short title: corresponding authors · 107 these ias traits, along with other previously measured...

1

Short title: 1

3D leaf intercellular airspace traits 2

3

Corresponding authors: 4

Guillaume Théroux-Rancourt ([email protected]): Department of 5

Plant Sciences, University of California Davis, Davis, CA, 95616, USA 6

Present address: Institute of Botany, University of Life Sciences and Natural Resources, 7

1180 Vienna, Austria 8

J. Mason Earles ([email protected]): School of Forestry & Environmental Studies, Yale 9

University, New Haven, CT 06511, USA 10

11

Article title: 12

Beyond porosity: 3D leaf intercellular airspace traits that impact mesophyll conductance 13

14

List of authors: 15

J. Mason Earles1*, Guillaume Théroux-Rancourt2*, Adam B. Roddy1, Matthew E. 16

Gilbert2, Andrew J. McElrone3,4, and Craig R. Brodersen1 17

18

1School of Forestry & Environmental Studies, Yale University, New Haven, CT, 06511, 19

USA 20

2Department of Plant Sciences, University of California Davis, Davis, CA, 95616, USA 21

3USDA-Agricultural Research Service, Davis, CA, 95616, USA 22

4Department of Viticulture and Enology, University of California, Davis, CA, 95616, USA 23

*: These authors contributed equally 24

25 One-sentence summary: 26

The gas phase of mesophyll conductance is impacted by the 3D traits tortuosity, path 27

lengthening and airspace connectivity, in addition to porosity. 28

29 Author Contributions: 30

Plant Physiology Preview. Published on July 24, 2018, as DOI:10.1104/pp.18.00550

Copyright 2018 by the American Society of Plant Biologists

www.plantphysiol.orgon May 7, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.plantphysiol.org

2

JME, GTR, and CRB conceived the study and developed the methods, with 31 contributions from MEG and AJM; JME and GTR acquired and analyzed the data; ABR 32 performed the phylogenetic analyses; JME and GTR wrote the manuscript; ABR, MEG, 33 AJM, and CRB complemented the writing. 34 35 Funding information: 36 GTR was supported by a Katherine Esau Postdoctoral Fellowship. ABR was supported 37 by the Yale Institute of Biospheric Studies. The Lawrence Berkeley National Laboratory 38 Advanced Light Source is supported by the Director, Office of Science, Office of Basic 39 Energy Sciences, of the U.S. Department of Energy under Contract No. DE-AC02-40 05CH11231. 41



3

ABSTRACT 42

The leaf intercellular airspace (IAS) is generally considered to have high conductance to 43

CO2 diffusion relative to the liquid phase. While previous studies accounted for leaf-level 44

variation in porosity and mesophyll thickness, they omitted 3D IAS traits that potentially 45

influence IAS conductance (gIAS). Here we re-evaluated the standard equation for gIAS 46

by incorporating tortuosity, lateral path lengthening, and IAS connectivity. We measured 47

and spatially mapped these geometric IAS traits for 19 Bromeliaceae species with CAM 48

or C3 photosynthetic pathways using X-ray microCT imaging and a novel computational 49

approach. We found substantial variation in porosity (0.04–0.73 m3 m-3), tortuosity 50

(1.09–3.33 m2 m-2), lateral path lengthening (1.12–3.19 m m-1), and IAS connectivity 51

(0.81–0.97 m2 m-2) across all bromeliad leaves. The revised gIAS model predicted 52

significantly lower gIAS in CAM (0.01–0.19 mol m-2 s-1 bar-1) than in C3 (0.41–2.38 mol 53

m-2 s-1 bar-1) plants due to a coordinated decline in these IAS traits. Our re-evaluated 54

equation also generally predicted lower gIAS values than the former one. Moreover, we 55

observed high spatial heterogeneity in these IAS geometric traits throughout the 56

mesophyll, especially within CAM leaves. Our data show that IAS traits that better 57

capture the 3D complexity of leaves strongly influence gIAS and that the impact of the 58

IAS on mesophyll conductance should be carefully considered with respect to leaf 59

anatomy. We provide a simple function to estimate tortuosity and lateral path 60

lengthening in the absence of access to imaging tools such as X-ray microCT or other 61

novel 3D image-processing techniques. 62



4

INTRODUCTION 63

By volume, as little as 3% (Slaton & Smith, 2002) and up to 73% (this study) of 64

the inside of a leaf is composed of air. Such a wide range of values results from the 65

multiple roles that mesophyll cells play in leaf function, the degree of reticulation of the 66

embedded vein network, and cell size and shape, all reflecting the various adaptations 67

plants have made in colonizing nearly every terrestrial habitat on Earth. From an 68

evolutionary perspective, the transition from oceans to land exposed plant tissues to air, 69

which dramatically lowered the resistance for CO2 diffusion to chloroplasts by ~10,000-70

fold. Evolutionary development of the leaf intercellular airspace (IAS) is therefore 71

considered a key innovation to profit from that lowered diffusion resistance (Ligrone et 72

al., 2012). Yet, terrestrial inhabitation also exposed leaves to the risk of desiccation. 73

Plants presumably navigated this trade-off by developing a complex spatial cellular 74

arrangement in order to produce a more or less tortuous 3D IAS network that rapidly 75

delivered CO2 to the chloroplasts, while maintaining a humid environment inside the leaf 76

to limit evaporative water loss. Perhaps it is unsurprising then that the IAS has long 77

been recognized as almost ubiquitous among terrestrial plants (Sifton, 1945). 78

Leaves utilizing Crassulacean acid metabolism (CAM) exhibit a major contrast in 79

their IAS properties to those engaging the C3 metabolic pathway for photosynthesis, 80

and they frequently occupy the lower end of the IAS volume morphospace. In 81

comparison to C3 leaves, CAM leaves tend to have larger cells that are more densely 82

packed into a given leaf volume, which typically results in lower porosity (Nelson et al., 83

2005). The tendency of CAM plants toward a higher cell volume fraction, i.e. lower 84

porosity, enables greater nighttime storage of CO2 as malic acid in vacuoles, which is 85

then decarboxylated and released as CO2 when stomata are closed during the light 86



5

period (Nelson & Sage, 2008). Consequently, CAM metabolism is generally observed in 87

plants such as epiphytes and succulents, which inhabit water-limited environments 88

(Males, 2016; Griffiths & Males, 2017). C3 plants, on the other hand, tend toward 89

smaller cell sizes, which presumably facilitates greater mesophyll surface exposure to 90

the IAS, allowing more efficient carbon fixation by Rubisco (Maxwell et al., 1997; 91

Griffiths et al., 2008). Lower leaf porosity, more typically associated with CAM 92

metabolism but observed in some C3 plants, lowers the conductance to gas diffusion in 93

the airspace, most often through lower exposure of mesophyll cells to the IAS (Galmés 94

et al., 2013; Sáez et al., 2017). Thus, CAM plants must maintain a trade-off that 95

maximizes vacuolar CO2 storage capacity via tight cell-packing, while avoiding 96

excessive diffusional costs as the IAS simultaneously shrinks. 97

Despite its potential impact on mesophyll conductance, the IAS is generally 98

thought to have relatively higher conductance to CO2 diffusion than the liquid pathways 99

in the leaf. In this study, we first examined the theoretical assumptions within the 100

standard equations used to estimate the effect of IAS geometry on mesophyll 101

conductance. This was done in the context of CAM versus C3 anatomies, as they 102

represent one of the strongest anatomical contrasts with respect to the IAS in the plant 103

kingdom. Specifically, we considered three IAS traits that are often overlooked due to 104

their inherently 3D derivation and difficulty of measurement: tortuosity, lateral path 105

lengthening, and IAS connectivity. Then, we measured and spatially mapped each of 106

these IAS traits, along with other previously measured anatomical traits, for nineteen 107

CAM and C3 Bromeliaceae leaves using X-ray micro-computed tomography (microCT) 108

imaging and used a novel set of computational algorithms. In doing this, we aimed to 109



6

more accurately bound the geometric effect of IAS geometry on mesophyll conductance 110

and provide direction for future research on the IAS. 111

112

A theoretical re-examination of mesophyll intercellular airspace conductance 113

A porous media approximation is typically used to calculate the effect of IAS 114

geometry on the conductance of gas diffusion within the mesophyll pore space (gIAS: 115

Syvertsen et al., 1995; Niinemets and Reichstein, 2003; Tomás et al., 2013): 116

117

gIAS

=θIASDm

Lmesτ [1]

118

where θIAS is mesophyll porosity [m3 m-3], Dm is the diffusivity of CO2 in air [m2 s-1], Lmes 119

is half mesophyll thickness [m], and τ is the tortuosity factor [m2 m-2]. Due to its ease of 120

measurement in two dimensions (2D), previous studies have focused almost exclusively 121

on variation in the porosity term when quantifying the geometric effect of the IAS on 122

mesophyll conductance. While no studies have calculated gIAS for CAM versus C3 123

species, the previously observed lower porosity values of CAM leaves (Nelson et al., 124

2005; Nelson & Sage, 2008) suggest a greater diffusive limitation in the IAS than for C3 125

plants, which corresponds with the very low mesophyll conductance values measured 126

for the CAM species Kalanchoë daigremontiana (Maxwell et al., 1997; Griffiths et al., 127

2008). 128

The complex interconnectivity of the mesophyll, in particular, should act to 129

increase the path length of gaseous diffusion. Yet, due to its inherently 3D nature, IAS 130

tortuosity has been measured only once, in leaves of Arabidopsis thaliana (Lehmeier et 131



7

al. 2017). Moreover, little discussion of its definition and physical derivation exists in the 132

plant literature. Tortuosity is defined as the ratio of the diffusive, or actual travelled, path 133

length (i.e. the geodesic distance or Lgeo) to the straight, or unobstructed, path length 134

(i.e. the Euclidean distance or LEuc) (Gommes et al., 2009; see Fig. 1 for a schematic 135

view of the distances measured, and Fig. 2 for a contrasting view of of Lgeo in two of the 136

measured species). Given that the time, t, required for a molecule to diffuse over a 137

given distance scales with the square of that distance, t ≈ L2/Dm, tortuosity has been 138

shown to have a squared effect on diffusivity in porous media (Gommes et al., 2009). 139

Consequently, the tortuosity factor, τ [m2 m-2], can be defined as the square of the 140

tortuosity: 141

142

τ= (Lgeo

LEuc

)

2

[2]

143

Based on theoretical values derived from the soil literature (Ball, 1981), the tortuosity 144

factor for leaves is typically assumed to equal 1.55 (as used by Syvertsen et al., 1995 145

modelled using the approach of Ball, 1981) or 1.57 (Niinemets and Reichstein, 2003). 146

However, the validity of this ubiquitous assumption in the plant literature and its 147

variability in actual leaves is unknown. In other porous media (e.g. batteries, soils, and 148

cement) a non-linear negative relationship is typically observed between porosity and 149

tortuosity (Boudreau, 1996; Moldrup et al., 2001; Shen & Chen, 2007; Zacharias et al., 150

2013). Hence, the low porosity of CAM leaves may be associated with high tortuosity, 151

which would further decrease the diffusive conductance within the IAS. 152



8

Lateral path lengthening is another inherently 3D property that is overlooked in 153

the standard equations for calculating mesophyll conductance from IAS geometry. 154

Lateral path lengthening results from CO2 entering the IAS through stomata which are 155

discretely distributed across the epidermal surface (Parkhurst, 1994; Pieruschka et al., 156

2005, 2006, 2008; Morison et al., 2005, 2007; Morison & Lawson, 2007). As a result, 157

CO2 must diffuse further to chloroplasts located along the mesophyll surface between 158

two stomata than if the chloroplast is located directly above a stomate. Models of gIAS 159

such as in Eqn. 1 are one-dimensional along the leaf thickness axis and, as noted by 160

Parkhurst (1994), assume that CO2 enters the IAS across the entire epidermis. We 161

propose that lateral path lengthening, λ [m m-1], should be added to Eqn. 1 to account 162

for this effect (Fig. 1): 163

164

gIAS

=θIASDm

λLmesτ [3]

165

As cell packing becomes tighter, such as in CAM species, plants potentially risk 166

disconnecting IAS channels completely, leading to isolated airspace volumes that only 167

link to the atmosphere via a liquid pathway through the cell. Since CO2 diffuses ~10,000 168

times slower in water than in air, IAS disconnection can dramatically reduce the CO2 169

supply rate to these isolated uptake sites, and their relative contribution to the total 170

mesophyll surface area available for chloroplast inhabitation, and ultimately leaf-level 171

photosynthetic capacity, should be low (Fig. 1). Except at coarse spatial scales (Long et 172

al., 1989; Morison et al., 2007), IAS connectivity has not been measured in leaves and, 173

thus, its biological significance in CAM versus C3 species is unknown. Further, IAS 174



9

connectivity (κSA; m2 m-2), which we define as the fraction of the mesophyll surface area 175

which is connected to the largest IAS pore (i.e. the largest connected airspace volume 176

within a leaf sample; see Fig. 1 for a schematic representation), is not currently 177

accounted for in the basic equations used to estimate conductance from mesophyll 178

anatomy. Such a modification to the standard equation (Nobel, 2009) for mesophyll 179

conductance would take the following form: 180

181

gm

= (1

gIAS

+1

κSASc

1

gliq

)

-1

[4]

182

where Sc is the chloroplast surface area exposed to the IAS per square meter of leaf 183

surface area and gliq is the liquid phase conductance which can be subdivided into 184

diffusive contributions from the cell wall, plasmalemma, cytosol, chloroplast envelope, 185

and chloroplast stroma (Evans et al., 2009). Thus, in our formulation, IAS disconnection 186

lowers mesophyll conductance by reducing the total mesophyll surface area available 187

for diffusion. 188

Based on these theoretical considerations, it is clear that 3D IAS traits, beyond 189

porosity, could meaningfully contribute to the gaseous phase of mesophyll conductance. 190

We have thus measured these geometric traits from actual 3D IAS geometries in 19 191

Bromeliaceae species (Table 1) that capture a broad gradient of C3 and CAM types 192

while constraining our study to a single family (see cross-sectional views in Fig. 3). 193

194

RESULTS 195

Porosity, cell packing, and mesophyll surface area 196



10

After controlling for phylogenetic relatedness, CAM and C3 bromeliads had 197

significant differences in porosity (θIAS) at 0.10 ± 0.01 and 0.37 ± 0.07 m3 m-3, 198

respectively (p < 0.01; Fig. 4). At the extreme ends of leaf porosity were the CAM 199

species Tillandsia recurvata (0.04 – Fig. 5a) and the C3 species of Brocchinia 200

hechtioides (0.73 – Fig. 5n; Table 2). Conversely, mesophyll tissue accounted on 201

average for 90% and 63% of total mesophyll volume, indicating a higher cell-packing 202

density in CAM versus C3 bromeliads. CAM mesophyll cells tended to have a 203

significantly larger diameter, Lcell, at 45 ± 3 µm than the cells in C3 species, at 21 ± 3 µm 204

(p < 0.01; Fig. 4), with a minimum of 12 µm in Guzmania lingulata and a maximum of 70 205

µm in Tillandsia recurvata. While no statistical difference in mesophyll surface area 206

exposure to the IAS on a leaf-surface-area basis (Sm) was observed between CAM and 207

C3 species (p < 0.25; Fig. 4), the larger cells, lower porosity, and higher cell-packing 208

density in CAM species corresponded with lower mesophyll surface area exposure to 209

the IAS on a mesophyll-volume basis (Ames/Vmes; p < 0.05; Fig. 4). 210

211

Diffusive path lengthening 212

CAM bromeliads had significantly thicker mesophyll tissue at 511 ± 47 µm than 213

C3 species at 249 ± 40 µm (Lmes; p < 0.01; Fig. 4). Aechmea fendleri has, however, 214

exceptionally thin CAM leaves with a mesophyll thickness of 130µm (Table 2). IAS 215

tortuosity (τleaf) was on average 1.67 ± 0.17 m m-1 for CAM and 1.16 ± 0.02 m m-1 for C3 216

bromeliads (p < 0.01; Fig. 4), reaching extreme values of 1.09 and 3.33 in Brocchinia 217

hechtioides (C3 – Fig. 6n) and Tillandsia usneoides (CAM – Fig. 6c) (Table 2). Lateral 218

path lengthening (λleaf), while not significantly different between CAM and C3 species (p 219



11

= 0.09), ranged broadly from 1.1 to 3.2 m m-1 (Fig. 4; Table 2) and was higher in 220

species with a low stomatal density and/or long horizontal IAS channels like Guzmania 221

zahnii (Fig. 7q) and Tillandsia caulescens (Fig. 7b). CAM bromeliads had an average 222

diffusive path length (leaf level averaged Lgeo, Lgeo,leaf) of 1186 ± 211 µm, whereas C3 223

species averaged 371 ± 56 µm (p < 0.01; Lgeo,leaf, Table 2; see also Fig. 2 for a 3D 224

rendering of Lgeo throughout the airspace of a C3 and CAM species). Thus, thicker 225

mesophyll tissue was associated with high tortuosity and long lateral path lengths that 226

amplify the average diffusive path length. 227

228

IAS connectivity 229

C3 bromeliads had a significantly higher fraction of their mesophyll surface area 230

connected to stomatal inlets, or κSA, at 0.94 ± 0.01 than CAM bromeliads at 0.88 ± 0.01 231

(p < 0.01; Fig. 4). Two CAM species, Aechmea penduliflora (Fig. 8j) and Bilbergia 232

elegans (Fig. 8i), had the lowest values of κSA at 0.79 and 0.81, respectively; whereas 233

the C3 species of Brocchinia hechtioides (Fig. 8n) had the highest κSA of 0.97 (Table 2). 234

235

Coordination of porosity with tortuosity, lateral diffusivity, and IAS connectivity 236

Porosity (θIAS) was non-linearly and negatively related to tortuosity with τleaf rising 237

steeply as porosity became lower than ~0.1 (Fig. 9; τleaf=θIASα

, α = -0.18, p < 0.01, R2 = 238

0.55). Similarly, θIAS was non-linearly and negatively related to the lateral diffusivity 239

factor (Fig. 9; λleaf=θIASα

, α = -0.26, p < 0.01, R2 = 0.48). IAS connectivity on a mesophyll 240

surface area basis (κSA), on the other hand, showed a non-linear and positive 241

relationship with θIAS (Fig. 9; κSA=θIASα

, α = 0.05, p < 0.01, R2 = 0.19). 242



12

243

IAS conductance 244

Conductance of the intercellular airspace (gIAS) was calculated using the 245

standard equation (Eqn. 4) and our modified equation (Eqn. 6). Using the standard 246

equation (Eqn. 4), which assumes a constant tortuosity factor of 1.57 and no lateral 247

diffusivity, the average gIAS was 0.17 ± 0.02 mol m-2 s-1 bar-1 for CAM species and 1.36 248

± 0.28 mol m-2 s-1 bar-1 for C3 (open circles, Fig. 10). After accounting for variation in 249

τleaf and λleaf across species (Eqn. 6), and for phylogenetic relatedness, CAM species 250

had a significantly lower value of gIAS at 0.11 ± 0.02 mol m-2 s-1 bar-1 compared to C3 251

plants at 1.31 ± 0.28 mol m-2 s-1 bar-1 (p > 0.05; filled circles, Fig. 10). These changes 252

corresponded with an average reduction in gIAS of 37 ± 25 (SD)% for CAM species and 253

3.5 ± 16% for C3 species, when compared to estimates using the assumed tortuosity 254

factor of 1.57 (Fig. 10). 255

256

Spatial localization of low IAS conductivity 257

The leaves of CAM and C3 bromeliads varied broadly in their spatial distribution 258

of porosity, tortuosity, lateral diffusivity, and intercellular airspace connectivity (Figs. 5 to 259

8). With the exception of the leaves of Ochagavia carnea, those of all C3 plants tended 260

to have a large central IAS pore that became less porous radially toward the veins and 261

epidermal surfaces (Fig. 5). While the leaves of some CAM plants, such as Aechmea 262

fulgens and Deuterochonia schreiteri, had one or a few central air channels, the IAS 263

tended to be smaller and more homogenous, also becoming less porous toward the 264

veins and epidermal surfaces (Fig. 5). In both CAM and C3 leaves, high τleaf, λleaf, and 265



13

κSA were often co-localized in low-porosity regions between the vein and the abaxial 266

epidermis, suggesting a consistent pattern for low gIAS in these regions across 267

bromeliads (Figs. 6 to 8). Several CAM species, such as Aechmea penduliflora and 268

Hechtia caerulea, had higher tortuosity and IAS disconnection surrounding the veins 269

and in the abaxial regions of the mesophyll tissue (Figs. 6 to 8). Large regions of high 270

tortuosity tissue occurred in Tillandsia caulescens, Tillandsia usneoides, and Quesnelia 271

marmorata (Fig. 6b, c, h). 272

273

DISCUSSION 274

CAM and C3 bromeliads have evolved distinct leaf geometries that correspond 275

with their tendency to inhabit drier and wetter environments, respectively. While most of 276

the plants sampled were grown in conservation greenhouses (see Table 1), which might 277

not reflect their natural growth environment and therefore might affect leaf anatomy and 278

δ13C values, our results were similar to previous observations for Orchidaceae (Silvera 279

et al., 2005, 2010), Asparagaceae (Heyduk et al., 2016), and Bromeliaceae (Maxwell, 280

2002; Pierce et al., 2002; Nelson et al., 2005) plants, with the values of some being 281

measured on specimens from their native environment. On average, we found thicker 282

leaves (Lmes) with larger cells (Lcell) in CAM versus C3 species (Fig. 4). When combined 283

with significantly lower porosity (θIAS; Fig. 4), these traits led to greater cell packing (as 284

in Nelson et al., 2005), giving rise to the “succulent syndrome” often associated with 285

CAM species (Griffiths et al., 2008; Arakaki et al., 2011; Griffiths & Males, 2017). 286

Hydraulically, high succulence allows for long-term water storage via chlorenchyma 287

and/or hydrenchyma cells, which can buffer the effects of dehydration during prolonged 288



14

periods without precipitation (Males, 2016). Larger cells with higher packing rates tend 289

to reduce the total surface area that CAM plants can pack into their mesophyll volume 290

(Ames/Vmes; Fig. 4), effectively lowering gas exchange capacity by decreasing the liquid 291

phase conductance at the leaf level (see Eqn. 4; Nelson et al., 2008). 292

Theoretically, the distinct anatomical features of CAM plants, i.e. thick mesophyll 293

and low porosity, should reduce mesophyll conductance (gm; see Lmes and θIAS in Eqn. 294

1). Consistent with this prediction were the results of Griffiths et al. (2008), who 295

measured a gm of 0.06 mol m-2 s-1 bar-1 in the CAM species Kalanchoë 296

daigremontiana—a value ~40% lower than that measured for the related C3 genus 297

Kalanchoë pinnata. Isotopic measurements also point toward diffusional limitations 298

within the mesophyll of Kalanchoë daigremontiana (Griffiths et al., 2007). To the best of 299

our knowledge, in addition to the studies by Griffiths and colleagues and the one by 300

Maxwell et al. (1997) on Kalanchoë daigremontiana, no other studies measured gm in 301

other CAM species (Ripley et al., 2013 did measure it in some Aizoaceae plants, but 302

these plants were largely performing C3 photosynthesis). More broadly across the plant 303

kingdom, and based on this single observation, CAM plants are thought to possess 304

among the lowest gm values, similar to or below those measured for evergreen 305

gymnosperms and evergreen angiosperms (see references in Flexas et al., 2008, and 306

the recent measurements reported by Veromann-Jürgenson et al., 2017). Our 307

estimation that on average, for twelve CAM bromeliads, gIAS is 0.11 ± 0.02 mol m-2 s-1 308

bar-1, with extreme values of 0.01 and 0.19 mol m-2 s-1 bar-1 (Fig. 10), implies that the gm 309

for these leaves is similar to or lower than the previously measured gm values for 310

Kalanchoë daigremontiana (0.06 mol m-2 s-1 bar-1; Maxwell et al., 1997; Griffiths et al. 311



15

2008) and at the lower end across the plant kingdom (Flexas et al., 2008; Fig. 10). 312

Thus, the IAS likely plays a critical role in controlling gm within these CAM bromeliads 313

and could represent about 50% of the total resistance to CO2 diffusion within the 314

mesophyll (gIAS-1/gm

-1 of Kalanchoë daigremontiana = 0.11-1/0.06-1 = 0.54). The C3 315

bromeliads, on the other hand, had an average gIAS of 1.31 mol m-2 s-1 bar-1, with 316

extreme minima and maxima of 0.41 mol m-2 s-1 bar-1 and 2.38 mol m-2 s-1 bar-1 (Fig. 317

10), respectively, suggesting that gliq is the dominant constraint on gm for these species 318

and as shown for multiple C3 species (Tomás et al., 2013; Tosens et al., 2016). 319

However, for an accurate comparison of the respective contributions of gIAS and gliq to 320

gm, one would need to measure cell anatomical features such as wall thickness, 321

measurements that are lacking in our microCT data. 322

Across various plant taxa, the IAS is considered to have a relatively small effect 323

on gm compared to liquid phase traits, particularly cell wall thickness (Flexas et al., 324

2008; Tomás et al., 2013; Carriquí et al., 2015). Typical estimations of gIAS, however, 325

assume that only mesophyll thickness and porosity contribute to its variation; the 326

tortuosity factor (τleaf) is generally held constant at 1.57, while potential effects of lateral 327

path lengthening (λleaf) and IAS connectivity (κSA) are neglected because they were not 328

empirically measurable until now. Here, we modified the standard equations to account 329

for these additional IAS traits that are difficult to measure with traditional microscopy 330

(Eqns. 1, 3 and 4). Incorporating variation in τleaf and λleaf in the estimation of gIAS had 331

greater consequences for CAM bromeliads, with our new equation producing mean gIAS 332

values 37 ± 25 (SD)% lower (range from +6 to -82%) than one would calculate with 333

previous equations. Our analysis of C3 leaf geometry, however, suggests that adding 334



16

these new terms to the gIAS equation yields estimates only 3.5 ± 16% lower, with most 335

species having estimates within 10% of those obtained using the old equation. Two 336

extreme C3 deviations for gIAS were found and these were caused by extreme λleaf 337

values (+27%, Brocchinia hechtioides; -28%, Guzmania zahnii; Fig. 10). This substantial 338

variation among species highlights the importance of characterizing the 3D properties of 339

the IAS when considering the relative contribution of gIAS to gm. 340

This study provides among the first measurements of leaf IAS tortuosity across a 341

large leaf anatomical spectrum (see Lehmeier et al., 2017 for tortuosity measurement in 342

Arabidopsis thaliana), as all other previous values were based on a simplified 343

theoretical model from the soil literature (Ball, 1981). Our microCT measurements 344

suggest that the standard assumption of 1.57 m2 m-2 for τleaf is an overestimate 345

compared to our purely geometrical estimates for C3 (average of 1.16) and an 346

underestimate for CAM bromeliads (average of 1.67; Fig. 4). Across the nineteen 347

species examined, we measured an approximately three-fold range for τleaf (Fig. 4; 348

Table 2), the value of which could be reasonably estimated as: τleaf=θIAS-0.18

(Fig. 9). 349

Depending on the degree of variability in θIAS (e.g. see Théroux-Rancourt et al., 2017), 350

this relationship could be used to estimate τleaf based on 2D sections. Thus, τleaf tends to 351

increase as porosity decreases, leading to a compounding effect on gIAS. In future 352

studies, it would be interesting to investigate if the range of tortuosity values observed 353

across CAM and C3 bromeliads are broadly representative for species throughout the 354

plant kingdom. 355

Early theoretical work identified the potential importance of lateral diffusion for 356

CO2 transport due to the discrete spacing of stomata (Parkhurst, 1977). Previous 357



17

studies have since empirically demonstrated that lateral diffusion can significantly 358

contribute to CO2 delivery within certain types of leaves by using spatially explicit gas 359

exchange and fluorescence measurements (Parkhurst, 1994; Pieruschka et al., 2005, 360

2006, 2008; Morison et al., 2005, 2007; Morison & Lawson, 2007). Despite these 361

findings, the standard equations for estimating the IAS contribution to gm does not 362

account for lateral diffusivity (Eqn. 1). This omission necessarily underestimates the 363

effect of lateral path lengthening (λleaf) for both CAM and C3 bromeliads, and reflects the 364

difficulty of making such measurements. We measured an average λleaf of 1.78 m m-1 365

for CAM and 1.42 m m-1 for C3 species, and a nearly three-fold range in variability (Fig. 366

4; Table 2). Similar to τleaf, a non-linear and negative relationship exists between λleaf 367

and θIAS (Fig. 9), suggesting a coordinated decline in gIAS due to multiple IAS traits 368

simultaneously. Accounting for the effect of λleaf on gm might be especially important for 369

species with low stomatal density and thin leaves. Non-angiosperms, such as 370

lycophytes, ferns, conifers, and cycads, for example, tend to have relatively low 371

stomatal densities (Franks & Beerling, 2009; Lammertsma et al., 2011), pointing toward 372

an interesting avenue for future research. 373

Despite its potential impact on gm, IAS connectivity has rarely been studied in 374

leaves. We are only aware of one investigation in which the upper and lower mesophyll 375

of Zea mays leaves were shown to have low connectivity based on serial sectioning 376

scanning electron microscopy (Long et al., 1989). In this study, we operationally define 377

IAS connectivity (κSA) as the fraction of mesophyll surface area that is connected to the 378

primary IAS pore. Presumably, CO2 diffusion due to pores (and associated surface 379

area) disconnected from the primary IAS would be quite limited due to the presence of 380



18

liquid cellular barriers. We measured an average κSA of 0.88 m2 m-2 for CAM and 0.94 381

m2 m-2 for C3 species, with that for leaves being as low as ~0.80 m2 m-2 (Figs. 4 and 8; 382

Table 2). The standard equations for estimating the IAS contribution to gm omit the 383

effect of κSA and, consequently, based on our measurements underestimate the effect of 384

IAS disconnection on gm for both CAM and C3 bromeliads. However, it is important to 385

note that the microCT scans used in this study have a voxel dimension of 0.64 µm 386

which results in a feature resolution of ~1.9 m. Since pore diameters below 1.9 µm 387

likely exist in the IAS, our values of κSA are likely an underestimation. That said, pores 388

around or below this diameter would be operating at the boundary of the Knudsen 389

diffusion regime, in which the length of the mean free diffusive path is similar to the pore 390

diameter (Leuning, 1983; Parkhurst, 1994), resulting in a ‘constrictivity’ effect on 391

diffusion. Moreover, as the ratio of mesophyll surface area to IAS volume increases with 392

shrinking pore diameter, local reactive demand would effectively increase the resistance 393

to vapor diffusion in favor of liquid diffusion. Future research using higher resolution 394

imaging could examine if, when, and where IAS pores are truly disconnected via cell-to-395

cell barriers, along with the theoretical effects of reaction-diffusion systems operating 396

within the Knudsen diffusion regime. 397

Vertical and lateral gradients in [CO2] are thought to exist throughout the leaf due 398

to geometric and biochemical heterogeneity (Parkhurst & Mott, 1990; Pieruschka et al., 399

2005; Evans & Vogelmann, 2006; Earles et al., 2017). Our observations suggest 400

substantial heterogeneity in gIAS throughout the mesophyll, as implicated by the spatial 401

patterns of θIAS, τleaf, λleaf, and κSA (Figs. 5 to 8). Moreover, we find the tendency toward 402

co-localization for each of these traits, often between the vein and the abaxial 403



19

epidermis, which would amplify the reduction in gIAS within certain regions of the 404

mesophyll. Depending on the distribution of reactive demand, this heterogeneity in gIAS 405

could contribute to the generation of strong [CO2] gradients throughout the leaf. Such 406

gradients may be particularly prevalent in CAM-type geometries during periods of 407

Rubisco carboxylation, creating regions in which chloroplasts would have very limited 408

access to CO2 unless CO2 is provided by malic acid decarboxylation. In this case, as 409

the source of carbon would now originate from neighboring cells and not stomata, τleaf 410

and λleaf values would be lowered, hence suggesting that CAM-type geometries could 411

be optimized for internal recycling of respiratory and decarboxylated CO2. It would also 412

be interesting to understand if low gIAS regions are effectively ‘uninhabitable’ for 413

chloroplasts due to low CO2 availability, a question that cannot currently be answered 414

using our microCT data because chloroplasts are not visible. Moreover, whether such 415

heterogeneity in gIAS corresponds with gradients in δ13C previously observed throughout 416

the leaf (Robinson et al., 1993) is unknown. 417

In the absence of access to microCT or volumetric leaf anatomical data to 418

measure τ and λ, we recommend estimating them together as a function of θIAS, 419

assuming that the porosity value is representative of the leaf (Théroux-Rancourt et al., 420

2017). Multiplying the two functions of porosity presented previously gives 421

(τleaf(θIAS)λleaf(θIAS))=θIAS-0.44

, or θIAS-0.53

when fitting a power function to the product of τleaf 422

and λleaf. Both functions are close to the assumption that tortuosity can be near θ-0.5 423

(e.g. Boudreau 1996). Our dataset covers a broad range of porosity values but is quite 424

specific to certain leaf anatomy. Hence, θIAS-0.5 would be a reasonable replacement of 425

τleaf and λleaf in Eqn. 3 and would be a better approach than using a literature value that 426



20

might be unrepresentative of the studied leaf anatomy, especially at porosity values 427

below 0.2 m3 m-3. 428

In conclusion, new methods such as microCT make IAS traits available and can 429

extend our understanding of internal leaf geometry beyond porosity, which makes it 430

possible to more accurately partition gm and gIAS. Based on our investigation of 19 CAM 431

and C3 Bromeliaceae species, tortuosity, lateral path lengthening, and IAS connectivity 432

are likely to have a significant impact on gIAS. Since these traits have largely not been 433

measured in leaves, their broader influence on gIAS across the plant kingdom is 434

unknown. Thus, we recommend that the potential impact of the IAS on gm be carefully 435

reconsidered, and we have provided a suggestion on how to obtain a more 436

representative tortuosity estimate from 2D cross sections based on a relationship to 437

porosity. Imaging tools such as X-ray microCT and the 3D image-processing techniques 438

employed in this study provide a platform for beginning to answer such questions. 439

440

METHODS 441

Plant materials 442

We selected 19 Bromeliaceae species for analysis (Table 1), which capture a 443

broad gradient of functional groups within both C3 and CAM types while constraining 444

our study to a single family (see cross-sectional views in Fig. 3). Plants were classified 445

as CAM or C3 based on the δ13C values described in Crayn et al. (2015; see Table 1). 446

While specifying an exact cutoff value is somewhat arbitrary, we defined CAM and C3 447

species as having δ13C values greater than −20‰ and less than −20‰, respectively, in 448

accordance with Pierce et al. (2002) and Winter et al. (2015). Plant specimens were 449



21

collected at the University of California Botanical Gardens (UCBG) from conservation 450

and display greenhouses and from outdoor displays (Berkeley, CA), and the UC Davis 451

(UCD) Botanical Conservatory greenhouse (Davis, CA; see Table 1 for growth 452

conditions). Both at UCBG and UCD, greenhouse plants were watered appropriately 453

several times per week by their respective staff, and species grown in the arid 454

greenhouse were watered once a week. Outdoor plants at UCBG received only rainfall 455

during winter and were lightly watered once a week during the dry and rain-free months 456

of summer, which might annually result in more water input than in their native habitats. 457

For each species, several leaves from healthy plants were excised, immediately placed 458

into a sealed plastic bag containing a damp paper towel and stored in a dark insulated 459

box. Leaves were then transported to the Lawrence Berkeley National Laboratory 460

Advanced Light Source (LBNL ALS) for X-ray microCT imaging at beamline 8.3.2 within 461

24 hours of excision. 462

463

X-ray microCT imaging, segmentation, and classification 464

Samples were prepared for microCT imaging as described in Théroux-Rancourt 465

et al. (2017). Before each scan (<30 min), one ~1.5-to-2-mm-wide and ~20-mm-long 466

sample was excised near the first third of the leaf, starting from the apex of a fully 467

developed leaf. They were then enclosed between two pieces of Kapton (polyimide) 468

tape to prevent desiccation while allowing high X-ray transmittance. Subsequently, they 469

were placed in a pipette tip, mounted in the sample holder, centered in the microCT X-470

ray beam, and scanned using the continuous tomography mode capturing 1,025 471



22

projection images at 21 keV, using a 10x objective lens, yielding a final pixel resolution 472

of 0.64 µm. Each scan was completed in approximately 15 minutes. 473

Image reconstruction was carried out using TomoPy, a Python-based framework 474

for reconstructing tomographic data (Gürsoy et al., 2014). Each raw dataset was 475

reconstructed using both the gridrec (Dowd et al., 1999) and phase retrieval 476

reconstruction methods (Davis et al., 1995). Image stacks were rotated and aligned 477

such that the veins were viewed in transverse section orthogonal to the epidermises. 478

We then cropped the tissue to focus on a region of interest between the two major 479

veins, such that the left and right image boundaries bisected two veins and the image 480

was composed entirely of mesophyll. Sample regions where desiccation occasionally 481

occurred during sample preparation were discarded. The final stacks contained ~500 8-482

bit greyscale images (downsampled from 32-bit). Image processing was applied equally 483

among scans using ImageJ software (Schneider et al., 2012). 484

The initial image segmentation and classification into intercellular airspace (IAS), 485

mesophyll cell, vein, and background voxels were also performed as described in 486

Théroux-Rancourt et al. (2017). For both the gridrec and phase-reconstructed images, 487

the airspace was segmented first by visually and subjectively defining a range of pixel 488

intensity threshold values between a minimum and maximum grayscale value to 489

optimize air space classification while minimizing false classification (i.e. non-airspace 490

pixels). After combining the binary image stacks from both reconstruction types, the 491

mesophyll, veins, and background voxels were manually classified, which resulted in a 492

composite image stack with cells, airspace, veins and background voxels classified 493

uniquely (Fig. 3). 494



23

495

Leaf-trait quantification from 3D images 496

Mesophyll and cell dimensions: Cell diameter, Lcell [µm], was averaged for each species 497

from measurements in ImageJ of 30 to 50 randomly selected cells in cross-section and 498

paradermal slices. The mesophyll thickness, Lmes [µm], considered as the tissue 499

excluding the epidermises and any hydrenchyma present, was averaged from over 10 500

cross-sections and manually measured in ImageJ. 501

502

Mesophyll porosity and surface area: As done by Théroux-Rancourt et al. (2017), the 503

ImageJ plugin BoneJ Particle Analyzer function (Doube et al., 2010) with a resampling 504

rate of one was used to quantify the IAS volume, VIAS [µm3], the total mesophyll volume 505

(minus veins and epidermis), Vmes [µm3], and the mesophyll surface area exposed to the 506

IAS, Ames [µm2]. Mesophyll porosity, θIAS [m3 m-3], was then calculated as the IAS 507

volume as a fraction of the total mesophyll volume. Cell packing was then simply 508

defined as 1 – θIAS. Mesophyll surface area per mesophyll volume, Ames/Vmes [µm2 µm-3], 509

was then calculated. Mesophyll surface area per projected leaf area, Sm [m2 m-2], was 510

then calculated as the ratio, Ames/Aleaf [m2 m-2], where Aleaf [m

2] is the surface area of the 511

leaf sample stack, defined as the image width multiplied by stack depth (i.e. the area of 512

the paradermal view). 513

514

Tortuosity, lateral diffusivity, and IAS conductance: As in Eqn. 2, the tortuosity factor, τ 515

[m2 m-2], was defined as the ratio of the diffusive path length within the IAS, i.e. the 516

actual path from the stomate to a cell surface (geodesic distance, Lgeo), to the straight 517



24

path length in the absence of any physical obstacles to diffusion between the stomate 518

and the cell surface (Euclidean distance, LEuc; Gommes et al., 2009; see Fig. 1 for a 519

visual description of the different lengths measured). To calculate Lgeo and LEuc, we first 520

generated a binary image of the stomatal inlets for each leaf. Then, we calculated two 521

geodesic distance maps using the ImageJ plugin MorpholibJ (Legland et al., 2016). The 522

first map, Lgeo, quantified the shortest distance from the nearest stomatal inlet to all 523

points along the mesophyll surface within the geometric bounds of the IAS, i.e. with 524

cells causing obstructions that increase the path length. The second map, LEuc, 525

quantified the Euclidean distance, i.e. the unobstructed distance, from the nearest 526

stomatal inlet to all points along the mesophyll surface. In this way, we defined Lgeo and 527

LEuc for all voxels along the mesophyll surface and simply calculated τ at these voxels 528

using Eqn. 2 for the entire 3D image array. The leaf-level tortuosity, τleaf, was then 529

calculated as the mean of τ, representing the average mesophyll surface voxel. 530

To calculate lateral path lengthening, λ [m m-1], we used the previously 531

generated distance map, LEuc. Then, we created a second distance map, again using 532

the ImageJ plugin MorpholibJ (Legland et al., 2016), to quantify the shortest 533

unobstructed straight-line distance between the lower epidermis and all points along the 534

mesophyll surface, Lepi (Fig. 1). From these two distance maps, we calculated λ at all 535

voxels along the mesophyll surface as: 536

λ=LEuc

Lepi

[5]

By doing this, we quantified the surface-area weighted deviation from the standard 1D 537

assumption that CO2 enters the IAS across the entire epidermis (Parkhurst, 1994). Leaf-538



25

level lateral path lengthening, λleaf, was then calculated as the mean of λ, representing 539

the average mesophyll surface voxel. 540

Using leaf-level tortuosity and lateral diffusivity factors, we then calculated leaf-541

level IAS conductance as: 542

gIAS

=θIASDm

λleafLmesτleaf

[6]

543

IAS connectivity: We define IAS connectivity (κSA, m2 m-2) as the fraction of the 544

mesophyll surface area which is connected to the largest IAS pore, i.e. the largest 545

airspace volume (or connected voxels) within the leaf from stomata to the palisade 546

mesophyll. Based on the examination of our microCT data, the largest IAS pore is 547

always connected to the stomata and, consequently, the atmosphere. Hence, any 548

mesophyll surface area or volume that is not connected to the largest IAS pore is 549

defined as disconnected. We apply the ImageJ plugin BoneJ Particle Analyzer function 550

(Doube et al., 2010), which applies a 3-pass non-recursive approach to map voxel 551

neighborhoods as in a graph and merges them, to quantify the volume and surface area 552

of unique particles. We then quantify κSA as the surface area of the largest IAS particle 553

divided by the sum of the surface area for all IAS particles. Since our microCT images 554

have an isotropic voxel resolution of 0.64 µm, our technique would be less able to 555

appropriately detect continuous IAS channels of a diameter less than three times the 556

voxel resolution (1.9 µm diameter), which would lead to an apparent disconnection 557

between two connecting larger volumes (addressed in the Discussion section). 558

559



26

2D spatial trait maps: To examine the spatial distribution of porosity, the tortuosity 560

factor, IAS connectivity, and the lateral diffusivity factor, we created 2D transverse 561

projections for each trait. These projections show an average voxel value for each trait 562

within a transverse leaf section. In the case of binary traits, like porosity and IAS 563

connectivity, the 2D porosity projection defines the likelihood of IAS presence and 564

connectivity respectively. Thus, these projections have values ranging from 0 to 1. 565

Importantly, the IAS connectivity likelihood value is conditional on IAS presence – so, a 566

value of 0.9 indicates a 90% chance of IAS connectivity for a voxel stack that contains 567

airspace. The tortuosity and lateral diffusivity factors, on the other hand, are average 568

voxel values for each trait. 569

570

Statistical analysis 571

Although many of the species used in the present study have not been included 572

in recently molecular phylogenetics studies of the Bromeliaceae, their taxonomy is well 573

accepted. We used the R package pastis (Thomas et al., 2013) to generate a Nexus-574

formatted input for MrBayes (v. 3.2.7; Ronquist et al., 2012), which used the species-575

level phylogeny from Givnish et al. (2011) as a constraint tree and the taxonomic 576

affinities of species sequenced by Givnish et al. (2011) to place the species in the 577

current study into a well-resolved phylogeny. Bayesian analysis of this existing 578

phylogeny was run for 50,000,000 generations with a 5,000,000 generation burn-in. 579

Phylogenetically controlled analyses were performed using the consensus tree 580

generated by MrBayes. Phylogenetic t-tests were performed using the phylANOVA 581

function in the R package phytools (Revell, 2012). To assess evolutionary correlations 582



27

between traits, Spearman rank correlations of phylogenetic independent contrasts 583

(Felsenstein, 1985) were performed using the cor.table function in the R package 584

picante (to improve normality, data were log-transformed; Kembel et al., 2010). 585

Because of the non-linearity of the correlations between many traits, we used the 586

nonparametric Spearman rank correlations rather than parametric Pearson correlations 587

between independent contrasts. To compare different methods for measuring the 588

conductance of the intercellular airspace (gIAS), we used a phylogenetic paired t-test 589

(phyl.pairedttest) as implemented in the R package phytools. Non-linear regressions 590

between traits were performed using the nls library in the base R package. 591

592

Acknowledgements 593

We thank Ernesto Sandoval (UC Davis Botanical Conservatory) and Holly 594

Forbes (UC Berkeley Botanical Garden) for the plant material collected. We also thank 595

Sean McDowell (UC Davis) for his assistance in data processing, and Jamie Males for 596

validating the growth habits of the studied Bromeliaceae plants. We thank John Evans 597

and two anonymous reviewers for their helpful comments on the manuscript. GTR was 598

supported by a Katherine Esau Postdoctoral Fellowship. ABR was supported by the 599

Yale Institute of Biospheric Studies. The Lawrence Berkeley National Laboratory 600

Advanced Light Source is supported by the Director, Office of Science, Office of Basic 601

Energy Sciences, of the U.S. Department of Energy under Contract No. DE-AC02-602

05CH11231. 603

604



28

Table 1: Nineteen Bromeliaceae species investigated and the associated δ13C values 605

from Crayn et al. (2015), CAM versus C3 classification based on a -20‰ threshold 606

(Winter et al., 2015) and IDs that correspond with images in Figure 3. Definitions for 607

plant habit are adapted from Males and Griffiths (2018). 608

609

Species δ13C (‰) Habit Growth conditions

ID

CAM

Tillandsia recurvata (L.) L. -15.9 Atmospheric epiphyte

GH a

Tillandsia caulescens Brongn. ex Baker -14.8 Atmospheric epiphyteb

GH b

Tillandsia usneoides (L.) L. -14.4 Atmospheric epiphyte

GH c

Acanthostachys strobiliacea (Schult. & Schult.f.) Klotzsch

-16.1 Epiphyte GH d

Aechmea fulgens Brongn. -13.5 Tank epiphyte GH (UCD) e Hechtia marnier-lapostolleii L.B.Sm. -11.9 Terrestrial Arid GH f Deuterochonia schreiteri A.Cast. -11.4 Terrestrial Outdoor g Quesnelia marmorata (Lem.) Read -14.0 Terrestrial GH h

Bilbergia elegans Mart. ex Schult. & Schult.f.

-16.6 Tank epiphyte GH (UCD) i

Aechmea penduliflora André -15.2 Tank epiphyte GH j Hechtia caerulea (Matuda) L.B.Sm. -15.8 Terrestrial Arid GH k Aechmea fendleri André ex Mez -11.1 Tank epiphyte GH (UCD) l

C3

Ochagavia carnea (Beer) L.B.Sm. & Looser

-21.5 Terrestrial Outdoor m

Brocchinia hechtioides Mez. -23.7 Tank lithophyte GHa n Greigia sphacelata (Ruiz & Pav.) Regel -31.3 Terrestrial Outdoor o Pitcairnia tabuliformis Linden -30.2 Terrestrial GH p

Guzmania zahnii (Hook.f.) Mez -24.0 Tank epiphyte GH q

Nidularium innocentii Lem. -33.3 Tank epiphyte GH (UCD) r Guzmania lingulata (L.) Mez -28.0 Tank epiphyte GH (UCD) s a: GH stands for greenhouse, and all plants were grown at the University of California Botanical 610 Garden (UCBG) except when specified (UCD: University of California - Davis Botanical 611 Conservatory). Growth conditions are described in the Methods section. 612 b: Tillandsia caulescens is probably a transition between tank and atmospheric epiphytes as it is 613 grown usually upwards and has some small tanks. 614 615



29

Table 2: For each species examined, leaf-level values of porosity (θIAS; m3 m-3), 616

mesophyll thickness (Lmes; µm), tortuosity factor (τleaf; m2 m-2), lateral path lengthening 617

(λleaf; m m-1), IAS connectivity (κSA; m2 m-2), leaf averaged geodesic path length (Lgeo,leaf; 618

µm), and IAS conductance (gIAS; mol m-2 s-1 bar-1) calculated from Eqn. 6. 619

620

Species θIAS Lmes τleaf λleaf κSA Lgeo,leaf gIAS

CAM

Acanthostachys strobiliacea 0.10 588 1.29 1.55 0.88 1035 0.10 Aechmea fendleri 0.05 130 1.57 2.51 0.92 409 0.11 Aechmea fulgens 0.12 519 1.64 1.53 0.87 1017 0.11 Aechmea penduliflora 0.08 364 1.65 1.35 0.79 631 0.12 Bilbergia elegans 0.15 474 1.37 1.49 0.81 827 0.19 Deuterochonia schreiteri 0.16 701 1.28 1.14 0.94 904 0.19 Hechtia caerulea 0.08 374 1.32 1.30 0.86 559 0.16 Hechtia marnier-lapostolleii 0.20 652 1.42 1.64 0.91 1274 0.16 Quesnelia marmorata 0.09 487 1.76 1.47 0.89 950 0.08 Tillandsia caulescens 0.04 540 2.20 3.19 0.92 2555 0.01 Tillandsia recurvata 0.10 707 1.26 1.70 0.89 1349 0.08 Tillandsia usneoides 0.04 591 3.33 2.52 0.90 2718 0.01

C3

Brocchinia hechtioides 0.73 340 1.09 1.12 0.97 398 2.17 Greigia sphacelata 0.38 396 1.14 1.41 0.92 596 0.73 Guzmania lingulata 0.40 127 1.12 1.46 0.90 196 2.38 Guzmania zahnii 0.37 168 1.13 1.90 0.94 339 1.28 Nidularium innocentii 0.30 152 1.23 1.33 0.94 224 1.48 Ochagavia carnea 0.19 335 1.23 1.42 0.95 528 0.41 Pitcairnia tabuliformis 0.20 223 1.17 1.30 0.92 314 0.74

621 622

623



30

Figure Legends 624

625

Figure 1: Diagram illustrating the derivation of the tortuosity factor (τ), lateral path 626

lengthening (λ), and intercellular airspace (IAS) connectivity on a mesophyll-surface-627

area basis (κSA). A simplified cross section through a leaf is shown on the left with 628

epidermal, stomatal, and parenchymal cells (green) and IAS (white). The vapor path 629

length through the IAS, or geodesic distance (Lgeo; pink dashed line) can be 630

decomposed into three components: lateral path length (Llat), epidermal path length 631

(Lepi), and Euclidean path length (LEuc). A disconnected region of IAS and the 632

associated mesophyll surface area is indicated by the solid orange outline. 633

634

Figure 2: Volumetric rendering of leaf segment in the C3 leaf of Greigia sphacelata (left; 635

δ13C = -31.3‰) and the CAM leaf of Aechmea penduliflora (right; δ13C = -15.1‰; δ13C 636

values from Crayn et al., 2015). Grey and white regions from the X-ray microCT image 637

correspond with cell and intercellular airspace (IAS), respectively. White arrows 638

indicated stomatal locations on the abaxial leaf surface. Diffusive path lengths (µm; Lgeo) 639

within the IAS of each leaf are shown for the right half of each leaf. 640

641

Figure 3: Segmented intercellular airspace (IAS; white), vascular and bundle sheath 642

tissue (blue), and mesophyll tissue (green) for the 19 Bromeliaceae species examined. 643

Letters correspond with the species outlined in Table 1. 644

645



31

Figure 4: Leaf anatomical traits values for the 19 Bromeliaceae species studied. For C3 646

(blue; δ13C < -20‰; n = 7) and CAM (grey; δ13C > -20 ‰; n = 12) bromeliads (see Table 647

1 for full species list), mesophyll thickness (Lmes; µm), mesophyll surface area per leaf 648

area (Sm; m2 m-2), average cell diameter (Lcell; µm), mesophyll surface area exposed to 649

the IAS per mesophyll volume (Ames/Vmes; µm2 µm-3), IAS porosity (θIAS; m3 m-3), IAS 650

tortuosity (τleaf; m m-1), lateral path lengthening (λleaf; m m-1), and IAS connectivity on a 651

mesophyll-surface-area basis (κSA; m2 m-2). Asterisks in the upper left corner of plots 652

indicate a significant difference (p < 0.05) between CAM and C3 bromeliads based on a 653

phylogenetic paired t-test. 654

655

Figure 5: Average cross-sectional porosity (θIAS) for the 19 Bromeliaceae species 656

examined in 3D collapsed into a 2D plane. Letters correspond with the species outlined 657

in Table 1. 658

659

Figure 6: Average cross-sectional tortuosity factor (τleaf) for the nineteen Bromeliaceae 660

species examined in 3D collapsed into a 2D plane. Letters correspond with the species 661

outlined in Table 1. 662

663

Figure 7: Average cross-sectional lateral path lengthening (λleaf) for the 19 664

Bromeliaceae species examined in 3D collapsed into a 2D plane. Letters correspond 665

with the species outlined in Table 1. 666

667



32

Figure 8: Average cross-sectional likelihood of IAS disconnection (1 - κSA) for the 668

nineteen Bromeliaceae species examined in 3D collapsed into a 2D plane. Letters 669

correspond with the species outlined in Table 1. 670

671

Figure 9: Relationship between leaf-level porosity (θIAS; m3 m-3) and IAS tortuosity 672

factor (τleaf; m2 m-2), lateral diffusivity factor (λleaf; m m-1), and IAS connectivity on the 673

basis of mesophyll surface area (κSA; m2 m-2) for C3 (blue; δ13C < -20 ‰; n = 7) and 674

CAM (grey; δ13C > -20 ‰; n = 12) bromeliads (see Table 1 for full species list). Non-675

linear regressions of the form y=θIASα

were used to relate θIAS to τleaf (α = -0.18, p < 0.01, 676

R2 = 0.55), λleaf (α = -0.26, p < 0.01, R2 = 0.48), and κSA (α = 0.05, p < 0.01, R2 = 0.19). 677

678

Figure 10: IAS conductance (gIAS; mol m-2 s-1 bar-1) calculated using the standard 679

equation (Eqn. 4; open circles) and the modified equation (Eqn. 6; closed circles) for C3 680

(blue; δ13C < -20‰; n = 7) and CAM (grey; δ13C > -20 ‰; n = 12) bromeliads. Percent 681

differences between the standard and modified equations are shown in parentheses to 682

the right of the points. The approximate range of observed gm values from the literature 683

as given in Flexas et al. (2008) is shown at the top of the figure. The presumed 684

phylogenetic tree based on Givnish et al. (2011) is shown on the far-left side. 685



33

REFERENCES 686

Arakaki M, Christin P-A, Nyffeler R, Lendel A, Eggli U, Ogburn RM, Spriggs E, Moore 687 MJ, Edwards EJ. 2011. Contemporaneous and recent radiations of the world’s major 688 succulent plant lineages. Proceedings of the National Academy of Sciences of the 689 United States of America 108: 8379–8384. 690

Ball BC. 1981. Modelling of soil pores as tubes using gas permeabilities, gas 691 diffusivities and water release. Journal of Soil Science 32: 465–481. 692

Boudreau BP. 1996. The diffusive tortuosity of fine-grained unlithified sediments. 693 Geochimica et Cosmochimica Acta 60: 3139–3142. 694

Carriquí M, Cabrera HM, Conesa M, Coopman RE, Douthe C, Gago J, Gallé A, Galmés 695 J, Ribas-Carbo M, Tomás M, et al. 2015. Diffusional limitations explain the lower 696 photosynthetic capacity of ferns as compared with angiosperms in a common garden 697 study. Plant, Cell and Environment 38: 448–460. 698

Crayn DM, Winter K, Schulte K, Smith JAC. 2015. Photosynthetic pathways in 699 Bromeliaceae: Phylogenetic and ecological significance of CAM and C3 based on 700 carbon isotope ratios for 1893 species. Botanical Journal of the Linnean Society 178: 701 169–221. 702

Doube M, Kłosowski M, Arganda-Carreras I, Cordeliéres F, Dougherty R, Jackson J, 703 Schmid B, Hutchinson J, Shefelbine S. 2010. BoneJ: free and extensible bone image 704 analysis in ImageJ. Bone 47: 1076–1079. 705

Earles JM, Théroux-Rancourt G, Gilbert ME, McElrone AJ, Brodersen C. 2017. Excess 706 diffuse light absorption in upper mesophyll limits CO2 drawdown and depresses 707 photosynthesis. Plant Physiology 174: pp.00223.2017. 708

Evans JR, Kaldenhoff R, Genty B, Terashima I. 2009. Resistances along the CO2 709 diffusion pathway inside leaves. Journal of Experimental Botany 60: 2235–2248. 710

Evans JR, Vogelmann TC. 2006. Photosynthesis within isobilateral Eucalyptus 711 pauciflora leaves. New Phytologist 171: 771–782. 712

Felsenstein J. 1985. Phylogenies and the Comparative Method. The American 713 Naturalist 125: 1–15. 714

Flexas J, Ribas-Carbo M, Diaz-Espejo A, Galmes J, Medrano H. 2008. Mesophyll 715 conductance to CO2 : current knowledge and future prospects. Plant, Cell and 716 Environment 31: 602–621. 717

Franks PJ, Beerling DJ. 2009. Maximum leaf conductance driven by CO2 effects on 718 stomatal size and density over geologic time. Proceedings of the National Academy of 719 Sciences of the United States of America 106: 10343–10347. 720



34

Galmés J, Ochogavía JM, Gago J, Roldán EJ, Cifre J, Conesa MÀ. 2013. Leaf 721 responses to drought stress in Mediterranean accessions of Solanum lycopersicum: 722 Anatomical adaptations in relation to gas exchange parameters. Plant, Cell and 723 Environment 36: 920–935. 724

Givnish TJ, Barfuss MHJ, van Ee B, Riina R, Schulte K, Horres R, Gonsiska PA, Jabaily 725 RS, Crayn DM, Smith JAC, et al. 2011. Phylogeny, adaptive radiation, and historical 726 biogeography in Bromeliaceae: Insights from an eight-locus plastid phylogeny. 727 American Journal of Botany 98: 872–895. 728

Gommes CJ, Bons A-J, Blacher S, Dunsmuir JH, Tsou AH. 2009. practical methods for 729 measuring the tortuosity of porous materials from binary or gray tone tomographic 730 reconstructions. AiChE Journal 55: 2000–2012. 731

Griffiths, Howard; Cousins, Asaph B; Badger, Murray R; von Caemmerer S. 2007. 732 Discrimination in the dark. Resolving the interplay between metabolic and physical 733 constraints to phosphoenolpyruvate carboxylase activity during the crassulacean acid 734 metabolism cycle. Plant physiology 143: 1055–67. 735

Griffiths H, Males J. 2017. Succulent plants. Current Biology 27: R890–R896. 736

Griffiths H, Robe WE, Girnus J, Maxwell K. 2008. Leaf succulence determines the 737 interplay between carboxylase systems and light use during Crassulacean acid 738 metabolism in Kalanchoë species. Journal of Experimental Botany.1851–1861. 739

Heyduk K, Mckain MR, Lalani F, Leebens-mack J. 2016. Molecular Phylogenetics and 740 Evolution Evolution of a CAM anatomy predates the origins of Crassulacean acid 741 metabolism in the Agavoideae (Asparagaceae). Molecular Phylogenetics and Evolution 742 105: 102–113. 743

Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg 744 SP, Webb CO. 2010. Picante: R tools for integrating phylogenies and ecology. 745 Bioinformatics 26: 1463–1464. 746

Lammertsma EI, de Boer HJ, Dekker SC, Dilcher DL, Lotter AF, Wagner-Cremer F. 747 2011. Global CO2 rise leads to reduced maximum stomatal conductance in Florida 748 vegetation. Proceedings of the National Academy of Sciences 108: 4035–4040. 749

Legland D, Arganda-Carreras I, Andrey P. 2016. MorphoLibJ: Integrated library and 750 plugins for mathematical morphology with ImageJ. Bioinformatics 32: 3532–3534. 751

Lehmeier C, Pajor R, Lundgren MR, Mathers A, Sloan J, Bauch M, Mitchell A, Bellasio 752 C, Green A, Bouyer D, et al. 2017. Cell density and airspace patterning in the leaf can 753 be manipulated to increase leaf photosynthetic capacity. The Plant Journal: 981–994. 754

Leuning R. 1983. Transport of gases into leaves. Plant, Cell & Environment 6: 181–194. 755

Ligrone R, Duckett JG, Renzaglia KS. 2012. Major transitions in the evolution of early 756



35

land plants: a bryological perspective. Annals of botany 109: 851–71. 757

Long SP, Farage PK, Bolhar-Nordenkampf HR, Rohrhofer U. 1989. Separating the 758 contribution of the upper and lower mesophyll to photosynthesis in Zea mays L. leaves. 759 Planta 177: 207–216. 760

Males J. 2016. Think tank: water relations of Bromeliaceae in their evolutionary context. 761 Botanical Journal of the Linnean Society 181: 415–440. 762

Males J, Griffiths H (2017) Functional types in the Bromeliaceae: relationships with 763 drought‐ resistance traits and bioclimatic distributions. Functional Ecology 31: 1868–764 1880 765

Maxwell K. 2002. Resistance is useful: Diurnal patterns of photosynthesis in C3 and 766 crassulacean acid metabolism epiphytic bromeliads. Functional Plant Biology 29: 679–767 687. 768

Maxwell K, Von Caemmerer S, Evans JR. 1997. Is a low internal conductance to CO2 769 diffuion a consequence of succulence in plants with crassulacean acid metabolism? 770 Australian Journal of Agricultural Research 24: 777–786. 771

Moldrup P, Olesen T, Komatsu T, Schjonning P, Rolston DE. 2001. Tortuosity, 772 Diffusivity, and Permeability in the Soil Liquid and Gaseous Phases. Soil Science 773 Society of America Journal 65: 613–623. 774

Morison JIL, Gallouët E, Lawson T, Cornic G, Herbin R, Baker NR. 2005. Lateral 775 Diffusion of CO2 in Leaves Is Not Sufficient to Support Photosynthesis. Plant physiology 776 139: 254–266. 777

Morison JIL, Lawson T. 2007. Does lateral gas diffusion in leaves matter? Plant, Cell 778 and Environment 30: 1072–1085. 779

Morison JIL, Lawson T, Cornic G. 2007. Lateral CO2 diffusion inside dicotyledonous 780 leaves can be substantial: quantification in different light intensities. Plant physiology 781 145: 680–690. 782

Nelson EA, Sage RF. 2008. Functional constraints of CAM leaf anatomy: Tight cell 783 packing is associated with increased CAM function across a gradient of CAM 784 expression. Journal of Experimental Botany 59: 1841–1850. 785

Nelson EA, Sage TL, Sage RF. 2005. Functional leaf anatomy of plants with 786 crassulacean acid metabolism. Functional Plant Biology.409–419. 787

Niinemets Ü, Reichstein M (2003) Controls on the emission of plant volatiles through 788 stomata: A sensitivity analysis. Journal of Geophysical Research 108: 4211 789

Nobel PS. 2009. Physicochemical and Environmental Plant Physiology. Oxford, UK: 790 Elsevier. 791



36

Parkhurst DF. 1977. A three-dimensional model for CO2 uptake by continuously 792 distributed mesophyll in leaves. Journal of Theoretical Biology 67: 471–488. 793

Parkhurst DF. 1994. Tansley Review No . 65. Diffusion of CO2 and other gases inside 794 leaves. New Phytologist 126: 449–479. 795

Parkhurst DF, Mott K a. 1990. Intercellular Diffusion Limits to CO2 Uptake in Leaves : 796 Studies in Air and Helox. Plant physiology 94: 1024–1032. 797

Pierce S, Winter K, Griffiths H. 2002. Carbon isotope ratio and the extend of daily CAM 798 use by Bromeliaceae. New Phytologist 156: 75–83. 799

Pieruschka R, Chavarría-Krauser A, Cloos K, Scharr H, Schurr U, Jahnke S. 2008. 800 Photosynthesis can be enhanced by lateral CO2 diffusion inside leaves over distances 801 of several millimeters. New Phytologist 178: 335–347. 802

Pieruschka R, Schurr U, Jahnke S. 2005. Lateral gas diffusion inside leaves. Journal of 803 Experimental Botany 56: 857–864. 804

Pieruschka R, Schurr U, Jensen M, Wolff WF, Jahnke S. 2006. Lateral diffusion of CO2 805 from shaded to illuminated leaf parts affects photosynthesis inside homobaric leaves. 806 New Phytologist 169: 779–788. 807

Revell LJ. 2012. phytools: An R package for phylogenetic comparative biology (and 808 other things). Methods in Ecology and Evolution 3: 217–223. 809

Ripley BS, Abraham T, Klak C, Cramer MD. 2013. How succulent leaves of Aizoaceae 810 avoid mesophyll conductance limitations of photosynthesis and survive drought. Journal 811 of Experimental Botany 64: 5485–5496. 812

Robinson SA, Osmond CB, Giles L. 1993. Interpretations of gradients in d13C value in 813 thick photosynthesis tissues of plants with Crassulacean acid metabolism. Planta 190: 814 271–276. 815

Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu 816 L, Suchard MA, Huelsenbeck JP. 2012. Mrbayes 3.2: Efficient bayesian phylogenetic 817 inference and model choice across a large model space. Systematic Biology 61: 539–818 542. 819

Sáez PL, Bravo LA, Cavieres LA, Vallejos V, Sanhueza C, Font-Carrascosa M, Gil-820 Pelegrín E, Javier Peguero-Pina J, Galmés J. 2017. Photosynthetic limitations in two 821 Antarctic vascular plants: Importance of leaf anatomical traits and Rubisco kinetic 822 parameters. Journal of Experimental Botany 68: 2871–2883. 823

Shen L, Chen Z. 2007. Critical review of the impact of tortuosity on diffusion. Chemical 824 Engineering Science 62: 3748–3755. 825

Sifton HB. 1945. Air-Space Tissue in Plants. Botanical Review 11: 108–143. 826



37

Silvera K, Neubig KM, Whitten WM, Williams NH, Winter K, Cushman JC. 2010. 827 Evolution along the crassulacean acid metabolism continuum. Functional Plant Biology 828 37: 995–1010. 829

Silvera K, Santiago LS, Winter K. 2005. Distribution of crassulacean acid metabolism in 830 orchids of Panama: Evidence of selection for weak and strong modes. Functional Plant 831 Biology 32: 397–407. 832

Slaton MR, Smith WK. 2002. Mesophyll Architecture and Cell Exposure to Intercellular 833 Air Space in Alpine, Desert, and Forest Species. International Journal of Plant Sciences 834 163: 937–948. 835

Syvertsen JP, Lloyd J, McConchie C, Kriedemann PE, Farquhar GD. 1995. On the 836 relationship between leaf anatomy and CO2 diffusion through the mesophyll of 837 hypostomatous leaves. Plant, Cell & Environment 18: 149–157. 838

Théroux-Rancourt G, Earles JM, Gilbert ME, Zwieniecki MA, Boyce CK, McElrone AJ, 839 Brodersen CR. 2017. The bias of a two-dimensional view: comparing two-dimensional 840 and three-dimensional mesophyll surface area estimates using noninvasive imaging. 841 New Phytologist 215: 1609–1622. 842

Thomas GH, Hartmann K, Jetz W, Joy JB, Mimoto A, Mooers AO. 2013. PASTIS: An R 843 package to facilitate phylogenetic assembly with soft taxonomic inferences. Methods in 844 Ecology and Evolution 4: 1011–1017. 845

Tomás M, Flexas J, Copolovici L, Galmés J, Hallik L, Medrano H, Ribas-Carbó M, 846 Tosens T, Vislap V, Niinemets Ü. 2013. Importance of leaf anatomy in determining 847 mesophyll diffusion conductance to CO2 across species: Quantitative limitations and 848 scaling up by models. Journal of Experimental Botany 64: 2269–2281. 849

Tosens T, Nishida K, Gago J, Coopman RE, Cabrera HM, Carriquí M, Laanisto L, 850 Morales L, Nadal M, Rojas R, et al (2016) The photosynthetic capacity in 35 ferns and 851 fern allies: mesophyll CO2 diffusion as a key trait. New Phytologist 209: 1576–1590 852

Veromann-Jürgenson LL, Tosens T, Laanisto L, Niinemets Ü. 2017. Extremely thick cell 853 walls and low mesophyll conductance: Welcome to the world of ancient living! Journal of 854 Experimental Botany 68: 1639–1653. 855

Winter K, Holtum JAM, Smith JAC. 2015. Crassulacean acid metabolism: a continuous 856 or discrete trait? The New phytologist 208: 73–8. 857

Zacharias N a, Nevers DR, Skelton C, Knackstedt K, Stephenson DE, Wheeler DR. 858 2013. Direct Measurements of Effective Ionic Transport in Porous Li-Ion Electrodes. 859 Journal of The Electrochemical Society 160: A306–A311. 860

861



1

Figure 1: Diagram illustrating the derivation of the tortuosity factor (τ), lateral path

lengthening (λ), and intercellular airspace (IAS) connectivity on a mesophyll-surface-

area basis (κSA). A simplified cross section through a leaf is shown on the left with

epidermal, stomatal, and parenchymal cells (green) and IAS (white). The vapor path

length through the IAS, or geodesic distance (Lgeo; pink dashed line) can be

decomposed into three components: lateral path length (Llat), epidermal path length

(Lepi), and Euclidean path length (LEuc). A disconnected region of IAS and the

associated mesophyll surface area is indicated by the solid orange outline.



1

Figure 2: Volumetric rendering of leaf segment in the C3 leaf of Greigia sphacelata (left;

mesophyll thickness = 396 µm; δ13C = -31.3‰) and the CAM leaf of Aechmea

penduliflora (right; mesophyll thickness = 364 µm; δ13C = -15.1‰; δ13C data from Crayn

et al., 2015). Grey and white regions from the X-ray microCT image correspond with cell

and intercellular airspace (IAS), respectively. White arrows indicated stomatal locations

on the abaxial leaf surface. Diffusive path lengths (µm; Lgeo) within the IAS of each leaf

are shown for the right half of each leaf.



1

Figure 3: Segmented intercellular airspace (IAS; white), vascular + bundle sheath

tissue (blue), and mesophyll tissue (green) for the 19 Bromeliaceae species examined.

Letters correspond with the species outlined in Table 1.



1

Figure 4: Leaf anatomical traits values for the 19 Bromeliaceae species studied. For C3

(blue; δ13C < -20‰; n = 7) and CAM (grey; δ13C > -20 ‰; n = 12) bromeliads (see Table

1 for full species list), mesophyll thickness (Lmes; µm), mesophyll surface area per leaf

area (Sm; m2 m-2), average cell diameter (Lcell; µm), mesophyll surface area exposed to

the IAS per mesophyll volume (Ames/Vmes; µm2 µm-3), IAS porosity (θIAS; m3 m-3), IAS

tortuosity (τleaf; m m-1), lateral path lengthening (λleaf; m m-1), and IAS connectivity on a

mesophyll-surface-area basis (κSA; m2 m-2). Asterisks in the upper left corner of plots

indicate a significant difference (p < 0.05) between CAM and C3 bromeliads based on a

phylogenetic paired t-test.



1

Figure 5: Average cross-sectional porosity (θIAS) for the 19 Bromeliaceae species

examined in 3D collapsed into a 2D plane. Letters correspond with the species outlined

in Table 1.



1

Figure 6: Average cross-sectional tortuosity factor (τleaf) for the 19 Bromeliaceae

species examined in 3D collapsed into a 2D plane. Letters correspond with the species

outlined in Table 1.



1

Figure 7: Average cross-sectional lateral path lengthening (λleaf) for the 19

Bromeliaceae species examined in 3D collapsed into a 2D plane. Letters correspond

with the species outlined in Table 1.



1

Figure 8: Average cross-sectional likelihood of IAS disconnection (1 - κSA) for the 19

Bromeliaceae species examined in 3D collapsed into a 2D plane. Letters correspond

with the species outlined in Table 1.



1

Figure 9: Relationship between leaf-level porosity (θIAS; m3 m-3) and IAS tortuosity

factor (τleaf; m2 m-2), lateral diffusivity factor (λleaf; m m-1), and IAS connectivity on the

basis of mesophyll surface area (κSA; m2 m-2) for C3 (blue; δ13C < -20 ‰; n = 7) and

CAM (grey; δ13C > -20 ‰; n = 12) bromeliads (see Table 1 for full species list). Non-

linear regressions of the form y=θIASα

were used to relate θIAS to τleaf (α = -0.18, p < 0.01,

R2 = 0.55), λleaf (α = -0.26, p < 0.01, R2 = 0.48), and κSA (α = 0.05, p < 0.01, R2 = 0.19).



1

Figure 10: IAS conductance (gIAS; mol m-2 s-1 bar-1) calculated using the standard

equation (Eqn. 4; open circles) and the modified equation (Eqn. 6; closed circles) for C3

(blue; δ13C < -20‰; n = 7) and CAM (grey; δ13C > -20 ‰; n = 12) bromeliads. Percent

differences between the standard and modified equations are shown in parentheses to

the right of the points. The approximate range of observed gm values from the literature

as given in Flexas et al. (2008) is shown at the top of the figure. The presumed

phylogenetic tree based on Givnish et al. (2011) is shown on the far-left side.



Parsed CitationsArakaki M, Christin P-A, Nyffeler R, Lendel A, Eggli U, Ogburn RM, Spriggs E, Moore MJ, Edwards EJ. 2011. Contemporaneous andrecent radiations of the world's major succulent plant lineages. Proceedings of the National Academy of Sciences of the United Statesof America 108: 8379–8384.

Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Ball BC. 1981. Modelling of soil pores as tubes using gas permeabilities, gas diffusivities and water release. Journal of Soil Science 32:465–481.


Boudreau BP. 1996. The diffusive tortuosity of fine-grained unlithified sediments. Geochimica et Cosmochimica Acta 60: 3139–3142.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Carriquí M, Cabrera HM, Conesa M, Coopman RE, Douthe C, Gago J, Gallé A, Galmés J, Ribas-Carbo M, Tomás M, et al. 2015.Diffusional limitations explain the lower photosynthetic capacity of ferns as compared with angiosperms in a common garden study.Plant, Cell and Environment 38: 448–460.


Crayn DM, Winter K, Schulte K, Smith JAC. 2015. Photosynthetic pathways in Bromeliaceae: Phylogenetic and ecological significanceof CAM and C3 based on carbon isotope ratios for 1893 species. Botanical Journal of the Linnean Society 178: 169–221.


Doube M, Kłosowski M, Arganda-Carreras I, Cordeliéres F, Dougherty R, Jackson J, Schmid B, Hutchinson J, Shefelbine S. 2010.BoneJ: free and extensible bone image analysis in ImageJ. Bone 47: 1076–1079.


Earles JM, Théroux-Rancourt G, Gilbert ME, McElrone AJ, Brodersen C. 2017. Excess diffuse light absorption in upper mesophylllimits CO2 drawdown and depresses photosynthesis. Plant Physiology 174: pp.00223.2017.


Evans JR, Kaldenhoff R, Genty B, Terashima I. 2009. Resistances along the CO2 diffusion pathway inside leaves. Journal ofExperimental Botany 60: 2235–2248.


Evans JR, Vogelmann TC. 2006. Photosynthesis within isobilateral Eucalyptus pauciflora leaves. New Phytologist 171: 771–782.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Felsenstein J. 1985. Phylogenies and the Comparative Method. The American Naturalist 125: 1–15.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Flexas J, Ribas-Carbo M, Diaz-Espejo A, Galmes J, Medrano H. 2008. Mesophyll conductance to CO2 : current knowledge and futureprospects. Plant, Cell and Environment 31: 602–621.


Franks PJ, Beerling DJ. 2009. Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time.Proceedings of the National Academy of Sciences of the United States of America 106: 10343–10347.


Galmés J, Ochogavía JM, Gago J, Roldán EJ, Cifre J, Conesa MÀ. 2013. Leaf responses to drought stress in Mediterranean accessionsof Solanum lycopersicum: Anatomical adaptations in relation to gas exchange parameters. Plant, Cell and Environment 36: 920–935.


Givnish TJ, Barfuss MHJ, van Ee B, Riina R, Schulte K, Horres R, Gonsiska PA, Jabaily RS, Crayn DM, Smith JAC, et al. 2011.Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: Insights from an eight-locus plastid phylogeny. AmericanJournal of Botany 98: 872–895.


Gommes CJ, Bons A-J, Blacher S, Dunsmuir JH, Tsou AH. 2009. practical methods for measuring the tortuosity of porous materialsfrom binary or gray tone tomographic reconstructions. AiChE Journal 55: 2000–2012. www.plantphysiol.orgon May 7, 2020 - Published by Downloaded from

Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Arakaki M%2C Christin P%2DA%2C Nyffeler R%2C Lendel A%2C Eggli U%2C Ogburn RM%2C Spriggs E%2C Moore MJ%2C Edwards EJ%2E 2011%2E Contemporaneous and recent radiations of the world%27s major succulent plant lineages%2E Proceedings of the National Academy of Sciences of the United States of America 108%3A 8379%26%23x2013%3B8384%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Arakaki&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Contemporaneous and recent radiations of the world's major succulent plant lineages&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Contemporaneous and recent radiations of the world's major succulent plant lineages&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Arakaki&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ball BC%2E 1981%2E Modelling of soil pores as tubes using gas permeabilities%2C gas diffusivities and water release%2E Journal of Soil Science 32%3A 465%26%23x2013%3B481%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ball&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Modelling of soil pores as tubes using gas permeabilities, gas diffusivities and water release&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Modelling of soil pores as tubes using gas permeabilities, gas diffusivities and water release&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ball&as_ylo=1981&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Boudreau BP%2E 1996%2E The diffusive tortuosity of fine%2Dgrained unlithified sediments%2E Geochimica et Cosmochimica Acta 60%3A 3139%26%23x2013%3B3142%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Boudreau&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The diffusive tortuosity of fine-grained unlithified sediments&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The diffusive tortuosity of fine-grained unlithified sediments&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Boudreau&as_ylo=1996&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Carriqu� M%2C Cabrera HM%2C Conesa M%2C Coopman RE%2C Douthe C%2C Gago J%2C Gall� A%2C Galm�s J%2C Ribas%2DCarbo M%2C Tom�s M%2C et al%2E 2015%2E Diffusional limitations explain the lower photosynthetic capacity of ferns as compared with angiosperms in a common garden study%2E Plant%2C Cell and Environment 38%3A 448%26%23x2013%3B460%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Carriquí&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Diffusional limitations explain the lower photosynthetic capacity of ferns as compared with angiosperms in a common garden study&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Diffusional limitations explain the lower photosynthetic capacity of ferns as compared with angiosperms in a common garden study&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Carriquí&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Crayn DM%2C Winter K%2C Schulte K%2C Smith JAC%2E 2015%2E Photosynthetic pathways in Bromeliaceae%3A Phylogenetic and ecological significance of CAM and C3 based on carbon isotope ratios for 1893 species%2E Botanical Journal of the Linnean Society 178%3A 169%26%23x2013%3B221%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Crayn&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Photosynthetic pathways in Bromeliaceae: Phylogenetic and ecological significance of CAM and C3 based on carbon isotope ratios for 1893 species&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Photosynthetic pathways in Bromeliaceae: Phylogenetic and ecological significance of CAM and C3 based on carbon isotope ratios for 1893 species&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Crayn&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Doube M%2C K�?osowski M%2C Arganda%2DCarreras I%2C Cordeliéres F%2C Dougherty R%2C Jackson J%2C Schmid B%2C Hutchinson J%2C Shefelbine S%2E 2010%2E BoneJ%3A free and extensible bone image analysis in ImageJ%2E Bone 47%3A 1076%26%23x2013%3B1079%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Doube&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=BoneJ: free and extensible bone image analysis in ImageJ&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=BoneJ: free and extensible bone image analysis in ImageJ&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Doube&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Earles JM%2C Th�roux%2DRancourt G%2C Gilbert ME%2C McElrone AJ%2C Brodersen C%2E 2017%2E Excess diffuse light absorption in upper mesophyll limits CO2 drawdown and depresses photosynthesis%2E Plant Physiology 174%3A pp%2E00223%2E2017%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Earles&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Excess diffuse light absorption in upper mesophyll limits CO2 drawdown and depresses photosynthesis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Excess diffuse light absorption in upper mesophyll limits CO2 drawdown and depresses photosynthesis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Earles&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Evans JR%2C Kaldenhoff R%2C Genty B%2C Terashima I%2E 2009%2E Resistances along the CO2 diffusion pathway inside leaves%2E Journal of Experimental Botany 60%3A 2235%26%23x2013%3B2248%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Evans&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Resistances along the CO2 diffusion pathway inside leaves&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Resistances along the CO2 diffusion pathway inside leaves&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Evans&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Evans JR%2C Vogelmann TC%2E 2006%2E Photosynthesis within isobilateral Eucalyptus pauciflora leaves%2E New Phytologist 171%3A 771%26%23x2013%3B782%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Evans&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Photosynthesis within isobilateral Eucalyptus pauciflora leaves&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Photosynthesis within isobilateral Eucalyptus pauciflora leaves&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Evans&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Felsenstein J%2E 1985%2E Phylogenies and the Comparative Method%2E The American Naturalist 125%3A 1%26%23x2013%3B15%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Felsenstein&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Phylogenies and the Comparative Method&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Phylogenies and the Comparative Method&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Felsenstein&as_ylo=1985&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Flexas J%2C Ribas%2DCarbo M%2C Diaz%2DEspejo A%2C Galmes J%2C Medrano H%2E 2008%2E Mesophyll conductance to CO2�?�%3A current knowledge and future prospects%2E Plant%2C Cell and Environment 31%3A 602%26%23x2013%3B621%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Flexas&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Mesophyll conductance to CO2â�?¯: current knowledge and future prospects&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Mesophyll conductance to CO2â�?¯: current knowledge and future prospects&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Flexas&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Franks PJ%2C Beerling DJ%2E 2009%2E Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time%2E Proceedings of the National Academy of Sciences of the United States of America 106%3A 10343%26%23x2013%3B10347%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Franks&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Franks&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Galm�s J%2C Ochogav�a JM%2C Gago J%2C Rold�n EJ%2C Cifre J%2C Conesa M�%2E 2013%2E Leaf responses to drought stress in Mediterranean accessions of Solanum lycopersicum%3A Anatomical adaptations in relation to gas exchange parameters%2E Plant%2C Cell and Environment 36%3A 920%26%23x2013%3B935%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Galmés&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Leaf responses to drought stress in Mediterranean accessions of Solanum lycopersicum: Anatomical adaptations in relation to gas exchange parameters&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Leaf responses to drought stress in Mediterranean accessions of Solanum lycopersicum: Anatomical adaptations in relation to gas exchange parameters&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Galmés&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Givnish TJ%2C Barfuss MHJ%2C van Ee B%2C Riina R%2C Schulte K%2C Horres R%2C Gonsiska PA%2C Jabaily RS%2C Crayn DM%2C Smith JAC%2C et al%2E 2011%2E Phylogeny%2C adaptive radiation%2C and historical biogeography in Bromeliaceae%3A Insights from an eight%2Dlocus plastid phylogeny%2E American Journal of Botany 98%3A 872%26%23x2013%3B895%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Givnish&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: Insights from an eight-locus plastid phylogeny&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: Insights from an eight-locus plastid phylogeny&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Givnish&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1



Griffiths, Howard; Cousins, Asaph B; Badger, Murray R; von Caemmerer S. 2007. Discrimination in the dark. Resolving the interplaybetween metabolic and physical constraints to phosphoenolpyruvate carboxylase activity during the crassulacean acid metabolismcycle. Plant physiology 143: 1055–67.


Griffiths H, Males J. 2017. Succulent plants. Current Biology 27: R890–R896.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Griffiths H, Robe WE, Girnus J, Maxwell K. 2008. Leaf succulence determines the interplay between carboxylase systems and light useduring Crassulacean acid metabolism in Kalanchoë species. Journal of Experimental Botany.1851–1861.


Heyduk K, Mckain MR, Lalani F, Leebens-mack J. 2016. Molecular Phylogenetics and Evolution Evolution of a CAM anatomy predatesthe origins of Crassulacean acid metabolism in the Agavoideae (Asparagaceae). Molecular Phylogenetics and Evolution 105: 102–113.


Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO. 2010. Picante: R tools for integratingphylogenies and ecology. Bioinformatics 26: 1463–1464.


Lammertsma EI, de Boer HJ, Dekker SC, Dilcher DL, Lotter AF, Wagner-Cremer F. 2011. Global CO2 rise leads to reduced maximumstomatal conductance in Florida vegetation. Proceedings of the National Academy of Sciences 108: 4035–4040.


Legland D, Arganda-Carreras I, Andrey P. 2016. MorphoLibJ: Integrated library and plugins for mathematical morphology with ImageJ.Bioinformatics 32: 3532–3534.


Lehmeier C, Pajor R, Lundgren MR, Mathers A, Sloan J, Bauch M, Mitchell A, Bellasio C, Green A, Bouyer D, et al. 2017. Cell densityand airspace patterning in the leaf can be manipulated to increase leaf photosynthetic capacity. The Plant Journal: 981–994.


Leuning R. 1983. Transport of gases into leaves. Plant, Cell & Environment 6: 181–194.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Ligrone R, Duckett JG, Renzaglia KS. 2012. Major transitions in the evolution of early land plants: a bryological perspective. Annals ofbotany 109: 851–71.


Long SP, Farage PK, Bolhar-Nordenkampf HR, Rohrhofer U. 1989. Separating the contribution of the upper and lower mesophyll tophotosynthesis in Zea mays L. leaves. Planta 177: 207–216.


Males J. 2016. Think tank: water relations of Bromeliaceae in their evolutionary context. Botanical Journal of the Linnean Society 181:415–440.


Males J, Griffiths H (2017) Functional types in the Bromeliaceae: relationships with drought‐resistance traits and bioclimaticdistributions. Functional Ecology 31: 1868–1880


Maxwell K. 2002. Resistance is useful: Diurnal patterns of photosynthesis in C3 and crassulacean acid metabolism epiphyticbromeliads. Functional Plant Biology 29: 679–687.


Maxwell K, Von Caemmerer S, Evans JR. 1997. Is a low internal conductance to CO2 diffuion a consequence of succulence in plantswith crassulacean acid metabolism? Australian Journal of Agricultural Research 24: 777–786.

Pubmed: Author and Title www.plantphysiol.orgon May 7, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Gommes CJ%2C Bons A%2DJ%2C Blacher S%2C Dunsmuir JH%2C Tsou AH%2E 2009%2E practical methods for measuring the tortuosity of porous materials from binary or gray tone tomographic reconstructions%2E AiChE Journal 55%3A 2000%26%23x2013%3B2012%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Gommes&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=practical methods for measuring the tortuosity of porous materials from binary or gray tone tomographic reconstructions&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=practical methods for measuring the tortuosity of porous materials from binary or gray tone tomographic reconstructions&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Gommes&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Griffiths%2C Howard%3B Cousins%2C Asaph B%3B Badger%2C Murray R%3B von Caemmerer S%2E 2007%2E Discrimination in the dark%2E Resolving the interplay between metabolic and physical constraints to phosphoenolpyruvate carboxylase activity during the crassulacean acid metabolism cycle%2E Plant physiology 143%3A 1055%26%23x2013%3B67%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Griffiths,&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Discrimination in the dark&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Discrimination in the dark&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Griffiths,&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Griffiths H%2C Males J%2E 2017%2E Succulent plants%2E Current Biology 27%3A R890%26%23x2013%3BR896%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Griffiths&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Succulent plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Succulent plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Griffiths&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Griffiths H%2C Robe WE%2C Girnus J%2C Maxwell K%2E 2008%2E Leaf succulence determines the interplay between carboxylase systems and light use during Crassulacean acid metabolism in Kalancho� species%2E Journal of Experimental Botany%2E1851%26%23x2013%3B1861%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Griffiths&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Leaf succulence determines the interplay between carboxylase systems and light use during Crassulacean acid metabolism in Kalanchoë species.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Leaf succulence determines the interplay between carboxylase systems and light use during Crassulacean acid metabolism in Kalanchoë species.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Griffiths&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Heyduk K%2C Mckain MR%2C Lalani F%2C Leebens%2Dmack J%2E 2016%2E Molecular Phylogenetics and Evolution Evolution of a CAM anatomy predates the origins of Crassulacean acid metabolism in the Agavoideae %28Asparagaceae%29%2E Molecular Phylogenetics and Evolution 105%3A 102%26%23x2013%3B113%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Heyduk&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Molecular Phylogenetics and Evolution Evolution of a CAM anatomy predates the origins of Crassulacean acid metabolism in the Agavoideae (Asparagaceae)&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Molecular Phylogenetics and Evolution Evolution of a CAM anatomy predates the origins of Crassulacean acid metabolism in the Agavoideae (Asparagaceae)&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Heyduk&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Kembel SW%2C Cowan PD%2C Helmus MR%2C Cornwell WK%2C Morlon H%2C Ackerly DD%2C Blomberg SP%2C Webb CO%2E 2010%2E Picante%3A R tools for integrating phylogenies and ecology%2E Bioinformatics 26%3A 1463%26%23x2013%3B1464%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Kembel&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Picante: R tools for integrating phylogenies and ecology&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Picante: R tools for integrating phylogenies and ecology&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Kembel&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lammertsma EI%2C de Boer HJ%2C Dekker SC%2C Dilcher DL%2C Lotter AF%2C Wagner%2DCremer F%2E 2011%2E Global CO2 rise leads to reduced maximum stomatal conductance in Florida vegetation%2E Proceedings of the National Academy of Sciences 108%3A 4035%26%23x2013%3B4040%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lammertsma&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Global CO2 rise leads to reduced maximum stomatal conductance in Florida vegetation&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Global CO2 rise leads to reduced maximum stomatal conductance in Florida vegetation&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lammertsma&as_ylo=2011&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Legland D%2C Arganda%2DCarreras I%2C Andrey P%2E 2016%2E MorphoLibJ%3A Integrated library and plugins for mathematical morphology with ImageJ%2E Bioinformatics 32%3A 3532%26%23x2013%3B3534%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Legland&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=MorphoLibJ: Integrated library and plugins for mathematical morphology with ImageJ&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=MorphoLibJ: Integrated library and plugins for mathematical morphology with ImageJ&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Legland&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Lehmeier C%2C Pajor R%2C Lundgren MR%2C Mathers A%2C Sloan J%2C Bauch M%2C Mitchell A%2C Bellasio C%2C Green A%2C Bouyer D%2C et al%2E 2017%2E Cell density and airspace patterning in the leaf can be manipulated to increase leaf photosynthetic capacity%2E The Plant Journal%3A 981%26%23x2013%3B994%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Lehmeier&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Cell density and airspace patterning in the leaf can be manipulated to increase leaf photosynthetic capacity.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Cell density and airspace patterning in the leaf can be manipulated to increase leaf photosynthetic capacity.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Lehmeier&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Leuning R%2E 1983%2E Transport of gases into leaves%2E Plant%2C Cell %26 Environment 6%3A 181%26%23x2013%3B194%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Leuning&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Transport of gases into leaves&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Transport of gases into leaves&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Leuning&as_ylo=1983&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ligrone R%2C Duckett JG%2C Renzaglia KS%2E 2012%2E Major transitions in the evolution of early land plants%3A a bryological perspective%2E Annals of botany 109%3A 851%26%23x2013%3B71%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ligrone&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Major transitions in the evolution of early land plants: a bryological perspective&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Major transitions in the evolution of early land plants: a bryological perspective&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ligrone&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Long SP%2C Farage PK%2C Bolhar%2DNordenkampf HR%2C Rohrhofer U%2E 1989%2E Separating the contribution of the upper and lower mesophyll to photosynthesis in Zea mays L%2E leaves%2E Planta 177%3A 207%26%23x2013%3B216%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Long&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Separating the contribution of the upper and lower mesophyll to photosynthesis in Zea mays L&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Separating the contribution of the upper and lower mesophyll to photosynthesis in Zea mays L&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Long&as_ylo=1989&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Males J%2E 2016%2E Think tank%3A water relations of Bromeliaceae in their evolutionary context%2E Botanical Journal of the Linnean Society 181%3A 415%26%23x2013%3B440%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Males&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Think tank: water relations of Bromeliaceae in their evolutionary context&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Think tank: water relations of Bromeliaceae in their evolutionary context&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Males&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Males J%2C Griffiths H %282017%29 Functional types in the Bromeliaceae%3A relationships with drought�?�resistance traits and bioclimatic distributions%2E Functional Ecology 31%3A 1868%26%23x2013%3B1880&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Males&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Functional types in the Bromeliaceae: relationships with droughtâ�?�resistance traits and bioclimatic distributions.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Functional types in the Bromeliaceae: relationships with droughtâ�?�resistance traits and bioclimatic distributions.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Males&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Maxwell K%2E 2002%2E Resistance is useful%3A Diurnal patterns of photosynthesis in C3 and crassulacean acid metabolism epiphytic bromeliads%2E Functional Plant Biology 29%3A 679%26%23x2013%3B687%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Maxwell&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Resistance is useful: Diurnal patterns of photosynthesis in C3 and crassulacean acid metabolism epiphytic bromeliads&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Resistance is useful: Diurnal patterns of photosynthesis in C3 and crassulacean acid metabolism epiphytic bromeliads&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Maxwell&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Maxwell K%2C Von Caemmerer S%2C Evans JR%2E 1997%2E Is a low internal conductance to CO2 diffuion a consequence of succulence in plants with crassulacean acid metabolism%3F Australian Journal of Agricultural Research 24%3A 777%26%23x2013%3B786%2E&dopt=abstract


Google Scholar: Author Only Title Only Author and Title

Moldrup P, Olesen T, Komatsu T, Schjonning P, Rolston DE. 2001. Tortuosity, Diffusivity, and Permeability in the Soil Liquid andGaseous Phases. Soil Science Society of America Journal 65: 613–623.


Morison JIL, Gallouët E, Lawson T, Cornic G, Herbin R, Baker NR. 2005. Lateral Diffusion of CO2 in Leaves Is Not Sufficient to SupportPhotosynthesis. Plant physiology 139: 254–266.


Morison JIL, Lawson T. 2007. Does lateral gas diffusion in leaves matter? Plant, Cell and Environment 30: 1072–1085.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Morison JIL, Lawson T, Cornic G. 2007. Lateral CO2 diffusion inside dicotyledonous leaves can be substantial: quantification indifferent light intensities. Plant physiology 145: 680–690.


Nelson EA, Sage RF. 2008. Functional constraints of CAM leaf anatomy: Tight cell packing is associated with increased CAM functionacross a gradient of CAM expression. Journal of Experimental Botany 59: 1841–1850.


Nelson EA, Sage TL, Sage RF. 2005. Functional leaf anatomy of plants with crassulacean acid metabolism. Functional PlantBiology.409–419.


Niinemets Ü, Reichstein M (2003) Controls on the emission of plant volatiles through stomata: A sensitivity analysis. Journal ofGeophysical Research 108: 4211


Nobel PS. 2009. Physicochemical and Environmental Plant Physiology. Oxford, UK: Elsevier.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Parkhurst DF. 1977. A three-dimensional model for CO2 uptake by continuously distributed mesophyll in leaves. Journal of TheoreticalBiology 67: 471–488.


Parkhurst DF. 1994. Tansley Review No . 65. Diffusion of CO2 and other gases inside leaves. New Phytologist 126: 449–479.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Parkhurst DF, Mott K a. 1990. Intercellular Diffusion Limits to CO2 Uptake in Leaves : Studies in Air and Helox. Plant physiology 94:1024–1032.


Pierce S, Winter K, Griffiths H. 2002. Carbon isotope ratio and the extend of daily CAM use by Bromeliaceae. New Phytologist 156: 75–83.


Pieruschka R, Chavarría-Krauser A, Cloos K, Scharr H, Schurr U, Jahnke S. 2008. Photosynthesis can be enhanced by lateral CO2diffusion inside leaves over distances of several millimeters. New Phytologist 178: 335–347.


Pieruschka R, Schurr U, Jahnke S. 2005. Lateral gas diffusion inside leaves. Journal of Experimental Botany 56: 857–864.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Pieruschka R, Schurr U, Jensen M, Wolff WF, Jahnke S. 2006. Lateral diffusion of CO2 from shaded to illuminated leaf parts affectsphotosynthesis inside homobaric leaves. New Phytologist 169: 779–788.


Revell LJ. 2012. phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 3:217–223. www.plantphysiol.orgon May 7, 2020 - Published by Downloaded from

Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Maxwell&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Is a low internal conductance to CO2 diffuion a consequence of succulence in plants with crassulacean acid metabolism&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Is a low internal conductance to CO2 diffuion a consequence of succulence in plants with crassulacean acid metabolism&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Maxwell&as_ylo=1997&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Moldrup P%2C Olesen T%2C Komatsu T%2C Schjonning P%2C Rolston DE%2E 2001%2E Tortuosity%2C Diffusivity%2C and Permeability in the Soil Liquid and Gaseous Phases%2E Soil Science Society of America Journal 65%3A 613%26%23x2013%3B623%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Moldrup&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Tortuosity, Diffusivity, and Permeability in the Soil Liquid and Gaseous Phases&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Tortuosity, Diffusivity, and Permeability in the Soil Liquid and Gaseous Phases&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Moldrup&as_ylo=2001&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Morison JIL%2C Gallou�t E%2C Lawson T%2C Cornic G%2C Herbin R%2C Baker NR%2E 2005%2E Lateral Diffusion of CO2 in Leaves Is Not Sufficient to Support Photosynthesis%2E Plant physiology 139%3A 254%26%23x2013%3B266%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Morison&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Lateral Diffusion of CO2 in Leaves Is Not Sufficient to Support Photosynthesis&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Lateral Diffusion of CO2 in Leaves Is Not Sufficient to Support Photosynthesis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Morison&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Morison JIL%2C Lawson T%2E 2007%2E Does lateral gas diffusion in leaves matter%3F Plant%2C Cell and Environment 30%3A 1072%26%23x2013%3B1085%2E&dopt=abstract


http://scholar.google.com/scholar?as_q=Does lateral gas diffusion in leaves matter&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Does lateral gas diffusion in leaves matter&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Morison&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Morison JIL%2C Lawson T%2C Cornic G%2E 2007%2E Lateral CO2 diffusion inside dicotyledonous leaves can be substantial%3A quantification in different light intensities%2E Plant physiology 145%3A 680%26%23x2013%3B690%2E&dopt=abstract


http://scholar.google.com/scholar?as_q=Lateral CO2 diffusion inside dicotyledonous leaves can be substantial: quantification in different light intensities&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Lateral CO2 diffusion inside dicotyledonous leaves can be substantial: quantification in different light intensities&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Morison&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Nelson EA%2C Sage RF%2E 2008%2E Functional constraints of CAM leaf anatomy%3A Tight cell packing is associated with increased CAM function across a gradient of CAM expression%2E Journal of Experimental Botany 59%3A 1841%26%23x2013%3B1850%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Nelson&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Functional constraints of CAM leaf anatomy: Tight cell packing is associated with increased CAM function across a gradient of CAM expression&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Functional constraints of CAM leaf anatomy: Tight cell packing is associated with increased CAM function across a gradient of CAM expression&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nelson&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Nelson EA%2C Sage TL%2C Sage RF%2E 2005%2E Functional leaf anatomy of plants with crassulacean acid metabolism%2E Functional Plant Biology%2E409%26%23x2013%3B419%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Nelson&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Functional leaf anatomy of plants with crassulacean acid metabolism.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Functional leaf anatomy of plants with crassulacean acid metabolism.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nelson&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Niinemets �%2C Reichstein M %282003%29 Controls on the emission of plant volatiles through stomata%3A A sensitivity analysis%2E Journal of Geophysical Research 108%3A 4211&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Niinemets&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Controls on the emission of plant volatiles through stomata: A sensitivity analysis.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Controls on the emission of plant volatiles through stomata: A sensitivity analysis.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Niinemets&as_ylo=2003&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Nobel PS%2E 2009%2E Physicochemical and Environmental Plant Physiology%2E Oxford%2C UK%3A Elsevier%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Nobel&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Physicochemical and Environmental Plant Physiology.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Physicochemical and Environmental Plant Physiology.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Nobel&as_ylo=2009&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Parkhurst DF%2E 1977%2E A three%2Ddimensional model for CO2 uptake by continuously distributed mesophyll in leaves%2E Journal of Theoretical Biology 67%3A 471%26%23x2013%3B488%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Parkhurst&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=A three-dimensional model for CO2 uptake by continuously distributed mesophyll in leaves&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=A three-dimensional model for CO2 uptake by continuously distributed mesophyll in leaves&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Parkhurst&as_ylo=1977&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Parkhurst DF%2E 1994%2E Tansley Review No %2E 65%2E Diffusion of CO2 and other gases inside leaves%2E New Phytologist 126%3A 449%26%23x2013%3B479%2E&dopt=abstract


http://scholar.google.com/scholar?as_q=Tansley Review No&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Tansley Review No&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Parkhurst&as_ylo=1994&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Parkhurst DF%2C Mott K a%2E 1990%2E Intercellular Diffusion Limits to CO2 Uptake in Leaves�?�%3A Studies in Air and Helox%2E Plant physiology 94%3A 1024%26%23x2013%3B1032%2E&dopt=abstract


http://scholar.google.com/scholar?as_q=Intercellular Diffusion Limits to CO2 Uptake in Leavesâ�?¯: Studies in Air and Helox&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Intercellular Diffusion Limits to CO2 Uptake in Leavesâ�?¯: Studies in Air and Helox&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Parkhurst&as_ylo=1990&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Pierce S%2C Winter K%2C Griffiths H%2E 2002%2E Carbon isotope ratio and the extend of daily CAM use by Bromeliaceae%2E New Phytologist 156%3A 75%26%23x2013%3B83%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Pierce&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Carbon isotope ratio and the extend of daily CAM use by Bromeliaceae&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Carbon isotope ratio and the extend of daily CAM use by Bromeliaceae&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pierce&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Pieruschka R%2C Chavarr�a%2DKrauser A%2C Cloos K%2C Scharr H%2C Schurr U%2C Jahnke S%2E 2008%2E Photosynthesis can be enhanced by lateral CO2 diffusion inside leaves over distances of several millimeters%2E New Phytologist 178%3A 335%26%23x2013%3B347%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Pieruschka&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Photosynthesis can be enhanced by lateral CO2 diffusion inside leaves over distances of several millimeters&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Photosynthesis can be enhanced by lateral CO2 diffusion inside leaves over distances of several millimeters&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pieruschka&as_ylo=2008&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Pieruschka R%2C Schurr U%2C Jahnke S%2E 2005%2E Lateral gas diffusion inside leaves%2E Journal of Experimental Botany 56%3A 857%26%23x2013%3B864%2E&dopt=abstract


http://scholar.google.com/scholar?as_q=Lateral gas diffusion inside leaves&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Lateral gas diffusion inside leaves&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pieruschka&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Pieruschka R%2C Schurr U%2C Jensen M%2C Wolff WF%2C Jahnke S%2E 2006%2E Lateral diffusion of CO2 from shaded to illuminated leaf parts affects photosynthesis inside homobaric leaves%2E New Phytologist 169%3A 779%26%23x2013%3B788%2E&dopt=abstract


http://scholar.google.com/scholar?as_q=Lateral diffusion of CO2 from shaded to illuminated leaf parts affects photosynthesis inside homobaric leaves&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Lateral diffusion of CO2 from shaded to illuminated leaf parts affects photosynthesis inside homobaric leaves&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Pieruschka&as_ylo=2006&as_allsubj=all&hl=en&c2coff=1



Ripley BS, Abraham T, Klak C, Cramer MD. 2013. How succulent leaves of Aizoaceae avoid mesophyll conductance limitations ofphotosynthesis and survive drought. Journal of Experimental Botany 64: 5485–5496.


Robinson SA, Osmond CB, Giles L. 1993. Interpretations of gradients in d13C value in thick photosynthesis tissues of plants withCrassulacean acid metabolism. Planta 190: 271–276.


Ronquist F, Teslenko M, Van Der Mark P, Ayres DL, Darling A, Höhna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP. 2012. Mrbayes3.2: Efficient bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61: 539–542.


Sáez PL, Bravo LA, Cavieres LA, Vallejos V, Sanhueza C, Font-Carrascosa M, Gil-Pelegrín E, Javier Peguero-Pina J, Galmés J. 2017.Photosynthetic limitations in two Antarctic vascular plants: Importance of leaf anatomical traits and Rubisco kinetic parameters. Journalof Experimental Botany 68: 2871–2883.


Shen L, Chen Z. 2007. Critical review of the impact of tortuosity on diffusion. Chemical Engineering Science 62: 3748–3755.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Sifton HB. 1945. Air-Space Tissue in Plants. Botanical Review 11: 108–143.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Silvera K, Neubig KM, Whitten WM, Williams NH, Winter K, Cushman JC. 2010. Evolution along the crassulacean acid metabolismcontinuum. Functional Plant Biology 37: 995–1010.


Silvera K, Santiago LS, Winter K. 2005. Distribution of crassulacean acid metabolism in orchids of Panama: Evidence of selection forweak and strong modes. Functional Plant Biology 32: 397–407.


Slaton MR, Smith WK. 2002. Mesophyll Architecture and Cell Exposure to Intercellular Air Space in Alpine, Desert, and Forest Species.International Journal of Plant Sciences 163: 937–948.


Syvertsen JP, Lloyd J, McConchie C, Kriedemann PE, Farquhar GD. 1995. On the relationship between leaf anatomy and CO2 diffusionthrough the mesophyll of hypostomatous leaves. Plant, Cell & Environment 18: 149–157.


Théroux-Rancourt G, Earles JM, Gilbert ME, Zwieniecki MA, Boyce CK, McElrone AJ, Brodersen CR. 2017. The bias of a two-dimensional view: comparing two-dimensional and three-dimensional mesophyll surface area estimates using noninvasive imaging.New Phytologist 215: 1609–1622.


Thomas GH, Hartmann K, Jetz W, Joy JB, Mimoto A, Mooers AO. 2013. PASTIS: An R package to facilitate phylogenetic assembly withsoft taxonomic inferences. Methods in Ecology and Evolution 4: 1011–1017.


Tomás M, Flexas J, Copolovici L, Galmés J, Hallik L, Medrano H, Ribas-Carbó M, Tosens T, Vislap V, Niinemets Ü. 2013. Importance ofleaf anatomy in determining mesophyll diffusion conductance to CO2 across species: Quantitative limitations and scaling up bymodels. Journal of Experimental Botany 64: 2269–2281.


Tosens T, Nishida K, Gago J, Coopman RE, Cabrera HM, Carriquí M, Laanisto L, Morales L, Nadal M, Rojas R, et al (2016) Thephotosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait. New Phytologist 209: 1576–1590


Veromann-Jürgenson LL, Tosens T, Laanisto L, Niinemets Ü. 2017. Extremely thick cell walls and low mesophyll conductance: Welcome www.plantphysiol.orgon May 7, 2020 - Published by Downloaded from Copyright © 2018 American Society of Plant Biologists. All rights reserved.

http://www.ncbi.nlm.nih.gov/pubmed?term=Revell LJ%2E 2012%2E phytools%3A An R package for phylogenetic comparative biology %28and other things%29%2E Methods in Ecology and Evolution 3%3A 217%26%23x2013%3B223%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Revell&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=phytools: An R package for phylogenetic comparative biology (and other things)&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=phytools: An R package for phylogenetic comparative biology (and other things)&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Revell&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ripley BS%2C Abraham T%2C Klak C%2C Cramer MD%2E 2013%2E How succulent leaves of Aizoaceae avoid mesophyll conductance limitations of photosynthesis and survive drought%2E Journal of Experimental Botany 64%3A 5485%26%23x2013%3B5496%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ripley&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=How succulent leaves of Aizoaceae avoid mesophyll conductance limitations of photosynthesis and survive drought&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=How succulent leaves of Aizoaceae avoid mesophyll conductance limitations of photosynthesis and survive drought&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ripley&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Robinson SA%2C Osmond CB%2C Giles L%2E 1993%2E Interpretations of gradients in d13C value in thick photosynthesis tissues of plants with Crassulacean acid metabolism%2E Planta 190%3A 271%26%23x2013%3B276%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Robinson&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Interpretations of gradients in d13C value in thick photosynthesis tissues of plants with Crassulacean acid metabolism&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Interpretations of gradients in d13C value in thick photosynthesis tissues of plants with Crassulacean acid metabolism&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Robinson&as_ylo=1993&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Ronquist F%2C Teslenko M%2C Van Der Mark P%2C Ayres DL%2C Darling A%2C H�hna S%2C Larget B%2C Liu L%2C Suchard MA%2C Huelsenbeck JP%2E 2012%2E Mrbayes 3%2E2%3A Efficient bayesian phylogenetic inference and model choice across a large model space%2E Systematic Biology 61%3A 539%26%23x2013%3B542%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Ronquist&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Mrbayes 3&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Mrbayes 3&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Ronquist&as_ylo=2012&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=S�ez PL%2C Bravo LA%2C Cavieres LA%2C Vallejos V%2C Sanhueza C%2C Font%2DCarrascosa M%2C Gil%2DPelegr�n E%2C Javier Peguero%2DPina J%2C Galm�s J%2E 2017%2E Photosynthetic limitations in two Antarctic vascular plants%3A Importance of leaf anatomical traits and Rubisco kinetic parameters%2E Journal of Experimental Botany 68%3A 2871%26%23x2013%3B2883%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Sáez&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Photosynthetic limitations in two Antarctic vascular plants: Importance of leaf anatomical traits and Rubisco kinetic parameters&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Photosynthetic limitations in two Antarctic vascular plants: Importance of leaf anatomical traits and Rubisco kinetic parameters&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sáez&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Shen L%2C Chen Z%2E 2007%2E Critical review of the impact of tortuosity on diffusion%2E Chemical Engineering Science 62%3A 3748%26%23x2013%3B3755%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Shen&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Critical review of the impact of tortuosity on diffusion&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Critical review of the impact of tortuosity on diffusion&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Shen&as_ylo=2007&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Sifton HB%2E 1945%2E Air%2DSpace Tissue in Plants%2E Botanical Review 11%3A 108%26%23x2013%3B143%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Sifton&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Air-Space Tissue in Plants&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Air-Space Tissue in Plants&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Sifton&as_ylo=1945&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Silvera K%2C Neubig KM%2C Whitten WM%2C Williams NH%2C Winter K%2C Cushman JC%2E 2010%2E Evolution along the crassulacean acid metabolism continuum%2E Functional Plant Biology 37%3A 995%26%23x2013%3B1010%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Silvera&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Evolution along the crassulacean acid metabolism continuum&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Evolution along the crassulacean acid metabolism continuum&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Silvera&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Silvera K%2C Santiago LS%2C Winter K%2E 2005%2E Distribution of crassulacean acid metabolism in orchids of Panama%3A Evidence of selection for weak and strong modes%2E Functional Plant Biology 32%3A 397%26%23x2013%3B407%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Silvera&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Distribution of crassulacean acid metabolism in orchids of Panama: Evidence of selection for weak and strong modes&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Distribution of crassulacean acid metabolism in orchids of Panama: Evidence of selection for weak and strong modes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Silvera&as_ylo=2005&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Slaton MR%2C Smith WK%2E 2002%2E Mesophyll Architecture and Cell Exposure to Intercellular Air Space in Alpine%2C Desert%2C and Forest Species%2E International Journal of Plant Sciences 163%3A 937%26%23x2013%3B948%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Slaton&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Mesophyll Architecture and Cell Exposure to Intercellular Air Space in Alpine, Desert, and Forest Species&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Mesophyll Architecture and Cell Exposure to Intercellular Air Space in Alpine, Desert, and Forest Species&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Slaton&as_ylo=2002&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Syvertsen JP%2C Lloyd J%2C McConchie C%2C Kriedemann PE%2C Farquhar GD%2E 1995%2E On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves%2E Plant%2C Cell %26 Environment 18%3A 149%26%23x2013%3B157%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Syvertsen&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=On the relationship between leaf anatomy and CO2 diffusion through the mesophyll of hypostomatous leaves&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Syvertsen&as_ylo=1995&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Th�roux%2DRancourt G%2C Earles JM%2C Gilbert ME%2C Zwieniecki MA%2C Boyce CK%2C McElrone AJ%2C Brodersen CR%2E 2017%2E The bias of a two%2Ddimensional view%3A comparing two%2Ddimensional and three%2Ddimensional mesophyll surface area estimates using noninvasive imaging%2E New Phytologist 215%3A 1609%26%23x2013%3B1622%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Théroux-Rancourt&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The bias of a two-dimensional view: comparing two-dimensional and three-dimensional mesophyll surface area estimates using noninvasive imaging&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The bias of a two-dimensional view: comparing two-dimensional and three-dimensional mesophyll surface area estimates using noninvasive imaging&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Théroux-Rancourt&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Thomas GH%2C Hartmann K%2C Jetz W%2C Joy JB%2C Mimoto A%2C Mooers AO%2E 2013%2E PASTIS%3A An R package to facilitate phylogenetic assembly with soft taxonomic inferences%2E Methods in Ecology and Evolution 4%3A 1011%26%23x2013%3B1017%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Thomas&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=PASTIS: An R package to facilitate phylogenetic assembly with soft taxonomic inferences&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=PASTIS: An R package to facilitate phylogenetic assembly with soft taxonomic inferences&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Thomas&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tom�s M%2C Flexas J%2C Copolovici L%2C Galm�s J%2C Hallik L%2C Medrano H%2C Ribas%2DCarb� M%2C Tosens T%2C Vislap V%2C Niinemets �%2E 2013%2E Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species%3A Quantitative limitations and scaling up by models%2E Journal of Experimental Botany 64%3A 2269%26%23x2013%3B2281%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Tomás&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: Quantitative limitations and scaling up by models&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Importance of leaf anatomy in determining mesophyll diffusion conductance to CO2 across species: Quantitative limitations and scaling up by models&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tomás&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Tosens T%2C Nishida K%2C Gago J%2C Coopman RE%2C Cabrera HM%2C Carriqu� M%2C Laanisto L%2C Morales L%2C Nadal M%2C Rojas R%2C et al %282016%29 The photosynthetic capacity in 35 ferns and fern allies%3A mesophyll CO2 diffusion as a key trait%2E New Phytologist 209%3A 1576%26%23x2013%3B1590&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Tosens&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait.&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=The photosynthetic capacity in 35 ferns and fern allies: mesophyll CO2 diffusion as a key trait.&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Tosens&as_ylo=2016&as_allsubj=all&hl=en&c2coff=1


to the world of ancient living! Journal of Experimental Botany 68: 1639–1653.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Winter K, Holtum JAM, Smith JAC. 2015. Crassulacean acid metabolism: a continuous or discrete trait? The New phytologist 208: 73–8.Pubmed: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Zacharias N a, Nevers DR, Skelton C, Knackstedt K, Stephenson DE, Wheeler DR. 2013. Direct Measurements of Effective IonicTransport in Porous Li-Ion Electrodes. Journal of The Electrochemical Society 160: A306–A311.



http://www.ncbi.nlm.nih.gov/pubmed?term=Veromann%2DJ�rgenson LL%2C Tosens T%2C Laanisto L%2C Niinemets �%2E 2017%2E Extremely thick cell walls and low mesophyll conductance%3A Welcome to the world of ancient living%21 Journal of Experimental Botany 68%3A 1639%26%23x2013%3B1653%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Veromann-Jürgenson&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Veromann-Jürgenson&as_ylo=2017&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Winter K%2C Holtum JAM%2C Smith JAC%2E 2015%2E Crassulacean acid metabolism%3A a continuous or discrete trait%3F The New phytologist 208%3A 73%26%23x2013%3B8%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Winter&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Crassulacean acid metabolism: a continuous or discrete trait&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Crassulacean acid metabolism: a continuous or discrete trait&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Winter&as_ylo=2015&as_allsubj=all&hl=en&c2coff=1

http://www.ncbi.nlm.nih.gov/pubmed?term=Zacharias N a%2C Nevers DR%2C Skelton C%2C Knackstedt K%2C Stephenson DE%2C Wheeler DR%2E 2013%2E Direct Measurements of Effective Ionic Transport in Porous Li%2DIon Electrodes%2E Journal of The Electrochemical Society 160%3A A306%26%23x2013%3BA311%2E&dopt=abstract

http://scholar.google.com/scholar?as_q=&num=10&as_occt=any&as_sauthors=Zacharias&hl=en&c2coff=1

http://scholar.google.com/scholar?as_q=Direct Measurements of Effective Ionic Transport in Porous Li-Ion Electrodes&num=10&btnG=Search+Scholar&as_epq=&as_oq=&as_eq=&as_occt=any&as_publication=&as_yhi=&as_allsubj=all&hl=en&lr=&c2coff=1

http://scholar.google.com/scholar?as_q=Direct Measurements of Effective Ionic Transport in Porous Li-Ion Electrodes&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zacharias&as_ylo=2013&as_allsubj=all&hl=en&c2coff=1


short title: corresponding authors · 107 these ias traits, along with other previously measured...

Documents