The unseen iceberg: plant roots in arctic tundra.

Review

Tansley review The unseen iceberg: plant roots in arctic tundra Author for correspondence: Colleen M. Iversen Tel: +1 865 241 3961 Email: [email protected]

Colleen M. Iversen1,2, Victoria L. Sloan1,2, Patrick F. Sullivan3, Eugenie S. Euskirchen4, A. David McGuire5, Richard J. Norby1,2, Anthony P. Walker1,2, Jeffrey M. Warren1,2 and Stan D. Wullschleger1,2

Received: 4 December 2013 Accepted: 10 July 2014

1

Climate Change Science Institute, Oak Ridge National Laboratory, Oak Ridge, TN 37831, USA; 2Environmental Sciences Division,

Oak Ridge National Laboratory, Oak Ridge, TN 37831-6301, USA; 3Environment and Natural Resources Institute, University of Alaska, Anchorage, AK 99508, USA; 4Institute of Arctic Biology, University of Alaska, Fairbanks, AK 99775, USA; 5

US Geological Survey, Alaska Cooperative Fish and Wildlife Research, University of Alaska, Fairbanks, AK 99775, USA

Contents Summary

34

I.

Arctic tundra and plant roots: an introduction

35

II.

A comprehensive literature review

35

III.

A brief history of fine-root studies in tundra ecosystems

41

IV.

Distribution and dynamics of tundra plant roots: current knowledge and future directions

43

V.

Contribution of living plant roots to fluxes of CO2 and CH4 from tundra ecosystems to the atmosphere

49

VI.

The role of fine roots in tundra ecosystem nutrient cycling

50

VII.

Opportunities for improving the representation of root processes in arctic models

51

VIII.

Conclusions and priorities for future research

52

Acknowledgements

53

References

53

Summary New Phytologist (2015) 205: 34–58 doi: 10.1111/nph.13003

Key words: arctic, fine roots, model, plant–soil, root biomass, root production, root turnover, tundra.

34 New Phytologist (2015) 205: 34–58 www.newphytologist.com

Plant roots play a critical role in ecosystem function in arctic tundra, but root dynamics in these ecosystems are poorly understood. To address this knowledge gap, we synthesized available literature on tundra roots, including their distribution, dynamics and contribution to ecosystem carbon and nutrient fluxes, and highlighted key aspects of their representation in terrestrial biosphere models. Across all tundra ecosystems, belowground plant biomass exceeded aboveground biomass, with the exception of polar desert tundra. Roots were shallowly distributed in the thin layer of soil that thaws annually, and were often found in surface organic soil horizons. Root traits – including distribution, chemistry, anatomy and resource partitioning – play an important role in controlling plant species competition, and therefore ecosystem carbon and nutrient fluxes, under changing climatic conditions, but have only been quantified for a small fraction of tundra plants. Further, the annual production and mortality of fine roots are key components of ecosystem processes in tundra, but extant data are sparse. Tundra root traits and dynamics should be the focus of future research efforts. Better representation of the dynamics and characteristics of tundra roots will improve the utility of models for the evaluation of the responses of tundra ecosystems to changing environmental conditions.

No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

New Phytologist I. Arctic tundra and plant roots: an introduction Arctic tundra is a large and varied biome characterized by shortstatured plant communities rooted in a thin layer of seasonally thawed soil underlain by permafrost (Walker et al., 2005). Bordered at its southern edge by the boreal treeline, and by ocean or sea ice to the north, arctic tundra covers c. 8% of the global terrestrial vegetated land surface (McGuire et al., 2012). Soils in the permafrost region, including tundra and boreal forest, contain nearly one-half of global soil organic carbon (C), a large majority of which is held in soils that have been perennially frozen since the last glaciation (Tarnocai et al., 2009; Hugelius et al., 2013). The uptake and release of carbon dioxide (CO2) and methane (CH4) in tundra ecosystems play an important role in the current global C cycle (McGuire et al., 2009), and the vulnerability of permafrost C stocks is expected to be a key factor in the response of the terrestrial biosphere to changing atmospheric and climatic conditions (Schuur et al., 2008). Ecosystem C and nutrient cycles in tundra are driven by complex interactions between plant communities, soil processes, environmental variables and landscape geomorphology (Wookey et al., 2009). Plant community structure has been shown to exert important controls over feedbacks of energy, CO2 and CH4 between arctic ecosystems and the global climate (Eskelinen et al., 2009; Sturm, 2010; Cahoon et al., 2012; Hartley et al., 2012). However, studies to date have largely emphasized the importance of leaf and canopy properties. Differences in rooting distribution and root longevity among tundra plant species may also have important consequences for the climate system through changes in soil C and nitrogen (N) cycling and storage (Mack et al., 2004; Sullivan et al., 2007; Eskelinen et al., 2009; Hartley et al., 2012). Unfortunately, the dynamics of roots and the rhizosphere – the region in which the root interacts most closely with the surrounding soil – remain some of the least understood aspects of plant function in the Arctic. Models projecting future climate scenarios need to capture climate-induced changes in tundra plant community structure and function, both above- and belowground, as these changes will result in large feedbacks of CO2 and CH4 to the atmosphere (Euskirchen et al., 2009). However, the representation of roots is extremely simple in most large-scale models (Jackson et al., 2000; Iversen, 2010). Nevertheless, explicit model representation of the links between root dynamics and key ecosystem processes will advance our understanding of the contribution of roots to ecosystem C and N cycling under current climatic conditions, and will also improve our ability to project the response of land surfaces, including the tundra, to future climatic conditions. We undertook this review to better understand the response of tundra ecosystems to rapidly changing environmental conditions in the Arctic. Our primary goals were to highlight current knowledge of roots and their role in key ecosystem processes in arctic tundra, and to identify priority areas for future research. Within each of several focused sections, ranging from the distribution and dynamics of tundra roots to the contribution of roots to ecosystem C and nutrient cycling, we touched on four key themes: (1) how tundra root traits and processes may differ from those observed in other biomes; (2) the relationships between No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

Tansley review

Review 35

belowground and aboveground tundra plant traits; (3) the response of roots to changing edaphic and environmental conditions; and (4) priorities for future research on fine roots in tundra ecosystems. In addition, we compared current experimental and observational knowledge with the representation of tundra roots in models used to simulate C and nutrient cycling in the Arctic. Our goal was to determine to what extent different model conceptualizations and parameterizations are needed to accurately represent the range of root traits and processes of species found in arctic tundra ecosystems.

II. A comprehensive literature review We systematically identified and compiled data on root traits and root–soil interactions in arctic tundra (e.g. Table 1). We defined arctic tundra according to Walker et al. (2005): low-growing vegetation north of the arctic treeline, encompassing five bioclimatic subzones ranging from the cold and barren subzone A to the warmer and more vegetated subzone E (Fig. 1b). Because data on roots in arctic tundra are scarce, we also included data from sites with similar plant species or plant communities (e.g. ‘subarctic tundra’ in Abisko, Sweden, and ‘subalpine tundra’ in Eagle Creek, Alaska, USA). Data were compiled from various sources, including primary literature, books and theses. The combinations of species and plant traits across the tundra are a result of environmental conditions unique to the Arctic, including a 24-h photoperiod in summer with constant darkness in winter, continuous permafrost over large areas, and an increasing volume of soil accessible to plant roots over the course of a growing season. However, the knowledge base presented here indicates that, although the root traits and processes associated with plant species in tundra ecosystems are a response to extreme environmental conditions, the traits themselves are not unique and are observed in similar environments world-wide. Our main focus in this literature review was on ‘fine’ plant roots, which are an important component of ecosystem C and nutrient budgets because of their high respiration rates, high nutrient content, short lifespan relative to larger diameter woody roots and their role in stimulating microbial activity through the release of water and soluble exudates. Fine roots have generally been defined as < 2 mm in diameter (Pregitzer, 2002), and we used this definition here because it was most appropriate to the available literature. Recently, the definition of fine roots has evolved to a more functional characterization, where fine roots are short-lived, non-woody roots whose main function is the uptake of nutrients and water from the soil (Guo et al., 2008). This functional definition is more relevant for the understanding of root processes and their representation in large-scale models, and we discuss how future measurements might improve our functional understanding of roots in tundra ecosystems. Throughout our review of the empirical literature, we briefly highlight key aspects of the treatment of fine roots across a range of models that simulate ecosystem and land surface dynamics in systems underlain by permafrost (as in McGuire et al., 2012); we refer to these models throughout the remainder of this article using the more inclusive term ‘terrestrial biosphere models’. We focus in New Phytologist (2015) 205: 34–58 www.newphytologist.com

New Phytologist (2015) 205: 34–58 www.newphytologist.com –

1.4(18) 0.5–1.8(18, 23) 3.2–7.0(6, 40) 1.6(18) 1.2(18) 1.3(18) – 6.5–9.5(106) 0.1–0.3(64) –

–

13(18)

1–29(18, 23)

153–1305(6, 40) 4(18)

3(18)

3(18) –

4–51(106) 0.2–1(64)

–

79, 98, 133)

2(79) 1–565(18, 23, 42,

40, 41, 79)

High(42)

98, 133)

23, 42, 79,

0.4(79) 3.0–23.1(18,

40, 79)

3.4–22.6(6, 29,

–

–

219–1055(6, 29,

4.3(40)

512(40)

2.9(65)

0.7(79)

0.4(79)

11(65)

6.4–6.6(65)

Belowground/ aboveground ratio

8–88(65)

Belowground biomass (g m 2)

–

– 10–15(22, 24) 3.7(80)

0.5–4.1(18, 23) – 2.2(18)

42, 98, 133)

– 3.0–18.4(18, 23,

16.8(29)

2.9(65)

– 30(90); Deep(42)

90, 115)

15–46(22, 24,

–

–

– –

– – –

– 1.5(34)

– –

2.9(18) –

– –

5.0– 10.0(22)

3.7(34)

–

– –

–

–

1.8(18)

4.0–6.0(22) –

–

2.7(18)

–

–

–

50(90)

–

–

3.4(34)

Root pop. longevity (yr)

3.3(80)

–

–

–

20(90)

–

–

–

Max. rooting depth (cm)

6.4–6.6(65)

Fine-root/leaf ratio

– 0.7–1.2(92, 148)

54, 63)

0.5–1.7(29, 43,

–

–

– –

– –

–

– –

–

–

–

–

–

–

0.7(63)

Root tissue N (%)

– –

54, 63)

0.01– 0.38(29, 43,

–

–

– –

– –

–

– –

–

–

–

–

–

–

0.17(63)

Root tissue P (%)

124, 125)

– NM(58, 93, 97, 99,

NM(125)

–

NM(81)

NM(76) NM(81)

– AM(97, 125), NM(93, 99) AM(125), EcM(125), NM(125) AM(125) –

AM(125)

AM(125)

NM(93, 99), AM(93)

–

–

AM(97), NM(81)

NM(81,99)

Mycorrhizal association

– Yes(90)

Yes(44, 90); Extensive(115)

–

–

– –

– –

–

Yes(44) –

–

–

–

–

Yesb

–

–

Aerenchymous (% porosity)

– NO3-N(108); ON = NH4-N(85)

NH4-N(85); NH4-N ≥ ON(95)

–

NH4-N(112)

– –

– –

–

– –

–

–

–

–

–

–

–

Preferred form of N

Tansley review

Carex atrofusca Schkuhr Carex bigelowii Torr. ex Schwein.

Nardus stricta L. Phippsia algida (Sol.) R. Br. Poa arctica R. Br. Puccinellia angustata (R. Br.) Rand & Redf. Puccinellia phryganodes (Trin.) Scribn. & Merr. Puccinellia vaginata (Lange) Fernald & Weath. Sedges Carex aquatilis Wahlenb.

Festuca rubra L.

Grasses Alopecurus magellanicus Lam.a Anthoxanthum monticola (Bigelow) Veldkamp ssp. alpinum (Sw. ex Willd.) Sorenga Arctophila fulva (Trin.) Rupr. ex Andersson Calamagrostis canadensis (Michx.) P. Beauv. Calamagrostis lapponica (Wahlenb.) Hartm. Deschampsia cespitosa (L.) P. Beauv. Deschampsia flexuosa (L.) Trin. Dupontia fisheri R. Br.a Festuca ovina L.

PFTs Species

Table 1 Species-specific biomass, biomass ratios and root traits

36 Review

New Phytologist


No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust 5.3–22.9(11, 23) – 2.4–3.5(31) – 1.8–6.6(6, 79) – 0.5–39.6(14, 42, 73, 79, 98, 148) ; Low(42)

1.5(11) 1.8(65) – 3.8–126.6(40, 65)

–

1.1–5.6(18, 79) –

330–2105(11, 23)

–

1–10(31) – 24–735(6, 79)

–

61–1968(42, 73,

–

1(65)

–

17–571(40, 65)

–

2–11(18, 79)

–

Carex nigra (L.) Reichard Carex parallela (Laest) Sommerf. Carex rupestris All. Carex vaginata Tausch Eriophorum angustifolium Honck. Eriophorum scheuchzeri Hoppe Eriophorum vaginatum L.

Dasiphora fruticosa (L.) Rydb.a Salix alaxensis (Andersson) Coville Salix arctica Pall.

Schoenus nigricans L. Rushes Juncus albescens (Lange) Fernalda Luzula arctica Blytt ssp. arctica Luzula confusa Lindeberg Deciduous shrubs Alnus viridis (Chaix) DC. ssp. crispa (Aiton) Turrilla Arctostaphylos alpina (L.) Spreng. Betula glandulosa Michx. Betula nana L.

1.1(79) – 0.6–1.4(31, 64, 65)

–

4–67(31, 64, 65)

Intermediate(42)

;

60, 79, 98, 123, 134)

15(79)

79, 98, 123, 134)

21–1722(42, 59,

0.2–8.2(42, 59,

– 0.8–1.0(31) 1.5–3.3(31)

– 0.3–3(31) 8–16(31)

Carex capillaris L. Carex misandra R. Br. Carex nardina Fr.

79, 98, 148)


PFTs Species


Table 1 (Continued)

–

6.8(34) 8.5(34)

– –

– – –

– 40(90) –

3–30(59, 90, 134); Intermediate(42)

–

0.5(63)

–

–

123, 148)

60, 92, 99,

0.4–2.0(45, 54,

–

–

30(90)

–

–

–

–

–

40(90)

0.8(63)

–

–

–

–

–

0.06(63)

–

–

54, 60)

0.08–0.12(45,

–

–

–

0.14(63)

–

–

–

69, 74, 89, 109)

129, 148)

74, 92, 109,

0.03–0.88(41, 45, 48, 54, 56,

0.3–2.8(41, 45,

–

–

– – 0.07(101)

–

– – 0.09– 0.28(31, 63) –

Root tissue P (%)

48, 54, 56, 69,

–

–

– – 0.5–1.1(101)

–

35–40(59, 90, 91); Intermediate(42)

–

– – 1.0(22)

–

–

– – 0.7(63)

Root tissue N (%)

EcM(58, 76, 99, 125)

–

AM(125)

99, 124, 125)

EcM(58, 93, 97,

EcM(81)

EcM(93), AbM(99)

–

NM(76, 81)

–

–

AM(125); NM(125)

AM(125), NM(58, 124, 125)

NM(76)

– NM(93, 99, 110, 125) AM(125), NM(125)

NM(125), AM(125) NM(99)

– NM(125) NM(125)


–

–

–

–

–

–

–

–

–

–

–

Yes(78, 90) (12–33%)(91)

– – Yes(44, 90) (23–31%)(91) Yes(78, 145)

Yes(104) (27%)(104) –

– – –


–

–

ON(85, 99); NH4-N(85, 108, 132) ; ON ≥ NH4-N(85) –

–

–

–

–

–

–

NH4-N ≥ ON(85, 95, 108) ; NH4-N ≥ NO3-N(77, 78) ON ≥ NH4-N ≥ NO3-N(83) –

–

– NO3-N(132) NH4-N(85)

NO3-N(132)

–

– – –

Preferred form of N

Tansley review

3.7(65)

–

–

98, 123, 134)

0.4–7.0(42, 60,

–

9.6(18)

–

3.8–126.6(65)

–

1.8(65)

–

79, 148)

0.5–4.0(42, 73,

–

– – 25–40(22, 24, 90, 91)

– – –

–

–

– –

– – –


2.9(80) – –


–

12.9(23)

– – –


New Phytologist Review 37

New Phytologist (2015) 205: 34–58 www.newphytologist.com

New Phytologist (2015) 205: 34–58 www.newphytologist.com 6.1(23) 1.9(79) 1.5–3.5(42, 59, 1.8(23) 11.7(40) 0.8–4.6(11, 18) 0.1–4.3(18, 42, 59, 79, 98) ; Intermediate(42)

120(23) 5(79)

13–390(59, 79)

33(23)

471(40)

4–687(11, 18) 0.4–224(18, 42,

Salix lapponum L. Salix phlebophylla Andersson Salix pulchra Cham.

Salix reticulata L.

Salix rotundifolia Trautv. Vaccinium myrtillus L. Vaccinium uliginosum L.

Loiseleuria procumbens (L.) Desv.a Phyllodoce caerulea (L.) Bab. Rhododendron lapponicum (L.) Wahlenb. Vaccinium oxycoccos L.a

0.8–7.0(18, 42, 59, 60, 79, 98) ; Intermediate(42) 0.4(79) – –

1.5–2.0(59, 79)

13–299(18, 42,

–

–

0.3–1(59, 79)

17(79)

59, 79, 98)

–

–

; Intermediate(42)

134, 144)

134, 144)

0.6–10.2(11, 18, 42, 59, 70, 79,

2–1291(11, 18,

Empetrum nigrum L. ssp. hermaphroditum (Lange ex Hagerup) €cher1 Bo Harrimanella hypnoides (L.) Covillea Ledum palustre L.a

1.6–7.0(11, 23, 127)

59, 70, 79,

59–673

(11, 23)

64, 140)

–

–

–

2.9(80)

–

–

10(90)

–

60, 98)

20–40(47, 59, 90); Intermediate(42)

0.9(80)

10–15(59, 70, 90, 134, 144) ; Shallow(42)

–

– 10(90)

12.5–15(70, 144) 1.3–10(80, 90, 134)

0.4–20.9(18, 42,

–

1.4–2.0(18, 134)

4.4(23)

– –

79, 98, 134)

1.5(127) 0.1–3.7(11, 31,

79, 98, 134)

– 12–561(11, 31,

64, 140)

– 2.0–5.4(134)

0.7(80) 10–25(47, 59, 90); Intermediate(42)

–

– 3.3–22.2(18) 1.3–18.1(18, 42)

1.8(80)

6.1(23)

72, 134)

–

–

–

–

– –

–

54, 92)

0.7–1.3(45,

–

–

–

0.6–0.7(68, 134)

–

–

1.0–1.6(99)

– 0.7(63)

–

– –

0.7(68) 0.7–1.0(63,

– 0.4–1.3(54, 63)

– –

– 7.5(103)

–

–

–

–

54, 148)

0.9–1.5(45,

–

2.3(60)

20–30(59, 90)

– –

– –

– –

15.3(23) –

– –

– –

30(90) –

Root tissue N (%)

– 3.2–6.8(18, 23)




0.8–73.6(70, 79) 0.3–5.3(31, 32,

5–1251(70, 79) 4–1311(31, 32,

Dryas octopetala L.

Evergreen shrubs Andromeda polifolia L. Cassiope tetragona (L.) D. Don Diapensia lapponica L. Dryas integrifolia Vahl

59, 79, 98)

1.2(79) 1.4–9.3(11, 18, 23)

648(79) 3–148(11, 18, 23)

Salix glauca L. Salix herbacea L.

60, 79)


PFTs Species


Table 1 (Continued)

–

–

–

–

0.08– 0.11(45, 54)

–

0.07(68)

0.08(68) 0.05– 0.06(63, 72) – 0.06– 0.07(31, 63) –

– 0.12– 0.14(54, 63)

–

0.09– 0.14(45, 54) –

– –

– –

Root tissue P (%)

ErM(125)

ErM(93, 99)

ErM(97, 99, 125)

ErM(58, 125)

ErM(58, 99, 124, 125) , EcM(39)

ErM(97), EcM(97)

99, 124, 125)

AM(125), EcM(58, 93, 99, 125) ErM(58, 93, 97,

ErM(97, 99, 125) ErM(93, 97, 99, 125), EcM(39, 58) ErM(58, 125) EcM(39, 76)

97, 99, 124, 125)

ErM(97, 99, 125) ErM(58, 76, 93,

–

93, 97, 125)

EcM(58, 81,

–

EcM(97) EcM(93, 97, 125), EeM(125) EcM(125) –


–

ON(93, 99)

–

–

–

–

NH4-N(108); ON(85)

–

NH4-N ≥ NO3-N(132), ON(93, 99)

ON ≥ NH4-N(99)

– –

ON(99) ON(93, 99)

– ON(93, 99)

–

ON(85); ON = NH4-N(85) –

– –

– –

Preferred form of N

–

–

–

–

–

–

– –

– –

– –

–

–

–

– –

– –


38 Review Tansley review

New Phytologist


No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust 15.7(59) 0.5–7.4(79, 98) 2.2(23)

28(59)

0.2–9(79, 98)

25(23)

Petasites Mill. species

Polygonum bistorta L.

Polygonum viviparum L.

59, 70, 79, 98, 144)

;

40–50(46, 90, 144); Intermediate(42)

– – 5–10(34)

– 3.3(18) – 15.0(42)

4–11(34)

1.5–2.1(80)

20(90)

–

6.3(23)

–

30–50(59, 90)

7–29(34)

–

–

–

–

1.1(80)

– – – – 30(90)

– 8.8(18) 4.7(18) – –

–

100(90)

–

1.6(80)

– – 9.5(80)

5–10(47, 59, 90); Shallow(42)


–

–

–

– 5.9(18) –

42, 98)

0.7–6.0(18, 23,


–

– – 4.0(34)

1.1(45)

– – –

–

–

–

–

–

–

1.2(63)

2.1(63)

–

1.5(63) – – – –

–

–

–

–

–

– – – – –

–

–

–

– – –

–

–

–

–

0.11(63)

0.22(63)

–

0.22(63) – – – –

–

–

–

13.0(34)

–

–

–

– – –

0.11(54)

– – –

0.6–1.3(54, 92)

–

Root tissue P (%)

– – –

Root tissue N (%)


NM(125); AM(124)

EeM(125) AM(125) –

NM(76, 99, 125), (H), EcM(39) AM(58, 125), NM(125) AM(124, 125), NM(125) NM(81, 97), EcM(93, 97, 99, 125), AM(125) –

–

NM(81)

NM(76) AM(125) AM(125), NM(125) AM(125) NM(125)

AM(125)

AM(125), NM(93, 97, 99, 125) , H(99) –

AM(125), NM(125) – AM(97, 125)

ErM(58, 93, 97, 99, 124) ; EcM(39)


–

– – –

–

–

–

–

–

–

–

– – – – –

–

–

–

– – –

–


–

– – –

–

–

–

–

–

–

–

– – – – –

–

–

–

– – –

NH4-N ≥ ON(108), ON(93)

Preferred form of N

Tansley review

High(42)

59, 70, 79, 98, 144)

1.9–259.5(42, 46,

0.4–1.3(79, 98)

0.2–3(79, 98)

4–2050(42, 46,

0.1(64)

1–11(64)

0.5(79) 2.4(18) –

0.3(64)

0.2(64)

1(79) 7(18) –

0.1–0.2(64, 79) 6.4(18) 3.1(18) 0.8(79) –

0.1–0.4(64, 79) 62(18) 16(18) 1(79) –

–

–

–

–

–

–

Cerastium arcticum Lange Chamerion angustifolium (L.) Holub ssp. angustifoliuma Draba L. species Geranium sylvaticum L. Geum rivale L. Linnaea borealis L. Lupinus arcticus S. Watson Minuartia rubella (Wahlenb.) Hiern. Papaver radicatum Rottb. Pedicularis L. species

Potentilla nana Willd. ex Schltdl. Pyrola L. species Ranunculus acris L. Ranunculus sabinei R. Br. Rubus chamaemorus L.

–

–

1.0–4.0(18, 23, 42, 59, 79, 98) ; Intermediate(42)


0.2(79) 4.4(18) –

42, 59, 79, 98)

4–230(18, 23,


0.1(79) 50(18) –

Forbs Aconitum L. species Alchemilla vulgaris coll. Antennaria dioica (L.) Gaertn. Bartsia alpina L.

Vaccinium vitis-idaea L.

PFTs Species

Table 1 (Continued)

New Phytologist Review 39


New Phytologist (2015) 205: 34–58 www.newphytologist.com Belowground/ aboveground ratio 0.1–1.3(31, 64, 65)

–

0.5–4.6(65, 79) – 0.5(79)

3–104(31, 64, 65)

–

0.1–6(65, 79) –

1(79)

Saxifraga species L.

Solidago multiradiata Aiton var. arctica (DC.) Fernald1 Stellaria L. species Tofieldia pusilla (Michx.) Pers. Valeriana capitata Pall. ex Link –

2.5(65) –

–

1.3(65)


–

– –

– 1.5–1.9(80) –

–

–

–

4.6(80)



–

– –

–

–

Root tissue N (%)

–

– –

–

0.12(31)

Root tissue P (%)

AM(125), NM(125) AM(97, 125), NM(93, 99) –

AM(125), NM(81, 125), EcM(76) AM(97, 118, 125)


–

– –

–

–


–

– –

–

–

Preferred form of N

Tundra plant communities are relatively species poor and are dominated by plants that are able to survive the harsh environmental conditions of the Arctic (Barry et al., 1981; Shaver et al., 1986). To synthesize the root dynamics of broadly similar plant species for model representation, we rely on the concept of plant functional types (PFTs). Here, we use PFTs as described by Chapin et al. (1996), which were defined using tundra plant traits that would best represent the functional responses of plant communities to future climatic conditions, including woodiness, leaf lifespan and form, and the presence of aerenchyma: grasses, sedges, rushes, deciduous and evergreen shrubs, and forbs. We only include species for which data were available on root biomass, depth distribution or resource partitioning; there are many-fold more vascular species found in arctic tundra. Root biomass and belowground/aboveground ratio data may include stems and roots, or belowground stems only, but do not include plants grown in pots or sampled by digging up entire tillers (although nutrient concentration data were taken from pot and tiller studies, and rooting depth and root lifespan were taken from tiller studies). Nutrient values were chosen from peak standing crop (c. August) where seasonal measurements were made. The papers used to compile these data are found in Supporting Information Table S1, and the numbers in parentheses correspond to the numbers listed adjacent to each paper in Table S1. Data were taken from the ‘control’ treatment in studies that imposed an experimental manipulation; see individual papers for information on treatment responses. Where data were only available in figures, calipers were used to precisely determine values. Many studies did not measure species-specific root biomass, but did measure below- to aboveground ratios at the level of PFT; together with the data from Table 1, these measurements are presented in Fig. 3. We used the USDA Plants Database (http://plants.usda. gov/) to determine the appropriate classification of the tundra species. AbM, arbutoid mycorrhizal; AM, arbuscular mycorrhizal; EcM, ectomycorrhizal; EeM, ectendomycorrhizal; ErM, ericoid mycorrhizal; H, hemiparasite; NM, non-mycorrhizal. a Synonyms commonly appearing in the root literature are: Alopecurus magellanicus (Alopecurus alpinus); Anthoxanthum monticola ssp. alpinum (Hierochloe odorata, Hierochloe alpina); Dasiphora fruticosa (Potentilla fruticosa); Dupontia fisheri (Dupontia psilosantha); Juncus albescens (Juncus triglumis ssp. albescens); Empetrum nigrum ssp. hermaphroditum (Empetrum hermaphroditum); Harrimanella hypnoides (Cassiope hypnoides); Ledum palustre (Rhododendron tomentosum); Loiseleuria procumbens (Kalmia procumbens); Luzula arctica ssp. arctica (Luzula nivalis); Vaccinium oxycoccos (Oxycoccus microcarpus); Alnus viridis ssp. crispa (Alnus crispa); Dasiphora fruticosa (Potentilla fruticosa); Chamerion angustifolium ssp. angustifolium (Epilobium angustifolium); Potentilla nana (Potentilla hyparctica); Solidago multiradiata var. arctica (Solidago virgauera). b Methane emissions were measured from the stems of Arctophila fulva growing in standing water in a lake, indicating the presence of aerenchyma (Chanton et al., 1992).

PFTs Species


Table 1 (Continued)

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(a)

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(b)

Fig. 1 The area of tundra represented by studies examining some aspect of root ecology is generally limited to locations associated with long-term ecological research sites; data points are represented by filled circles overlain on two maps (n = 1039 species-specific sampling points). Map (a) is the Circum-Arctic Map of Permafrost and Ground Ice Conditions Map (Brown et al., 1997) and Map (b) is the Circum-Arctic Vegetation Map (Walker et al., 2005). Colors in (a) correspond to the extent of permafrost in the Arctic (i.e. continuous, C; discontinuous, D; isolated, I; and sporadic, S). Land mass north of 45°N not underlain by permafrost is represented in gray, and the map includes additional information on the location of lakes (dark blue) and glacier (stippled). Colors in (b) correspond to the different bioclimatic subzones in arctic tundra: Subzone A is characterized by cryptogam, forb barrens, and includes polar desert and semi-desert tundra; Subzone B is also characterized by cryptogam, forb barrens, but vegetated areas are characterized by graminoid- or prostrate dwarf shrub-dominated tundra; Subzone C is characterized by graminoid, prostrate dwarf shrub and forb tundra; Subzone D is characterized by areas of non-tussock sedge, dwarf shrub and moss tundra; and Subzone E is characterized by erect shrub vegetation (see Walker et al., 2005 for more detailed descriptions of bioclimatic subzones).

detail on a subsample of models that showcase a range of belowground representations (summarized in Table 2). The models were chosen based on their prevalence in tundra literature (ecosystem models) or their use in on-going model inter-comparison activities associated with the Vulnerability of Permafrost Carbon Research Coordination Network (land surface models). Models such as those presented here are necessary to understand and predict how future atmospheric and climatic change will alter tundra ecosystems. Most terrestrial biosphere models represent the complexity of vegetation dynamics at a global scale by aggregating plant species into plant functional types (PFTs) with similar form or function (Wullschleger et al., 2014). Although terrestrial biosphere models have recently begun to incorporate characteristics unique to tundra plants into PFTs (Miller & Smith, 2012), focus has been primarily on the aboveground plant components, with little attention paid to roots (Wullschleger et al., 2014). No single set of characteristics of roots and root processes can be used to describe the entire arctic region, but no work has assessed which root traits and processes are considered in these models, and which traits have not been considered at all (Table 3). We conclude this review with suggestions on a path forward to evaluate and improve the representation of fine roots in arctic models.

III. A brief history of fine-root studies in tundra ecosystems We found and assessed 149 studies that examined some aspect of root biomass, distribution, production, turnover or decomposition in arctic tundra (Supporting Information Table S1); this is a small body of work compared with the root literature available for temperate and tropical ecosystems. Many early studies on roots in arctic tundra focused on root biomass distribution, determined from excavated soil monoliths (e.g. Billings et al., 1973, 1976, 1977, 1978; Chapin, 1974; Shaver & Billings, 1977; No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

Chapin et al., 1980b; Kummerow et al., 1983). Net root production has been estimated using sequential soil coring and in-growth cores (Wielgolaski, 1975; Muc, 1977; Shaver et al., 1986; Nadelhoffer et al., 2002; Sullivan et al., 2007, 2008; Campioli et al., 2009; Sloan, 2011), and root population turnover has been estimated using ratios of living to dead tissue or tiller age (Shaver & Billings, 1975; Wielgolaski, 1975; Dennis, 1977). The production and mortality of individual roots have been quantified by tracing root elongation on a Plexiglas face of intact tundra blocks (Billings et al., 1977) and on the outer wall of a glass tube installed in the tundra and filled with sand (Bell & Bliss, 1978), and using minirhizotrons in a small number of more recent studies in Alaska, Greenland, northern Scandinavia and across Fennoscandia (Sullivan & Welker, 2005; Bj€ork et al., 2007; Sullivan et al., 2007, 2008; Sloan, 2011). Minirhizotrons have provided invaluable information on the production, phenology and turnover of fine-root populations in tundra ecosystems. However, excavated soil monoliths, where the main purpose is the quantification of soil characteristics, continue to be one of the main ways in which we gain information on tundra roots (e.g. Kutzbach et al., 2004; Mack et al., 2004; Ping et al., 2005; Borden et al., 2010). As with all aspects of arctic research, the area of tundra represented by studies examining some part of root ecology is generally limited to locations associated with long-term ecological research sites (Fig. 1a,b). These studies have overwhelmingly focused on graminoid and wetland tundra, but these plant community types represent a small fraction of the areal extent of tundra ecosystems (Walker et al., 2005), highlighting the lack of data for comprehensive assessment of tundra root dynamics. The root and rhizosphere dynamics of shrubs, which are projected to play an important role in climate-mediated changes in plant community composition and feedbacks of glasshouse gases to the atmosphere (Sturm, 2010), are increasingly a topic of investigation (Sullivan et al., 2007; Deslippe & Simard, 2011; Sloan et al., 2013). New Phytologist (2015) 205: 34–58 www.newphytologist.com


N/A

Implicit in wholeplant turnover N/A

Production

Turnover

Plants compete for soil N based on NUE

Respiration: None

Mycorrhizas Water uptake

Rootdependent N uptake

Carbon fluxes

N/A

Root litter allocated to soil pools based on C fractions; decomposition is f (SWC, air temperature, microbial efficiency)

Respiration: f (root N content, root C : N, air temperature) Exudation: None CH4 flux: None

f (root N content, air temperature)

None N/A

None

None Target C : N ratio

f (soil temperature, SWC, soil C : N)

Exudation: None CH4 flux: None (see Fan et al., 2013)

None: see peatland DOSTEM (Fan et al., 2013) None f (plant demand, root proportion, SWC) f (plant demand, root proportion and mass, root respiration, air temperature, SWC, available N) Respiration: f (root biomass, air temperature)

Balance of production and mortality Fixed partitioning: Target based on field data (root/ leaf = 0.1–1.7) Phenology: Same as leaves Standing crop/production (1–4 yr) Exponential decay of fraction with depth to maximum rooting depth None Target C : N ratio

DVM-DOS-TEM C and N cycle Multiple soil layers

Exudation: 17.5% of NPP CH4 flux: f (cross-sectional area of tillers; phenology; root depth) f (soil temperature, SWC)

Respiration: f (root biomass, root C : N, soil temperature)

Yes (flood-tolerant C3 graminoid PFT) None f (plant demand, root proportion, SWC) N/A

None N/A

Balance of production and mortality Functional balance: Nitrogen, moisture limitation (max root/ leaf = 1–5) Phenology: Same as leaves Fixed fraction 0.5–0.7 yr 1 (1.4–2 yr) 70–93% in upper soil

LPJ-GUESS WhyMe C cycle Multiple soil layers

Roots allocated to litter pools based on C fractions and N content; decomposition is f (soil temperature, SWC, O2, soil depth, soil mineral N availability)

Exudation: None CH4 flux: f (root porosity, root length, root depth)

Respiration: f (root biomass, root C : N, soil temperature)

Double-exponential for water; exponential for C inputs (decoupled from mass) None Fixed C : N and labile C: cellulose : lignin Root porosity differs by PFT; aerenchyma area f (NPP, LAI) None f (plant demand, root proportion, SWC) None

Phenology: Same as leaves Same as leaves (< 1 yr)

Balance of production and mortality Fixed partitioning (root/leaf = 1 for arctic PFT)

CLM4.5-BGC C and N cycle Multiple soil layers

Roots allocated to litter pools based on C fractions; decomposition is f (soil Temperature, SWC)

Respiration: f (root biomass, root C : N, soil temperature) Exudation: None CH4 flux: f (LAI)

None f (plant demand, root proportion, SWC) N/A

None Fixed C : N and lignin : N (implied) Not explicit

Exponential (decoupled from mass)

Phenology: Same as leaves Same as leaves (< 1 yr)

Balance of production and mortality Functional balance: Moisture, light limitation

Orchidee-WET C cycle Multiple soil layers

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ArcVeg and MBL-GEM III are community or ecosystem-scale models, and DVM-DOS-TEM, LPJ-GUESS WhyMe, CLM4.5BGC and ORCHIDEE are land surface models used at regional or global scales. ArcVeg does not explicitly represent the dynamics of fine roots, but root biomass and growth are considered implicitly in the growth and nitrogen (N) uptake of tundra vegetation (Epstein et al., 2000). DVM-DOS-TEM and LPJ-GUESS WhyMe are dynamic vegetation models (DVMs), whereby PFTs may compete for light, water and N depending on the model. There are other important arctic models (e.g. SiBCASA; Schaefer et al., 2008) that we did not include here because they simulate roots in ways already represented in this table. Key references for each model are as follows: ArcVeg (Epstein et al., 2000); MBL-GEM III (Rastetter et al., 1991; Le Dizes et al., 2003); DVM-DOS-TEM (Euskirchen et al., 2009; Yi et al., 2010; Yuan et al., 2012); LPJ GUESS-WhyMe (Smith et al., 2001; Wania et al., 2009, 2010; Miller & Smith, 2012); CLM4.5-BGC (Riley et al., 2011; Koven et al., 2013; Oleson et al., 2013); ORCHIDEE (Krinner et al., 2005; Koven et al., 2011; Ringeval et al., 2011). B/A, belowground/aboveground ratio; NPP, net primary production; NUE, nitrogen-uptake efficiency; PFT, plant functional type; SWC, soil water content; LAI, leaf area index. N/A, not applicable. Rootdependent N uptake indicates that modeled N uptake is dependent on the amount of root length or biomass.

Decomposition

N/A N/A

Aerenchyma

Exudation: None CH4 flux: None

N/A Implicit in wholeplant N content N/A

Morphology Chemistry

Depth distribution

Balance of production and mortality Functional balance: Nitrogen limitation

B/A = 2–25

Biomass

Phenology: Constant Fixed fraction 0.164 yr 1 (c. 6 yr) None

MBL-GEM III C and N cycle Single soil layer

ArcVeg C and N cycle Single soil layer

Model parameter/ process

Table 2 Representation of roots in models commonly used to simulate processes in arctic tundra

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Table 3 Summary of the degree of attention received by arctic root traits and processes in models commonly used to simulate processes in arctic tundra (as in Table 2)

Arctic root trait

Relative data availability

Conceptual representation in models

Parameter estimation specific to the arctic

Model validation specific to the arctic

Parameter sensitivity/ uncertainty analyses specific to the arctic

Root biomass Root morphology Root depth distribution Root production Root phenology Root turnover Root decomposition Root respiration Root exudation Root transport of CH4 Root nutrient uptake Timing of resource acquisition Mycorrhizal symbioses Root nutrient content

+++ + +++ + + + ++ + + + ++ + ++ +++

+++ None + +++ + +++ +++ +++ + + + + None +

+ None + + None + + + None + + + None +

+ None + + None + + None None + + + None +

None None None None None None None None None + None None None None

We provide a comparison of relative data availability for various root traits as many (+++), some (++) or limited (+) data available. For models, the entries of ‘+++’, ‘++ and +’ and ‘none’ indicate that the issue has been considered by most, some or none of the models for a particular step in the modeling process. Conceptual consideration refers to whether the general root issue is considered in models, whereas parameter estimations, validation and parameter sensitivity/uncertainty analysis refer to whether these issues are specifically focused on tundra roots. Noteworthy disconnections between tundra root observations and model representation are: (1) the lack of a conceptual representation for links between root morphology and root function in models, and (2) although root production and turnover are generally well represented in terrestrial biosphere models, there are few data from tundra ecosystems to support the parameterization of these processes. These areas should be priorities for future tundra root research.

IV. Distribution and dynamics of tundra plant roots: current knowledge and future directions 1. Biomass The relative amount of C partitioned belowground exerts important controls over biogeochemical cycling in biomes from the tropics to the tundra (Jobbagy & Jackson, 2000, 2001). Across the Arctic tundra, belowground plant biomass exceeded aboveground biomass (Fig. 2), indicating that aboveground biomass is just the ‘tip of the iceberg’ in these ecosystems. Indeed, some studies estimated that up to 90% of vascular plant biomass in tundra was belowground (Kjelvik & K€arenlampi, 1975; Chapin et al., 1980b; Tikhomirov et al., 1981; Bliss & Svoboda, 1984; Wallen, 1986; Henry et al., 1990; Campioli et al., 2009). A conspicuous exception was the barren, polar desert and semidesert tundra (e.g. Fig. 2), where root biomass was a relatively small component of total plant biomass (Bell & Bliss, 1978; Bliss & Svoboda, 1984; Bliss et al., 1984). The ratio of belowground to aboveground biomass for tundra PFTs ranged from a median of 0.7 for forbs to 5.1 for sedges (Table 1; Fig. 3), although this can change somewhat over the course of a growing season (e.g. Bell & Bliss, 1978). These ratios were large compared with recent estimates of belowground to aboveground ratios in other biomes, which ranged from a median of c. 0.2–0.6 in forests, c. 4 in shrublands and c. 1.9–4.5 in grasslands (Mokany et al., 2006). Although impressive, the relative amount of belowground biomass in tundra does not reflect the importance of small-diameter, short-lived fine roots, because they are not differentiated from coarse roots and rhizomes. Coarse roots No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

and rhizomes have a high mass, but essentially act as storage organs, whereas fine roots have much less mass, but a high surface area to mass ratio for resource acquisition (Guo et al., 2008). This problem is exacerbated by environmental conditions in the Arctic, where organic soils accumulate over stems of prostrate shrubs, which can have 15–20 times more biomass than fine roots (Shaver & Cutler, 1979; Chapin et al., 1980b; Miller et al., 1982; Wallen, 1986; Hobbie & Chapin, 1998). Furthermore, although the ratio of belowground to aboveground biomass in tundra was large relative to that of other biomes, the absolute amount of root biomass in low-productivity tundra tended to be relatively small in comparison. Tundra root biomass in our literature review ranged from 0.1 to c. 3700 g m 2, averaging c. 350 g m 2 (Table 1; Fig. 2); comparable values in forests and temperate grasslands averaged c. 5000 and 1400 g m 2, respectively (Jackson et al., 1996). Increased plant investment in root biomass is often associated with limited soil resources, and plant production in tundra is strongly limited by the availability of soil N, soil phosphorus (P), or both (Chapin, 1974; Caldwell, 1987; Shaver & Chapin, 1995). It has also been suggested that the large investment in belowground biomass, especially in belowground stems and rhizomes used for carbohydrate and nutrient storage and vegetative propagation, is related to harsh environmental conditions in tundra, including low temperatures, high soil moisture, high winds or high levels of grazing (Webber, 1977; Dennis et al., 1978; Chapin & Slack, 1979; Chapin et al., 1980a; Wielgolaski et al., 1981). At the environmental extreme of polar desert tundra ecosystems, relatively low investment in belowground biomass relative to other tundra ecosystems may be a result of the cushion growth forms, stunted New Phytologist (2015) 205: 34–58 www.newphytologist.com

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Fig. 2 Below- and aboveground biomass for tundra plant functional types. The dashed line indicates a 1 : 1 line; data points that fall above this line indicate relatively larger belowground biomass than aboveground biomass. The inset is a closer view of biomass data ranging from 0 to 100 g m 2. Data from forbs growing in polar desert tundra ecosystems were plotted separately to highlight their generally low biomass and low relative belowground biomass. (Data from the polar desert were dominated by forbs, but also included a few samples from shrub and graminoid PFTs that are not plotted, where belowground biomass ranged from 12 to 67 g m 2 and 0.2 to 519 g m 2, respectively.) Belowground data may include stems and roots, or belowground stems only, but do not include plants grown in pots or sampled by digging up entire tillers. The papers used to compile these data are found in Supporting Information Table S1.

growth and low percentage cover of many of the plant species, the relative unimportance of rhizomes for carbohydrate storage, as well as cold soil temperatures or low soil water potentials, and soil instability related to frost-heave and cracking (e.g. Bell & Bliss, 1978; Bliss et al., 1984). One caveat when estimating root biomass from tundra and similar ecosystems is that cold, saturated, and often acidic soil conditions limit the decomposition of dead roots, and the proportion of total root mass in tundra soil that is alive and functional can be quite small (Billings et al., 1978; Kummerow & Krause, 1982). For example, the percentage of living roots in soil can range from < 5% to > 80% of total root mass (Dennis & Johnson, 1970; Kjelvik & K€arenlampi, 1975; Wielgolaski, 1975; Dennis, 1977; Muc, 1977; Tikhomirov et al., 1981; Bliss & Svoboda, 1984; Henry et al., 1990; Hill & Henry, 2011). Many studies specifically indicated that they quantified the mass of living roots, but we urge caution in the interpretation of the literature given that some studies were not explicit regarding this division. Future research should focus on the quantification and characterization of living fine roots, particularly for shrubs, which will play an important role in tundra community response to changing environmental conditions (Walker et al., 2006; Sturm, 2010), and for which we have relatively little information (Table 1). Although radioisotope analyses or staining can assist with the differentiation of living from dead roots (e.g. Wielgolaski, 1975; Muc, 1977; Bell & Bliss, 1978), new sampling strategies will be required to improve our understanding of the relative role of living roots involved in resource acquisition in tundra ecosystems. New Phytologist (2015) 205: 34–58 www.newphytologist.com

We know from other biomes that root morphology is strongly linked with root function and chemistry; distal roots (i.e. ‘firstorder’ roots) tend to have narrower diameters, higher nutrient content, shorter lifespans and greater mycorrhizal colonization than higher order roots (Guo et al., 2008; Valenzuela-Estrada et al., 2008). This functional approach needs to be applied to the study of tundra roots. A few studies have indicated that distal roots < 250 lm in diameter make up a large fraction of fine-root biomass across a number of tundra ecosystems, and that these roots have the largest rates of resource acquisition, exudation and radial O2 loss resulting in rhizosphere oxidation (Chapin & Tryon, 1982; Miller et al., 1982; Jones, 1998; Olsrud & Christensen, 2004; Laanbroek, 2010). However, root traits differ strongly among species and PFTs (e.g. Fig. 4), and the morphological characteristics and root branching patterns of individual tundra plant species can take years to develop (e.g. Bell & Bliss, 1978). Quantification of root morphology, anatomy and chemistry, and associated function, will require careful and species-specific collection of intact root branches of mature tundra plants. A better understanding of the effects of environmental change on the relative amount of C partitioned belowground to roots is also needed. Perhaps the largest outstanding question in arctic tundra is related to the effects of warming, and interactions between warming and soil nutrient availability, on relative belowground C partitioning (Walker et al., 2008). Data on root response to increased nutrient availability in tundra are inconclusive, in part because of the challenge of separating community-level from species-level root responses to nutrient availability. In some instances, plants invested relatively less biomass in fine roots as nutrient availability increased across a range of tundra ecosystems, No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

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Fig. 3 The belowground to aboveground biomass ratio of five major plant functional types was nearly always > 1 (dashed line), indicating that root biomass is equal to or greater than aboveground biomass in most tundra ecosystems. The line in each bar is the median value, and the bar encompasses the 25th–75th percentile; whiskers are the 10th and 90th percentiles, and the outliers are shown as gray circles. There were four data points associated with the ‘Rush’ PFT (ranging from 1.8 to 126.6) which are not represented in this figure. The mean and number of data points for each PFT were: grass (3.3, n = 20); sedge (8.2, n = 59); forb (6.3, n = 63); deciduous shrub (2.7, n = 60); evergreen shrub (3.2, n = 82). Ratio estimates from polar desert tundra ecosystems were included in PFT ranges, but generally fall as outliers at the low end of the belowground to aboveground ratios.

and also within a given ecosystem in response to greater nutrient availability through fertilization and warming (Wielgolaski, 1975; Dennis, 1977; McGraw & Chapin, 1989; Chapin & Shaver, 1996; Clemmensen et al., 2006; Sullivan et al., 2008; Sloan et al., 2013). However, this was not true in all studies (van Wijk et al., 2003; Clemmensen et al., 2006; Bj€ork et al., 2007; Sullivan et al., 2007, 2008). Further studies of community- and species-specific response to fertilization addition are warranted, and these studies should consider the timing, duration, type and amount of fertilizer added. Models simulating processes in tundra generally represent root biomass as the result of a balance between root productivity and turnover (Table 2), but they do not reproduce the relatively large fraction of belowground biomass observed across all tundra PFTs. This could be a result of the assumption in some models that root production rate is equal to that of leaves (e.g. Oleson et al., 2013), and also to the relatively fast turnover times of roots in the models as compared with observations (Sloan et al., 2013; Table 2). 2. Distribution The distribution of roots throughout the soil profile determines patterns of nutrient and water acquisition, interaction among roots and soil microbial communities, and the contribution of root litter to soil C and nutrient accumulation (e.g. Jobbagy & Jackson, 2000). Compared with other biomes, rooting distributions in arctic tundra are extremely shallow. A previous compilation of literature found that c. 96% of tundra root mass was found in the top 30 cm of the soil profile, compared with only 52–83% in temperate and No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

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tropical biomes (Jackson et al., 1996). Shallow rooting distributions were a common observation across different tundra ecosystems, including wet, coastal tundra (Dennis & Johnson, 1970; Dennis, 1977), moist, acidic tussock tundra and non-acidic tussock tundra (van Wijk et al., 2003; Sullivan et al., 2007; Borden et al., 2010), subarctic and arctic shrublands and meadows (Wielgolaski, 1975; Michelsen et al., 1996; Campioli et al., 2009; Deslippe & Simard, 2011) and the High Arctic (Muc, 1977; Bliss et al., 1984; Joabsson & Christensen, 2001). The vertical distribution of roots in tundra is constrained by the limited thickness of the ‘active layer’ (i.e. the layer of soil that thaws each year) in soils underlain by permafrost (e.g. Borden et al., 2010). The thaw depth of the active layer, which can range from a shallow 20 cm to > 1 m in thickness, changes seasonally and annually depending on the soil temperature at the end of winter, the air temperature during the growing season, soil insulation by organic soils or mosses, solar radiation, soil moisture and vegetation leaf area (e.g. Dennis & Johnson, 1970; van der Wal et al., 2001; Str€om et al., 2012; Yi et al., 2013). Rocky terrain on ridge tops and fellfields can also limit rooting depth to very shallow soils (< 5 cm; Campioli et al., 2009), as can frost-heave, where vertical soil shifts of up to 3 cm yr 1 can damage roots (Jonasson & Callaghan, 1992). In addition, the pooling of water at the surface of some soils underlain by permafrost can create an anoxic environment, which further restricts the rooting depth of species that lack special adaptations to withstand anaerobic conditions (Hinzman et al., 1991; Gebauer et al., 1996; Kutzbach et al., 2004). Most belowground biomass in tundra ecosystems, including fine roots and their mycorrhizal fungal associates, rhizomes and belowground stems, are found in a shallow layer of organic matter at the soil surface that has accumulated as a result of limited decomposition rates in cold, sometimes saturated, arctic soils (Bell & Bliss, 1978; Shaver & Cutler, 1979; Miller et al., 1982; Kielland, 1994; BassiriRad et al., 1996; Gebauer et al., 1996; Michelsen et al., 1996; Ping et al., 1998, 2005; Clemmensen et al., 2006; Bardgett et al., 2007; Bj€ork et al., 2007; Campioli et al., 2009; Borden et al., 2010; Harden et al., 2012). Greater root growth in shallow organic soil layers may be a result of differences in nutrient and water availability between the organic and mineral soil layers (Tieszen et al., 1981; Miller et al., 1984; Hinzman et al., 1991; Harms & Jones, 2012), as well as the fact that soil temperature drops precipitously throughout the active layer, ranging from up to 20°C at the soil surface to 0°C at the bottom of the thawed layer (Shaver & Billings, 1977). However, PFTs in tundra exhibit inherent differences in their vertical root distribution (Table 1). A number of studies, based on soil profiles, minirhizotron observations and plant acquisition of the stable 15N isotope, have indicated that sedges tend to be more deeply rooted in the soil profile than shrubs and forbs (Shaver & Cutler, 1979; Miller et al., 1982; Marion et al., 1987; Chapin & Shaver, 1996; Nadelhoffer et al., 1996; McKane et al., 2002; Sullivan et al., 2007; Sloan, 2011). Rooting depth distributions also differ among species within traditionally defined PFTs (Shaver & Billings, 1975, 1977; Billings et al., 1978; Table 1). Species-specific differences in rooting depth distribution have important implications for plant competition, and therefore New Phytologist (2015) 205: 34–58 www.newphytologist.com

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(b)

(a)

(c)

(d)

(e)

1 cm Fig. 4 Contrasting root morphologies of selected Arctic plant species sampled at Barrow, Alaska, in July 2012. (a) Saxifraga cernua (forb, non-mycorrhizal); (b) Salix pulchra (deciduous shrub, ectomycorrhizal); (c) Dupontia fisheri (grass/wet tundra graminoid, non-mycorrhizal, numerous root hairs on first-order roots); (d) Eriophorum angustifolium (sedge/wet tundra graminoid, non-mycorrhizal, roots either unbranched or with few sparse laterals); (e) Vaccinium vitis-idaea (evergreen shrub, ericoid mycorrhizal). Photo credits: V. Sloan. Sedge and grass roots are either produced mainly at the stem base (in E. angustifolium) or at new, spreading tillers in the case of Carex aquatilis and D. fisherii (Shaver & Billings, 1975). Root morphology and color vary among plant €rk et al., 2007). For example, species colonizing arctic tundra, even those within similar plant functional types (Chapin et al., 1980b; Miller et al., 1982, 1984; Bjo ericaceous shrub roots have an average diameter < 100 lm (Valenzuela-Estrada et al., 2008), whereas the diameter of sedge roots is an order of magnitude larger (Chapin, 1974; Sullivan & Welker, 2005), in part to support aerenchyma formation in anaerobic soils (e.g. Chapin, 1974). The morphological characteristics of plants growing in tundra ecosystems (e.g. diameter, tensile strength, growth form, growth angle and branching pattern) may better adapt them to horizontal and vertical soil movement related to freeze–thaw cycles and patterned ground (Bell & Bliss, 1978; Jonasson & Callaghan, 1992).

ecosystem C and nutrient fluxes, in response to changing environmental conditions. For example, a shift in species composition from a more deeply-rooted to a more shallowly-rooted species in response to long-term fertilization in acidic tussock tundra probably contributed to large losses of soil organic C from deeper soils over time because of an imbalance between root litter inputs and the decomposition of organic matter in deeper soil (Sullivan et al., 2007). A better understanding of the relative importance of speciesspecific preferences, soil properties and environmental conditions in controlling rooting depth distribution will allow us to better understand and predict the responses of plant communities to future climate change, including warming and increased resource availability. The confinement of most plant roots to upper organic New Phytologist (2015) 205: 34–58 www.newphytologist.com

horizons suggests that, although global warming may cause a deepening of the active layer into lower mineral horizons, this may not have a large effect on rooting depth distribution unless the thickness of the organic layer also increases in response to warming (e.g. Gebauer et al., 1996; Bj€ork et al., 2007). Indeed, warming has been found to shift rooting distributions upward into the organic soil layer in some tundra ecosystems (Bj€ork et al., 2007). Root distribution over multiple soil layers is a recent addition to many terrestrial biosphere models, although distributions are static rather than dynamic, and most models do not implement root production or mortality for a given depth layer (Table 2). The inclusion of an organic soil horizon in models could potentially serve as a general bound on the representation of rooting depth distribution for many tundra ecosystems (e.g. Yuan et al., 2012). No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

New Phytologist 3. Production The few direct measurements of annual root production in tundra ecosystems indicate that fine roots are a relatively large fraction of plant net primary production (NPP). Estimates of root contribution to total annual vascular NPP ranged from 30% to 90% in sedge-dominated tundra (Chapin et al., 1988; Henry et al., 1990; Nadelhoffer et al., 2002; Sullivan et al., 2008; Sloan, 2011), and from 10% to 60% in tundra dominated by shrubs (Kjelvik & K€arenlampi, 1975; Wielgolaski, 1975; Campioli et al., 2009; Sloan, 2011). Emerging patterns in production across species and ecosystems are difficult to summarize given that there are very few data on the growth, phenology and lifespan of fine roots in tundra. The paucity of data is mainly a result of the fact that minirhizotrons have not been used to track the dynamics of individual roots across the vast majority of the tundra. Minirhizotron use has perhaps been limited because of the remoteness of tundra sites, which precludes weekly, bi-weekly or monthly image collection, but also because characteristics associated with saturated, cold sites can complicate minirhizotron installation and anchorage, the capture and analysis of minirhizotron images, and the upscaling of minirhizotron data (reviewed in Iversen et al., 2012). However, these issues can be overcome, and minirhizotrons have provided invaluable information on root production and turnover when used in studies of shrub and tussock tundra (Sullivan & Welker, 2005; Sullivan et al., 2007, 2008; Sloan et al., 2013). Roots of many arctic species have relatively low optimal temperatures for initiation and growth compared with closely related species in temperate climates (Chapin, 1974, 1978; Shaver & Billings, 1975; Billings et al., 1977, 1978; Bell & Bliss, 1978; Ellis & Kummerow, 1982). A high tolerance for low soil temperatures allows roots to function in cold, arctic soils, and may allow roots to elongate early in the growing season and grow more deeply into the soil profile (Billings et al., 1977, 1978; Shaver & Cutler, 1979; Marion et al., 1987; Gebauer et al., 1996; Nadelhoffer et al., 1996; Sloan, 2011; Keuper et al., 2012). Indeed, roots of some arctic sedges have been shown to elongate directly on top of permafrost (or at temperatures < 0°C) without damage, or to resume growth within hours after thaw (Billings et al., 1977, 1978; Shaver & Billings, 1977; Ellis & Kummerow, 1982). However, root temperature tolerance appears to differ among arctic species (Shaver & Billings, 1975, 1977; Billings et al., 1978). Although tundra roots have a high tolerance for cold, root growth and tiller formation responded positively to warming in some, but not all, dominant graminoid species in wet and tussock tundra (Billings et al., 1977; Chapin, 1978; Kummerow et al., 1980; Sullivan & Welker, 2005) and polar semidesert (Bell & Bliss, 1978). However, too much warming may be detrimental to root growth in tundra ecosystems, as root respiration at higher temperatures may exhaust root reserves of non-structural carbohydrates (Bell & Bliss, 1978; Ellis & Kummerow, 1982). Given the adaptation of tundra plants to low temperatures, factors other than temperature may exert equally important controls over root growth (Chapin, 1981, 1983). Tundra ecosystems are exposed to a 24-h photoperiod over much of the growing No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

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season (Barry et al., 1981). Root growth may be correlated with light availability (ostensibly through interactions with photosynthesis and resulting C availability); under controlled laboratory conditions, root growth slowed and even stopped at day lengths < 15 h (Shaver & Billings, 1977; Billings et al., 1978). Water availability in tundra is rarely limited enough to reduce annual productivity or cause mortality under current climatic conditions (Billings & Mooney, 1968; Miller et al., 1978; Tieszen et al., 1981; but see Bell & Bliss, 1978), but saturated soil may limit root growth (e.g. Billings et al., 1977). As portions of the tundra become warmer and drier in response to changing climatic conditions – in some cases associated with shifting microtopography in response to permafrost degradation – the interplay between plant water demand, root growth and water uptake, and the soil–plant– atmosphere continuum, will be an important area for future research (Shaver et al., 1979; Stewart & Freedman, 1994; McGuire et al., 2009). Minirhizotron-based measurements of the initiation and growth of tundra roots, and the response of root growth to changing environmental conditions, are high priorities for the next generation of tundra ecosystem measurements. These measurements will also help to inform model representation of root production. Currently, models allocate a portion of primary production to fine roots based either on a fixed partitioning ratio specified for different PFTs, or through a functional balance, resource limitation approach, whereby the partitioning of production to roots increases with some combination of increasing nutrient or water limitation, or decreasing light limitation (Table 2). 4. Phenology The timing of root production has important implications for plant access to nutrients in thawing soil, and also for fluxes of C from the land surface to the atmosphere (e.g. McConnell et al., 2013). In tundra, belowground production has been predicted to be asynchronous with aboveground production, given that soil temperature peaks later in the growing season than solar irradiance (Sullivan & Welker, 2005; Sloan, 2011). Indeed, across a wide range of shrub tundra communities in Fennoscandia, root production rates were low during periods of peak leaf production in the early summer, and increased towards the end of the growing season, immediately before leaf senescence (Wielgolaski, 1975; Olsrud & Christensen, 2004; Sloan, 2011); a similar pattern was observed for forbs and rushes in polar semidesert (Bell & Bliss, 1978). Furthermore, roots may remain active in the soil after aboveground senescence, supporting the notion that the ‘growing season’ is longer than aboveground green vegetation would indicate (Chapin & Bloom, 1976). Although the tussock-forming sedge, Eriophorum vaginatum, also initiated root production later in the summer than leaf production (Chapin, 1974; Kummerow & Russell, 1980; Shaver et al., 1986; Sullivan & Welker, 2005), the predicted asynchronous growth pattern did not always hold true in tundra dominated by sedges or grasses, where the timing of root production was similar to, or earlier than, leaf production (Allessio & Tieszen, 1975; Bell & Bliss, 1978; Sloan, 2011). New Phytologist (2015) 205: 34–58 www.newphytologist.com

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Models generally link the phenology of root production with the phenology of leaves (Table 2), but representing the asynchronous phenology observed in the roots and leaves of some important tundra ecosystems may improve model simulations of plant growth and nutrient uptake, soil CO2 efflux and plant-mediated soil CH4 fluxes. 5. Turnover Across the globe, the lifespan of individual roots is species specific, increases with increasing root order, and changes in response to environmental variables, including nutrient availability, water and temperature (e.g. Eissenstat & Yanai, 1997; Valenzuela-Estrada et al., 2008). Roots from high-latitude ecosystems may have a longer lifespan than roots from locations nearer the equator because of colder temperatures, low nutrient availability and long leaf lifespans of some arctic plants (Eissenstat & Yanai, 1997; Gill & Jackson, 2000). Population-level estimates of root turnover (the relative fraction of a root population that is replaced each year under equilibrium conditions) can be calculated as the ratio of annual root production to peak root standing crop; the inverse of turnover is the average lifespan of the root population (Gill & Jackson, 2000). This calculation assumes that root production and mortality are in equilibrium, and that peak root mass consists solely of living roots (Eissenstat & Yanai, 1997), which may require careful consideration in many tundra ecosystems. The few estimates of root lifespan from tundra ecosystems – many based on calculations of population-level turnover rates – differed among dominant plant species (Table 1). The average fine-root population lifespan of grasses, sedges, rushes, shrubs and forbs was estimated at > 5 yr across a range of tundra ecosystems (Shaver & Billings, 1975; Dennis, 1977; Bell & Bliss, 1978; Billings et al., 1978; Sullivan et al., 2007, 2008; Sloan, 2011), which is similar to previous estimates of root population turnover in high-latitude ecosystems (Gill & Jackson, 2000). Exceptions were sedges in the Eriophorum genus, which have roots that only live for 1–2 yr (Chapin, 1974; Shaver & Billings, 1975; Sullivan et al., 2007; Sloan, 2011), which is simlar to the lifespan of fine roots of the forb, Phippsia algida, in polar semidesert (Bell & Bliss, 1978). The lifespan of first-order, ephemeral, roots has been linked with root traits, including diameter, specific root length and chemistry, as well as plant traits such as wood density, in temperate forest trees (reviewed in McCormack et al., 2012). However, we have little information on the controls over root lifespan in tundra ecosystems, and we could not find any data on the lifespan of individual roots of tundra plants. Lifespan measurements in tundra may be hindered by freeze–thaw dynamics that shift minirhizotron tubes, making it difficult to track individual roots, and by slow decomposition rates in saturated ecosystems, which make it difficult to pinpoint the timing of root death from minirhizotron images (e.g. Iversen et al., 2012). However, an increased focus on direct measurements of the lifespan of individual tundra roots could avoid some of the artifacts potentially associated with population-level estimates of root turnover (reviewed in Eissenstat & Yanai, 1997). New Phytologist (2015) 205: 34–58 www.newphytologist.com

Given the importance of root longevity to ecosystem C and nutrient fluxes, the development of relationships among plant traits and root lifespan is a key area for future research. For example, root and leaf lifespans were positively correlated in shrub tundra, although the relative rate of root turnover was much lower than that of leaves (Sloan, 2011; Sloan et al., 2013), indicating that root turnover may be estimated from more easily made aboveground measurements. An exploration of the linkages between leaf and root turnover rates is a good subject area for future research (e.g. Withington et al., 2006) in order to determine to what extent this relationship is broadly generalizable across tundra ecosystems. This information can be used to inform parameterization of root turnover in models, especially those that simulate root turnover rate as the same as leaf turnover rate (Table 2). 6. Decomposition Decaying fine roots are an important and persistent source of soil organic matter in tundra because of the relatively large amounts of belowground biomass and low rates of root decomposition (Hobbie, 1996; Parton et al., 2007; Harmon et al., 2009; Freschet et al., 2012a,b). Root inputs in tundra affect the chemistry of soil organic matter and the composition of microbial communities, contribute to the formation of raised ‘tussocks’ in tussock tundra, and contribute to the accumulation of C in long-term soil organic matter pools, including in deeper soil (Chapin et al., 1996; Gebauer et al., 1996; Loya et al., 2002; Nowinski et al., 2008; Eskelinen et al., 2009). Litter C : N and lignin : N ratios are often used as a proxy for ‘decomposability’ by empiricists and modelers alike. As in temperate biomes, decomposition of roots from tundra plant species was positively related to root carbohydrate content, and negatively related to root lignin content (Hobbie, 1996). However, our understanding of the decomposition of plant tissues is evolving from a focus on single chemical parameters to a more holistic understanding, in which the natural variation in plant traits can be used as a tool to understand the relationship between plant function and its surrounding environment (Cornwell et al., 2008). Natural covariation in plant traits related to nutrient acquisition and conservation (e.g. tissue structure and chemistry) exerts important controls over the decomposition of leaf, stem and fineroot litter world-wide (Cornwell et al., 2008; Freschet et al., 2012a, b, 2013). Indeed, in tundra ecosystems, variation among plant species and functional types was more important than environmental conditions as a driver of root decomposition (Hobbie, 1996; Hobbie et al., 2000; Freschet et al., 2012a,b). In general, roots of deciduous and evergreen shrubs tended to decompose more slowly than sedge and forb roots (Hobbie, 1996; Freschet et al., 2012a). Although it is generally believed that N and P content are the same for living and dead roots based on a long-held assumption that nutrients are not resorbed from roots during senescence (Chapin et al., 1978; Aerts et al., 1992), this assumption has recently been challenged in the subarctic. New calculations indicate that roots may resorb between 3% and 75% of N and between 18% and 80% of P as they senesce (Freschet et al., 2010b), which has important No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

New Phytologist implications both for decomposition methodology (i.e. the substitution of living roots as root ‘litter’) and our understanding of tundra ecosystem C and nutrient fluxes. Environmental conditions also exert strong controls over root decomposition in arctic tundra. Root decomposition generally increases in response to natural and experimental increases in soil temperature (Hobbie, 1996; Hobbie et al., 2000; Parton et al., 2007). Water availability plays an important role in mediating the response of litter decomposition in tundra (Rosswall et al., 1975; Aerts, 2006); at one extreme, saturated soil conditions common in wet tundra may limit litter decomposition, whereas, at the other extreme, limited water availability may constrain the extent to which microbial populations can respond to warmer temperatures (Rosswall et al., 1975; Hobbie et al., 2000; Aerts, 2006). Globally, root decomposition rates were greatest in warm, moist environments, and lowest in cold, dry environments (Parton et al., 2007). Strong freeze–thaw mechanics unique to frozen soils (Washburn, 1973) also affect root decomposition rates and nutrient release through physical processes, such as tissue damage and associated leaching of labile material; decomposition can be greatest during the freeze–thaw season (i.e. the autumn and spring), rather than during summer months (Hobbie & Chapin, 1996; Wu et al., 2010). Importantly for parameterization of the decomposition of fine roots in models for which little belowground information exists, the relative decomposition rates of leaf, stem and root litter were strongly correlated among species, although roots tended to decompose more slowly than leaf litter (Freschet et al., 2012a). More studies that examine the interactions among plant traits – above- and belowground – with their surrounding environment to determine litter decomposition are needed for arctic ecosystems (e.g. Freschet et al., 2012b). However, it is worth considering that models do not currently represent the complicated covariance among litter traits, or their effects on decomposition (Table 2). Further, no models currently simulate the potential physical effects of freeze–thaw dynamics on root decomposition, and many models consider nutrient resorption from fine roots to be negligible (but see Euskirchen et al., 2009).

V. Contribution of living plant roots to fluxes of CO2 and CH4 from tundra ecosystems to the atmosphere Feedbacks of CO2 and CH4 from the tundra land surface to the atmosphere have global implications (McGuire et al., 2009). Living roots in tundra ecosystems contribute to ecosystem C fluxes through respiration (Crow & Wieder, 2005; Segal & Sullivan, 2014), and through the release (‘exudation’) of low-molecularweight compounds, including organic acids and amino acids, that fuel microbial biosynthesis and respiration of CO2 and CH4 (Jones, 1998; Hicks Pries et al., 2013). Roots with aerenchyma also serve as passive conduits for CH4 flux to the atmosphere (Str€om et al., 2012), and can affect the production of CO2 vs CH4 through oxygenation of the rhizosphere (Gebauer et al., 1996). The relative importance of these processes has major implications for the global climate, as CH4 has c. 30 times the long-term global warming potential of CO2, on a mass basis (Myhre et al., 2013, table 8.7). No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

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Repeated, seasonal measurements indicate that root respiration can contribute > 50% of tundra soil CO2 efflux, and from 15% to 45% of whole ecosystem respiration, depending on the time of the season, soil temperature and depth of thaw (Billings et al., 1977; Hicks Pries et al., 2013; McConnell et al., 2013; Segal & Sullivan, 2014). Root respiration in tundra ecosystems is correlated with root N or P content, although the strength of the relationship varies among tundra plant species (Chapin & Tryon, 1982; Limbach et al., 1982; Segal & Sullivan, 2014). In particular, roots with a short lifespan (e.g. Eriophorum sedges) had greater respiration rates per unit root mass than other species (Segal & Sullivan, 2014), and greater than predicted based on nutrient concentration (Billings et al., 1977; Chapin & Tryon, 1982). This could be related to the high respiration rates observed in young, actively elongating, unsuberized roots with high rates of nutrient absorption (Chapin, 1974; Billings et al., 1977; Chapin & Tryon, 1982). Root respiration increased exponentially with increases in soil temperature (Q10 ~ 1.5–2.5; Billings et al., 1977; Limbach et al., 1982; BassiriRad et al., 1996; Segal & Sullivan, 2014). Estimates of the sensitivity of root respiration to temperature and nutrient content across species and root orders can help to constrain ecosystem C budgets, as well as model simulations of land surface CO2 fluxes (Table 2). Root exudation of low-molecular-weight compounds is an important C source for microbial populations (Jones, 1998), including those in tundra soils (Hicks Pries et al., 2013). Organic acids derived from root exudates are also an important, and continuous, substrate for methanogenesis in tundra ecosystems € with anaerobic soils (Joabsson & Christensen, 2001; Oquist & Svensson, 2002; Str€om et al., 2003, 2012). Exudate production appears to differ among plant species, even within similar functional groups. For example, exudation by sedges in the Eriophorum genus tended to be high compared with other graminoids, although this was dependent on soil nutrient availability (Str€om et al., 2003, 2005, 2012; Koelbener et al., 2010). Further, exudation rates may change seasonally, increasing in autumn to facilitate the accumulation of nutrients for the following spring (Olsrud & Christensen, 2004). In temperate systems, studies have focused on the importance of rhizosphere priming (i.e. the stimulation or suppression of soil organic matter decomposition through root exudation) and its response to changing environmental conditions (Cheng et al., 2014). This could be an interesting, and important, avenue for future work in tundra ecosystems. Root exudates are starting to be included in terrestrial biosphere models (Table 2), in part because of their importance to methane emissions from high-latitude wetlands (Wania et al., 2009). Arctic soils, especially those underlain by continuous permafrost, are frequently flooded or frozen during part or all of the growing season, which limits the diffusion of oxygen belowground to support root metabolism (Gebauer et al., 1996; Vartapetian & Jackson, 1997; Kutzbach et al., 2004). A common morphological adaptation of plants to reduce stress under anaerobic soil conditions is the development of aerenchyma – enlarged and interconnected intercellular gas spaces in roots and stems that facilitate the transport of oxygen from the atmosphere to roots (Vartapetian & New Phytologist (2015) 205: 34–58 www.newphytologist.com

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Jackson, 1997). Aerenchyma formation has been observed in tundra plants that inhabit flooded or saturated sites, including sedge species of the Carex and Eriophorum genera, but also in grasses, Dupontia fisheri and Arctophila fulva, which could be characterized as ‘wet tundra’ graminoids (Table 1). Plants with aerenchyma serve as passive conduits for CH4 flux to the atmosphere, bypassing aerobic soil regions that would otherwise support methane oxidation (Torn & Chapin, 1993; € Schimel, 1995; Oquist & Svensson, 2002; Str€om et al., 2012). Plant-mediated CH4 flux in wet tundra has been estimated to range from < 33% to nearly 100% of total ecosystem CH4 fluxes, depending on plant species composition, microtopography and depth to water table (Torn & Chapin, 1993; Schimel, 1995; Kutzbach et al., 2004). A competing process, radial O2 loss from roots via aerenchyma – evidenced by iron oxide deposits in the soil surrounding aerenchymous sedge roots in tundra ecosystems (e.g. Koch et al., 1991) – can suppress methanogenesis and oxygenate CH4 to CO2 (reviewed in Laanbroek, 2010). The presence or absence of aerenchymous roots was found to be an important variable differentiating tundra PFTs (Chapin et al., 1996). However, we have very little information on which species of sedges and grasses are aerenchymous (Table 1), and only infrequent measurements of the extent of root porosity for tundra plants. Tundra root porosity, and how it varies with root morphology, root age and changing environmental conditions, is needed to predict the effects of tundra plants on losses of CH4 and CO2 to the atmosphere (e.g. Gebauer et al., 1996; Kutzbach et al., 2004). Furthermore, simulated global CH4 emissions are highly sensitive to aerenchyma properties and plant-mediated CH4 oxidation (Table 2), indicating the need for additional data from saturated tundra ecosystems (Riley et al., 2011).

VI. The role of fine roots in tundra ecosystem nutrient cycling The relative amount of nutrients acquired by plant roots is a key determinant of species persistence in tundra ecosystems under current and future environmental conditions (e.g. van Wijk et al., 2003). Competition for soil N between plants and microbes is especially strong in nutrient-limited tundra (Schimel & Chapin, 1996; Grogan & Jonasson, 2003; Henry & Jefferies, 2003; Bardgett et al., 2007; Sorensen et al., 2008). Furthermore, mosses and lichens, even without rooting systems, are also important competitors for nutrients in the Arctic (Marion et al., 1987; Tye et al., 2005). A general consensus has emerged that tundra plants are able to take up many forms of N, including amino acids, NH4+, and NO3 (Koch et al., 1991; Atkin et al., 1993; Chapin et al., 1993; Kielland, 1994; Atkin, 1996; Nadelhoffer et al., 1996; McKane et al., 2002; Tye et al., 2005; Clemmensen et al., 2008; Sorensen et al., 2008). However, the relative availability of mineral and organic N can differ among tundra ecosystems (Kielland, 1994; Atkin, 1996; Gebauer et al., 1996; Sorensen et al., 2008), and there are conflicting reports on the relative importance of mineral N compared with organic soil N for plant uptake (Chapin et al., 1993; Schimel & Chapin, 1996; Henry & Jefferies, 2003; Hobbie & New Phytologist (2015) 205: 34–58 www.newphytologist.com

New Phytologist Hobbie, 2006; N€asholm et al., 2009). In addition, acidic, infertile, anaerobic and cold conditions in tundra tend to limit soil nitrification, and plant-available NO3 is relatively low compared with NH4+ and organic N (Atkin & Cummins, 1994; Kielland, 1994; Atkin, 1996; Gebauer et al., 1996; Michelsen et al., 1996; Tye et al., 2005; Sorensen et al., 2008; Keuper et al., 2012). There appear to be species-specific differences in the preferential uptake of different N forms (Chapin et al., 1993; Kielland, 1994; Michelsen et al., 1996; Nadelhoffer et al., 1996; McKane et al., 2002; Sorensen et al., 2008). Our synthesis of the few data available on this topic indicated that species in the Carex genus may prefer NO3 , whereas other sedges, grasses and shrubs may prefer organic N or NH4+ (Table 1). Differences in the relative availability of different forms of N under changing climatic conditions might affect the competitive ability of species in a given plant community (Chapin & Bloom, 1976; McKane et al., 2002; Walker et al., 2006; Hill & Henry, 2011). For example, a preference for NO3 could prove useful if ratios of NO3 to NH4+ increase in response to drier, warmer soil conditions (Nadelhoffer et al., 1991; Atkin, 1996). Factorial fertilization experiments have indicated that slowly cycling soil P also limits plant production in tundra ecosystems (Chapin, 1978; Chapin et al., 1978; Shaver & Chapin, 1995), and P availability may drive the distribution of a number of important graminoid tundra species (Webber, 1978). Sedges (especially Carex species) had rates of P uptake that were an order of magnitude greater than other species, although rates differed among species, across microtopographic gradients and in response to defoliation (Chapin & Slack, 1979; Shaver et al., 1979; Chapin & Tryon, 1982; Kielland & Chapin, 1994). Plants in nutrient-limited ecosystems have evolved ways to increase their access to a limited pool of soil nutrients. For example, nutrient limitation increased the exudation rates of some tundra plants, which resulted in increased microbial nutrient mineralization (Koelbener et al., 2010). The development of biotic interactions with mycorrhizal fungi may also play an important role in increasing plant access to limited soil nutrients (Kielland, 1994; Read et al., 2004). Between 61% and 86% of foliar N in some tundra plant species is obtained via mycorrhizal fungi, which, in turn, receive between 8% and 17% of photosynthetic C for growth and respiration (Hobbie & Hobbie, 2006; Deslippe & Simard, 2011). Mycorrhizal associations occur in many tundra plant species (Table 1; Fig. 4). Generally, roots of grasses, sedges and forbs were non-mycorrhizal or associated with arbuscular mycorrhizas, whereas woody shrubs tended to associate with ericoid or ectomycorrhizal fungi. Forb communities tended to have the lowest, and shrub communities the highest, amount of mycorrhizal biomass, and mycorrhizal colonization tended to be infrequent or absent in polar desert tundra (Miller, 1982; Newsham et al., 2009). Plant species forming associations with ericoid or ectomycorrhizal fungi with the ability to break down complex polymers into simple organic compounds through the release of extracellular enzymes are considered to have an advantage over nonmycorrhizal plants in nutrient acquisition (Kielland, 1994; Michelsen et al., 1996, 1998; Read et al., 2004; Hobbie & Hobbie, 2006; Clemmensen et al., 2008). Indeed, mycorrhizal No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

New Phytologist colonization may explain the preference of shrub species for organic N (Table 1), as mycorrhizas in tundra ecosystems show a strong preference for glycine (and NH4+) over NO3 (Clemmensen et al., 2008). Further, the association of ericaceous shrubs with ericoid mycorrhizal fungi, combined with extremely fine roots (as narrow as 40 lm in diameter), improved their access to soil P (reviewed in Read et al., 2004), and arbuscular mycorrhizas have also been found to be important for plant P acquisition in arctic tundra (reviewed in Newsham et al., 2009). Although mycorrhizas are not simulated in any of the terrestrial biosphere models reviewed here (Table 2), their demonstrated importance to tundra ecosystem C and nutrient budgets makes them a prime candidate for model inclusion (e.g. Orwin et al., 2011). Given the differences in root phenology among PFTs, seasonal variation in nutrient availability also has important implications for plant nutrient acquisition. Although tundra plants are capable of taking up N during snowmelt when soil temperatures are still at or below freezing, this N does not appear to be an important component of annual N uptake in tundra systems, perhaps in part because of competition from microbes (Bilbrough et al., 2000; Edwards & Jefferies, 2010). Instead, late-season nutrient uptake may be a disproportionately important component of annual plant nutrient acquisition in tundra. In contrast with non-permafrost ecosystems, the volume of soil accessible to plant roots increases throughout the growing season as the active layer thaws (Chapin et al., 1980a; Shaver et al., 1986; Gebauer et al., 1996). Further, tundra plant roots continue to acquire and store nutrients when aboveground tissue is largely sencescent (Chapin & Bloom, 1976). However, this delicate balance may change in response to warming, which increased early root growth in tussock tundra (Sullivan & Welker, 2005), perhaps allowing plants increased access to the earlyseason peak in nutrient availability (Weintraub & Schimel, 2005). Differences in rooting depth distribution among tundra plant species (Table 1) may also have important implications for plant competition and plant community composition under future environmental conditions. Recent work indicates that deeply rooted plant species may benefit from access to additional N released near the bottom of the active layer as previously stable permafrost thaws in response to warmer temperatures (Keuper, 2012; Keuper et al., 2012). However, we are unaware of any other simultaneous measurements of relative rooting depth distribution and the cumulative availability of soil nutrients in the thawing active layer. Technological advances, including novel instrumentation to simultaneously track root and fungal dynamics in concert with soil environmental conditions (e.g. Hernandez & Allen, 2013), could help to improve our understanding of the root– soil interface in tundra, and help to inform the relatively meager representation of plant–soil interactions in current arctic models (e.g. McGuire et al., 2010; Koven et al., 2013; Table 2). The recycling of nutrients is often more important than the uptake of available soil nutrients to sustain plant production in nutrient-limited tundra (Chapin et al., 1975). Tundra plants tend to maintain higher nutrient concentrations in fine roots relative to temperate species (Table 1). This may be because of the high rates of production and metabolic activity associated with short growing No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

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seasons and cold temperatures in the Arctic (Chapin, 1981, 1983), or colonization with mycorrhizal fungi with a high tissue nutrient content (Michelsen et al., 1998; Clemmensen et al., 2006). Many tundra plant species are highly dependent on belowground stores of C and nutrients for growth (Chapin & Bloom, 1976; Chapin & Slack, 1979; Chapin et al., 1980b; Maessen et al., 1983; Shaver et al., 1986; Shaver & Chapin, 1991), and some sedges have been shown to survive for years by relying solely on internal nutrient supplies (Shaver et al., 1979). Plant nutrient demand in models is often simulated as a function of target C : N ratios that models aim to maintain (e.g. Oleson et al., 2013; Table 2). However, the target C : N ratio of fine roots in some large-scale models is universally applied, rather than specific to individual PFTs (e.g. Oleson et al., 2013), and often does not vary with environmental conditions. Given the paucity of data on tundra root nutrient content (Table 1), relationships among root, leaf and stem chemistry (e.g. the ‘plant economics spectrum’, Freschet et al., 2010a) could be used to derive PFT-specific C : N for tundra roots.

VII. Opportunities for improving the representation of root processes in arctic models Models are needed to understand and predict the role of arctic tundra in the current and future global C cycle. However, the representation of roots is extremely simple in most large-scale models, including those used to simulate processes in arctic tundra. Although most of the models considered here conceptually represent root biomass, root production, root decomposition, and root respiration, some root traits, such as root morphology or mycorrhizal symbioses, are not represented. Furthermore, few models explicitly represent interactions between roots and the surrounding soil (Tables 2, 3). Even where root traits and processes are considered by arctic models, many of the models do not parameterize or validate these processes specifically for the Arctic (Table 3, but see Euskirchen et al., 2009). Of the models that explicitly represent processes for the Arctic, some use multiple PFTs to represent the variety of plant functions in tundra ecosystems (Euskirchen et al., 2009), whereas others use just one PFT to represent all arctic tundra plants (Oleson et al., 2013). The knowledge base reviewed here indicates that species and PFTs in arctic tundra have many strategies for root biomass allocation, growth, and resource uptake (e.g. Table 1 and Fig. 3), and that a single parameterization will not capture important tundra root processes and associated changes in ecosystem function. Given the diversity of approaches for the inclusion of root processes in models and for the simulation of tundra root structure and function, our recommendations for improved data–model interactions are three-fold: (1) a critical evaluation of the importance of conceptual representations of root processes for model projections of tundra land surface C and nutrient fluxes; (2) the development of values for root-related model parameters that are specific to arctic vegetation; and (3) comprehensive sensitivity and uncertainty analyses to evaluate whether model behavior is adequately constrained by extant data. This review identifies New Phytologist (2015) 205: 34–58 www.newphytologist.com

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information that is currently available for better testing and parameterization of root processes represented in arctic models, and these data can serve as the beginning of a tundra root trait database that could be expanded for future model benchmarking (Iversen et al., 2014). We recommend starting with a systematic evaluation of model conceptual representations of root production and turnover to determine at which spatial or temporal scales different representations of these processes make a difference in arctic model dynamics. Conceptual representation of processes not currently included in arctic models (e.g. Table 3) will also be important for future model evaluation, and those root traits and processes that substantively affect model behavior should be given priority for future data collection.

VIII. Conclusions and priorities for future research Arctic tundra is a unique and varied biome in which plant growth, the cycling of nutrients and water, and the activity of soil organisms are inextricably bound together by plant roots in a thin layer of thawed soil. Throughout our review of tundra root distribution and dynamics, and their role in ecosystem C and nutrient cycles, we touched on several key themes:

New Phytologist (1) Tundra root distribution and dynamics differ in many ways from those observed in other biomes. Compared with other biomes, arctic tundra is inhabited by plant species that allocate a relatively large fraction of their biomass belowground. Tundra plants tend to be more shallowly rooted, and have roots with relatively lower optimal growth temperatures, a longer lifespan and higher nutrient concentrations compared with closely related species in temperate climates. Tundra plants also have root traits that increase their access to a limited pool of soil nutrients, but the root traits themselves are not unique, and are observed in similar environments world-wide. (2) There are strong linkages between belowground and aboveground tundra plant traits. Relative belowground biomass allocation differs in predictable ways among tundra PFTs, as does the synchronicity of root and leaf phenology, and mycorrhizal associations. There are tantalizing links between root and leaf lifespan, and also significant covariation among the decomposition rates of roots, leaves and wood for many tundra plant species. (3) Edaphic and environmental conditions exert important controls over tundra root distribution and dynamics. The most obvious edaphic control over rooting distribution and dynamics in tundra is the limited thickness of the active layer, which limits

Fig. 5 Many lingering questions remain to be addressed to improve our understanding of tundra ecosystems. These questions are focused in large part on species-specific root growth and lifespan, root functional traits and root–soil interactions, and how these characteristics and processes change in response to changing environmental conditions (e.g. warming and increased nutrient availability). We have highlighted in gray the highest priorities for future research on tundra roots: linking root form with root function for individual tundra plant species and quantifying root dynamics (including production, lifespan and turnover) in response to changing environmental conditions. Technology developed or improved over the past several decades, including minirhizotrons and soil observatories, can help researchers to address some of these major questions. Furthermore, linkages between below- and aboveground traits will help to scale root properties to the ecosystem and landscape level. Root and soil image from Miller et al. (1982) (used with permission from John Wiley and Sons). Image is a cross-section of dwarf shrub tundra near Berry Camp, Alaska, where the plant community includes shallowly rooted Vaccinium vitis-idaea and larger and more deeply rooted Salix pulchra. New Phytologist (2015) 205: 34–58 www.newphytologist.com


New Phytologist rooting depth distribution. Other edaphic and environmental conditions, such as soil nutrient availability, soil temperature, soil moisture and photoperiod, affect tundra plant belowground C allocation, and root growth, respiration, exudation and decomposition. (4) There are clear priorities for future research on fine roots in tundra ecosystems. Despite a history of research on roots in arctic tundra that stretches back to the early days of the International Biological Programme (1964), our knowledge of tundra root dynamics is limited. The available data do not wholly capture the heterogeneity of the arctic region, making it difficult to know whether models are accurately representing the arctic landscape. Therefore, the burden of the data–model interaction in tundra falls disproportionately on the shoulders of empirical scientists. Given the gaps in the knowledge base reviewed here, we feel that the highest priorities for future research on tundra roots fall into two broad categories: (1) linking root form with root function for individual tundra plant species, and (2) quantifying root dynamics (including production, lifespan and turnover) in response to changing environmental conditions, such as warming and increased nutrient availability. Although these are the highest measurement priorities moving forwards, there are many fundamental knowledge gaps that remain to be addressed to improve our understanding and model representation of tundra ecosystems; we have listed some of these in Fig. 5. Our vision for future research on root traits and root dynamics is in the context of species interactions and competition for resources in a changing environment rather than to fill holes in a catalog of static species properties. The capacity for change in root traits and dynamics, at both the species and ecosystem levels, will be an important determinant of tundra plant community composition, and therefore ecosystem C and nutrient fluxes, under changing climatic conditions. Empiricists and modelers alike face the challenge of developing innovative ways to migrate emerging fine-scale knowledge about root structure and function to larger scales (Warren et al., 2014). The arctic community is beginning to tackle this through multiscale modeling approaches, modularization, and parameterizations that explicitly take into account both temporal and spatial scales. A strong and iterative relationship between field measurements and model structure and process will improve our understanding of the complex world beneath our feet, and the important role that roots will play in the response of tundra ecosystems to an uncertain future. Furthermore, model–data interaction, including sensitivity and uncertainty analyses, can help the community of empirical scientists to determine when we have a sufficient knowledge base to understand and predict tundra ecosystem function, and the important role of roots in contributing to important ecosystem processes. We have made a good start, but have so far only uncovered the tip of the iceberg.

Acknowledgements The Next-Generation Ecosystem Experiments (NGEE Arctic) project is supported by the Office of Biological and Environmental Research in the US Department of Energy Office of Science. Oak No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

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Ridge National Laboratory is managed by UT-Battelle, LLC, for the US Department of Energy under contract DE-AC0500OR22725. Thank you to Santonu Goswami for assistance in preparing Fig. 1.

References Aerts R. 2006. The freezer defrosting: global warming and litter decomposition rates in cold biomes. Journal of Ecology 94: 713–724. Aerts R, Bakker C, Decaluwe H. 1992. Root turnover as determinant of the cycling of C, N, and P in a dry heathland ecosystem. Biogeochemistry 15: 175–190. Allessio ML, Tieszen LL. 1975. Patterns of carbon allocation in an arctic tundra grass, Dupontia fischeri (Gramineae), at Barrow, Alaska. American Journal of Botany 62: 797–807. Atkin OK. 1996. Reassessing the nitrogen relations of Arctic plants: a mini-review. Plant, Cell & Environment 19: 695–704. Atkin OK, Cummins WR. 1994. The effect of root temperature on the induction of nitrate reductase activites and nitrogen uptake rates in arctic plant species. Plant and Soil 159: 187–197. Atkin OK, Villar R, Cummins WR. 1993. The ability of several high arctic plant species to utilize nitrate-nitrogen under field conditions. Oecologia 96: 239–245. Bardgett RD, van der Wal R, Jonsdottir IS, Quirk H, Dutton S. 2007. Temporal variability in plant and soil nitrogen pools in a high-Arctic ecosystem. Soil Biology & Biochemistry 39: 2129–2137. Barry RG, Courtin GM, Labine C. 1981. Tundra climates. In: Bliss LC, Heal OW, Moore JJ, eds. Tundra ecosystems: a comparative analysis. New York, NY, USA: Cambridge University Press, 81–114. BassiriRad H, Tissue DT, Reynolds JF, Chapin FS. 1996. Response of Eriophorum vaginatum to CO2 enrichment at different soil temperatures: effects on growth, root respiration and PO43 uptake kinetics. New Phytologist 133: 423–430. Bell KL, Bliss LC. 1978. Root growth in a polar semidesert environment. Canadian Journal of Botany 56: 2470–2490. Bilbrough CJ, Welker JM, Bowman WD. 2000. Early spring nitrogen uptake by snow-covered plants: a comparison of arctic and alpine plant function under the snowpack. Arctic, Antarctic and Alpine Research 32: 404–411. Billings WD, Mooney HA. 1968. Ecology of arctic and alpine plants. Biological Reviews of the Cambridge Philosophical Society 43: 481–529. Billings WD, Peterson KM, Shaver GR. 1978. Growth, turnover, and respiration rates of roots and tillers in tundra graminoids. In: Tieszen LL, ed. Vegetation and production ecology of an Alaskan arctic tundra. New York, NY, USA: Springer-Verlag, 415–434. Billings WD, Peterson KM, Shaver GR, Trent AW. 1977. Root growth, respiration, and carbon-dioxide evolution in an arctic tundra soil. Arctic and Alpine Research 9: 129–137. Billings WD, Shaver GR, Trent AW. 1973. Temperature effects on growth and respiration of roots and rhizomes in tundra graminoids. In: Bliss LC, Wielgolaski FE, eds. Primary production and production processes. Stockholm, Sweden: IBP Tundra Biome Steering Committee, 57–63. Billings WD, Shaver G, Trent AW. 1976. Measurement of root growth in simulated and natural temperature gradients over permafrost. Arctic and Alpine Research 8: 247–250. Bj€ork RG, Majdi H, Klemedtsson L, Lewis-Jonsson L, Molau U. 2007. Long-term warming effects on root morphology, root mass distribution, and microbial activity in two dry tundra plant communities in northern Sweden. New Phytologist 176: 862–873. Bliss LC, Svoboda J. 1984. Plant-communities and plant-production in the Western Queen Elizabeth Islands. Holarctic Ecology 7: 325–344. Bliss LC, Svoboda J, Bliss DI. 1984. Polar deserts, their plant cover and plant-production in the Canadian High Arctic. Holarctic Ecology 7: 305–324. Borden PW, Ping CL, McCarthy PJ, Naidu S. 2010. Clay mineralogy in Arctic Tundra Gelisols, northern Alaska. Soil Science Society of America Journal 74: 580–592. Brown J, Ferrians OJ Jr, Heginbottom JA, Melnikov ES, eds. 1997. Circum-Arctic map of permafrost and ground-ice conditions. Washington, DC, USA: US New Phytologist (2015) 205: 34–58 www.newphytologist.com

54 Review

Tansley review

Geological Survey in Cooperation with the Circum-Pacific Council for Energy and Mineral Resources. Circum-Pacific Map Series CP-45, scale 1 : 10,000,000. Cahoon SMP, Sullivan PF, Shaver GR, Welker JM, Post E. 2012. Interactions among shrub cover and the soil microclimate may determine future Arctic carbon budgets. Ecology Letters 15: 1415–1422. Caldwell MM. 1987. Competition between root systems in natural communities. In: Gregory P, Lake J, Rose D, eds. Root development and function. Cambridge, UK: Cambridge University Press, 167–186. Campioli M, Michelsen A, Demey A, Vermeulen A, Samson R, Lemeur R. 2009. Net primary production and carbon stocks for subarctic mesic-dry tundras with contrasting microtopography, altitude, and dominant species. Ecosystems 12: 760–776. Chanton JP, Martens CS, Kelley CA, Crill PM, Showers WJ. 1992. Methane transport mechanisms and isotopic fractionation in emergent macrophytes of an Alaskan tundra lake. Journal of Geophysical Research 97: 16681–16688. Chapin FS. 1974. Morphological and physiological mechanisms of temperature compensation in phosphate absorption along a latitudinal gradient. Ecology 55: 1180–1198. Chapin FS. 1978. Phosphate uptake and nutrient utilization by Barrow tundra vegetation. In: Tieszen LL, ed. Vegetation and production ecology of an Alaskan arctic tundra. New York, NY, USA: Springer-Verlag New York Inc, 483–507. Chapin FS. 1981. Field measurements of growth and phosphate absorption in Carex aquatilis along a latitudinal gradient. Arctic and Alpine Research 13: 83–94. Chapin FS. 1983. Direct and indirect effects of temperature on arctic plants. Polar Biology 2: 47–52. Chapin FS, Barsdate RJ, Barel D. 1978. Phosphorus cycling in Alaskan coastal tundra: hypothesis for the regulation of nutrient cycling. Oikos 31: 189–199. Chapin FS, Bloom A. 1976. Phosphate absorption: adaptation of tundra graminoids to a low temperature, low phosphorus environment. Oikos 27: 111–121. Chapin FS, BretHarte MS, Hobbie SE, Zhong HL. 1996. Plant functional types as predictors of transient responses of arctic vegetation to global change. Journal of Vegetation Science 7: 347–358. Chapin FS, Fetcher N, Kielland K, Everett KR, Linkins AE. 1988. Productivity and nutrient cycling of Alaskan tundra: enhancement by flowing soil-water. Ecology 69: 693–702. Chapin FS, Johnson DA, McKendrick JD. 1980b. Seasonal movement of nutrients in plants of differing growth form in an Alaskan tundra ecosystem: implications for herbivory. Journal of Ecology 68: 189–209. Chapin FS, Moilanen L, Kielland K. 1993. Preferential use of organic nitrogen for growth by a nonmycorrhizal arctic sedge. Nature 361: 150–153. Chapin FS, Shaver GR. 1996. Physiological and growth responses of arctic plants to a field experiment simulating climatic change. Ecology 77: 822–840. Chapin FS, Slack M. 1979. Effect of defoliation upon root growth, phosphate absorption and respiration in nutrient-limited tundra graminoids. Oecologia 42: 67–79. Chapin FS, Tieszen LL, Lewis MC, Miller PC, McCown BH. 1980a. Control of tundra plant allocation patterns and growth. In: Brown J, Miller PC, Tieszen LL, Bunnell FL, eds. An arctic ecosystem: the coastal tundra at Barrow, Alaska. Stroudsburg, PA, USA: Dowden, Hutchinson & Ross, Inc., 140–185. Chapin FS, Tryon PR. 1982. Phosphate absorption and root respiration of different plant growth forms from northern Alaska. Holarctic Ecology 5: 164–171. Chapin FS, van Cleve K, Tieszen LL. 1975. Seasonal nutrient dynamics of tundra vegetation at Barrow, Alaska. Arctic and Alpine Research 7: 209–226. Cheng WX, Parton WJ, Gonzalez-Meler MA, Phillips R, Asao S, McNickle GG, Brzostek E, Jastrow JD. 2014. Synthesis and modeling perspectives of rhizosphere priming. New Phytologist 201: 31–44. Clemmensen KE, Michelsen A, Jonasson S, Shaver GR. 2006. Increased ectomycorrhizal fungal abundance after long-term fertilization and warming of two arctic tundra ecosystems. New Phytologist 171: 391–404. Clemmensen KE, Sorensen PL, Michelsen A, Jonasson S, Strom L. 2008. Site-dependent N uptake from N-form mixtures by arctic plants, soil microbes and ectomycorrhizal fungi. Oecologia 155: 771–783. Cornwell WK, Cornelissen JHC, Amatangelo K, Dorrepaal E, Eviner VT, Godoy O, Hobbie SE, Hoorens B, Kurokawa H, Perez-Harguindeguy N et al. 2008. New Phytologist (2015) 205: 34–58 www.newphytologist.com

New Phytologist Plant species traits are the predominant control on litter decomposition rates within biomes worldwide. Ecology Letters 11: 1065–1071. Crow SE, Wieder RK. 2005. Sources of CO2 emission from a northern peatland: root respiration, exudation, and decomposition. Ecology 86: 1825–1834. Dennis JG. 1977. Distribution patterns of belowground standing crop in arctic tundra at Barrow, Alaska. Arctic and Alpine Research 9: 113–127. Dennis JG, Johnson PL. 1970. Shoot and rhizome-root standing crops of tundra vegetation at Barrow, Alaska. Arctic and Alpine Research 2: 253–266. Dennis JG, Tieszen LL, Vetter MA. 1978. Seasonal dynamics of above- and belowground production of vascular plants at Barrow, Alaska. In: Tieszen LL, ed. Vegetation and production ecology of an Alaskan arctic tundra. New York, NY, USA: Springer-Verlag New York Inc, 113–140. Deslippe JR, Simard SW. 2011. Below-ground carbon transfer among Betula nana may increase with warming in Arctic tundra. New Phytologist 192: 689–698. Edwards KA, Jefferies RL. 2010. Nitrogen uptake by Carex aquatilis during the winter–spring transition in a low Arctic wet meadow. Journal of Ecology 98: 737–744. Eissenstat DM, Yanai RD. 1997. The ecology of root lifespan. In: Begon M, Fitter AH, eds. Advances in ecological research, Vol. 27. New York, NY, USA: Academic Press, 1–60. Ellis BA, Kummerow J. 1982. Temperature effect on growth rates of Eriophorum vaginatum roots. Oecologia 54: 136–137. Epstein HE, Walker MD, Chapin FS, Starfield AM. 2000. A transient nutrient-based model of Arctic plant community response to climatic warming. Ecological Applications 10: 824–841. Eskelinen A, Stark S, Mannisto M. 2009. Links between plant community composition, soil organic matter quality and microbial communities in contrasting tundra habitats. Oecologia 161: 113–123. Euskirchen ES, McGuire AD, Chapin FS, Yi S, Thompson CC. 2009. Changes in vegetation in northern Alaska under scenarios of climate change, 2003–2100: implications for climate feedbacks. Ecological Applications 19: 1022–1043. Fan Z, McGuire AD, Turetsky MR, Harden JW, Waddington JM, Kane ES. 2013. The response of soil organic carbon of a rich fen peatland in interior Alaska to projected climate change. Global Change Biology 19: 604–620. Freschet GT, Aerts R, Cornelissen JHC. 2012a. A plant economics spectrum of litter decomposability. Functional Ecology 26: 56–65. Freschet GT, Aerts R, Cornelissen JHC. 2012b. Multiple mechanisms for trait effects on litter decomposition: moving beyond home-field advantage with a new hypothesis. Journal of Ecology 100: 619–630. Freschet GT, Cornelissen JHC, van Logtestijn RSP, Aerts R. 2010a. Evidence of the ‘plant economics spectrum’ in a subarctic flora. Journal of Ecology 98: 362–373. Freschet GT, Cornelissen JHC, van Logtestijn RSP, Aerts R. 2010b. Substantial nutrient resorption from leaves, stems and roots in a subarctic flora: what is the link with other resource economics traits? New Phytologist 186: 879–889. Freschet GT, Cornwell WK, Wardle DA, Elumeeva TG, Liu WD, Jackson BG, Onipchenko VG, Soudzilovskaia NA, Tao JP, Cornelissen JHC. 2013. Linking litter decomposition of above- and below-ground organs to plant–soil feedbacks worldwide. Journal of Ecology 101: 943–952. Gebauer RLE, Tenhunen JD, Reynolds JF. 1996. Soil aeration in relation to soil physical properties, nitrogen availability, and root characteristics within an arctic watershed. Plant and Soil 178: 37–48. Gill RA, Jackson RB. 2000. Global patterns of root turnover for terrestrial ecosystems. New Phytologist 147: 13–31. Grogan P, Jonasson S. 2003. Controls on annual nitrogen cycling in the understory of a subarctic birch forest. Ecology 84: 202–218. Guo DL, Xia MX, Wei X, Chang WJ, Liu Y, Wang ZQ. 2008. Anatomical traits associated with absorption and mycorrhizal colonization are linked to root branch order in twenty-three Chinese temperate tree species. New Phytologist 180: 673– 683. Harden JW, Koven CD, Ping CL, Hugelius G, McGuire AD, Camill P, Jorgenson T, Kuhry P, Michaelson GJ, O’Donnell JA et al. 2012. Field information links permafrost carbon to physical vulnerabilities of thawing. Geophysical Research Letters 39: 6. Harmon ME, Silver WL, Fasth B, Chen H, Burke IC, Parton WJ, Hart SC, Currie WS. 2009. Long-term patterns of mass loss during the decomposition of leaf and fine root litter: an intersite comparison. Global Change Biology 15: 1320–1338. No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

New Phytologist Harms TK, Jones JB. 2012. Thaw depth determines reaction and transport of inorganic nitrogen in valley bottom permafrost soils. Global Change Biology 18: 2958–2968. Hartley IP, Garnett MH, Sommerkorn M, Hopkins DW, Fletcher BJ, Sloan VL, Phoenix GK, Wookey PA. 2012. A potential loss of carbon associated with greater plant growth in the European Arctic. Nature Climate Change 2: 875–879. Henry GHR, Svoboda J, Freedman B. 1990. Standing crop and net production of sedge meadows of an ungrazed polar desert oasis. Canadian Journal of Botany 68: 2660–2667. Henry HAL, Jefferies RL. 2003. Plant amino acid uptake, soluble N turnover and microbial N capture in soils of a grazed Arctic salt marsh. Journal of Ecology 91: 627–636. Hernandez RR, Allen MF. 2013. Diurnal patterns of productivity of arbuscular mycorrhizal fungi revealed with the Soil Ecosystem Observatory. New Phytologist 200: 547–557. Hicks Pries CE, Schuur EAG, Crummer KG. 2013. Thawing permafrost increases old soil and autotrophic respiration in tundra: partitioning ecosystem respiration using d13C and d14C. Global Change Biology 19: 649–661. Hill GB, Henry GHR. 2011. Responses of High Arctic wet sedge tundra to climate warming since 1980. Global Change Biology 17: 276–287. Hinzman LD, Kane DL, Gieck RE, Everett KR. 1991. Hydrologic and thermal properties of the active layer in the Alaskan arctic. Cold Regions Science and Technology 19: 95–110. Hobbie SE. 1996. Temperature and plant species control over litter decomposition in Alaskan tundra. Ecological Monographs 66: 503–522. Hobbie SE, Chapin FS. 1996. Winter regulation of tundra litter carbon and nitrogen dynamics. Biogeochemistry 35: 327–338. Hobbie SE, Chapin FSI. 1998. The response of tundra plant biomass, aboveground production, nitrogen, and CO2 flux to experimental warming. Ecology 79: 1526– 1544. Hobbie JE, Hobbie EA. 2006. 15N in symbiotic fungi and plants estimates nitrogen and carbon flux rates in Arctic tundra. Ecology 87: 816–822. Hobbie SE, Schimel JP, Trumbore SE, Randerson JR. 2000. Controls over carbon storage and turnover in high-latitude soils. Global Change Biology 6: 196–210. Hugelius G, Bockheim JG, Camill P, Elberling B, Grosse G, Harden JW, Johnson K, Jorgenson T, Koven CD, Kuhry P et al. 2013. A new data set for estimating organic carbon storage to 3 m depth in soils of the northern circumpolar permafrost region. Earth System Science Data 5: 393–402. Iversen CM. 2010. Digging deeper: fine-root responses to rising atmospheric CO2 concentration in forested ecosystems. New Phytologist 186: 346–357. Iversen CM, Murphy MT, Allen MF, Childs J, Eissenstat DM, Lilleskov EA, Sarjala TM, Sloan VL, Sullivan PF. 2012. Advancing the use of minirhizotrons in wetlands. Plant and Soil 352: 23–39. Iversen CM, Sloan VL, Sullivan PF, Euskirchen ES, McGuire AD, Norby RJ, Walker AP, Warren JM, Wullschleger SD. 2014. Plant roots in arctic tundra. Next generation ecosystem experiments arctic data Collection. Oak Ridge, Tennessee, USA: Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory. Dataset doi: 10.5440/1114222. Jackson RB, Canadell J, Ehleringer JR, Mooney HA, Sala OE, Schulze ED. 1996. A global analysis of root distributions for terrestrial biomes. Oecologia 108: 389– 411. Jackson RB, Schenk HJ, Jobba gy EG, Canadell J, Colello GD, Dickinson RE, Field CB, Friedlingstein P, Heimann M, Hibbard K et al. 2000. Belowground consequences of vegetation change and their treatment in models. Ecological Applications 10: 470–483. Joabsson A, Christensen TR. 2001. Methane emissions from wetlands and their relationship with vascular plants: an Arctic example. Global Change Biology 7: 919–932. Jobba gy EG, Jackson RB. 2000. The vertical distribution of soil organic carbon and its relation to climate and vegetation. Ecological Applications 10: 423–436. Jobba gy EG, Jackson RB. 2001. The distribution of soil nutrients with depth: global patterns and the imprint of plants. Biogeochemistry 53: 51–77. Jonasson S, Callaghan TV. 1992. Root mechanical properties related to disturbed and stressed habitats in the Arctic. New Phytologist 122: 179–186. Jones DL. 1998. Organic acids in the rhizosphere – a critical review. Plant and Soil 205: 25–44. No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

Tansley review

Review 55

Keuper FK. 2012. Direct and indirect effects of climatic changes on vegetation productivity and species composition of permafrost peatlands. PhD Thesis, VU University, Amsterdam, the Netherlands. Keuper FK, van Bodegom PM, Dorrepaal E, Weedon JT, van Hal J, van Logtestijn RSP, Aerts R. 2012. A frozen feast: thawing permafrost increases plant-available nitrogen in subarctic peatlands. Global Change Biology 18: 1998–2007. Kielland K. 1994. Amino-acid absorption by arctic plants: implications for plant nutrition and nitrogen cycling. Ecology 75: 2373–2383. Kielland K, Chapin FS. 1994. Phosphate uptake in arctic plants in relation to phosphate supply: the role of spatial and temporal variability. Oikos 70: 443–448. Kjelvik S, K€a renlampi L. 1975. Plant biomass and primary production of Fennoscandian subarctic and subalpine forests and of alpine willow and heath ecosystems. In: Wielgolaski FE, ed. Fennoscandian tundra ecosystems. New York, NY, USA: Springer-Verlag, 111–120. Koch GW, Bloom AJ, Chapin FS. 1991. Ammonium and nitrate as nitrogen sources in two Eriophorum species. Oecologia 88: 570–573. Koelbener A, Strom L, Edwards PJ, Venterink HO. 2010. Plant species from mesotrophic wetlands cause relatively high methane emissions from peat soil. Plant and Soil 326: 147–158. Koven CD, Riley WJ, Subin ZM, Tang JY, Torn MS, Collins WD, Bonan GB, Lawrence DM, Swenson SC. 2013. The effect of vertically-resolved soil biogeochemistry and alternate soil C and N models on C dynamics of CLM4. Biogeosciences Discussions 10: 7201–7256. Koven CD, Ringeval B, Friedlingstein P, Ciais P, Cadule P, Khvorostyanov D, Krinner G, Tarnocai C. 2011. Permafrost carbon–climate feedbacks accelerate global warming. Proceedings of the National Academy of Sciences, USA 108: 14769– 14774. Krinner G, Viovy N, de Noblet-Ducoudre N, Ogee J, Polcher J, Friedlingstein P, Ciais P, Sitch S, Prentice IC. 2005. A dynamic global vegetation model for studies of the coupled atmosphere–biosphere system. Global Biogeochemical Cycles 19: 1015. Kummerow J, Ellis BA, Kummerow S, Chapin FS. 1983. Spring growth of shoots and roots in shrubs of an Alaskan muskeg. American Journal of Botany 70: 1509–1515. Kummerow J, Krause D. 1982. The effects of variable nitrogen and phosphorus concentrations on Eriophorum vaginatum tillers grown in nutrient solutions. Holarctic Ecology 5: 187–193. Kummerow J, McMaster GS, Krause DA. 1980. Temperature effect on growth and nutrient contents in Eriophorum vaginatum under controlled environmental conditions. Arctic and Alpine Research 12: 335–342. Kummerow J, Russell M. 1980. Seasonal root growth in the arctic tussock tundra. Oecologia 47: 196–199. Kutzbach L, Wagner D, Pfeiffer EM. 2004. Effect of microrelief and vegetation on methane emission from wet polygonal tundra, Lena Delta, northern Siberia. Biogeochemistry 69: 341–362. Laanbroek HJ. 2010. Methane emission from natural wetlands: interplay between emergent macrophytes and soil microbial processes. A mini-review. Annals of Botany 105: 141–153. Le Dizes S, Kwiatkowski BL, Rastetter EB, Hope A, Hobbie JE, Stow D, Daeschner S. 2003. Modeling biogeochemical responses of tundra ecosystems to temporal and spatial variations in climate in the Kuparuk River Basin (Alaska). Journal of Geophysical Research-Atmospheres 108: D2. Limbach WE, Oechel WC, Lowell W. 1982. Photosynthetic and respiratory responses to temperature and light of three Alaskan tundra growth forms. Holarctic Ecology 5: 150–157. Loya WM, Johnson LC, Kling GW, King JY, Reeburgh WS, Nadelhoffer KJ. 2002. Pulse-labeling studies of carbon cycling in arctic tundra ecosystems: contribution of photosynthates to soil organic matter. Global Biogeochemical Cycles 16: 1101. Mack MC, Schuur EAG, Bret-Harte MS, Shaver GR, Chapin FS. 2004. Ecosystem carbon storage in arctic tundra reduced by long-term nutrient fertilization. Nature 431: 440–443. Maessen O, Freedman B, Nams MLN, Svoboda J. 1983. Resource allocation in High Arctic vascular plants of differing growth form. Canadian Journal of Botany 61: 1680–1691. Marion GM, Miller PC, Black CH. 1987. Competition for tracer 15N in tussock tundra ecosystems. Holarctic Ecology 10: 230–234. New Phytologist (2015) 205: 34–58 www.newphytologist.com

56 Review

Tansley review

McConnell NA, Turetsky MR, McGuire AD, Kane ES, Waldrop MP, Harden JW. 2013. Controls on ecosystem and root respiration across a permafrost and wetland gradient in interior Alaska. Environmental Research Letters 8: 045029. McCormack ML, Thomas SA, Smithwick EAH, Eissenstat DM. 2012. Predicting fine root lifespan from plant functional traits in temperate trees. New Phytologist 195: 823–831. McGraw JB, Chapin FS. 1989. Competititive ability and adaptation to fertile and infertile soils in two Eriophorum species. Ecology 70: 736–749. McGuire AD, Anderson LG, Christensen TR, Dallimore S, Guo LD, Hayes DJ, Heimann M, Lorenson TD, Macdonald RW, Roulet N. 2009. Sensitivity of the carbon cycle in the Arctic to climate change. Ecological Monographs 79: 523–555. McGuire AD, Christensen TR, Hayes D, Heroult A, Euskirchen E, Kimball JS, Koven C, Lafleur P, Miller PA, Oechel W et al. 2012. An assessment of the carbon balance of Arctic tundra: comparisons among observations, process models, and atmospheric inversions. Biogeosciences 9: 3185–3204. McGuire AD, Hayes DJ, Kicklighter DW, Manizza M, Zhuang Q, Chen M, Follows MJ, Gurney KR, McClelland JW, Melillo JM et al. 2010. An analysis of the carbon balance of the Arctic Basin from 1997 to 2006. Tellus Series B-Chemical and Physical Meteorology 62: 455–474. McKane RB, Johnson LC, Shaver GR, Nadelhoffer KJ, Rastetter EB, Fry B, Giblin AE, Kielland K, Kwiatkowski BL, Laundre JA et al. 2002. Resource-based niche provides a basis for plant species diversity and dominance in arctic tundra. Nature 415: 68–71. Michelsen A, Quarmby C, Sleep D, Jonasson S. 1998. Vascular plant 15N natural abundance in heath and forest tundra ecosystems is closely correlated with presence and type of mycorrhizal fungi in roots. Oecologia 115: 406–418. Michelsen A, Schmidt IK, Jonasson S, Quarmby C, Sleep D. 1996. Leaf 15N abundance of subarctic plants provides field evidence that ericoid, ectomycorrhizal and non- and arbuscular mycorrhizal species access different sources of soil nitrogen. Oecologia 105: 53–63. Miller OK. 1982. Mycorrhizae, mycorrhizal fungi and fungal biomass in subalpine tundra at Eagle Summit, Alaska. Holarctic Ecology 5: 125–134. Miller PA, Smith B. 2012. Modelling tundra vegetation response to recent arctic warming. Ambio 41: 281–291. Miller PC, Mangan R, Kummerow J. 1982. Vertical distribution of organic matter in eight vegetation types near Eagle Summit, Alaska. Holarctic Ecology 5: 117–124. Miller PC, Miller PM, Blakejacobson M, Chapin FS, Everett KR, Hilbert DW, Kummerow J, Linkins AE, Marion GM, Oechel WC et al. 1984. Plant–soil processes in Eriophorum vaginatum tussock tundra in Alaska: a systems modeling approach. Ecological Monographs 54: 361–405. Miller PC, Stoner WA, Ehleringer JR. 1978. Some aspects of water relations of arctic and alpine regions. In: Tieszen LL, ed. Vegetation and production ecology of an Alaskan arctic tundra. New York, NY, USA: Springer-Verlag, 343–369. Mokany K, Raison RJ, Prokushkin AS. 2006. Critical analysis of root : shoot ratios in terrestrial biomes. Global Change Biology 12: 84–96. Muc M. 1977. Ecology and primary production of sedge-moss meadow communities, Truelove Lowland. In: Bliss LC, ed. Truelove Lowland, Devon Island, Canada: a high arctic ecosystem. Edmonton, AB, Canada: University of Alberta Press, 157–184. Myhre G, Shindell D, Breon F-M, Collins W, Fuglestvedt J, Huang J, Koch D, Lamarque J-F, Lee D, Mendoza B et al. 2013. Anthropogenic and natural radiative forcing. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM, eds. Climate change. The physical science basis. Contribution of Working Group I to the fifth assessment report of the Intergovernmental Panel on Climate Change. New York, NY, USA: Cambridge University Press, 659–740. Nadelhoffer K, Shaver G, Fry B, Giblin A, Johnson L, McKane R. 1996. 15N natural abundances and N use by tundra plants. Oecologia 107: 386–394. Nadelhoffer KJ, Giblin AE, Shaver GR, Laundre JA. 1991. Effects of temperature and substrate quality on element mineralization in six arctic soils. Ecology 72: 242–253. Nadelhoffer KJ, Johnson L, Laundre J, Giblin AE, Shaver GR. 2002. Fine root production and nutrient content in wet and moist arctic tundras as influenced by chronic fertilization. Plant and Soil 242: 107–113. N€asholm T, Kielland K, Ganeteg U. 2009. Uptake of organic nitrogen by plants. New Phytologist 182: 31–48. New Phytologist (2015) 205: 34–58 www.newphytologist.com

New Phytologist Newsham KK, Upson R, Read DJ. 2009. Mycorrhizas and dark septate root endophytes in polar regions. Fungal Ecology 2: 10–20. Nowinski NS, Trumbore SE, Schuur EAG, Mack MC, Shaver GR. 2008. Nutrient addition prompts rapid destabilization of organic matter in an arctic tundra ecosystem. Ecosystems 11: 16–25. Oleson KW, Lawrence DM, Bonan GB, Drewniak B, Huang M, Koven CD, Levis S, Li F, Riley WJ, Subin ZM et al. 2013. Technical description of version 4.5 of the Community Land Model (CLM). NCAR/TN-503+STR NCAR Technical Note. Olsrud M, Christensen TR. 2004. Carbon cycling in subarctic tundra; seasonal variation in ecosystem partitioning based on in situ 14C pulse-labelling. Soil Biology & Biochemistry 36: 245–253. € Oquist MG, Svensson BH. 2002. Vascular plants as regulators of methane emissions from a subarctic mire ecosystem. Journal of Geophysical Research-Atmospheres 107: 4580. Orwin KH, Kirschbaum MUF, St John MG, Dickie IA. 2011. Organic nutrient uptake by mycorrhizal fungi enhances ecosystem carbon storage: a model-based assessment. Ecology Letters 14: 493–502. Parton W, Silver WL, Burke IC, Grassens L, Harmon ME, Currie WS, King JY, Adair EC, Brandt LA, Hart SC et al. 2007. Global-scale similarities in nitrogen release patterns during long-term decomposition. Science 315: 361–364. Ping CL, Bockheim JG, Kimble JM, Michaelson GJ, Walker DA. 1998. Characteristics of cryogenic soils along a latitudinal transect in Arctic Alaska. Journal of Geophysical Research-Atmospheres 103: 28917–28928. Ping CL, Michaelson GJ, Packee EC, Stiles CA, Swanson DK, Yoshikawa K. 2005. Soil catena sequences and fire ecology in the boreal forest of Alaska. Soil Science Society of America Journal 69: 1761–1772. Pregitzer KS. 2002. Fine roots of trees – a new perspective. New Phytologist 154: 267–270. Rastetter EB, Ryan MG, Shaver GR, Melillo JM, Nadelhoffer KJ, Hobbie JE, Aber JD. 1991. A general biogeochemical model describing the responses of the C-cycle and N-cycle in terrestrial ecosystems to changes in CO2, climate, and N-deposition. Tree Physiology 9: 101–126. Read DJ, Leake JR, Perez-Moreno J. 2004. Mycorrhizal fungi as drivers of ecosystem processes in heathland and boreal forest biomes. Canadian Journal of Botany 82: 1243–1263. Riley WJ, Subin ZM, Lawrence DM, Swenson SC, Torn MS, Meng L, Mahowald NM, Hess P. 2011. Barriers to predicting changes in global terrestrial methane fluxes: analyses using CLM4Me, a methane biogeochemistry model integrated in CESM. Biogeosciences 8: 1925–1953. Ringeval B, Friedlingstein P, Koven C, Ciais P, de Noblet-Ducoudre N, Decharme B, Cadule P. 2011. Climate–CH4 feedback from wetlands and its interaction with the climate–CO2 feedback. Biogeosciences 8: 2137–2157. Rosswall T, Veum AK, K€a renlampi L. 1975. Plant litter decomposition at Fennoscandian tundra sites. In: Wielgolaski FE, ed. Fennoscandian tundra ecosystems. New York, NY, USA: Springer-Verlag, 268–278. Schaefer K, Collatz GJ, Tans P, Denning AS, Baker I, Berry J, Prihodko L, Suits N, Philpott A. 2008. Combined Simple Biosphere/Carnegie-Ames-Stanford Approach terrestrial carbon cycle model. Journal of Geophysical Research-Biogeosciences 113: G3. Schimel JP. 1995. Plant transport and methane production as controls on methane flux from arctic wet meadow tundra. Biogeochemistry 28: 183–200. Schimel JP, Chapin FS. 1996. Tundra plant uptake of amino acid and NH4+ nitrogen in situ: plants compete well for amino acid N. Ecology 77: 2142–2147. Schuur EAG, Bockheim J, Canadell JG, Euskirchen E, Field CB, Goryachkin SV, Hagemann S, Kuhry P, Lafleur PM, Lee H et al. 2008. Vulnerability of permafrost carbon to climate change: implications for the global carbon cycle. BioScience 58: 701–714. Segal AD, Sullivan PF. 2014. Identifying the sources and uncertainties of ecosystem respiration in Arctic tussock tundra. Biogeochemistry. doi: 10.1007/s10533-0140017-8. Shaver GR, Billings WD. 1975. Root production and root turnover in a wet tundra ecosystem, Barrow, Alaska. Ecology 56: 401–409. Shaver GR, Billings WD. 1977. Effects of daylength and temperature on root elongation in tundra graminoids. Oecologia 28: 57–65. Shaver GR, Chapin FS III. 1991. Production : biomass relationships and element cycling in contrasting arctic vegetation types. Ecological Monographs 61: 1–31. No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

New Phytologist Shaver GR, Chapin FS III. 1995. Long-term responses to factorial, NPK fertilizer treatment by Alaskan wet and moist tundra sedge species. Ecography 18: 259–275. Shaver GR, Chapin FS, Billings WD. 1979. Ecotypic differentiation in Carex aquatilis on ice-wedge polygons in the Alaskan coastal tundra. Journal of Ecology 67: 1025–1046. Shaver GR, Chapin FS III, Gartner BL. 1986. Factors limiting seasonal growth and peak biomass accumulation in Eriophorum vaginatum in Alaskan tussock tundra. Journal of Ecology 74: 257–278. Shaver GR, Cutler JC. 1979. Vertical distribution of live vascular phytomass in cottongrass tussock tundra. Arctic and Alpine Research 11: 335–342. Sloan VL. 2011. Plant roots in arctic ecosystems: stocks and dynamics, and their coupling to above-ground parameters. PhD Thesis, University of Sheffield, Sheffield, UK. Sloan VL, Fletcher BJ, Press MC, Williams M, Phoenix GK. 2013. Leaf and fine root carbon stocks and turnover are coupled across Arctic ecosystems. Global Change Biology 19: 3668–3676. Smith B, Prentice IC, Sykes MT. 2001. Representation of vegetation dynamics in the modelling of terrestrial ecosystems: comparing two contrasting approaches within European climate space. Global Ecology and Biogeography 10: 621–637. Sorensen PL, Clemmensen KE, Michelsen A, Jonasson S, Strom L. 2008. Plant and microbial uptake and allocation of organic and inorganic nitrogen related to plant growth forms and soil conditions at two subarctic tundra sites in Sweden. Arctic, Antarctic, and Alpine Research 40: 171–180. Stewart J, Freedman B. 1994. Biomass allocation in ten Saxifraga species in the high arctic. In: Svoboda J, Freedman B, eds. Ecology of a polar oasis: Alexandra Fiord, Ellesmere Island, Canada. New York, ON, Canada: Captus Press Inc., 123–136. Str€om L, Ekberg A, Mastepanov M, Christensen TR. 2003. The effect of vascular plants on carbon turnover and methane emissions from a tundra wetland. Global Change Biology 9: 1185–1192. Str€om L, Mastepanov M, Christensen TR. 2005. Species-specific effects of vascular plants on carbon turnover and methane emissions from wetlands. Biogeochemistry 75: 65–82. Str€om L, Tagesson T, Mastepanov M, Christensen TR. 2012. Presence of Eriophorum scheuchzeri enhances substrate availability and methane emission in an Arctic wetland. Soil Biology & Biochemistry 45: 61–70. Sturm M. 2010. Arctic plants feel the heat. Scientific American 302: 66–73. Sullivan PF, Arens SJT, Chimner RA, Welker JM. 2008. Temperature and microtopography interact to control carbon cycling in a high arctic fen. Ecosystems 11: 61–76. Sullivan PF, Sommerkorn M, Rueth HM, Nadelhoffer KJ, Shaver GR, Welker JM. 2007. Climate and species affect fine root production with long-term fertilization in acidic tussock tundra near Toolik Lake, Alaska. Oecologia 153: 643–652. Sullivan PF, Welker JM. 2005. Warming chambers stimulate early season growth of an arctic sedge: results of a minirhizotron field study. Oecologia 142: 616–626. Tarnocai C, Canadell JG, Schuur EAG, Kuhry P, Mazhitova G, Zimov S. 2009. Soil organic carbon pools in the northern circumpolar permafrost region. Global Biogeochemical Cycles 23: 11. Tieszen LL, Lewis MC, Miller PC, Mayo J, Chapin FS III, Oechel WC. 1981. An analysis of processes of primary production in tundra growth forms. In: Bliss LC, Heal OW, Moore JJ, eds. Tundra ecosystems: a comparative analysis. New York, NY, USA: Cambridge University Press, 647–684. Tikhomirov BA, Shamurin VF, Aleksandrova VD. 1981. Phytomass and primary production of tundra communities, USSR. In: Bliss LC, Heal OW, Moore JJ, eds. Tundra ecosystems: a comparative analysis. New York, NY, USA: Cambridge University Press, 227–238. Torn MS, Chapin FS. 1993. Environmental and biotic controls over methane flux from arctic tundra. Chemosphere 26: 357–368. Tye AM, Young SD, Crout NMJ, West HM, Stapleton LM, Poulton PR, Laybourn-Parry J. 2005. The fate of 15N added to high Arctic tundra to mimic increased inputs of atmospheric nitrogen released from a melting snowpack. Global Change Biology 11: 1640–1654. Valenzuela-Estrada LR, Vera-Caraballo V, Ruth LE, Eissenstat DM. 2008. Root anatomy, morphology, and longevity among root orders in Vaccinium corymbosum (Ericaceae). American Journal of Botany 95: 1506–1514. Vartapetian BB, Jackson MB. 1997. Plant adaptations to anaerobic stress. Annals of Botany 79: 3–20. van der Wal R, van Lieshout SMJ, Loonen M. 2001. Herbivore impact on moss depth, soil temperature and arctic plant growth. Polar Biology 24: 29–32. No claim to original US Government works New Phytologist Ó 2014 New Phytologist Trust

Tansley review

Review 57

Walker DA, Raynolds MK, Daniels FJA, Einarsson E, Elvebakk A, Gould WA, Katenin AE, Kholod SS, Markon CJ, Melnikov ES et al. 2005. The Circumpolar Arctic vegetation map. Journal of Vegetation Science 16: 267–282. Walker JKM, Egger KN, Henry GHR. 2008. Long-term experimental warming alters nitrogen-cycling communities but site factors remain the primary drivers of community structure in high arctic tundra soils. ISME Journal 2: 982–995. Walker MD, Wahren CH, Hollister RD, Henry GHR, Ahlquist LE, Alatalo JM, Bret-Harte MS, Calef MP, Callaghan TV, Carroll AB et al. 2006. Plant community responses to experimental warming across the tundra biome. Proceedings of the National Academy of Sciences, USA 103: 1342–1346. Wallen B. 1986. Above- and belowground dry mass of the three main vascular plants on hummocks on a sub-arctic peat bog. Oikos 46: 51–56. Wania R, Ross I, Prentice IC. 2009. Integrating peatlands and permafrost into a dynamic global vegetation model: 2. Evaluation and sensitivity of vegetation and carbon cycle processes. Global Biogeochemical Cycles 23: GB3015. Wania R, Ross I, Prentice IC. 2010. Implementation and evaluation of a new methane model within a dynamic global vegetation model: LPJ-WHyMe v1.3.1. Geoscientific Model Development 3: 565–584. Warren JM, Hanson PJ, Iversen CM, Kumar J, Walker AP, Wullschleger SD. 2014. Root structural and functional dynamics in terrestrial biosphere models – Evaluation and recommendations. New Phytologist, in press. doi: 10.1111/nph. 13034. Washburn AL. 1973. Soil deformation resulting from some laboratory freeze–thaw experiments. Proceedings of the 2nd International Permafrost Conference. Washington, DC, USA: National Academy of Sciences, 757–762. Webber PJ. 1977. Belowground tundra research – commentary. Arctic and Alpine Research 9: 105–111. Webber PJ. 1978. Spatial and temporal variation of the vegetation and its productivity. In: Tieszen LL, ed. Vegetation and production ecology of an Alaskan arctic tundra. New York, NY, USA: Springer-Verlag New York Inc, 37–112. Weintraub MN, Schimel JP. 2005. The seasonal dynamics of amino acids and other nutrients in Alaskan arctic tundra soils. Biogeochemistry 73: 359–380. Wielgolaski FE. 1975. Primary productivity of alpine meadow communities. In: Wielgolaski FE, ed. Fennoscandian tundra ecosystems. New York, NY, USA: Springer-Verlag, 121–128. Wielgolaski FE, Bliss LC, Svoboda J, Doyle G. 1981. Primary production of tundra. In: Bliss LC, Heal OW, Moore JJ, eds. Tundra ecosystems: a comparative analysis. New York, NY, USA: Cambridge University Press, 187–225. van Wijk MT, Williams M, Gough L, Hobbie SE, Shaver GR. 2003. Luxury consumption of soil nutrients: a possible competitive strategy in above-ground and below-ground biomass allocation and root morphology for slow-growing arctic vegetation? Journal of Ecology 91: 664–676. Withington JM, Reich PB, Oleksyn J, Eissenstat DM. 2006. Comparisons of structure and life span in roots and leaves among temperate trees. Ecological Monographs 76: 381–397. Wookey PA, Aerts R, Bardgett RD, Baptist F, Brathen KA, Cornelissen JHC, Gough L, Hartley IP, Hopkins DW, Lavorel S et al. 2009. Ecosystem feedbacks and cascade processes: understanding their role in the responses of Arctic and alpine ecosystems to environmental change. Global Change Biology 15: 1153– 1172. Wu FZ, Yang WQ, Zhang J, Deng RJ. 2010. Fine root decomposition in two subalpine forests during the freeze–thaw season. Canadian Journal of Forest Research 40: 298–307. Wullschleger SD, Epstein HE, Box EO, Euskirchen ES, Goswami S, Iversen CM, Kattge J, Norby RJ, van Bodegom PM, Xu X. 2014. Plant functional types in Earth System Models: past experiences and future directions for application of dynamic vegetation models in high-latitude ecosystems. Annals of Botany 114: 1–16. Yi S, Li N, Xiang B, Wang X, Ye B, McGuire AD. 2013. Simulating the effects of alpine grassland vegetation cover on soil thermal dynamics for the Qinghai-Tibetan Plateau. Journal of Geophysical Research – Biogeosciences 118: 1186–1199. Yi SH, McGuire AD, Kasischke E, Harden J, Manies K, Mack M, Turetsky M. 2010. A dynamic organic soil biogeochemical model for simulating the effects of wildfire on soil environmental conditions and carbon dynamics of black spruce forests. Journal of Geophysical Research-Biogeosciences 115: G04015. New Phytologist (2015) 205: 34–58 www.newphytologist.com

58 Review

New Phytologist

Tansley review

Yuan F-M, Yi S-H, McGuire AD, Johnson KD, Liang J-J, Harden WJ, Kasischke E, Kurz WA. 2012. Assessment of historical boreal forest carbon dynamics in the Yukon River Basin: relative roles of climate warming and fire regime changes. Ecological Applications 22: 2091–2109.

Supporting Information Additional supporting information may be found in the online version of this article.

Table S1 A list of the papers containing information on tundra rooting distribution and dynamics used in this review Please note: Wiley Blackwell are not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing material) should be directed to the New Phytologist Central Office.

New Phytologist is an electronic (online-only) journal owned by the New Phytologist Trust, a not-for-profit organization dedicated to the promotion of plant science, facilitating projects from symposia to free access for our Tansley reviews. Regular papers, Letters, Research reviews, Rapid reports and both Modelling/Theory and Methods papers are encouraged. We are committed to rapid processing, from online submission through to publication ‘as ready’ via Early View – our average time to decision is

Importance of Marine-Derived Nutrients Supplied by Planktivorous Seabirds to High Arctic Tundra Plant Communities.

Recent Arctic tundra fire initiates widespread thermokarst development.

Vegetation-associated impacts on arctic tundra bacterial and microeukaryotic communities.

Terrimonas arctica sp. nov., isolated from Arctic tundra soil.

Fire-severity effects on plant-fungal interactions after a novel tundra wildfire disturbance: implications for arctic shrub and tree migration.

Diversification of Nitrogen Sources in Various Tundra Vegetation Types in the High Arctic.

The effect of silver nanoparticles on seasonal change in arctic tundra bacterial and fungal assemblages.

Microbial iron oxidation in the Arctic tundra and its implications for biogeochemical cycling.

Microbial Community and Functional Gene Changes in Arctic Tundra Soils in a Microcosm Warming Experiment.

Rough-legged buzzards, Arctic foxes and red foxes in a tundra ecosystem without rodents.

Long-term experimental warming alters community composition of ascomycetes in Alaskan moist and dry arctic tundra.

Carbon-degrading enzyme activities stimulated by increased nutrient availability in Arctic tundra soils.

Soil bacterial community composition altered by increased nutrient availability in Arctic tundra soils.

Greater shrub dominance alters breeding habitat and food resources for migratory songbirds in Alaskan arctic tundra.

Uncovering unseen fungal diversity from plant DNA banks.

Summer temperature increase has distinct effects on the ectomycorrhizal fungal communities of moist tussock and dry tundra in Arctic Alaska.

New vascular plant records for the Canadian Arctic Archipelago.

Commentary: the iceberg revisited.

Effect of thaw depth on fluxes of CO₂ and CH₄ in manipulated Arctic coastal tundra of Barrow, Alaska.

The unseen invaders: introduced earthworms as drivers of change in plant communities in North American forests (a meta-analysis).

The development of plant roots: new approaches to underground problems.

Signalling in systemic plant defence - roots put in hard graft.

Community and species-specific responses of plant traits to 23 years of experimental warming across subarctic tundra plant communities.

Abiotic stress responses in plant roots: a proteomics perspective.