IN PLANT NUTRITION ‘Breath figures’ on leaf surfaces – formation and effects of microscopic leaf wetness Jürgen Burkhardt and Mauricio Hunsche Journal Name: Frontiers in Plant Science ISSN: 1664-462X Article type: Hypothesis & Theory Article Received on: 01 Jul 2013 Accepted on: 04 Oct 2013 Provisional PDF published on: 04 Oct 2013 Frontiers website link: www.frontiersin.org Citation: Burkhardt J and Hunsche M(2013) ‘Breath figures’ on leaf surfaces – formation and effects of microscopic leaf wetness 4:422 doi:10.3389/fpls.2013.00422 Article URL: http://www.frontiersin.org/Journal/Abstract.aspx?s=1220& name=plant%20nutrition&ART_DOI=10.3389/fpls.2013.00422 (If clicking on the link doesn't work, try copying and pasting it into your browser.) Copyright statement: © 2013 Burkhardt and Hunsche This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice No use, distribution or reproduction is permitted which does not comply with these terms This Provisional PDF corresponds to the article as it appeared upon acceptance, after rigorous peer-review Fully formatted PDF and full text (HTML) versions will be made available soon 1 1 ‘Breath figures’ on leaf surfaces – formation and effects of 2 microscopic leaf wetness 3 Juergen Burkhardt1 & M Hunsche2 4 5 6 Revision 7 8 9 10 11 University of Bonn, Karlrobert-Kreiten-Str 13 12 D-53115 Bonn, Germany Institute of Crop Science and Resource Conservation, Plant Nutrition Group 13 14 15 University of Bonn, Auf dem Hügel 16 D-53121 Bonn, Germany Institute of Crop Science and Resource Conservation, Horticultural Science Group 17 18 Corresponding author: 19 Juergen Burkhardt, Tel +49 228 732186, email: j.burkhardt@uni-bonn.de, 20 21 22 Submitted to Frontiers in Plant Nutrition 2 23 Abstract 24 ‘Microscopic leaf wetness’ means minute amounts of persistent liquid water on leaf surfaces which are 25 invisible to the naked eye The water is mainly maintained by transpired water vapor condensing onto 26 the leaf surface and to attached leaf surface particles With an estimated average thickness of less than 27 µm, microscopic leaf wetness it is about orders of magnitude thinner than morning dewfall 28 The most important physical processes which reduce the saturation vapor pressure and promote 29 condensation are cuticular absorption and the deliquescence of hygroscopic leaf surface particles 30 Deliquescent salts form highly concentrated solutions Depending on the amount and concentration of 31 the dissolved ions, the physicochemical properties of microscopic leaf wetness can be considerably 32 different from those of pure water Microscopic leaf wetness can form continuous thin layers on 33 hydrophobic leaf surfaces and in specific cases can act similar to surfactants, enabling a strong 34 potential influence on the foliar exchange of ions Microscopic leaf wetness can also enhance the 35 dissolution, the emission, and the reaction of specific atmospheric trace gases e.g ammonia, SO2, or 36 ozone, leading to a strong potential role for microscopic leaf wetness in plant/atmosphere interaction 37 Due to its difficult detection, there is little knowledge about the occurrence and the properties of 38 microscopic leaf wetness However, based on the existing evidence and on physicochemical reasoning 39 it can be hypothesized that microscopic leaf wetness occurs on almost any plant worldwide and often 40 permanently, and that it significantly influences the exchange processes of the leaf surface with its 41 neighboring compartments, i.e., the plant interior and the atmosphere The omission of microscopic 42 water in general leaf wetness concepts has caused far-reaching, misleading conclusions in the past 43 44 Keywords: 45 aerosols, cloud condensation nuclei, contact angle, deliquescence point, dew, foliar nutrition, 46 Hofmeister series, leaf surfaces, leaf boundary layer, plant-atmosphere interaction, surface tension, 47 stomatal uptake 3 48 Abbreviations AMS: ammonium sulphate, CET: Central European Time, DRH: deliquescence 49 relative humidity, ESEM: environmental scanning electron microscope, HAS: hydraulic activation of 50 stomata, LBL: Leaf boundary layer, PAR: photosynthetically active radiation, RH: relative humidity, 51 RHs: relative humidity at the leaf surface, SEM: scanning electron microscopy 52 53 54 55 56 57 58 59 60 61 62 63 64 65 4 66 Introduction 67 ‘Breath figures‘ is a term used in material science to describe the condensation as well as the linked 68 wetting and dewetting processes on different kinds of surfaces (Blaschke et al., 2012) The 69 examination of breath figures has then been used as a method to characterize the degree of 70 contamination on an otherwise homogenous surface (Kumar and Whitesides, 1994) The term was 71 originally introduced by Aitken (1914) who noticed that water from exhaled breath condensing to 72 clean glass surfaces was clearly visible as separate droplets If the glass was contaminated with fine 73 particles, however, the condensation would be strong but not visible, due to the formation of thin 74 water films (Aitken, 1911) Condensation to deposited particles (‘contaminants’) is also considered an 75 essential factor in corrosion, and according to ISO 9223 wetting happens at 80% RH and above due to 76 particle hygroscopicity (Schindelholz and Kelly, 2012) 77 In plant science, the influence of particles on condensation has not been considered sufficiently so far 78 On leaf surfaces, the commonly known form of condensation is morning dewfall It develops during 79 clear, calm nights, when plant surfaces cool down by radiational heat loss, and the surface temperature 80 eventually reaches the dew point of the surrounding air According to this common meteorological 81 definition, dew formation thus starts when 100% relative humidity (RH) is reached at the actual leaf 82 surface temperature, which normally means about 90% RH of the surrounding air (Monteith, 1957) It 83 is usually neglected that the initiation of condensation on leaf surfaces likely starts on condensation 84 nuclei, analogously to atmospheric cloud formation (Beysens, 1995) These nuclei are tiny 85 hygroscopic particles, which are present on all kinds of leaf surfaces They result from atmospheric 86 dry deposition of aerosols or residues from evaporated rain droplets, while removal by rain is never 87 complete (Neinhuis and Barthlott, 1998; Freer-Smith et al., 2005) Almost all aerosols are (partly) 88 hygroscopic (Pöschl, 2005) and therefore cause a local reduction of the saturation vapor pressure 89 Even the commonly used expression ‘dry deposition’ for aerosols is usually misleading, because many 90 of the deposited substances become deliquescent at higher humidities (e.g., 75 % RH for a NaCl 5 91 particle) Equilibration with the surrounding RH happens very quickly (Pilinis et al., 1989) and many 92 particles will therefore reach a transpiring leaf surface in deliquescent form 93 Neglecting particle deliquescence can cause misleading conclusions An example is the ‘wax 94 degradation’ phenomenon that was frequently found on conifer needles which were affected by air 95 pollution caused forest decline The phenomenon was intensively investigated in the 1980s and 90s, 96 but the investigations concentrated on the chemical composition of the waxes and could not explain 97 the development of the phenomenon However, the characteristic, amorphous appearance of 98 epicuticular waxes can also be produced in a simple way by deliquescent particles covering the 99 structures of the epicuticular waxes This alternative explanation was suggested recently (Burkhardt, 100 2010) and its capability to explain the phenomenon was meanwhile demonstrated by experiment 101 (Burkhardt and Pariyar, 2013) Because the minimum epidermal conductance gmin, a key factor of tree 102 drought tolerance, was also reduced by salt particles, and given the fact that particle accumulation on 103 conifers can reach the amount of leaf waxes (up to more than 50 µg cm-2, Saebo et al., 2012), a direct 104 link between particulate air pollution and drought symptoms of conifers might exist, with ‘wax 105 degradation’ as an indication of particle load (Burkhardt and Pariyar, 2013) 106 The second neglected factor for the formation of leaf wetness is foliar (mainly stomatal) transpiration 107 In the common definition of dewfall, the main source of water vapor for dew formation on plants is 108 the surrounding atmosphere, with an eventual contribution by ‘distillation’ from the soil (Monteith, 109 1957) On leaf surfaces, however, foliar transpiration is an additional water vapor source The leaf 110 boundary layer is humidified by this water vapor, leading to high water vapor concentration especially 111 at the leaf surface (Schuepp, 1993; Roth-Nebelsick, 2007), which together with hygroscopic 112 substances will lead to the formation of microscopic leaf wetness (Burkhardt and Eiden, 1994; 113 Burkhardt et al., 1999) Although this process only involves small amounts of water, it might 114 considerably change the transport between the leaf surface and the neighboring compartments, which 115 is supported by the dependence of trace gas deposition on RH: For easily soluble compounds like NH3 116 and SO2, increasing trace gas deposition to cuticular surfaces (‘non-stomatal fluxes’) was already 117 found for 70% RH (van Hove et al., 1989;Burkhardt and Eiden, 1994;Wichink Kruit et al., 2008) The 6 118 trace gas deposition to microscopic leaf wetness is also dependent on the chemical composition of the 119 water, e.g on pH or on leached manganese ions catalyzing SO2 oxidation (Burkhardt and Drechsel, 120 1997) Non-stomatal deposition is also significant for ozone, making up between 1/3 and 2/3 of total 121 deposition (Coyle et al., 2009;Fowler et al., 2009; Launiainen et al., 2013) A positive relation of 122 ozone deposition with relative humidity was also found (Pleijel et al., 1995, Altimir et al., 2006 123 Lamaud et al., 2009) 124 Foliar fertilization is a complicated process with foliar uptake being the first decisive step (Fernandez 125 and Brow, 2013) Continuing microscopic leaf wetness might contribute considerably to the foliar 126 exchange of ions When dilute solutions are applied, the highest uptake rates into leaves occur during 127 the drying phase, presumably as a consequence of increasing concentrations (Eichert and Burkhardt, 128 2001) The high concentrations of electrolytes in deliquescent particles are expected to promote the 129 gradient dependent exchange process across the leaf surface, and maintenance of high concentrations 130 would therefore lead to high transport rates 131 Macroscopic leaf wetness, i.e visible wetting of leaves, usually has a large influence on the 132 phyllosphere For phyllospheric organisms, water is a key issue to survive (Beattie, 2011; Vorholt, 133 2012) The amount of water needed depends on the organism but usually ‘free water’ (probably 134 meaning visible water) is required by phyllospheric organisms like fungi, bacteria or insects and thus 135 fosters phyllospheric life including plant pathogens (Huber and Gillespie, 1992) Microscopic leaf 136 wetness might also influence the phyllosphere to a certain degree, but cannot be treated here in depth 137 The aim of this contribution is to elucidate the mechanisms and conditions by which microscopic leaf 138 wetness is formed and maintained So far there have only been isolated reports and phenomenological 139 descriptions, while an integrated view and a general concept detailing the occurrence and the functions 140 of microscopic liquid water at the plant/atmosphere interface is missing 141 142 7 143 Detection of microscopic leaf wetness 144 The most common method to determine (macroscopic) leaf wetness duration is the electrical resistance 145 measurement of artificial leaves A continuous resistance signal is produced, which is divided into 146 ‘wet’ or ‘dry’ by defining a resistance threshold, based on the visual observation of wetness (Gillespie 147 and Kidd, 1978;Fuentes and Gillespie, 1992;Huber and Gillespie, 1992;Armstrong et al., 148 1993;Sentelhas et al., 2007) For the detection of microscopic leaf wetness, a similar electronic device 149 can be used, but the sensors to measure the electric resistance are directly attached to the leaf surface 150 (Burkhardt and Gerchau, 1994) The signal is then compared to ambient RH (Burkhardt and Eiden, 151 1994), or to the signal of a commercial leaf wetness sensor, i.e an artificial leaf An example for the 152 latter procedure is shown in Figure The electrical conductance on potato leaves was measured in 153 Southern Germany during a hot summer week, and was compared to the continuous signal of an 154 artificial leaf sensor (237 Leaf Wetness Sensing Grid, Campbell Scientific, Logan, UT, USA) which 155 was installed in close proximity Photosynthetically active radiation (PAR) and ambient relative 156 humidity (RH) data were obtained from a weather station on the same field For both wetness sensors, 157 the nighttime increase is clearly visible and goes parallel with each other, with a significant decrease 158 of resistance starting at about 60 to 70% RH of the surrounding air During daytime, a different course 159 of the signals is observed, with the sensor on the potato leaves showing a regular increase in the 160 mornings, which is missing on the artificial leaf 161 162 Insert Fig here 163 164 Because the leaf wetness signal is highly correlated with PAR, it is most probably the consequence of 165 changing stomatal conductance, where transpired water coming from the stomata re-condenses on the 166 leaf surface This interpretation is supported by the results of a detailed study under completely 167 controlled conditions using the same type of leaf wetness sensors on bean leaves Under constant 8 168 humidity and by changing light or changing CO2 concentration was the electrical leaf surface 169 conductance closely correlated with stomatal conductance (Burkhardt et al., 1999) These results 170 indicate that microscopic water can exist on leaf surfaces for extended times, even under hot, dry 171 summertime conditions, and that the liquid water therefore is in an equilibrium state, reacting quickly 172 to increased transpiration by the formation of more liquid water, and by a reduction of the water 173 amount when the stomata close This phenomenon can be explained by two processes One is the leaf 174 transpiration which creates a humid leaf boundary layer (LBL) including the proper leaf surface 175 During times of open stomata, leaf surface humidity (RHs) will mostly be determined by transpiration, 176 with only limited influence by ambient RH The distribution of leaf surface humidity is heterogeneous 177 and will especially be high near to stomata (Schuepp, 1993;Roth-Nebelsick, 2007).The second process 178 is a local reduction of the saturation vapor pressure by effects of the leaf surface material (sorption by 179 the cuticle, deliquescence of hygrocopic leaf surface particles), or geometry (capillary condensation), 180 which will be discussed in more detail within the next section As also calculated in the next section, 181 the hypothetical homogenous thickness of the liquid water is less than µm This small amount of 182 water is not visible and is two orders of magnitude smaller than normal morning dewfall of up to 0.5 183 mm (Monteith, 1957) Although microscopic leaf wetness could be interpreted as a specific form of 184 dewfall, meteorological instruments are not sensitive enough to detect and to filter it from other 185 signals, neither by lysimeters for the amount of water, nor by flux measurements for the contribution 186 to the energy budget 187 So far, no field measurement techniques are known other than the indirect method where the signals 188 from leaf wetness sensors are compared to ambient relative humidity or to the signals from artificial 189 leaf wetness sensors Microscopic leaf wetness is also not visible without the use of microscopic 190 techniques While a combination of a gas exchange cuvette with a light microscope enabled the 191 observation of microscopic water formed by stomatal transpiration and showed the influence of the 192 leaf boundary layer (Burkhardt et al., 2001), the resolution of a light microscope is not high enough to 193 study the interactions between leaf surface particles and stomatal transpiration Detailed observations 194 are enabled by environmental scanning electron microscopy (ESEM), where it is possible to study 9 195 condensation processes at high resolution and under controlled humidity A limitation of the ESEM 196 technique to keep in mind is the fact that leaves are abscised and are not transpiring anymore, so RH 197 and RHs are only regulated from outside Another difficulty is the exact detection of leaf surface 198 temperature in case thicker leaves or needles are used, because the necessary cooling happens from a 199 small table below the sample The ESEM observations are usually done at low temperatures of 2°C to 200 5°C in order to reduce the necessary amount of water vapor molecules to reach high RH, which in 201 most cases is not a limitation ESEM observations have been used to study both condensation on 202 ambient, untreated leaves and the changes resulting from changes in RH after spraying leaves with 203 different types of solutions or dry aerosols (Burkhardt et al., 2012; Burkhardt and Pariyar, 2013) 204 205 206 207 208 209 210 211 212 213 214 16 370 371 Insert Movie here 372 373 374 It is important to note that both movies not show transpiration effects, as needles were abscised and 375 were within the vacuum chamber of the ESEM RH was only manipulated from outside It also has to 376 be noted that the ‘stomatal openings’ only show the entrance to the epistomatal chamber of the pine 377 needles The guard cells are located at the bottom of this opening and cannot be seen Nevertheless, 378 regarding the geometrical situation of interest, the epistomatal chamber has the same features as an 379 open stoma, i.e., a diverging and a converging portion This makes it comparable to the geometrical 380 situation used by (Schönherr and Bukovac, 1972) to derive their conclusion that water uptake into the 381 stomata is impossible 382 In both movies, the strong dynamics of deliquescence can be seen Movie shows the repeated 383 deliquescence and efflorescence of KI The efflorescence of the KI crystals is highly unpredictable and 384 repeatedly the crystallization takes place within the epistomatal chambers, a clear indication that KI 385 solution had entered there The movement of the solution into epistomatal chambers can be seen even 386 clearer in Movie Here, KSCN was used because it is on the far chaotropic side of the Hofmeister 387 series The movies follow one deliquescence process of KSCN The solution shows an extremely flat 388 contact angle, and it is clearly recognizable that the deliquescent KSCN solution enters the epistomatal 389 chamber The movies can thus be taken as an additional proof for stomatal uptake of aqueous 390 solutions They can also be interpreted as a first successful support for the hypothesis that chaotropic 391 salts are more easily penetrating into the stomata Finally, they can be taken as a confirmation of 392 Aitken’s observation of ‘breath figures’, i.e liquid water in a flat, non-droplet like shape on a 393 hydrophobic surface, which is spreading out easily and forming a thin water layer on the leaf surface 394 17 395 Conclusions and recommendations 396 Microscopic leaf wetness can play an important role for trace gas deposition and for ion fluxes across 397 the plant surface Increased ammonia deposition over a Douglas fir forest was observed above 70 % 398 RH at night and even lower at daytime (Wyers and Erisman, 1998), and over a grassland above 71 % 399 RH (Wichink Kruit et al., 2008) During daytime, a contribution of 66% to 88% was found for 400 ‘cuticular ammonia deposition’ to a maize canopy (Walker et al., 2013) For ammonia, this 401 microscopic leaf wetness will enable bi-directional ‘cuticular’ gaseous exchange, depending on 402 dynamic environmental conditions and the respective compensation points for different trace gases 403 (Flechard et al., 1999;Burkhardt et al., 2009;Sutton et al., 2009) Non-stomatal ozone deposition is 404 more difficult to explain, as ozone is less soluble than ammonia, and no obvious chemical reactions 405 can account for the observed non-stomatal losses However, several reaction mechanisms of ozone 406 with atmospheric aerosols have been discussed (Jacob, 2000;Oum et al., 2003;Roeselova, 2003), and 407 although such mechanisms have so far been out of focus in the search for reasons explaining non- 408 stomatal ozone deposition, they should be re-considered taking into account the likely continuing 409 occurrence of highly concentrated solutions on leaf surfaces 410 Microscopic leaf wetness influences plant physiology Leaf surface particles increase HAS, and the 411 liquid water connections formed between the leaf surface and the apoplast along the stomatal walls 412 have an influence on water and nutrient fluxes Increased transpiration and reduced water use 413 efficiency caused by leaf surface particles was observed for particle exclusion (Pariyar et al., 2013) as 414 well as for particle amendment (Burkhardt et al., 2001) The stomatal uptake of nutrients is enabled as 415 well as the stomatal leaching of ions, although an experimental proof for the latter is still missing 416 Sound reasons for nocturnal transpiration (Caird et al., 2007) have so far been missing, and nocturnal 417 stomatal nutrient uptake might represent one benefit for the plant 418 The development of models addressing both the physical mechanisms as well as the 419 (physico)chemistry of microscopic leaf wetness would be useful So far, morning dewfall is 420 considered a micrometeorological phenomenon and is assessed via a negative energy balance In order 18 421 to address the relevance of the mechanism, the implementation of microphysical aerosol models would 422 be useful, introducing ‘DCN’ (dew condensation nuclei) on leaf surfaces, with a similar formalism as 423 atmospheric CCN For this purpose, advanced chemical aerosol models could be introduced into 424 models of plant-atmosphere interaction 425 The influence of deposited aerosols on plant physiology and on plant-atmosphere interactions has so 426 far been neglected in plant science as well as in micrometeorology Leaf surface particles were 427 assumed to stay chemically inert Leaf surface wetness was defined by visible detection and was 428 considered to exist as pure water or strongly dilute solutions Microscopic leaf wetness develops by 429 the hygroscopic action of fine particles, with water vapor mainly from stomatal transpiration ‘Breath 430 figures’ on leaf surfaces are microscopically thin films as well as droplets, which are highly dynamic 431 in concentration and extension They interact with the atmosphere by bi-directional gas fluxes and 432 with the apoplast via HAS by hydraulic signals and the exchange of aqueous solutions The 433 consideration of these processes in broadened concepts of plant-atmosphere interactions is highly 434 desirable Including existing aerosol models into leaf surface 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(Palo Alto: Annual Reviews), 63‐83. 650 651 652 653 654 655 656 657 658 659 660 28 661 Figure 662 663 Figure 1: 664 Measurement of leaf wetness on a potato field, comparing an artificial leaf Campbell Leaf wetness 665 sensor 237 (blue line, upper image; Campbell Scientific, Logan, UT, USA), and a leaf wetness sensor 666 directly attached to a potato leaf (red line, upper image; construction see Burkhardt & Gerchau, 1994) 667 Ambient air humidity (black line, lower picture) and photosyntheticcally active radiation (pink line, 668 lower picture) are also shown CET: Central European Time 669 670 671 Movies 672 Movie 1: 673 Potassium iodide (KI) crystals on a Pinus sylvestris needle under changing humidity in an 674 environmental scanning electron microscope Three deliquescence/efflorescence cycles are shown, 675 cycling between approximately 55% and 70% RH 676 677 Movie 2: 678 Potassium thyocyanate (KSCN) crystals on a Pinus sylvestris needle under increasing humidity in an 679 environmental scanning electron microscope Humidity increases from 60 to 65 % RH 680 681 Figure 1.TIFF Copyright of Frontiers in Plant Science is the property of Frontiers Media S.A and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission However, users may print, download, or email articles for individual use ...1 1 ? ?Breath figures? ?? on leaf surfaces – formation and effects of 2 microscopic leaf wetness 3 Juergen Burkhardt1 & M Hunsche2 4 5 6 Revision 7 8 9 10 11 University of Bonn, Karlrobert-Kreiten-Str... Depending on the amount and concentration of 31 the dissolved ions, the physicochemical properties of microscopic leaf wetness can be considerably 32 different from those of pure water Microscopic leaf. .. exchange of ions Microscopic leaf wetness can also enhance the 35 dissolution, the emission, and the reaction of specific atmospheric trace gases e.g ammonia, SO2, or 36 ozone, leading to a strong