Plant volatiles in extreme terrestrial and marine environments.

Plant volatiles in extreme terrestrial and marine environments1

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Running title: Plant volatiles in extreme environments

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Riikka Rinnan1,2*, Michael Steinke3, Terry McGenity3, Francesco Loreto4

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DK-2100 Copenhagen Ø, Denmark

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Terrestrial Ecology Section, Department of Biology, University of Copenhagen, Universitetsparken 15,

Centre for Permafrost (CENPERM), University of Copenhagen, Øster Voldgade 10, DK-1350

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Copenhagen K, Denmark

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Piazzale Aldo, Moro 7, 00185 Roma, Italy

School of Biological Sciences, University of Essex, Colchester CO4 3SQ, United Kingdom Dipartimento di Scienze Bio-Agroalimentari (DISBA), Consiglio Nazionale delle Ricerche (CNR),

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*Corresponding author: Riikka Rinnan, Terrestrial Ecology Section, Department of Biology, University

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of Copenhagen, Universitetsparken 15, DK-2100 Copenhagen Ø, Denmark

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Email: [email protected]

This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/pce.12320

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ABSTRACT

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This review summarizes the current understanding on plant and algal volatile organic compound

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(VOC) production and emission in extreme environments, where temperature, water availability,

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salinity or other environmental factors pose stress on vegetation. Here, the extreme environments

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include terrestrial systems, such as arctic tundra, deserts, CO2 springs and wetlands, and marine

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systems such as sea ice, tidal rockpools and hypersaline environments, with mangroves and salt

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marshes at the land-sea interface. The emission potentials at fixed temperature and light level or

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actual emission rates for phototrophs in extreme environments are frequently higher than for

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organisms from less stressful environments. For example, plants from the arctic tundra appear to

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have higher emission potentials for isoprenoids than temperate species, and hypersaline marine

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habitats contribute to global dimethyl sulphide (DMS) emissions in significant amounts. DMS

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emissions are more widespread than previously considered, for example in salt marshes and some

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desert plants. The reason for widespread VOC, especially isoprenoid, emissions from different

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extreme environments deserves further attention, as these compounds may have important roles in

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stress-resistance and adaptation to extremes. Climate warming is likely to significantly increase VOC

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emissions from extreme environments both by direct effects on VOC production and volatility, and

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indirectly by altering the composition of the vegetation.

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Key-words: Arctic, BVOC, desert, DMS, drought, hypersaline, isoprenoid, mangrove, marine,

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temperature


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INTRODUCTION

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The study of plant volatile organic compounds (VOCs) has expanded from boreal (Rinne et al. 2009)

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and Mediterranean ecosystems (Owen et al. 2001) to rainforests (Kesselmeier et al. 2009), and

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recently to more extreme environments. Here, extreme environments are considered as systems

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having unusually challenging conditions that are stressful for most organisms, and result from

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extremes in temperature, water availability, salinity, oxygen, CO2 concentration, or fluctuation in

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frequency and amplitude of environmental conditions. In order to cope in such challenging habitats,

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extremophile plants have evolved protective mechanisms, both physical (e.g. plant/leaf size and

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posture, structural adaptations such as waxes, hairs or spikes) and chemical (e.g. secondary

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metabolites, VOCs).

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Several recent reviews addressed the roles of different VOCs in enhancing the tolerance of plants to

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various general environmental stressors (Holopainen & Gershenzon 2010; Loreto & Schnitzler 2010;

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Possell & Loreto 2013). We caution that the term ‘stress’ is debatable in the ecological sense (see

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e.g. Grime 1989; Körner 2003). In the case of extreme ecosystems, adapted organisms might actually

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experience stress in what is typically referred to as more ordinary environments. In this review, we

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touch on both adaptation and acclimation to extreme environments. Adaptation involves genetic

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changes in the organism caused by long-term exposure, that accumulate over generation’s time

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scale, while acclimation is typically a reversible adjustment, which occurs in shorter term in response

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to a transient stress (Morgan-Kiss et al. 2006).

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This review will summarize the current understanding of plant and algal volatile production and

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emission in extreme environments, including both terrestrial and aquatic environments. The

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terrestrial part focuses on the cold, especially arctic, ecosystems and deserts, as they are widespread

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around the globe and most affected by climate change (IPCC 2007). In addition, we report on findings

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from CO2 springs, which are extreme environments that provide a natural laboratory for assessing 3 This article is protected by copyright. All rights reserved.

how plants may adapt to future high CO2 conditions. Finally, we move from terrestrial to marine

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environments via flooded systems, a section which discusses naturally waterlogged and often anoxic

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environments like freshwater wetlands, mangroves and salt marshes. The aquatic part includes

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examples from polar regions and hypersaline environments.

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The VOCs from the large range of ecosystems covered in this review also include compounds that are

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not typically studied in terrestrial habitats. We do not include methane, but do consider

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methylhalides, dimethyl sulphide (DMS) and other heavier VOCs. We use specific compound names,

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when possible, and the term ‘isoprenoids’ when discussing the group consisting of isoprene,

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monoterpenes and sesquiterpenes.

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The study of volatiles is motivated by the significance of these compounds for atmospheric processes

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that influence the atmospheric burden of pollutants and climate change in several ways. First, VOCs

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are main biogenic precursors of ozone, which is a greenhouse gas and a toxic air pollutant

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(Fehsenfeld et al. 1992). Second, the photo-oxidation of VOCs leads to formation of secondary

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organic aerosols (Kavouras et al. 1998; Claeys et al. 2004), which have potential for complex climate

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feedbacks (Carslaw et al. 2010), and third, they affect the oxidizing capacity of the atmosphere and

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thereby increase the lifetime of other compounds such as the greenhouse gas methane (Di Carlo et

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al. 2004).

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Our overall aim is to address the following initial questions:

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1) Do plants living in extreme environments have innate high VOC emission potential, i.e.

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emission rate at standard temperature (30°C) and light (photosynthetic photon flux density

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(PPFD) of 1000 µmol m-2 s-1) levels, relative to corresponding plant species from less extreme

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environments? This could be expected if higher volatile emissions would serve as a

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mechanism for plant adaptations to extreme environments for similar reasons as the general

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stress-induced elevated VOC emissions.


2) How will volatile emissions from plants living in extreme environments respond to climate

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warming and other future changes in the environment? This is an important question as

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alleviation of the extreme conditions, e.g. by warming of the Arctic, may actually cause stress

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to the vegetation adapted to these conditions, or VOC production may trigger acclimation

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processes to rapid climate changes.

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TERRESTRIAL EXTREME ENVIRONMENTS

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Cold ecosystems

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A global model of biogenic VOC emissions from 1995 gave minimal VOC emissions for the polar

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regions (Guenther et al. 1995). The low emissions were estimated based on the small foliar density

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derived from climatic variables and satellite data, low temperature and solar angle. The first actual

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field measurements in the polar region were conducted a decade later (see Table S1). While the

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foliar density in the Arctic is inevitably low and the growing season short, we discuss here some

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evidence suggesting that VOC emissions from arctic ecosystems can be higher than expected due to

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high temperature fluctuation, high temperature sensitivity of the vegetation (Faubert et al. 2010a;

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Holst et al. 2010) and a large discrepancy between air and leaf temperatures (e.g. Körner 2006;

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Svoboda 2009).

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Emission potential of plants in cold ecosystems

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Only 0.4% of all vascular plant species are established in the Arctic (Billings 1992), where the

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vegetation is generally dwarf and composed of a mixture of bryophytes, sedges, and shrubs. Many of

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the shrubs are actually miniature trees - same species that are found in warmer climates - growth of

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which is limited by harsh environmental conditions and shortage of available nutrients. Of the

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common tundra plant species, at least mosses (Hanson et al. 1999; Hellén et al. 2006; Ekberg et al.

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2011a), sedges (Tiiva et al. 2007a; Ekberg et al. 2009; Tiiva et al. 2009) and willow species (Rinnan et 5 This article is protected by copyright. All rights reserved.

al. 2011; Potosnak et al. 2013) emit isoprene. However, Fineschi et al. (2013) reported that in cold

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environments, only 17-22% of the plant species emit isoprene with rates clearly exceeding 1 µg g-1 h-

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isoprene emission capacity in arctic plants is relatively low, while the emission capacity of other

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isoprenoids is at higher level. We have a closer look at four examples of plant species common in the

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Arctic.

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First, willows (Salix spp.) are common isoprene emitters in the Arctic (Rinnan et al. 2011; Potosnak et

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al. 2013), and the emission potential appears to be similar or lower than in willows from warmer

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areas. For example, Salix phylicifolia had isoprene emission potential of 32 µg g-1 h-1 in a boreal forest

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(Hakola et al. 1998) but only of 16 µg g-1 h-1 in a fell heath in the Subarctic (Rinnan et al. 2011). In

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contrast, the isoprene emission potential for the arctic willow, Salix arctica, from high arctic

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Greenland was approx. 31 µg g-1 h-1 in the middle of the growing season (Schollert, Kivimäenpää &

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Rinnan, unpublished data), which is similar to the boreal willows (Hakola et al. 1998). Interestingly,

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the monoterpene emission potential for both willow species from the Arctic was clearly higher (1.0

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µg g-1 h-1) than in the boreal forest (0.33 µg g-1 h-1) (Hakola et al. 1998; Rinnan et al. 2011).

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Another example is Betula pubescens (the downy birch) which was - according to an early qualitative

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emission inventory - reported to lack monoterpene emissions (Hewitt & Street 1992). Later studies

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showed that there is great tree-to-tree variation, and that the species has emission potentials for

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monoterpenes and sesquiterpenes of 0.17-5.49 and 0.31-6.94 µg g-1 h-1, respectively (Hakola et al.

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2001). In contrast, the arctic subspecies, Betula pubescens ssp. czerepanovii, has been shown to have

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more than twice as high emission potential for monoterpenes (0.6-12 µg g-1 h-1) and varying but high

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emission potential for sesquiterpenes (0.26-16 µg g-1 h-1) (Table 1; Haapanala et al. 2009). Haapanala

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et al. (2009) speculate that the herbivory pressure by the two geometrid moth species Epirrita

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autumnata and Operopthera brumata on B. pubescens ssp. czerepanovii can cause relatively high

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emissions of volatiles related to biotic stresses. The herbivore outbreaks that occur in a cyclic manner

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cause complete defoliation of subarctic birch forests, and both these and the non-outbreak insect

, which was less than in temperate or tropical ecosystems. The limited data indeed suggests that


herbivory are expected to increase with climate warming in the Arctic (Callaghan et al. 2013). These

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outbreaks do not occur further south most probably due to higher generalist predation pressure

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(Neuvonen et al. 2005).

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The arctic circumpolar evergreen shrub, Arctic bell-heather (Cassiope tetragona (L) D. Don) is known

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for its strong scent, its richness in secondary compounds and for not being grazed by herbivores

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(Callaghan et al. 1989). The volatile emissions of this long-lived and common arctic and alpine plant

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species are mainly composed of monoterpenes and sesquiterpenes (Rinnan et al. 2011). The mean

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monoterpene emission potential of C. tetragona (3.6-4.4 µg g-1 h-1, June-August; Rinnan et al. 2011) is

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more than two orders of magnitude higher than that of common heather (Calluna vulgaris, ~0.02 µg

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g-1 h-1; Tiiva, Michelsen & Rinnan, unpublished data) or Mediterranean heather (Erica multiflora,

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≤0.01 µg g-1 h-1; Owen et al. 2001). Similarly, the sesquiterpene emission potential of C. tetragona

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(1.1-2.5 µg g-1 h-1, June-August; Rinnan et al. 2011) is much higher than that of C. vulgaris (~0.01 µg g-

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tetragona is densely covered with two types of trichomes that potentially serve as storage organs for

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its volatiles: long ones and flat ones (Fig. 1; Kivimäenpää, personal communication), the latter of

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which resemble glandular trichomes previously described as storage structures for VOCs (Biswas et

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al. 2009).

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Siberian forests experience extreme cold temperatures during the winter and heat during the

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summer. They cover an area of 6 million km2 of which close to half is dominated by the deciduous

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Siberian larch (Larix sibirica) species, which is our last example of VOC emission potentials for arctic

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plant species. Measurements of VOC emissions from Siberian larch saplings suggest that these trees

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have considerably higher monoterpene emission potential (5.2–21 µg g-1 h-1; Ruuskanen et al. 2007)

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than other boreal forest trees, e.g. Scots pine (~1-2 µg g-1 h-1) or Norway spruce (0.2-8.3 µg g-1 h-1)

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(Rinne et al. 2009). A high proportion of the monoterpenes emitted from Siberian larch originates

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from storage pools (Ghirardo et al. 2010). Field measurements of mature Larix cajanderi trees

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growing on permafrost have confirmed that the VOC emissions from larch forests greatly exceed the

h-1; Tiiva, Michelsen & Rinnan, unpublished data). The surface of the deeply grooved leaves of C.


current model estimates; the emission potential for monoterpenes varied between 0.5 and 18.5 µg g-

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h-1 (Kajos et al. 2013). It may, however, be that the relative contribution of larch forests to the

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subarctic/arctic VOC emissions decreases in the future, because the larch-dominated forest is likely

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to shift to evergreen conifer forest in response to increased temperatures (Shuman et al. 2011) due

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to decoupling of the taiga–permafrost coupled system (Zhang et al. 2011).

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Impact of climate change in cold ecosystems

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The Arctic is the area of the globe experiencing a warming that proceeds at approximately twice the

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global rate (IPCC 2007). The impact of temperature on volatile emissions is already now different in

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the arctic ecosystems than in forests from subtropical to boreal zones, where leaf temperatures have

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been shown to remain at constant 21°C regardless of air temperature (Helliker & Richter 2008).

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During clear-sky conditions when solar radiation effectively heats up the soil and the dark low-

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stature plant surface in the tundra, the temperature of the microclimate surrounding plants can be

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15°C above the ambient air temperature and reach values exceeding 30°C (Rinnan, personal

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observation; Svoboda 2009). No data are currently available for precisely describing the effect of

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rapid warming on VOC emission in the Arctic. However, this uncoupling makes it impossible to model

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arctic emissions on the basis of air temperature data, as proposed for temperate environments

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(Guenther et al. 2006).

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Because of adaptation to low temperatures, standardization of volatile isoprenoid emissions to 20°C

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instead of the commonly used 30°C has repeatedly been suggested for calculation of emission

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potentials for boreal and arctic ecosystems (e.g. Ekberg et al. 2009; Holst et al. 2010). For example,

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Holst et al. (2010) used non-linear curve-fitting to test for temperature and light dependency of

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isoprene fluxes measured in a subarctic wetland dominated by sedges. They observed very high

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temperature sensitivity of isoprene emissions with unusually high values when emissions were

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standardized to 30°C, and recommended using 20°C as the standardization temperature. It is likely 8 This article is protected by copyright. All rights reserved.

that the leaf temperature of sedges growing in wetlands of the cold regions is more coupled to the

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ambient air temperature because of their upright nature and the cooling effect on leaf temperature

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from transpiration in a wet growth environment (Körner 2006), and thus standardization to 20°C in

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these ecosystems would be advisable. However, in the arctic dry tundra with low plant height, and

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because of the aforementioned efficient heat absorption to the plant/soil surface, and the

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concomitant rise of leaf temperatures, we recommend standardization to 30°C.

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In general, the emission of volatile isoprenoids decreases above an optimum of 40-45°C, because of

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thermal denaturation of the key enzymes catalysing the biosynthesis of the volatiles, or because of

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metabolic down-regulation of the pathway, involving reduced photosynthesis and reduced formation

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of isoprenoid precursors (Singsaas & Sharkey 2000, Loreto et al. 2006). It is unlikely that these high

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temperatures will be reached in the Arctic despite the predicted air temperature increase of up to 7-

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8°C in the next 100 years (ACIA 2005, IPCC 2007). This is due to the increased plant height growth

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under warmer conditions (Campioli et al. 2012) leading to increasing coupling of leaf temperatures to

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air temperature. However, if the isoprenoid emission of the cold-adapted plants acclimates to

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growth temperature as shown by Fares et al. (2011) in a laboratory study with Populus ×

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euramericana saplings, the rapid warming may drive emissions of volatile isoprenoids at rates much

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higher than those predicted by current models. Fares et al. (2011) demonstrated this temperature

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acclimation by showing that plants grown at 25°C emit more isoprene than plants grown at 35°C

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when the emission for both is monitored at 35°C. This suggests that the relatively large temperature

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increases in the cold environments can lead to relatively higher emission increases than climate

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warming would cause in plants from lower latitudes.

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Tiiva et al. (2008) and Faubert et al. (2010a) used a long-term field experiment located in subarctic

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Sweden to assess whether experimentally increased temperatures would increase VOC emissions

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from subarctic heath vegetation communities. They found that warming of only 2°C reproduced in

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open-top greenhouses doubled the emissions of monoterpenes and sesquiterpenes, and increased

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the emission of isoprene by 50-80%. This is a more drastic response than expected (Faubert et al. 9 This article is protected by copyright. All rights reserved.

2010a; Michelsen et al. 2012) that is in agreement with data by Holst et al. (2010), who also observed

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a stronger temperature dependency in subarctic plants than elsewhere. These findings also support

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the suggestion that acclimation of plants to a cold environment may drive higher rates of emissions

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once the plants are exposed to warmer temperatures (Fares et al. 2011).

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The temperature change in the Arctic is also causing other alterations in the environment, likely

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resulting in an increase in isoprenoid emissions from this area (Fig. 2). One of the alterations is

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thawing of permanently frozen ground, i.e. permafrost. Permafrost covers 22% of the land surface

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area in the Northern Hemisphere and stores almost half of the global soil carbon and a large pool of

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nutrients (Schuur et al. 2008). Both warming and permafrost thaw lead to increased mineralization of

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nutrients locked in the soil organic matter alleviating nutrient limitation of plant growth (Mack et al.

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2004; Schuur et al. 2007). The increased plant production and altered vegetation composition (see

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below) lead to a decrease in albedo and an additional positive feedback to climate warming along

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with albedo changes due to lengthening of the snow-free season (Chapin et al. 2005; Fig. 2).

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Climate change is altering vegetation composition and generally increasing the currently low plant

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biomass of the Arctic, leading to the expansion of forest trees into open tundra and of tundra

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vegetation into polar deserts (ACIA 2005). Such changes are likely to impact on the quantity and

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quality of the volatile emissions from this area. A recent study from subarctic Sweden recorded a

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19% increase in mountain birch (B. pubescens ssp. czerepanovii) biomass density over 13 years,

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mainly within the established birch forest (Hedenås et al. 2011). According to a recent overview

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paper (Callaghan et al. 2013), aspen (Populus tremula L.), grey alder (Alnus incana) and willows have

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also been spreading northwards and to higher altitudes. Tape et al. (2006) presented convincing

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evidence for the greening of the Arctic due to shrub expansion and suggested that a pan-Arctic

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vegetation transition is underway.

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The responses to warming in the understory show strong regional variation: shrubs increase in

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warmer arctic locations, while graminoids increase in cold locations (Elmendorf et al. 2012, 10

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Michelsen et al. 2012). These changes are likely to increase emissions of all types of plant volatiles,

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but a larger increase in isoprene emission can be expected because of the spreading of high isoprene

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emitters of the Salicaceae family (Loreto et al. 2013; Fig. 2).

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Winter emissions

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The vegetation growing in boreal and arctic areas is inevitably exposed to cold stress and freeze-thaw

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events, especially during spring and autumn. Unfortunately, most of the studies conducted in cold

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environments have focused on the short growing season with few studies extending towards winter.

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Six-carbon (C6) volatiles (also called “green leaf volatiles”, GLVs) are products of the lipoxygenase

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pathway and indicate membrane denaturation, especially when plants are exposed to high

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temperatures (Loreto et al. 2006). However, cold stress appears to cause a similar response as heat

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stress in tomato (Solanum lycopersicum L.), which is not a cold-adapted species (Copolovici et al.

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2012). Copolovici et al. (2012) used this model plant to assess effects of two antagonistic stresses –

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cold and heat – on volatile emissions. They found that despite their generally opposite effects on

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membrane fluidity, the contrasting temperature stresses applied as a short-lived shock treatment

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and followed by VOC measurements at 30°C caused a similar induction in the emissions of C6-

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volatiles when the temperature rose above or declined below a certain threshold value. In contrast,

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the emission of monoterpenes and sesquiterpenes increased gradually with temperature decreasing

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from 30 to -15°C, and for sesquiterpenes this increase after cold stress was relatively greater than

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after heat stress (Copolovici et al. 2012).

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Aaltonen et al. (2011) observed peaking emissions of mainly monoterpenes from the boreal forest

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floor during early spring and autumn with air temperatures as low as 10°C. A study on VOC

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concentrations in the snowpack of the same forest floor demonstrated that the concentration of

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monoterpenes and sesquiterpenes increased from the atmosphere towards the soil surface


(Aaltonen et al. 2012). While these emissions were suggested to be derived from plant litter

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(Aaltonen et al. 2012), frost-induced plant volatiles provide a potential alternative explanation. Arctic

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evergreen shrubs have been shown to continue to photosynthesise even under snow cover (Starr &

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Oberbauer 2003; Grogan & Jonasson 2006; Larsen et al. 2007), suggesting that plant volatiles may

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also be produced at very low temperatures and when plants are covered with snow. Moreover, as

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the snowpack may contain layers of ice separating the atmosphere from the headspace below, plant

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volatiles can, similarly to CO2 and methane, accumulate in these air pockets and be rapidly released

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to the atmosphere upon snowmelt in spring. To our knowledge, no data exist on this potential

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production and accumulation of VOCs, but Gudleifsson (2009) reported on observations from Iceland

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of strong odour on hayfields upon melting of the ice cover, and suggested that the odour originates

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from plant metabolites from anaerobic respiration (mainly acetate and butyrate) accumulated during

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ice encasement. The odour could also be related to volatiles derived from microbial fermentation

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processes.

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Little is also known about plant volatiles and trophic interactions between the ecosystem

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components in the Arctic, especially those occurring during winter. However, herders have observed

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that the reindeer dig through snow for lichens, their most important winter forage, only on spots

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where the ground under the snow is covered by lichen (Turunen, personal communication),

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suggesting that lichens emit volatiles triggering grazing activity. Further, the reindeer avoid digging

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areas where the lichens are attacked by mould. This observation suggests that volatiles emitted by

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the fungal parasites serve as chemical repellent for the reindeer. Both of these hypotheses on

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significance of volatiles in communication between organisms in the Arctic could be experimentally

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tested.

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Rapid weather changes, like a rapid rise in winter temperatures including melting of the insulating

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snow layer, are likely to become more frequent (Phoenix & Lee 2004). A return to freezing

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temperatures after a winter warming event that allows plants to enter the vegetative stage can

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cause much heavier plant damage than a sustained freezing environment to which plants are 12 This article is protected by copyright. All rights reserved.

physiologically acclimated (Bokhorst et al. 2010). Experiments carried out in the Sub-Arctic have

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shown that a single short winter warming event generated using infrared heaters above a subarctic

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dwarf shrub heath decreased bud production, flowering and berry production in the dominant dwarf

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shrubs, but had no effects on photosynthesis (Bokhorst et al. 2008). In the following summer and

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after repeated winter warming events, plant damage due to the severe stress was obvious, and the

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treatments significantly decreased total isoprenoid emission rates (Ekberg et al. 2011b).

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To summarise, the cold-adapted plant species inhabiting polar regions have relatively high isoprenoid

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emission potentials, but the annual emissions are limited due to the low emitting biomass and the

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short growing seasons. However, significance of processes occurring in winter and especially during

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the shoulder seasons are largely unstudied. The polar regions are experiencing drastic changes in the

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climate and environment, which all lead to potential for increased future emissions of VOCs.

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Desert ecosystems

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Deserts support a relatively low plant biomass, but are nevertheless a potentially high source of VOCs

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due to the high daytime temperatures (Geron et al. 2006) and large surface area covered, ~20% of

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the terrestrial land. By definition, deserts have annual precipitation below 250-300 mm and

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evapotranspiration exceeding precipitation, and hence these habitats are characterized by drought

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stress. General effects of drought stress on isoprene emission have been discussed in detail in many

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papers (e.g. Sharkey & Loreto 1993; Brilli et al. 2007; Fortunati et al. 2008). These papers agree that

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the emission of volatile isoprenoids is resistant to drought stress and may even be stimulated by it,

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before down-regulation due to photosynthesis inhibition. The temporary stimulation of isoprenoid

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biosynthesis in drought-stressed leaves might be caused by low intercellular CO2 concentration

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(Guidolotti et al. 2011). Another emission peak may also be observed when plants are rewatered

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following drought, concurrent with stomatal opening and restored photosynthesis (Sharkey & Loreto

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1993).


Plants from deserts have adapted to life under extreme conditions, involving not only lack of water

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but also extreme temperatures and intense solar radiation. All of these factors in general cause

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oxidative stress, with which plants cope by producing secondary metabolites, such as isoprenoids,

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phenols and alkaloids (Loreto & Schnitzler 2010). We hypothesise that a high production of

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secondary metabolites may also play a role as an adaptive mechanism in some desert plants, e.g. the

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creosote bush (Larrea tridentata), that are known for their strong scent (Jardine et al. 2010), and for

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considerable emissions of isoprenoids (mainly monoterpenes and sesquiterpenes), GLVs and

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oxygenated compounds such as acetaldehyde, ethanol and acetic acid, and many volatiles unusual

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for terrestrial plants (Geron et al. 2006; Matsunaga et al. 2009; Jardine et al. 2010; Jardine et al.

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2012). The latter are discussed in more detail below.

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Among plants adapted to desert conditions, little quantitative work has been done with Cactaceae,

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which for many years had been suggested not to emit any volatiles (Fuentes et al. 2000). However, a

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qualitative assessment of volatile emissions from non-flowering Opuntia stricta (prickly pear cactus),

329

using solid phase micro-extraction fibres and GC-MS analysis, showed that several mono- and

330

sesquiterpenes are emitted by this important cactus, the main volatile being the sesquiterpene β-

331

caryophyllene (Pophof et al. 2005). It appears that several of these compounds function as

332

attractants for the moth Cactoblastis cactorum as they elicited responses in the olfactory receptor

333

cells studied by electroantennography and single sensillum recording techniques (Pophof et al.

334

2005). Also, flowers of the cacti release a variety of floral scents in order to attract pollinators, mainly

335

moths or bats (Kaiser & Tollsten 1995; Raguso et al. 2003a; Raguso et al. 2003b; Schlumpberger &

336

Raguso 2008). The studies mentioned above do not report on isoprene emissions from floral or

337

vegetative organs of cacti.

338 339

Adaptation of isoprenoid emission to high temperature and light

340

Isoprene emission does not appear to be a common trait in deserts (Table S2). Only two out of the 10 14


species in the Mojave and Sonoran Desert screened by Geron et al. (2006) showed isoprene emission

Accepted Article

341 342

capacity: Fremont dalea (Psorothamnus fremontii) and mormon tea (Ephedra nevadensis). However,

343

isoprene emission seems to be common at least in some resurrection plants, the

344

poikilochlorophyllous Xerophyta humilis (Beckett et al. 2012) and the homoiochlorophyllous Talbotia

345

elegans (Loreto, unpublished data). These observations suggest that the trait is independent of the

346

mechanisms that allow resurrection plants to withstand severe drought and to immediately recover

347

when receiving precipitation: poikilochlorophyllous plants namely lose chlorophyll and thylakoids

348

when desiccated and need to re-synthesise them upon hydration, while homoiochlorophyllous plants

349

retain their chlorophyll during desiccation. Isoprene emission from resurrection plants seems rather

350

to be an early protection mechanism against reactive oxygen species formed upon desiccation. When

351

the stress gets severe, however, volatile isoprenoids are replaced by non-volatile antioxidants, such

352

as xanthophylls, which are clearly more effective as protective agents (Beckett et al. 2012). The

353

discovery of isoprene emission in resurrection plants provides evidence that the trait is widespread

354

in many environments and conditions, including arid areas. The search for phylogenetic or

355

phylogeographic patterns linking isoprenoid emitters is complicated (Loreto et al. 2013), but the trait

356

may be more often lost in desert than in temperate species because plants are forced to evolve more

357

robust protective mechanisms, than isoprene emission, against heavy environmental constraints.

358

The temperature-driven increase in isoprene emission from P. fremontii and E. nevadensis continued

359

to temperatures as high as 54°C (Geron et al. 2006) suggesting that isoprene fulfils an important role

360

in lipid membrane stabilization (Velikova et al. 2011) also in plants adapted to high growth

361

temperatures. This observation also suggests that acclimation (i.e. down-regulation) of isoprene

362

emission to high temperatures in boreal species (Fares et al. 2011) may not occur when plants adapt

363

to extremely high temperature conditions. The proportion of assimilated carbon that is invested into

364

isoprene emission by desert plants rises from 1-2% at 30°C to 5-30% at 40°C (Geron et al. 2006).

365

Isoprene emission is light-dependent and does not saturate even at very high light intensities (Loreto

366

& Schnitzler 2010). In the desert, isoprene emission appears to be adapted to even stronger light 15 This article is protected by copyright. All rights reserved.

exposure than in general. Indeed, a decrease in the PPFD from 2000 to 1000 µmol m-2 s-1 decreased

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367 368

isoprene emission from P. fremontii by 40%, a much higher percentage than generally observed in

369

mesophytes from temperate regions (Geron et al. 2006). In contrast, no light dependency was

370

observed for the high monoterpene emissions from the same species, as the emission originated

371

from storage pools instead of de novo synthesis (Geron et al. 2006).

372

Geron et al. (2006) examined how increasing relative humidity from 70% in the branch

373

cuvette in situ affected VOC emissions from plants in the Sonoran Desert. This experimental

374

humidification treatment increased the total monoterpene emissions 2-3-fold without affecting

375

relative amounts of individual compounds. The authors could not show how much of this increase

376

was actually from higher plant emissions under moister conditions and how much was rather due to

377

potentially enhanced recovery efficiency from the sampling and/or analytical system (Geron et al.

378

2006). Theoretically, humidity could positively feed forward on emissions of volatiles in at least two

379

ways: i) by allowing wider stomatal opening, and ii) by swelling and then rupturing structures where

380

volatiles (especially isoprenoids such as monoterpenes and sesquiterpenes) are stored, thus

381

favouring the spill-over of these compounds.

382 383

Emissions of rarely reported biogenic VOCs

384

Matsunaga et al. (2008) studied volatile emissions from eight common desert plants using GC-based

385

techniques and focusing on compounds with high molecular weight (>C15) and/or an oxygenated

386

group. These authors observed that blackbrush (Coleogyne ramosissima), desert willow (Chilopsis

387

linearis), and mesquite (Prosopis glandulosa) released salicylic esters at rates above 1 μg C g−1 h−1.

388

They proposed that the salicylic esters identified as 2-ethylhexenyl salicylate and 3,3,5-

389

trimethylcyclohexenyl salicylate are beneficial for the studied desert plants due to the protection

390

they provide against ultraviolet radiation (Matsunaga et al. 2008). Methyl salicylate is a well-known

391

stress signal compound activating systemic defence responses in plants against biotic and abiotic 16


stress (Rivas-San Vicente & Plasencia 2011). However, accumulation of methyl salicylate may reduce

Accepted Article

392 393

antioxidant protection provided by other secondary metabolites, including volatile isoprenoids, in

394

response to heat stress (Llusià et al. 2005). Thus, it may be hypothesized that formation of salicylic

395

esters in desert plants helps to regulate the presence of methyl salicylate for optimal stress signalling

396

activity.

397

Jardine et al. (2010) measured branch emissions of volatiles from the creosote bush, common in

398

South and North American deserts, using PTR-MS, a more sensitive technique compared to GC-MS,

399

which was used in previous studies (Geron et al. 2006; Papiez et al. 2009). In fact, much higher

400

emissions of isoprenoids, contributing up to a third of the total emissions, and a variety of

401

oxygenated VOC and fatty acid oxygenation products was observed in the midday emissions (Jardine

402

et al. 2010). They also detected a significant 8% contribution by aromatic compounds to the midday

403

biogenic VOC blend (Jardine et al. 2010). Jardine et al. (2010) speculate that the emitted aromatics

404

(benzene, phenol, xylene, benzaldehyde, acetophenone, and 1-chloro-2-methoxybenzene), with a

405

total average noon emission rate of 5.5 μg C gdw−1 h−1, originate from the shikimic acid pathway, also

406

producing flavonoids and lignin. Such emissions of aromatic compounds may get overlooked as they

407

are traditionally considered to be anthropogenic.

408

Emissions of DMS, 1-chloro-2-methoxybenzene and isobutyronitrile have also been found in the

409

creosote bush (Jardine et al. 2010). Dimethyl sulphide is largely emitted by phytoplankton in the

410

oceans (Andreae & Raemdonck 1983; see also below), and so the discovery of a terrestrial source of

411

DMS from desert plants is remarkable. Indeed, the observed DMS emission by creosote bush, at 0.2

412

μg C g−1 h−1, was several orders of magnitude higher than previous estimates for terrestrial plants.

413

DMS is the main natural source of reduced sulphur released to the atmosphere (Bates et al. 1987;

414

Kettle & Andreae 2000). Despite controversy about its function in a negative feedback mechanism to

415

global warming (Quinn & Bates 2011), the atmospheric oxidation products of DMS play a major role

416

in the formation of clouds, cloud albedo and thus in the regulation of global climate (Charlson et al.

417

1987; Simó 2001). 17 This article is protected by copyright. All rights reserved.

Flowers of some Cactaceae have been observed to release a peculiar volatile, a mould and earth-

Accepted Article

418 419

smelling dehydrogeosmin (DHG), and this flower scent is unique to Cactaceae (Kaiser & Nussbaumer

420

1990; Schlumpberger et al. 2004). Floral emission of DHG has been found in 55 cactus species from

421

seven genera, and it follows a clear diurnal rhythm suggesting that it has an ecological function in

422

attraction of floral visitors (Schlumpberger et al. 2004). As elsewhere, volatiles also function in plant-

423

plant communication in deserts. For instance, it has been suggested that volatile communication

424

between the root systems of Ambrosia and Larrea controls distribution and competition of these

425

desert shrubs (Mahall & Callaway 1991).

426

In summary, the limited data on VOC emissions from desert vegetation suggest that – in addition to

427

mono- and sesquiterpenes (and for some species isoprene) – desert plants may emit a range of

428

unusual VOCs whose biochemical origin, and physiological role remains to be elucidated, but which

429

can largely contribute to ecological adaptation and biosphere-atmosphere interactions in the desert

430

environment. The lack of data prevents us from properly addressing the first question presented in

431

the introduction, i.e. the VOC emission potential of desert plants relative to other plants. Although

432

(or perhaps because of) living in one of the most extreme environments on earth, desert plants

433

appear resilient to the predicted changes in precipitation (decrease in many areas) and CO2

434

concentration (Tielbörger & Salguero-Gómez 2014). However, it is not known how climate change

435

affects VOC emissions from these plants. Moreover, differences in emission rates between dry and

436

wet seasons remain to be elucidated.

437 438

CO2 springs

439

Natural CO2 springs are among the most extreme environments on earth, as the CO2 concentration

440

inside the craters from where the CO2 is released reaches – in the absence of air movement - super-

441

high concentrations and makes the surrounding environment anoxic (Scholefield et al. 2004).


Vegetation growing in the vicinity of these environments has developed under permanent high CO2

Accepted Article

442 443

enrichment and provides an interesting possibility for studies assessing effects of CO2 on vegetation.

444

Super-high CO2 concentration has been shown to have a dramatically negative effect on isoprene

445

emission by stands of Phragmites australis living inside the CO2 spring craters (Scholefield et al.

446

2004). This finding is in agreement with the surprising but repeatedly observed effect of elevated CO2

447

inhibiting isoprene emission by plants. Indeed, it could be expected that rising CO2, allowing for

448

higher photosynthesis, would also increase emissions of those isoprenoids that are directly formed

449

during carbon fixation. However, isoprene production appears to be limited by insufficient supply of

450

phosphoenolpyruvate (Loreto et al. 2007) or other substrates that are also used by competing

451

respiratory processes (Rosenstiel et al. 2003). Emission of monoterpenes was similar in mature holm

452

oak (Quercus ilex L.) growing around natural CO2 springs at CO2 concentration of 400 and 1500 µmol

453

mol-1 (Rapparini et al. 2004), showing that lifetime exposure to high CO2 did not affect the emission

454

of isoprenoids other than isoprene.

455 456

Flooded environments

457

When excess water poses a stress for the prevailing vegetation, flooded systems can also be

458

considered extreme environments. Water-logged soils are anoxic, and as plants are aerobic

459

organisms, they become stressed and typically initiate fermentative processes (for a recent review,

460

see Kreuzwieser & Rennenberg 2013). Alcoholic fermentation produces ethanol, and both ethanol

461

and its oxidation product acetaldehyde, and in lesser quantities acetic acid, are emitted from flooded

462

trees (Kreuzwieser & Rennenberg 2013 and references therein). Emissions of nitric oxide, GLVs and

463

methanol have also been reported to be induced by waterlogging of the root systems (Copolovici &

464

Niinemets 2010). Flooding with saline water also causes transient increases of emissions of several

465

volatile isoprenoids in Citrus leaves, especially limonene (Velikova et al. 2012). Once again, the

466

induction of volatile isoprenoids in response to flooding indicates that these compounds are 19


important in signalling stress responses, possibly directly protecting plants from stressors (Loreto and

Accepted Article

467 468

Schnitzler 2010).

469

In the following, we focus on volatile emissions from natural ecosystems characterized by high or

470

fluctuating water table, such as wetlands or the intertidal zone including mangroves and salt

471

marshes, where the plant species are adapted to the flooded conditions. Here, the fluctuations in the

472

conditions or a decline in the water table depth - rather than constantly flooded conditions – could

473

pose a stress on the vegetation.

474

Sedges and grasses like Carex spp., Arundo spp. and Eriophorum spp. have developed aerenchyma in

475

their roots and shoots, in order to conduct air into their rhizosphere (Schütz et al. 1991), and the

476

gases produced in the rhizosphere have a fast transport route to the atmosphere using the same

477

channel (Joabsson et al. 1999). The gases produced include methane and also other VOCs (Faubert et

478

al. 2010b; Faubert et al. 2011). It is likely that the abundance of aerenchymatous plants thus affects

479

the net emission of VOCs produced in the root zone both by plants, soil microorganisms and possible

480

chemical reactions producing volatile intermediates. This is because the compounds transported via

481

plants bypass the microbial consumption processes in the soil which could occur when transported

482

to the atmosphere via diffusion (Joabsson et al. 1999).

483

A considerable part of the arctic and boreal regions is covered by wetlands, where the plants are

484

adapted to growth in the waterlogged soil. Wetland plants, such as sedges and mosses, are isoprene

485

emitters (Table S1; Hanson et al. 1999; Tiiva et al. 2007a; Tiiva et al. 2007b; Ekberg et al. 2009;

486

Ekberg et al. 2011a; Loreto et al. 2013), and significant emissions of methanol, acetaldehyde and

487

acetone have also been detected (Holst et al. 2010). As noted above, the release of these low

488

molecular weight compounds may be related to the stress caused by flooding (Copolovici &

489

Niinemets 2010; Kreuzwieser & Rennenberg 2013), but here it is more likely that they originate from

490

microbial fermentation in anaerobic peat, and are only transported through the sedges, which

491

maintain sufficient oxygen concentrations in their roots with the help of aerenchyma. On the other 20


hand, the emission of isoprene is plant-related and constitutive, which raises the question of why this

Accepted Article

492 493

trait is so largely diffused in plants living at the interface with water (Loreto et al. 2013).

494

Using automated chambers over three growing seasons in the same location as Holst et al. (2010),

495

Bäckstrand et al. (2008) monitored total non-methane hydrocarbon emissions from a subarctic

496

wetland using a Total Hydrocarbon Analyzer and subtracted manually measured methane emissions

497

from the flux. The total non-methane hydrocarbon emissions were lowest from the dry palsa

498

(hummock) vegetation (2.25 mg C m−2 day−1) and clearly higher from wet surfaces: 6.7 mg C m−2 day−1

499

from Sphagnum lawn and 18.6 mg C m−2 day−1 from Eriophorum lawn (Bäckstrand et al. 2008). These

500

data lend further evidence to the suggested role of sedges (Eriophorum spp.) in both production and

501

transport of volatiles to the atmosphere, but the relative significance of these two roles cannot be

502

separated.

503

Mangrove plants are specialised to growing in the tidal coasts of the Tropics and Subtropics, and they

504

cover about 5% of the forest areas of the world (Patra & Thatoi 2011). Despite their traditional

505

medicinal use due to the anti-microbial, -viral, -oxidant etc. properties in the leaf phytochemicals

506

(Patra & Thatoi 2011), surprisingly little is known about VOC emissions from mangrove plants. Red

507

mangrove (Rhizophora mangle L.) has been shown to emit isoprene and monoterpenes (Barr et al.

508

2003). The detected monoterpenes were reported to originate from mangrove flowers (Barr et al.

509

2003), which in general emit a wide range of floral scents typical for other angiosperms (Azuma et al.

510

2002). Volatiles from several mangrove species have been observed to reduce germination and

511

growth of other species (Chen & Peng 2008; Li et al. 2010). Basyuni et al. (2009) observed a positive

512

correlation between salinity levels and mRNA level of terpenoid synthase in the roots of the

513

halophytic Kandelia candel and Bruguiera gymnorrhiza, and in the leaves of K. candel, which suggests

514

that salinity levels rather than waterlogging affect isoprenoid emissions from these halophytes.

515

Similarly, salt marsh plants have been largely overlooked as a source of VOC. Most evidence points

516

towards vegetated salt marsh acting as a source of methyl halides (see Rhew & Mazéas 2010), and 21


similar observation has been made regarding a boreal coastal meadow dominated by the halophyte

Accepted Article

517 518

Salicornia europaea (Valtanen et al. 2009). Furthermore, the breakdown of high levels of

519

dimethylsulphoniopropionate (DMSP) in Spartina alterniflora (Otte et al. 2004), for example, results

520

in DMS release from salt marshes (Steudler & Peterson 1984; Yoch 2002). Molecular genetic

521

evidence suggests that DMS is primarily a product of microbial degradation of (usually) phototroph-

522

derived DMSP (Johnston et al. 2008). Eugenia copacabanensis Kiaersk. (Myrtaceae), a Brazilian salt

523

marsh plant, has been shown to be rich in monoterpenes, which are located in the oil secretory

524

cavities in the mesophyll (Arruda & Victório 2011), but to our knowledge isoprenoid fluxes have not

525

been investigated in salt marshes.

526 527

MARINE EXTREME ENVIRONMENTS

528

Marine environments are a source of numerous trace gases that have been studied for their impact

529

on atmospheric processes and climate (Carpenter et al. 2012), sensitivity to increasing CO2 and

530

warming (Hopkins et al. 2010; Arnold et al. 2013), their possible ecological roles as infochemicals

531

(Steinke et al. 2002; Pohnert et al. 2007) and their function in the stress physiology of aquatic

532

phototrophs (Sunda et al. 2002; Husband et al. 2012). Particular focus has been on non-methane

533

hydrocarbons including isoprene, halocarbons and DMS (Carpenter et al. 2012), and, over the last 25

534

years, research on DMS has stimulated the ongoing debate about its role in climate regulation via

535

oceanic phytoplankton sulphur emissions (Charlson et al. 1987; Quinn & Bates 2011).

536

Although DMS production has been documented in terrestrial plants (see above; Jardine et al. 2010),

537

its major source is the ocean (Andreae & Raemdonck 1983). Correspondingly, almost all marine

538

micro- and macro-algae tested to date emit isoprene (see Broadgate et al. 2004; Shaw et al. 2010;

539

Exton et al. 2013), but in contrast to many terrestrial plants, only a very small fraction of

540

photosynthate from marine microalgae is converted to isoprene (Shaw et al. 2003). This results in the

541

clearly differentiated pattern of high isoprene production on the continents and high DMS 22


production in the oceans. However, it remains to be seen whether this is because DMS or other

Accepted Article

542 543

compounds serve the same role in microalgae as isoprene does in terrestrial plants, or due to the

544

buffering by water of changes in temperature and reactive oxygen species impacts, which would

545

reduce the demand for isoprene’s protective effects in the marine environment. Furthermore, data

546

on oceanic isoprene are scarce so that great uncertainty exists over net marine isoprene emissions,

547

with estimates ranging from 0.1-11.6 Tg C y-1 (Milne et al. 1995; Palmer & Shaw 2005; Gantt et al.

548

2009; Luo and Yu 2010), which may be 50% higher if models account for sea surface temperature

549

(Exton et al. 2013).

550 551

Ice-algal communities

552

Brine channels in annual and multi-year sea ice are important habitats for ice-algal communities and

553

provide much of the seasonal primary productivity in polar waters (Arrigo 2003). It is likely that the

554

melting of sea ice in a warming climate will increase primary productivity and the production of

555

selected VOCs in the Arctic (Levasseur 2013). Current estimates for the total primary production in

556

the Antarctic Seasonal Ice Zone (SIZ) suggest that the contribution of sea-ice algae ranges from 1% in

557

February to 10% in October with highest contribution of 35% by sea-ice algae in the Indian sector of

558

the SIZ (Lizotte 2001).

559

These communities are adapted to extreme salinities by the intracellular accumulation of

560

osmoprotectants or compatible solutes that counteract the high extracellular concentrations of NaCl

561

that can exceed 1.7 M equivalent to a three-fold increase in seawater salinity (Kirst 1990). Sea-ice

562

diatoms accumulate high concentrations of the compatible solute DMSP, the main precursor of DMS,

563

and high concentrations of DMSP have been reported for the bottom of the sea ice (15,000 nM;

564

Levasseur 2013). Hence, it is not surprising that, in comparison to the global ocean concentration

565

range of DMS (1 to 7 nM; Lana et al. 2011), sea-ice environments are a rich source of DMS ranging in

566

maximum concentrations from 22 nM at the ice edge to 2,000 nM in sea ice (Leck & Persson 1996; 23


Levasseur 2013). As a result, high latitude areas contribute significantly to the total sea-to-air flux of

Accepted Article

567 568

DMS that is estimated at 54.5 Tg DMS per year (Lana et al. 2011) and future warming may further

569

increase DMS production and emission as seasonal sea-ice cover recedes (Levasseur 2013).

570

Little information exists on production of other VOCs by sea-ice communities. Exton et al. (2013)

571

found that isoprene production is significantly lower in three species of sea-ice diatoms (0.03±0.01

572

μmol [g Chl a]-1 h-1) in comparison to 10 different strains from temperate and tropical environments

573

(0.31±0.06 and 0.75±0.1 μmol [g Chl a]-1 h-1, respectively). However, the often high biomass in sea-ice

574

brine channels can still produce considerable amounts of VOCs that lead to increased under-ice

575

concentrations, which become available for sea-air transfer upon ice melt in spring/summer (e.g.

576

bromoform: Nomura et al. 2011).

577 578

Tidal rockpools, estuaries and hypersaline environments

579

Unusually high DMS production has been shown in hypersaline environments in addition to sea ice,

580

such as soda-lake microbial mats (Visscher et al. 1996), Antarctic lakes (Gibson et al. 1991) and the

581

inland Salton Sea (salinity of 4.8%), which is also eutrophic and has an average surface DMS

582

concentration of 2,500 nM with a maximum of 11,000 nM corresponding with high algal biomass

583

(Reese & Anderson 2009). Thus, there is a clear correlation with salinity, production of DMSP as, inter

584

alia, an osmoprotectant, and DMS release from microbial degradation of DMSP.

585

The intertidal zone experiences large fluctuations in salinity, and rockpool and mudflat communities

586

living in this zone are further exposed to extremes in temperature, light and water availability.

587

Broadgate et al. (2004) investigated the hydrocarbon production profiles in temperate seaweeds and

588

rockpools, and estimated the flux of selected alkanes and alkenes (ethane, ethene, propane,

589

propene, i-butene, n-pentane, isoprene) ranging on average from 0.08 μg m-2 h-1 for propane and n-

590

pentane to 0.43 and 0.93 µg m-2 h-1 for ethene and isoprene in September-October. Exton et al.


(2012) investigated isoprene production from the almost freshwater head to the marine mouth of a

Accepted Article

591 592

temperate estuary over the course of a year, and found that sediment isoprene emissions, most

593

likely from benthic diatoms, correlated with light and temperature (Exton et al. 2012). Higher

594

concentrations of isoprene in waters at the lower-salinity head of the estuary were due to the higher

595

sediment-surface-area to water-volume ratio rather than any influence of salinity, supported by the

596

observations that there was an increase in water isoprene concentration at low tide and no spatial

597

variation in sediment production (Exton et al. 2012).

598

The impact of extremely high salinities on isoprene concentration was tested in brines from a saltern

599

in Mallorca, and no significant difference between samples at 4, 15 and 23% salinity was found

600

(Exton, Steinke & McGenity, unpublished data; Fig. 3). However, the isoprene concentrations were

601

high, approximating those found at the head of the aforementioned estuary (Exton et al. 2012). The

602

dominant phototrophs in such high-salinity ponds are Dunaliella salina and related members of this

603

chlorophyte genus, while in the sediment, cyanobacteria like Aphanothece sp. tend to dominate (see

604

McGenity & Oren 2012). Based on known production by related species (Exton et al. 2013) they are

605

the most likely source of isoprene, but contributions from the abundant heterotrophic haloarchaea

606

and other microbes cannot be discounted. Also, whether these halophiles produce isoprene to

607

protect against high salinity and associated environmental stresses, such as high ultraviolet radiation,

608

remains to be elucidated.

609

Thus, isoprene production is high at extreme salinities, and given the global abundance of

610

hypersaline environments, particularly vast inland salt pans, they should be considered in regional

611

isoprene budgets. Similarly, the contribution of hypersaline environments to emissions of other VOCs

612

may be globally significant; the aforementioned inland Salton Sea (980 km2), for example, releases as

613

much DMS annually as an area of the ocean equivalent in size to the Bering Sea (800,000 km2; Kiel et

614

al. 2009).

615


CONCLUSIONS

Accepted Article

616 617

Based on our synthesis, plants and photosynthetic aquatic organisms living in extreme environments

618

appear to have high VOC emission potentials (e.g. plants from arctic ecosystems) or high emissions

619

under their living conditions (e.g. desert plants, ice-algal communities or phototrophs from

620

hypersaline areas). The plant biomass of extreme terrestrial environments, such as tundra and

621

deserts, is relatively low, but taking into account the large surface area covered (tundra ~5.6 and

622

deserts ~27.7 million km2), the emissions from these areas have to be considered in the global

623

budgets of biogenic volatiles. Moreover, the volatile emission, especially that of DMS, from coastal

624

areas (e.g. salt marshes and mangroves) and marine extreme environments discussed here are

625

sufficiently high to affect global budgets.

626

The reason for widespread VOC, especially isoprenoid, emissions from different extreme

627

environments deserves to be studied further, as these compounds may have important functions in

628

adaptation to extremes and in driving organismic relationships in environments subjected to rapid

629

and strong climate changes. Moreover, our current understanding of VOC emissions from extreme

630

environments is scarce, and there are still high uncertainties in the emission rates. The current data

631

are limited both in space and time, and measurements covering longer time periods also outside of

632

the peak growth period are required.

633

The net VOC emissions measured at ecosystem level are a balance between the actual gross

634

emissions and the ecosystem/atmospheric uptake. VOCs can be consumed at different rates

635

depending on the structure of the molecule, its volatility, reactivity, quantity, and the pathway from

636

source to the atmosphere. The consumption of VOCs in soils, sediments and aqueous environments,

637

in which diffusion is retarded, is likely to be more significant than on the leaf surface, and especially

638

significant in many of the extreme environments that we have highlighted. For example, most of the

639

marine DMS is likely fuelling heterotrophic processes in the sea with only about 10% escaping to the

640

atmosphere (Kiene & Bates 1990). The abundance of methylotrophs on most leaf surfaces (Knief et 26


al. 2010) is testament to the plants’ supply, and the relatively low volatility, of methanol. However,

Accepted Article

641 642

microbial consumption of the more volatile isoprene, although demonstrated in soils (Cleveland &

643

Yavitt 1998) and estuarine waters and sediments (Acuña Alvarez et al. 2009), has not to our

644

knowledge been examined on the phyllosphere, although uptake of oxidation products of isoprene

645

by vegetation has been demonstrated (Karl et al. 2010).

646

Finally, extreme environments may represent a future major source of volatiles in a warming

647

atmosphere. Rising global temperature will provide direct (e.g. increased volatility of gaseous

648

compounds) and indirect (e.g. vegetation changes) effects that are likely to augment the contribution

649

of extreme environments to the global VOC budget. Whether the temperature effect is partially

650

balanced by the inhibitory effect of rising CO2, as predicted in more temperate environments at least

651

for isoprene (Arneth et al. 2008), remains to be assessed.

652 653

ACKNOWLEDGMENTS

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We would like to thank Prof. Christian Körner for insightful discussion on plant stress responses and

655

two anonymous reviewers for constructive comments on a previous version of this manuscript. R.R.

656

would like to acknowledge the financial support from the Danish Council for Independent Research |

657

Natural Sciences, the Villum Foundation, Maj and Tor Nessling Foundation, and the Danish National

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Research Foundation for supporting the activities within the Center for Permafrost (CENPERM

659

DNRF100). T.J.M. and M.S. were supported by a research grant from the UK Natural Environment

660

Research Council (NE/J009555/1) and M.S. also through a grant (NE/H009485/1). F.L. acknowledges

661

the support from the The European Commission FP7-KBBE project “Development of improved

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perennial non-food biomass and bio-product crops for water stressed environments” (WATBIO); the

663

European Commission FP7-Environment project ”Effects of Climate Change on Air Pollution and

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Response Strategies for European Ecosystems (ECLAIRE); and the European Science Foundation -

665

EUROCORES project “Molecular and metabolic bases of isoprenoid emissions (EuroVOL-MOMEVIP). 27


Minna Kivimäenpää and Hanna Valolahti are thanked for providing the photographs of Cassiope

Accepted Article

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tetragona and Daniel Exton for data presented in Fig. 3, and Balbina Nogales, Rafael Bosch and

668

Ramon Rosselló-Móra for support with sampling.

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potential methanogenic substrate in Mono Lake sediments. In Biological and Environmental

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Figure legends

Accepted Article

1077 1078

Fig. 1. Surface structures of a Cassiope tetragona leaf. (a) A scanning electron micrograph showing a

1079

deeply grooved leaf covered by spiky and flat trichomes. (b) A light micrograph showing a cross

1080

section of a part of the leaf including flat trichomes (arrows). Photographs courtesy of Hanna

1081

Valolahti and Minna Kivimäenpää.

1082

Fig. 2. Schematic overview of effects of climate warming on the emissions of isoprene, monoterpenes

1083

(MT) and sesquiterpenes (SQT) from the arctic tundra. Temperature increase has direct positive

1084

effect on the volatile emissions but it also accelerates permafrost thaw and nutrient mineralization

1085

and thereby availability in soil. Upon permafrost thaw, greenhouse gases trapped in the frozen soil

1086

are released feeding back on climate warming. Temperature increase, permafrost thaw and

1087

increased nutrient availability all increase plant biomass, which in turn decreases albedo and thereby

1088

reinforces warming. The increase of graminoids, aspen and willows is likely to increase isoprene

1089

emissions and that of shrubs and birch monoterpene and sesquiterpene emissions.

1090

Fig. 3. Isoprene concentration (mean ± SE, n = 3) in saltern ponds of Salinas de S’Avall, Mallorca,

1091

(39°19´26.38N 2°59´21.14E) plotted against salinity (Exton, Steinke & McGenity, unpublished data).

1092

Salinity was measured with a hand-held refractometer. The 4% salinity sample was from a channel

1093

bringing seawater into the saltern while the higher salinity samples were from evaporation ponds

1094

that were coloured red. Samples were placed in 120-ml serum bottles filled to the brim, and sealed

1095

with a PTFE-lined butyl rubber stopper, cooled to 4°C and transported on ice, before isoprene

1096

measurement the next day using the method of Exton et al. (2012). There was no significant

1097

difference (1-way Anova) between samples. For comparison, the upper dotted line shows the

1098

average, low-tide isoprene concentration for the head of the Colne Estuary, U.K. (194.3 pmol l-1), and

1099

the lower dotted line shows the same information for the mouth of the Colne Estuary (56 pmol l-1);

1100

the latter representing typical seawater concentrations (Exton et al. 2012).


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1101 1102

FIGURES

1103

1104 1105

Fig. 1


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1107 1108 1109

Fig. 2

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Fig. 3


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