5 Anatomy and biogenic volatile organic compound

FACULTY OF SCIENCE UNIVERSITY OF COPENHAGEN

PhD thesis Michelle Schollert

Arctic vegetation under climate change – biogenic volatile organic compound emissions and leaf anatomy

Academic advisors: Riikka Rinnan & Minna Kivimäenpää Submitted: April 7 t h 2015 Section of Terrestrial Ecology Department of Biology Center for Permafrost (CENPERM) Department of Geosciences and Natural Resource Management

FACULTY OF SCIENCE UNIVERSITY OF COPENHAGEN

PhD thesis Michelle Schollert

Arctic vegetation under climate change – biogenic volatile organic compound emissions and leaf anatomy

Academic advisors: Riikka Rinnan & Minna Kivimäenpää Submitted: April 7 t h 2015 Section of Terrestrial Ecology Department of Biology Center for Permafrost (CENPERM) Department of Geosciences and Natural Resource Management

Author’s address:

University of Copenhagen Department of Biology Section of Terrestrial Ecology Universitetsparken 15, Building 1 2100 Copenhagen Ø Department of Geosciences and Natural Resource Management Center for Permafrost (CENPERM) Øster Voldgade 10 1350 Copenhagen K DENMARK Email: [email protected]

Supervisors:

Associate Professor Riikka Rinnan, PhD University of Copenhagen Department of Biology Section of Terrestrial Ecology Universitetsparken 15, Building 1 2100 Copenhagen Ø Department of Geosciences and Natural Resource Management Center for Permafrost (CENPERM) Øster Voldgade 10 1350 Copenhagen K DENMARK Email: [email protected] Researcher Minna Kivimäenpää, PhD University of Eastern Finland Department of Environmental Science PO Box 1627 70211 Kuopio FINLAND Email: [email protected]

Chairman:

Professor Inger Kappel Schmidt, PhD University of Copenhagen Department of Geosciences and Natural Resource Management DENMARK Email: [email protected]

External opponents:

Professor Jaana Bäck, PhD University of Helsinki Department of Forest Sciences FINLAND Email: [email protected] Scientist Carlo Calfapietra, PhD National Research Council Institute of Agro-Environmental & Forest Biology ITALY Email: [email protected]

Abstract Biogenic volatile organic compounds (BVOCs) emitted from terrestrial vegetation are highly reactive non-methane hydrocarbons which participate in oxidative reactions in the atmosphere prolonging the lifetime of methane and contribute to the formation of secondary organic aerosols. The BVOC emissions from the arctic region are assumed to be low, but data from the region is lacking. BVOC emissions are furthermore expected to change drastically due to the rapidly proceeding climate change in the Arctic, which can provide a feedback to climate warming of unknown direction and magnitude. BVOC measurements in this thesis were performed using a dynamic enclosure system and collection of BVOCs into adsorbent cartridges analyzed by gas chromatography-mass spectrometry following thermal desorption. Also modifications in leaf anatomy in response to the studied effects of climate change were assessed by the use of light microscopy and scanning electron microscopy. This thesis reports the first estimates of high arctic BVOC emissions, which suggest that arctic environments can be a considerable source of BVOCs to the atmosphere. The BVOC emissions differed qualitatively and quantitatively for the studied common arctic plant species, illustrating the great importance of vegetation composition for determining ecosystem BVOC emissions. Additionally, this thesis assesses the BVOC emission responses in common arctic plant species to effects of climate change: warming, shading and snow addition. Against expectations, only a few effects of long-term warming and shading on BVOC emissions were found. The snow addition effects on BVOC emissions, presented in this thesis, reflect responses after one year of treatment and more effects are expected to become apparent after a longer treatment period. The results demonstrate that leaf anatomy responds rapidly to changes in the environment and that the responses are highly species-specific. The results in this thesis further suggest that anatomical modifications caused by long-term experimental climate change treatment may partly explain the low number of observed treatment effects on BVOC emissions. Furthermore, the anatomy of arctic plants seems to respond differently to warming than species at lower latitudes. The results in this thesis demonstrate the complexity of the effects of climate change on BVOC emissions and leaf anatomy of arctic plant species. The presented results add to the understanding of present and future arctic BVOC emissions, necessary to adjust the estimates of global BVOC emissions, which are for example used in climate models.

Sammendrag Biogene flygtige organiske forbindelser (BVOC) er reaktive carbonhydrider som via komplekse reaktioner i atmosfæren forlænger metans atmosfæriske levetid og bidrager til dannelsen af sekundære organiske aerosoler. Arktiske BVOC emissionerne formodes at være minimale, men der findes utilstrækkeligt med data fra arktiske systemer. Emissionerne forventes samtidig at ændre sig drastisk som følge af de store klimaforandringer i Arktis. Dette kan både have en opvarmende og afkølende effekt på klimaet. I denne afhandling blev BVOC emissionerne målt med en dynamisk kammermetode, hvor BVOC blev opfanget i adsorberende stålrør, frigivet igen ved termisk desorption og analyseret ved hjælp af gaskromatografi og massespektrometri. Også ændringer i bladanatomi, forårsaget af klimabehandlinger, blev undersøgt. Dette blev gjort ved brug af lysmikroskopi og scanning elektronmikroskopi. Denne afhandling præsenterer de første estimater af højarktiske BVOC emissioner, hvilke indikerer, at arktiske systemer kan være en betydelig kilde af BVOC til atmosfæren. Emissionerne varierede kvalitativt og kvantitativt for de undersøgte arktiske plantearter, hvilket illustrerer betydningen af vegetationssammensætningen for BVOC emissionen fra et økosystem. Herudover blev det i denne afhandling undersøgt hvordan BVOC emissioner fra arktiske plantearter påvirkes af klimamæssige forandringer: opvarmning, skygge og øget snedybde. Mod forventning blev kun få påvirkninger af langvarig opvarmning og skygge på BVOC emissionerne påvist. Påvirkningerne af øget snedybde, som blev fundet i denne afhandling, afspejler effekten af ét års eksperimentel behandling. Flere påvirkninger forventes at blive synlige efter en længere behandlingsperiode. Resultaterne viser, at bladanatomi forandrer sig hurtigt når planternes miljø ændres, og at forandringerne i høj grad er artspecifikke. Resultaterne i denne afhandling indikerer yderligere at anatomiske ændringer, forårsaget af langvarige eksperimentelle klimabehandlinger, delvist kan forklare den begrænsede behandlingspåvirkning af BVOC emissionerne. Derudover reagerer arktiske plantearters bladanatomi tilsyneladende anderledes på opvarmning end arter fra lavere breddegrader. Resultaterne i denne afhandling illustrerer kompleksiteten af klimamæssige påvirkninger på arktiske planters BVOC emission og bladanatomi. De præsenterede resultater øger vores forståelse af arktiske BVOC emissioner, hvilket er nødvendigt for at forbedre de globale BVOC emissionsmodeller, som eksempelvis bruges i klimamodellering.

”Trees in the Arctic have an aura of implacable endurance about them…Much of the tundra, of course, appears to be treeless when, in many places, it is actually covered with trees – a thick matting of short, ancient willows and birches. You realize suddenly that you are wandering around on top of a forest.” - Barry Lopez, Arctic Dreams, 1986

Acknowledgements This thesis is a result of a three year PhD project carried out at the Section of Terrestrial Ecology, Department of Biology and Center for Permafrost (CENPERM), Department of Geosciences and Natural Resource Management, University of Copenhagen. The project was funded by the Villum Foundation, the Danish Council for Independent Research | Natural Sciences. This PhD project has been a great and challenging journey, which has involved many people to whom I am truly thankful. I feel lucky and grateful to have had such a competent and ambitious supervisor as Riikka Rinnan, who has always been available and supportive. Your ideas, thorough comments and way of guidance have been absolutely essential for this project. I furthermore feel fortunate to have had Minna Kivimäenpää as my co-supervisor. Thank you for showing your fascination of leaf anatomy and for your always so encouraging words, which have often kept me going and made me feel like a world champion when I needed it. I also thanks to Gosha Sylvester, Esben V. Nielsen, Timo Oksanen, Virpi Miettinen for technical support. I thank Anders Michelsen for his support (often transmitted through ironic jokes) and for being the reason that I was introduced to the Arctic. I am especially happy to have been part of the “BVOC group”, and I would like to thank all of you for great journal clubs, discussions and contributions – it has been great to develop together with you. Hanna Valolahti, I appreciate our trips together and your company has made the long dark days in Kuopio enjoyable. Frida Lindwall, thank you for your inputs, support and friendship. I would like to thank everyone at the Section of Terrestrial Ecology for creating an environment, which has made me enjoy my years at the section. I also want to acknowledge my fellow PhD students at CENPERM for social events, nice company and general conversations about the PhD life. Ever since my first trip to the Arctic I have been absolutely in love with the fantastic intriguing environment. Not only have I been fortunate to have had the opportunity to do field work at different arctic locations, it has also brought me great experiences and not the least many good friends. You are priceless and I am grateful to every one of you! Thank you, Tora F. Nielsen for being a great field assistant in so many ways. Thanks to my family for giving me a solid foundation and support and for teaching me to not give up. Finally, thank you Jeroen – no words can describe the support and love you show me every day. You have been essential for this thesis and journey.

Michelle Schollert, Copenhagen, April 2015

List of papers This thesis is based on the studies presented in the following papers. The papers are referred to in the text by their chapter numbers.

Chapter 2

Schollert M, Burchard S, Faubert P, Michelsen A, Rinnan R (2014). Biogenic volatile organic compound emissions in four vegetation types in high arctic Greenland. Polar Biology 37: 237-249

Chapter 3

Vedel-Petersen I, Schollert M, Nymand J, Rinnan R. Volatile organic compound emission profiles of four common arctic plants. Submitted to Atmospheric Environment

Chapter 4

Schollert M, Kivimäenpää M, Valolahti HM, Rinnan R. Climate change alters leaf anatomy but has no effects on volatile emissions from arctic plants. Plant, Cell and Environment. In press

Chapter 5

Schollert M, Kivimäenpää M, Michelsen A, Blok D, Rinnan R. Anatomy and biogenic volatile organic compound emissions of arctic plants after one year of climate change manipulation. In preparation for Annals of Botany

Chapter 2 was reprinted with the permission from Springer Chapter 4 was reprinted with the permission from John Wiley and Sons

Table of contents 1 General introduction

13

1.1 An enhanced greenhouse effect

13

1.2 A changing arctic climate

13

1.3 Biogenic volatile organic compounds (BVOCs)

15

1.3.1 Definition and function

15

1.3.2 Atmospheric chemistry

16

1.3.2.1 Feedback to climate warming 1.3.3 Terpenoids

17 18

1.3.3.1 Isoprene

18

1.3.3.2 MTs and SQTs

19

1.3.4 ORVOCs and OVOCs

20

1.4 Modifications in leaf anatomy due to environmental changes

21

1.5 Research objectives and overview of experiments

22

1.6 References

26

2 Biogenic volatile organic compound emissions in four vegetation types in high arctic Greenland

35

3 Volatile organic compound emission profiles of four common arctic plants

57

4 Climate change alters leaf anatomy but has no effects on volatile emissions from arctic plants

89

5 Anatomy and biogenic volatile organic compound emissions of arctic plants after one year of climate change manipulation

149

6 General discussion

187

6.1 Arctic BVOC emission rates

187

6.1.1 Emission profiles of vegetation types and plant species

187

6.2 Leaf anatomy of the studied arctic plant species

193

6.3 Effects of climate change factors

195

6.3.1 BVOC emission rates

195

6.3.2 Leaf anatomy and the possible connection with BVOC emission rates

198

6.4 Manipulative field experiments – confounding effects

202

6.5 Conclusions and implications

203

6.6 References

206

1 General introduction 1.1 An enhanced greenhouse effect The climate system of the Earth is driven by shortwave radiation from the sun. About 30 % of the incoming shortwave radiation is reflected directly back to space by gases, aerosols and clouds in the atmosphere and by the Earth’s surface (i.e. the albedo effect), whereas the rest is absorbed by the Earth’s surface and atmosphere (Cubasch et al. 2013). The incoming radiation is balanced by outgoing long-wave radiation emitted from the Earth’s surface. The presence of certain gases in the atmosphere makes the Earth inhabitable as they trap outgoing long-wave radiation (Mitchell 1989; Cubasch et al. 2013). This result in a mean global temperature of 15 °C in contrast to temperatures far below the freezing point in the absence of an atmosphere (Mitchell 1989; Cubasch et al. 2013). This is what is called the greenhouse effect (Mitchell 1989; Cubasch et al. 2013). The most important greenhouse gas is water vapor followed by carbon dioxide (CO2) and also methane (CH4), ozone (O3) and nitrous oxide (N2O) (Cubasch et al. 2013). Since the beginning of the Industrial Era (1750), the greenhouse effect has been enhanced due to human activities increasing the emissions of greenhouse gases (Ciais et al. 2013). The atmospheric CO2 concentration has especially increased considerably due to burning of fossil fuels and land use changes (mainly deforestation) and is now more than 390 parts per million (ppm), which is about 40 % greater than in 1750 (Ciais et al. 2013). The globe has experienced an average surface warming of 0.89 °C in the period 1901-2012 and the past three decades have furthermore been warmer than all previous decades in the instrumental record (Hartmann et al. 2013). The global temperature is predicted to rise further during this century if greenhouse gas emissions continue unabatedly (Collins et al. 2013). However, even if the emissions would stop today, much of the warming would still persist for centuries due to the large ocean inertia and the long atmospheric lifetime of many greenhouse gases (Collins et al. 2013).

1.2 A changing arctic climate The Arctic has had a warming trend of about 1 °C per decade over the last three decades, which is considerably greater than the global mean (Hartmann et al. 2013). The rapid temperature increase at high latitudes is projected to continue, and by 2100, the Arctic is likely to experience a warming of 3-11 °C, which is between 2.2-2.4 times the global average 13

warming (Collins et al. 2013). The pronounced effects of climate warming in the Arctic make this region particularly important for studying climate change responses. Arctic ecosystems are adapted to extreme environmental conditions and are sensitive to even small changes. Plant growth in the Arctic is limited by low temperatures, short growing season, low nutrient availability and extremes in water availability (Bliss 1999). About 24 % of the land area in the Northern Hemisphere is underlain by permafrost ( i.e. permanently frozen ground) (Zhang et al. 1999), which contains an enormous pool of soil organic matter built up over thousands of years (Schuur et al. 2008; Tarnocai et al. 2009). The thawing of permafrost caused by climate warming (Collins et al. 2013; Vaughan et al. 2013) increases the decomposition of the stored organic matter thereby releasing nutrients and alleviating the nutrient limitation of plant growth (Mack et al. 2004; Schuur et al. 2007). Summer warming may additionally increase the decomposition rates as long as soil moisture does not become limiting for the microbial decomposer community (Hicks Pries et al. 2013). Furthermore, the rising temperatures can lead to a longer growing season due to earlier snowmelt in the spring and later snow accumulation in the autumn (Anisimov et al. 2007). Due to the climate warming, the Arctic will also experience alterations in precipitation, evaporation patterns and cloud cover (Collins et al. 2013). An increased cloud cover at high latitudes has the potential to reduce the solar radiation reaching the surface of the Earth and might cause a net cooling (Stanhill and Cohen 2001; Collins et al. 2013). The annual mean evaporation is very likely to increase over land in the high latitudes, which is consistent with an increased precipitation and an increased potential evaporation due to rising temperatures (Collins et al. 2013). Precipitation increases of more than 50 % in the Arctic by 2100 are among the highest projected globally (Collins et al. 2013). The increases can be attributed to both an enhanced local evaporation and an intensified poleward moisture transport from lower latitudes (Bintanja and Selten 2014). The projections are rather uncertain about the proportion of liquid and solid precipitation in the future. The proportion of solid precipitation might decrease as a result of higher winter temperatures leading to a decline in snow cover. A greater snowfall is however expected in colder regions due to increased rates of winter precipitation (Collins et al. 2013). Through its insulating effect, the snow cover rises the soil and canopy temperatures during winter and spring and thus protects the vegetation against detrimentally low air temperatures (Wipf and Rixen 2010). The snow cover can control the nutrient availability via 14

the effect of warming on microbial activity and decomposition rates (Schimel et al. 2004; Saccone et al. 2013; Vankoughnett and Grogan 2014) and can additionally affect the growing season soil moisture (Wipf and Rixen 2010). Furthermore, the melting of the snow cover determines the start and thereby also the length of the growing season. Although the snow cover might melt faster in a warmer climate, a thicker cover might lead to a delayed snowmelt and resulting shorter growing season (Wipf and Rixen 2010). The timing of snowmelt has an effect on flowering phenology, plant productivity and can cause considerable alterations in vegetation composition (Smith et al. 1995; Wahren et al. 2005; Wipf and Rixen 2010; Semenchuk et al. 2013). Tape et al. (2006) already presented evidence for an expansion of shrubs (alder, willow and birch) in Alaska and suggested that a pan-Arctic vegetation transition is underway. This is supported by Pearson et al. (2013) predicting an increase in woody cover by 52 %. Experimental warming has likewise been shown to result in an increase in the height and cover of shrubs and graminoids in the Arctic (Walker et al. 2006; Elmendorf et al. 2012). Changes in vegetation cover can have substantial implications for the Arctic ecosystems and for the potential feedbacks to climate change. E.g. a decreased albedo due shrub expansion leads to an increased absorbed solar radiation and a resulting positive feedback to regional warming (Chapin et al. 2005). According to Pearson et al. (2013), the vegetation changes are likely to result in an overall positive feedback possibly causing a greater warming than previously predicted.

1.3 Biogenic volatile organic compounds (BVOCs) 1.3.1 Definition and function All living organisms have the potential to emit biogenic volatile organic compounds (BVOCs) also known as non-methane hydrocarbons (Possell and Loreto 2013). On a global scale, the emissions of volatile organic compounds from biogenic sources far exceed the emissions from anthropogenic sources (Fuentes et al. 2000; Guenther et al. 2000; Peñuelas and Llusià 2003). The main source of BVOCs in the terrestrial biosphere is vegetation (Fuentes et al. 2000). Emissions by plants were first reported in the 1950s and 1960s (e.g. Sanadze 1956; Went 1960) and plants are now known to release a diverse variety of BVOCs, including compounds such as terpenoids (isoprene, monoterpenes, sesquiterpenes), alcohols, aldehydes, ketones, alkanes, alkenes, esters, ethers, acids and carbonyls (Kesselmeier and Staudt 1999; Laothawornkitkul et al. 2009; Possell and Loreto 2013; Monson and Baldocchi 2014). 15

BVOCs are emitted by all plant parts (Possell and Loreto 2013) and under stressful conditions, constitute up to 10 % of the carbon fixed by photosynthesis (Peñuelas and Llusià 2003). The widest variety of BVOCs is emitted from flowers and fruits, while the highest emission rates are from leaves (Laothawornkitkul et al. 2009). BVOC emission profiles vary greatly with time, space and plant species (Kesselmeier and Staudt 1999). The total annual global BVOC flux from vegetation is highly uncertain, but is likely in the range of 700-1000 × 1012 g C y-1 (Laothawornkitkul et al. 2009; Guenther et al. 2012). About 400-600 × 1012 g C of the annual BVOC flux to the atmosphere is constituted by the most emitted single BVOC, isoprene (C5H8, 2-methyl-1,3-butadiene) (Arneth et al. 2008; Laothawornkitkul et al. 2009; Guenther et al. 2012; Ashworth et al. 2013). The reason why plants constitutively emit BVOCs is still debated and the function of many of the compounds is still not clearly known (Peñuelas and Llusià 2004; Laothawornkitkul et al. 2009; Vickers et al. 2009). However, BVOCs are known to be involved in plant defense against herbivores and pathogens, attraction of pollinators and seed dispersers, growth, development and communication (Laothawornkitkul et al. 2009; Peñuelas and Staudt 2010; Fineschi and Loreto 2012). BVOCs, and especially isoprene, are additionally known for their protection against abiotic stresses such as heat and oxidative stress (Vickers et al. 2009; Loreto and Schnitzler 2010; Possell and Loreto 2013). The protection by isoprene is thought to be mediated through stabilization of the thylakoid membranes in the chloroplasts, scavenging of reactive oxygen species (Loreto and Schnitzler 2010; Possell and Loreto 2013) or reduction in the production of reactive oxygen and nitrogen species (Velikova et al. 2012). 1.3.2 Atmospheric chemistry BVOCs provide a strong link between the terrestrial biosphere, the atmosphere and the climate. BVOCs have atmospheric lifetimes ranging from a few seconds to several years and play important roles in the atmospheric chemistry (Monson and Baldocchi 2014). Once released, BVOCs participate in complex oxidative reactions with hydroxyl radicals (OH), O3 and nitrate radicals (NO3), which potentially lead to CO2 and water as the ultimate products (Laothawornkitkul et al. 2009; Monson and Baldocchi 2014). However, the complete oxidation only occurs for a fraction of the emitted BVOCs as many of the intermediate products are lost through wet and dry deposition (Laothawornkitkul et al. 2009; Monson and Baldocchi 2014).

16

The oxidation of BVOCs is primarily initiated by reaction with OH radicals, which is also the principal oxidant for the potent greenhouse gas CH4. By competing for OH radicals, BVOCs indirectly prolong the lifetime of CH4 in the atmosphere (Laothawornkitkul et al. 2009; Monson and Baldocchi 2014). BVOCs furthermore contribute to the formation and consumption of tropospheric O3. In the presence of nitrogen oxides (NOx = NO + NO2), which result from e.g. fossil fuel combustion, power generation, road transport and fertilizer application, BVOCs can lead to the formation of O3 (The Royal Society 2008; Laothawornkitkul et al. 2009; Monson and Baldocchi 2014). However, in unpolluted air with low NOx concentrations, oxidation of BVOCs can lead to consumption of O3 (Laothawornkitkul et al. 2009). BVOCs not only affect gas phase atmospheric chemistry, but are also known as precursors of secondary organic aerosols (SOAs) (Laothawornkitkul et al. 2009; Monson and Baldocchi 2014). SOAs influence the climate system directly by scattering solar radiation and indirectly by acting as cloud condensation nuclei (Fuentes et al. 2000; Laothawornkitkul et al. 2009; Kulmala et al. 2013; Monson and Baldocchi 2014). This results in a reduction of the fraction of solar radiation penetrating the atmosphere and thus mitigates the warming caused by greenhouse gases in the atmosphere (Boucher et al. 2013; Kulmala et al. 2013). 1.3.2.1 Feedback to climate warming Emissions of BVOCs from vegetation are strongly dependent on abiotic factors such as temperature and light (see 1.3.3 for more details), and overall, the climate warming is expected to result in increased BVOC emission (Laothawornkitkul et al. 2009; Peñuelas and Staudt 2010). Alterations in BVOC emissions are of great interest as they, through their roles in atmospheric chemistry, have the potential to indirectly feed back both positively and negatively on the climate warming (Arneth et al. 2010; Kulmala et al. 2013). An increased BVOC emission strengthens the cooling effect of aerosols (Paasonen et al. 2013), but can also increase the diffuse radiation via scattering by aerosols leading to enhanced plant photosynthesis and further enhanced emission (Kulmala et al. 2013). The magnitude and sign of the overall feedback of increased BVOC emissions are uncertain (Kirtman et al. 2013; Myhre et al. 2013). One of the greatest uncertainties in the current climate models is the role of SOAs in modifying the radiation budget of the Earth (Boucher et al. 2013; Monson and Baldocchi 2014).

17

In this thesis, BVOCs will be divided into the following groups: isoprene, monoterpenes (MTs), sesquiterpenes (SQTs), other reactive volatile organic compounds (ORVOCs, having atmospheric lifetimes of < 24 hours, Guenther et al. 1995) and other volatile organic compounds (OVOCs). 1.3.3 Terpenoids Terpenoids constitute the most important BVOCs in terms of atmospheric chemistry. The most common terpenoids are hemiterpenes (C5Hn, e.g. isoprene), MTs (C10Hn, e.g. α-pinene) and SQTs (C15Hn, e.g. α-humulene) (Kesselmeier and Staudt 1999; Kulmala et al. 2013; Monson and Baldocchi 2014). The majority of BVOCs are made up by isoprene and MTs (Li and Sharkey 2013). All terpenoids are synthesized via a common C5 unit, isopentenyl pyrophosphate (IPP), which can be reversibly converted to dimethylallyl pyrosphosphate (DMAPP). IPP can be synthesized via two pathways: the mevalonic acid (MVA) pathway and the methylerythritol phosphate (MEP, also called the non-mevalonate pathway) pathway (Kesselmeier and Staudt 1999; Laothawornkitkul et al. 2009; Loreto and Schnitzler 2010; Li and Sharkey 2013). The MVA pathway takes place in the cytosol and converts acetyl-CoA to IPP, while the MEP pathway takes place in the chloroplasts and uses pyruvate and glycealdehyde-3-phosphate to produce IPP (Li and Sharkey 2013). Isoprene and most MTs are produced by the MEP pathway, where DMAPP is converted to isoprene by isoprene synthase, while MTs are made by terpene synthases from geranyl pyrophosphate (GPP). GPP is produced as a result of geranyl pyrophosphate synthase combining DMAPP with one IPP (Kesselmeier and Staudt 1999; Li and Sharkey 2013). SQTs are produced by the MVA pathway, where DMAPP is combined with two IPP units resulting in the SQT precursor farnesyl pyrophosphate (FPP). FPP is then converted to specific SQTs by different terpene synthases (Loreto and Schnitzler 2010; Li and Sharkey 2013). Terpenoids can either be directly emitted or stored in specialized storage structures (e.g. glandular trichomes or resin ducts) for later release e.g. upon mechanical stress (Fineschi et al. 2013). 1.3.3.1 Isoprene Isoprene is never stored in plants but is directly emitted from de novo synthesis, which is tightly bound to the photosynthetic C metabolism (Loreto and Schnitzler 2010; Li and Sharkey 2013; Monson and Baldocchi 2014). Isoprene almost entirely escapes through stomata when these are open (Harley 2013; Niinemets et al. 2014). Upon stomatal closure, the intercellular isoprene concentration increases rapidly, leading to an increase in the diffusion 18

gradient across the cuticle, which forces the release of isoprene in order to resume steady state. Isoprene emission can thus not be controlled by stomatal conductance (Niinemets et al. 2004; Harley 2013). Isoprene emission exhibits strong temperature dependence up to 40-45 °C caused by an increased isoprene synthase activity (Li and Sharkey 2013). However, while the optimum temperature for isoprene synthase is ~ 50 °C, the accumulation of DMAPP and intermediate metabolites in the MEP pathway is largest at ~ 35 °C after which it decreases (Li et al. 2011; rewieved by Li and Sharkey 2013). As a result, the emission at temperatures above 40 °C is only sustainable for shorter periods as a shortage of substrates rapidly occurs (Li et al. 2011). Isoprene emission is also light dependent (Kesselmeier and Staudt 1999; Li and Sharkey 2013), which is possibly explained by changes in substrate levels presumably related to the light reactions of the photosynthesis (reviewed by Li and Sharkey 2013). Isoprene-emitting species occur in many plant taxa (Kesselmeier and Staudt 1999; Monson et al. 2013). However, strong isoprene emitters are especially found within woody plant species including poplars (Populus spp.), willows (Salix spp.) and oaks (Quercus spp.) (Kesselmeier and Staudt 1999; Fineschi et al. 2013). The global isoprene emission is highest in the Tropics with the highest contributions observed between 12 °N and 24 °S (Guenther et al. 1995). In the Arctic, Salix spp. are the most common isoprene emitters (Potosnak et al. 2013). 1.3.3.2 MTs and SQTs Traditionally, MT emissions have been assumed to originate from specialized storage structures (Kesselmeier and Staudt 1999; Laothawornkitkul et al. 2009). However, a substantial part of MTs are directly emitted by de novo synthesis (Ghirardo et al. 2010). Emissions of all MTs are temperature dependent (Laothawornkitkul et al. 2009; Loreto and Schnitzler 2010). However, while stored compounds escape directly to the atmosphere mainly depending

on

the

temperature-dependent

volatilization

from

the

storage

pools

(Laothawornkitkul et al. 2009), de novo synthesized compounds are additionally controlled by light (Tarvainen et al. 2005). As for isoprene, the emissions of non-oxygenated monoterpenes are independent of stomatal conductance (Niinemets et al. 2014). However, unlike isoprene, some compounds build up slowly in the intercellular space (Niinemets et al. 2004). E.g. hydrophilic compounds such as the oxygenated MT linalool can be non-specifically stored in the aqueous phase of the leaf 19

(Niinemets et al. 2004). Thus, upon stomata closure, the diffusion gradient across the cuticle increases slower and it takes longer before a steady state is resumed (Niinemets et al. 2004, 2014). Emissions of some monoterpenes can even continue at the expense of the non-specific storage for at least 10-15 min (Niinemets et al. 2004). MTs are known for their roles in defense against pathogens and herbivores (Holopainen 2004) and in plant-plant interactions (Peñuelas and Staudt 2010). They have additionally been proposed to have a similar function to that of isoprene in protecting against elevated temperatures and O3 levels (Loreto et al. 1998, 2004). The oxidation of MTs is an important contributor to SOA formation and growth (Cahill et al. 2006; Hallquist et al. 2009). The boreal landscape is considered to be a great MT source due to the predominance of strong MT emitters such as conifers and birches (Rinne et al. 2009). SQTs are among the most reactive terpenes, and like MTs, the oxidation of these compounds is an important source of SOAs in the atmosphere (Monson and Baldocchi 2014). SQTs are usually strongly smelling compounds (Kesselmeier and Staudt 1999). They are typically found in flower fragrances (Chen et al. 2003) and the emission is highly dependent on the plant phenological stage (Duhl et al. 2008). The emission of SQTs is additionally enhanced by biotic stresses (Loreto and Schnitzler 2010) and play critical roles in plant-herbivore and plant-plant interactions (Holopainen 2004; Duhl et al. 2008). SQTs are typically stored compounds and their emissions are highly temperature dependent (Duhl et al. 2008). However, some SQTs are also known to be affected by light (reviewed by Duhl et al. 2008). SQTs have been poorly investigated, which is largely due to their high reactivity and the relative low vapor pressure making them challenging to study (Duhl et al. 2008). 1.3.4 ORVOCs and OVOCs Besides terpenoids, plants also emit a great range of other compounds (e.g. Kesselmeier and Staudt 1999). In this thesis, these non-terpenoid compounds are divided into ORVOCs and OVOCs based on their reactivity in the atmosphere. The ORVOCs, which have atmospheric lifetimes of 24 hours in the atmosphere (Guenther et al. 1995; Kesselmeier and Staudt 1999), and can thus, potentially be transported over long distances in the atmosphere. Methanol (CH4O) is an example of an OVOC especially emitted from expanding leaves (Kesselmeier and Staudt 1999; Monson 2013). Methanol was however not measured in this thesis. Examples of OVOCs in this thesis include e.g. acetophenone (C8H8O), isopropylcyclobutane (C7H14) and 1-butyl-2-methylcyclopropane (C8H16). ORVOCs and OVOCs might constitute volatile compounds, which are traditionally considered to be anthropogenic. Although not comparable to arctic plant species, Jardine et al. (2010) found creosotebush (Larrea tridentate) to emit non-terpenoid compounds such as aromatic compounds including benzene. This suggests that some compounds normally assumed to be anthropogenic might be emitted from vegetation. Soil, litter and microorganisms are also known to be responsible for emissions of several compounds belonging to ORVOCs and OVOCs (Leff and Fierer 2008; Insam and Seewald 2010). Compared with especially isoprene and MTs, the emissions of other volatile compounds from vegetation have in general been relatively poorly investigated (Kesselmeier and Staudt 1999).

1.4 Modifications in leaf anatomy due to environmental changes Leaf anatomy is highly flexible and reacts sensitively to changes in environmental factors such as light, temperature, nutrients, drought, CO2 and ozone (Fink 1999; Luomala et al. 2005 and references herein). Alterations in leaf anatomy develop rapidly and studies have shown modifications in leaf anatomy already during the first growing season for leaves developed under e.g. increased temperature, nitrogen fertilization, elevated O3 and drought (Pääkkönen and Holopainen 1995; Pääkkönen et al. 1998; Hartikainen et al. 2009, 2014). Relatively much information exists on the leaf anatomical acclimation of tree species, whereas it is largely unknown how the leaf anatomy of arctic plants species respond to changes in the environment. Elevated temperature has been observed to induce thinner leaves/needles and leaf tissues, and larger leaf area in deciduous and conifer trees (Higuchi et al. 1999; Luomala et al. 2005; Hartikainen et al. 2009, 2014). Similarly, shade-adapted leaves are usually thinner than sun21

adapted leaves (Larcher 2003; Terashima et al. 2006). Both warming and shading have been shown to reduce the density of trichomes on the leaf surface (Marques et al. 1999; Hartikainen et al. 2014). Changes in the environment can also lead to modifications in stomatal density (Beerling and Chaloner 1993; Luomala et al. 2005). Stomatal density has been observed to decrease in response to warming and shading (Larcher 2003; Luomala et al. 2005). The leaf anatomy also responds to soil moisture, and a xeric environment generally leads to thicker leaves and epidermis, higher trichome density and smaller but more numerous stomata (Bosabalidis and Kofidis 2002; Larcher 2003; Guerfel et al. 2009). Leaf anatomy has been shown to influence BVOC emissions. Hartikainen et al. (2009) suggested that warming-induced thinner leaves, with shorter diffusion pathways for BVOCs, could be linked to increased BVOC emissions from Populus tremula under warming. And recently, Rasulov et al. (2014) showed that leaf structural modifications were the primary reasons for temperature acclimation of photosynthesis and isoprene emission of hybrid aspen (P. tremula x P. tremuloides).

1.5 Research objectives and overview of experiments The BVOC emissions from the arctic region are assumed to be low due to sparse vegetation cover, low temperatures and short growing seasons (Rinnan et al. 2014). However, data from the region is insufficient for giving any exact numbers on magnitudes of arctic emissions. Studies have observed emissions of isoprene and other BVOCs from subarctic environments of the same magnitude as the emissions from boreal environments (Tiiva et al. 2008; Bäckstrand et al. 2010; Holst et al. 2010). Emissions from boreal, subarctic and high arctic environments might nevertheless only constitute a minor fraction of the global BVOC emission (Guenther et al. 1995; Bäckstrand et al. 2008). Yet, as pointed out earlier, the Arctic is likely to experience the most pronounced effects of climate warming, which can lead to substantial increases in the arctic BVOC emissions (Lathière et al. 2005; Rinnan et al. 2014). Studies from the Subarctic have shown experimental warming by 2-3 °C to increase the BVOC emissions at ecosystem level by as much as 50-250 % depending on compound and year (Tiiva et al. 2008; Faubert et al. 2010). The low emissions at high latitudes have additionally been suggested to be mostly due to low temperatures rather than to low emission potentials of the prevalent vegetation (Holst et al. 2010). The quantity and quality of BVOC emissions are furthermore expected to change due

22

to alterations in growing season length and vegetation biomass and composition (e.g. Rinnan et al. 2014). The objectives of this thesis are as follows: •

As data on BVOC emissions from the arctic region is lacking, an aim of this thesis was to obtain estimates of high arctic BVOC emissions in different vegetation types on ecosystem level (Chapter 2).

•

This thesis aimed to elucidate BVOC emission profiles and magnitudes for dominant arctic plant species since information on plant species level BVOC emissions is limited and as climate change will lead to changes in the vegetation composition (Chapter 3).

•

Due to the rapid advancement of climate change in the Arctic, the thesis aimed to assess the responses of BVOC emissions to climate change factors from shoots of dominant arctic plant species in situ using field manipulation experiments. Understanding how BVOC emissions respond to climate change will help us to predict the future feedbacks of BVOCs on the local and global climate. In this thesis, the effects of warming by open-top chambers (OTCs), shading, snow addition and the combination of warming and snow addition were examined (Chapters 4 and 5)

•

Since leaf function and anatomy are inter-related, the aim was to examine the modification of leaf anatomy of dominant arctic plant species to warming, shading, snow addition and the combination of warming and snow addition applied in field manipulation experiments (Chapters 4 and 5).

The measurements for this thesis were conducted at subarctic, low arctic and high arctic locations. An overview of the experiments in this thesis can be seen in Table 1.1. Photos of the field manipulation experiments in Zackenberg, NE Greenland (71°30’ N, 20°30’ W), Abisko, N Sweden (68°21’ N, 18°49’ E) and on Disko Island, W Greenland (69°15’N, 53°34’W) can be seen in Fig. 1.1.

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Table 1.1 Field experiments used in this thesis. Location Zackenberg NE Greenland (71°30’ N, 20°30’ W)

Climate Plant species/vegetation type Treatments High Arctic Cassiope tetragona heath No treatments Salix arctica heath Vaccinium uliginosum heath Mixed heatha

Kobbefjord SW Greenland (64°07’ N, 51°21’ W)

Low Arctic

Established

Chapter 2

Empetrum nigrum ssp. hermaphroditum Betula nana Salix arctophila Salix glauca High Arctic Cassiope tetragona

No treatments

Warming Shading

2004

4

Zackenberg NE Greenland (71°30’ N, 20°30’ W)

High Arctic Salix arctica

Warming Shading

2004

4

Abisko N Sweden (68°21’ N, 18°49’ E)

Subarctic

Empetrum nigrum ssp. hermaphroditum Cassiope tetragona Betula nana

Warming Shading

1989

4

Disko Island W Greenland (69°15’N, 53°34’W)

Low Arctic

Empetrum nigrum ssp. hermaphroditum Vaccinium uliginosum Betula nana

Warming Snow addition and their interaction

2012

5

Zackenberg NE Greenland (71°30’ N, 20°30’ W)

a

3

mixture of Kobresia myosuroides, Dryas spp. and Poa arctica

As BVOC emissions are known to vary greatly for different plant species (Kesselmeier and Staudt 1999), the rates and profiles of the BVOC emissions were expected to vary considerably for the studied vegetation types and plant species (Chapters 2 and 3). Warming by OTCs was hypothesized to increase the emissions from individual plant shoots in a similar manner as observed at ecosystem level in the Subarctic (Tiiva et al. 2008; Faubert et al. 2010) (Chapters 4 and 5). Since the field manipulation experiment on Disko Island was set up only one year prior to the measurements in this thesis, increased BVOC emissions due to warming were expected to be driven by a direct temperature response (Chapter 5). Shading was expected to decrease the BVOC emissions due to the light-dependency of many BVOCs (Laothawornkitkul et al. 2009; Monson and Baldocchi 2014) (Chapter 4). Due to a later snow melt of a thicker snow cover, snow addition was hypothesized to lead to a delayed plant activity and thus BVOC emissions (Chapter 5). In the long-term field manipulation experiments in Zackenberg and Abisko (Chapter 4), it was hypothesized that warming would lead to thinner leaves as commonly observed for trees 24

(Higuchi et al. 1999; Luomala et al. 2005; Hartikainen et al. 2009, 2014). Shading was likewise expected to result in thinner leaves and reduced density of trichomes and stomata (Marques et al. 1999; Larcher 2003; Terashima et al. 2006). I expected that modifications in leaf anatomy could explain some of the variation in BVOC emissions in a similar manner as found by Hartikainen et al. (2009). As leaf anatomy is very sensitive to changing environmental conditions, modifications were expected in the experiment on Disko Island despite the short treatment period of a year (Chapter 5). (a)

(b)

(c)

(d)

Figure 1.1 Field manipulation experiments with shading and warming treatment in a Abisko, N Sweden (68°21’ N, 18°49’ E) and b in Cassiope tetragona-dominated heath in Zackenberg, NE Greenland (71°30’ N, 20°30’ W). c One block in the snow fence (arrow) experiment on Disko Island, W Greenland (69°15’N, 53°34’W) with d open-top chambers (circle).

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2 Biogenic volatile organic compound emissions in four vegetation types in high arctic Greenland Schollert M, Burchard S, Faubert P, Michelsen A and Rinnan R (2014) Polar Biology 37: 237-249

Reprinted with the permission from Springer

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Polar Biol (2014) 37:237–249 DOI 10.1007/s00300-013-1427-0

ORIGINAL PAPER

Biogenic volatile organic compound emissions in four vegetation types in high arctic Greenland Michelle Schollert • Sebrina Burchard Patrick Faubert • Anders Michelsen • Riikka Rinnan

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Received: 16 May 2013 / Revised: 18 October 2013 / Accepted: 12 November 2013 / Published online: 22 November 2013 Ó Springer-Verlag Berlin Heidelberg 2013

Abstract Biogenic volatile organic compounds (BVOCs) emitted from terrestrial vegetation participate in oxidative reactions in the atmosphere, leading to the formation of secondary organic aerosols and longer lifetime of methane. Global models of BVOC emissions have assumed minimal emissions from the high latitudes. However, measurements from this region are lacking, and studies from the high arctic are yet to be published. This study aimed to obtain estimates for BVOC emissions from the high arctic, and hereby to add new knowledge to the understanding of global BVOC emissions. Measurements were conducted in four vegetation types dominated by Cassiope tetragona, Salix arctica, Vaccinium uliginosum and a mixture of Kobresia myosuroides, Dryas spp. and Poa arctica. Emissions were measured by an enclosure technique and collection of volatiles into adsorbent cartridges in August. Volatiles were analyzed by gas chromatography–mass spectrometry following thermal desorption. Isoprene

showed highest emissions in S. arctica heath. Monoterpene and sesquiterpene emissions were especially associated with C. tetragona heath. Total observed emissions were comparable in magnitude to emissions previously found in the subarctic, whereas isoprene emissions were lower. This study shows that considerable amounts of BVOCs are emitted from the high arctic. The results are also of importance as the emissions from this region are expected to increase in the future as a result of the predicted climate warming in the high arctic. We suggest further studies to assess the effects of climate changes in the region in order to gain new knowledge and understanding of future global BVOC emissions. Keywords Biogenic volatile organic compounds  VOC  Isoprene  Monoterpene  Sesquiterpene  Arctic ecosystems

Introduction Electronic supplementary material The online version of this article (doi:10.1007/s00300-013-1427-0) contains supplementary material, which is available to authorized users. M. Schollert (&)  S. Burchard  A. Michelsen  R. Rinnan Terrestrial Ecology Section, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen Ø, Denmark e-mail: [email protected] M. Schollert  A. Michelsen  R. Rinnan Department of Geoscience and Natural Resource Management, Center for Permafrost (CENPERM), University of Copenhagen, Øster Voldgade 10, 1350 Copenhagen K, Denmark P. Faubert Chaire en E´co-conseil, De´partement des Sciences Fondamentales, Universite´ du Que´bec a` Chicoutimi, 555, boulevard de l’Universite´, Chicoutimi, QC G7H 2B1, Canada

Vegetation releases a diverse group of biogenic volatile organic compounds (BVOCs), which comprise compounds such as isoprenoids (isoprene, monoterpenes, sesquiterpenes) and oxygenated hydrocarbons (alcohols, aldehydes and ketones) (Kesselmeier and Staudt 1999; Pen˜uelas and Llusia` 2001; Laothawornkitkul et al. 2009; Possell and Loreto 2013). The most prominent single BVOC is isoprene (C5H8, 2-methyl-1,3-butadiene), which annually adds an estimated 400–600 Tg carbon to the atmosphere (Guenther et al. 1995; Laothawornkitkul et al. 2009; Ashworth et al. 2013). BVOCs are involved in plant defense, reproduction, growth, development and communication (Laothawornkitkul et al. 2009). Isoprenoids can be either directly emitted, as always for isoprene, or stored in

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specialized storage structures for later release, e.g., upon mechanical stress (Fineschi et al. 2013). The high reactivity of most BVOCs makes them highly important to the atmospheric chemistry. Once released, BVOCs participate in oxidative reactions with hydroxyl radicals (OH), ozone (O3) and nitrate radicals (NO3) and contribute to the formation and consumption of tropospheric O3 (Laothawornkitkul et al. 2009). Oxides of nitrogen (NOx = NO ? NO2), which result from, e.g., fossil fuel combustion, power generation and road transport, can also contribute to the formation of O3 (Fowler et al. 2008; Laothawornkitkul et al. 2009). However, low NOx concentrations in clean air, such as in remote arctic environments, lead to consumption of O3. By competing for OH radicals, BVOCs also indirectly prolong the lifetime of the greenhouse gas methane (CH4). BVOCs are furthermore known to be precursors of secondary organic aerosols (SOAs), which scatter solar radiation and function as cloud condensation nuclei (Fuentes et al. 2000; Laothawornkitkul et al. 2009; Kulmala et al. 2013). Thus, BVOCs provide a strong link between the terrestrial biosphere, the atmosphere and the climate. Total BVOC emissions vary considerably in time, space and between species (Kesselmeier and Staudt 1999), and emissions are strongly influenced by temperature and light (Guenther et al. 1993; Duhl et al. 2008). The total global BVOC pool is dominated by emissions from the tropics, and the emissions then decrease toward the poles (Guenther et al. 1995). Global models of BVOC emissions have assumed minimal emissions from the high latitudes due to low temperatures, short growing seasons and sparse vegetation cover (Guenther et al. 1995; Arneth et al. 2008). However, measurements from this region of the world are lacking, and emissions from the high arctic are yet to be quantified. Here, the high arctic is defined as the northern part of the arctic with a mean temperature for the warmest month of *6 °C. While the southern part of the arctic, the low arctic, has higher more closed lush vegetation, the high arctic has open, very low-stature vegetation (Walker et al. 2005; Meltofte and Rasch 2008). Studies have shown that substantial amounts of isoprene and other BVOCs are emitted from subarctic environments, concluding that the measured emissions are of the same order of magnitude as those from boreal environments (Tiiva et al. 2008; Ba¨ckstrand et al. 2010; Holst et al. 2010). Although boreal and subarctic ecosystems might only represent a minor source of BVOCs globally, the emissions still comprise a measurable amount of carbon lost from these environments (Ba¨ckstrand et al. 2008; Tiiva et al. 2008; Faubert et al. 2012). As pointed out by Potosnak et al. (2013), more experimental data are needed in order to improve global models on isoprene emissions.

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Likewise, high arctic BVOC emissions need to be addressed in order to gain new knowledge and to adjust the estimates on the global BVOC emissions. Hence, the aim of the present study was to obtain estimates of BVOC emissions from the high arctic. To account for spatial variation, measurements were taken in four different vegetation types. We compared plant species distribution and BVOC emission profiles obtained by principal component analysis (PCA) in order to shed light on the differences between the relative amounts of BVOCs emitted in relation to vegetation distribution. The capacity to emit isoprene has been gained and lost multiple times during the evolution of plants, and this suggests that there is only a narrow range of conditions in which isoprene emission is advantageous (reviewed by Fineschi et al. 2013; Monson 2013). Isoprene is known to protect against abiotic stress, especially high temperatures, and oxidative stress (Vickers et al. 2009; Possell and Loreto 2013), and thus, high isoprene emitters could be expected to have a competitive advantage in warm, dry and polluted environments (Fineschi et al. 2013), and therefore, we expect low isoprene emissions from the high arctic vegetation.

Materials and methods Experimental setup The study was conducted in the vicinity of the Zackenberg Research Station in the Zackenberg Valley, NE Greenland (74°300 N, 20°300 W), in August 2009. The area is in a zone with continuous permafrost (Meltofte and Thing 1996), the mean annual air temperature 2 m above terrain is -7.9 °C (2003–2005), and the average annual precipitation is approximately 261 mm (1996–2005) (Hansen et al. 2008). The growing season lasts 2–3.5 months depending upon year and vegetation type (Ellebjerg et al. 2008; Arndal et al. 2009). Mean monthly air temperatures vary between 3 and 7 °C in July and August (1996–2005), and July is the warmest month of the year with a mean monthly air temperature of 5.8 °C (Hansen et al. 2008). However, conditions of low-stature vegetation are known to be decoupled from conditions in the free atmosphere with near-ground temperatures clearly exceeding air temperatures (Ko¨rner et al. 2003; Scherrer and Ko¨rner 2009). BVOC emissions were measured in four mesic to dry heath vegetation types dominated by Cassiope tetragona, Salix arctica, Vaccinium uliginosum and a mixture of Kobresia myosuroides, Dryas spp. and Poa arctica. In each community, five (or six for the mixed heath) plots of 0.5 9 0.5 m (1 9 1 m for C. tetragona and S. arctica

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heath) were selected and marked. In the plots, aluminum chamber bases for BVOC measurements (21 9 21 cm) were inserted into the soil to a depth of approximately 10 cm. Chamber bases were permanently installed in July 2007 for C. tetragona and S. arctica heath, in July 2008 for V. uliginosum heath and on July 1, 2009, for mixed heath. This recovery time after chamber base placement was long enough not to cause any induced BVOC emissions because release of induced BVOCs after physical disturbance of vegetation ceases within a day after cutting (Rinnan et al. 2013). On the other hand, the inevitable cutting of some roots by the chamber bases could have led to lower aboveand belowground plant biomass inside the chamber bases, which may have caused reduced BVOC emissions. BVOC measurements and analysis Five measurement campaigns (I–V) were conducted in the period August 5–27, 2009. BVOC emissions from the plant/soil system were measured by a push–pull enclosure technique using a transparent polycarbonate chamber (volume 10 L). The chamber was placed on the chamber base and sealed airtight by water during measurements. Air was circulated through the chamber by battery-operated pumps (12 V; Rietschle Thomas, Puchheim, Germany) with outflow set to 200 ml min-1 and inflow to 215 ml min-1 keeping a slight overpressure in the chamber to avoid air leakage from the outside (Staudt et al. 2000). The incoming air was purified by a charcoal filter to remove particles and VOCs present in ambient air and by a MnO2 scrubber to remove O3 (Ortega and Helmig 2008). As air was pumped out of the chamber, BVOCs were adsorbed in stainless steel adsorbent cartridges (Perkin Elmer; Boston, MA, USA) containing Tenax TA and Carbopack B adsorbents (100 mg each, mesh 60/80; Supelco, Bellefonte, PA, USA). The detection limit of BVOCs is about 1 ng depending on compound. The period for BVOC sampling was 0.5 h and represented a sampled air volume of 6 L. The chamber was equipped with a fan to ensure mixing of air during the sampling. Temperature and relative humidity inside the chamber (Tinyview Plus; Gemini Data loggers Ltd., Chichester, UK) and photosynthetic photon flux density (PPFD) (quantum sensor; Li-Cor, Lincoln, NE, USA) were recorded every third minute during the sampling period. Furthermore, the temperature in the canopy at 2–5 cm above the soil surface was recorded during sampling (Tinytag; Gemini Data loggers Ltd., Chichester, UK). The adsorbent cartridges were sealed with Teflon-coated brass caps and transported to laboratory for analysis. BVOCs were analyzed by thermal desorption (ATD400; Perkin Elmer, Wellesley, MA, USA) and gas chromatography–mass spectrometry (GC 6890, MSD 5973; Hewlett

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Packard, Palo Alto, CA, USA) (see Faubert et al. 2010a for details). BVOCs were identified according to the mass spectra in the Wiley data library (Wiley and Sons Ltd., Chichester, UK) and quantified using pure standard solutions for isoprene, a-pinene, camphene, sabinene, 3-carene, limonene, 1,8-cineole, c-terpinene, a-copaene, d-cadiene, aromadendrene and cis-3-hexanyl acetate in methanol (Fluka, Buchs, Switzerland) (Faubert et al. 2010a). Standard solutions were injected in cartridges and analyzed by thermal desorption and gas chromatography–mass spectrometry as samples. The BVOCs were classified into the following groups: isoprene, monoterpenes (MTs), sesquiterpenes (SQTs) and other reactive volatile organic compounds [ORVOCs, having atmospheric lifetimes of\1 day (Guenther et al. 1995)]. When quantifying compounds for which no pure standard was available, a-pinene was used for quantification of MTs, a-copaene for SQTs and cis-3hexanyl acetate for ORVOCs. Chromatograms were analyzed using Enhanced ChemStation software (G1701CA C.00.00 21 Dec 1999; Agilent Technologies, Santa Clara, CA, USA). Compounds that appeared in at least 10 % of the measurements and had an identification quality in the Wiley data library of above 90 % were included in the dataset, whereas compounds that originated from measurement material or the analysis system, based on blank measurements, were excluded. The BVOC concentrations (lg L-1) in the cartridges and emission rates (lg m-2 ground h-1) were calculated as by Faubert et al. (2012). Vegetation analysis The percentage vegetation cover in the plots was estimated using the point intercept method in August 2009 (Jonasson 1988). The analysis was conducted using a transparent polycarbonate plate with evenly distributed holes. For each hole, the presence of vascular plant species, moss, lichens, litter, organic crust and bare soil was recorded. A total of 42 holes were used for the mixed heath in an area of 21 9 21 cm, while 56 holes were used for the three remaining vegetation types. Statistical analyses Statistical analyses were conducted using SAS 9.2 (SAS institute Inc. 2003). One-way ANOVA was applied to test for differences in the emissions of isoprene, total MTs, SQTs and ORVOCs between vegetation types within each measurement campaign. Each measurement campaign had to be tested separately because not all vegetation types could be measured within each campaign. Chamber temperature was included as a covariate in the model when p \ 0.2 in order to account for the varying environmental

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conditions. ANOVA was followed by Tukey’s test to distinguish the significantly different means. Likewise, oneway ANOVA and Tukey’s test were used for analyzing differences in vegetation cover between vegetation types. Spearman’s rank correlation was used to inspect the influence of chamber temperature and PPFD on the emissions of isoprene, total MTs, SQTs and ORVOCs. Principal component analysis was performed on BVOC emission data and vegetation cover percentages using LatentiXÓ (data analysis software, version 2.11). This was done in order to investigate how emission profiles, i.e., the relative amounts of the emitted individual BVOCs, differed for vegetation types and to examine the differences in vegetation cover between the vegetation types. Principal components (PCs) were extracted for each model following centering and unit variance scaling of the variables and removal of one outlier for the PCA on BVOC emissions. The PCA scores for the two first PCs for both models were analyzed using one-way ANOVA followed by Tukey’s test.

Results Temperature and light conditions The mean daytime air temperature was below 10 °C and gradually decreased through August (Fig. 1). Chamber temperatures during measurements were considerably higher, but were very similar to canopy temperature measured at 2–5 cm above the soil surface in the same periods (Fig. 1). PPFD was generally high during measurements but decreased during the month of measurements (Fig. 1). BVOC emissions from the vegetation types All in all 28 BVOCs were detected: isoprene, 9 MTs, 7 SQTs and 11 ORVOCs. The total non-standardized BVOC emissions ranged from 21.0 ± 7.9 (mean ± SE) to 64.1 ± 18.0 lg m-2 h-1, and the composition of emitted compounds was different in each vegetation type (Figs. 2, 3). Emission potentials at 1,000 lmol m-2 s-1 PPFD and 20 or 30 °C are presented in Table S1 and show similar significant differences between vegetation types as before the standardization. Cassiope tetragona heath had the highest total BVOC emission rate averaging at 64.1 ± 18.0 lg m-2 h-1. The MT and SQT emissions averaged over all campaigns were 24.4 ± 6.5 and 9.4 ± 4.2 lg m-2 h-1 (Table S2) constituting 38 and 15 % of the total BVOC emissions, respectively (Fig. 2). In comparison, isoprene constituted only 2 % of the total emissions (Figs. 2, 3a). Limonene was the most emitted MT, while c-eudesmol was the SQT emitted

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at the highest rate (Table S2). During measurement campaign V, the MT and SQT emissions were approximately zero in this vegetation type (Fig. 3b, c), coinciding with a chamber temperature below 5 °C and PPFD about 100 lmol m-2 s-1 (Fig. 1). In S. arctica heath, isoprene was the most emitted single BVOC, constituting 28 % of the total emissions (Fig. 2). Isoprene emission was from three to more than ten times higher in S. arctica heath than in the remaining investigated vegetation types (Fig. 3a). However, the emission of isoprene decreased below detection limit in the end of August when the chamber temperatures were at or below 10 °C (Fig. 1). MT emissions, dominated by limonene, represented 12 % of the total in S. arctica heath, while no SQTs were detected (Fig. 2; Table S2). Vaccinium uliginosum heath had the lowest total BVOC emissions (Fig. 3). MTs contributed 50 % to the total, while SQTs accounted for 16 % (Fig. 2). Again, limonene and c-eudesmol dominated the MT and SQT emissions, respectively (Table S2). In this heath type, ORVOCs contributed 31 % (6.5 ± 2.7 lg m-2 h-1) of the total (Fig. 2). Mixed heath had the highest relative emissions of ORVOCs, constituting 81 % of the total (Figs. 2, 3d). The two most dominant ORVOCs were methylcyclohexane and 3-methylhexane (Table S2). MTs, mostly comprising limonene, were 14 % of the total, whereas virtually no SQTs were detected (Fig. 2; Table S2). When isoprene emission was plotted against MT emissions including the whole dataset (all campaigns and vegetation types), an inverse relationship between these emissions was revealed with a high isoprene emission generally corresponding to low total MT emissions and vice versa (Fig. S1). The Spearman’s rank correlation test performed using data from all campaigns and across vegetation type showed significant positive correlations between emissions of isoprene, MTs, SQTs and chamber temperature and PPFD (Table 1). In contrast, the emissions of ORVOCs showed no correlation with either chamber temperature or PPFD. Vegetation cover in the vegetation types The evergreen C. tetragona was by far the most dominant vascular plant species in the C. tetragona heath. Only four other vascular species, which had covers of 1 % or below, were also registered in the vegetation type (Table 2). The C. tetragona heath had a notable abundance of lichens, which was higher than in the remaining studied communities. S. arctica heath had high abundances of the deciduous S. arctica and V. uliginosum contributing to the large cover of leaf litter ([50 %). V. uliginosum heath also had a high litter abundance, which could here be attributed to the

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Fig. 1 a Mean daytime (9 am to 7 pm), air temperature (2 m above terrain) during August 2009, mean chamber temperature (Chamber T), mean canopy temperature (Canopy T) and b photosynthetic photon flux density (PPFD) (±SE, N = 5–6) during measurements. 10 °C is marked with a dashed horizontal line. Dashed vertical lines separate the five measurement campaigns

dominance of the deciduous V. uliginosum. Both C. tetragona and S. arctica were also present in this vegetation type. Dryas spp. dominated in the mixed heath, followed by K. myosuroides and P. arctica. This was the only vegetation type with complete absence of moss and with sparse vegetation revealing bare soil, which covered about 9 % of the plots. In the PCA performed on the vegetation cover data, all vegetation types had significantly different vegetation cover either on PC1 or on PC2 (explained 24 and 17 % of the variance, respectively; Fig. 4). The vegetation cover in

the C. tetragona heath differed significantly from the one in S. arctica and V. uliginosum heath on both PCs (Fig. 4a). Likewise, the cover in mixed heath was significantly different than the one in V. uliginosum heath (Fig. 4a). BVOC profiles associated with vegetation type PCA was used to describe and distinguish between the four vegetation types based on BVOC emission profiles (Fig. 5). The first PC explained 40 % of the variation in the data and mainly accounted for the variation in MT and SQT

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Polar Biol (2014) 37:237–249 Fig. 3 The mean (±SE; N = 5–6) emissions of a isoprene, b mon-c oterpenes, c sesquiterpenes and d other reactive volatile organic compounds (ORVOCs) from the four vegetation types measured during five campaigns (I–V) in August 2009. Note the different y-axis scales. Different measurement campaigns are indicated by alternately gray and white areas. Vegetation types that do not share letters have significantly different means of emissions within each campaign (Tukey’s test, p \ 0.05). Tendencies shown as:  p \ 0.1

Discussion

Fig. 2 Percentage contribution of isoprene, monoterpenes, sesquiterpenes and other reactive volatile organic compounds (ORVOCs) to total BVOC emissions from C. tetragona, S. arctica, V. uligonosum and mixed heath, respectively. The percentages are calculated from emission rates averaged across the measurement campaigns

emissions. The various MT and SQT emissions were especially associated with C. tetragona heath, which had a significantly different BVOC profile than S. arctica heath and mixed heath on PC1 (Fig. 5a). The V. uliginosum heath was not significantly different from C. tetragona heath with common relatively high importance of MTs and SQTs, or from S. arctica heath, but it differed from the mixed heath on PC2. Emissions of SQTs and the majority of MTs were correlated with each other (Fig. 5b). Due to overlapping scores, the BVOC profiles of the S. arctica and mixed heath appeared similar, despite the differences in isoprene emission between the vegetation types. The isoprene emission variable (compound number 25 in Fig. 5b) is located near the center of the loading plot and is thus of low importance in the model consisting of PC1 and PC2. The similarity between emission profiles of the S. arctica and mixed heaths on PC1 seems to be partially explained by the emissions of the three ORVOCs: 3-methylhexane, 1,2-dimethylcyclopentane and methylcyclohexane (compound numbers 26–28 in Fig. 5b) in these vegetation types, constituting higher percentage of the total emissions than in the remaining two communities (Table S2). The majority of the ORVOCs are separated into two groups, one close to isoprene (compound numbers 21, 22, 25–28 in Fig. 5b) and another with low values on PC2 (compound numbers 18–20, 23 in Fig. 5b), the latter being more characteristic for the emissions from mixed heath. The MT 3-carene (compound number 24 in Fig. 5b) is the only MT important for mixed heath emissions (Fig. 5b; Table S2).

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BVOC emission profiles vary widely between plant species and vegetation types (Kesselmeier and Staudt 1999). Studies conducted in the subarctic have also shown BVOC emission rates and profiles to differ according to vegetation type (Ba¨ckstrand et al. 2008; Faubert et al. 2012). In agreement with this, the studied high arctic vegetation types also had contrasting BVOC profiles, reflecting the differences in vegetation cover. The emission profiles for S. arctica and C. tetragona heath were especially distinct from each other, which owed to the significantly different vegetation covers. Salix arctica heath was the only vegetation type with significant isoprene emission, which is not surprising as Salix spp. are known to be significant isoprene emitters (Hakola et al. 1998; Klinger et al. 2002; Rinne et al. 2009; Rinnan et al. 2011; Fineschi et al. 2013). Salix spp. are commonly found in Greenland dominated by S. glauca in the south and S. arctica in the north (Bo¨cher et al. 1968). S. arctica is circumpolar distributed and widespread in the present study area (Bo¨cher et al. 1968; Bay 1998; Elberling et al. 2008). However, isoprene emission from this high arctic heath was clearly lower than the emission rates observed previously in subarctic ecosystems with denser vegetation and higher ambient temperature (Tiiva et al. 2007; Tiiva et al. 2008; Holst et al. 2010). Tiiva et al. (2008) measured mean growing season isoprene emission between 33 and 46 lg m-2 h-1 from a subarctic heath, which is two to three times higher than the mean rates measured here in this S. arctica heath. Likewise, the estimated emission potential for isoprene at 1,000 lmol m-2 s-1 PPFD and 30 °C was one order of magnitude higher in the study by Tiiva et al. (2008) than calculated here. Of the four vegetation types, S. arctica heath emitted the lowest amounts of MTs (12 % of total) and no SQTs above detection limit, which is in accordance with the findings showing low emissions of MTs and SQTs from S. phylicifolia (Hakola et al. 1998; Rinnan et al. 2011). The well-known protecting role of isoprene against abiotic stress, and especially heat stress (Vickers et al. 2009; reviewed by Possell and Loreto 2013), is thought to be mediated through stabilization of the thylakoid membranes in the chloroplasts, scavenging of reactive oxygen species (reviewed by Loreto and Schnitzler 2010; Possell and Loreto 2013) or reduction in the production of reactive oxygen and nitrogen species (Velikova et al. 2012). The trait for isoprene emission has been frequently lost and gained during the

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evolution of plants, and it has thus been suggested that the trait is only advantageous in a narrow range of conditions, e.g., in warm environments (Sharkey et al. 2008; Fineschi et al. 2013; Monson 2013). Fineschi et al. (2013) stated that only 17–22 % of plant species in cold ecosystems emit isoprene (rates of [1 lg g-1 h-1), which is less than the worldwide average of 29 %. The low ecosystem scale emission rates observed in the four vegetation types studied here support this general view. Of the studied high arctic vegetation types, C. tetragona heath had the highest total BVOC emission rate. C. tetragona heath was associated with emissions of several

Table 1 Spearman correlation coefficients between the emissions of various groups of BVOCs and photosynthetic photon flux density (PPFD) as well as chamber temperature (T) PPFD

T

Isoprene

0.57**

0.49**

Total monoterpenes

0.47**

0.59**

Total sesquiterpenes Total ORVOCs

0.42** 0.08

0.61** 0.11

Total BVOCs

0.38**

0.45**

Correlation tests were performed across vegetation types (N = 83). Significant correlations are shown in bold ** p \ 0.01

MTs and SQTs, representing more than 50 % of the total emissions, which is in consistency with earlier results suggesting C. tetragona to be a significant MT and SQT emitter (Rinnan et al. 2011). The total BVOC emissions in V. uliginosum heath were 47–72 % lower than in the other heath types, but the emissions of MTs and SQTs were only lower than from the C. tetragona heath. The emissions were comprised of 50 % MTs, 16 % SQTs and 4 % isoprene, which was in agreement with other studies finding Vaccinium spp. to be MT rather than SQT and isoprene emitters (Aaltonen et al. 2011; Faubert et al. 2012). Despite a lower vegetation cover in the mixed heath relative to the remaining vegetation types, the total BVOC emissions were not correspondingly lower. Most of the emissions owed to ORVOCs, non-isoprenoid hydrocarbons and aromatic compounds. The high proportion of ORVOCs of the total emission is likely to be associated with the presence of bare soil, since soil, litter and microorganisms are responsible for emissions of several non-isoprenoid BVOCs that belong to ORVOCs (Leff and Fierer 2008; Insam and Seewald 2010). As the only group of BVOCs, emissions of ORVOCs were not found to correlate with either PPFD or chamber temperature. This observation further supports our suggestion that the measured ORVOCs are not emitted by plants, since plant emissions of these types of compounds would be expected to show light and temperature dependency (see Jardine et al. 2010), and

Table 2 Mean percentage cover (±SE, N = 5–6) of vascular plants, organic crust, lichens, mosses, litter and bare soil in the four vegetation types in August 2009 C. tetragona heath

S. arctica heath

Cassiope tetragona (green)

28.6 ± 2.3a

0.0 ± 0.0c

Cassiope tetragona (brown)

9.3 ± 4.3a

0.0 ± 0.0b

Cassiope tetragona (gray) Salix arctica

V. uliginosum heath 12.1 ± 3.3b 2.9 ± 1.1ab

Mixed heath

Statistical significance

0.0 ± 0.0c

**

0.0 ± 0.0b

*

67.5 ± 6.0a

0.0 ± 0.0c

13.2 ± 3.4b

0.0 ± 0.0c

**

0.7 ± 0.4b

19.3 ± 5.0a

5.0 ± 4.6b

2.4 ± 2.4b

**

Luzula confusa

1.1 ± 0.4

5.4 ± 3.1

1.1 ± 1.1

0.0 ± 0.0

Vaccinium uliginosum Dryas ssp.

0.0 ± 0.0 0.0 ± 0.0

14.3 ± 9.2 9.3 ± 5.7

17.9 ± 7.1 3.9 ± 2.4

0.0 ± 0.0 15.5 ± 5.5

Arctagrostis latifolia

0.0 ± 0.0b

0.0 ± 0.0b

4.6 ± 1.6a

0.0 ± 0.0b

Polygonum viviparum

0.7 ± 0.4

0.0 ± 0.0

1.8 ± 1.4

0.0 ± 0.0 11.9 ± 6.8

Kobresia myosuroides

0.0 ± 0.0

0.0 ± 0.0

0.0 ± 0.0

Carex rupestris

0.0 ± 0.0b

0.0 ± 0.0b

0.0 ± 0.0b

6.7 ± 2.6a 11.1 ± 10.6

  **   **

Poa arctica

0.4 ± 0.4

1.4 ± 1.0

0.7 ± 0.4

Organic crust

1.1 ± 0.7

1.4 ± 1.0

0.0 ± 0.0

2.0 ± 1.6

Lichens

15.4 ± 3.6a

4.3 ± 2.0b

8.9 ± 2.5ab

1.2 ± 0.8b

**

Moss

11.1 ± 4.2ab

16.4 ± 5.7a

22.1 ± 3.5a

0.0 ± 0.0b

**

Litter

8.2 ± 1.5b

55.0 ± 8.2a

45.4 ± 4.2a

19.4 ± 6.8b

**

Soil

0.0 ± 0.0

0.0 ± 0.0

0.0 ± 0.0

8.7 ± 6.9

Vegetation types that do not share letters have significantly different cover of the corresponding species or category (Tukey’s test, p \ 0.05)   p \ 0.1; * p \ 0.05; ** p \ 0.01

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Fig. 4 Principal component analysis on the vegetation cover in the four vegetation types. a The mean scores (±SE; N = 5–6) of the principal components (PC1 and PC2) and b the corresponding loading variables. The variance explained by each PC is shown in parenthesis.

Vegetation types that do not share letters have significant differences between means along the respective PC (Tukey’s test, p \ 0.05). Note that a rotated solution is presented

Fig. 5 Principal component analysis on the BVOC emissions from the four vegetation types. a The mean scores (±SE; N = 15–25) of the principal components (PC1 and PC2) for all campaigns and b the corresponding loading variables. The variance explained by each PC is shown in parenthesis. Vegetation types that do not share letters have significant differences between means along the respective PC (Tukey’s test, p \ 0.05). Compound names: 1 1,8-cineole, 2 a-selinene, 3 c-

eudesmol, 4 1 s-cis-calamenene, 5 copaene, 6 cadinene, 7 camphene, 8 sabinene, 9 7,7-dimethyl-2-methylene-bicyclo(2,2,1)heptanes, 10 limonene, 11 4-cymene, 12 o-cymene, 13 a-muurolene, 14 (-)-pin2(3)ene, 15 a-pinene, 16 c-terpinene, 17 aromadendrene, 18 1-octene, 19 2-heptene, 20 4-xylene, 21 n-ethyl-1,3-dithioisoindoline, 22 4-methylnonane, 23 ethylbenzene, 24 3-carene, 25 isoprene 26 3-methylhexane, 27 1,2-dimethylcyclopentane, 28 methylcyclohexane

because soil emissions are driven more by, e.g., microbial composition and biomass, nutrient availability and other soil characteristics (Leff and Fierer 2008). Further studies are needed to assess the importance of soil emissions in the arctic, especially considering permafrost thaw. In consistency with Faubert et al. (2012), who found no SQT emissions from bare soil plots in subarctic Sweden, virtually no SQT emissions were detected in this vegetation type. Mixed heath emitted 3-carene, which is a normal MT emitted from vegetation (e.g., Faubert et al. 2010b; Faubert et al. 2012). While Faubert et al. (2010b) found emission of 3-carene from vegetation, this compound has also been found in the soil atmosphere under spruce and pine in northern Finland (Smolander et al. 2006).

Both mean MT and SQT emission rates were comparable to the rates measured in the subarctic (Faubert et al. 2010a; Faubert et al. 2012). Despite lower temperature during the present measurements, the total mean BVOC emissions were of the same order of magnitude as found in subarctic forest floor (Faubert et al. 2012) and in subarctic wet heath, which had mean growing season total BVOC emissions of 44–61 lg m-2 h-1 (calculated from Tiiva et al. 2008 and Faubert et al. 2010a). Based on preliminary data on atmospheric BVOC concentration in low arctic Greenland (T. Holst, personal communication), it similarly seems that concentrations might be of the same magnitude as measured in the subarctic (Holst et al. 2010). Differences in factors such as nutrient availability, substrate

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quality, soil temperature, pH, moisture content and microbial community composition influence the amount and profile of BVOCs produced (Insam and Seewald 2010). In this context, the presence of continuous permafrost in the high arctic might conceivably play a role in, e.g., the quality of available substrate in the thawed active layer during the summer. Also, even though litter might only emit BVOCs at low rates, litter forms a considerable part of the aboveground carbon mass in high arctic ecosystems, and varying litter layer could have an effect, as litter has been shown to emit a great diversity of BVOCs (Leff and Fierer 2008). The relative amount of plant biomass is low compared with the carbon pool in soil and litter in the high arctic, and the studied high arctic vegetation types have lower plant biomass relative to the litter biomass than, e.g., subarctic ecosystems. It has been observed that plant species predominantly or entirely emit either isoprene or MTs. This was illustrated by Harrison et al. (2013) based on emissions from 192 plant species. In the present study, we demonstrated a similar inverse relationship between the emissions of isoprene and MTs, which was mostly driven by emissions from S. arctica and C. tetragona heath. While isoprene is known for its protective role (reviewed by Possell and Loreto 2013), MTs are known for a variety of functions including herbivore deterrence (Blande et al. 2007; Dicke and Baldwin 2010). However, MTs might also be induced by stress in the same way as isoprene (Brilli et al. 2009), and volatile isoprenoids might in general be important in the protection against oxidative stress (Vickers et al. 2009; Loreto and Schnitzler 2010). The inverse relationship between the emissions might reflect a competition between isoprene and MT biosynthesis for common precursors and reducing power (Harrison et al. 2013), and as stated by Brilli et al. (2009), the carbon might be shifted from isoprene to other volatiles needed for plant defense. In the present study, the trade-off between isoprene and MT emissions is not as evident as shown by Harrison et al. (2013), as the emissions were measured on an ecosystem scale with several plant species occurring within a plot. In the present study, the BVOC emissions were highest in the beginning of August as a likely result of higher air temperature and incoming PPFD than during the following campaigns. From mid-August onward, the chamber temperatures approached 10 °C and the PPFD values remained below 600 lmol m-2 s-1, and concomitantly, the BVOC emissions decreased to a very low level. Significant positive correlations between PPFD and chamber temperature, respectively, and emissions of isoprene, total MTs and SQTs were additionally observed, which corroborates the well-known importance of temperature and light regarding plant BVOC emissions (see review by Grote et al. 2013; Li and Sharkey 2013).

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There is evidence that the temperature of a preceding time period can influence the emission rate of isoprene (Ekberg et al. 2009; Ekberg et al. 2011; Potosnak et al. 2013). In the present study, the mean daytime air temperature varied between 5 and 10 °C until the fourth measurement campaign, which was preceded by a day with mean daytime temperature of 10.5 °C. This warmest day during the measurement period was, however, not reflected in the emission rates in the following measurement campaign. By the end of August, the senescence of the vegetation had advanced far, and the generally low emissions of BVOCs in the measurement campaign IV and V might rather be caused by senescence (Ellebjerg et al. 2008) than by abiotic conditions. As S. arctica in the study area already showed signs of senescence in August (Ellebjerg et al. 2008), higher isoprene emission may have occurred earlier in the growing season and prior to our measurement period. Due to the strong temperature dependency of isoprene emission (Guenther et al. 1993; Sharkey and Loreto 1993; Hakola et al. 1998; Kesselmeier and Staudt 1999; Sharkey et al. 2008; Tiiva et al. 2008), the highest emissions could also be expected in July when the temperature is peaking (Hansen et al. 2008). Furthermore, high emissions might coincide with high PPFD in June and July (Sigsgaard et al. 2010) as isoprene formation is closely related to photosynthesis (Sharkey and Loreto 1993; Sanadze 2004) and thus to PPFD (Hakola et al. 1998). Vegetation growing in warmer environments has been observed to respond differently to temperature than vegetation in colder environments and has a higher temperature optimum for emissions (see, e.g., Geron et al. 2006). Fares et al. (2011) found acclimation of isoprene emission to growth temperature in hybrid poplars, and likewise, emissions from vegetation in the high arctic could be acclimated to lower temperatures. However, the arctic heath vegetation might experience temperatures considerably higher than the air temperature typically measured 2 m above terrain. On bright days, Scherrer and Ko¨rner (2009) found surface temperatures at alpine and arctic alpine slopes to be 2–9 °C higher than air temperatures. And likewise, Svoboda (2009) stated that the near-ground temperature of tundra vegetation can be remarkably higher (reaching up to *30 °C) than the air temperature. In consistency with this, we found canopy temperatures in the low-stature high arctic vegetation to be *4–14 °C higher than air temperatures. High arctic plants may therefore be exposed to higher temperatures than may be anticipated from their high latitudinal position, and near-ground summer temperatures in the high arctic might be surprisingly similar to temperatures found at lower latitudes. Day length at high latitudes could furthermore affect integrated BVOC emissions. The potential effect of nocturnal emissions during the summer solstice with 24 h of sunlight cannot be

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ignored, and further research is needed to assess the impact of these emissions.

emissions and implications for biological interactions and atmospheric chemistry.

Implications

Acknowledgments This work was funded by The Danish Council for Independent Research | Natural Sciences and the Villum Foundation. We are grateful to the Zackenberg Research Station for provision of meteorological data and logistic support. Also thanks to the Danish National Research Foundation for supporting activities (DNRF100) within the Center for Permafrost (CENPERM), University of Copenhagen.

Emissions from boreal, subarctic and high arctic environments might only constitute a minor source of BVOCs globally (Guenther et al. 1995; Ba¨ckstrand et al. 2008). However, the predicted pronounced climate warming at high latitudes (ACIA 2005) is expected to increase the BVOC emissions in the future (e.g., Lathie`re et al. 2005). Studies conducted in the subarctic have already shown experimental warming to directly increase the emission of BVOCs (Tiiva et al. 2008; Faubert et al. 2010a). Additionally, vegetation in the subarctic seems to be more temperature sensitive than vegetation growing at lower latitudes (Holst et al. 2010). Accordingly, Faubert et al. (2010a) observed a greater temperature sensitivity of MT and SQT emissions than expected based on commonly used temperature dependence models. Thus, these results lend further evidence on the suggestion by Holst et al. (2010) that low emissions at high latitudes are mostly due to low temperature rather than to low emission potentials of the prevalent vegetation. Other factors such as altered plant biomass, species composition and increased length of the growing season are likely to additionally affect BVOC emissions. Experimental warming has several times been shown to result in increases in the height and cover of graminoids and shrubs in the arctic (Walker et al. 2006; Elmendorf et al. 2012). An increase in woody species dominance in a warmer climate could alter the emission of especially isoprene from tundra vegetation. However, the responses in high arctic were not reported to be as pronounced as at lower latitudes, and responses by shrubs here could only be transitional. Nevertheless, Schmidt et al. (2012) found substantial changes in vegetation cover in the Zackenberg Valley differing for plant functional types and plant communities. Changes in vegetation composition and cover will inevitably lead to changes in the composition of BVOC emissions and possibly also to higher emissions. Also, the amount of litter appears to increase with warming (Walker et al. 2006; Elmendorf et al. 2012; Schmidt et al. 2012), and it has correspondingly the potential to alter BVOC emissions (see Leff and Fierer 2008). The estimates of high arctic BVOC emissions, which are presented in this study, propose that even these cold and vegetation-poor environments are sources of various BVOCs when ambient air temperature near the ground is above 10 °C. Moreover, emissions may be comparable in magnitude to emissions in the subarctic. We suggest that further studies should be conducted to investigate the effects of climate changes in the region in order to gain new knowledge and understanding of future global BVOC

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Polar Biol (2014) 37:237–249 Lathie`re J, Hauglustaine DA, De Noblet-Ducoudre´ N, Krinner G, Folberth GA (2005) Past and future changes in biogenic volatile organic compound emissions simulated with a global dynamic vegetation model. Geophys Res Lett 32:L20818 Leff JW, Fierer N (2008) Volatile organic compound (VOC) emissions from soil and litter samples. Soil Biol Biochem 40(7):1629–1636. doi:10.1016/j.soilbio.2008.01.018 Li Z, Sharkey TD (2013) Molecular and pathway controls on biogenic ¨ , Monson volatile organic compound emissions. In: Niinemets U RK (eds) Biology, controls and models of tree volatile organic compound emissions, Tree Physiology 5. Springer, Berlin, pp 119–150 Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15(3):154–166 Meltofte H, Rasch M (2008) The study area at Zackenberg. In: Meltofte H, Christensen TR, Elberling B, Forchhammer MC, Rasch M (eds) High-Arctic ecosystem dynamics in a changing climate—ten years of monitoring and research at Zackenberg Research Station, Northeast Greenland, vol 40., Advances in ecological researchAcademic Press, London, pp 101–110 Meltofte H, Thing H (eds) (1996) Zackenberg ecological research operations, 1st Annual Report, 1995. Danish Polar Center, Ministry of Research and Technology, Copenhagen Monson RK (2013) Metabolic and gene expression controls on the production of biogenic volatile organic compounds. In: Niine¨ , Monson RK (eds) Biology, controls and models of tree mets U volatile organic compound emissions, Tree Physiology 5. Springer, Berlin, pp 153–180 Ortega J, Helmig D (2008) Approaches for quantifying reactive and low-volatility biogenic organic compound emissions by vegetation enclosure techniques—part A. Chemosphere 72(3):343–364 Pen˜uelas J, Llusia` J (2001) The complexity of factors driving volatile organic compound emissions by plants. Biol Plantarum 44(4):481–487 Possell M, Loreto F (2013) The role of volatile organic compounds in plant resistance to abiotic stresses: Responses and mechanisms. ¨ , Monson RK (eds) Biology, controls and models In: Niinemets U of tree volatile organic compound emissions, Tree Physiology 5. Springer, Berlin, pp 209–235 Potosnak MJ, Baker BM, LeStourgeon L, Disher SM, Griffin KL, Bret-Harte MS, Starr G (2013) Isoprene emissions from a tundra ecosystem. Biogeosciences 10(2):871–889. doi:10.5194/bg-10871-2013 Rinnan R, Rinnan A, Faubert P, Tiiva P, Holopainen JK, Michelsen A (2011) Few long-term effects of simulated climate change on volatile organic compound emissions and leaf chemistry of three subarctic dwarf shrubs. Environ Exp Bot 72(3):377–386. doi:10. 1016/j.envexpbot.2010.11.006 Rinnan R, Gierth D, Bilde M, Rosenørn T, Michelsen A (2013) Offseason biogenic volatile organic compound emissions from heath mesocosms: responses to vegetation cutting. Front Microbiol 4:224. doi:10.3389/fmicb.2013.00224 Rinne J, Ba¨ck J, Hakola H (2009) Biogenic volatile organic compound emissions from the Eurasian taiga: current knowledge and future directions. Boreal Environ Res 14(4):807–826 Sanadze GA (2004) Biogenic isoprene (a review). Russ J Plant Physiol 51(6):729–741 Scherrer D, Ko¨rner C (2009) Infra-red thermometry of alpine landscapes challenges climatic warming projections. Glob Change Biol. doi:10.1111/j.1365-2486.2009.02122.x

249 Schmidt NM, Kristensen DK, Michelsen A, Bay C (2012) High arctic plant community responses to a decade of ambient warming. Biodiversity 13(3–4):191–199 Sharkey T, Loreto F (1993) Water stress, temperature, and light effects on the capacity for isoprene emission and photosynthesis of kudzu leaves. Oecologia 95(3):328–333. doi:10.1007/ BF00320984 Sharkey TD, Wiberley AE, Donohue AR (2008) Isoprene emission from plants: why and how. Ann Bot-London 101:5–18. doi:10. 1093/aob/mcm240 Sigsgaard C, Thorsøe K, Lund M, Kandrup N, Larsen M, Falk JM, Hansen BU, Stro¨m L, Christensen TR, Tamstorf MP (2010) Zackenberg basic. The ClimateBasis and GeoBasis programmes. In: Jensen LM, Rasch M (eds) Zackenberg ecological research operations, 15th annual report, 2009. National Environmental Research Institute, Aarhus University, Denmark, pp 12–35 Smolander A, Ketola RA, Kotiaho T, Kanerva S, Suominen K, Kitunen V (2006) Volatile monoterpenes in soil atmosphere under birch and conifers: effects on soil N transformations. Soil Biol Biochem 38:3436–3442 Staudt M, Bertin N, Frenzel B, Seufert G (2000) Seasonal variation in amount and composition of monoterpenes emitted by young pinus pinea trees—implications for emission modeling. J Atmos Chem 35(1):77–99. doi:10.1023/A:1006233010748 Svoboda J (2009) Evolution of plant cold hardiness and its manifestation along the latitudinal gradient in the Canadian arctic. In: Gusta L, Wisniewski M, Tanino K (eds) Plant cold hardiness: from the laboratory to the field. CABI, Cambridge, MA, pp 140–162 Tiiva P, Rinnan R, Faubert P, Rasanen J, Holopainen T, Kyro E, Holopainen JK (2007) Isoprene emission from a subarctic peatland under enhanced UV-B radiation. New Phytol 176:346–355. doi:10.1111/j.1469-8137.2007.02164.x Tiiva P, Faubert P, Michelsen A, Holopainen T, Holopainen JK, Rinnan R (2008) Climatic warming increases isoprene emission from a subarctic heath. New Phytol 180(4):853–863. doi:10. 1111/j.1469-8137.2008.02587.x Velikova V, Sharkey TD, Loreto F (2012) Stabilization of thylakoid membranes in isoprene-emitting plants reduces formation of reactive oxygen species. Plant Signal Behav 7(1):139–141. doi:10.4161/psb.7.1.18521 Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5(5):283–291 Walker DA, Raynolds MK, Danie¨ls FJA, Einarsson E, Elvebakk A, Gould WA, Katenin AE, Kholod SS, Markon CJ, Melnikov ES, Moskalenko NG, Talbot SS, Yurtsev BA, Members of the CAVM team (2005) The circumpolar arctic vegetation map. J Veg Sci 16:267–282 Walker MD, Wahren CH, Hollister RD, Henry GHR, Ahlquist LE, Alatalo JM, Bret-Harte MS, Calef MP, Callaghan TV, Carroll AB, Epstein HE, Jo´nsdo´ttir IS, Klein JA, Magnu´sson B, Molau U, Oberbauer SF, Rewa SP, Robinson CH, Shaver GR, Suding KN, Thompson CC, Tolvanen A, Totland Ø, Lee Turner P, Tweedie CE, Webber PJ, Wookey PA (2006) Plant community responses to experimental warming across the tundra biome. PNAS 103(5):1342–1346

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Electronic supplementary information Biogenic volatile organic compound emissions in four vegetation types in high arctic Greenland

In Polar Biology

Michelle Schollert*, Sebrina Burchard, Patrick Faubert, Anders Michelsen, Riikka Rinnan

*Corresponding author: Michelle Schollert, Terrestrial Ecology Section, Department of Biology, University of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark and Center for Permafrost (CENPERM), Department of Geography and Geology, University of Copenhagen, Øster Voldgade 10, DK-1350 Copenhagen K Denmark. E-mail: [email protected]

Fig. S1 Total monoterpene emission against isoprene emission across measurement campaign and vegetation type, i.e. using all 83 data points

Table S1 Standardized emissions of isoprene, monoterpenes and sesquiterpenes (µg m-2 h-1, N = 15-25) from C. tetragona, S. arctica, V. uligonosum and mixed heath, respectively, averaged across the five measurement campaigns. Emissions were standardized by using the algorithms presented by Guenther et al. (1993). Isoprene emissions were standardized to a PPFD of 1000 µmol m-2 s-1 and temperature of 20°C and 30°C. Monoterpene and sesquiterpene emissions were standardized to 20°C and 30°C. A β coefficient of 0.09°C-1 was used for monoterpenes (Guenther et al. 1993) and 0.18°C-1 for sesquiterpenes (Hakola et al. 2001; Helmig et al. 2007). Vegetation types that do not share letters have significantly different means of standardized emissions of isoprene, monoterpenes and sesquiterpenes, respectively (Tukey’s test, p < 0.05)

Level of significance

C. tetragona heath

S. arctica heath

V. uliginosum heath

Mixed heath

mean ± SE

mean ± SE

mean ± SE

mean ± SE

20°C Isoprene

1.63 ± 0.87b

10.72 ± 2.61a

0.66 ± 0.48b

2.64 ± 1.46b

**

Total monoterpenes

27.33 ± 5.99a

5.41 ± 1.22b

12.58 ± 3.4ab

9.18 ± 3.29b

**

Total sesquiterpenes

9.71 ± 3.22a

0 ± 0b

4.22 ± 1.46ab

0.32 ± 0.32b

**

30°C Isoprene

5.91 ± 3.16b

38.8 ± 9.45a

2.4 ± 1.72b

9.56 ± 5.28b

**

Total monoterpenes

67.22 ± 14.73a

13.3 ± 3b

30.95 ± 8.37ab

22.59 ± 8.08b

**

Total sesquiterpenes **, p < 0.01

58.73 ± 19.46a

0 ± 0b

25.5 ± 8.81ab

1.94 ± 1.94b

**

Table S2 Biogenic volatile organic compound emissions (µg m-2 h-1, N = 15-25) from C. tetragona, S. arctica, V. uligonosum and mixed heath, respectively, averaged across the five measurement campaigns

C. tetragona heath

S. arctica heath

V. uliginosum heath

Mixed heath

mean ± SE

mean ± SE

mean ± SE

mean ± SE

Isoprene (-)-Pin-2(3)-ene

1.56 ± 0.93 1.70 ± 1.03

7.91 ± 2.13 0.08 ± 0.05

0.76 ± 0.57 0.41 ± 0.34

1.63 ± 0.93 nd ± nd

α-Pinene 7,7-Dimethyl-2methylenebicyclo(2.2.1)heptane

4.73 ± 1.46

0.76 ± 0.32

2.79 ± 1.31

0.66 ± 0.25

0.36 ± 0.17

nd ± nd

0.04 ± 0.03

nd ± nd

Camphene

1.48 ± 0.45

nd ± nd

0.93 ± 0.49

0.18 ± 0.10

Sabinene

3.87 ± 1.32

0.22 ± 0.12

1.05 ± 0.54

nd ± nd

3-Carene

0.18 ± 0.09

0.78 ± 0.19

0.17 ± 0.12

1.39 ± 0.91

Limonene

6.00 ± 2.00

1.56 ± 1.02

2.88 ± 1.00

2.71 ± 0.98

1,8-Cineole

3.88 ± 1.15

0.07 ± 0.04

1.56 ± 0.66

nd ± nd

γ-Terpinene

2.22 ± 0.82

nd ± nd

0.63 ± 0.36

0.05 ± 0.05

Total monoterpenes Copaene

24.41 ± 6.52 1.46 ± 0.64

3.47 ± 1.06 nd ± nd

10.46 ± 3.83 0.70 ± 0.23

4.99 ± 1.89 0.05 ± 0.05

α-Muurolene

0.57 ± 0.32

nd ± nd

0.39 ± 0.19

nd ± nd

α-Selinene

1.54 ± 0.57

nd ± nd

0.49 ± 0.17

nd ± nd

Cadinene

1.33 ± 0.61

nd ± nd

0.64 ± 0.25

0.07 ± 0.07

1s-Cis-Calamenene

0.70 ± 0.41

nd ± nd

0.16 ± 0.08

nd ± nd

Aromadendrene

0.59 ± 0.32

nd ± nd

0.09 ± 0.05

nd ± nd

γ-Eudesmol

3.18 ± 1.39

nd ± nd

0.83 ± 0.48

nd ± nd

Total sesquiterpenes 3-Methylhexane

9.38 ± 4.20 3.07 ± 2.19

nd ± nd 3.95 ± 1.73

3.30 ± 1.33 0.87 ± 0.43

0.12 ± 0.12 5.65 ± 4.01

1,2-Dimethylcyclopentane

0.81 ± 0.53

1.20 ± 0.65

0.16 ± 0.11

2.86 ± 2.35

2-Heptene

3.56 ± 1.37

4.59 ± 1.13

1.07 ± 0.78

3.61 ± 1.43

Methylcyclohexane

5.41 ± 2.44

3.06 ± 1.57

0.71 ± 0.25

6.81 ± 4.81

1-Octene

1.58 ± 0.81

0.67 ± 0.25

nd ± nd

1.16 ± 0.53

n-Ethyl-1,3-Dithioisoindoline

0.11 ± 0.07

0.1 ± 0.07

0.08 ± 0.08

0.04 ± 0.04

4-Methylnonane

0.30 ± 0.23

1.31 ± 1.02

0.92 ± 0.51

0.41 ± 0.31

ethyl benzene

0.27 ± 0.27

0.33 ± 0.24

0.28 ± 0.28

2.22 ± 0.97

4-Xylene

1.41 ± 0.68

1.70 ± 0.89

0.87 ± 0.49

3.24 ± 1.99

4-Cymene

7.19 ± 4.57

nd ± nd

1.53 ± 1.28

nd ± nd

o-Cymene

5.07 ± 3.35

nd ± nd

nd ± nd

3.05 ± 2.12

Total ORVOCs

28.78 ± 8.39

16.9 ± 4.69

6.47 ± 2.66

29.06 ± 12.34

64.14 ± 18.00

28.29 ± 5.59

21 ± 7.88

35.8 ± 13.12

Total BVOCs nd: not detected

References Guenther AB, Zimmerman PR, Harley PC, Monson RK, Fall R (1993) Isoprene and monoterpene emission rate variability: model evaluations and sensitivity analyses. J Geophys Res 98:12609-12617. doi:10.1029/93JD00527 Hakola H, Laurila T, Lindfors V, Hellen H, Gaman A, Rinne J (2001) Variation of the VOC emission rates of birch species during the growing season. Boreal Environ Res 6:237-249 Helmig D, Ortega J, Duhl T, Tanner D, Guenther A, Harley P, Wiedinmyer C, Milford J, Sakulyanontvittaya T (2007) Sesquiterpene emissions from pine trees - Identifications, emission rates and flux estimates for the contiguous United States. Environ Sci Technol 41 (5):1545-1553. doi:10.1021/es0618907

3 Volatile organic compound emission profiles of four common arctic plants Vedel-Petersen I, Schollert M, Nymand J and Rinnan R. Submitted to Atmospheric Environment

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1

Volatile organic compound emission profiles of four common arctic plants Ida Vedel-Petersena, Michelle Schollerta, b, Josephine Nymandc, Riikka Rinnana, b*

a

Terrestrial Ecology Section, Department of Biology, University of Copenhagen,

Universitetsparken 15, 2100 Copenhagen E, Denmark b

Center for Permafrost (CENPERM), Department of Geoscience and Natural Resource

Management, University of Copenhagen, Øster Voldgade 10, 1350 Copenhagen K, Denmark c

Pinngortitaleriffik - Greenland Institute of Natural Resources, Kivioq 2, Postboks 570, 3900

Nuuk, Greenland

E-mail addresses: [email protected] (R. Rinnan), [email protected] (I. VedelPetersen), [email protected] (M. Schollert), [email protected] (J. Nymand).

*Corresponding author: Tel.: +45 51827039, [email protected] (R. Rinnan), Address: Terrestrial Ecology Section, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen E, Denmark

2

Abstract The biogenic volatile organic compound (BVOC) emissions from plants impact atmosphere and climate. The species-specific emissions, and thereby the atmospheric impact, of many plant species are still unknown. Knowledge of BVOC emission from arctic plants is particularly limited. The vast area and relatively high leaf temperature give the Arctic potential for emissions that cannot be neglected. This field study aimed to elucidate the BVOC emission profiles for four common arctic plant species in their natural environment during the growing season. BVOCs were sampled from aboveground parts of Empetrum hermaphroditum, Salix glauca, Salix arctophila and Betula nana using the dynamic enclosure technique and collection of volatiles in adsorbent cartridges, analyzed by gas chromatography-mass spectrometry. Sampling occurred three times: in late June/early July, in mid-July and in early August. E. hermaphroditum emitted the least BVOCs, dominated by sesquiterpenes (SQTs) and non-isoprenoid BVOCs. The Salix spp. emitted the most, dominated by isoprene. The emissions of B. nana were composed of about two-thirds nonisoprenoid BVOCs, with moderate amounts of monoterpenes (MTs) and SQTs. The total B. nana emissions and the MT and SQT emission potentials were highest in the first measurement in early July, while the other species had the highest emissions in the last measurement in early August. As climate change is expected to increase plant biomass and change vegetation composition in the Arctic, the BVOC emissions from arctic ecosystems will also change. Our results suggest that if the abundance of deciduous shrubs like Betula and Salix spp. increases at the expense of slower growing evergreens like E. hermaphroditum, there is the potential for increased emissions of isoprene, MTs and non-isoprenoid BVOCs in the Arctic.

Keywords: BVOC, isoprene, monoterpene, sesquiterpene, Betula nana, Empetrum hermaphroditum, Salix

3

1. Introduction Vegetation impacts the atmosphere by emitting biogenic volatile organic compounds (BVOCs). The global BVOC emissions from the terrestrial biosphere to the atmosphere are, with large uncertainties, estimated to be between 700-1000 ×1012 g C per year (Laothawornkitkul et al., 2009). Many BVOCs are highly reactive and their chemical degradation processes influence air quality and climate (Laothawornkitkul et al., 2009), contributing to complex climate feedback mechanisms in the atmosphere associated with global climate change (Peñuelas & Staudt, 2010). Information on BVOC emissions in all regions is needed to improve the understanding of global BVOC emissions (Guenther et al., 1995). Emissions from the Arctic have been considered negligible because of low temperatures, short summers and low vegetation biomass (Guenther et al., 1995). BVOC emissions are highly temperature dependent, often showing an exponential relationship with increasing temperature (Laothawornkitkul et al., 2009). Low-statured vegetation canopies in high latitude ecosystems have been observed to have canopy temperatures up to 15°C warmer than the ambient air temperature (Helliker & Richter, 2008; Scherrer & Körner, 2009; Rinnan et al., 2014). Due to the temperature dependence of BVOC emissions, arctic plants might therefore be of greater importance than previously expected despite the low air temperatures. Indeed, the Arctic is vast, and the first ecosystem-level measurements suggest significant emissions from this poorly studied region (Potosnak et al., 2013; Schollert et al., 2013). BVOCs play key roles in plant reproduction and in protection against abiotic and biotic stressors (Laothawornkitkul et al., 2009). The emissions are thus important for plant survival and are regulated in interaction with the surrounding environment (Laothawornkitkul et al., 2009). The quality and the quantity of BVOC emissions (i.e. the BVOC emission profiles) are species-specific, and depend on plant phenology and environmental factors, most importantly temperature and photosynthetically active radiation (PAR) (Laothawornkitkul et al., 2009; Niinemets et al., 2010; Llusia et al., 2013). As a result of rapidly changing climate in the Arctic (IPCC, 2013), arctic shrubs are increasing in abundance (Tape et al., 2006; Elmendorf et al., 2012; Walker et al., 2014). Since emission profiles of plants are species-specific, the proportion of different BVOCs emitted from the vegetation depends on the species composition. Therefore a change in vegetation

4 composition and shrub abundance is likely to alter the BVOC emissions profile of the arctic region (Rinnan et al., 2014). Our aim was to obtain an estimate of the emission rates and profiles of common arctic shrub species Betula nana, Empetrum hermaphroditum, Salix arctophila and Salix glauca in situ in low arctic Greenland. Further, we aimed to investigate changes in emission profiles during the growing season. B. nana (dwarf birch) is a common circumboreal-polar shrub in the Northern Hemisphere, and it can be dominant on both dry and wet tundra (Bliss & Matveyeva, 1992; Elven, 2014). E. hermaphroditum (black crowberry) is a common circumboreal-polar dwarf shrub in the Northern Hemisphere and also occurs in the Southern Hemisphere (Anderberg, 1994; Tybirk & Nilsson, 2000; Popp et al., 2011). S. arctophila (arctic marsh willow) is a common dwarf shrub found on mires and along streams in Canada, Alaska, and Greenland (Elven, 2014). S. glauca (greyleaf willow) is a common circumboreal-polar shrub species (Böcher et al., 1968; Elven, 2014).

2. Materials and methods 2.1. Study area The field study was conducted from late June to early August 2013 in the bottom of Kobbefjord (Kangerluarssunguaq), South Western Greenland (64°07’N, 51°21’W). The climate is characterized as low arctic with a mean annual precipitation of 752 mm (19611990) (Aastrup et al., 2009). In 2013, the mean annual temperature was 0.2°C which is the same as for 2008-2013, and the frost-free period lasted from 9 June to 14 September (Jensen & Christensen, 2014). The BVOC sampling was conducted in situ in two areas about 50-60 meters apart, one in a wet and one in a dry area. The wet area had sporadically occurring wet suppressions. The vegetation was heterogenic; it had spots of Sphagnum moss spp. and the vascular vegetation was dominated by B. nana and S. arctophila occasionally together with high growing graminoids. The dry area was overall more homogeneous with spots of bare ground. The vegetation was dominated by E. hermaphroditum with S. glauca as a subdominant species. 2.2. BVOC sampling In the wet area, shoots from six individuals of B. nana and S. arctophila were measured in three campaigns, on July 5, July 23 and August 4 (from here on out early July, mid-July and early August). In the dry area, six individuals of E. hermaphroditum and S. glauca were also

5 measured in three campaigns, on June 30-July 1, July 15-17 and August 2-3 (from here on out early July, mid-July and early August). Polyethylene terephthalate (PET) bags (Rul-Let, Abena A/S, Aabenraa, Denmark), pre-heated at 120°C for 1 hour, were used as enclosures in the dynamic enclosure measurements (Niinemets et al., 2011; Ortega & Helmig, 2008; Stewart-Jones & Poppy, 2006). The PET bag with a volume of 1 L was gently attached around the plant shoot and a teflon tube, supplying an air inflow of 500 ml min-1 was connected. The incoming air was purified by a charcoal filter to remove particles and VOCs present in the ambient air, and by a Manganese oxide (MnO2) scrubber to remove ozone (Ortega & Helmig, 2008). After running for 5 min to reach steady state conditions, sampling was started by attaching a stainless steel cartridge filled with Tenax TA (150 mg) and Carbograph 1TD (200 mg) (Markes International, Llantrisant, UK) through a hole in the bag. Air was sampled with an outflow of 200 ml min-1 for 0.5 h, representing a sampled volume of 6 L. The air flows were maintained with battery-operated sampling pumps (12V; Rietschle Thomas, Puchheim, Germany). Immediately after sampling, the adsorbent cartridges were sealed with teflon-coated brass caps and stored refrigerated until analysis. Soil moisture at 6 cm depth was measured manually with a Theta-probe (Sensor type ML2x), and soil temperature at 5 cm depth with M-Log5W Wireless Temperature Data Loggers (GeoPrecision GmbH, Ettlingen, Germany). Air temperature and relative humidity in the PET bag and in ambient air were monitored by shaded loggers at one-minute intervals during sampling (i-Wire Hygrochron, Maxim Intergrated, San Jose, USA). PAR was recorded every 10 seconds with PAR sensors (S-LIA-M003) connected to a HOBO micro station data logger (H21-002, Onset computers corporation, Boston, USA). Immediately after sampling at the wet area, the measured shoots for B. nana and S. arctophila were harvested. The shoots measured in the dry site were not harvested until after the last sampling campaign, and thus the same shoots for each species were measured in all three campaigns. The leaf area of the harvested shoots was measured from digital photographs using Photoshop (Adobe Photoshop CS6 v. 13). Dry mass was determined after oven drying at 70°C for 24h. 2.3. BVOC analysis BVOCs were analyzed by thermal desorption (UNITY2 thermal desorber, Markes, Llantrisant, UK) coupled to an ULTRA autosampler and gas chromatograph-mass

6 spectrometer (7890A Series GC coupled with a 5975C inert MSD/DS Performance Turbo EI System, Agilent, Santa Clara, CA, USA). BVOCs were separated using an HP-5 capillary column (50 m × 0.2 mm, film thickness 0.33 µm). The carrier gas was helium. The oven temperature was 40°C for one minute, raised to 210°C at a rate of 5°C min-1, and then raised to 250°C at a rate of 20°C min-1. Chromatograms were analyzed using Enhanced ChemStation (MSD ChemStation E.02.01.1177, Copyright 1989-2010 Agilent Technologies, Inc.). For identification of the compounds in the samples, standard compounds and the mass spectra in the NIST 8.0 database were used. Compounds with an identification quality ≥90% and presence in minimum two samples per species were included in the dataset (as in Faubert et al., 2010). Compounds from the sampling or analysis system were removed based on blank measurements. The isoprenoid compounds were classified as isoprene, monoterpenes (MTs) and sesquiterpenes (SQTs). Other non-isoprenoid compounds were classified as other volatile organic compounds (other VOCs). Pure standard solutions were used for quantification. The pure standards contained 2-methylfuran, toluene, (e)-2-hexenal, 1-octen-3-ol, (e)-3-hexenyl acetate, nonanal, (e)-3-hexenyl butyrate, isoprene, α-pinene, camphene, sabinene, β-pinene, βmyrcene, α-phellandrene, 3-carene, limonene, eucalyptol, γ-terpinene, terpinolene, linalool, eDMNT, camphor, borneol, terpinen-4-ol, α-terpineol, bornylacetate, α-copaene, longifolene, (z)-caryophyllene, (z)-β-farnesene, aromandendrene and α-humulene. For compounds with no available pure standard, we used α-pinene for MTs, eucalyptol for oxygenated MTs, αhumulene for SQTs and as structurally similar compound as possible for other VOCs (Faubert et al., 2010). Emission rates were calculated according to Ortega & Helmig (2008). For MTs and SQTs, which are temperature dependent, the emission was standardized to 30°C (see Rinnan et al., 2014) and for isoprene the emission was standardized to 30°C and to a PAR level of 1000 µmol m−2 s−1 using the algorithms described in Guenther et al. (1993; 1995). The empirical coefficient of 0.09 was used for MTs and that of 0.18 for SQTs (Guenther et al., 1993; Hakola et al., 2001; Rinnan et al., 2011).

3. Results 3.1. Betula nana Averaged over the three measurement campaigns, B. nana had a total BVOC emission of 5.0 µg g-1 dw h-1 (Fig. 1a). Of this, other VOCs, MTs, SQTs and isoprene accounted for 67%, 18%, 14%, and 1%, respectively (Fig. 1b). The MT that was emitted the most was limonene,

7 for SQTs it was caryophyllene, and the other VOCs that were emitted the most were 3-hexen1-ol and (e)-2-hexenal (Table S1). B. nana had the highest total BVOC emission, 9.6 µg g -1 dw h-1, in early July (Fig. 2a). By mid-July and early August, the emissions had fallen considerably to 14% and 37%, respectively, compared to early July. The emission rate of the other VOCs was 5.9 µg g-1 dw h-1 in early July, and followed the same overall pattern as the total BVOC emissions (Fig. 2a). The relative proportion of other VOCs increased for each subsequent measurement campaign, reaching up to 80% of the total emissions by early August. Standardized SQT and MT emission potentials across all campaigns were on average 1.4 and 1.3 µg g-1 dw h-1, respectively. The SQT emission potential was 2.5 µg g -1 dw h-1 in early July, decreasing to 50% of that in mid-July and by early August it was 25% of early July levels (Fig. 3a). The MT emission potential was 2.7 µg g -1 dw h-1 by early July and decreased to 20% of that the two last campaigns (Fig. 3a). 3.2. Empetrum hermaphroditum E. hermaphroditum emitted on average 2.6 µg g-1 dw h-1 across all three measurement campaigns (Fig. 1a). The emissions of SQTs and other VOCs constituted 50% and 46% of the total BVOC emissions, respectively (Fig. 1b). The most emitted SQTs were copaene and cadinene, and the most emitted other VOCs were 3-hexen-1-ol and 3-hexenyl acetate (Table S2). E. hermaphroditum had low total emissions between 0.7-1.0 µg g-1 dw h-1, in early and midJuly, while the emission by early August was more than 7-fold higher (Fig. 2b). The SQT emissions were stabile low, 0.4 µg g-1 dw h-1, in the first two measurement campaigns and then increased to 3.2 µg g-1 dw h-1 by early August (Fig. 2b). The proportion of SQTs increased from 36% in early July to more than 50% in the two last campaigns (Fig. 2b). The emission rate of MTs was also highest in early August, but the highest relative proportion of MTs (13%) was found in mid-July, which was the campaign with the lowest total BVOC emission (Fig. 2b). The SQT emission potential across all measurement campaigns was on average 2.5 µg g-1 dw h-1. MT emission potential increased gradually from first measuring campaign to the last, ending with 0.3 µg g-1 dw h-1, in early August. The SQT emission potential was lowest in early July and highest, 3.7 µg g-1 dw h-1, in early August (Fig. 3b).

8 3.3. Salix arctophila Averaged across all measurement campaigns, S. arctophila had a total BVOC emission of 8.0 µg g-1 dw h-1 (Fig. 1a), with isoprene as the main component at 76% (Fig. 1b). The remaining emission profile consisted of other VOCs and MTs, with contributions of 15% and 9%, respectively (Fig. 1b). The most emitted MTs were limonene and eucalyptol, and for other VOCs it was 3-hexen-1-ol (Table S3). S. arctophila had similar total BVOC emissions in the first two campaigns, whereas in early August, three times higher emissions were observed (Fig. 2c). Isoprene emission went from 3.9 µg g -1dw h-1 in early July 5, to 3.0 µg g -1dw h-1 in mid-July, and was highest by early August, 11.5 µg g -1dw h-1. The emission of other VOCs and MTs were also highest on August 4 (Fig. 2c). This measurement campaign was the only one where minor SQT emissions were detected in the S. arctophila emissions. The isoprene and MT emission potentials averaged across all measurement campaigns were 16.0 and 1.2 µg g-1 dw h-1, respectively. The isoprene emission potential for S. arctophila consistently increased and reached 26.5 µg g-1 dw h-1 by early August (Fig. 3c). The MT emission potential also increased over time reaching 1.9 µg g-1 dw h-1 by early August (Fig. 3c). 3.4. Salix glauca S. glauca emitted across all measurement campaigns on average 7.3 µg g-1 dw h-1 BVOCs with 84% contribution of isoprene and 15% of other VOCs (Fig. 1). The other VOCs that were emitted the most were 3-hexen-1-ol, (e)-2-hexenal and nonanal and of MTs it was βtrans-ocimene (Table S4). Total BVOC emissions of S. glauca were initially low and increased notably in subsequent measurement campaigns (Fig. 2d). Total isoprene also increased markedly across campaigns. In early July the isoprene emission was 1.0 µg g-1 dw h-1, by mid-July it was five times higher and by early August it was 14 times that of early July levels. The largest proportion of isoprene was 94% in mid-July. The emission of other VOCs was highest, 1.9 µg g -1 dw h-1, in early August, but the relative proportion was highest, 56%, by early July (Fig. 2d). The MT emission was low and increased between the measurement campaigns reaching 0.1 µg g-1 dw h-1 in early August. Like for S. arctophila, emission of SQTs was detected in minor amounts in the last campaign, in early August.

9 Averaged across all measurement campaigns the isoprene emission potential was 10.1 µg g 1

dw h-1. It increased during the growing season, being 3.3 µg g -1dw h-1 in early July, and 16.7

µg g-1 dw h-1 in early August (Fig. 3d). The MT emission potential was highest, 0.2 µg g-1 dw h-1, in mid-July. 3.5. Environmental conditions during measurements During the measurement campaigns of B. nana and S. arctophila, the air temperature in the enclosure was 27°C, 17°C, and 23°C for early July, mid-July and early August, respectively (Fig. 2a; 2c). The PAR levels for the same campaigns changed from 1400-1500 µmol m-2 s-1 in early July to 500 µmol m-2 s-1 in mid-July and to 1500 µmol m-2 s-1 in early August. For E. hermaphroditum and S. glauca, the enclosure temperature was lowest, 21°C, in early July, and increased to 24°C in mid-July, and further to 29°C in early August (Fig. 2b; 2d). The corresponding PAR levels were 800, 1300 and 1000 µmol m-2 s-1, respectively. The emission rates in general followed changes in temperature and PAR (Fig. 2). Soil temperature increased over the measurement period. The mean soil temperature at 5 cm depth was 10°C in early July and up to 5.5°C higher in early August (Table S5). Mean soil moisture at 6 cm depth was higher in the wet heath with S. arctophila and B. nana, 37-47%, than in the dry heath with E. hermaphroditum and S. glauca, where it was 15-21% (Table S5). The soil moisture was highest in mid-July.

4. Discussion 4.1. Emission profiles The large differences in the BVOC emission profiles between the arctic plant species in the present study is in agreement with earlier findings of diverse emission profiles in arctic vegetation dominated by different species (Faubert et al., 2012; Schollert et al., 2013). This highlights that vegetation composition is highly relevant for determining ecosystem BVOC emissions. The dominance of non-isoprenoid BVOCs in the emission profile of B. nana is in agreement with an earlier study from Abisko, subarctic Sweden, in which the emission profile in midJuly consisted of 88% non-isoprenoid BVOCs (Rinnan et al., 2011). The MT emission potential we measured for B. nana was similar but the SQT emission potential nearly three times larger than found by Rinnan et al. (2011). In another study from Abisko, BVOC emissions from Betula pubescens ssp. czerepanovii (mountain birch) were sampled from June

10 to August 2006 (Haapanala et al., 2009). They found MT and SQT emission potentials for B. pubescens ssp. czerepanovii to be as high as 3.0 µg g-1 dw h-1 and 8.1 µg g -1dw h-1, respectively (Haapanala et al., 2009). An even higher mean MT emission potential of 5.4 µg g-1 dw h-1 was reported for Betula pendula (silver birch) averaged over the growing season in boreal forest, Finland (Hakola et al., 1998). The emission potentials for these boreal-polar Betula spp. are in the same range. Besides, due to species-specific emissions, the difference can be caused by differences in climate, the weather history prior to the measurements, time of day during measurements, sampling methods and plant phenological state during measurements (Guenther et al., 1995; Niinemets et al., 2010, 2011; Lindwall et al., 2015). The non-isoprenoid BVOC emission of B. nana included a group of compounds also known as green leaf volatiles (GLVs), e.g. 3-hexen-1-ol, and (e)-2-hexenal. Hakola et al. (2001) found that mechanical stress exemplified by pressing the leaves of Betula spp. with the hands prior to BVOC sampling markedly increased emissions of 3-hexen-1-ol, 3-hexenylacetate, (e)-2-hexenal and 1-hexanol. Therefore, high amounts of these compounds could suggest mechanical damage on the plant shoots measured. However, the emissions of 3-hexen-1-ol and (e)-2-hexenal in the present study are likely to be true emissions, as the method used does not involve pressing the leaves and the PET bags used as enclosures are easy to attach without disturbing the plant. Further, in their paper on isoprenoid emissions from B. pubescens ssp. czerepanovii, Haapanala et al. (2009) noted high emissions of SQTs typical for stress responses suggesting that the Betula spp. growing in subarctic areas may constitutively emit stress-related compounds. The genus Empetrum has glandular trichomes (Muravnik & Shavarda, 2012) which are common structures for storage of BVOCs (Biswas et al., 2008). These structures indicate that E. hermaphroditum stores BVOCs in the leaves. BVOC storing species are generally moderate BVOC emitters (Kesselmeier & Staudt, 1999), and our data on E. hermaphroditum supports this suggestion. The BVOC emission from E. hermaphroditum was lower than that from the other species, but contained twice as many different compounds. The large relative contribution of SQTs (on average 50%), especially copaene and cadinene, to the emission profile, is in agreement with findings from a Subarctic forest floor dominated by E. hermaphroditum (Faubert et al., 2012). In contrast, Schollert et al. (2015) found E. hermaphroditum, growing on a subarctic heath in Abisko, North Sweden, to have a BVOC emission profile containing only 12% SQTs. Instead, the major part of the emission was non-

11 isoprenoid BVOCs (Schollert et al., 2015), which comprised 46% of the total emissions in the present study. The Salix species in the present study emitted predominantly isoprene, which is characteristic for the Salix genus in general (Hakola et al., 1998; Rinne et al., 2009; Fineschi et al., 2013; Rinnan et al., 2014). The observed average isoprene emission potentials of 16.0 and 10.1 µg g-1 dw h-1 for S. arctophila and S. glauca, respectively, are comparable with an isoprene emission potential of 16 µg g-1dw h-1 reported for Salix phylicifolia in mid-July in Abisko, subarctic Sweden (Rinnan et al., 2011), and the emission potential for Salix pulchra growing in Alaska, 15.1 µg C g-1dw h-1 (17.1 µg g-1dw h-1; Potosnak et al., 2013). These emission potentials are generally lower than those Steinbrecher et al. (2009) collected from literature in order to model BVOC emission from Europe: Their survey included isoprene emission potentials ranging from 18.9 µg g-1 dw h-1 for Salix caprea to 37.2 µg g-1 dw h-1 for Salix alba. Potosnak et al. (2013) reviews that the general isoprene emission potential for Salix spp. is 27.2 µg C g-1dw h-1 (30.8 µg g-1 dw h-1). In summary, it appears that isoprene emission potentials for arctic Salix spp. are slightly lower than for Salix spp. growing at lower latitudes. 4.2. Seasonal variation The emission pattern during the study period differed between the species. B. nana had the highest BVOC emission rate and highest MT and SQT emission potentials during the first campaign in early July. This is in agreement with Hakola et al. (1998), who found B. pendula to emit a large amount of BVOCs, especially MTs, in the early growing season. They suggested that the early season emission peak might have been caused by higher level of chemical defense in young leaves (Hakola et al., 1998). This is supported by Valkama et al. (2003), who found the density of trichomes to be highest in young Betula leaves for protection against herbivores and pathogens. Furthermore, resin glands of Betula spp. develop through the growing season and are most active and important in new leaves at the start of the season and gradually decrease as other defense mechanisms build up (Lapinjoki et al., 1991). Both trichomes and resin glands are therefore likely to contribute to the early summer emissions (observed here) from Betula spp. E. hermaphroditum and the two Salix spp. had the largest emission rates in early August. This pattern can partly be explained by differences in climatic conditions during measurements and partly by plant phenology, which is different for E. hermaphroditum and Salix spp.

12 The large emission potentials in early August for E. hermaphroditum may be related to it being an evergreen. The current year leaves of evergreen arctic species might have higher emissions than the old leaves. As evergreens in general are slower growing than deciduous species, the peak in E. hermaphroditum emissions in August may be related to slow maturation of the current year leaves. This is in agreement with BVOC emission potentials for the evergreen Cassiope tetragona in Abisko increasing between June and August (Rinnan et al., 2011). It is also possible that some of the emissions in August originated from the berries of E. hermaphroditum maturing in August, as berries are known to emit BVOCs in order to attract animals to distribute the seeds (Laothawornkitkul et al., 2009; Peñuelas & Staudt, 2010). The isoprene emission pattern for the Salix spp. appears to be typical. Isoprene emissions are known to be strongly light and temperature dependent (Guenther et al., 1995; Lerdau & Gray, 2003), and therefore, the differences in the emission rates might be best explained by variation in these environmental factors during measurement. However, when the isoprene emissions were standardized to constant temperature and PAR, the emissions from both Salix spp. still increased from the end of June to early August. This suggests that the isoprene emission potentials were also affected by plant phenology or other environmental factors. Increased isoprene emission in late summer is also in agreement with earlier studies on high latitude vegetation (Tiiva et al., 2008). Tiiva et al. (2008) suggested that fully developed plants have a larger capacity for isoprene emission, which is in agreement with several findings of broadleaved plants to first initiate isoprene production when the leaves are fully expanded, which is linked to the onset of the activity of isoprene synthase (Hakola et al., 1998; Lerdau & Gray, 2003). 4.3. Insights into future vegetation changes As a consequence of global warming, arctic regions will experience pronounced temperature increases, increased soil nutrient availability and longer growing seasons (ACIA, 2004; IPCC, 2013). This is expected to change the competitive balance between plant species (Körner, 2006). Additionally, studies using temperature manipulation experiments and surveys of past vegetation changes have found that the vegetation in the Arctic responds to warming with increasing canopy height, vascular plant biomass and changing species composition ( Tape et al., 2006; Elmendorf et al., 2012; Michelsen et al., 2012; Walker et al., 2014).

13 Analyzing vegetation records from 61 in-situ warming experiments, Elmendorf et al. (2012) found vegetation composition alterations to differ between locations, with expansion of deciduous shrubs in the Sub- and Low Arctic, and expansion of graminoids in the High Arctic. Kaarlejärvi et al. (2012) observed, with data from three experiments with 11-12 years of passive warming in sub-arctic Scandinavia, that B. nana increased more in abundance than E. hermaphroditum in the tundra. Further, it has been suggested that E. hermaphroditum might lose the competition for nutrients to deciduous species and therefore potentially decrease in abundance if soil nutrient availability increases (Faubert et al., 2012). The question whether deciduous shrubs gain an advantage from climate warming compared with evergreen shrubs is still not fully elucidated (Elmendorf et al., 2012; Kaarlejärvi et al., 2012). Elmendorf et al. (2012) observed that warming increased the abundance of deciduous shrubs and decreased that of mosses and lichens, while not having a significant impact on evergreens. On the other hand, Tape et al. (2006) studied aerial photos, vegetation plot analysis and remote sensing by satellite, and found low and tall deciduous shrubs (Alnus, Salix and Betula spp.) to increase in Alaska. They found this to be consistent with plot and remote sensing evidence from Canada, Scandinavia and Russia, and all together suggests a Pan-Arctic expansion of deciduous shrubs (Tape et al., 2006). These changes over the past 50 years, in large undisturbed vegetation, are caused by climatic changes, including increased temperatures, and it is likely that they show the direction of future changes in the vegetation. These potential changes in future vegetation composition will inevitably change the BVOC emission from the Arctic (Potosnak et al., 2013; Rinnan et al., 2014). If species such as E. hermaphroditum are replaced with the expanding deciduous Salix and Betula spp. (Elmendorf et al., 2012; Tape et al., 2006), our results suggest that this would lead to increased total BVOC emissions and higher relative contributions of isoprene, MTs and non-terpenoid BVOCs into the arctic atmosphere.

5. Conclusions This study showed that arctic plant species have considerable BVOC emissions. At the studied low arctic site, B. nana was a moderate emitter of non-terpenoid BVOCs, followed by MTs and SQTs, E. hermaphroditum was a moderate emitter primarily releasing SQTs and non-isoprenoid BVOCs, and the Salix spp. were isoprene emitters. The studied species showed species-specific emission variation during the growing season. For E. hermaphroditum, S. arctophila and S. glauca, the total BVOC emission was highest in

14 August whereas B. nana had the highest emission in early July. The pattern is consistent even when standardized for temperature and PAR, suggesting other controlling factors and suggesting a linkage between plant phenology and the emission. It is important to consider the species differences when estimating and up-scaling BVOC emissions. Climate change-induced increased plant height and biomass growth together with a possible expansion in the abundance of deciduous shrubs like Betula and Salix spp., has the potential to increase the emissions of isoprene, MTs and non-isoprenoid BVOCs in the Arctic.

Acknowledgements This work was supported by Maj and Tor Nessling Foundation, the Danish Council for Independent Research | Natural Sciences, the Villum Foundation, and the Danish National Research Foundation (activities within the Center for Permafrost, CENPERM DNRF100). I.V.-P. received a travel grant from Ingeniør Svend Fiedler og Hustrus Fond. We would like to thank Gosha Sylvester and Esben V. Nielsen for laboratory assistance and Peter Laszlo Horvath for language revision. Pinngortitaleriffik - Greenland Institute of Natural Resources and Greenland Ecosystem Monitoring Programme provided an excellent logistical basis for the work.

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Figure legends

Fig. 1. (a) Mean emissions (+SE; n = 18; µg g-1 dw h-1) of isoprene, monoterpenes (MTs), sesquiterpenes (SQTs) and other volatile organic compounds (other VOCs) for Betula nana, Empetrum hermaphroditum, Salix arctophila and Salix glauca averaged for the measurement period. Mean photosynthetically active radiation (PAR, µmol m−2 s−1), temperature (°C) and relative humidity (RH, %) measured in the enclosure during sampling are shown. (b) The percentage of each BVOC group of the total BVOC emission.

Fig. 2. Mean emissions (+SE, n=6; µg g-1 dw h-1) of isoprene, monoterpenes (MTs), sesquiterpenes (SQTs) and other volatile organic compounds (other VOCs) during the measurement period for (a) Betula nana, (b) Empetrum hermaphroditum, (c) Salix arctophila and (d) Salix glauca. Mean photosynthetically active radiation (PAR, µmol m−2 s−1) and temperature (°C) measured in the enclosure during sampling are shown. Note the different yaxis scales.

Fig. 3. Mean emission potentials (temperature of 30°C, PAR of 1000 µmol m-2 s-1; Guenther et al., 1993) (+SE, n=6) for isoprene, monoterpenes (MTs), and sesquiterpenes (SQTs) during the measurement period for (a) Betula nana, (b) Empetrum hermaphroditum, (c) Salix arctophila and (d) Salix glauca. Note the different y-axis scales.

Figure 1

Figure 2

Figure 3

Electronic supplementary information

Volatile organic compound emission profiles of four common arctic plants

In Atmospheric Environment

Ida Vedel-Petersena, Michelle Schollerta, b, Josephine Nymandc, Riikka Rinnana, b* a

Terrestrial Ecology Section, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen K, Denmark b

Center for Permafrost (CENPERM), Department of Geoscience and Natural Resource Management, University of Copenhagen, Øster Voldgade 10, DK-1350 Copenhagen K, Denmark

c

Pinngortitaleriffik - Greenland Institute of Natural Resources, Kivioq 2, Postboks 570, 3900 Nuuk, Greenland *Correspondemce Riikka Rinnan, Terrestrial Ecology Section, Department of Biology, University of Copenhagen, Universitetsparken 15, 2100 Copenhagen K, Denmark, Tel.: +45 51827039; E-mail: [email protected].

Contents: Table S1. Mean emissions rates (± SE, n = 6; ng g-1 dw h-1) of individual BVOCs and total monoterpenes, sesquiterpenes, other VOCs, and BVOCs from Betula nana in the three campaigns. Table S2. Mean emissions rates (± SE, n = 6; ng g-1 dw h-1) of individual BVOCs and total monoterpenes, sesquiterpenes, other VOCs, and BVOCs from Empetrum hermaphroditum in the three campaigns. Table S3. Mean emissions rates (± SE, n = 6; ng g-1 dw h-1) of individual BVOCs and total monoterpenes, sesquiterpenes, other VOCs, and BVOCs from Salix arctophila in the three campaigns. Table S4. Mean emissions rates (± SE, n = 6; ng g-1 dw h-1) of individual BVOCs and total monoterpenes, sesquiterpenes, other VOCs, and BVOCs from Salix glauca in the three campaigns. Table S5. Soil temperature at 5 cm depth (°C) and soil moisture at 6 cm depth (%) during sampling (mean ± SE, n=6 (5 July and 4 August n=12).

1

Table S1. Mean emissions rates (± SE, n = 6; ng g-1 dw h-1) of individual BVOCs and total monoterpenes, sesquiterpenes, other VOCs, and BVOCs from Betula nana in the three campaigns.

isoprene α-pinene camphene sabinene β-pinene β-myrcene 3-carene unidentified MT 1 limonene β-phellandrene γ-terpinene e-DMNT α-thujone Total monoterpenes caryophyllene β-cubebene α-caryophyllene α-farnesene Total sesquiterpenes (e)-2-hexenal 3-hexen-1-ol 1,4-hexadiene p-xylene benzaldehyde 1,2,3-trimethylbenzene (z)-3-hexenyl acetate methylpentadiene 1,4-dimethyl-2-ethylbenzene undecane 1-phenyl-2-methylpropene nonanal 4a-methyldecahydronaphthalene 2-hexenyl butanoate dodecane bornylacetate tridecane cyclohexylbenzene tetradecane toluene Total other VOCs Total BVOCs

5 July