The hidden life of plants : fine root dynamics in northern ecosystems

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The hidden life of plants

Fine root dynamics in northern ecosystems

Gesche Blume-Werry

Department of Ecology and Environmental Science Umeå 2016

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This work is protected by the Swedish Copyright Legislation (Act 1960:729) ISBN: 978-91-7601-533-9

Cover illustration by the author.

Electronic version available at http://umu.diva-portal.org/ Printed by: Print and Media

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“it is hardly an exaggeration to say that the [root] tip…acts like the brain of one of the lower animals; the brain being seated within the anterior end of the body, receiving impressions from the sense organs, and directing the several movements”

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List of papers

This thesis is based on the following four studies, which are referred to in the text by their respective Roman numerals:

Paper I

G. Blume-Werry, S. D. Wilson, J. Kreyling and A. Milbau (2016)

“The hidden season: growing season is 50 % longer below than above ground along an arctic elevation gradient”, New Phytologist, 209: 978-986.

Paper II

G. Blume-Werry, R. Jansson and A. Milbau

“Root phenology unresponsive to earlier snowmelt despite advanced aboveground phenology in two subarctic plant communities”, In review in Functional Ecology.

Paper III

G. Blume-Werry, A. Milbau, L. M. Teuber, M. Johansson and E. Dorrepaal

“Dwelling in the deep– permafrost thawing strongly increases plant root growth and root litter input”, Manuscript.

Paper IV

G. Blume-Werry, J. Kreyling, H. Laudon and A. Milbau (2016)

“Short-term climate change manipulation effects do not scale up to long-term legacies: Effects of an absent snow cover on boreal forest plants”, Journal of Ecology, in press.

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Author contributions

Paper I

GBW, SDW and AM planned and designed the research; GBW performed fieldwork; GBW, JK and AM analysed the data; GBW wrote the manuscript with contributions from all authors.

Paper II

GBW and AM designed the study, GBW performed field work and analysed the data with input from RJ and AM, GBW wrote the manuscript with contributions from all authors.

Paper III

GBW, AM, MJ and ED designed the study, GBW and LT performed fieldwork, GBW analysed the data with input from LT and ED, GBW wrote the manuscript with contributions from all authors.

Paper IV

GBW, JK, HL and AM designed the study, GBW performed fieldwork, GBW analysed the data with input from JK and AM, GBW wrote the manuscript with contributions from all authors.

Authors

AM: Ann Milbau, ED: Ellen Dorrepaal, GBW: Gesche Blume-Werry, HL: Hjalmar Laudon, JK: Juergen Kreyling, LT: Laurenz M. Teuber, MJ: Margareta Johansson, RJ: Roland Jansson, SDW: Scott D. Wilson

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Abstract

Fine roots constitute a large part of the primary production in northern (arctic and boreal) ecosystems, and are key players in ecosystem fluxes of water, nutrients and carbon. Data on root dynamics are generally rare, especially so in northern ecosystems. However, those ecosystems undergo the most rapid climatic changes on the planet and a profound understanding of form, function and dynamics of roots in such ecosystems is essential. This thesis aimed to advance our knowledge about fine root dynamics in northern ecosystems, with a focus on fine root phenology in natural plant communities and how climate change might alter it. Factors considered included thickness and duration of snow cover, thawing of permafrost, as well as natural gradients in temperature. Experiments and observational studies were located around Abisko (68°21' N, 18°45' E), and in a boreal forest close to Vindeln (64°14'N, 19°46'E), northern Sweden. Root responses included root growth, total root length, and root litter input, always involving seasonal changes therein, measured with minirhizotrons. Root biomass was also determined with destructive soil sampling. Additionally, aboveground response parameters, such as phenology and growth, and environmental parameters, such as air and soil temperatures, were assessed.

This thesis reveals that aboveground patterns or responses cannot be directly translated belowground and urges a decoupling of above- and belowground phenology in terrestrial biosphere models. Specifically, root growth occurred outside of the photosynthetically active period of tundra plants. Moreover, patterns observed in arctic and boreal ecosystems diverged from those of temperate systems, and models including root parameters may thus need specific parameterization for northern ecosystems. In addition, this thesis showed that plant communities differ in root properties, and that changes in plant community compositions can thus induce changes in root dynamics and functioning. This underlines the importance of a thorough understanding of root dynamics in different plant community types in order to understand and predict how changes in plant communities in response to climate change will translate into root dynamics. Overall, this thesis describes root dynamics in response to a variety of factors, because a deeper knowledge about root dynamics will enable a better understanding of ecosystem processes, as well as improve model prediction of how northern ecosystems will respond to climate change.

Keywords: Arctic, belowground, boreal, climate change, fine roots, heath,

meadow, minirhizotron, permafrost, phenology, plant community, root biomass, root growth, root litter, root production, subarctic, tundra

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Fine root dynamics in northern ecosystems

Root dynamics in northern ecosystems

General background

A large portion of plant biomass is situated belowground in northern (here: arctic and boreal) ecosystems: 30% in boreal forests and 80% in tundra (Mokany et al., 2006). Moreover, fine root production and turnover represent a large part of terrestrial net primary production, with estimates of 32% in boreal forests (Yuan & Chen, 2010), 30-90% in sedge-dominated tundra and 10-60% in shrub-dominated tundra (Iversen et al., 2014). It is well known that roots directly influence biogeochemical cycles in terrestrial ecosystems, as plant roots take up water and nutrients, move photosynthetically fixed carbon into the soil through litter and exudates, and stimulate soil microbial activity (Matamala et al., 2003; Pendall et al., 2004). Roots and their associated fungi drive long-term carbon sequestration in high latitude systems (Loya et al., 2004; Clemmensen et al., 2013), which contain about 50% of all global belowground organic carbon (McGuire & Anderson, 2009). Nevertheless, roots are notoriously understudied, mainly due to the methodological difficulties associated with studying roots that are hidden in the ‘black box’ of the soil. Root studies in natural communities with naturally occurring factors, such as competition for resources in time and space, thus continue to be rare. Furthermore, the majority of studies that have measured roots in natural communities have focused on temperate ecosystems. This lack of available data, together with the high importance of roots for various biogeochemical processes, makes ‘quantifying root dynamics (including production, lifespan, turnover) in response to changing environmental conditions’ a high research priority in northern ecosystems (Iversen et al., 2014).

For an overview of the published studies on roots in the Arctic and Subarctic, I performed a standardized search for relevant literature in the Web of Science in February 2014 with the following search string: “root* AND (arctic OR subarctic OR tundra)”, refined by subject area “ecology” or “plant sciences”, and type “article” or “review”, which resulted in a total of 369 records. I further refined the list by excluding studies that did not mention roots in the title or abstract, that studied a different ecosystem than the Arctic, limnological or marine papers, papers that did not investigate vascular plants and paleoecological studies. This resulted in a total of only 78 relevant papers from 1975 to February 2014, of which 5 were reviews and 73 research articles. Only 53% of the relevant studies from the standardized search had roots as one of their main objectives, whereas the other 47% measured any kind of root response as one of many response parameters. On average only two papers were published each year (Fig. 1). Even more

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The hidden life of plants

remarkable, most of these papers measured response parameters related to root form (such as root biomass, root architecture, rooting depth; 71% of all relevant articles) rather than their function (such as growth, phenology, respiration, exudation; 29% of articles, Fig. 1), and root biomass was by far the most commonly measured response parameter. This illustrates the general paucity of data regarding roots in northern ecosystems, especially in regard to root function, and papers published on this topic since February 2014 do not change this conclusion.

Fig. 1: Temporal development of published studies regarding roots in arctic or

subarctic ecosystems, with the response parameters being related to (a) Form (such as root architecture, rooting depth, root biomass) or (b) Function (such as growth, phenology, respiration, exudation) of roots.

Even though a large portion of plant biomass is located belowground, the total amounts of root biomass are relatively low in tundra and boreal forests, around 1.2 kg m-2_{and 2.9 kg m}-2_{respectively, compared to other biomes}

such as temperate and tropical forests (around 4.4 kg m-2_{, Jackson et al.,}

1996). Traditionally, roots are classified into ‘coarse’ or ‘fine’ according to their diameter using a cut-off value of 2 mm diameter. According to this classification, around 80% of the total amounts of roots are fine roots in tundra, and around 20% in boreal forest (Jackson et al., 1997). Yet it becomes increasingly evident, that the traditional classification of ‘fine’ roots includes roots that are functionally very different (Keel et al., 2012; McCormack et al., 2015). The unbranched, ephemeral, first-order roots perform the greatest deal of root function in terms of water and nutrient uptake as well as carbon input, whereas higher order roots are responsible for transport, storage, and lateral root production (McCormack et al., 2015).

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Northern ecosystems possess several exceptional features that can influence root distribution and dynamics, such as rooting depth, growth and phenology. The rooting depth of plants is restricted in many areas of northern ecosystems because soils often are shallow, or underlain by permafrost (perennially frozen ground), which restricts roots to the active layer (upper part of the soil column that thaws annually). Consequently, more than 90% of the root biomass of arctic plants is located in the upper 30 cm of the soil (Callaghan et al., 1991; Jackson et al., 1996), and most roots are found in organic soil horizons at the surface (Iversen et al., 2014). Similarly, Canadell et al. (1996) found that the maximum rooting depth of tundra species is only 0.5 ± 0.1 m, while the global average was 4.6 ± 0.5 m. Rooting depth also varies between functional groups and species, with shrubs generally having a shallower rooting distribution than sedges (Iversen et al., 2014).

Root phenology, the timing of root growth, influences root associated processes, such as water and nutrient uptake or soil carbon input and stimulation of microbial activity (Matamala et al., 2003). Root phenology in turn can be influenced by both exogenous (such as temperature, nutrient availability, light availability) and endogenous factors (such as availability of recent photosynthates) and their roles might differ between ecosystems or even species, balancing competitive needs for water and nutrients with internal carbon allocation (Abramoff & Finzi, 2015; Radville et al., 2016a). Differentiating between exogenous and endogenous factors can be difficult in the field as changes in temperature, daylight, and availability of photosynthesized C or nutrients are closely related in time. Many studies have shown a positive relationship between root growth and soil temperatures in seasonal environments (Pregitzer et al., 2000; Abramoff & Finzi, 2015; Radville et al., 2016a). Yet this generally observed correlation might be a result of including the winter season with very limited root growth and low soil temperatures. The relationship between soil temperature and root growth may not always be straightforward under field conditions and detailed observations of root phenology are generally rare, and very few in arctic or boreal systems. Compared to temperate regions, arctic and boreal plants deal with low soil temperatures year-round. Even at a relatively mild subarctic site in Abisko, northern Sweden, mean soil temperatures at a depth of 5 cm reached only 9.6 °C in the warmest month (August) and were −2.9 °C in the coldest month (February) (1990-2013, Abisko Scientific Research Station). There are many sites in the Arctic where soil temperatures rarely exceed 7 °C even in summer, temperatures at which most temperate species would not even grow roots at all (Alvarez-Uria & Körner, 2007). In arctic sedges on the other hand, root growth has been

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observed at temperatures around 0 °C (Shaver & Billings, 1975, 1977; Kummerow & Ellis, 1984).

The balance of root growth and mortality determines root turnover rates, which range from weeks to years. Generally, the smaller the root diameter, the higher the turnover rate (Eissenstat et al., 2000; Brunner et al., 2013; Chen & Brassard, 2013). Typical turnover estimates of ephemeral fine roots are 0.5-2.5 yr-1_{, whereas more persistent fine roots lie in the range of 0.1-0.4}

yr-1_{(McCormack et al., 2013). Temperature is strongly correlated to root}

turnover on a global scale with colder, higher latitudes having a lower turnover than temperate or tropical regions (Gill & Jackson, 2000), because maintenance respiration of roots increases exponentially with temperature, low mineralization rates limit the activity of short-lived roots, and damages to roots from herbivores and pathogens occur less in soils that are cold and freeze seasonally (Eissenstat et al., 2000; Gill & Jackson, 2000; Chen & Brassard, 2013). Estimates of life-span of fine roots in northern ecosystems are usually longer than 5 years (Shaver & Billings, 1975; Gill & Jackson, 2000; Sloan et al., 2013), except for sedge species from the Eriophorum genus, which have roots with lifespans of only 1-2 years (Shaver & Billings, 1975; Sullivan et al., 2007).

Climate change impacts on roots in northern ecosystems

High latitudes are experiencing more rapid and severe climate change than the rest of the world (ACIA, 2004; IPCC, 2013). Such climatic change will influence form and function of roots in northern ecosystems both directly, e.g., through increases in soil temperatures, and indirectly, e.g., through changes in plant community composition. Even though these changes might be profound for ecosystem functioning, very little is known about how root dynamics will respond to climate change, especially with regard to root functional parameters.

Growing season length

One prominent response to climate warming is a change in plant phenology (the timing of periodic life-history events, such as bud break), as vegetation is increasingly observed to become active earlier in spring (Wolkovich et al., 2012; Richardson et al., 2013). Changes in phenology and growing season length are expected and observed to be most pronounced in regions with a strongly seasonal climate, such as northern ecosystems (Pau et al., 2011; Barichivich et al., 2013; Xu et al., 2013). Even though growing season length, phenology and changes therein are generally well documented, our knowledge about it almost exclusively comes from aboveground measures, which are used as sole indicators for whole-plant responses. It was long

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flush of root growth in spring and significant mortality in the fall simultaneously with canopy senescence, as is often observed in temperate systems (Abramoff & Finzi, 2015). However, many ecosystems do not show this pattern (Abramoff & Finzi, 2015), and it is unclear if the period of plant growth and activity is similar above- and belowground in arctic plant communities, and whether or not this differs between vegetation types or depends on the harshness of the climate. To get more insight into the relationship between root and shoot growth, Paper I compared the growing season length above- and belowground along an arctic elevation gradient, encompassing different vegetation types.

Earlier snowmelt

Warmer temperatures during winter and spring can lead to earlier snowmelt, due to thinner snow cover during winter or faster melting in spring (ACIA, 2004). Snowmelt is an important driver of plant phenology in seasonally snow covered systems, and an earlier snowmelt thus leads to advanced aboveground phenology of many species (Dunne et al., 2003; Wipf & Rixen, 2010; Khorsand Rosa et al., 2015). However, it is unknown if root phenology will change in a similar manner. Paper II therefore measured belowground phenology in response to earlier snowmelt, which was done in two contrasting plant community types: heath and meadow.

Thawing permafrost

One important consequence of climate warming is the thawing of permafrost and deepening of the active layer in many northern areas (IPCC, 2013; Schuur et al., 2015). Thawing of permafrost will not only provide previously unoccupied soil volume to plant roots, but also release considerable amounts of plant-available nitrogen (Keuper et al., 2012). Deep-rooted species might profit from these newly available resources, but they only become available at the time of maximum thaw, which presumably is after the time that is relevant for plant uptake (Koven et al., 2015). Increased resource availability has important implications for species composition, especially if only a few of the species present have access to these resources (Keuper et al., 2012). In addition, it may induce changes in root dynamics, such as rooting depth, growth and mortality. Nevertheless, it remains unknown whether changes in soil properties and vegetation composition upon permafrost thaw alter root dynamics. Paper III therefore examined which, if any, plant species take up nitrogen that is released at the time and depth of permafrost thaw, and if root dynamics change in a long-term permafrost thaw experiment.

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Reductions in snow cover thickness and duration

Boreal forests are shaped by a thick snow cover, which insulates vegetation and soils from cold air temperatures during winter (Haei et al., 2013). Warmer temperatures and more precipitation falling as rain instead of snow during winter decrease the extent and duration of snow cover (ACIA, 2004; IPCC, 2013). The current duration of snow cover in northern Sweden is 5-6 months (Laudon & Löfvenius, 2015) but is expected to shorten by 73-93 days within the next century (Mellander et al., 2007). Such a decrease in snow cover can lead to ‘colder soils in a warmer world’ (Groffman et al., 2001) and expose roots, as well as understorey plants aboveground, to colder temperatures and more freeze-thaw cycles. Due to their position within the soil, roots are usually less hardy as they are more protected against freezing temperatures compared to aboveground plant parts. Frost damage to roots can thus already occur at relatively milder temperatures compared to aboveground plant parts (Sakai & Larcher, 1987; Schaberg et al., 2008). Frost-induced damages to the root system can feedback to the whole plant, as well as biogeochemical cycling in the ecosystem. However, how roots of mature plants respond to severe frost under natural conditions remains poorly understood. Paper IV therefore examines the effects of an absent snow cover on plant biomass, growth and phenology above- and belowground, in both a short- and long-term experiment.

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Aims of this thesis

The overall aim of this thesis was to advance the knowledge about fine root dynamics in northern ecosystems, with a focus on how fine root phenology responds to climate change (Fig. 2). I aimed to describe and quantify root dynamics in natural plant communities with interactions and competition among species. Specifically, the chapters of this thesis focus on the following questions:

Paper I

1) Does fine root phenology reflect or differ from shoot phenology?

2) Is the growing season similar in length and timing above and below

ground across arctic plant communities along an arctic elevation gradient?

3) Which abiotic factors influenced seasonal patterns of root growth and do

those differ among plant communities?

Paper II

1) Does earlier snowmelt advance both above- and belowground phenology? 2) Do plant community types differ in their responsiveness to earlier

snowmelt?

Paper III

1) Which species, if any, are able to take up nitrogen at the depth and time of

maximum active layer depth in permafrost soils?

2) Do maximum root length and depth distribution of the main plant

functional types change with permafrost thaw?

3) Do plant functional types differ in their root growth distribution over

depth and time under ambient conditions and with permafrost thaw?

4) Do amounts and depth distribution of root mortality change with

permafrost thaw?

Paper IV

1) Does the absence of snow and concomitant stronger (soil-) frost modify

plant biomass, growth and phenology both above- and belowground?

2) Do conclusions about plant responses to a reduced snow cover differ

depending on the duration of the treatments?

Materials and methods

Study areas

This thesis is based on field research in northern Sweden. Study areas of

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(68°21' N, 18°45' E), 200 km north of the Arctic Circle. The surroundings of Abisko have a long tradition of (sub-)arctic research, due to the Abisko Scientific Research Station, which was established in 1913 and provides more than 100 years of climate data. The area around Abisko has a subarctic climate with a mean annual air temperature of −0.1 °C, a mean July temperature of 11.6 °C, a mean January temperature of −9.9 °C and a mean annual precipitation of 335 mm (1981–2010, Abisko Scientific Research Station), and lies in the discontinuous to sporadic permafrost zone (Johansson et al., 2013). The tree line is situated at around 600 m a.s.l, and is formed by mountain birch (Betula pubescens ssp. czerepanovii). The mountainous surroundings of Abisko, reaching to about 1990 m a.s.l., offer a high diversity of habitats, with strong gradients in temperature (through elevation) and precipitation (from just over 300 mm yr-1_{in Abisko to over}

1000 mm yr-1_{in Riksgränsen, only 30 km apart; Swedish Meteorological}

Institute SMHI, 1961-1990). Research for this thesis was conducted in different plant communities and on different elevations.

The study area of Paper IV was the Krycklan catchment at the Svartberget Field Station (64°14'N, 19°46'E), close to Vindeln and about 60 km north-west of Umeå. The Krycklan catchment provides a long-term and accessible field research infrastructure. It lies in the boreal zone with a mean annual air temperature in the study area of 1.8 °C, a mean July temperature of 14.6 °C, a mean January temperature of −9.5 °C and a mean annual precipitation of 623 mm (1980–2009). The vegetation is a Norway spruce forest (Picea abies) with an understory layer dominated by dwarf shrubs and bryophytes, with a high overlap in species composition with the communities in Abisko. About 40% of the annual precipitation in this area falls as snow, and the timing, depth and duration of the snow cover strongly influences soil temperature (Laudon & Löfvenius, 2015). An early, thick and constant snow cover leads to warm soils, whereas a late onset of snow or a thin snow cover — as can happen in warmer winters with more precipitation falls as rain instead of snow — leads to colder soils.

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Fig. 3: Map of the study areas, field work for Papers I – III was conducted in the

Abisko area, and for Paper IV close to Vindeln.

Experimental designs

The study for Paper I was set up along an elevational gradient from mountain birch forest to high alpine tundra, using the decreasing temperature with increasing elevation to study root phenology in different climates (space-for-time substitution, Körner (2007)). Ten plots were established at each elevation, and above- and belowground phenology were measured during two growing seasons. The experiment for Paper II was set up in heath and meadow communities, which co-occur in many areas of Fennoscandia and differ strongly in species composition and soil properties (Sundqvist et al., 2011, 2014; Milbau et al., 2013). Heath communities were dominated by evergreen and deciduous dwarf shrubs and had low species diversity, whereas meadow communities were dominated by forbs and graminoids and had higher species diversity. In each of the plant community types, seven paired plots were established, of which one plot per pair received the treatment of an earlier snowmelt. Snowmelt was accelerated by placing black cloth on top of the snow. For Paper III a deep-fertilization

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experiment, in which fertilizer was injected at 50 cm depth in October, and a long-term permafrost-thaw experiment (Johansson et al., 2013) were used. Both treatments had six replicates and were located on a peatland, which represents the typical location of lowland permafrost in the Abisko area. As this permafrost was formed under climates colder than present, it can only persist under certain circumstances, so called ‘ecosystem–protected permafrost’ (Shur & Jorgenson, 2008). Two main factors support ecosystem–protected permafrost: a thin snow cover during winter (supported by low growing vegetation and strong winds), and the presence of peat. The heat conductivity of peat changes dramatically with moisture levels, resulting in cooling of the soil: when it is dry during summer, it prevents heat from penetrating the ground, and moist conditions during the rest of the year allow cold temperatures to reach deep into the soil profile. Permafrost temperatures are relatively warm in this area, and small increases in temperature or snow cover can result in dramatic thawing of permafrost (Åkerman & Johansson, 2008). The thawing of permafrost in this experiment was induced by snow fences, set up perpendicular to the main wind direction, which increased snow cover during the winter since the experiment was started in 2005. Paper IV used a long-term (11 years) snow removal experiment, as well as a similar short-term (1 year) set of plots, with each three replicates. Shelters excluded snow from the plots during winter, but that snow was added to the plots at snowmelt, such that the same amounts of water and nutrients entered the plots as in control plots.

Root phenology (Minirhizotrons)

Minirhizotrons are composed of transparent surfaces to provide a ‘window’ into the soil and observe root growth along that surface. They are transparent tubes (made from cellulose acetate butyrate, Bartz Technology Corp., Carpinteria, CA, USA) that are permanently installed in the soil. A camera is inserted into the tube to take pictures of the soil-tube interface, including roots, which can then be used to observe root growth by going back to the same spot and taking images repeatedly (Fig. 4). Herein lies the main advantage of minirhizotrons: the possibility to have a non-destructive, in-situ method to observe growth rates, root phenology (seasonal timing of root growth), root mortality, life-span and turnover. Also rooting depth and seasonal changes therein can be assessed with minirhizotrons. In addition, minirhizotrons capture the dynamics of the smallest and most ephemeral roots, those responsible for absorbing nutrients and water (Iversen et al., 2011; McCormack et al., 2015), which are difficult to analyse with destructive root sampling when around 40% of those can be missed (Robinson, 2004). Thus, assessing root dynamics of tundra systems with minirhizotrons, specifically the initiation and seasonal patterns of root growth, as well as the

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identified as high priority for the next generation of tundra ecosystem measurements (Iversen et al., 2014).

Minirhizotrons can be installed at an angle (typically 45 °, to observe different depths, Paper III and Paper IV) or horizontally using natural steps in the terrain (replicating the depth at which most activity is expected,

Paper I and Paper II). The end of the tube which sticks out of the soil was

covered in tape and had a lid to prevent light entering the tube. After installation of the minirhizotrons, we waited for 1-4 years to give the vegetation time to recover. The frequency of image collection was chosen to be every week (Paper II), every two weeks (Paper I & III) and every three weeks (Paper IV) depending on the temporal resolution needed to answer the research questions. In general, there is a risk of not detecting roots if they grow and die between sampling times, but this risk is presumably higher in more productive systems and a recent study showed that sampling intervals of up to three weeks did not underestimate root production and mortality in five contrasting sites (Balogianni et al., 2016).

Fig. 4: Example of a minirhizotron image series. Here, each picture represents a

1.4 × 1.8 cm viewing area and there are two weeks between the pictures.

Other methods

Aboveground phenology was measured in several papers. In Paper I, I used digital photography and measures of greenness as an indicator for aboveground phenology, in Paper II, I used plot-scale assessments of leaf-out and flowering for each species, and in Paper IV, I recorded leaf and flowering status on marked individuals. Other methods included destructive soil sampling for root biomass, shoot growth measurements, sampling of leaf tissue and isotopic labelling. In each study, also various environmental parameters were measured, such as air and soil temperature, snow depth, or active layer depth.

Data analyses

For statistical analyses of the data, I mainly used linear models or linear mixed effect models with analysis of variance. Linear mixed effect models were used if a random factor needed to be included because measurements were not independent in space or time. I used R statistical software (R Core Team, Vienna, Austria) for all analyses with various packages.

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Major results and discussion

This thesis aimed to advance our knowledge about fine root dynamics in northern ecosystems, thereby focussing on fine root phenology. A recent and comprehensive review by Iversen et al. (2014) describes the current knowledge about roots in arctic tundra, and lays out the most important research questions for the next generation of tundra root research. Many of these questions were touched upon in this thesis: ‘What are the […] dynamics of roots across a diversity of ecosystems in Arctic tundra?’ (Paper I, Paper II, and Paper III), ‘What are the differences among tundra plant species in root phenology [and] lifespan […]?’ (Paper III), ‘How do changes in plant community composition manifest belowground, what are the consequences for ecosystem functioning?’ (Paper I, Paper II, and Paper III), ‘What factors control root growth and mortality in tundra?’ (Paper I, Paper II, and Paper III), ‘How do root dynamics in tundra respond to environmental forcing?’ (Paper II and Paper III), ‘How is root phenology in tundra related to the depth of thaw of the active layer?’ (Paper III), and ‘Will tundra plant species with deeper rooting distributions have greater access to soil nutrients as permafrost thaws?’ (Paper III). While the research for Paper IV was not conducted in arctic tundra, but in boreal forest, many species of the understorey are shared with arctic tundra and therefore the results from that paper are also relevant for many tundra plant processes (such as ‘How do root dynamics in tundra respond to environmental forcing?’). Even though this thesis can by no means conclusively answer all these questions, it provides an important step towards a better understanding of root dynamics in northern ecosystems. The major results of each paper are presented and briefly discussed below.

The hidden season

Paper I compared phenology, and peaks in production and growing season

length above- and belowground along an arctic elevation gradient. Vegetation phenology was not synchronized above- and belowground in sub– alpine birch forest, low alpine tundra or high alpine tundra. Peaks in production did not coincide in time, and root growth continued for weeks after aboveground senescence. This shows that current observations of phenology in arctic tundra misrepresent the growing season length and production patterns of > 80% of the plant biomass. These results also clearly indicate that substantial root growth can be fuelled by stored carbon reserves and is not dependent on recent photosynthates. The asynchrony between above- and belowground plant compartments observed here is much stronger than in any other biome (Abramoff & Finzi, 2015), but similar to

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Furthermore, the importance of soil temperature for root growth was highest in the sub-alpine forest and decreased with elevation, whereas the importance of time of year for belowground phenology increased with elevation. Thus, relatively more productive systems seem more able to use higher temperatures for enhanced root growth compared to systems adapted to a harsher climate.

These findings show that root phenology should be explicitly considered in ecosystem processes. Predictions of changes in carbon and nutrient cycles with climate change may improve if terrestrial biosphere models do no longer couple above- and belowground phenology or limit the duration of root production to the aboveground growing season.

Root phenology and earlier snowmelt

Paper II explored the above- and belowground phenological responses to

experimentally advanced snowmelt in two contrasting plant communities, heath and meadow. The timing of snowmelt is an important cue for aboveground phenology of many plant species in northern ecosystems (Dunne et al., 2003; Wipf & Rixen, 2010; Khorsand Rosa et al., 2015), and this study was no exception: advanced snowmelt led to an earlier leaf-out and flowering in both heath and meadow communities. However, root phenology remained unchanged, despite these aboveground advances and increased soil temperatures in the early snowmelt treatment. Interestingly, the phenological responses of heath and meadow to advanced snowmelt were similar even though they differed distinctly in species composition and root properties. Heath vegetation had higher root biomass than meadow, but less growth and lower turnover. This is similar to their aboveground growth and turnover patterns and thus indicates whole-plant strategies in these respects (Freschet et al., 2013; Sloan et al., 2013).

Soil temperature and availability of recent photosynthates have previously been linked to initiation of root growth (Abramoff & Finzi, 2015; Radville et al., 2016a). This study demonstrated that soil temperature was not a good or general cue for the start of the belowground growing season, even though a correlation between soil temperatures and root growth is often observed in seasonal environments (Abramoff & Finzi, 2015; Radville et al., 2016a). If aboveground cues, such as the availability of recent photosynthates, would be the main driver in initiating root growth, above- and belowground phenology should be tightly coupled in spring or root growth should lag behind leaf-out. Moreover, this coupling should be even stronger in heath, where many evergreen species are present that can photosynthesize immediately upon snowmelt. However, root growth started very early

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(before average leaf-out) and did not advance in a similar manner as aboveground phenology.

These findings demonstrate that the drivers of root phenology are still poorly understood, and that aboveground responses to environmental forcing cannot simply be translated belowground.

Deep roots in thawing permafrost

Paper III explored whether certain tundra species can benefit from

nitrogen availability at depth, and whether or not root dynamics change upon permafrost thaw and associated vegetation changes. It used a long-term permafrost thaw experiment and a short-long-term, deep-fertilization experiment (mimicking nitrogen release with permafrost thaw). Eriophorum vaginatum and Rubus chamaemorus, both deep-rooting tundra species, took up nitrogen released at the depth (50 cm) and time of maximum thaw (mid-October). Root depth distribution, growth and mortality changed dramatically in response to thawing permafrost. After a decade of permafrost thaw, dwarf shrubs abundance had decreased and abundance of the only graminoid present, E. vaginatum, had increased and this was mirrored in the root length responses of each plant functional type. Thereby increases in E. vaginatum mass were greater below- than aboveground. It has previously been shown that roots of E. vaginatum follow the thaw front over the season (Shaver & Billings, 1975, 1977). Consequently, with the increase in abundance of E. vaginatum, more roots were present deeper in the soil profile, even reaching into the thawed permafrost. In contrast to most tundra species, E. vaginatum has a high root turnover, which led to strong increases in root litter inputs both within the active layer as well as in thawed permafrost.

This study showed that contrary to previous assumptions (Koven et al., 2015), there is no mismatch between nitrogen availability with permafrost thaw and plant nutrient uptake. Root growth shifts into deeper layers over the season and, upon permafrost thaw, reaches into soil depths that have previously been detached from plant influences. Increased root growth and biomass can contribute to long-term soil carbon storage (Loya et al., 2002; Freschet et al., 2012), but increased root presence and litter inputs can also stimulate microbial decomposition from soil organic matter (Kuzyakov et al., 2000; Fontaine et al., 2007) and thus reduce soil carbon stocks. These changes in root dynamics are particularly important in the Arctic, because permafrost soils store large amounts of carbon with significance to the global climate system (Koven et al., 2015; Schuur et al., 2015).

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Short-and long-term absence of snow

Paper IV tested the effects of an absent snow cover during winter on plant

abundance. I examined shoot growth, phenology and visible frost damage of the two most common dwarf shrubs, Vaccinium myrtillus and V. vitis-idaea, in the understorey of a Norway spruce forest. In addition, root growth and root biomass were assessed. To compare short- and long-term effects of an absent snow cover, and to examine whether or not the responses from a short-term experiment can be extrapolated to long-term effects, this was done both in a short-term (1 year) and long-term (11 years) snow manipulation. A lack of snow cover during the winter exposed plants and soils to very low temperatures. This reduced plant abundance in the understorey, and led to aboveground frost damage in both dwarf shrub species, and reduced shoot elongation in V. myrtillus. In contrast to previous studies of freezing soil temperatures on root dynamics in forests (Tierney et al., 2001; Cleavitt et al., 2008), there was no compensatory root growth in the next growing season but instead reduced root growth and biomass. This discrepancy highlights the need for more studies on changing snow cover and root dynamics in mature forest systems.

This study included both a short-term and long-term experiment side-by-side, instead of comparing the results of the first year(s) of a study to later ones. The advantage of this approach was that other environmental parameters were similar at the time of measurement, offering a better comparison of short- and long-term effects. The comparison showed that ecologically significant changes already occurred after one year without snow cover, but also that long-term effects were less strong than what would be predicted from the short-term experiment.

Concluding remarks

Fine roots and their dynamics are a fundamental part of ecosystem functioning and influence patterns of terrestrial carbon, water and nutrient fluxes (Pendall et al., 2008; McCormack et al., 2013). As arctic ecosystems have one of the highest proportions of belowground biomass on the planet (Mokany et al., 2006), and high latitudes undergo the most far-reaching changes due to rapid climate warming (ACIA, 2004; IPCC, 2013), a profound understanding of form and function of roots in northern ecosystems is essential. Importantly, for the most pressing and least understood questions, i.e., those related to root function, we have to focus on the finest, ephemeral roots which are not captured with destructive sampling methods. This thesis aimed to improve our understanding of fine root dynamics in northern ecosystems, and provides important information on how root dynamics of different plant communities relate to aboveground dynamics, and how they

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respond to a variety of climate change factors. Several common threads were revealed in this thesis. First and foremost, I showed that aboveground patterns or responses cannot be directly translated to belowground responses (Paper I, Paper II, Paper III). These results urge a decoupling of above- and belowground phenology in terrestrial biosphere models, specifically including the possibility of root growth outside of the photosynthetically active period of tundra plants. This relates to the finding that responses of arctic and boreal ecosystems can diverge from those of temperate systems (Paper I, Paper IV), which is where a large portion of our knowledge about ecosystem processes comes from, and models thus need specific parameterization for northern ecosystems. In addition, this thesis showed that plant communities differ in root properties (Paper II, Paper IV), and that changes in plant community composition can thus induce changes in root dynamics. This may not be surprising, but underlines the importance of a thorough understanding of root dynamics in different plant community types, or species, in order to understand and predict how changes in plant communities in response to climate change, such as increases in shrubs (Myers-Smith et al., 2011) or graminoids (Natali et al., 2012), will affect root dynamics.

There are good reasons for the lack of available data on root dynamics in northern ecosystems, such as the methodological difficulties that are associated with studying roots in their natural environment, the inaccessibility of the Arctic in general, the interactions between different abiotic factors, and the struggle to relate observations at a millimetre scale to processes at an ecosystem or even global scale. It is unlikely that we will ever be able to compile data that is equally thorough belowground as aboveground, which is why it would be beneficial to use aboveground parameters to infer on belowground processes (Norby & Jackson, 2000; Sloan et al., 2013). Nevertheless, we need explicit root studies to find out for which response parameters these linkages are possible and for which they are not. In addition, established correlations between above- and belowground traits might change in the future, when above- and belowground responses to climate change factors vary and induce new relationships. With a deeper knowledge about these processes, we will be able to include the belowground compartment into models predicting vegetation responses to, and feedbacks on climatic changes. Roots have long been ‘out of sight, out of mind’ but are so essential for plant and ecosystem functioning, that we need to make them visible and reveal the hidden life of plants.

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Looking further

This thesis focused on community-level responses in natural conditions, as these allow conclusions for ‘real world’ responses, i.e., plant communities in their natural environment with interacting biotic and abiotic factors. However, this approach, as well as the observational nature of the studies, does not allow to distinguish between responses of single species, or to clearly disentangle co-varying environmental factors (such as snowmelt and soil temperature, or permafrost thaw and soil moisture). In order to distinguish between single species’ responses or effects of single environmental drivers, experiments under controlled conditions and with single species would be needed. As in any thesis, the amount of climate change factors that could be manipulated was limited, and future root studies would benefit from including other factors.

In addition, the results of this thesis are from a relatively restricted geographical area. Even if many different habitat and plant community types were included in this thesis, and both species and environmental drivers are similar to wider circumpolar areas, it would be good to expand these studies to other boreal and arctic areas.

Acknowledgements

Thanks to Ann Milbau, Roland Jansson, Scott Wilson and Signe Lett for commenting on previous drafts of this summary. The work of this thesis has been partly supported by the Climate Impacts Research Centre (CIRC), the Natural Sciences and Engineering Research Council of Canada (awarded to S. D. Wilson), the Kempe Foundation (awarded to A. Milbau), Stiftelsen Oscar och Lili Lamms Minne (awarded to A. Milbau), the Gunnar och Ruth Björkmans fond för norrländsk botanisk forskning (awarded to G. Blume-Werry), EU COST Action ‘ClimMani’ (ES1308, awarded to G. Blume-Blume-Werry), VR (Grant no. 621-2011-5444, awarded to E. Dorrepaal), Formas (Grant no. 214-2011-788, awarded to E. Dorrepaal), Wallenberg (Grant no. KAW 2012.0152, awarded to E. Dorrepaal). Krycklan is supported by SITES (VR), ForWater (Formas), Kempe Foundation, FOMA (SLU) and SKB. The Abisko Scientific Research Station provided climatic data and practical support throughout this thesis.

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Many thanks!

First and foremost, I want to thank my supervisors. Ann, thank you for the freedom and trust you gave me throughout this journey, thanks for pushing me, always valuing my opinion, for often wearing your heart on your sleeve, and for trying to teach me not to take things too seriously. Roland, thank you for your wonderful support, especially towards the end of this thesis, both in scientific and administrative struggles. Your understanding and encouraging attitude was a great addition to the team. Scott, thank you for sharing your experience with roots and minirhizotrons, and for all your advice during this time – always with a hint of irony and twinkle in the eye.

Apart from my team of supervisors, I have had the opportunity to work with other people that have guided and supported me throughout my PhD. Ellen, thank you for your dedication and guidance, for taking me to frozen ground and for ‘adopting’ me into your group. Jürgen, I’m not sure if you are aware of how much working with you during my master thesis has inspired me to do science. Thank you for always being encouraging, calm and clear, and having great ideas. Maggan and Hjalmar, both of you have let me work in your long-term and beloved experiments for which I am very grateful. You also share an ease to give compliments and get wonderfully excited, which makes working with you a joy. I still don’t know how it happened that after talking ten minutes to Hjalmar my thesis suddenly had a new chapter, but I am happy it did!

The staff at the Abisko Naturvetenskapliga Station has been great help and company over the years. Thanks to all of you! I feel very lucky to have spent so much time at the station, both during the long winters with quiet but cosy fika breaks and during the busy summers when the station feels like a beehive. It was great to be surrounded by so many researchers from all over the world united by the interest in arctic ecosystems.

Thanks to all colleagues at EMG ‘down in Umeå’, especially to those that always made me feel welcome when I was visiting. Thanks to the CIRC members, both present and former, for being a great group for scientific discussion! Thanks to those colleagues and friends in Abisko, Ann, Christian, Ellen, Erik, Eva, Frida, Gerard, Ive, Katie, Keith, Koko, Ludmilla, Makoto, Maria M, Maria V, Niklas, Per, Philipp, Rob, Stern, Sylvain, Tuukka and Tyler, for the above, but also for all the fun we had skiing, ice skating, climbing, at dance parties, barbeques, saunas, board games and so much more. Special thanks to Signe, for being a wonderful PhD colleague and a wonderful friend. I am so happy that we shared (almost) all the time of this journey!

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The work of this thesis would not have been possible without the help of many assistants in the field and lab. Over the years, I have met so many nice people and enjoyed their company: Adèle Binétruy, Peder Blomkvist, Jan Borgelt, Alisa Brandt, Emilie Eriksson, Charly Geron, Robert Holden, Maria-Theresa (Mia) Jessen, Frida Keuper, Marlene Kassel, Susanne Korff, Keith Larson, Niki Leblans, Jonathan Ramsay, Aline Schneider, Max Schuchardt, Viktor Sjöblom, Anna Sundelin and Ive Van Krunkelsven. Thanks to all of you for making long days go by quickly, for sharing the load of heavy equipment up and down mountains and through snow, for enduring mosquitoes, freezing hands, and uncooperative technology, but also for sharing the beauty of the mountains, the midnight sun, the autumn colours and the snow. Sorry to those of you that have gotten infected by the Abisko-fever, and some of you have it bad, I can tell you from experience that it is not something that can be cured easily…. Alisa and Mia, thank you both so much for the strained eyes and dreaming of roots, you were an incredible help! Sarah and Jan, thanks for being great students and making supervision such a nice experience, and for sharing your chocolate in moments of need. Maja, seven years ago we shared a cabin in Abisko, and you took me into the Arctic and introduced me to research. I doubt very much that I would be here now without that experience. Thanks for teaching me Swedish and for teaching me that hard work is only efficient when enjoying the breaks. Thanks to everyone else that made courses, conferences, coffee breaks or long journeys so much fun.

Many thanks also to my friends outside of this PhD, especially Esther, Rena and Paddy, for being wonderful company over so many years. I am so happy to have you in my life. Thanks to the Teubers, who let me take their son/brother/nephew/uncle to venture so far away, and still always make me feel welcome and part of the family.

Thanks to my parents and my brother, who not only do their best to understand what I am doing and why I would choose to live at the end of the world, but have also always supported and believed in me. Thank you Antje and Roland for initiating curiosity and the love of an adventure in Eike and me.

Laurenz, thank you for your understanding, your enthusiasm, being my rock, and for always rooting for me.

The hidden life of plants : fine root dynamics in northern ecosystems