acta oecologica 31 (2007) 168–173
available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/actoec
Original article
Leaf mass per area ratio in Quercus ilex leaves under a wide
range of climatic conditions. The importance of low
temperatures
Romà Ogaya*, Josep Peñuelas
Unitat d’Ecofisiologia CSIC-CEAB-CREAF, CREAF (Centre de Recerca Ecològica i Aplicacions Forestals), Universitat
Autònoma de Barcelona, E-08193 Bellaterra, Barcelona, Spain
article info
abstract
Article history:
The Digital Climatic Atlas and the Ecological and the Forestry Inventory of Catalonia (NE
Received 20 July 2005
Spain) were analysed to study the climate effect on leaf mass per area (LMA) and leaf
Accepted 27 July 2006
area index (LAI) on Quercus ilex L., one of the most widely spread tree species in the Med-
Published online 23 January 2007
iterranean region. 195 sites in this region of 31,895 km2 were considered. The relationship
between climatic variables (total annual rainfall, mean annual temperature, mean mini-
Keywords:
mum winter temperatures, and mean annual solar radiation) and LMA and LAI were ana-
Climate influence
lysed by simple and multiple regressions. LMA was higher in the drier sites and specially in
Leaf area index (LAI)
the colder sites. There was also a significant correlation between solar radiation and LMA.
Leaf mass per area (LMA)
On the contrary, LAI values, which were negatively correlated with LMA values, were lower
Mediterranean vegetation
in drier and colder sites, and were not significantly affected by solar radiation. The results
Quercus ilex
highlight that high LMA values do not seem to be a specific protection to dry conditions but
to a wide range of environmental stress factors, including low temperatures.
ª 2006 Elsevier Masson SAS. All rights reserved.
1.
Introduction
Climate influence on leaf traits such as morphology, longevity,
nutrient content, and photosynthetic rate are widely described in all biomes of the world (Field and Mooney, 1986;
Reich et al., 1992, 1997; Niinemets, 2001; Wright et al., 2004;
Traiser et al., 2005). A large number of studies have related
high LMA with evergreeness, long leaf longevity, thick cuticle,
low nitrogen content, and low photosynthetic rates (Körner,
1989; Turner, 1994; Eamus and Prichard, 1998; Aerts, 1995;
Yin, 2002). They are related with high solar irradiance (Chabot
and Chabot, 1977; Sobrado and Medina, 1980; Yun and Taylor,
1986; Witkowsky and Lamont, 1991; Groom and Lamont, 1997),
and drought conditions (Salleo and Lo Gullo, 1990; Witkowsky
and Lamont, 1991; Turner, 1994; Groom and Lamont, 1997; Niinemets, 2001).
Mediterranean environments are characterized by summer
drought as the most critical period for plant development
(Mooney, 1983) but winter cold is also described as an important
factor limiting plant photosynthetic rate and growth (Mitrakos,
1980; Terradas and Savé, 1992; Larcher, 2000; Oliveira and
Peñuelas, 2000, 2001, 2002, 2004). Holm oak (Quercus ilex L.) is
a drought-adapted tree widely distributed in the Mediterranean
Basin (Fig. 1; Debazach, 1983; Terradas, 1999), but this species
* Corresponding author. Tel.: þ34 9 3581 4036; fax: þ34 9 3581 4151.
E-mail address: [email protected] (R. Ogaya).
1146-609X/$ – see front matter ª 2006 Elsevier Masson SAS. All rights reserved.
doi:10.1016/j.actao.2006.07.004
acta oecologica 31 (2007) 168–173
169
Fig. 1 – Quercus ilex L. distribution in the Mediterranean basin and localization of the 150 sites from the Ecological and
Forestry Inventory of Catalonia where we sampled Q. ilex leaves.
shows lower resistance to dry conditions and higher tolerance
to low temperatures than other co-occurring Mediterranean
trees or shrubs such as Phillyrea latifolia (Lloret and Siscart,
1995; Peñuelas et al., 1998, 2000; Ogaya and Peñuelas, 2003), so
Q. ilex must compete with more drought-tolerant species in
the driest sites of its distribution and with temperate species
in the more mesic environments, where winter cold poses
severe limitations on Q. ilex photosynthetic activity and growth
(Oliveira and Peñuelas, 2000, 2001; Tretiach, 1993; Tretiach
et al., 1997).
In Q. ilex, low LMA values during the wettest periods have
often been observed (Gratani, 1996; Gratani and Varone,
2006), and LMA values were lower in leaves of resprouts
than in leaves of undisturbed trees in a clear-cut experiment
(Peña-Rojas et al., 2005). On the other hand, winter cold increases leaf photoinhibition and LMA values in response to
cold temperatures (Oliveira and Peñuelas, 2004). Moreover,
Clemente et al. (2005) have observed lower LMA in seedlings
and resprouts than in mature Mediterranean plants before
a fire due to higher water availability for seedlings and
resprouts.
We aimed to study the influence of the different climatic
variables (temperature, radiation, and rainfall) on LMA, LAI
and foliar nitrogen concentrations of Q. ilex trees living in
the field under a wide range of climatic conditions. Our focus
was to discern the effect of other environmental stressors
apart from the well known drought effects.
2.
Materials and methods
The data of this work were obtained from the Ecological
and Forestry Inventory of Catalonia (CREAF, Barcelona,
2003) (http://www.creaf.uab.es/iefc/) and from the digital
climatic atlas of Catalonia (http://magno.uab.es/atles-climatic/) (Pons, 1996; Ninyerola et al., 2000). One hundred
well-developed mature leaves from several Quercus ilex
mature trees were randomly collected from different parts
of the canopy, and they were used to measure LMA in
each one of 195 plots of this forestry inventory (Fig. 1).
The 195 plots were monitored (one time per plot) in campaigns throughout the whole year and only well-developed
mature leaves were collected. Nearby plots in space (but
with different climatic conditions due to local orography)
were measured during the same period, and some plots
with similar climate but well separated in space from
each other were measured during different periods within
the year. Therefore there were clusters of plots with similar
climate measured at different times of the year, greatly
buffering the variance associated to the measurement period. Each one of the 19,500 leaves (each sample was
obtained with a hole punch) were weighted after drying
at 70 C in an oven during three days, and LMA values
were calculated by the ratio of leaf dry weight and the
leaf surface area of the hole punch. The arithmetic mean
values of LMA of the 100 single leaf samples per plot
were used for stand level analyses. In 53 plots, all leaves
sampled at a plot were combined to a bulk sample; this
bulk was crushed and dried (75 C), and foliar nitrogen concentration in each one of those 53 plots was measured using an elemental analyser (Model NA 1500, Carlo Elba
Instrumentazione, Milan, Italy). LAI was obtained from allometric relationships between stem diameter and tree leaf
biomass calculated for each one of the 195 sites (always
highly significant, p < 0.001).
Total annual rainfall, mean annual solar radiation, and
mean annual and mean minimum winter temperatures
(obtained from meteorological stations data, from 1951 to
1999) were depicted in each one of the considered plots inserting plot coordinates in the digital climatic atlas. In the atlas,
climatic data were interpolated for each point in the map
(360 m between two consecutive points) with regressions between climatic variables and geographical variables, and the
regressions were readjusted with climatic data obtained
170
acta oecologica 31 (2007) 168–173
Fig. 2 – Total annual rainfall (a); mean annual air temperature (b); and solar radiation (c) of Catalonia (from the digital
climatic atlas of Catalonia) (Ninyerola et al., 2000; Pons, 1996). The location of the studied sites are depicted with asterisks.
from the meteorological stations (see detailed descriptions in
http://magno.uab.es/atles-climatic/; Pons, 1996; Ninyerola
et al., 2000).
2.1.
multiple linear regressions analyses were conducted to test
climatic relationships with LAI and foliar nitrogen concentration values. All regressions were performed with the Statistica
software package (Statsoft Inc., Tulsa, OK, USA).
Statistical analyses
Simple linear regressions were conducted to examine the relationships between LMA values and total annual rainfall (P),
mean annual solar radiation (R), mean annual temperature
(Tmean), and mean minimum winter temperatures (Tmin).
Two multiple linear regressions were conducted to test meteorological influence on LMA values, the first multiple regression was conducted with LMA values as dependent variable
and total annual rainfall, mean annual solar radiation, and
mean annual temperature as predictor variables, and the
other multiple regression was conducted with LMA values as
dependent variable and total annual rainfall, mean annual
solar radiation, and mean minimum winter temperatures as
predictor variables. In these two multiple regressions, the
forward stepwise regression technique was used.
Other simple linear regressions were conducted to examine the relationships between LMA and LAI values, and
between LMA and foliar nitrogen concentration values. Other
35
3.
Results
At the regional scale of this study, the range of climatic conditions of the studied Catalonia Q. ilex forests is very large including most of the typical climatic environments of the
Mediterranean region. The annual rainfall ranged from 436
to 1157 mm, the mean annual solar radiation from 10.9 to
17.1 MJ m2 day1, the mean annual temperature from 7.4 to
15.4 C (Fig. 2), and the mean minimum winter temperature
from 4.4 to 5.2 C.
LMA was negatively related to total annual rainfall, mean
annual temperature, and mean minimum winter temperatures, and it was positively correlated with solar radiation
(Fig. 3). The relationship between LMA and rainfall was very
weak (R2 ¼ 0.03; P ¼ 0.014). It was slightly stronger with solar
radiation (R2 ¼ 0.16; P < 0.001). The strongest climatic relationship was that with air temperatures (R2 ¼ 0.26 and R2 ¼ 0.34 for
2
y = 20.97 - 0.0050x R2= 0.031
2
2
y = -1.66 + 0.013x R = 0.16
y = 17.15 - 1.06x R = 0.34
y = 31.08 - 1.17x R = 0.26
25
20
15
a
b
Annual rainfall (mm)
c
Solar radiation
(MJ m-2 day-1)
d
10
5
12
10
600
LMA (mg cm-2)
30
Annual mean
temperature (ºC)
Mean minimum
winter temperature (ºC)
Fig. 3 – Linear relationships between LMA (leaf per mass area) values of Q. ilex in the 195 studied sites of Catalonia and
total annual rainfall (a); solar radiation (b); mean annual air temperature (c); and mean minimum winter air temperatures (d).
171
acta oecologica 31 (2007) 168–173
30
y = 25.32 - 7.62x R2= 0.14
y = 17.19 - 2.53log(x) R2= 0.38
LMA (mg cm-2)
25
20
15
10
5
0
2
4
6
8
LAI
10
1.2
1.4
1.6
1.8
2
Foliar nitrogen concentration (%dry weight)
Fig. 4 – Relationship between LMA (leaf per mass area) of Q. ilex and LAI (leaf area index) values (n [ 195 studied sites of
Catalonia), and between LMA and foliar nitrogen concentrations (n [ 53 studied sites of Catalonia).
mean annual temperature and mean minimum winter temperatures, respectively; and P < 0.001 in both cases; Fig. 3).
LMA was logarithmically and negatively correlated with LAI
(R2 ¼ 0.38; P < 0.001), and LMA was negatively correlated with
foliar nitrogen concentrations (R2 ¼ 0.14; P ¼ 0.006; Fig. 4).
Stepwise multiple regressions showed a strong influence of
precipitation, temperature and radiation on LMA values
(R2 ¼ 0.42 or R2 ¼ 0.45 depending on whether mean annual temperature or mean minimum winter temperatures are
considered; P < 0.01 in both cases) (Table 1). LAI values were
also dependent on climatic conditions, but less than LMA values
(R2 ¼ 0.25 and R2 ¼ 0.30 when mean annual temperature and
mean minimum winter temperatures were considered,
respectively; P < 0.001 in both cases; Table 1). LAI was positively
correlated with total annual rainfall, mean annual temperature,
and mean minimum winter temperatures, and was slightly negatively correlated with solar radiation: (LAI ¼ 1.24 þ 0.004 P;
R2 ¼ 0.12; P < 0.001), (LAI ¼ 0.44 þ 0.18 Tmean; R2 ¼ 0.04;
P ¼ 0.003), (LAI ¼ 1.67 þ 0.23 Tmin; R2 ¼ 0.11; P < 0.001), and
(LAI ¼ 4.81 0.002 R; R2 ¼ 0.03; P ¼ 0.012). Foliar nitrogen concentrations were not significantly correlated with any climatic
variable.
4.
Discussion
The results showed negative correlation between LMA and
temperature i.e. they did not apparently fit with those of
Table 1 – Multiple linear regression equations for LMA
(leaf per mass area) and LAI (leaf area index) values for
Q. ilex depending on different climatic variables: ‘‘P’’ is
total annual rainfall (mm), ‘‘Tmean’’ is mean annual
temperature ( C), ‘‘Tmin’’ is mean minimum winter
temperatures ( C), and ‘‘R’’ is solar radiation
(MJ mL2 dayL1)
LMA ¼ 37.24 0.011 P 1.399 Tmin þ 0.004 R
LMA ¼ 38.79 0.012 P 0.141 Tmean þ 0.004 R
LAI ¼ 2.25 þ 0.005 P þ 0.306 Tmin
LAI ¼ 6.66 þ 0.005 P þ 0.343 Tmean
r2 ¼ 0.45
r2 ¼ 0.42
r2 ¼ 0.30
r2 ¼ 0.25
p < 0.001
p < 0.001
p < 0.001
p < 0.001
a recent comprehensive study that considered a great amount
of vascular plant species (2370) from a wide range of vegetation types around the world (163 sites), in which in general
a low climate influence on leaf traits was found, but in which
LMA values increased when temperature increased (Wright
et al., 2004). As expected, in our study LAI values were lower
in driest sites, showing lower transpirational surface, but
LAI values increased also with temperature, despite of the
high evaporative demand of the warmest sites. The relationship between LAI and temperature could indirectly explain
a part of the inverse relationship between LMA and LAI, because lower LAI values were found at colder sites and LMA
was inversely correlated with temperature. But the major
part of the inverse relationship between LMA and LAI must
be accounted for a LAI effect by itself because the relationship
between LAI and temperature was very weak. LAI values can
vary in the same site depending on the local topography (i.e.
the top of a ridge, the bottom of a valley.) (Sala et al., 1994).
Canopies with low LAI values have a greater proportion of
sun leaves than canopies with high LAI values, and sun leaves
have larger LMA values than shade leaves (Sala et al., 1994).
The unexpected low LMA and high LAI values with high
temperatures, and the inverse relationship between LMA and
LAI suggest that under higher water availabilities and warmer
temperatures, Q. ilex tends to have more leaves with less LMA,
which is more efficient to maximize photosynthetic gain. But
under harder climatic conditions such as lower water availabilities and lower temperatures, Q. ilex plants invest more resources in strong and rigid leaves to resist climatic
adversities. High LMA values in Mediterranean vegetation are
often related to leaf resistance to dry conditions (Harley et al.,
1987; Kyparissis and Manetas, 1993; Gratani, 1996; Niinemets,
2001), and to high vapour pressure deficit and potential evapotranspiration (Wright et al., 2004). The results of this study
show higher LMA values in Q. ilex leaves in conditions of low
air temperatures, despite of relative high water availability of
cold sites compared to hot sites. Winter cold poses strong limitations to the photosynthetic activity in Mediterranean plants,
and leaves with higher LMA seem to be more capable to resist
low temperatures (Oliveira and Peñuelas, 2002, 2004). In
Q. ilex seedlings, lower leaf area is observed in plants from
172
acta oecologica 31 (2007) 168–173
colder sites and higher leaf density in plants from hotter sites,
which provides higher photosynthetic rates for smaller leaves
at low temperatures and higher water use efficiency for more
dense leaves at high temperatures (Gratani et al., 2003). A recent study conducted with different European flora species
also revealed minimum temperatures were the most important factor influencing some physiognomic characters such
as leaf size, which is lower in colder sites (Traiser et al., 2005).
In this Mediterranean species, Q. ilex, high LMA values did
not seem to be a protection only against dry conditions, indicating that a high LMA is a good adaptation trait to a wide
range of environmental stresses and not exclusive to any particular one (Turner, 1994).
Acknowledgments
We are grateful to Teresa Mata and Joan Josep Ibáñez for supplying the data from Inventari Ecològic i Forestal de Catalunya. This
research was financially supported by MEC projects REN200304871, and CGL2004-01402/BOS from the Spanish Government,
by the European project ALARM (Contract 506675, EU sixth
framework programme) and by a Fundación BBVA 2004 and
a SGR2005-00312 AGAUR-Generalitat de Catalunya grants.
references
Aerts, R., 1995. The advantages of being evergreen. Trends Ecol.
Evol. 10, 402–407.
Chabot, B.F., Chabot, J.F., 1977. Effects of light and temperature on
leaf anatomy and photosynthesis in Fragaria vesca. Oecologia
26, 363–377.
Clemente, A.S., Rego, F.C., Correia, O.A., 2005. Growth, water relations and photosynthesis of seedlings and resprouts after
fire. Acta Oecol. 27, 233–243.
Debazach, E.F., 1983. Temperate broad-lived evergreen forests of
the Mediterranean region and Middle East. In: Ovington, J.D.
(Ed.), Temperate Broad-leaved Evergreen Forests. Elsevier,
Amsterdam, pp. 107–123.
Eamus, D., Prichard, H., 1998. A cost-benefit analysis of leaves of
four Australian savanna species. Tree Physiol. 18, 537–545.
Field, C., Mooney, H.A., 1986. The photosynthesis-nitrogen relationship in wild plants. In: Givnish, T.J. (Ed.), On the Economy
of Plant Form and Function. Cambridge University Press,
Cambridge, pp. 25–55.
Gratani, L., 1996. Leaf and shoot growth dynamics of Quercus ilex
L. Acta Oecol. 17, 17–27.
Gratani, L., Varone, L., 2006. Long-time variations in leaf mass and
area of Mediterranean evergreen broad-leaf and narrow-leaf
maquis species. Photosynthetica 44, 161–168.
Gratani, L., Meneghini, M., Pesoli, P., Crescente, M.F., 2003.
Structural and functional plasticity of Quercus ilex seedlings of
different provenances in Italy. Trees 17, 515–521.
Groom, P.K., Lamont, B.B., 1997. Xerophytic implications of increased sclerophylly: interactions with water and light in
Hakea psilorryncha seedlings. New Phytol. 136, 231–237.
Harley, P.C., Tenhunen, J.D., Beyschlag, W., Lange, O.L., 1987.
Seasonal changes in net photosynthesis rates and photosynthetic capacity in leaves of Cistus salvifolius, a European Mediterranean semi-deciduous shrub. Oecologia 74, 380–388.
Körner, C., 1989. The nutritional status of plants from high altitudes. Oecologia 81, 379–391.
Kyparissis, A., Manetas, Y., 1993. Seasonal leaf dimorphism in
a semi-deciduous Mediterranean shrub: ecophysiological
comparisons between winter and summer leaves. Acta Oecol.
14, 23–32.
Larcher, W., 2000. Temperature stress and survival ability of
Mediterranean sclerophyllous plants. Plant Biosyst. 134,
279–295.
Lloret, F., Siscart, D., 1995. Los efectos demogràficos de la sequı́a
en poblaciones de encina. Cuad. Soc. Esp. Cien. For. 2, 77–81.
Mitrakos, K.A., 1980. A theory for Mediterranean plant life. Acta
Oecol. 1, 245–252.
Mooney, H.A., 1983. Carbon-gaining capacity and allocation patterns of Mediterranean climate plants. In: Kruger, F.J.,
Mitchell, D.T., Jarvis, J.U.M. (Eds.), Mediterranean-type Ecosystems: The Role of Nutrients. Springer, Berlin, pp. 103–119.
Niinemets, U., 2001. Global-scale climatic controls of leaf dry
mass per area, density, and thickness in trees and shrubs.
Ecology 82, 2390–2401.
Ninyerola, M., Pons, X., Roure, J.M., 2000. A methodological approach of climatological modelling of air temperature and
precipitation through GIS techniques. Int. J. Climatol. 20, 1823–
1841.
Ogaya, R., Peñuelas, J., 2003. Comparative field study of Quercus
ilex and Phillyrea latifolia: photosynthetic response to experimental drought conditions. Environ. Exp. Bot. 50, 137–148.
Oliveira, G., Peñuelas, J., 2000. Comparative photochemical and
phenomorhological responses to winter stress of an evergreen
(Quercus ilex L.) and a semi-deciduous (Cistus albidus L.) Mediterranean woody species. Acta Oecol. 21, 97–107.
Oliveira, G., Peñuelas, J., 2001. Allocation of absorbed light energy
into photochemistry and dissipation in a semi-deciduous and
an evergreen Mediterranean woody species during winter.
Aust. J. Plant Physiol. 28, 1–10.
Oliveira, G., Peñuelas, J., 2002. Comparative protective strategies
of Cistus albidus and Quercus ilex facing photoinhibitory
winter conditions. Env. Exp. Bot. 47, 281–289.
Oliveira, G., Peñuelas, J., 2004. The effect of winter cold stress on
photosynthesis and photochemical efficiency of PSII of two
Mediterranean woody species – Cistus albidus and Quercus ilex.
Plant Ecol. 175, 179–191.
Peña-Rojas, K., Aranda, X., Joffre, R., Fleck, I., 2005. Leaf morphology, photochemistry and water status changes in resprouting Quercus ilex during drought. Funct. Plant Biol. 32,
117–130.
Peñuelas, J., Filella, I., Llusià, J., Siscart, D., Piñol, J., 1998. Comparative field study of spring and summer leaf gas exchange
and photobiology of the Mediterranean trees Quercus ilex and
Phillyrea latifolia. J. Exp. Bot. 49, 229–238.
Peñuelas, J., Filella, I., Lloret, F., Piñol, J., Siscart, D., 2000. Effects of
a severe drought on water and nitrogen use by Quercus ilex and
Phillyrea latifolia. Biol. Plant 43, 47–53.
Pons, X., 1996. Estimación de la Radiación Solar a partir de modelos digitales de elevaciones. Propuesta metodológica. In:
Juaristi, J., Moro, I. (Eds.), Modelos y Sistemas de Información
en Geografı́a. Departamento de Geografı́a, Prehistoria y Arqueologı́a, Universidad del Paı́s Vasco, y Grupo de Métodos
Cuantitativos de la Asociación de Geógrafos Españoles, Vitoria-Gasteiz, ISBN 84-605-5896-7, pp. 87–97.
Reich, P.B., Walters, M.B., Ellsworth, D.S., 1992. Leaf life-span in
relation to leaf, plant, and stand characteristics among diverse
ecosystems. Ecol. Monogr. 62, 365–392.
Reich, P.B., Walters, M.B., Ellsworth, D.S., 1997. From tropics to
tundra: global convergence in plant functioning. Proc. Natl.
Acad. Sci. USA. 94, 13730–13734.
Sala, A., Sabaté, S., Gracia, C., Tenhunen, J.D., 1994. Canopy
structure within a Quercus ilex forested watershed: variations
due to location, phenological development, and water availability. Trees 8, 254–261.
acta oecologica 31 (2007) 168–173
Salleo, S., Lo Gullo, M.A., 1990. Sclerophylly and plant water relations
in three Mediterranean Quercus species. Ann. Bot. 65, 259–270.
Sobrado, M.A., Medina, E., 1980. General morphology, anatomical
structure, and nutrient content of sclerophyllous leaves of
‘‘the Bana’’ vegetation of Amazonas. Oecologia 45, 341–345.
Terradas, J., 1999. Holm Oak and Holm Oak Forests: An Introduction. In: Rodà, F., Retana, J., Gracia, C.A., Llebot, J. (Eds.),
Ecology of Mediterranean Evergreen Oak Forests. SpringerVerlag, Berlin Heidelberg, pp. 3–14.
Terradas, J., Savé, R., 1992. The influence of summer and winter
stress and water relationships on the distribution of Quercus
ilex L. Vegetatio 99/100, 137–145.
Traiser, C., Klotz, S., Uhl, D., Mosbrugger, V., 2005. Environmentals signals from leaves: a physiognomic analysis of European
vegetation. New Phytol. 166, 465–484.
Tretiach, M., 1993. Photosynthesis and transpiration of evergreen
Mediterranean and deciduous trees in an ecotone during
a growing season. Acta Oecol. 14, 341–360.
173
Tretiach, M., Bolognini, G., Rondi, A., 1997. Photosynthetic activity
of Quercus ilex at the extremes of a transect between Mediterranean and submediterranean vegetation (Trieste-NE Italy).
Flora 192, 369–378.
Turner, I.M., 1994. Sclerophylly: primarily protective? Func. Ecol.
8, 669–675.
Witkowsky, E.T.F., Lamont, B.B., 1991. Leaf specific mass
confounds leaf density and thickness. Oecologia 88,
486–493.
Wright, I.J., et al., 2004. The worldwide leaf economics spectrum.
Nature 428, 821–827.
Yin, X., 2002. Responses of leaf nitrogen concentration and
specific leaf area to atmospheric CO2 enrichment: a retrospective synthesis across 62 species. Global Change Biol. 8,
631–642.
Yun, J.I., Taylor, S.E., 1986. Adaptative implication of leaf thickness for sun- and shade-grown Abutilon theophrasti. Ecology 67,
1314–1318.