1 Running Head - Plant Physiology · 52 stomatal conductance) ... and diurnal variation of stomatal conductance and ... (electrolyte leakage). 153 154 Soil humidity

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Running Head 1

Hydraulic variation in three Ranunculus species 2

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Corresponding Author 4

Markus Nolf, Hawkesbury Institute for the Environment, Western Sydney University, 5

Richmond NSW 2753, Australia, Phone: +61 2 4570 1028, Email: 6

[email protected] 7

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Research Area 9

Ecophysiology and Sustainability 10

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Plant Physiology Preview. Published on February 19, 2016, as DOI:10.1104/pp.15.01664

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Title 13

Herb hydraulics: Inter- and intraspecific variation in three Ranunculus species 14

15

Authors 16

Markus Nolf1,2, Andrea Rosani1, Andrea Ganthaler1, Barbara Beikircher1, Stefan Mayr1 17

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Address 19

1 Institute of Botany, University of Innsbruck, 6020 Innsbruck, Austria 20

2 Hawkesbury Institute for the Environment, Western Sydney University, Richmond NSW 21

2753, Australia 22

23

Author Contributions 24

The study was led by M.N. and S.M; all authors contributed to the experimental design and 25

methodical developments; A.G., A.R., B.B. and M.N. conducted field and laboratory 26

measurements and performed data analysis. M.N. prepared the manuscript with 27

contributions of all the authors. S.M. supervised and complemented the writing. 28

29

Summary 30

Small herbaceous species are vulnerable to water stress, but adjusted to their habitat 31

conditions and internally coordinated to avoid hydraulic failure. 32

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3

Financial sources 34

The study was supported by the Austrian Science Fund, FWF projects I826-B25 and T-667. 35

Markus Nolf is a recipient of a DOC-fellowship of the Austrian Academy of Sciences. 36

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38

Present Address 39

Hawkesbury Institute for the Environment, Western Sydney University, Richmond NSW 40

2753, Australia 41

42

Corresponding Author 43

Markus Nolf, [email protected] 44

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4

Abstract 46

The requirements to the water transport system of small herbaceous species differ 47

considerably from those of woody species. Despite their ecological importance for many 48

biomes, knowledge regarding herb hydraulics remains very limited. 49

We compared key hydraulic features (vulnerability to drought-induced hydraulic decline, 50

pressure-volume relations, onset of cellular damage, in situ variation of water potential and 51

stomatal conductance) of three Ranunculus species differing in their soil humidity 52

preferences and ecological amplitude. 53

All species were very vulnerable to water stress (50 % reduction in whole-leaf hydraulic 54

conductance (kleaf) at -0.2 to -0.8 MPa). In species with narrow ecological amplitude, the 55

drought-exposed R. bulbosus was less vulnerable to desiccation (analysed via loss of kleaf 56

and turgor loss point (TLP)) than the humid-habitat R. lanuginosus. Accordingly, water stress 57

exposed plants from the broad-amplitude R. acris revealed tendencies of lower vulnerability 58

to water stress (e.g. osmotic potential at full turgor, cell damage, stomatal closure) than 59

conspecific plants from the humid site. 60

We show that small herbs can adjust to their habitat conditions on inter- and intraspecific 61

levels in various hydraulic parameters. Coordination of hydraulic thresholds (50 and 88 % 62

loss of kleaf, TLP, minimum in situ water potential) enabled the study species to avoid 63

hydraulic failure and damage to living cells. Reversible recovery of hydraulic conductance, 64

desiccation-tolerant seeds, or rhizomes may allow them to prioritise towards a more efficient 65

but vulnerable water transport system while avoiding the severe effects that water stress 66

poses on woody species. 67

68



5

Introduction 69

The resistance of terrestrial plant species to water stress is an important determinant of their 70

spatial distribution (Engelbrecht et al., 2007), and in a globally changing climate, resistance 71

to water stress induced damage to the water transport system is an essential parameter for 72

the prediction of species survival and future changes in biodiversity and species composition. 73

The hydraulic vulnerability to drought-induced embolism in woody species is adjusted to their 74

environmental conditions on a global scale (Choat et al., 2012), but increased hydraulic 75

safety entails several tradeoffs, such as transport efficiency, as plants can reduce the risk of 76

hydraulic failure by formation of smaller and hydraulically less efficient conduits (e.g. Tyree et 77

al., 1994; Wagner et al., 1998, Gleason et al., 2015). 78

While many studies have dealt with the hydraulics of woody species (see e.g. Maherali et al., 79

2004; Choat et al., 2012), hydraulic characteristics of small herbaceous species are largely 80

understudied and our knowledge regarding their water transport system including 81

vulnerability to drought-induced loss of conductivity remains very limited (e.g. Iovi et al., 82

2009; Kocacinar and Sage, 2003; Brodribb and Holbrook, 2004; Holloway-Phillips and 83

Brodribb, 2011a; Tixier et al., 2013). Yet herbs play an important ecological role in many 84

biomes such as grasslands or the alpine zone (e.g. Billings and Mooney, 1968; Gilliam, 85

2007; Scholz et al., 2010) and represent a significant percentage of crop plants (Monfreda et 86

al., 2008), and are therefore interesting from an eco-physiological viewpoint. 87

The requirements to the water transport system of herbs differ in several ways from those of 88

woody species (Mencuccini, 2003). Firstly, transport distances and supported leaf areas are 89

much smaller in herbs and reversible extra-xylary limitations (Brodribb and Holbrook, 2005; 90

Kim and Steudle, 2007) may have a stronger effect on hydraulic conductivity. Secondly, 91

herbs often don’t feature an essential, lignified main axis designed for long-term functioning, 92

in which hydraulic failure may mean whole-plant mortality. Thirdly, small plants may more 93

easily restore water transport capacity in case of embolism formation, because, due to 94

smaller size, a water potential (Ψ) at or near zero can be reached quickly under favourable 95

conditions due to positive root pressure (e.g. Tyree and Sperry, 1989; Tyree and Ewers, 96

1991; Stiller and Sperry, 2002; Tyree and Zimmermann, 2002, Ganthaler and Mayr, 2015). 97

Thus, herbs may not be as threatened by drought-induced failure as taller woody species. 98

Hydraulic failure occurs when vulnerability thresholds are exceeded under water stress and 99

the xylem tension is suddenly released as water is replaced by air, effectively blocking water 100

transport in the affected conduits (Tyree and Zimmermann, 2002). Vulnerability to drought-101

induced embolism can thus be analysed hydraulically by measuring decreases in 102

conductance during increasing water stress (e.g. Sperry et al., 1988a; Cochard, 2002; 103

Cochard et al., 2013), by non-invasive imaging of xylem water content (e.g. Choat et al., 104



6

2010, Brodersen et al., 2013; Cochard et al., 2015), or indirectly by monitoring of ultrasonic 105

acoustic emissions (UE) which occur during the spontaneous energy release at embolism 106

formation (e.g. Milburn and Johnson, 1966; Mayr and Rosner, 2011; Ponomarenko et al., 107

2014). However, the usability of UE analysis to non-invasively study hydraulic vulnerability 108

remains under discussion (e.g. Sandford and Grace, 1985; Kikuta, 2003; Wolkerstorfer et al., 109

2012; Cochard et al., 2013; Rosner, 2014). 110

On the leaf level, desiccation may induce turgor loss, decreases in mesophyll conductance 111

(Kim and Steudle, 2007, Scoffoni et al., 2014), or cell collapse (Blackman et al., 2010; 112

Holloway-Phillips and Brodribb, 2011a) and limit hydraulic conductance, gas exchange, and 113

thus photosynthesis before embolism occurs. When water stress further increases, living 114

cells may incur damage resulting in tissue and leaf mortality. 115

In this study, we compared key hydraulic features (vulnerability to drought-induced loss of 116

conductance as measured via hydraulic flow and xylem staining, pressure-volume relations, 117

onset of cellular damage) of three species from the genus Ranunculus, which is distributed 118

almost worldwide and contains species adapted to dry and humid habitats, respectively, as 119

well as species with broad ecological amplitude. We hypothesised that herbaceous species 120

would be more vulnerable to water stress than woody species, but would also show inter- 121

and intraspecific adjustment in hydraulic vulnerability based on the water availability of their 122

respective habitats. Namely, the hydraulics of species with narrow ecological amplitude were 123

hypothesised to reflect their respective habitat conditions, and broad-amplitude species 124

should show adequate intraspecific variation to enable growth in dry and humid habitats. 125

126

Materials and Methods 127

Study sites and plant material 128

The study was conducted at three sites in Innsbruck, Austria (47.267° N, 11.393° E), with 129

896.5 mm of precipitation and an average air temperature of 8.5°C in the 30-year-mean 130

(ZAMG, 2002). Three species of Ranunculus, which occur frequently within the study area, 131

were chosen for analysis due to their differing habitat conditions: R. bulbosus is a typical 132

species of dry meadows and nutrient-poor grasslands, and grows up to 15-40 cm tall (Hegi, 133

1974; Fischer et al., 2008). The species dies back to perennial bulb-like corms in July and 134

remains dormant until the following spring (Coles, 1973; Sarukhan, 1974). Sample plants 135

were taken from a south-exposed, non-intensively managed meadow (Hötting). In contrast, 136

R. lanuginosus is found in humid, shaded environments such as riparian forests or gorges, 137

and grows up to 50-70 cm (Hegi, 1974; Fischer et al., 2008). Plants were collected in a small 138

gorge (Sillschlucht) at the south end of the city. The third species, R. acris agg., occurs in a 139



7

range of humidity conditions from dry to humid meadows and reaches intermediate heights 140

of 30-60 cm (Hegi, 1974; Polatschek, 2000; Fischer et al., 2008). For this species, a “dry” 141

population co-occurring with the sampled R. bulbosus population and a “humid” population 142

occurring on a separate high-humidity site (Völs) were used for analysis. 143

Soil humidity, species composition, and diurnal variation of stomatal conductance and Ψleaf 144

were recorded on site in late spring and summer (May to August) in two consecutive years. 145

For all other analyses, whole plants including major roots were collected from the field sites 146

between May and August, immediately placed in dark plastic bags to limit water loss, and 147

transported to the laboratory within 30 min. Plants were rehydrated over night with their roots 148

in water and covered with a dark plastic bag. Measurements were made on healthy, fully-149

developed leaves including petioles (pressure-volume relations, leaf hydraulic vulnerability, 150

conductive xylem staining), leaf petioles with intact laminas (acoustic emissions), and leaf 151

discs cut from the leaf laminas (electrolyte leakage). 152

153

Soil humidity 154

Soil humidity was analysed in situ in two years during dry periods with the Hydrosense II Soil 155

Moisture Measurement System (Campbell Scientific Ltd., Shepshed, UK), whereby 156

volumetric soil water content (SWC) was measured 24 h after strong rainfall (SWCfield capacity), 157

and after seven days without rain (SWCdry) in 10 samples per site and date. The relative 158

SWC (SWCrel; % of field capacity) after seven days without rain was calculated as 159

SWCrel = SWCdry

mean (SWCfield capacity)× 100 (1) 160

161

Additionally, we recorded species composition at the three sites and characterized water 162

availability using averaged ecological indicator values (humidity value; Ellenberg et al., 1992; 163

Schaffers and Sykora, 2000). 164

165

Water potential determination 166

Leaf water potential (Ψleaf) was measured with a pressure chamber (Model 1000 Pressure 167

Chamber, PMS Instrument Co., Corvallis, OR, USA) by applying pressure to an excised leaf 168

sealed into the chamber, with the petiole protruding out through a rubber gasket (Scholander 169

et al., 1965). Air pressure inside the chamber was slowly increased until the xylem sap 170

meniscus became visible at the cutting site. 171

172



8

Pressure-volume analysis 173

Pressure-volume analyses (Tyree and Hammel, 1972; Bartlett et al., 2012; Sack et al., 2011) 174

were carried out on five leaves per species/population to determine turgor loss point (TLP), 175

osmotic potential at full turgor (Π0), and modulus of elasticity (ε). Leaves were fully saturated 176

before dehydration and regular measurements of Ψleaf and fresh weight. Relative water 177

content (RWC) was calculated from saturated, fresh, and dry weights, and plotted against the 178

inverse of Ψleaf to find the TLP (transition point between the linear and curved portions of the 179

graph), Π0 (negative inverse of the linear graph portion’s intercept with the y-axis), and ε 180

(slope of the curve above and including TLP). Parameters were calculated individually per 181

leaf and then averaged per species/population. 182

183

Leaf hydraulic vulnerability 184

Declines in leaf hydraulic conductance due to increasing desiccation were analysed with a 185

modified non-steady-state leaf rehydration technique (Brodribb and Cochard, 2009; 186

Blackman and Brodribb, 2011) and bench-top dehydration. For 39-45 leaves per 187

species/population, we measured the decay of initial water uptake into the leaf from a small 188

water container placed on a digital balance (CP64, Sartorius, Göttingen, Germany), which 189

was connected to the leaf petiole via hydraulic tubing (see below). 190

At increasing levels of dehydration, plants were equilibrated in dark plastic bags and plant Ψ 191

was determined on two leaves per plant. If Ψ between both leaves differed by 10% or less, 192

the decay of initial flow was measured by excising a third leaf under water (including approx. 193

3 cm of the petiole), immediately connecting the leaf to hydraulic tubing, and covering the 194

leaf with a moist paper towel to prevent transpiration. Thus, hydraulic flow was measured on 195

non-light-acclimated, non-transpiring leaves. Flow rates (kleaf, mmol m-2 s-1 MPa-1) were 196

determined by linear regression of decreasing mass readings (water uptake) during the first 197

10 seconds, and adjusted for temperature and leaf area. Maximum leaf hydraulic 198

conductance (kleaf max) was calculated as the average of five maximum conductances 199

observed per species/population. No cutting artefact (Wheeler et al., 2013) was expected for 200

leaves excised under water (Scoffoni and Sack, 2014). 201

The reparameterized Weibull function (Ogle et al., 2009) was fitted to plots of relative kleaf vs. 202

Ψ using the fitplc package for R v. 3.1.1 (R Core Team, 2014; Duursma, 2014): 203

204

= 1 − 205



9

= (2) 206

= − 100 ln 1 − 100

where k is the expected hydraulic conductance at X% loss of conductance, kleaf max is the k at 207

full saturation (i.e. k at 0 MPa), P is the positive-valued Ψ (P = -Ψ), Px is the Ψ at X% loss of 208

conductance, and Sx is the slope of the vulnerability curve at P = Px. Pk50 and Pk88 were 209

defined as the Ψ at 50 and 88% loss of bulk leaf hydraulic conductance, respectively. 210

211

Staining of conducting xylem elements 212

To confirm the observed high levels of leaf hydraulic vulnerability, we stained conducting 213

xylem elements in leaves of R. acris from the dry site. At increasing levels of dehydration, 214

whole plants were equilibrated in dark plastic bags and plant Ψ was determined on one leaf 215

per plant. Two additional leaves of the same plant were excised under water and 216

immediately placed in a beaker containing a) 1% (w/v) Phloxine B (modified after Nardini et 217

al., 2003) to reveal ongoing water transport in the lamina and b) 0.05% (w/v) Safranin 218

(modified after Sperry et al., 1988b) to stain water conducting conduits in the petioles. 219

Samples were exposed to sunlight for about 10 min. Transpiration was favoured by partially 220

removing the cuticle and confirmed with an SC-1 Leaf Porometer (Decagon Devices, 221

Pullman, WA, USA). We analysed images of the lamina taken with a digital camera, and 222

petiole cross sections (approx. 3 cm from the lamina) taken with a light microscope (Olympus 223

BX41; Olympus Austria, Vienna, Austria) and interfaced digital camera (ProgRes CT3, 224

Jenoptik, Jena, Germany). To prevent artefacts by passive dye diffusion, only samples with 225

unstained parenchyma and phloem were used. 226

227

Electrolyte leakage 228

The vulnerability of living tissues to dehydration (Morin et al., 2007; Hu et al., 2010; Vilagrosa 229

et al., 2010; Beikircher et al., 2013) was analysed by bench-top dehydrating plants and 230

comparing the leakage of electrolytes from 52 to 82 leaves per species at increasing levels of 231

dehydration. After Ψ determination, three to ten circular discs (0.6 cm in diameter) were cut 232

from each leaf by use of a cork borer while avoiding major leaf veins. Leaf disks were pooled 233

for each sample leaf, submerged in 15 ml distilled water in individual centrifuge tubes and 234

shaken for 24 h on a horizontal shaker (ST5 Bidimensional shaker, CAT, Staufen, Germany) 235

at 5 °C, followed by electrolytic conductivity measurement at room temperature (after 1 h of 236



10

temperature equilibration) using a 4-electrode conductivity sensor (Tetracon 325, WTW, 237

Weilheim, Germany). Samples were then autoclaved at 120 °C for 30 min and shaken over 238

night at room temperature, before final electrolytic conductivity was measured. 239

Relative electrolyte leakage (REL) was calculated as 240

REL = × 100 (3) 241

where C1 and C2 are the initial and final electrolytic conductivities, respectively. REL was 242

then standardised to percentage of cellular lysis by relating each sample’s REL to the REL of 243

the control (RELc; Morin et al., 2007), in this case, samples measured at Ψ ≥ -0.2 MPa: 244

Cellular lysis % = REL RELc RELc× 100 (4) 245

246

Vulnerability thresholds were again calculated by curve-fitting to Eq. (2), where k is the 247

percentage of intact cells (k = 100 - percentage of cellular lysis). The onset of damage to 248

living cells (P12CL) was defined as the Ψ at 12% cellular lysis. 249

250

Diurnal variation of stomatal conductance and Ψleaf 251

We monitored the diurnal progression of stomatal conductance (using an SC-1 Leaf 252

Porometer; Decagon Devices, Pullman WA, USA) and corresponding Ψleaf between sunrise 253

and sunset on one clear, sunny day per species following a period of rainfall. For each data 254

point, stomatal conductance (gs) was measured on the lower leaf side of four to five 255

undamaged, fully developed leaves of different plants, whereas Ψleaf was determined on 256

three undamaged, fully developed leaves of different plants. 257

258

Statistical analyses 259

Data for curve-fitting was pooled per species/population and method before further analysis. 260

Vulnerability thresholds were statistically tested for differences using bootstrapped 261

confidence intervals (CI, n = 999 bootstrap estimates). Other data was normally distributed 262

(QQ-plots, Shapiro-Wilk Test) and tested for differences using Student’s t-Test 263

(homoscedastic data as determined by the robust Brown-Forsythe Levene-type test) or 264

Welch’s Two-Sample t-Test (heteroscedastic data), respectively. All analyses were done in 265

R 3.1.1 (R Core Team, 2014) at a significance level of P < 0.05, whereas P was Bonferroni-266

corrected for multiple comparisons. Values are presented as mean ± standard error (SE) or 267

mean (lower CI, upper CI), respectively. 268



11

269

Results 270

Volumetric soil water content (SWC) at field capacity was 40.4% (dry site), 51.0% (humid 271

site: R. acris), and 30.4% (humid site: R. lanuginosus). Relative SWC after seven rain-free 272

days was above 90% at the humid sites and 43 to 58% at the dry site (Tab. I). The low field 273

capacity SWC of the second humid site was due to the soil composition (thin layer of humus 274

and litter on top of gravel substrate), yet the SWC remained constant due to the humid 275

conditions inside the gorge. The reason for a SWCrel ≥ 100% at this site may lie in water 276

seeping through the slope from uphill soils. Ecological indicator values for the study species 277

and co-occurring species at the sampling sites supported the observed differences in water 278

availability: Averaged humidity values were 4.4 at the dry site, and notably higher at 5.5 (R. 279

acris site) and 5.7 (R. lanuginosus site) at the humid sites, respectively (Tab. I). At the dry 280

site, R. bulbosus (humidity index: 3, indicator for dry sites) and R. acris (humidity index: 6, 281

indicator for humid sites but broad amplitude) were accompanied by dry-habitat species such 282

as Bromus erectus, Knautia arvensis, and Lotus corniculatus. In contrast, at the humid sites 283

R. lanuginosus (humidity index: 6) and R. acris were co-occurring with other species typical 284

for moist habitats, including Polygonum bistorta, Rumex conglomeratus, Urtica dioica, and 285

Solanum dulcamara (Table S1). 286

The turgor loss point (TLP) was least negative in R. lanuginosus at a leaf water potential 287

(Ψleaf) of -1.1 ± 0.1 MPa, and was reached at -1.4 ± 0.0 MPa in R. bulbosus, and -1.6 ± 0.1 to 288

-1.7 ± 0.1 MPa in R. acris (Tab. I). The osmotic potential (Π0) followed a similar trend 289

at -0.9 ± 0.1 MPa (R. lanuginosus), -1.3 ± 0.0 MPa (R. bulbosus), and -1.4 ± 0.1 290

to -1.5 ± 0.1 MPa (R. acris), respectively. In contrast, the modulus of elasticity (ε) was lowest 291

(i.e. cells were more elastic) at 9.6 ± 1.9 MPa in R. lanuginosus and 1.5 to 2.5 times higher in 292

the other species (R. bulbosus: 16.7 ± 1.3 MPa; R. acris: 20.4 ± 4.4 to 24.9 ± 3.6 MPa). 293

Maximum whole-leaf hydraulic conductance (kleaf max) was between 23.4 and 28.0 mmol m-2 294

s-1 MPa-1 and did not differ between species (Tab. I). Hydraulically measured Pk50 was least 295

negative in R. lanuginosus (-0.2 MPa) and more negative in R. acris and R. bulbosus (-0.6 to 296

-0.8 MPa; Tab. II, Fig. 1). Similarly, Pk88 were highest in R. lanuginosus (-0.4 MPa) and 297

significantly more negative in the other two species (-1.5 to -3.3 MPa; Tab. II, Fig. 1). 298

Conductive xylem staining in R. acris (dry) showed first notable signs of embolism in minor 299

leaf veins and vascular bundles at -2.0 MPa, with significant losses of even first-order leaf 300

veins by -2.7 MPa (Fig. 2). 301

Significant cellular lysis started at more negative Ψ than Pk50, with P12CL between -1.1 and -302

2.0 MPa (Tab. II, Fig. 3), whereas thresholds for cell damage did not correspond to humidity 303



12

conditions. In contrast, the onset of ultrasonic emissions (UE) was observed at less negative 304

Ψ than hydraulic vulnerability thresholds, with peak activity at ≥ -1.1 MPa (Supplemental; 305

Information, Tab. S2, Fig. S2). 306

In situ, species reached minimum Ψleaf (Ψmin) of -0.4 ± 0.1 to -2.2 ± 0.1 MPa, whereby Ψmin 307

was lower at the dry site (Tab. I, Fig. 4). In contrast, stomatal conductance (gs) exhibited 308

considerable variability at more negative Ψ. Maximum stomatal conductance (gs max) was 309

between 492.1 ± 86.1 and 885.0 ± 37.3 mmol m-2 s-1 and did not reflect soil humidity 310

differences between sites (Tab. I, Fig. 4). The progression of Ψleaf and gs in the field 311

(illustrated in Fig. 4 for R. acris) revealed that stomatal conductance was reduced in all 312

species when Ψmin was reached. Theoretical kleaf as calculated from measured Ψleaf and 313

transpiration (E; based on measured gs and climate data from the closest weather station at 314

approx. 3 km distance) agreed well with kleaf predicted from vulnerability curves. However, 315

vapour pressure deficit and transpirational demand were expected to be lower in the lowest 316

canopy layer than calculated here (Wohlfahrt et al., 2010). Both Ψleaf and gs were compared 317

on representative, sunny days, but environmental conditions (wind, prolonged drought 318

stress) may lead to more extreme values. Because of windy (R. bulbosus) or shady 319

conditions (R. lanuginosus, due to its understorey gorge habitat) during in situ measurements 320

(Fig. S1), diurnal variation data for only R. acris was used for further interpretation. 321

322

Discussion 323

We found that all studied species were generally vulnerable to dehydration, but differences 324

between species/populations reflected the humidity conditions of their respective habitats. 325

Sites differed in their water availability, as the relative soil water content (SWCrel) between 326

dry and humid sites differed significantly after only seven days without precipitation. At the 327

dry site, SWCrel decreased to less than 60% of field capacity (FC) after only one rain-free 328

week, whereas the humid sites experienced hardly any reduction in soil humidity. The low 329

SWC at the humid site of R. lanuginosus, which was due to soil composition, was 330

compensated by the humid conditions inside the gorge so that SWCrel did not decrease 331

during the rain-free period. Species composition and ecological indicator values supported 332

the distinction between dry and humid sites (Tab. I, Tab. S1). 333

334

Herb hydraulics 335

Leaf hydraulic conductance (kleaf) is known to vary widely across species and plant functional 336

types, with an average kleaf of 11.5 ± 0.9 mmol m-2 s-1 MPa-1 across 107 woody and 337



13

herbaceous species, and individual species ranging between 0.8 and 49.0 mmol m-2 s-1 338

MPa-1 (Sack and Holbrook, 2006). Leaf hydraulic efficiency in herbaceous crops was above 339

average at 24.1 ± 2.2 mmol m-2 s-1 MPa-1 (Sack and Holbrook, 2006), and other, non-340

cultivated herbaceous angiosperms in the literature were between 2.7 and 22.0 mmol m-2 s-1 341

MPa-1 (Brodribb and Holbrook, 2004; Bunce, 2006; Galmes et al., 2007). Our study species 342

were within the range known for herbaceous plants, and therefore showed much higher 343

hydraulic efficiency than woody species (Tab. I, Fig. 1). 344

Leaf hydraulic vulnerability studies on small herbaceous species found 50 % reduction in kleaf 345

between -1.0 MPa and -1.8 MPa (perennial grasses; Brodribb and Holbrook, 2004; Holloway-346

Phillips and Brodribb, 2011a; also see Holloway-Phillips and Brodribb, 2011b). Woody 347

species generally feature leaves that are less vulnerable to water stress, with an average 348

Pk50 of -1.8 ± 0.1 MPa across 81 woody angiosperm species when measured with 349

comparable methods (compiled in Nolf et al., 2015). Although some of these species also 350

had very vulnerable leaves at Pk50 ≥ -1 MPa (e.g. Hao et al., 2008; Chen et al., 2009; 351

Blackman et al., 2012; Guyot et al., 2012), the majority of previously studied species 352

exhibited Pk50 of ≤ -1.5 MPa and down to -4.3 MPa (e.g. Sack and Holbrook, 2006; Blackman 353

et al., 2010; Johnson et al., 2012; Nardini et al., 2012; Bucci et al., 2013). Accordingly, stems 354

were typically also more vulnerable to drought-induced hydraulic failure in herbs (-1.0 to -3.8 355

MPa; e.g. Kocacinar and Sage, 2003; Rosenthal et al., 2010; Tixier et al., 2013; Nolf et al., 356

2014) than in woody species (-0.1 to -14.1 MPa, -3.4 ± 0.1 MPa across 480 species; Choat 357

et al., 2012). 358

Leaf hydraulic analysis in our study showed that all three Ranunculus species were very 359

vulnerable to water stress, with Pk50 ≥ -0.8 MPa in leaf hydraulic conductance across all 360

species (Tab. II, Fig. 1). However, xylem staining indicated that early hydraulic conductivity 361

losses at moderate Ψ were due to extra-xylary, likely reversible, effects rather than xylem 362

embolism. Stained petiole sections and leaves revealed loss of conductivity due to embolism 363

and suggested an estimated xylem P50 (50 % loss of xylem hydraulic conductivity due to 364

embolism) of ≤ -2 MPa in R. acris (dry) (Fig. 2). Thus, despite the fact that plants were still 365

very vulnerable to drought, it is important to stress that the employed leaf hydraulics method 366

measured bulk hydraulic conductivity including both xylary and extra-xylary (e.g. mesophyll) 367

pathways and reflected the total effect on symplastic and apoplastic transport. Interestingly, 368

stained cross-sections also indicated an all-or-nothing effect, where in most cases, individual 369

vascular bundles lost all conductivity at once (Fig. 2C). 370

Compared to staining results, ultrasonic activity was observed at much less negative Ψ than 371

expected (Tab. S2, Fig. S2). We believe that other signal sources unrelated to water 372

transport (e.g. parenchyma and sclerenchyma) were responsible for a considerable portion 373



14

of emissions, skewing acoustic analysis. Thus, interpretation of UE analyses on herbs is 374

difficult and requires further methodical optimisation. 375

With daily minimum leaf water potential (Ψmin) being 0.3 to 1.4 MPa lower than Pk50, at least 376

two of our species would incur significant water transport reduction during the course of the 377

day (Tab. I and Tab. II; Stiller et al., 2003), limiting transpiration and thus, according to Ohm’s 378

law, preventing a further decrease of Ψ. However, the staining experiment suggests that 379

embolism only plays a minor role in hydraulic decline at the observed in situ water potentials 380

(Fig. 2) and water transport is therefore mainly limited by reversible extra-xylary effects (e.g. 381

turgor loss or cell collapse and associated mesophyll conductance losses; Brodribb and 382

Holbrook, 2005; Kim and Steudle, 2007; Blackman et al., 2010; Holloway-Phillips and 383

Brodribb, 2011a; Scoffoni et al., 2014). 384

Like significant hydraulic transport reductions, the turgor loss point (TLP) is another critical 385

point plants need to avoid so they can maintain photosynthesis, transport of solutes, and 386

growth (e.g. Frensch and Hsiao, 1994; Kramer and Boyer, 1995; Brodribb and Holbrook, 387

2003; Bartlett et al., 2012). In our study species, the TLP was lower than hydraulic K50 , 388

indicating that all studied species would face notable reductions in transport capacity under 389

limited water supply before leaves would lose turgor (Tab. I and Tab. II). This indicates that 390

impairment of whole-leaf water transport is the first critical event during water stress. 391

Pressure-volume analysis revealed that TLPs in this study were mainly determined by the 392

osmotic potential (Π0), whereas a mediating, opposite effect caused by the observed trends 393

in bulk elasticity was small. Only in R. lanuginosus, the high elasticity may have 394

compensated for the species’ weak water-holding capability (high Π0) to longer maintain 395

turgor. 396

Electrolyte leakage analysis showed that desiccation-induced damage to living cells (P12CL) 397

would only begin long after significant hydraulic decline (Pk50, Tab. II, Fig. 1 and Fig. 3). Since 398

leaves were bench-top dehydrated for up to several hours, we would even expect a higher 399

apparent vulnerability due to continuous exposure to low Ψ on these measurements, 400

compared to shorter in situ stress peaks followed by stomatal regulation and Ψ recovery. 401

Thus, living cells were well protected from desiccation-induced cell damage, as found 402

previously by other authors (e.g. Vilagrosa et al., 2010; Beikircher et al., 2013). Interestingly, 403

plants from dry habitats did not appear more resistant to cell damage than plants from humid 404

sites (Tab. II, Fig. 3). While we only sampled fully developed, mature leaves, we do note that 405

R. bulbosus required measurement one to two months earlier than other species due to their 406

summer dormancy (see Study sites and plant material). 407

408



15

Interspecific differences 409

Study species with narrow ecological amplitude (R. bulbosus, R. lanuginosus) showed 410

significant differences in some hydraulic key parameters (TLP, Pk50, and Pk88) which were 411

correlated with their respective soil humidity conditions. The corresponding trend in daily Ψmin 412

further indicated that Ψleaf was regulated near Pk88 in both species. In contrast, maximum leaf 413

hydraulic conductance (kleaf

max), maximum stomatal conductance (daily gs max), and 414

vulnerability of living cells (P12CL) revealed no corresponding trend, which suggests that these 415

parameters are more evolutionarily conserved. 416

The hydraulics of R. acris with its broad ecological amplitude showed characteristics closer 417

to the drought-adapted species (e.g. Pk50, Pk88; see Tab. II) regarding hydraulic 418

measurements, and did not reveal the intermediate values we expected. The fact that Pk50, 419

Pk88 and P12CL were more negative in R. acris than in R. bulbosus may suggest that although 420

R. acris also occurs frequently in humid sites, it is generally well-adapted for dry habitats. 421

Another possible explanation is that, by dying back to perennial tubers in early summer, R. 422

bulbosus effectively avoids periods of intense water stress in summer and autumn (Coles, 423

1973; Sarukhan, 1974, Larcher, 1995). 424

425

Intraspecific acclimation 426

Within-species variation in hydraulic parameters was previously found for woody (e.g. 427

Matzner et al., 2001; Cochard et al., 2007; Beikircher and Mayr, 2009; Charra-Vaskou et al., 428

2012) and herbaceous species (Holste et al., 2006; Tixier et al., 2013; Nolf et al., 2014). R. 429

acris was chosen for its wide distribution and broad ecological amplitude, and showed trends 430

for intraspecific variation. While most of the species’ hydraulic traits indicated adjustment to 431

dry habitats when compared to other species (Tab. I, Tab. II, Fig. 1, Fig. 3, Fig. 4), plants 432

from the dry site tended to have more negative vulnerability thresholds (Pk50, Pk88), TLP, and 433

daily Ψmin than conspecific plants from the humid site. Thus we suggest that intraspecific 434

variability in hydraulic parameters of R. acris allows the species to retain fitness over a range 435

of humidity conditions (Rejmanek, 1999), and is a major factor determining its wide 436

distribution as found for other herbaceous species (e.g. Hao et al., 2013; Nolf et al., 2014). 437

Interestingly, the onset of desiccation-induced cellular damage (P12CL; Tab. II, Fig. 3) was 438

constant across sites, indicating that this parameter was not subject to adjustment. 439

440



16

Conclusion 441

Overall, all of our study species were very vulnerable to water stress, even R. bulbosus, 442

which is a typical species of dry meadows. However, the first effect of drought in these 443

species was found to be a loss of whole-leaf hydraulic conductance at moderate Ψ based on 444

extra-xylary pathways rather than embolism formation. This may be an effective, easily 445

reversible way for plants to avoid critical decreases in Ψ and subsequent hydraulic failure. 446

Yet, also in these herbs, differences in vulnerability to water stress were observed on inter- 447

and intraspecific levels: In narrow-amplitude species, some key hydraulic parameters were 448

correlated to the humidity conditions of their respective habitats (TLP, daily Ψmin, Pk50, Pk88), 449

while other parameters (kleaf max, gs max, P12CL) did not reveal such trends. In contrast, the 450

broad-amplitude species showed correlations or trends in intraspecific adjustment to different 451

habitat conditions. Due to the ecological importance of herbaceous species in many 452

ecosystems, better knowledge regarding their hydraulics will be essential to improve 453

evaluations of water stress vulnerability on vegetation- and ecosystem levels. 454

455

Supplemental Materials 456

The following supplemental materials are available. 457

Supplemental Table S1: Species composition and corresponding ecological indicator values 458

(humidity value; Ellenberg et al., 2012) at the dry site (R. bulbosus, R. acris), humid R. acris 459

site, and humid R. lanuginosus site, respectively. 460

Supplemental Table S2: Water potential at 50 and 88% of total cumulative ultrasonic 461

emissions above -3 MPa (P50UE and P88UE; MPa). Thresholds computed after fitting the 462

reparameterized Weibull function (Ogle et al., 2009) to vulnerability curves. Mean and 95% 463

confidence intervals. Letters indicate significant differences in each row (P < 0.05). 464

Supplemental Figure S1: Diurnal variation of water potential (MPa; closed circles, solid black 465

lines) and stomatal conductance (mmol m-2 s-1; open circles, dashed red lines) in R. bulbosus 466

and R. lanuginosus. Vertical line (dashed) indicates meteorological dawn, yellow boxes 467

indicate direct sunlight. Mean ± SE. 468

Supplemental Figure S2: Relative cumulative ultrasonic emissions (UE; % of total number of 469

recorded UE above -3 MPa) vs. water potential in Ranunculus bulbosus, R. lanuginosus, and 470

dry and humid R. acris populations. Vertical lines indicate fitted hydraulic parameters P50UE 471

(solid) and P88UE (dashed). Curves were extrapolated using the same equation and 472

parameters used for vulnerability curves (Eq. (2)). 473



17

Supplemental Text: Description of Method for Ultrasonic Emission analysis 474

475

Acknowledgements 476

We thank Dr. Georg Wohlfahrt for providing valuable microclimate data and Mag. Birgit 477

Dämon for excellent technical assistance. 478

479



18

Figure Legends 480

Fig. 1: Leaf hydraulic conductance vs. water potential in Ranunculus bulbosus, R. 481

lanuginosus, and dry and humid R. acris populations measured with the rehydration 482

technique. Vertical lines indicate fitted hydraulic vulnerability parameters Pk50 (solid) and Pk88 483

(dashed). Curves were extrapolated using the same equation and parameters used for 484

vulnerability curves (Eq. (2)). 485

486

Fig. 2: Stained leaf laminas and petiole cross sections of R. acris (dry) indicating loss of 487

hydraulic conductance at increasing levels of dehydration. Conducting elements appear red 488

while embolised conduits remain unstained. A: leaf lamina underside and petiole (bar = 20 489

mm), B: leaf lamina detail (bar = 5 mm), C: petiole cross section approx. 3 cm from the 490

lamina (bar = 200 µm), D: vascular bundle detail from cross section (bar = 50 µm). 491

492

Fig. 3: Cellular lysis (% of maximum after autoclaving) vs. water potential in Ranunculus 493

bulbosus, R. lanuginosus, and dry and humid R. acris populations. Vertical line (dashed) 494

indicates the onset of damage to living cells (P12CL). Curves were extrapolated using the 495

same equation and parameters used for vulnerability curves (Eq. (2)). 496

497

Fig. 4: Diurnal variation of water potential (MPa; closed circles, solid black lines) and 498

stomatal conductance (mmol m-2 s-1; open circles, dashed red lines) in R. acris populations 499

on dry and humid sites. Vertical line (dashed) indicates meteorological dawn, yellow boxes 500

indicate direct sunlight. Mean ± SE. 501

502

Fig. S1: Diurnal variation of water potential (MPa; closed circles, solid black lines) and 503

stomatal conductance (mmol m-2 s-1; open circles, dashed red lines) in R. bulbosus and R. 504

lanuginosus. Vertical line (dashed) indicates meteorological dawn, yellow boxes indicate 505

direct sunlight. Mean ± SE. 506

507

Fig. S2: Relative cumulative ultrasonic emissions (UE; % of total number of recorded UE 508

above -3 MPa) vs. water potential in Ranunculus bulbosus, R. lanuginosus, and dry and 509

humid R. acris populations. Vertical lines indicate fitted hydraulic parameters P50UE (solid) 510

and P88UE (dashed). Curves were extrapolated using the same equation and parameters 511

used for vulnerability curves (Eq. (2)). 512



19

Tables 513

Tab. I: Relative soil water content (SWCrel; % of SWC at field capacity after seven days 514

without rain, measured in summer 2014 and 2015; n = 10), averaged humidity value (n = 10-515

13), maximum leaf hydraulic conductance (kleaf max; mmol m-2 s-1 MPa-1; n = 5), turgor loss 516

point (TLP; MPa; n = 5), diurnal minimum leaf water potential (Ψmin; MPa; n = 3; see Fig. 4, 517

Fig S1), and diurnal maximum stomatal conductance (gs max; mmol m-2 s-1; n = 5; see Fig. 4, 518

Fig S1). Mean ± SE. Letters indicate significant differences in each row (P < 0.05). 519

Species SWCrel 2014 SWCrel 2015 Humidity

value TLP kleaf max Ψmin gs max

R. bulbosus

(dry)

57.57 ±

4.03a

43.29 ±

2.42a

4.40 ±

0.34a

-1.43 ±

0.02a

28.00 ±

0.78a

-1.70 ±

0.03a

537.7 ±

105.3a

R.

lanuginosus

(humid)

102.72 ±

6.14b

98.34 ±

2.31b

5.69 ±

0.26b

-1.14 ±

0.05b

27.77 ±

1.12a

-0.42 ±

0.12b

492.1 ±

86.1a

R. acris

(dry)

57.57 ±

4.03a

43.29 ±

2.42a

4.40 ±

0.34a

-1.72 ±

0.08c

23.40 ±

0.42a

-2.20 ±

0.06c

756.6 ±

195.9a

R. acris

(humid)

93.40 ±

1.87b

90.59 ±

1.30c

5.50 ±

0.23b

-1.63 ±

0.05ac

24.06 ±

0.78a

-1.48 ±

0.15a

885.0 ±

37.3a

520

521



20

Tab. II: Water potential at 50 and 88% loss of leaf hydraulic conductance (Pk50 and Pk88; 522 MPa), and 12% of cellular lysis (P12CL; MPa). Thresholds computed after fitting the 523 reparameterized Weibull function (Ogle et al., 2009) to vulnerability curves. Mean and 95% 524 confidence intervals. Letters indicate significant differences in each row (P < 0.05). 525

Species Leaf rehydration Electrolyte leakage

Pk50 Pk88 P12CL

R. bulbosus

(dry) -0.57 (-0.63, -0.48)a -1.53 (<-1.55, -1.31)a -1.11 (-1.53, -0.84)a

R. lanuginosus

(humid) -0.15 (-0.19, -0.10)b -0.44 (-0.60, -0.35)b -1.16 (-1.47, -0.88)a

R. acris

(dry) -0.82 (-1.08, -0.54)a -3.27 (<-3.27, -2.64)c -2.02 (-2.43, -1.64)b

R. acris

(humid) -0.73 (-0.93, -0.50)a -2.84 (<-3.15, -2.25)c -2.02 (-2.29, -1.62)b

526

527



21

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Brodribb TJ, Holbrook NM (2004) Stomatal protection against hydraulic failure: a comparison of coexisting ferns and angiosperms.New Phytol 162: 663-670


Brodribb TJ, Holbrook NM (2005) Water stress deforms tracheids peripheral to the leaf vein of a tropical conifer. Plant Physiol 137:1139-1146


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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Biol Rev Camb Philos Soc%5BTitle%5D%29 AND 43%5BVolume%5D AND 481%5BPagination%5D AND Billings WD%2C Mooney HA%5BAuthor%5D&dopt=abstract

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1 Running Head - Plant Physiology · 52 stomatal conductance) ... and diurnal variation of stomatal conductance and ... (electrolyte leakage). 153 154 Soil humidity