Leaf Photosynthetic Rate of Tropical Ferns Is Evolutionarily Linked to Water Transport Capacity

<div><p>Ferns usually have relatively lower photosynthetic potential than angiosperms. However, it is unclear whether low photosynthetic potential of ferns is linked to leaf water supply. We hypothesized that there is an evolutionary association of leaf water transport capacity with photosynthesis and stomatal density in ferns. In the present study, a series of functional traits relating to leaf anatomy, hydraulics and physiology were assessed in 19 terrestrial and 11 epiphytic ferns in a common garden, and analyzed by a comparative phylogenetics method. Compared with epiphytic ferns, terrestrial ferns had higher vein density (D_vein), stomatal density (SD), stomatal conductance (g_s), and photosynthetic capacity (A_max), but lower values for lower epidermal thickness (LET) and leaf thickness (LT). Across species, all traits varied significantly, but only stomatal length (SL) showed strong phylogenetic conservatism. A_max was positively correlated with D_vein and g_s with and without phylogenetic corrections. SD correlated positively with A_max, D_vein and g_s, with the correlation between SD and D_vein being significant after phylogenetic correction. Leaf water content showed significant correlations with LET, LT, and mesophyll thickness. Our results provide evidence that A_max of the studied ferns is linked to leaf water transport capacity, and there was an evolutionary association between water supply and demand in ferns. These findings add new insights into the evolutionary correlations among traits involving carbon and water economy in ferns.</p></div

Pearson correlations (a–d) and phylogenetically independent contrast correlations (e–h) of leaf water content (LWC) with cuticle thickness (CT), lower epidermal thickness (LET), leaf thickness (LT), and mesophyll thickness (MT) across 30 fern species.

<p>Pearson correlations (a–d) and phylogenetically independent contrast correlations (e–h) of leaf water content (LWC) with cuticle thickness (CT), lower epidermal thickness (LET), leaf thickness (LT), and mesophyll thickness (MT) across 30 fern species.</p

Phylogenetic signals (<i>K</i>-statistics) for 14 leaf functional traits from 30 fern species.

<p><i>K</i> value <1 indicates that relatives resemble each other less than expected under Brownian motion evolution along the phylogenetic tree; <i>K</i> value >1 shows that close relatives are more similar than expected.</p

Pearson correlations (a–b) and phylogenetically independent contrast correlations (c–d) of maximum photosynthetic rate (A_max) with stomatal conductance (g_s) and leaf water content (LWC) across 30 fern species.

<p>Pearson correlations (a–b) and phylogenetically independent contrast correlations (c–d) of maximum photosynthetic rate (A_max) with stomatal conductance (g_s) and leaf water content (LWC) across 30 fern species.</p

Leaf traits examined in this study.

<p>Leaf traits examined in this study.</p

Pearson correlations (a–c) and phylogenetically independent contrast correlations (d–f) of maximum photosynthetic rate (A_max) with vein density (D_vein), stomatal density (SD), and leaf mass per unit area (LMA) across 30 fern species.

<p>Pearson correlations (a–c) and phylogenetically independent contrast correlations (d–f) of maximum photosynthetic rate (A_max) with vein density (D_vein), stomatal density (SD), and leaf mass per unit area (LMA) across 30 fern species.</p

Differences in 16 leaf traits between terrestrial and epiphytic ferns.

<p>See <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0084682#pone-0084682-t001" target="_blank">Table 1</a> for trait units. The statistical differences for each trait were determined with independent-samples <i>t</i>-test. The sign of the significance is indicated as: ns, <i>p</i>>0.05; *, <i>p</i><0.05; **, <i>p</i><0.01; ***, <i>p</i><0.001.</p

Phylogeny with labeled nodes used for comparative analysis of trait variation among 30 fern species along with trait values (mean ± 1 SE) for maximum photosynthetic rate (A_max; a), vein density (D_vein; b), stomatal density (SD; c), and stomatal length (SL; d).

<p>Phylogeny with labeled nodes used for comparative analysis of trait variation among 30 fern species along with trait values (mean ± 1 SE) for maximum photosynthetic rate (A_max; a), vein density (D_vein; b), stomatal density (SD; c), and stomatal length (SL; d).</p

Pearson correlations (a–c) and phylogenetically independent contrast correlations (d–f) of stomatal density (SD) with stomatal conductance (g_s), vein density (D_vein) and cuticle thickness (CT) across 30 fern species.

<p>Pearson correlations (a–c) and phylogenetically independent contrast correlations (d–f) of stomatal density (SD) with stomatal conductance (g_s), vein density (D_vein) and cuticle thickness (CT) across 30 fern species.</p

Differences in stomatal traits and leaf thickness of <i>Paphiopedilum</i> due to growth habit.

<p>SD, stomatal density; VD, vein density; SL, stomatal length; and LT, leaf thickness. Different letters above bars for each component indicate statistically different mean values (<i>p</i>≤0.05), as determined by LSD multiple comparison tests.</p