter soil temperatures, active layer depths, and rates of soil decomposition [126]. Willows are an important forage species for caribou, moose, ptarmigan and other wildlife species [55, 127, 128], and either increases or decreases in willow cover may influence the populations of these species. In addition to the potential impacts on biodiversity, ecosystem function and wildlife, altered vegetation structure in tundra ecosystems might influence human access to traditional travel routes, berry harvesting, reindeer herding or hunting of wildlife species.

Our review highlights the growing number of observations of shrub increase around the circumpolar Arctic and in high-latitude and alpine tundra ecosystems (figure 2 and table 1); however, the differences in species specific responses to warming have yet to be adequately quantified within and between sites. The International Tundra Experiment (ITEX) tested the response of tundra plots to warming across the Arctic [129, 130]; however, warming experiments with larger plots encompassing larger statured shrub species have only been conducted at a few locations [9, 111, 131]. Understanding the key differences among shrub species responses to climate warming could improve predictions of vegetation change across the Arctic. Birch has been the focus of many experimental field studies [6, 50, 58, 107], but the potential responses of willow, alder and other shrub species to changes in environmental conditions are less well characterized. Furthermore, a whole host of species-level interactions may determine future shrub distributions, with, for example, caribou preferentially browsing willow over birch or alder, birch roots forming an association with an ectomycorrhizal fungal partner, or alder forming a symbiosis with nitrogen-fixing bacteria. Species-level studies are urgently required to evaluate and interpret current patterns of shrub change, as well as to predict future change.

Many of the observations of increasing shrubs are from discrete locations, and variation in rate of shrub change is seldom quantified across the landscape (figure 2 and table 1). Studies that have conducted landscape-level analyses of shrub change find both increasing and more stable patches sometimes located in close proximity [15, 132]. Tall shrubs generally occur in patches across the tundra landscape where conditions favor enhanced nutrient cycling and productivity, such as areas of preferential water flow, or areas where snow accumulates and protects the shoots from winter damage [15]. Topography therefore is likely to be an important constraint on the potential for increased shrub growth and expansion as the climate warms. Thus, landscape-scale studies are required to parameterize realistic models of shrub proliferation and close examination of the current patterns of shrub expansion for key species in relation to local hydrology and wind protection are needed. New applications of remote sensing to measure shrub distributions and changes in shrub cover and associated ecosystem processes in greater detail over large areas will facilitate these avenues of research.

Much of the current research on shrub expansion focuses on the factors that control shrub growth (figure 2 and table 1), and only a few studies have addressed changes in recruitment of shrub species [16, 17, 99]. Since shifts in abundance and range expansions will be mediated primarily by the establishment of new individuals, future research should focus on the factors controlling pollination, germination, recruitment and survival. The interactions between warming, disturbance and increased recruitment of shrub species should also be further explored so that we can better project future shrub increase. Seed viability experiments, demographic studies of shrub populations and experimental studies of seedling establishment would all contribute to our understanding of shrub recruitment in tundra ecosystems.

A growing number of studies have identified increases in shrub cover at low Arctic sites, but few have investigated change at the range edge of shrub species (figure 2 and table 1). Many tundra shrub species have very large geographic ranges, and at higher latitudes these species have a more diminutive growth form with lower canopy heights and reduced ground cover [26]. Little is known about whether individuals growing at the range edge have the ability to form larger more dominant canopies if growing conditions improve. The current size and growth form of northern or high-elevation populations of tall shrub species may represent genetically-based local adaptation to extremely harsh growing conditions. The ITEX experiments [129, 130] examined phenological variation in rates of plant growth between warmed and control plots. Common garden experiments or reciprocal transplants [133, 134] have tested how individuals from different sites at different latitudes grow under the same conditions. However, further work exploring phenotypic plasticity, local adaptation and latitudinal clines in size and fecundity should be conducted to improve our understanding of future shrub change at the range edge of tundra shrub species.

Feedbacks of shrub expansion to abiotic processes remain poorly understood (figure 3). Several studies have proposed hypotheses and experimentally tested ecosystem impacts of increasing shrub cover (table 2); however, studies that integrate processes across the entire year have yet to be conducted. Winter biological processes were initially hypothesized to create positive feedbacks to future shrub encroachment [108, 109]; however, recent studies have also highlighted the importance of the summer season [25, 107]. Further observational and experimental work is required to answer questions, such as what the overall effect is of shrubs on soil nutrient availability, integrating the influence of soil temperatures in the summer, winter and shoulder seasons.

The influence of shrub canopies on ground shading, snow depth, soil temperatures and biological processes varies with the cover, height, density and structure of the shrub canopy [135, 136], but additional research is required to characterize the nature of these linear or non-linear relationships. For example, we do not yet know whether shrub expansion is accelerated by positive feedbacks involving snow cover and thickness, surface albedo and atmospheric heating. Nor do we know whether the strength of these potential feedbacks varies with shrub density, cover and canopy height. Future investigations using canopy removals, artificial canopies and other experimental techniques across variation in shrub cover, density and canopy heights will improve our understanding of the relative balance of positive and negative feedbacks to shrub encroachment.