Research

Are correlations among foliar traits in ferns consistent with

Blackwell Publishing Ltd

those in the seed plants?

Amanda L. Karst1,* and Martin J. Lechowicz2
1
Department of Biology, University of Regina, 3737 Wascana Parkway, SK, S4S 0A2, Canada; 2Department of Biology, McGill University, 1205 Avenue
Dr Penfield, Montreal, QC, H3A 1B1, Canada; *Present address: Center for Indigenous Environmental Resources, 245 McDermot Ave, Winnipeg, MB,
R3B 0S6, Canada

Summary

Author for correspondence: • Broad-based studies of gymnosperms and angiosperms reveal consistent and
Amanda L. Karst functionally significant correlations among foliar traits such as leaf mass per area
Tel: +1 204 783 2842
(LMA), maximum photosynthetic rate (Aarea), foliar nitrogen (Narea), foliar chloro-
Fax: +1 204 956 1895
Email: akarst@cier.ca phyll (Chl) and leaf longevity.
• To assess the generality of these relationships, we studied 20 fern species growing
Received: 7 June 2006
Accepted: 12 September 2006
in the understorey of a temperate deciduous forest.
• We found that foliar Narea increases with LMA, and that foliar Narea and Aarea are
positively correlated with one another, as are foliar Narea and Chl. The ferns in general
have very low LMA compared with most seed plants; Aarea, Narea and Chl are below
median values for seed plants but are not extreme. Species with overwintering
fronds have significantly higher LMA than species with fronds that senesce at the
end of the growing season, as well as a significantly higher C : N ratio in frond tissue
and relatively high foliar N on an areal basis.
• Correlations among foliar traits associated with gas exchange in these forest
understorey ferns are in accordance with patterns reported for seed plants, suggest-
ing a high degree of functional constraint on the interrelationships among key
elements in foliar design.
Abbreviations: LMA, leaf mass per area (g DW m−2); Aarea, maximum photosyn-
thetic rate, expressed per unit leaf area (µmol CO2 m−2 s−1); Narea, mass of N per unit
leaf area (g m−2); Chl, chlorophyll per unit leaf area (mg m−2).

Key words: chlorophyll content, foliar design, GLOPNET, leaf economics spectrum,
leaf mass per area (LMA), net photosynthetic rate, nitrogen content, seedless
vascular plants.

New Phytologist (2007) 173: 306 –312

© The Authors (2006). Journal compilation © New Phytologist (2006)

doi: 10.1111/j.1469-8137.2006.01914.x

organizing the evolution of functional diversity in higher

Introduction
An appreciation has begun to emerge of some apparently
fundamental relationships among key functional traits in
gymnosperms and angiosperms, especially with regard to the
form and function of leaves (Westoby et al., 2002; Reich
et al., 2003; Wright et al., 2004; Shipley et al., 2006). Central
to these relationships is the tendency of leaf mass per unit area
(LMA) to increase with leaf longevity, a relationship that
Westoby et al. (2002) consider one of three critical tradeoffs
plants. Other traits critical to the function of leaves as photo-
synthetic organs (photosynthetic capacity, foliar nitrogen and
chlorophyll concentration) are correlated to these two key
traits, although the relationships can vary somewhat depending
on whether traits are expressed per unit foliar area or per unit
foliar mass (Reich & Walters, 1994; Shipley & Lechowicz,
2000; Reich et al., 1999, 2003; Wright et al., 2004). For
example, when expressed per unit mass, both foliar N con-
centrations and photosynthetic capacity decrease as LMA

306 www.newphytologist.org

increases, but when expressed on an areal basis, foliar N
increases with LMA and photosynthetic capacity has no
significant relationship to LMA (Wright et al., 2004). These
sorts of relationships among foliar traits persist despite large
variation in the values of the traits across individual species
with very diverse phylogenetic, biogeographical and environ-
mental affinities (Wright et al., 2004), and appear to arise in
fundamental ecophysiological and evolutionary tradeoffs in
leaf design (Shipley et al., 2006).
The existence of these apparently global trends suggests
that certain relationships among functionally important foliar
traits may have been conserved throughout the evolution of
vascular plants (Reich et al., 2003; Shipley et al., 2006), but in
fact these relationships have not been studied in the most
ancient vascular lineages, the seedless vascular plants. The data
collated by Wright et al. (2004) for 2021 vascular plant
species include estimates of photosynthetic capacity for only
six fern species. Ferns represent a distinct path in vascular
plant evolution (Page, 2002), in which the generality of pat-
terns in foliar form and function can be assessed. The ancestry
of angiosperms and gymnosperms diverged from that of the
ferns relatively early in the evolutionary history of terrestrial
plants (Rothwell, 1996; Pryer et al., 2001), although diversi-
fication of the modern ferns occurred predominantly during
the Cretaceous (Schneider et al., 2004). Here we make an initial
comparison of the relationships among foliar traits in ferns with
those reported in the seed plants. Specifically, we examined
the interrelationships among leaf mass per unit area (LMA),
photosynthetic capacity, N concentration, chlorophyll con-
centration, and the C : N ratio in fronds from 20 species of
fern growing in the understorey of a temperate deciduous
forest. We were able to consider possible longevity effects only
by comparing species with overwintering fronds (winter-green)
and nonoverwintering fronds (Tessier, 2001; Tani & Kudo, 2003,
2005; Reudink et al., 2005). We expected that the relationships
among foliar traits in this sample of ferns from temperate forest
understorey would be qualitatively consistent with trends
observed in the seed plants. While this is the first broad com-
parative study of foliar traits among co-occurring fern species,
we recognize that its limited geographical and phylogenetic
scope allows only a preliminary assessment of this expectation.
Materials and Methods
Field work was conducted at the Gault Nature Reserve (http://
www.mcgill.ca/gault) located on Mont St Hilaire, 32 km
south-east of Montréal, Québec, Canada. The reserve is a 10-km2
tract of old-growth deciduous forest on a rugged hill complex
that rises to an elevation of 300 m above the surrounding
countryside. The flora and vegetation of the reserve have been well
characterized (Maycock, 1961; Arii & Lechowicz, 2002); 38 fern
species occur in a wide variety of habitats within the reserve.
Twenty-nine sampling locales were chosen based on acces-
sibility and fern abundance, all at lower elevations within the
© The Authors (2006). Journal compilation © New Phytologist (2006) www.newphytologist.org
Research 307
reserve. All were in forest understorey or in small openings
along streams and trails. Twenty fern species in six families
(Table S1 in Supplementary Material) were chosen to obtain
a broad range in traits such as plant size, frond color, degree
of frond dissection and frond thickness. Four fern species with
overwintering fronds (Morin, 1993) were available, allowing
only preliminary comparisons of the effects of leaf longevity
on foliar characteristics. In these four species, overwintering
fronds that develop in the spring senesce the following spring
when new fronds develop.
A portable gas-exchange system (Li-Cor 6400, Lincoln,
NE, USA) was used to record photosynthetic CO2 assimila-
tion and leaf water vapor conductance under consistent assay
conditions. Ferns at three to four sampling sites were meas-
ured each day over a total of 15 d between 3 July and 8 August
2001. The order of species measured at each site was chosen
at random. Ferns to be sampled were selected and watered the
evening before measurement to minimize stomatal limitations
on photosynthetic CO2 assimilation.
Photosynthetic measurements were taken between 06 : 30
and 10 : 30 h (solar time), to minimize effects of afternoon
stomatal closure and because photosynthetic rates are typi-
cally highest during the morning (Gildner & Larson, 1992).
All photosynthetic measurements were made at ambient
humidity while maintaining CO2 concentration at 350 ppm,
photosynthetic photon flux density at 2000 µmol m−1 s−1,
and temperature at 25°C. We assumed all fern species
sampled had stomata on only the underside of the frond
(cf. Ludlow & Wolf, 1975). Only healthy, mature and vegeta-
tive fronds were used, and the cuvette was placed on the frond
so as to avoid mid-veins.
The sampled portion of the frond was excised and promptly
photocopied; leaf area was determined from the photocopy
using a digital area analyser (DIAS II, Decagon Devices Inc.,
Pullman, WA, USA). The leaf samples were then dried and
weighed. We sampled two to five fronds from each ‘individual/
plant’ (presumed genotypic colony) at a site. In total, two to
five plants of each species (four to 13 fronds in total, averaging
two fronds per plant) were sampled (Table S1).
Using a hand-held meter (SPAD-502, Minolta Corp.,
Ramsey, NJ, USA), we made 20 measurements on each frond
used in the gas-exchange assays to estimate foliar chlorophyll
concentration (Monje & Bugbee, 1992); the SPAD-502 meter,
which senses absorption at 650 nm, gives a robust estimate of
chlorophyll for comparisons across species (Ichie et al., 2002).
The fronds measured for gas exchange and chlorophyll con-
tent were harvested and dried at 70°C for 48 h, ground in a
mortar and pestle, and analysed for C : N using an EA1108
elemental analyser (VG Elemental, Fisons Instruments, Beverly,
MA, USA). We calculated area-based N values by multiplying
the N concentration from the elemental analyser and LMA.
The LMA was determined from the portion of the frond used
in the Li-Cor cuvette, while the rest of the frond was used for
C : N analysis.
New Phytologist (2007) 173: 306–312
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Statistical analysis
All variables were log-transformed except the C : N ratios.
Frond values were averaged within individual plants and
individual plants within species to use in the regressions. Table S1
indicates the total number of fronds as well as the total number
of plants measured for each species. To test for significant
relationships between LMA, Aarea, Amass (nmol CO2 g−1 s−1),
foliar Narea, foliar Nmass (mg g−1) and chlorophyll, we used type
II regression in the program (S)MATR (STANDARDISED MAJOR AXIS
TESTS & ROUTINES, ver. 1.0, 2003). We calculated standardized
major axis regressions to determine if there were significant
differences in slope between groups of data: (1) our four
overwintering vs 16 nonoverwintering fern species; and (2) all
our 20 fern species vs the GLOPNET leaf economics data set of
Wright et al., 2004 (2021 species; supplementary information
at http://www.nature.com/nature/supplements/index.html).
Significant differences in slope values between groups were
reported only if both groups individually had significant
correlations between variables. Differences in LMA, Aarea,
foliar Narea, Chl and C : N ratios between the two leaf longevity
categories were compared using a Kruskal–Wallis test on species
means. Values reported are nontransformed means ± SD. Kruskal–
Wallis tests were performed using SYSTAT (ver. 9, 1998, SPSS
Inc., Chicago, IL, USA). We collated some additional fern
data from the literature (Brach et al., 1993; Russell et al.,
1998; Durand & Goldstein, 2001; Saldana et al., 2005) to
extend the analyses and enrich the illustrations. Fig. 1 Regression of (a) species mean area-based foliar nitrogen
(r2 = 0.728; P < 0.0001) and (b) species mean area-based maximal
net photosynthetic rate (Amax) (r2 = 0.193; P > 0.05) on leaf mass per
Results area (LMA), all variables log-transformed. Only significant
relationships show regression lines.
The overall qualitative relationships among foliar traits were
consistent with those reported for seed plants (Wright et al.,
2004). Both LMA (r 2 = 0.728, P < 0.0001; Fig. 1a) and Aarea
(r2 = 0.39, P < 0.005; Fig. 2) had significant positive relation-
ships with foliar N (Table 1). Considering only fern species
with nonoverwintering fronds, Aarea increased with LMA
(r2 = 0.514, P < 0.002), but this relationship was only margin-
ally significant when species with overwintering fronds were
included in the analysis (r 2 = 0.193, P = 0.0525; Table 1;
Fig. 1b). Additional literature data for fern species with a
greater range of LMA values suggest that this relationship is
not significant for ferns in general (cf. Fig. 4a; r 2 = 0.030;
P = 0.29), as is also the case for seed plants (Wright et al., 2004).
As in the seed plants (Wright et al., 2004), areal and mass-based
estimates of photosynthetic capacity are highly correlated
(r2 = 0.485; P < 0.001; Table 1), and the relationship between Fig. 2 Regression of species mean area-based maximal net
photosynthetic capacity and foliar N remained the same regardless photosynthetic rate (Amax) on area-based nitrogen, both variables log
of expression on an areal or mass-basis (Table 1). Foliar Chl transformed (r2 = 0.39; P < 0.005).
increased with increasing N (r 2 = 0.645, P < 0.0001; Fig. 3).
Although our sample size is small, ferns with overwinter- differ in Aarea (P > 0.05). Overwintering fronds also had sig-
ing fronds stand out as a fairly distinct subset (Figs 1–3). nificantly higher C : N ratios (P < 0.01; Table S1), due to
Overwintering species have higher LMA (P < 0.01, Kruskal– their relatively heavy investment in carbon compared with N.
Wallis test), Narea (P < 0.02) and Chl (P < 0.05), but do not When separate regressions were done for each leaf longevity

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 Research 309

Table 1 Type II regression values: r2, slope,

confidence intervals (CI) and P for both Foliar trait r2 Slope Lower CI Upper CI P P (H0 = slope)
regressions and the common slope test
between fern data and the GLOPNET data set Aarea vs Narea 0.390 1.41 0.96 2.05 0.0032 0.435
of Wright et al. (2004) using (S)MATR software Aarea vs LMA 0.193 1.27 0.83 1.96 0.0525 0.163
between both area-based and mass-based Narea vs LMA 0.728 0.904 0.70 1.17 0.0001 0.017
foliar variables Chl vs Narea 0.645 0.867 0.648 1.16 0.0001 –
Aarea vs Amass 0.485 0.950 0.671 1.35 0.001 –
Amass vs Nmass 0.370 2.42 1.65 3.54 0.0045 0.078
Amass vs LMA 0.113 −1.21 −1.90 −0.77 0.1466 0.679
Nmass vs LMA 0.181 −0.50 −0.77 −0.32 0.0615 0.028
Chl vs Nmass 0.016 1.57 0.98 2.52 0.5992 –

Aarea, maximum photosynthetic rate per unit area; Narea, foliar nitrogen per unit area; LMA, leaf
mass per area; Chl, foliar chlorophyll; Amass, maximum photosynthetic rate per unit mass;
Nmass, foliar nitrogen per unit mass.

Fig. 3 Regressions of species mean chlorophyll per unit area on area-
based nitrogen, both variables log-transformed (r2 = 0.645;
P < 0.0001).
category, N and Chl remained significantly correlated for
nonoverwintering fronds (r 2 = 0.636, P < 0.005), but the
sample size was too small to detect a correlation with overwin-
tering fronds (r 2 = 0.593, P > 0.05). However, the scatter plot
suggests that chlorophyll increases more rapidly with increas-
ing N in overwintering fronds (Fig. 3).
When comparing slopes between our fern data and the
GLOPNET data (Wright et al., 2004; Figs 4 & 5), the rela-
tionship between Narea vs LMA had significantly different slopes
(P = 0.017; Fig. 4b); the same applies for Nmass (P = 0.028;
Table 1), although here the Nmass–LMA relationship for our
fern data is not quite significant (Table 1). In both cases,
however, the trends are similarly positive and differ only
quantitatively. All other bivariate relationships showed no
difference in slope between our fern data and the GLOPNET
data, or did not have adequate data to detect a difference.
Discussion
Although the values for LMA, Aarea and Narea all fall well below
the median values reported for seed plants, the relationships
among the traits are generally consistent with those observed
in the seed plants (Wright et al., 2004). For example, Aarea and
Narea are positively correlated, and Narea increases with increas-
ing LMA. The lack of significant relationship between Aarea
and LMA is also consistent with trends in seed plants (Wright
et al., 2004). Foliar relationships in ferns, however, were
stronger when expressed on an areal basis than when expressed
per unit foliar mass (Table 1), which is contrary to some previ-
ous studies of seed plants (Reich et al., 1992, 1994, 1997, 1998).
This nuance aside, the overall qualitative relationships among
foliar traits in ferns closely follow those reported for seed plants.
The most striking quantitative difference between ferns and
seed plants is that the LMA of ferns is at the lower end of the
range for seed plants, at least for the temperate understorey
ferns that have been most studied. Values of Aarea and Narea are
not nearly as extreme in their divergence from seed plant norms.
These low LMA values might be explained because most fern
species in temperate regions show a strong affinity for at least
partially shaded understorey habitats (Greer et al., 1997), and
therefore could be expected to have lower LMA than sun-
adapted species (Brach et al., 1993; Terashima et al., 2001).
However, this does not appear to be the case. In controlled
experiments on acclimation to shade vs sun in Dryopteris
intermedia and Dennstaedtia punctilobula (Brach et al., 1993),
both species had higher LMA when grown in sun but values
were still at the low end of the range for seed plants. Saldana
et al. (2005) report similar results for three understorey species
of Blechnum in a broadleaf evergreen temperate forest. Even in
a fern such as Pteridium aquilinum that is common in open
habitats, reported values of LMA and photosynthetic capacity
are not particularly high (Table S1; Oikawa et al., 2004).
Two other explanations for these low LMA values in ferns
merit investigation. The first is the possibility that a wider
sampling of fern growth forms and provenances would reveal
the observed values to be characteristic of only temperate
understorey species. Studies of tree ferns (Durand & Gold-
stein, 2001) and climbing ferns (Russell et al., 1998) in
Hawaii report LMA values in the mid-range observed for
other vascular plants, but no ferns have LMA values as high
as those commonly associated with many gymnosperms and
angiosperms having multi-age cohorts of long-lived foliage.

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310 Research
Ferns do not appear to have frond longevities exceeding 2–
3 yr (Sato, 1982; literature cited by Sharpe, 1997). A second
possibility is that there are constraints imposed by the hydrau-
lic architecture of ferns that limit the thickening or increased
density of fern fronds. Ferns have well developed vascular sys-
tems, some containing xylem vessels as well as tracheids; a few
of our study species are among those containing vessels (Car-
lquist & Schneider, 2001). Nonetheless, there is evidence that
fern hydraulic conductance capacity is at the low end of that
for seed plants (Brodribb et al., 2005). More comprehensive
comparison of ferns with other vascular plants should yield
insight into alternative paths for the evolution of both hydrau-
lic and foliar function at the whole-plant level.
Finally, with regard to leaf longevity patterns, it is notewor-
thy that overwintering fronds have the highest LMA among
these understorey ferns. This is consistent with expectations
New Phytologist (2007) 173: 306–312 www.newphytologist.org © The Authors (2006). Journal compilation © New Phytologist (2006)
Fig. 4 Scatter plot of (a) area-based maximal
net photosynthetic rate (Amax) and (b) area-
based nitrogen with leaf mass per area (LMA)
for all species cited by Wright et al. (2004)
and fern species measured in this study
(category ‘Ferns: other’ includes data
collected from papers that were not originally
in the GLOPNET data set); all variables log-
transformed. The two data sets had
significantly different slopes for area-based N
vs LMA (Wright et al., 2004; slope = 0.651,
fern slope = 0.904; P < 0.02). Only significant
relationships show regression lines.
based on their somewhat greater longevity (Westoby et al.,
2002; Wright et al., 2004), but not with other foliar traits.
Based on earlier investigation of seed plants, we would also
expect species with overwintering fronds to have lower foliar
N and less photosynthetic capacity on an areal basis compared
with fronds from nonoverwintering species (Wright et al., 2004).
In fact, on an areal basis ferns with overwintering fronds had
similar photosynthetic capacity and decidedly high levels of
foliar N. Although there was a linear relationship between
Aarea and foliar Narea, for a given amount of foliar Narea the
overwintering fronds actually had lower Aarea. Compared with
fronds in nonoverwintering ferns, species with overwintering
fronds have relatively low N concentration on a mass basis
and relatively high investment in foliar C – characteristics
associated with sclerophylly in seed plants. The significantly
higher C : N ratio in fronds of overwintering compared with

Fig. 5 Scatter plot of area-based maximal net
photosynthetic rate (Amax) and area-based
nitrogen for all data cited by Wright et al.
(2004) and for fern species measured in this
study (category ‘Fern: other’ includes data
collected from papers that were not originally
in the GLOPNET data set); all variables are
log-transformed. The two data sets showed
significant differences along a common slope
(Wright et al., 2004; slope = 1.21, fern
slope = 1.41; P < 0.001).
nonoverwintering fern species is consistent with previous
findings that overwintering leaves allocate more C for struc-
tural purposes, which dilutes total N and results in a higher
C : N ratio (Reich et al., 1999). These results emphasize that it
may not be LMA that principally organizes functional variation
in foliar traits (Westoby et al., 2002), but rather the ratio of cell
sap to cell wall that independently influences LMA, maximum
photosynthetic rate, N and longevity (Shipley et al., 2006).
The overwintering habit provides potential benefits (Tessier,
2001; Tani & Kudo, 2003, 2005; Reudink et al., 2005), but
also constrains the relationships among foliar LMA, maxi-
mum photosynthetic rate and N. Increased leaf lifespan in
understorey plants (such as ferns) has been described as a strat-
egy to exploit the high irradiance levels that occur when can-
opy tree species in temperate deciduous forests have not yet
begun growing in spring, or are senescing in autumn (Reich
et al., 1992). This is consistent with our observation that ferns
with overwintering fronds partition more chlorophyll per
unit foliar N than has been found in many slow-growing over-
wintering species grown either in high or low light (Reich,
1993; Poorter & Evans, 1998). Overwintering fronds not only
extend their period of photosynthesis, but also decrease over-
all construction costs of new fronds by keeping nutrients in
overwintering fronds and redistributing them in the spring
directly to the new fronds (Norden & Wagner, 1997). Rela-
tively high C investments in cell structure (high LMA) ensure
frond integrity over winter and reduce N concentration on a
mass basis but, given frond morphology, also increase N con-
centration on an areal basis; this accounts for the tendency
of the relationships between both A and N vs LMA to reverse
sign when expressed on an areal vs mass-basis (Table 1), and
further emphasizes that LMA is not the dominant element in
foliar design (Shipley et al., 2006).
In conclusion, the interrelationships among foliar traits in
ferns and seed plants are broadly consistent, but do differ in
© The Authors (2006). Journal compilation © New Phytologist (2006) www.newphytologist.org
Research 311
some respects. These differences are most apparent in the rela-
tionship of traits to leaf longevity in overwintering vs non-
overwintering species. The correlations between LMA and
traits such as Aarea, N and Chl follow expectations based on
previous work on seed plants, as does the high C : N ratio
associated with overwintering fronds. The LMA itself for
ferns is at the low end of values observed in seed plants, per-
haps due to limitations imposed by the hydraulic systems in
ferns. The relationships of LMA to other foliar characteristics
in ferns and the influence of modest variation in leaf longevity
are consistent with general principles of foliar design expressed
in a forest understorey environment, which has been the
primary venue for the evolutionary diversification of ferns
(Schneider et al., 2004).
Acknowledgements
We thank Harold Weger for support to A.K. throughout the
project, Craig Willis for help in the field and for comments on
the manuscript. Rolf Vinebrooke and Jim Rusak provided
statistical advice. The comments of two anonymous referees
significantly improved the manuscript. Christian Marks and
Marisha Futer provided technical support. Jeff Yuen, Anneli
Jokela and Valerie Roy helped process samples. We acknowledge
scholarship support (A.K.) and research funding (M.J.L.) from the
Natural Sciences and Engineering Research Council of Canada.
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Supplementary Material
The following supplementary material is available for this
article online:
Table S1 Species and family names, number of fronds and
plants measured, and mean values of all area-based foliar
variables measured for each fern species
This material is available as part of the online article from:
http://www.blackwell-synergy.com/doi/abs/10.1111/j.1469-
8137.2006.01914.x
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