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Leaf Form and Photosynthetic Physiology of Dryopte
Leaf Form and Photosynthetic Physiology of Dryopte
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Summary
1. Despite the ubiquity of ferns and at least tacit recognition by botanists that their physio-
logy is unique among land plants, most studies on fern physiology have focused on only a few,
locally distributed, usually distantly related species. No previous study has attempted to
examine physiological adaptations in a group of widespread taxa that are closely related and
whose relationships are well understood. Here we report leaf form and physiological measures
for such a group, the 11 eastern North American species of Dryopteris (Dryopteridaceae), and
examine differences in these parameters for evidence of adaptation to light availability.
2. Economic theory predicts that species from sunnier habitats should have narrower, more
steeply inclined leaves, lower specific leaf area, higher stomatal density, higher rates of maxi-
mum photosynthesis, respiration and stomatal conductance, and require more light to saturate
photosynthesis. Species should show adaptive crossover in net carbon uptake per unit leaf
mass, with a relative advantage by sun-associated species at high photon flux densities (PFDs)
and by shade-associated species at low PFDs.
3. Field studies allow us to begin characterizing the range of native light environments
occupied by members of this group, and to examine interspecific variation in several aspects of
leaf form and photosynthetic light response for evidence of adaption to light availability. We
also present a novel means for incorporating phylogeny in tests of correlated evolution in a
reticulate lineage.
4. Synthesis. Observed trends in physiology and morphology generally agree with qualitative
predictions but are often not statistically significant. We found no support for adaptive cross-
over in mass-based carbon uptake, and thus for light availability being the most important var-
iable driving morphological and physiological adaptation in these ferns. We propose that
hydraulic factors related to water balance may have played a larger role in determining their
morphological and physiological variation. Allopolyploid hybrids did not show transgression
in any physiological parameter that may have allowed them to coexist regionally with their
parents. The results of our phylogenetically structured analyses highlight the importance of
incorporating phylogeny into comparative studies, particularly when hybrid or polyploid taxa
are present.
Key-words: comparative methods, ferns, gas exchange, hydraulics, light regimes, photosyn-
thetic light response, polyploidy, transgressive trait expression
allowed them to persist despite limiting constraints of their constraint on survival and competitive success under dif-
biology. Ferns are characterized ecologically by an inde- ferent light regimes than variation in photosynthetic
pendent, ephemeral gametophyte stage (Watkins, Mack & parameters. A comparative study of the evolution of pho-
Mulkey 2007), low rates of photosynthesis, vascular tissue tosynthetic parameters among related fern species native
development and leaf hydraulic conductance (Brodribb & to different light regimes should thus be illuminating,
Holbrook 2004; Brodribb, Feild & Jordan 2007; Boyce regardless of whether the traditional patterns seen in flow-
et al. 2009; Watkins, Holbrook & Zwieniecki 2010), rela- ering plants are observed in ferns or not.
tively high photosynthetic capacity in low light (Page A better understanding of traits that drive adaptation to
2002), slow plant growth rates (Page 2002) and low stoma- different environments and lead to niche differentiation
tal densities (Franks & Farquhar 2006; Kessler et al. may also allow us to evaluate possible mechanisms for the
2007). persistence of hybrid and polyploid taxa, which are extre-
Biologists have traditionally viewed ferns as once-domi- mely common in ferns (Manton 1950; Wood et al. 2009).
nant organisms of ancient ecosystems that were quickly Newly formed polyploids are subject to minority cytotype
out-competed and relegated to the shadows following the exclusion, in which polyploid cytotypes experience a fre-
evolution of seed plants in the Devonian, and especially quency-dependent mating disadvantage and waste repro-
after the rise of flowering plants in the Cretaceous (Niklas, ductive effort in ineffective matings with the established
Tiffney & Knoll 1983; Lupia, Lidgard & Crane 1999; Nag- parental cytotype (Levin 1975). Niche differentiation
alingum et al. 2002). Recent research has challenged this between progenitors and offspring has been suggested as a
view (Rothwell 1996), and studies based on fossil and potential mechanism allowing polyploids to persist region-
molecular dating evidence have demonstrated that ferns ally with their parental species on evolutionary time-scales
underwent their major radiation into modern lineages only (Rodriguez 1996). In particular, ploidy increases are likely
after the appearance of the angiosperms in the Cretaceous to increase cell volume (Melaragno, Mehrota & Coleman
(Schneider et al. 2004; Schuettpelz & Pryer 2009). Recent 1993; Comai 2005), potentially increasing values for traits
research has identified several physiological features of such as specific leaf area (SLA, cm2 g1), as well as tra-
ferns that may have contributed to their success in various cheid diameters and thus hydraulic conductance. Such
terrestrial ecosystems, including cavitation-resistant, tra- increases may have important implications for light
cheid-based xylem (Watkins, Holbrook & Zwieniecki 2010; capture and water loss, potentially making hybrids less
Pittermann et al. 2011), a host of adaptations to xeric hab- susceptible to internal self-shading and drought.
itats (Hietz 2010), and chimeric photoreceptors that The 11 eastern North American members of the wood-
enhance plastid movement in response to light at low flu- fern genus, Dryopteris, are an ideal group for addressing
ences (Kawai et al. 2003; Suetsugu et al. 2005; Kanegae these questions. These species vary extensively in leaf mor-
et al. 2006). Chimeric photoreceptors combine phyto- phology and habitat, from species found only on brightly
chrome and phototropin functionality to allow red light, lit, well-drained cliff faces and possessing narrow, short,
which is typically enriched relative to blue light in forest erect fronds (e.g. D. fragrans), to species of heavily shaded,
understoreys (Endler 1993), to trigger phototrophic mesic forest understoreys that often have relatively broad,
responses and chloroplast relocation, which are typically tall, sprawling fronds (e.g. D. goldiana; Fig. 1). Some of
initiated only by blue or UV light. Arens (1997) found that these species also occur in Europe and Asia, but eight are
several leaf characters in tree ferns are strongly correlated endemic to eastern North America. Sessa, Zimmer &
with light environment; together these data suggest that Givnish (2012a) recently demonstrated that the 11 North
traits related to light response may have played an impor- American species are not each others’ closest relatives, and
tant role in shaping fern evolution. However, no study has that each of the six diploids in the group is more closely
yet attempted to test the extent to which adaptation to dif- related to Asian or European species than to other North
ferent light environments may drive the evolution of mor- American diploid taxa. The remaining five eastern North
phological and physiological characters within a fern American species are allopolyploids, formed over the last
lineage, or to trace the evolution of such traits in a phylo- 13 million years via hybridization and genome doubling
genetic framework. A high sensitivity of plastid movement involving three of the extant North American diploids and
to light, for example, opens the possibility that tight corre- one extinct progenitor (Sessa, Zimmer & Givnish 2012b;
lations among the photosynthetic parameters Amax, R and Table 1). Tani & Kudo (2003, 2005), and Tessier & Bornn
k (maximum photosynthetic rate, dark respiration rate and (2007) have examined biomass allocation and the contribu-
the amount of light required to half-saturate photosynthe- tions of overwintering leaves to carbon uptake in several
sis, respectively) seen in many angiosperms (e.g. see Dryopteris species, and R€ unk, Zobel & Zobel (2010) and
Bj€orkman 1981; Givnish 1988; Walters & Reich 1996; R€ unk & Zobel (2007) have compared growth and survival of
Givnish, Montgomery & Goldstein 2004; Chen et al. 2011) a few European species as a function of edaphic conditions
might break down in ferns, with plastid motion affecting and light availability, but no rigorous study of photosyn-
Amax strongly and k and R more weakly, if at all. Alterna- thetic adaptations to light regime has been undertaken for
tively, the low leaf hydraulic conductance of ferns may the North American group, despite their strikingly different
make differential modulation of hydraulic traits a greater habitats and leaf morphologies.
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 28, 108–123
110 E. B. Sessa & T. J. Givnish
(j) (k)
Table 1. North American allopolyploid Dryopteris species and In this paper, we present gas exchange data from field
their putative progenitors, with ploidy indicated. The ploidy of the studies and tests for correlated evolution of several mor-
extinct progenitor “D. semicristata” is unknown, but it is hypothe-
sized to have been diploid (Montgomery & Wagner 1993)
phological and physiological traits with light regime, which
we predict based on the following three hypotheses:
Allopolyploid Putative parents 1. Species from brighter environments should have nar-
rower, more steeply inclined leaves, lower SLA
D. campyloptera (49) D. expansa (29), D. intermedia (29)
(cm2 g1) and higher maximum photosynthetic rates
D. carthusiana (49) D. intermedia (29), “D. semicristata”
(29) (Amax, lmol CO2 m2 per s), light compensation points
D. celsa (49) D. goldiana (29), D. ludoviciana [the instantaneous light compensation point, ICP and
(29) the leaf compensation point, LCP, the latter incorporat-
D. clintoniana (69) D. cristata (49), D. goldiana (29) ing night-time respiration and leaf construction costs,
D. cristata (49) D. ludoviciana (29), “D. semicristata”
both measured in photon flux density (PFD, lmol pho-
(29)
tons m2 per s)], dark respiration rates (R, lmol
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 28, 108–123
Leaf form and photosynthesis in Dryopteris 111
CO2 m2 per s), maximum stomatal conductances (gs, Goldstein 2004). In C3 plants, stomatal conductance (gs) –
mol H2O m2 per s) and stomatal densities (per mm2) determined by stomatal size, depth and density per unit
compared to species from shadier environments area (Franks & Beerling 2009b; Franks, Drake & Beerling
(Bj€
orkman, Ludlow & Morrow 1972; Bj€ orkman 1981; 2009; Taylor et al. 2012) – is expected to be greater in
Givnish 1988; Givnish, Montgomery & Goldstein 2004); brighter, moister and/or more fertile microsites (Givnish &
2. Species should show adaptive crossover in net carbon Vermeij 1976; Cowan & Farquhar 1977; Wong, Cowan &
uptake per unit leaf mass as a function of PFD, with Farquhar 1979; Farquhar & Sharkey 1982; Givnish 1986;
sun-associated species outperforming others at high Franks & Beerling 2009a; Taylor et al. 2012) in order to
PFDs and shade-associated species outperforming oth- maximize photosynthetic rate at a given rate or cost of
ers at lower PFDs (Bj€
orkman, Ludlow & Morrow 1972; water loss, and lower in drier microsites in order to protect
Givnish 1988, 1995; Givnish, Montgomery & Goldstein the hydraulic pathway leading from the roots to the leaves
2004); and from cavitation (Brodribb & Holbrook 2004, 2006). Across
3. Allopolyploid species should exhibit physiological, C3 plants, stomatal density and individual size are nega-
morphological or ecological traits that fall outside the tively correlated, and high stomatal conductance is posi-
range of variation exhibited by their parental taxa [i.e. tively correlated with stomatal density and photosynthetic
they should be transgressive relative to their progenitors capacity (Franks & Beerling 2009a,b; Franks, Drake &
(Rieseberg, Archer & Wayne 1999)], and doing so may Beerling 2009; Taylor et al. 2012). In general, we might
enable them to coexist regionally with those progenitors expect photosynthesis per unit leaf mass to be higher in
in the long term. species native to sunnier microsites in comparisons made
at higher PFDs, and higher in species from shadier
The rationale for these predictions is as follows: in microsites in comparisons made at lower PFDs (Bj€ orkman,
brightly lit sites with high heat loads and/or vapour pres- Ludlow & Morrow 1972; Givnish 1988, 1995; Givnish,
sure deficits, plants must balance increased rates of photo- Montgomery & Goldstein 2004).
synthetic carbon gain due to increased light and For hybrid allopolyploid taxa, it is possible that the
temperature with greater water loss and low leaf water expression of certain morphological, physiological or eco-
potentials, which can lead to desiccation. Narrower leaves logical traits extends significantly beyond that seen in one
are expected in such environments in order to maintain or both parents. Successful polyploids are often those that
high rates of photosynthesis while reducing water loss and inhabit an ecological niche different from either parent
high leaf temperatures (Givnish & Vermeij 1976; Givnish (Schwarzbach, Donovan & Rieseberg 2001; Maherali,
1979), as are more steeply inclined leaves, which reduce Walden & Husband 2009), or that display phenotypic traits
heat load and transpiration by decreasing the angle of inci- which are outside the range exhibited by the parents [i.e.
dent radiation on the leaf (Givnish 1979). For deeply transgressive character expression (Rieseberg et al. 2003)],
divided foliage, however, such as most Dryopteris share, especially if their distributions overlap. The conspicuous
the main effect of shorter, narrower fronds may be to success of allopolyploid taxa in the Dryopteris complex,
reduce the drop in local leaf water potential across the several of which occupy ranges that are transgressive rela-
length and breadth of the frond, favouring narrow, short tive to one or both parents (Sessa, Zimmer & Givnish
fronds in sunny microsites with high evaporative loads, 2012b), may be due to such transgressive expression, which
and broader, taller fronds in shadier microsites. Greater would have allowed them to avoid minority cytotype exclu-
stature should also increase competitive ability, especially sion following polyploidization (Abbott & Lowe 2004;
in sites with dense coverage by competitors (Givnish 1982, Quintanilla & Escudero 2006; Jimenez et al. 2009).
1995). SLA is a measure of leaf area per unit dry mass; Here we present data on native light regime, leaf form
thicker leaves or leaves with denser tissue have more dry and photosynthetic light response from field studies of 11
biomass per unit area and thus lower levels of SLA (Evans Dryopteris species in eastern North America. These data
& Poorter 2001; Wright et al. 2004; Shipley et al. 2005). allow us to test the hypotheses described above, in order
SLA is positively correlated with high photosynthetic rates to determine whether leaf traits and photosynthetic param-
per unit leaf mass and high rates of whole-plant growth eters show the expected patterns of correlated evolution
(Shipley 1995; Kruger & Volin 2006; Shipley et al. 2006) with photosynthetic light availability in these species’
and is expected to decline with increasing light and native habitats.
decreasing moisture availability (Givnish 1978, 1988; Ack-
erly et al. 2002). According to classical economic theory
(Bj€
orkman 1981; Givnish 1988), maximum photosynthetic Materials and methods
rates (Amax) are expected to be higher in species from
brighter environments, as are dark respiration rates (R), SPECIES, STUDY SITES AND LIGHT REGIMES
the amount of light required to half-saturate photosynthe-
For 10 species of eastern North American Dryopteris – D. campy-
sis (k) and the amount of light needed to balance leaf loptera*, D. carthusiana*, D. celsa*, D. clintoniana*, D. cristata*,
respiration on an instantaneous basis (ICP, instantaneous D. expansa, D. fragrans, D. goldiana, D. ludoviciana, and D. mar-
light compensation point; Givnish, Montgomery & ginalis – we located one field population and measured 5–10 plants
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 28, 108–123
112 E. B. Sessa & T. J. Givnish
D. campyloptera Bear Pen Gap, Blue Ridge Parkway, North Carolina 35°19′16″N, 82°53′25″W
D. carthusiana Huron Mountains, Big Bay, Michigan 46°53′22″N, 87°53′56″W
D. celsa Private property, Hertford, North Carolina 36°13′46″N, 76°33′53″W
D. clintoniana Thurber Preserve, Dryden, New York 42°33′17″N, 76°″W
D. cristata Huron Mountains, Big Bay, Michigan 46°53′22″N, 87°53′56″W
D. expansa Chequamegon-Nicolet National Forest, Wisconsin 46°17′46″N, 90°49′40″W
D. fragrans Huron Mountains, Big Bay, Michigan 46°53′08″N, 87°54′22″W
D. goldiana Fernwood Gardens, Niles, Michigan 41°51′55″N, 86°20′52″W
D. intermedia Huron Mountains, Big Bay, Michigan 46°53′22″N, 87°53′56″W
D. ludoviciana Rocky Hock Swamp Preserve, Hertford, North Carolina 36°11′19″N, 76°40′37″W
D. marginalis Private property, Madison, New York 42°52′07″N, 75°30′57″W
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 28, 108–123
Leaf form and photosynthesis in Dryopteris 113
ships, which we derived from the multilabelled phylogeny pro- from 129 14% for D. goldiana to 356 19% for
duced by Sessa, Zimmer & Givnish (2012b) based on the biparen- D. clintoniana (Table 3). Of the 13 traits measured, most
tally inherited nuclear marker gapCp (Fig. 2). In order to
were positively correlated with canopy transmittance
standardize branch lengths, we added a small value (00001) to
edges with negligible (≤000000001) branch lengths, so that across species in nonphylogenetically corrected analyses,
unequal weight would not be given to contrasts involving shorter but the correlation was significant only for Amax
branches (Garland, Harvey & Ives 1992). Tetraploid and hexa- (r = 052*) with gs (r = 058*; Fig. 4, Table 4). Several
ploid taxa possess two and three copies, respectively, of nuclear other traits were significantly correlated with each other,
loci due to whole-genome duplication and are thus represented by
including Amax with k (r = 081**), frond narrowness
multiple tips on the gapCp tree. If left uncorrected, this multila-
belled nature would lead to each tetraploid taxon being inter- (r = 069*) with gs (r = 094***); Rmass with Amax, mass
preted as two separate species and each hexaploid as three (r = 044*); R and Rmass with each other (r = 088***) and
separate species during calculation of contrasts. To avoid this, we each with ICP (R, r = 089***; Rmass r = 074**) with LCP
used a novel repetitive process to perform contrast analyses, con- (R, r = 083**; Rmass r = 072*); SLA with Amax, mass
sidering each possible combination of polyploid positions on the
(r = 072**), Rmass (r = 066*), frond narrowness
tree. In the first step, tips were dropped from the tree at random
such that polyploids were represented by only one tip each (r = 072**), gs (r = 054*) with average stomatal den-
(Fig. 3). Contrasts were then calculated for per cent canopy open- sity (r = 076**); ICP with LCP (r = 098***); plant nar-
ness and each of the dependent trait variables using this random rowness with leaf tip angle (r = 064*); and gs and k each
tree, and a standard linear regression carried out on the contrasts with frond narrowness (gs, r = 075**; k, r = 066*), and
and forced through the origin (Garland, Harvey & Ives 1992).
with each other (r = 086***; Table 4). There was no evi-
P-values were stored at each step and the process repeated 10 000
times to ensure that all possible binary tree topologies (48) were dence of adaptive crossover in static light response curves
sampled in the contrast analyses. We produced histograms of on either a mass or area basis; species from the brightest
P-values for contrasts of each trait against contrasts of per cent environments consistently outperformed species from the
canopy openness in order to assess the frequency of regression shadiest environments (Fig. 5). Average SLA did not differ
analyses that produced significant vs. nonsignificant results. Val-
significantly between polyploid (382 39 cm2 per g) and
ues of the correlation coefficient (r) for each of the 10 000 repeti-
tions were also recorded, in order to determine the percentage of diploid (298 49 cm2 per g) taxa (P = 023).
correlations for each set of contrasts that were positive or negative. In the phylogenetically structured analyses, we found
Finally, we performed a one-tailed t-test to determine a significant correlation (P ≤ 005) between trait and
whether SLA differed significantly between polyploid and diploid canopy transmittance contrasts in a majority of the
species.
10 000 regression analyses on binary trees for Amax
(58% with P ≤ 005), SLA (61% with P ≤ 005) and k
(61% with P ≤ 005; Table 5, Appendix S1 in Support-
Results
ing Information). Contrasts for each of the other 10
In the field, Dryopteris occupies a range of light regimes, traits were not significantly correlated with per cent can-
with canopy transmittance varying 28-fold across species, opy transmittance contrasts for a majority of repetitions.
D. cristata B
D. clintoniana A
D. celsa B
D. ludoviciana
D. celsa A
D. goldiana
D. clintoniana B
D. expansa
D. campyloptera B
D. carthusiana A
Fig. 2. Initial phylogenetic tree used in the
phylogenetically independent contrast D. campyloptera A
(PIC) analyses, based on a maximum likeli-
D. intermedia
hood topology from Sessa, Zimmer &
Givnish (2012a). A, B, C following taxon D. carthusiana B
names denote multiple genomes present in
D. cristata A
polyploid species. Tips were dropped ran-
domly in the regression analyses so that D. clintoniana C
each polyploid was represented by only one
tip at a time (see Fig. 3). Branches are pro- D. marginalis
portional to expected number of nucleotide D. fragrans
substitutions per site. Bar indicates 001
changes. 0·01
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 28, 108–123
114 E. B. Sessa & T. J. Givnish
D. ludoviciana
D. celsa A
D. goldiana
D. clintoniana B
D. expansa
D. campyloptera B
D. carthusiana A
D. intermedia
Fig. 3. One random binary tree (out of 48
D. cristata A possible trees) used in the phylogenetically
D. marginalis independent contrast (PIC) calculations for
D. fragrans the field studies. Branches are proportional
to expected number of nucleotide substitu-
0·01 tions per site. Bar indicates 001 changes.
Table 3. Environmental, morphological, photosynthetic and functional traits measured in the field. Means standard errors are given.
No stomatal density data were collected for D. fragrans due to density of abaxial trichomes
D. campyloptera 280 13 400 04 030 004 294 48 235 05 43 093 190 27
D. carthusiana 205 20 527 05 033 009 444 58 266 055 49 110 223 21
D. celsa 249 34 245 03 045 024 278 38 763 506 2208 1726 84 6
D. clintoniana 356 19 669 05 046 005 413 38 312 043 569 082 160 14
D. cristata 253 12 596 03 039 005 499 43 348 051 634 097 259 15
D. expansa 174 14 411 04 103 023 298 46 1012 273 2575 847 202 16
D. fragrans 292 25 713 04 047 006 643 63 441 06 799 11 115 31
D. goldiana 129 14 353 04 032 007 284 43 296 079 57 172 123 15
D. intermedia 212 16 494 02 067 011 464 30 830 186 1843 489 155 11
D. ludoviciana 229 27 486 03 044 007 324 29 311 033 577 07 100 7
D. marginalis 326 14 499 02 016 002 283 18 094 011 166 02 126 5
D. campyloptera 141 26 452 18 327 18 062 006 201 003 876 10 006 001
D. carthusiana 146 41 433 33 273 13 081 003 271 004 650 17 007 001
D. celsa 132 51 341 23 369 20 098 006 325 007 623 38 003 00
D. clintoniana 113 17 246 14 398 14 127 011 401 008 450 41 01 001
D. cristata 172 23 439 15 349 18 120 008 430 009 553 22 009 001
D. expansa 515 116 497 27 347 19 091 006 223 004 560 22 004 001
D. fragrans 73 18 155 35 – 064 005 477 010 852 36 014 001
D. goldiana 114 27 356 17 282 14 077 003 272 005 700 29 004 00
D. intermedia 182 22 316 20 442 17 076 003 303 003 638 12 006 00
D. ludoviciana 89 13 211 6 521 29 129 018 399 010 749 35 007 00
D. marginalis 40 04 256 12 544 38 065 004 333 003 720 19 007 001
ICP, instantaneous compensation point; LCP, leaf compensation point; SLA, specific leaf area.
For all traits, regressions on binary trees produced both contrasts, while the unstructured analysis produced a
positive and negative correlations between trait contrasts positive correlation (Tables 4, 5).
and native per cent canopy transmittance contrasts
(Table 5). For most traits, the direction of the correla-
Discussion
tion (either positive or negative) for the majority of rep-
etitions was the same as in the phylogenetically
CORRELATED EVOLUTION OF PHOTOSYNTHETIC
unstructured analyses. For three traits – Amax, LCP and
PARAMETERS AND LEAF TRAITS WITH LIGHT REGIME
ICP – exactly half of the correlations were positive and
half negative, and for one trait – k – the majority of Our field measurements indicate that trends in photosyn-
repetitions in the phylogenetically structured analyses thetic, morphological and ecological traits in eastern
produced negative correlations with light availability North American Dryopteris generally accord with
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 28, 108–123
Leaf form and photosynthesis in Dryopteris 115
(a) (b)
D. campyloptera
1·2
D. carthusiana
7
D. celsa
D. clintoniana
D. cristata
1·0
Amax (µmol CO2 m−2 s−1)
6 D. expansa
D. fragrans
0·8
D. ludoviciana
5
D. marginalis
0·6
4
0·4
3
0·2
2
10 15 20 25 30 35 40 10 15 20 25 30 35 40
% Canopy transmittance % Canopy transmittance
(c) (d)
70
12
60
10
ICP (µmol m−2 s−1)
k (µmol m−2 s−1)
8
50
6
40
4
30
10 15 20 25 30 35 40 10 15 20 25 30 35 40
% Canopy transmittance % Canopy transmittance
(e) (f)
40
250
Amax mass (nmol CO2 g−2 s−1)
30
LCP (µmol m−2 s−1)
200
20
150
10
100
0
10 15 20 25 30 35 40 10 15 20 25 30 35 40
% Canopy transmittance % Canopy transmittance
Fig. 4. Field measurements of gas exchange, morphological and functional traits plotted against per cent canopy transmittance. Species
means SE are shown, and standard linear regression lines are plotted for those traits that were significantly correlated with per cent can-
opy transmittance. (a) Amax; (b) R; (c) k; (d) ICP; (e) LCP; (f) Amax, mass (g) Rmass; (h) specific leaf area (SLA); (i) average stomatal density;
(j) plant narrowness; (k) frond narrowness; (l) leaf tip angle; (m) gs. Data points are coloured by species according to the legend in (a);
polyploids are shown as squares, diploids circles (For interpretation of the references to colour in this figure legend, the reader is referred
to the online version of this article.). ICP, instantaneous compensation point; LCP, leaf compensation point.
theoretical predictions based on classical economic theory longer than broad; Fig. 4). We did not find significant
(Bj€
orkman, Ludlow & Morrow 1972; Bj€ orkman 1981; statistical support for most of these results, however, as
Givnish 1988; Givnish, Montgomery & Goldstein 2004). only Amax and gs are significantly correlated with light
Species from sunnier habitats tend to have higher photo- availability in the phylogenetically unstructured analyses,
synthetic and stomatal conductance rates per unit area, the remaining correlations being in the expected direc-
require more light to saturate photosynthesis, have lower tions but not achieving statistical significance at the 5%
SLAs, higher stomatal densities and increased frond nar- level (Table 4). In the phylogenetically structured analy-
rowness (the latter indicating that leaves were generally ses, Amax is again significantly correlated with per cent
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 28, 108–123
116 E. B. Sessa & T. J. Givnish
(g) (h)
500
60
50
Rmass (nmol g−2 s−1)
400
SLA (cm2 g−1)
40
300
30
20
200
10
10 15 20 25 30 35 40 10 15 20 25 30 35 40
% Canopy transmittance % Canopy transmittance
(i) (j)
1·4
Average number of stomata mm−2
55
1·2
45
1·0
40
0·8
35
0·6
30
10 15 20 25 30 35 40 10 15 20 25 30 35 40
% Canopy transmittance % Canopy transmittance
(k)
5·0
(l)
90
Frond narrowness (length:width)
4·5
80
4·0
60
3·0
50
2·5
40
2·0
10 15 20 25 30 35 40 10 15 20 25 30 35 40
% Canopy transmittance % Canopy transmittance
(m)
0·14
0·12
gs (mol m−2 s−1)
0·10
0·08
0·06
0·04
10 15 20 25 30 35 40
% Canopy transmittance
Fig. 4. Continued.
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 28, 108–123
Leaf form and photosynthesis in Dryopteris 117
Average
stomatal Plant Frond Leaf tip
Amax R k ICP LCP Amax, mass Rmass SLA density narrowness narrowness angle gs
Canopy 052 037 022 040 038 009 046 047 048 010 047 001 058
Amax – 007 081 032 044 027 024 046 022 015 069 008 094
R – – 006 089 083 016 088 028 009 017 018 038 014
k – – – 000 013 024 018 034 013 003 066 004 086
ICP – – – – 098 002 074 027 012 004 022 033 031
LCP – – – – – 008 072 030 011 004 028 034 041
Amax, mass – – – – – – 044 072 049 009 021 033 011
Rmass – – – – – – – 066 032 007 047 038 035
SLA – – – – – – – – 076 008 072 024 054
Average – – – – – – – – – 017 047 010 019
stomatal
density
Plant – – – – – – – – – – 043 064 003
narrowness
Frond – – – – – – – – – – – 008 075
narrowness
Leaf tip – – – – – – – – – – – – 008
angle
gs – – – – – – – – – – – – –
ICP, instantaneous compensation point; LCP, leaf compensation point; SLA, specific leaf area.
See text and Table 3 for data and units. Significant correlations (P ≤ 005) are shown in bold.
canopy transmittance in a majority of analyses, as are eqn (1) (Farquhar & Sharkey 1982): when maximum pho-
SLA and k. Amax is thus the only trait to be strongly tosynthetic rate increases, so too should the PFD required
correlated with light availability in both the phylogeneti- to half-saturate photosynthesis. R and Rmass are also both
cally structured and unstructured analyses. Our measures strongly positively correlated with ICP and LCP, and the
of plant stature (plant narrowness and leaf tip angle) PFDs at which carbon consumed by respiration and pro-
show very little or no correlation with PFD (Fig. 4, duced by photosynthesis are balanced. As respiration
Table 4). increases (i.e. more carbon is lost to respiration), the
The values of Amax and other photosynthetic parameters amount of light required to balance carbon consumption
that we report here for Dryopteris are similar to those that must increase. ICPs and LCPs range from 001% to 02%
have been found in ferns previously. Amax in our species full sunlight and are each well below the PFDs necessary
ranged from 25 03 to 71 04 lmol CO2 m2 per s, to partly saturate photosynthesis. Both are negatively cor-
which corresponds roughly to the middle of the range of related with PFD, which is contrary to expectations, as the
Amax values that have been reported for other fern genera amount of light required to balance respiration should
(Ludlow & Wolf 1975; Nobel, Calkin & Gibson 1984; increase with daily PFD to which a species is adapted
Hollinger 1987; Brodribb, Feild & Jordan 2007). Previous (Givnish, Montgomery & Goldstein 2004).
estimates for Dryopteris range from 18 lmol CO2 m2 Several photosynthetic parameters show greater integra-
per s in Asian D. crassirhizoma (Maeda, 1970) to 40 lmol tion with each other and with other traits when considered
CO2 m2 per s in D. arguta (Pittermann et al. 2011) and on a mass rather than an area basis (Table 4), although
90 lmol CO2 m2 per s in D. filix-mas (Bauer, Gallmetzer only area-based Amax is significantly correlated with native
& Sato 1991). Previous researchers have reported instanta- PFD. Because competition should favour plants that
neous light compensation points in ferns infrequently, but maximize returns on energy investment (Givnish 1988,
our values (Table 3) are somewhat higher than those docu- 1995), and mass-based estimates incorporate energy invest-
mented previously for Dryopteris [which ranged from ment in leaf construction, photosynthesis on a mass basis
05 lmol m2 per s in the shade to 17 lmol m2 per s in should be more closely tied to relative performance and
the sun (Bannister & Wildish 1982)], and are more similar competition between species than photosynthesis on an
to values reported by Hollinger (1987) for two understorey area basis. It is therefore surprising that Amax but not
species of Blechnum and Pteridium (73 and 116 lmol m2 Amax, mass is significantly correlated with native PFD; in
per s, respectively). fact, Amax, mass shows almost no relationship to native
In addition to the relationships with PFD, several traits PFD (Fig. 4f). However, ferns are known to respond con-
are also correlated with each other as expected based on servatively to desiccation (Brodribb & Holbrook 2004),
theoretical predictions. Amax is significantly positively cor- and this sensitivity is driven at least in part by low rates of
related with k, as expected based on the Michaelis–Menten area-based leaf hydraulic conductance (Woodhouse &
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 28, 108–123
118 E. B. Sessa & T. J. Givnish
Amax 58 50
R 45 42
k 61 33
ICP 17 50
LCP 17 50
Amax, mass 49 33
Rmass 39 25
SLA 61 8
Average stomatal density 34 81
Plant narrowness 42 55
Frond narrowness 39 59
Leaf tip angle 42 33
gs 42 83
(b)
ICP, instantaneous compensation point; LCP, leaf compensation
point; SLA, specific leaf area.
Percentages indicate the frequency of binary trees (out of 48 possi-
ble topologies) for which P-values were below 005 and r was posi-
tive.
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 28, 108–123
Leaf form and photosynthesis in Dryopteris 119
canopy openness varying only 28-fold across species. A for our general observation of expected but nonsignificant
narrow range of PFD decreases by itself the likelihood of correlations between traits and PFD, and for the lack of
significant relationships of individual traits to PFD across expected pairwise performance comparisons at the species
species, even if such relationships can be seen for species level between taxa from sun and shade environments. It is
inhabiting a broader gradient. We note that many of the important to recognize that several traits expected to show
expected positive relationships among plant traits and positive relationships to PFD based on classic economic
PFD were observed but were simply not significant; per- theory (i.e. based solely on the putative effects of PFD)
haps a greater number of species, or occupancy of a might also show such relationships based on hydraulic
broader range of light regimes, might have made these considerations. As we suggested in the Introduction, a
patterns significant. greater sensitivity of plastid movement to PFD in ferns
Finally, and perhaps most importantly, many of the might preserve a positive relationship of Amax to PFD
traits we examined are likely influenced not just by light while reducing or eliminating that of k and R, by reducing
availability but by the correlation of PFD with tempera- self-shading and maintaining a constant plastid mass.
ture, vapour pressure deficit, wind speed and other envi- Thicker leaves or leaves with higher mass per unit area
ronmental variables. Several previous studies on ferns have may be an adaptation to greater evaporative demand in
documented one or more of the expected relationships brighter sites, reducing leaf and evaporative surfaces in
among photosynthetic parameters that we see in Dryopter- order to reduce tissue desiccation and preserve xylem func-
is. In a study of three species from different genera (Adian- tion (Creese, Lee & Sack 2011). Our gs values were signifi-
tum, Thelypteris and Woodwardia) growing in different cantly correlated with PFD (Table 4), but this correlation
light regimes, Hill (1972) found that species from sunnier could also have been driven by differences in water avail-
habitats had higher maximum photosynthetic rates, light ability between the sites, if brighter habitats happened also
compensation points and light saturation points compared to be drier. Conductance in several fern species has been
with species from a shadier habitat. Lower compensation reported to be more strongly influenced by soil water sta-
points and SLAs in species from shady habitats have been tus than by other variables (Nobel 1978; Hollinger 1987),
documented in single species from several fern genera and several recent studies have revealed that fern stomata
(Ludlow & Wolf 1975; Bannister & Wildish 1982; Brach, lack many of the active control mechanisms found in an-
McNaughton & Raynal 1993), as have higher stomatal giosperms (Doi, Wada & Shimazaki 2006; Doi & Shima-
densities (Ludlow & Wolf 1975) in species from sunny zaki 2008; Brodribb et al. 2009; Brodribb & McAdam
habitats. Higher photosynthetic capacity with increasing 2011), instead opening and closing passively in response to
light availability has also been documented in Blechnum hydraulic changes and leaf water status (Brodribb &
(Salda~na et al. 2009), Adiantum (Yeh & Wang 2000) and McAdam 2011; McAdam & Brodribb 2012). This further
in D. intermedia (Brach, McNaughton & Raynal 1993), suggests that hydraulic constraints, rather than responses
among others. However, in additional studies examining to PFD per se, may be primarily responsible for shaping
fern traits and habitat preference, soil moisture was found morphological and physiological diversity in these ferns.
to be a primary factor influencing fern distributions in Indeed, decreased conductance in brighter environments
Ohio (Greer, Lloyd & McCarthy 1997) and Quebec (Karst, could countervail the general tendency towards higher
Gilbert & Lechowicz 2005), and Nobel, Calkin & Gibson Amax, k and R and lower SLAs in higher-PFD environ-
(1984), in a study of gas exchange in 14 species of ferns in ments.
a greenhouse, found that water vapour and CO2 conduc-
tance were better predictors of maximum photosynthetic
TRANSGRESSIVE TRAIT EXPRESSION IN POLYPLOIDS
rates than was PFD. Reudink et al. (2005) noted that
D. intermedia growing in a damp, but open site appeared The eastern North American Dryopteris complex includes
to experience greater water stress, as indicated by negative five allopolyploids – tetraploids D. carthusiana, D. cristata,
water potential, than other species growing in the same D. campyloptera, D. celsa and hexaploid D. clintoniana –
environment, and concluded that D. intermedia’s ability to the latter three of which have both parental species extant
acclimate to high PFDs was limited, with moisture playing (Sessa, Zimmer & Givnish 2012b). We expected to see evi-
a greater role in determining its distribution. R€ unk, Zobel dence of transgressive expression in these species relative
& Zobel (2010), in a study of three Estonian species of to their parents in at least some of the traits measured.
Dryopteris (including D. carthusiana and D. expansa), Novel or extreme trait expression can allow hybrids to
determined that species’ distributions and abundance were escape competition and the effects of minority cytotype
most influenced either by edaphic factors or by ‘locale exclusion and will tend to favour their establishment and
effects’ that were not specifically related to any one vari- long-term success (Abbott 1992; Rieseberg 1997; Riese-
able. Taken together, these results suggest that fern distri- berg, Archer & Wayne 1999; Buerkle et al. 2000; Rieseberg
butions and adaptation of specific traits are likely shaped et al. 2003; Quintanilla & Escudero 2006). Two recent
by the interaction of a number of environmental factors. studies have also shown that polyploids tend to occupy
That light availability is probably joined in its effects by larger geographic ranges than their progenitor taxa
moisture availability and evaporative demand may account (Parisod, Holderegger & Brochmann 2010; Parisod 2012).
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 28, 108–123
120 E. B. Sessa & T. J. Givnish
This is true of D. campyloptera, D. celsa and D. clintoni- which traits can be compared among species grown within
ana (Sessa, Zimmer & Givnish 2012b) and suggests that in the same PFD and related to the native PFDs of each
some traits they must be transgressive relative to their species in the field (Givnish, Montgomery & Goldstein
parents. Sessa, Zimmer & Givnish (2012b) also found 2004), and ‘hard’ tests, which will allow us to ask whether
that the allotetraploid hybrids have resulted from crosses species showing the highest realized rates of photosynthesis
between diploid parents that display intermediate levels shift with light treatment, and if they are the species
of genetic divergence relative to all possible progenitor that occupy habitats with similar native light regimes. Our
pairs. Such intermediate levels of parental divergence results also indicate that hydraulic demands may have
have been found to be linked to transgressive trait played a key role in the physiological and morphological
expression in hybrid angiosperms (Stelkens & Seehausen evolution of these ferns, supporting results from several
2009). recent studies that have found significant differences
Contrary to our expectations, we found little evidence between ferns and other land plants in traits related to
for transgressive trait expression in any of the three allopo- water balance, including hydraulic conductance, vein
lyploids we examined. In almost all traits, measurements density and the nature of fern stomatal responses
in the polyploids were intermediate relative to their parents (Brodribb & Holbrook 2004; Brodribb, Feild & Jordan
and frequently overlapped significantly with one or both 2007; Boyce et al. 2009; Watkins, Holbrook & Zwieniecki
parents (Fig. 4). SLA was also not significantly different 2010; Brodribb & McAdam 2011; McAdam & Brodribb
between polyploids and diploids. Transgressive expression 2012).
of photosynthetic parameters is therefore evidently not the This study is the first to propose a statistical framework
means by which these allopolyploid taxa are being main- for incorporating phylogeny into comparative analyses
tained. However, the native PFDs of two of the three when the subjects include species with reticulate evolution-
allopolyploids (D. campyloptera and D. clintoniana) were ary histories. Phylogenetic relationships must be consid-
transgressive relative to their parental species (Fig. 4), with ered in comparative analyses due to the danger of inflating
each allopolyploid occupying a much brighter habitat type I error rates when species are erroneously considered
than its parents. Coupled with the transgressive ranges of to be independent samples (Felsenstein 1985). The method
these species relative to their parents, this points to the we present allows for the incorporation of phylogeny even
existence of physiological differences that provided the in the case of hybridization or polyploidy, by accounting
allopolyploid taxa an advantage in geographic range that for all possible sets of relationships (trees) for a given set
apparently allowed them to coexist with their progenitors of taxa. The results of the phylogenetically structured and
at a regional scale. As discussed above, water balance unstructured analyses presented here are largely congruent
mediated by hydraulics is the most likely driving factor. with each other, and this agreement increases our confi-
Although we found no significant difference in SLA dence in the results. However, the distribution of negative
between polyploids and diploids, this does not rule out the and positive r values (Table 5) obtained from repetitive
possibility of an increase in tracheid size due to polyploidy PIC analyses utilizing all possible trees indicates that the
that could affect species’ hydraulic conductance and thus placement of hybrid species in the tree can greatly
their ability to tolerate brighter habitats. Further studies influence the results of such analyses, and speaks to the
of the allopolyploids and their parents, including sampling importance of incorporating phylogeny in comparative
from multiple populations of each in the field, will be studies and considering carefully the placement of reticu-
needed in order to determine the relative roles of light and late taxa. If we had selected only a single tree, for example,
water availability in influencing these species’ evolution. our results for any given trait would have been either
100% positive or negative, when in fact there is a distribu-
tion between negative and positive correlations depending
Conclusions
on which tree is utilized in a given repetition of the analy-
The current study is the first to document physiological sis. Many researchers now incorporate phylogeny into
and morphological traits in a widespread, closely related their comparative studies of ecological and physiological
group of ferns whose phylogeny is well understood, and to traits, and we hope that the method presented here will be
attempt to determine whether photosynthetic PFD has useful in such studies involving hybrid and/or polyploid
been a primary factor driving adaptation in fern leaf form organisms.
and physiology. Although we found little evidence to sup-
port PFD as the main determinant of diversification in the
traits measured, our results suggest several avenues for Acknowledgements
future studies. Common garden studies, in which species The authors thank A. Jandl, T. Goforth, P. Gonsiska, C. Line, J. Perry
are grown together and environmental variables can be and K. Woods for help in the field, and the Finger Lakes Land Trust, Nat-
carefully controlled, will be particularly important, and ure Conservancy of North Carolina, Huron Mountain Club, Blue Ridge
Parkway, Fernwood Botanical Gardens, and J.E. Watkins, Jr. and J. Perry
will allow us to more rigorously examine the extent to for allowing us access to field populations. Many thanks to E. Kruger for
which species may be adapted to their native light regimes. advice on this manuscript, and to C. Ane for assistance with developing the
Such studies will allow both ‘soft’ tests of adaptation, in statistical tools used in this study, particularly for the phylogenetically
© 2013 The Authors. Functional Ecology © 2013 British Ecological Society, Functional Ecology, 28, 108–123
Leaf form and photosynthesis in Dryopteris 121
structured analyses of polyploids. Financial support for this research was Creese, C., Lee, A. & Sack, L. (2011) Drivers of morphological diversity and
provided by the Huron Mountain Wildlife Foundation (EBS, TJG), a mi- distribution in the Hawaiian fern flora: trait associations with size, growth
croMORPH award from the National Science Foundation (EBS), and form, and environment. American Journal of Botany, 98, 956–966.
graduate research awards from the Botanical Society of America, the Doi, M. & Shimazaki, K.-I. (2008) The stomata of the fern Adiantum capil-
American Society of Plant Taxonomists and the Torrey Botanical Society lus-veneris do not respond to CO2 in the dark and open by photosynthe-
(EBS). The authors declare no conflict of interest. sis in guard cells. Plant Physiology, 147, 922–930.
Doi, M., Wada, M. & Shimazaki, K.-I. (2006) The fern Adiantum capillus-
veneris lacks stomatal responses to blue light. Plant and Cell Physiology,
Data Accessibility 47, 748–755.
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dryad.38h06). growth irradiance: the relative importance of specific leaf area and nitro-
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