Ecological Response to Permafrost Thaw and Consequences for Local and Global Ecosystem Services

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Annual Review of Ecology, Evolution, and Systematics Ecological Response to Permafrost Thaw and Consequences for Local and Global Ecosystem Services

Edward A.G. Schuur and Michelle C. Mack

Center for Ecosystem Science and Society, and Department of Biological Sciences, Northern Arizona University, Flagstaff, Arizona 86011, USA; email: [email protected]

Annu. Rev. Ecol. Evol. Syst. 2018. 49:279–301 Keywords The Annual Review of Ecology, Evolution, and carbon, nutrient, climate, vegetation change, disturbance, Arctic Systematics is online at ecolsys.annualreviews.org ecosystem, boreal ecosystem https://doi.org/10.1146/annurev-ecolsys-121415- 032349 Abstract Copyright c 2018 by Annual Reviews. The Arctic may seem remote, but the unprecedented environmental changes All rights reserved occurring there have important consequences for global society. Of all Arc- tic system components, changes in permafrost (perennially frozen ground) are one of the least documented. Permafrost is degrading as a result of cli- Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org mate warming, and evidence is mounting that changing permafrost will have signiﬁcant impacts within and outside the region. This review asks: What are key structural and functional properties of ecosystems that interact with changing permafrost, and how do these ecosystem changes affect local and global society? Here, we look beyond the classic deﬁnition of permafrost to include a broadened focus on the composition of frozen ground, including the ice and the soil organic carbon content, and how it is changing. This ecological perspective of permafrost serves to identify areas of both vulnerability and resilience as climate, ecological disturbance regimes, and the human footprint all continue to change in this sensitive and critical region of Earth.

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1. INTRODUCTION The Arctic may seem distant and remote, but the unprecedented environmental changes occurring there have important consequences for global society. Temperature rise is amplified in northern high-latitude regions, occurring 2.5 times faster than the whole Earth (IPCC 2013), with important impacts on the frozen places of the planet (the cryosphere). Changing sea ice affects global climate, ecosystems and fisheries, and ocean transportation; shrinking ice sheets and glaciers influence water supplies and sea level; degrading permafrost (perennially frozen ground) impacts infrastructure, ecosystem services, and global climate (AMAP 2017). Well-developed satellite observing systems that record sea ice extent daily (NSIDC 2018) and the Greenland ice sheet mass monthly (Wiese et al. 2016) have observed record-breaking low measurements over the last several decades. In contrast, no record of permafrost change with similar spatial or temporal resolution has been made (Biskaborn et al. 2015, Brown & Romanovsky 2008), despite the potential for significant impacts within and outside high-latitude regions. This review focuses on this lesser-known cryospheric domain to address a key societal question: What are key structural and functional properties of ecosystems that interact with changing permafrost, and how do these interactions affect local and global society? Permafrost is perennially frozen ground (rock, soil, ice) that underlies natural ecosystems and human communities in high-latitude areas of Earth. Permafrost is narrowly defined by temperature (<0◦C for at least 2 consecutive years), essentially marking the long-term phase change from liquid water to ice. As a result, permafrost plays a role in defining both the physical structure of ground as well as modulating resource availability to organisms, including people, living on permafrost. In turn, permafrost itself is modified by the overlying ecosystem. The plant community, its associated surface soil organic layer, and other physical and biotic effects on ecosystem energy balance help define where and when permafrost persists (Shur & Jorgenson 2007). Ecological and geomorphological processes are highly sensitive to the phase change between water and ice. This transition point makes the structure and function of permafrost ecosystems unique and also vulnerable to major change in a warming climate. Here, we look beyond the classic definition of permafrost to include a broadened focus on the composition of permafrost and how it is changing. In particular, the ice content and the soil organic carbon in permafrost are key regulators of ecosystem function and provide important services to local people as well as to global society (Schuur et al. 2008). Temperature may classically define permafrost, but ecosystems and people also depend on other factors and resources such as water and nutrients, the availability of which is modulated by frozen ground. Temperature, water, and nutrients are examined within an ecosystem context to highlight aspects of permafrost ecosystems that make their ecological function unique. Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org Permafrost is not static. It depends on regional and global climate conditions, the dynamics of ecosystems through ecological succession, and the impacts of people living within permafrost ecosystems. This review outlines the triggers of changing permafrost in the context of changing northern high-latitude regions as well as the implications for ecological succession and the future state of permafrost ecosystems including the organisms that live there. Finally, the review concludes with the impacts of current and projected ecosystem change on the needs of people living on permafrost as well as on global society. Indeed, the effects of permafrost change reach far outside the northern high latitudes to affect the entire Earth system. Over the last decade and more, the study of permafrost has grown from its geophysical roots to more fully realize the interplay between geophysical and biological processes that define ecosystem function. It is the hope of these authors that this ecological perspective of permafrost serves to identify areas

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of both vulnerability and resilience as climate, ecological disturbance regimes, and the human footprint all continue to change in this sensitive and critical region of Earth.

2. WHAT DEFINES PERMAFROST AND WHERE IS IT?

2.1. Temperature Frozen ground can be considered a three-part system with (a) the active layer at the surface, which thaws each summer and refreezes in the winter; (b) the transient layer located below, which is ice rich compared with the active layer and has likely alternated in and out of permafrost over timescales of decades to centuries; and (c) permafrost, which is deepest, perennially frozen over timescales of centuries to millennia, and can contain massive blocks of ice interspersed with frozen soil (Shur & Jorgenson 2007). The thickness of the active layer ranges from tens of centimeters to several meters depending on the local climatic conditions as well as the thickness of the soil organic layer and structure of vegetation that develops during ecological succession and insulates the permafrost (Nelson et al. 2004). The active layer is the zone featuring heightened biological activity during the short growing season experienced by these ecosystems. Permafrost itself can extend several to hundreds of meters in depth, but the state of near-surface permafrost, defined as ∼0–3 m depth (Lawrence & Slater 2005), is often a much more useful metric relative to ecosystems and people living on top of frozen ground. The permafrost zone occupies 24% of the exposed land surface in the Northern Hemisphere, where most of it is located (entire area is 22.8 × 106 km2) (Brown et al. 2002; Zhang et al. 2000) (Figure 1). Within the Northern Hemisphere, 47% of the permafrost zone is classified as “continuous permafrost,” defined as having >90% of the land surface underlain by permafrost approximately –15 to –2◦C. Another 19% is classified as “discontinuous permafrost,” where 50% to 90% of the land surface is underlain by permafrost. The remaining 34% of the total permafrost zone is split between “sporadic” and “isolated” permafrost, where 10% to 50% and <10% of the land surface is underlain by permafrost, respectively. The latter three categories have relatively warmer permafrost close to the freezing point, approximately –2 to 0◦C, interspersed by soils without permafrost. When permafrost temperature is relatively warm, ecosystem properties related to vegetation structure, snow accumulation, and the soil organic layer, as well as human and natural disturbances that affect them, exert relatively more influence on permafrost distribution ( Jorgenson et al. 2010). Although the majority of permafrost is terrestrial, an additional 3 × 106 km2 area of shallow continental shelf under the Arctic Ocean has the potential for permafrost (Brown et al. 2002). This undersea permafrost initially formed on land when sea levels were lower during the last glacial period (Strauss et al. 2013, Walter et al. 2007). Submergence with seawater over Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org thousands of years helped thaw some, but not all, continental shelf permafrost (Anisimov et al. 2012) leaving an uncertain amount persisting under the ocean (Brothers et al. 2016).

2.2. Ground Ice The amount and distribution of ice within permafrost are controlled by the local and regional climate as well as by geomorphological processes over recent geologic time (Kokelj et al. 2017). On a very local scale (20%), medium (10–20%), and low (<10%) ice content by volume (Zhang et al. 1999).

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Permafrost zone Biomes Glaciers/ice sheets Sporadic permafrost (10–50%) Boreal forests/taiga Continuous permafrost (90–100%) Isolated permafrost (0–10%) Tundra Discontinuous permafrost (50–90%) Subsea permafrost

Figure 1 Permafrost zone regions shown in shades of blue with percent of ground underlain by permafrost in parentheses. Generalized biome Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org area for tundra and boreal regions shows intersection with permafrost across most, but not all, of these regions. Map created by Chris DeRolph, Oak Ridge National Laboratory, using data from the International Permafrost Association; Brown et al. (2002); World Wildlife Fund (2012); and Olson et al. (2001).

Roughly two-thirds of the total permafrost zone is classiﬁed as having low ice content, with the other one-third having medium or high ice content (Zhang et al. 1999). The high-ice category has a large range of ice content, with so-called Yedoma (Ice Complex) deposits in Siberia, Alaska, and the Yukon in Canada containing up to 50–80% ground ice by volume (Strauss et al. 2017, Zimov et al. 2006). The Yedoma regions were not covered by ice sheets during the Last Glacial Maximum and accumulated wind- and waterborne sediments tens of meters deep (Kanevskiy et al. 2011). Three-dimensional networks of ice formed along with the upward accumulation of sediment,

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making this region, including most of the area now submerged on the shallow continental shelf, particularly ice rich. Excess ground ice affects both the rate at which permafrost can thaw and the ecosystem consequences when it does so ( Jorgenson et al. 2015). Higher ice content slows the advance of permafrost thaw because of the substantial heat required to turn ice to liquid. At the same time, thawing of high-ice permafrost has more serious consequences relative to low-ice permafrost. When conditions change and ground ice melts, the ground surface subsides and collapses into the volume previously occupied by ice, causing disturbance to overlying ecosystems and human infrastructure. Mapping ice volume has proven difficult despite its importance for predicting where permafrost thaw will lead to significant ground surface disturbance. Regional to continental ground ice mapping has relied primarily on identification of surface features (e.g., thaw lakes, patterned ground formed by ground ice, etc.) by remote sensing because their presence is likely to indicate regions of high ice. At the site scale, geophysical measurements such as electrical resistivity tomography (Lewkowicz et al. 2011) and ground-penetrating radar (Minsley et al. 2012) have been used successfully to identify the distribution and content of ground ice. Of the three key components of frozen ground, significant new advances have been made over the last decade monitoring permafrost temperature (Biskaborn et al. 2015, Romanovsky et al. 2017) and understanding the organic carbon distribution in permafrost (Hugelius et al. 2014, Tarnocai et al. 2009, Zimov et al. 2006). However, progress toward updating and improving the resolution of the only existing circumpolar permafrost ice content map has lagged ( Jorgenson & Grosse 2016).

2.3. Organic Carbon Recent recognition that the permafrost zone is a large, climate-sensitive reservoir of carbon has spurred a new body of work (Kuhry et al. 2010) to define both the size of the permafrost carbon pool and its potential to be rapidly decayed and transferred to the atmosphere as carbon dioxide or methane as permafrost thaws in a warming climate (Schuur et al. 2008, 2015). Additional greenhouse gases released from northern ecosystems have the potential to accelerate the pace of climate change, and the new (and ongoing) work has helped to define the level of risk and timescale of change. Related to this global climate regulation service, we propose that soil and the organic carbon it contains be defined as the third key component of frozen ground as it relates to ecosystems and people. This component links the traditional geophysical perspective of permafrost with biology because organic carbon in permafrost represents the long-term balance between plant productivity and decomposition interacting with soil development and the physical components described above. Substantial carbon pools in northern high latitudes have been recognized for Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org decades (Gorham 1991), but it was more recently that permafrost soil carbon pools (outside of peatlands) were shown to be much larger at depth than previously recognized because of cryogenic (freeze-thaw) mixing (Ping et al. 2008) and sediment deposition (Zimov et al. 2006). The current best estimate of total organic soil carbon (terrestrial) in the northern circumpolar permafrost zone is 1,460 to 1,600 petagrams (Pg) (1 Pg = 1 billion metric tons or 1 × 1015 g) (Hugelius et al. 2014, Schuur et al. 2018). All permafrost zone soils estimated to 3 m in depth contain 1,035 ± 150 Pg of carbon, with approximately two-thirds of this amount in Eurasia and the remaining one-third in North America (Tarnocai et al. 2009). The Yedoma region of Siberia and Alaska contain 327 to 466 Pg carbon below 3 m (Strauss et al. 2013, Walter Anthony et al. 2014, Zimov et al. 2006), with 96 ± 55 Pg carbon in Arctic river deltas (Hugelius et al. 2014, Tarnocai et al. 2009). Beyond this quantified inventory of permafrost carbon, hundreds of petagrams of uncounted carbon may be contained in deep terrestrial sediments in the circumpolar region outside

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of the Yedoma region and undersea in permafrost that remains on the shallow continental shelf (Schuur et al. 2015, Strauss et al. 2013). Additionally, permafrost on the Tibetan Plateau and northern China outside of the circumpolar region contains another 37 Pg carbon in the top 3 m of soil (Ding et al. 2016). This pool of carbon stored in permafrost zone soils is large relative to other soil and vegetation carbon pools, and it contains approximately twice as much carbon as the atmosphere. Soils in the top 3 m of the rest of Earth’s biomes (excluding tundra and boreal biomes) contain 2,050 Pg organic carbon ( Jobbagy´ & Jackson 2000). The 1,035 Pg of soil carbon quantiﬁed from the northern circumpolar permafrost zone adds another 50% to this 3-m inventory, even though it occupies only 15% of the total global soil area (Schuur et al. 2015). Additionally, the 3-m inventory of soil carbon in the northern circumpolar permafrost zone is 10 times larger than the carbon contained in both above- and belowground live vegetation biomass (55 Pg carbon) and litter plus dead wood (45 Pg carbon) in tundra and boreal forest in the circumpolar region (Schuur et al. 2018). Release of just a fraction of this permafrost carbon pool as greenhouse gases would be signiﬁcant relative to the 10 Pg carbon per year emitted into the atmosphere from human activities that is currently driving climate change (IPCC 2013). Together, the composition of frozen ground as represented by temperature, ground ice, and organic carbon forms an integrated view of permafrost that dictates much of its response to change and the consequences for ecosystems and society.

3. PERMAFROST AS A STRUCTURAL COMPONENT REGULATING ECOSYSTEMS 3.1. Temperature Temperature is a direct control over organisms, and the freeze-thaw dynamics of permafrost soils require a key suite of traits for the survival of organisms living in permafrost soils. The active layer that thaws during summer deﬁnes the soil volume available for plant rooting, nutrient and water access, and heterotrophic activity across the soil food web. Depth within the active layer dictates the temperature regime of any particular soil layer, with soil near the bottom of the active layer remaining only a degree or two above 0◦C when thawed. In stark contrast, moss and surface organic soil, and the microorganisms that inhabit them, can reach temperatures up to 25–30◦C during midday (Gersony et al. 2016). Thus, some organisms in high-latitude ecosystems must tolerate extreme heat as well as extreme cold. The effects of temperature on rates of ecosystem processes such as soil organic matter decomposition and plant and animal physiology have been well researched. A signiﬁcant new direction Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org for temperature control over permafrost ecosystem function relates to biological activity during the nonsummer seasons. More data are now available from fall, winter, and spring that quantify their importance relative to the short summer season. For example, in the fall, when cold air begins to freeze the surface of the active layer while the bottom refreezes upward from the permafrost, the middle of the active layer remains poised at the freezing point for a period of time known as the zero-curtain. During the zero-curtain, this zone of the active layer supports belowground activity even while aboveground plant activity has largely ceased. Although rates of plant and microbial respiration are low, they can account for ∼15% of total annual respiration because the zero-curtain period persists for several months (Celis et al. 2017, Webb et al. 2016). This can shift permafrost ecosystems from being summer net carbon sinks, when summer season

carbon dioxide (CO2) uptake by plants exceeds CO2 release to the atmosphere from heterotrophic (mostly microbial) decomposition of organic matter, into annual net carbon sources, when carbon

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release to the atmosphere dominates (Belshe et al. 2013). For methane (CH4), the fall period of

net release to the atmosphere from soil microbial activity may exceed total summer CH4 release in some (Mastepanov et al. 2008) but not all sites (Zona et al. 2016). In permafrost that is degrading, or is adjacent to relatively warm water bodies (streams, rivers, lakes), the active layer may not completely refreeze in the fall, leaving a talik, a soil layer that remains poised at the zero-curtain throughout the winter. This allows for sustained soil microbial activity even in winter, giving rise

to phenomena such as CH4 bubbles trapped in lake ice (Walter et al. 2006).

Gases (CO2,CH4) produced by biological activity during the zero-curtain period can accumulate in soil or ice and are released by physical processes at a later time. Episodic gas releases from soil to the atmosphere can be triggered by changes in atmospheric pressure, soil cracking in extreme cold, or brief winter warming events. These episodic releases are difﬁcult to quantify

because they happen sporadically but can make an important contribution to the annual CO2

(Raz-Yaseef et al. 2016) and CH4 (Song et al. 2012) budgets of these ecosystems. Although microbial activity has been documented well below freezing, diffusion of carbon substrates required for metabolism becomes much more limited when soil water is frozen. This makes biological activity during the zero-curtain period, when soils are still thawed, proportionally more important for deﬁning ecosystem function across the entire duration of the nonsummer season.

3.2. Water Permafrost temperature, ground ice, and organic carbon all have physical effects on the structure of soil that modulates water flowpaths and water availability to organisms. Precipitation in high latitudes is relatively low, but water perched at the top of the thaw layer is a common feature of these ecosystems during the summer (Walvoord & Kurylyk 2016). This perching of water leads to increased evaporation and runoff and decreased infiltration deeper into the soil. Global lake and wetland occurrence is concentrated at high latitudes as a result of this physical effect of permafrost interacting with local geomorphology at the landscape scale (Muster et al. 2017). Reduced infiltration has contrasting effects on organisms. Plants have more access to water perched at the top of the thaw layer than they would if soils were freely draining, which can be important because summer rainfall is low and sporadic. Indeed, drought in some parts of the permafrost zone is already thought to be important for regulating plant growth (Walker et al. 2015) and may increase with warming air temperature as well as receding permafrost. Nonvascular mosses and lichens that lack root systems and are widespread in in tundra and boreal biomes also benefit from water trapped at the thaw surface. Thawing permafrost that allows the standing water table to move deeper into the soil profile can lead to dieback of nonvascular plants and their loss from the plant community (Osterkamp et al. 2009). Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org Although plant access to water may be elevated by permafrost, restricted drainage means that plant roots and heterotrophic organisms within the active layer may experience anoxic conditions. Early thinking suggested that cold temperatures and low metabolism did not deplete soil water oxygen levels, but a preponderance of research shows that certain strictly anaerobic processes carried out by soil microorganisms, such as methanogenesis (Zona et al. 2016), denitrification (Repo et al. 2009), and iron reduction (gleying) (Harden et al. 2012), occur widely in permafrost ecosystems (Xue et al. 2016), even those that are typically considered upland ecosystems. Standing water can slow overall decomposition processes and therefore carbon release from soils and alter the net ecosystem exchange of carbon with the atmosphere (Mauritz et al. 2017) as well as modulate the decomposition of old soil organic carbon deep in the soil profile (Natali et al. 2015). Plants are also affected by low-oxygen conditions. Sedges that dominate many permafrost ecosystems have anatomical adaptations such as aerenchyma that allow oxygen transport downward within the root

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system. This transport allows sedge roots to access nutrients deep in the soil despite anaerobic conditions. In summary, in addition to the cold temperatures caused by permafrost presence, the effect of permafrost as a physical barrier to water movement and availability is equally important to ecosystem structure and function.

3.3. Nutrients Nutrient demand by tundra and boreal vegetation has been shown to outstrip nutrient supply. Nitrogen is the element most likely to limit plant growth on permafrost soils despite relatively large organic nitrogen pools in the active layer and permafrost. In the active layer, near-freezing temperatures inhibit the activity of decomposer microorganisms that would otherwise release this nitrogen into plant-available forms, whereas nitrogen in permafrost is rendered inaccessible by being frozen. Experimental addition of nitrogen stimulates plant productivity (Mack et al. 2004), suggesting that the microbial release of this element through decomposition proximally limits productivity. Seasonal thaw depth and permafrost temperature dictate the soil volume available for microbial nutrient release and the temperature at which it occurs. These factors also constrain where and when plants can acquire nutrients. The short time that soil layers deeper in the profile are thawed each growing season allows for microbial decomposition and nutrient mineralization but may not support extensive root growth (Keuper et al. 2012). This could be because plant root growth lags behind microbial growth in deep soil layers that thaw late in the season when plant activity is already slowing, or because low temperature and oxygen availability are more restrictive to plants and their mycorrhizal symbionts than to heterotrophic microbes. In lowland permafrost soils, mineral nitrogen availability is high in the deep active layer where anoxic conditions exclude roots (Finger et al. 2016), and this may also be true in some uplands with perched water on top of permafrost. Mineral nitrogen in deep, cold soils may be vulnerable to loss from the ecosystem. In variably oxic environments, ammonium can be oxidized to nitrate, which is susceptible to loss through leaching or denitrification (Harms & Jones 2012). Water that is restricted from draining through the soil and subsoil moves laterally across the permafrost surface, moving relatively high loads of dissolved organic carbon and nutrients into aquatic ecosystems. In fact, because flowing water is mostly moving through surface organic soils, and soil water and frozen subsurface soil and sediment materials have limited contact, the potential for adsorption of solutes onto clay minerals is low in permafrost soils, which contributes to high concentrations being exported to streams and rivers (Striegl et al. 2005). At the same time, weathering of new rock-derived nutrients may be limited to the degree that unweathered rock remains frozen in permafrost and bypassed by water flowpaths (Keller et al. 2010). Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only.

Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org 4. WARMING CLIMATE AND CHANGING DISTURBANCE REGIMES: TRIGGERS FOR PERMAFROST THAW Changes in permafrost arise as a result of changes in both climate and ecosystem processes. Changes in temperature and precipitation act as gradual press (continuous) disturbances that affect permafrost directly through thaw and indirectly through biological processes that regulate the soil organic layer. Climate changes also can modify the occurrence and magnitude of biological disturbances, such as insect outbreaks; abrupt physical disturbances, such as ﬁre and extreme drought; and soil subsidence and erosion resulting from ice-rich permafrost thaw. These pulse (discrete) disturbances often are part of the ongoing successional cycle in tundra and boreal ecosystems, but changing rates of occurrence alter the landscape distribution of successional ecosystem states, which, in turn, affect permafrost distribution. Together, these processes are expected to reduce near-surface permafrost extent by dramatic amounts over this century and are already doing so at present.

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4.1. Climate The most pronounced change in high-latitude climate during the last half century is the increase in average air temperatures by 1–2◦C over the last 20–30 years (Overland et al. 2014), and continued climate change threatens permafrost globally. Global temperature change is ampliﬁed in high- latitude regions, as seen in high-latitude ecosystems where temperature rise is approximately 2.5 times faster than that for the whole Earth (IPCC 2013). Warming is most noticeable during the winter, but summer temperatures are also on the rise, and this pattern of greater winter warming is expected to continue in the future. Observed changes in climate have triggered a substantial increase in permafrost temperatures during the last 40 years (Romanovsky et al. 2017). The greatest temperature increase is found in colder permafrost (approximately –15 to –2◦C), where current permafrost temperatures are more than 2–2.5◦C higher than they were 30 years ago. In areas with warmer permafrost (approximately –2 to 0◦C), the absolute temperature change in permafrost has been much smaller, with increases generally less than 1◦C since the 1980s (Romanovsky et al. 2017). Lower absolute temperature rise in permafrost already near the freezing point is caused by greater partitioning of heat into the ice-to-water phase change associated with surface permafrost degradation. Future changes in climate projected by different Earth System Models (Representative Concentration Pathway 8.5 emission scenario) all feature rapid disappearance of near-surface permafrost over this century ranging from 30% to 100% (Koven et al. 2013).

4.2. Fire Beyond documented changes in climate that have affected permafrost directly as a press disturbance, recent observations suggest that climate-sensitive pulse disturbance events that also influence permafrost, such as wildfire and landslides, are increasing across high-latitude regions. Pulse disturbances often rapidly remove the insulating soil organic layer, leading to permafrost degradation and loss in locations where permafrost temperature is already just below zero. Of all pulse disturbance types, wildfire affects the most land area annually, immediately reduces the thickness of the soil organic layer, and is currently the best characterized at the regional-to-continental scale. Based on satellite imagery, an estimated 8 million hectares (ha) of boreal area was burned globally per year from 1997 to 2011 (van der Werf et al. 2017). However, extreme fire years in northern Canada during 2014 and in Alaska during 2015 doubled the long-term (1997–2011) average area burned annually in this region. Interestingly, these extreme North American fire years were bal- anced by lower-than-average area burned in Eurasian forests, resulting in a 5% overall increase in global boreal area burned. Decadal trends (Kasischke & Turetsky 2006) and paleoecological reconstructions (Kelly et al. 2013) support the idea that area burned, fire frequency, and number of extreme fire years per decade are higher now than in the first half of the last century, or even Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org in the last 10,000 years. Fire also is expanding as a novel disturbance into tundra and forest–tundra boundary regions previously protected by cool, moist climates (Hu et al. 2015). The annual area burned in Arctic tundra is still generally small compared with the forested boreal biome. In Alaska—the only region where estimates of burned area exist for both boreal forest and tundra vegetation types—tundra burning averaged approximately 0.3 million ha per year during the last half century (French et al. 2015), accounting for 12% of the average annual area burned throughout the state even though tundra accounts for 28% of the total area of the state (Zhu & McGuire 2016). Overall, many climate scenarios project that the trend of increasing fire will continue for the rest of the century across most of Alaska (Rupp et al. 2016). However, shifts in vegetation where deciduous stands replace evergreen stands following fire could decrease future forest flammability even as fire weather increases ( Johnstone et al. 2011).

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5. IMPACT OF CHANGING PERMAFROST ON ECOSYSTEM PROCESSES Permafrost thaw has a cascade of effects within ecosystems, and these interact with local and regional topography at the landscape scale, where flat lowlands experience different ecosystem consequences relative to flat uplands or steeper hillslopes (Schuur et al. 2008) (Figure 2). Changing permafrost can be viewed through the same press and pulse framework that defined the triggers for permafrost thaw. Permafrost temperature is controlled by the surface energy balance and the downward flux of heat into the ground. Increases in ground heat flux because of climate warming or disturbance of surface properties cause permafrost to thaw from the top, increasing the depth of the active layer. Most biogeochemical models and Earth System models only represent active-layer thickening (McGuire et al. 2016). But, because of ice content, permafrost thaw abruptly transitions from temperature change alone to include geomorphological changes that have a profound impact on ecosystem structure and function. Shrinking ice volume in permafrost causes the soil surface to subside and collapse into the volume previously occupied by ice (Kokelj & Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org

Figure 2 Landscape perspective of ecological and geomorphological change as a result of permafrost thaw and melting of ground ice. Increasing active-layer thickness as a result of changing climate and ﬁre leads to melting ground ice () and degradation of ice wedge networks (). Ground subsidence from the loss of ice creates thermokarst terrain. In lowlands, ground subsidence can accumulate water-forming ponds, lakes, and wetlands (), but continued thawing also can cause these water features to drain (). In uplands, permafrost can thaw abruptly as a result of active-layer slides () and subsequent thermal erosion. Physical erosion can lead to gullying along water tracks ()aswellasthawslumps() and bank failures ( ) that occur elsewhere, often at the margins of water bodies. Image drawn by Victor Leshyk, Northern Arizona University.

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Jorgenson 2013). Subsided ground also causes surface water perched on the thaw surface to channel toward thawing areas, further degrading permafrost through advective heat transport, a process known as thermal erosion. Thermal erosion can also be tied to physical erosion of soil and sediment materials, further exposing deeper permafrost to continued degradation ( Jorgenson 2013). These local hydrologic effects can cause abrupt change in permafrost at point locations much faster than changes in air temperature alone would predict (Shur & Jorgenson 2007). This abrupt thaw process results in microtopographic patterns of subsided ground, where networks of melting ground ice cause subsequent ecosystem disturbance and form what is known as thermokarst terrain ( Jorgenson 2013). Press or pulse permafrost thaw events may be reversible if conditions shift. Active layers can become thinner if climate conditions cool, insulating snow depth decreases, or if disturbed soil organic layers recover. Of course, permafrost temperature is likely to be the permafrost attribute most reversible if conditions were to shift away from thawing (Shur & Jorgenson 2007). In contrast, melting ground ice and erosion of soil materials from a site are essentially per- manent on ecological timescales. Even if permafrost reformed, ecosystem structure and function would be irreversibly altered.

5.1. Uplands Abrupt thaw interacts with both the amount of ground ice and local geomorphology to produce a range of ecosystem effects (Figure 3). Without ground ice, there is no subsidence and thus a limit to internal thermal erosion feedbacks that cause abrupt thaw. The extreme end point of this interaction is rocky permafrost that can thaw without ground subsidence. Without ice to lose, thermokarst terrain would not form ( Jorgenson 2013). Along with the rate of permafrost thaw, geomorphology is the second important physical factor deﬁning the ecosystem consequences of abrupt thaw. Abrupt thaw in upland landforms that readily lose water, soil, sediment, and rocks downslope creates disturbances unique from lowlands, where these materials are retained. Ecosystem disturbance in uplands has a range of effects depending on slope angle. Low-relief uplands may simply subside as a result of losing ground ice, with low slope angle limiting the physical loss of soil and sediment downslope even as excess moisture leaves the site. Permafrost thaw on steeper slopes can cause catastrophic hillslope failures during the summer, particularly following precipitation events, when the surface ground layer abruptly slides downslope along the thaw interface (Balser et al. 2014). In the absence of surface insulation, exposure of deeper ground to rain and warm air accelerates further permafrost degradation and erosion. Additional thaw and downslope movement of water and soil can progress until physical processes reestablish slope stability and stop continued degradation (Cassidy et al. 2017). Abrupt thaw features on hillslopes often end in streams or lakes where sediment is exported, thus allowing the erosion Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org cycle to continue. When sediment is no longer exported, the concave center of the thaw feature ﬁlls with eroded materials and slope stability is regained. Abrupt thaw features often coincide with hillslope hydrologic networks because of the interaction between thawing permafrost, water redistribution, and erosional movement of materials (Kokelj et al. 2017).

5.2. Lowlands Permafrost lowlands also undergo abrupt thaw, but patterns differ from uplands because water and materials remain on the landscape. Abrupt thaw in permafrost lowlands can be broadly divided into wetland thermokarst and lake thermokarst (Olefeldt et al. 2016). These ecosystem types have characteristic water depth and movement, plant communities that develop after ground subsidence, and trajectories of successional change. Wetland thermokarst landscapes are often

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a d

b e

c f

Figure 3 Examples of abrupt permafrost thaw in different landscapes. (a) Hillslope exposure in Northeastern Siberia showing the surface seasonally thawed active layer (∼50 cm) underlain by permafrost, including frozen soil interspersed with massive ice wedges. Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org (b) Upland thermokarst in low-relief terrain at the north slope of the Alaska Range, Denali National Park, where the network of ice wedges has degraded and drained with little physical erosion or export of soil. (c) Ground disturbance as a result of thawing permafrost a few years after a ﬁre at the tundra–forest ecotone in Northeastern Siberia. (d) Upland slope failure and thermal erosion depositing sediment into the Noatak River, northwestern Alaska. (e) Wetland thermokarst landscape with a mosaic of raised spruce forest on permafrost interspersed with permafrost-free fen and bog vegetation near Scotty Creek, northwestern Canada. ( f ) Lake thermokarst landscape showing lakes and old lake margins as a result of drying and draining in Kotzebue, western Alaska. Photos provided by (a) Ted Schuur, (b) David Schirokauer, (c) Heather Alexander, (d) Ted Schuur, (e) Oliver Sonnetag, and ( f ) Peter Grifﬁth.

a mosaic of wetland vegetation (Sphagnum moss and sedge-dominated fens and bogs), where permafrost has degraded and vegetation is near the surface of the water table, interspersed with higher and drier vegetation communities (lichen and feathermoss forest and shrubland) on intact permafrost (Finger et al. 2016, Jorgenson 2013). In these wetland environments, the water table is usually restricted by deep ground materials with limited permeability that promote the formation

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of wetlands independent of the permafrost table. Here, permafrost degradation usually occurs when fire disturbs the surface organic layer, changes in lateral flows of water thaw the edges of permafrost plateaus, or changes in air temperature or snow cause raised permafrost communities to collapse into the wetlands (Brown et al. 2015). In lake thermokarst landscapes, permafrost thaw and ground subsidence can form shallow ponds where the initial exposure of open water at the surface with low albedo (surface reflectivity) causes a feedback that thaws permafrost. Smaller ponds can then expand into lakes as a result of thawing permafrost along banks and below the body of water. Eventually, lakes expand through bank erosion and can undergo catastrophic drainage and connect to waterways if lake water thaws through impounding permafrost ( Jones et al. 2011). Once lakes abruptly drain, terrestrial succession can restore soil organic layers through surface insulation, and permafrost can reform (Briggs et al. 2014).

5.3. Succession and Biome Shifts Abrupt thaw events that damage and kill dominant plants initiate primary or secondary successional processes that, in some cases, permanently shift vegetation composition, plant biomass, and productivity (Baltzer et al. 2014). Primary succession includes examples where terrestrial ecosystems transition to aquatic lakes or wetlands (Karlsson et al. 2012) or where uplands suffer extensive surface erosion that exposes bare subsoil (Pizano et al. 2014). Lake formation can lead to a complete turnover in the plant community and replacement of low-productivity terrestrial species with high-productivity aquatic mosses that maintain the ecosystem as a carbon sink relative to the atmosphere, even as old stored carbon is released by respiration (Walter Anthony et al. 2014). Exposed mineral soil opens up unique opportunities for community change as new plants recruit from seeds or spores. Tall deciduous shrub species such as willow and alder and deciduous tree species such as aspen, balsam poplar, or birch ( Johnstone et al. 2010) have tiny, wind-dispersed seeds that preferentially recruit on mineral soil seedbeds, leading to rapid and persistent increases in both biomass and productivity of these species during the early decades after abrupt thaw (Pizano et al. 2014). Increasing rates of abrupt disturbance could create more seed sources, accelerating regional rates of shrub and tree expansion into tundra (Myers-Smith et al. 2011). Secondary succession is also common following permafrost thaw as there is usually some remaining biotic pool from which the ecosystem recovers. Upland thaw subsidence with little or no erosion alters soil nutrient and water availability as the active layer thickens (Schuur et al. 2009). Thickening of the active layer increases soil volume but also moves standing water out of the rooting zone. More thawed soil volume increases microbial decomposition and nutrient release, which favors plant species with greater nutrient demand and faster growth rates, such as deciduous Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org shrubs and trees. These species can outcompete graminoids (sedges and grasses) and evergreen trees and shrubs when nutrient availability is high. As active layers thicken, nonvascular mosses and lichens may become increasingly separated from soil water and may die or be outcompeted by species with deeper roots (Osterkamp et al. 2009). Shrubs and trees have been observed to increase in upland tundra ecosystems when thaw increases soil drainage (Fraser et al. 2014), whereas in lowlands, thaw and subsidence inundates the rooting zone, killing trees and shrubs and favor- ing wetland sedges and mosses (Baltzer et al. 2014). Secondary succession also occurs in uplands where signiﬁcant soil erosion has occurred but intact mats of vegetation are deposited into stabilizing erosional features (Pizano et al. 2014). Many perennials propagate vegetatively, and intact vegetation mats can serve as initial points of establishment for the successional plant community. Fire is a trigger for permafrost thaw; thus, postﬁre plant community succession is shaped by physical changes associated with permafrost thaw as well as organismal responses and adaptations

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to fire. Trees in the boreal biome are commonly killed by stand-replacing fires, but understory vegetation can resprout depending on the depth of burning of the surface soil organic layer, which is one aspect of fire severity (Kasischke & Johnstone 2005). Fire severity affects vegetation directly but also decreases the insulating effect of the soil organic layer, increasing permafrost thaw and setting in motion the types of physical changes described above (Brown et al. 2015). Although evergreen boreal trees do not resprout, the remaining soil organic layer has been shown to strongly control species reestablishment due to plant life history traits and soil characteristics ( Johnstone & Kasischke 2005). In boreal Alaska, spruce, aspen, and birch have high seedling recruitment on bare mineral soil because of its high water-holding capacity ( Johnstone et al. 2010). Organic soil seedbeds have a low water-holding capacity and dry quickly; only spruce seedlings persist on these surfaces. Thus, fire severity effects on organic-layer thickness also provide a control point over stand replacement that interacts with permafrost. The low-severity fire regime that historically characterized spruce-dominated Alaskan forests preserved soil organic layers and permafrost, leading to spruce reestablishment after fire ( Johnstone et al. 2010). The recent increase in high- severity fires could be shifting the landscape toward dominance by deciduous trees on permafrost- free soil.

5.4. Coupled Terrestrial–Aquatic Ecosystems Press and pulse permafrost thaw affects the movement of water, nutrients, and other soil materials into wetlands, streams, rivers, and lakes (Liljedahl et al. 2016), altering aquatic ecosystem structure and function. Stream baseflow (stream flow that occurs between storms) is projected to increase as permafrost thaws, because more water infiltrates into soil instead of running off. More baseflow is likely to sustain stream flow and regulate stream temperature (Walvoord & Kurylyk 2016). The modulation of extreme conditions in high-latitude streams and rivers may reduce thermal and physical constraints on dispersal of organisms throughout stream networks. These constraints have, in the past, limited biological colonization. Lessening them potentially opens these ecosystems to invasion by new species (Hotaling et al. 2017). Water also delivers nutrients and soil materials that can stimulate aquatic food webs. Increases in surface water connectivity can enhance lateral movement of nutrients, such as when permafrost peat plateaus collapse into wetlands (Connon et al. 2014). Multiple modes of permafrost thaw have been shown to enhance transfer of nutrients from land to water (Vonk et al. 2015), leading to heightened primary productivity in freshwater ecosystems (Wrona et al. 2016). Although a thickening active layer can expose more soil to water movement and increase lateral carbon and nutrient exports, deeper flowpaths develop when permafrost no longer separates perched surface water from groundwater. Deeper flowpaths expose more soil mineral surfaces to weathering, and Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org they act as adsorptive surfaces to remove dissolved materials from water before it enters aquatic ecosystems. Abrupt thaw events that deliver soil and sediment to streams or lakes can be a local disturbance depending on whether sediment is buried or exported downstream. Increased turbidity can reduce light penetration and suppress primary productivity. But, food webs may ultimately be stimulated because of increased delivery of key nutrients such as nitrogen, phosphorus, and organic carbon that can be utilized by microorganisms (Blaen et al. 2014). This pulse of materials typically at- tenuates over time as the upland ecosystem stabilizes and recovers. The export of organic carbon previously stabilized in permafrost can move it into aerobic environments where decomposition and loss of carbon to the atmosphere are stimulated by higher temperatures (Grosse et al. 2011, Schuur et al. 2008) and photooxidation (Cory et al. 2014). Alternatively, permafrost carbon may be

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buried into deeper aquatic sediments and stabilized by low-oxygen conditions or mineral sorption (Koven et al. 2009), or it may be exported to aquatic ecosystems (Kokelj & Jorgenson 2013). Inputs to lakes may be stabilized in anaerobic sediments (Walter et al. 2006), whereas in streams or rivers, rapid aerobic processing may result in immediate return to the atmosphere.

6. CONSEQUENCES OF ECOSYSTEM CHANGE TO THE SERVICES PROVIDED TO PEOPLE Ecosystems impacted by permafrost thaw provide a number of services to humans both locally and regionally as well as to global society across all four domains of ecosystem services: provisioning, regulating, supporting, and cultural. At the global scale, people are affected by the net release of greenhouse gases from permafrost to the atmosphere—a regulating function of these ecosystems. Release of just a fraction of frozen

permafrost carbon as CO2 and CH4 into the atmosphere would signiﬁcantly increase the rate of future global climate warming (Schuur et al. 2008, 2015). Although circumpolar permafrost warming has been documented over the past decades (Romanovsky et al. 2017), we do not have similar direct measurements of changes in permafrost carbon at the regional to circumpolar scale.

Measurements of CO2 and CH4 fluxes between the ecosystem and the atmosphere provide snap- shots of whether ecosystems are acting as net sources of carbon to the atmosphere or as net sinks, removing carbon from the atmosphere. Recent syntheses demonstrate that tundra (McGuire et al. 2012) and boreal ecosystems act as carbon sinks (Ueyama et al. 2012) during summer, but this effect is offset by carbon losses in fall, winter, and spring when microbes are still metabolically active and plants are largely dormant. The latest synthesis supported previous findings that the summer carbon sink increased in the 2000s compared with the 1990s (Belshe et al. 2013); however, it also suggested that the mean tundra flux remained a carbon source annually across the 1990s and 2000s. Recent aircraft-based measurements of atmospheric greenhouse gas concentrations

over Alaska between 2012 and 2014 showed that tundra regions were an annual net CO2 source to the atmosphere, whereas boreal forests were either neutral or a net annual CO2 sink (Commane et al. 2017). Wildﬁre combustion contributed to the larger interannual variability of boreal forests. Averaged across this short time period, the Alaska study region (tundra and boreal) was estimated to be a net carbon source to the atmosphere of 25 ± 14 teragrams (1 Tg = 1 × 1012 g) C per year. If this Alaskan region (1.6 × 106 km2) was representative of the entire northern circumpolar permafrost zone soil area (17.8 × 106 km2), it would be equivalent to a region-wide net source of 0.3 Pg C per year, which is equivalent to approximately one-third of global net annual land- use change emissions to the atmosphere. This pattern—ecosystems and regions as net carbon sources to the atmosphere—is consistent with the expected effect of degrading permafrost, where Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org previously stored soil carbon is decomposed and plant growth cannot fully compensate. Model projections show that the loss of permafrost carbon is expected to increase in the future under business-as-usual warming scenarios (Representative Concentration Pathway 8.5 emission scenario). Early models projected potential carbon release from the permafrost zone ranging from 37 to 174 Pg C by 2100 (Schaefer et al. 2014). This range is consistent with several data-driven modeling approaches that have estimated that soil carbon releases by 2100 will be 57–87 Pg C (Koven et al. 2015, Schneider von Deimling et al. 2015) and an updated estimate of 102 Pg C from one of the previous models (MacDougall & Knutti 2016). Additional model runs performed with either structural enhancements to better represent permafrost carbon dynamics (Burke et al. 2017) or common environmental input data (McGuire et al. 2016) show similar soil carbon losses, but they also indicate the potential for stimulated plant growth caused by increased nutrients, warmer

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temperatures, longer growing seasons, and higher atmospheric CO2 that offsets some or all of these soil losses by sequestering new carbon into plant biomass and increasing detritus carbon inputs into the surface soil. However, the offset by plant carbon uptake is sensitive to how nutrients liberated from de- composing organic matter are treated within the model structure. Nutrient availability is a key constraint to plant growth in many high-latitude ecosystems, and models often represent an efﬁ- cient transfer of nutrients directly back to plants, where new growth can then offset soil carbon loss. A separate model-data synthesis that does not represent this connection from soil carbon loss and new plant growth in the same tight way puts the range of potential permafrost carbon loss at 65–240 Pg C by 2100, with potential offsets by plant growth and new organic matter formation at only 34 Pg C (Schuur et al. 2015). Even the models that projected initial offsetting carbon uptake by plants forecasted that, over long timescales, plant uptake would fail to offset carbon losses and carbon released from thawing permafrost would affect global climate for centuries. Although the exact magnitude of carbon releases over these time frames is understandably uncertain, these model projections illustrate that the momentum of a warming climate that thaws near-surface

permafrost will cause a future long-term release of CO2 and CH4, as microbes slowly decompose newly thawed permafrost carbon, and will augment future climate warming. Changing plant community composition as a result of permafrost thaw alone or coupled with fire can also affect climate directly by modifying albedo. Albedo influences climate by shifting the amount of incoming energy that is absorbed by the ecosystem and reradiated into the atmosphere as heat. Taller shrubs and trees encroaching into graminoid tundra following abrupt thaw or active-layer thickening are likely to decrease albedo during the spring because the larger-statured vegetation absorbs more radiation than the snow-covered surface; this effect is greatest in spring before snow melts, when incoming sunlight is relatively high (Loranty et al. 2014, Pearson et al. 2013). The strength of regional albedo feedbacks to global climate will be altered by changes in vegetation distribution (Abe et al. 2017). If trees and shrubs expand northward and replace lower- statured vegetation, as predicted, the accompanying decrease in albedo will increase the amount of solar energy absorbed by the ecosystem, which will feed back positively to regional atmospheric warming (Pearson et al. 2013). Replacement of evergreen trees by deciduous trees, by contrast, can lower the albedo in winter and spring when deciduous species are without leaves, exposing highly reflective snow (Beck & Goetz 2011). Similarly, forest loss through the formation of thermokarst wetlands (e.g., in western Canada) could have a stabilizing climate feedback through increased albedo and increased evaporative cooling (latent heat fluxes) (Helbig et al. 2016). Lastly, increasing vegetation cover can protect permafrost directly by canopy shading and decreased ground heat flux (Fisher et al. 2016). In sum, albedo effects can both increase and decrease local climate warming depending on the specifics of vegetation change—including, in particular, interactions with snow Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org cover. Although feedbacks through climate can be felt around the world, people living on frozen ground experience other changes in provisioning, supporting, regulating, and cultural services provided by these ecosystems (Knapp & Trainor 2015). For many people living in permafrost ecosystems, foods from hunting wild fish and animals and harvesting wild plants and berries remain an important part of their daily diet (ICC-AK 2015). These activities preserve culture and knowledge; social gatherings and celebrations are often tied to seasonal cycles of the landscape and the wildlife. Shifting vegetation and biomes connected to thawing permafrost and other changes have an impact on the distribution of animals that migrate across terrestrial and freshwater aquatic landscapes, although it is sometimes difficult to link these changes directly, or solely, to thawing permafrost (Mallory & Boyce 2018). One important and direct aspect of changing permafrost is that subsiding ground and erosion of sediment into waterways can alter transportation routes,

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which rely heavily on overland trails and rivers. This kind of transportation is important for hunting, harvesting, and intercommunity travel that binds people together in these regions. An- other impact of changing permafrost on food harvesting and food security is the use and reliability of permafrost storage cellars to both preserve and prepare food (Evengard & McMichael 2011). Spoilage as a result of warming and thawing permafrost has health consequences and increases harvesting needs. Other health consequences of thawing permafrost include increasing bioaccumulation of mercury in aquatic food webs and toxicity of wild foods that pose health risks to humans (Gordon et al. 2016). Long-range atmospheric transport of mercury from anthropogenic sources (coal burning) at lower latitudes has led to enhanced mercury deposition and accumulation in the vegetation, soils, and sediments of northern ecosystems. Boreal peatlands and permafrost soils may contain some of the largest northern stocks of mercury, up to 10 times greater than stocks in forested upland soils (Schuster et al. 2018). Mercury trapped in soil can be remobilized by ﬁre and permafrost thaw (Stern et al. 2012). In anaerobic environments, such as waterlogged soils, sediments, or lake water columns, bacteria can methylate elemental or oxidized mercury (Hu et al. 2013), resulting in the formation of toxic methylmercury. Methylmercury is a potent neurotoxin that accumulates within food webs and animal species hunted by people. Large stocks of mercury in permafrost ecosystems are likely to be sensitive to how climate change and disturbance impact drainage—whether landscapes become drier or wetter and whether they become more hydro- logically connected. Mercury may be stabilized in soils that become drier after permafrost thaw yet may also be vulnerable to combustion and emission to the atmosphere. In soils that become wetter, mercury is more likely to become mobile in the toxic form that can ultimately end up in the diets of people living in these changing landscapes far from the industry that is the source.

7. RESEARCH RECOMMENDATIONS The changes described in this review would be difficult to mitigate directly in the northern high- latitude region and can only be addressed by slowing the overall pace of climate and high-latitude change with a focus on reducing human emissions. In parallel, sustained research in northern high latitudes will be key for documenting system changes as they unfold. Despite the many research advances that have been made, the potential for new research discoveries, and even surprises, in this remote region remains high. Several critical areas need further research. The first research need is an updated understanding of ground ice distribution at the circumpolar scale including under the sea. Permafrost with high ice content has the biggest potential for abrupt thaw as a result of changing climate and disturbances, which we know has large effects on ecosystems and people. Improving our knowledge of ground ice will help identify vulnerable regions in advance of Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org the major changes that are expected. A second related research need is the incorporation of abrupt thaw distribution and mechanisms into models, in particular those forecasting carbon exchange with the atmosphere. At present, regional and global models consider only top-down warming of permafrost, whereas field observations show the most dramatic change to ecosystems when abrupt thaw occurs. Additionally, abrupt thaw is often triggered by wildfire, and that disturbance appears to be intensifying. Scaling point observations of abrupt thaw and its interactions with wildfire to regional and circumpolar landscapes, as well as representing these processes that occur on scales smaller than the current model grid size into dynamical models, would help to improve forecasts of change in this region. Finally, expanded carbon cycle observations of changing plant and soil carbon pools, and the fluxes of carbon that drive those changes, are needed. Such an observation system would quantify the release of carbon into the atmosphere and thus its potential for accelerating climate change and the potential of ecosystems to offset these releases with new

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plant growth. Although tundra and boreal ecosystems will not remain the same as they were in the face of this unprecedented environmental change, these research directions will help to advance new knowledge that is important for adaptation of both residents of the region and global society impacted by these changes.

DISCLOSURE STATEMENT The authors are not aware of any afﬁliations, memberships, funding, or ﬁnancial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS The authors acknowledge the National Science Foundation (NSF) Study of Environmental Arctic Change (SEARCH) (grant #133100) and the NASA Arctic Boreal Research Experiment (ABoVE) (#NNX15AT71A) for support during the development of this review as well as additional support from the US Department of Energy Terrestrial Ecosystem Science (TES) program, NSF Long-Term Ecological Research (LTER) program, and Department of Defense Strategic Envi- ronmental Research and Development Program (SERDP).

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Annual Review of Ecology, Evolution, and Systematics Contents Volume 49, 2018

Behavioral Isolation and Incipient Speciation in Birds J. Albert C. Uy, Darren E. Irwin, and Michael S. Webster ppppppppppppppppppppppppppppppppp1 The Ecology and Evolution of Alien Plants Mark van Kleunen, Oliver Bossdorf, and Wayne Dawson pppppppppppppppppppppppppppppppppp25 Biodiversity and Functional Ecology of Mesophotic Coral Reefs Michael P. Lesser, Marc Slattery, and Curtis D. Mobley ppppppppppppppppppppppppppppppppppp49 Evolutionary Conﬂict David C. Queller and Joan E. Strassmann pppppppppppppppppppppppppppppppppppppppppppppppppp73 Evaluating Model Performance in Evolutionary Biology Jeremy M. Brown and Robert C. Thomson pppppppppppppppppppppppppppppppppppppppppppppppppp95 Plant Secondary Metabolite Diversity and Species Interactions Andr´e Kessler and Aino Kalske ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp115 Variation and Evolution of Function-Valued Traits Richard Gomulkiewicz, Joel G. Kingsolver, Patrick A. Carter, and Nancy Heckman ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp139 Climate Change and Phenological Mismatch in Trophic Interactions Among Plants, Insects, and Vertebrates Susanne S. Renner and Constantin M. Zohner pppppppppppppppppppppppppppppppppppppppppppp165 Bivalve Impacts in Freshwater and Marine Ecosystems Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org Caryn C. Vaughn and Timothy J. Hoellein ppppppppppppppppppppppppppppppppppppppppppppppp183 Uses and Misuses of Environmental DNA in Biodiversity Science and Conservation Melania E. Cristescu and Paul D.N. Hebert pppppppppppppppppppppppppppppppppppppppppppppp209 Frontiers in Metapopulation Biology: The Legacy of Ilkka Hanski Otso Ovaskainen and Marjo Saastamoinen pppppppppppppppppppppppppppppppppppppppppppppppp231 Integrating Networks, Phylogenomics, and Population Genomics for the Study of Polyploidy Paul D. Blischak, Makenzie E. Mabry, Gavin C. Conant, and J. Chris Pires pppppppppp253

Contents v ES49_FrontMatter ARI 18 September 2018 17:50

Ecological Response to Permafrost Thaw and Consequences for Local and Global Ecosystem Services Edward A.G. Schuur and Michelle C. Mack pppppppppppppppppppppppppppppppppppppppppppppp279 (Non)Parallel Evolution Daniel I. Bolnick, Rowan D.H. Barrett, Krista B. Oke, Diana J. Rennison, and Yoel E. Stuart pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp303 Mechanisms of Plastic Rescue in Novel Environments Emilie C. Snell-Rood, Megan E. Kobiela, Kristin L. Sikkink, and Alexander M. Shephard ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp331 Challenging Dogma Concerning Biogeographic Patterns of Antarctica and the Southern Ocean Kenneth M. Halanych and Andrew R. Mahon pppppppppppppppppppppppppppppppppppppppppppp355 Dinosaur Macroevolution and Macroecology Roger B.J. Benson ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp379 Life in Dry Soils: Effects of Drought on Soil Microbial Communities and Processes Joshua P. Schimel ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp409 Using Genomic Data to Infer Historic Population Dynamics of Nonmodel Organisms Annabel C. Beichman, Emilia Huerta-Sanchez, and Kirk E. Lohmueller ppppppppppppppp433 The Contemporary Evolution of Fitness Andrew P. Hendry, Daniel J. Schoen, Matthew E. Wolak, and Jane M. Reid pppppppppp457 The Deep Past Controls the Phylogenetic Structure of Present, Local Communities Pille Gerhold, Marcos B. Carlucci, S¸erban Proche¸s, and Andreas Prinzing pppppppppppppp477 Development and Evolutionary Constraints in Animals Frietson Galis, Johan A.J. Metz, and Jacques J.M. van Alphen ppppppppppppppppppppppppp499

Indexes Access provided by University of Alaska - Fairbanks on 02/04/19. For personal use only. Annu. Rev. Ecol. Evol. Syst. 2018.49:279-301. Downloaded from www.annualreviews.org

Cumulative Index of Contributing Authors, Volumes 45–49 ppppppppppppppppppppppppppp523 Cumulative Index of Article Titles, Volumes 45–49 ppppppppppppppppppppppppppppppppppppp527

Errata

An online log of corrections to Annual Review of Ecology, Evolution, and Systematics articles may be found at http://www.annualreviews.org/errata/ecolsys

vi Contents