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(American Journal of Botany. 2008;95:1366-1374.) doi: 10.3732/ajb.0800019 © 2008 Botanical Society of America, Inc.

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Do bryophyte shoot systems function like vascular plant leaves or canopies? Functional trait relationships in Sphagnum mosses (Sphagnaceae)¹

³ Department of Biological Sciences, Union College, Schenectady, New York 12308 USA ⁴ Department of Biology, University of New Mexico, Albuquerque, New Mexico 87131 USA

Received for publication 16 January 2008. Accepted for publication 11 September 2008.

ABSTRACT

Vascular plant leaf traits that influence photosynthetic function form the basis of mechanistic models of carbon exchange. Given their unique tissue organization, bryophytes may not express similar patterns. We investigated relationships among tissue, shoot, and canopy traits, and their associations with photosynthetic characteristics in 10 Sphagnum species. Trait relationships were organized around a primary dimension accounting for 43% of variation in 12 traits. There was no significant relationship between nitrogen content of shoot systems and maximum photosynthesis expressed on mass (A_mass) or area (A_area) bases due to nitrogen sequestration and storage within the canopy interior. This pattern differs from the distribution of nitrogen in vascular plant canopies. Thus, nitrogen and its relationship to carbon uptake in Sphagnum shoots does not conform to patterns of either vascular plant leaves or canopies. Species that concentrate biomass and nitrogen in the capitulum have enhanced rates of A_mass and A_area. Consequently, A_area was positively associated with N_area of the capitulum only. Overall, water content and carotenoid concentration were the strongest predictors of both A_mass and A_area and these were expressed as inverse relationships. The relationships of plant traits in Sphagnum defines a principal trade-off between species that tolerate environmental stress and those that maximize carbon assimilation.

Key Words: bryophyte • carbon isotope fractionation • carotenoid • nitrogen concentration • peatmoss • photoinhibition • plant functional type

Species in the bryophyte genus Sphagnum are among the world’s most important ecosystem engineers because they dominate northern peatland ecosystems that cover 3.5 x 10⁶ ha and store 455 Pg of carbon, about one-third of the world’s soil carbon (Gorham, 1991). In these systems, Sphagnum species control hydrology, nutrient cycling, carbon sequestration, and successional dynamics (O’Neill, 2000; Vitt, 2000; Turetsky, 2003; Rydin and Jeglum, 2006). Consequently, sphagna from peatland systems in North America and Europe have been the focus of substantial physiological investigations (reviewed in Rydin and Jeglum, 2006). However, these studies have concentrated on a narrow suite of species within boreal and arctic ecosystems and the breadth of functional variation within the genus remains understudied. Species of Sphagnum occupy diverse habitats and differ in their allocation to photosynthetic chemistry, cell, and tissue composition and in their morphology and canopy structure in ways that influence their physiological function (Johansson and Linder, 1980; Proctor, 1980; Hayward and Clymo, 1983; Titus and Wagner, 1984; Rice, 1995, Rice, 2000; Rice and Schuepp, 1995). Comparative studies within Sphagnum present an opportunity to understand the form of plant trait relationships that can provide the basis of functional models of carbon exchange in peatland ecosystems.

In vascular plants, the recognition and circumscription of "functional types" for discrete qualities and "functional spectra" for continuous variables has led to the development of general models of vascular plant performance and distribution that not only have explanatory, but also predictive power (Grime et al., 1997; Smith et al., 1997; Hodgson et al., 1999; Diaz et al., 2001; Reich et al. 2003; Wright et al., 2004b; Shipley et al., 2006). For example, photosynthetic metabolism demands over 50% of leaf nitrogen (Evans, 1983; Field and Mooney, 1983; Evans and Seemann, 1989). Consequently, leaf nitrogen expressed on mass concentration (N_mass) or area (N_area) bases is highly correlated with maximum rates of photosynthetic assimilation (expressed by mass, A_mass, or area, A_area) in vascular plant leaves (Hikosaka, 2004; Wright et al., 2004a, 2004b). In global and regional analyses, functional leaf traits vary continuously and range from those optimized for rapid, yet metabolically expensive, short-term carbon gain (e.g., high rates of carbon assimilation, high nitrogen concentrations, low investment in structural compounds, low leaf mass per area, short leaf life span) to ones adapted for prolonged, yet slow carbon uptake.

Although bryophyte shoot systems (group of individuals with a continuous canopy) are considered analogous to vascular plant leaves (Proctor, 1981, 2000), they differ dramatically in the relative role of boundary-layer conductance and external water films as limits to carbon uptake, in the specialization of leaf cells that enhance water storage (e.g., hyaline cells) or ion exchange, in the magnitude of respiratory carbon loss, and in the vertical distribution of photosynthesis, which can span up to two orders of magnitude thicker than vascular plant leaves (Sveinbjörnsson and Oechel, 1992; Proctor, 2000; Rydin and Jeglum, 2006). These qualities may influence the partitioning of plant nitrogen, affect photosynthetic characteristics, and alter the relationships among functional plant traits when compared with vascular plant leaves. Alternatively, bryophyte shoot systems may function more like vascular plant canopies, where the distribution of leaf nitrogen parallels the light gradient within the canopy (Kull and Niinemets, 1998; Hikosaka, 2004). Under these conditions, leaf nitrogen and light availability can colimit carbon uptake at each layer in the canopy, which may optimize whole canopy photosynthesis relative to nitrogen. It is not known whether plant traits in bryophytes function similarly to vascular plant leaves, canopies, or if they represent a unique functional type (Cornelissen et al., 2007).

To understand the dimensions of plant trait variation and their relationships to photosynthetic performance in Sphagnum mosses, we evaluated tissue, shoot, canopy, and photosynthetic traits in 10 species representing diverse taxonomic, geographic, and ecological groups. The objectives of this study were to assess the correlation structure among tissue, shoot, and canopy traits and to evaluate how these attributes relate to photosynthetic performance (A_mass, A_area).

MATERIALS AND METHODS

Study taxa and culture conditions
Ten species of Sphagnum were chosen for study, two from each of five monophyletic sections within the genus (Shaw et al., 2003). Within sections, taxa were chosen that occupy different habitats and/or distinct geographic ranges. Approximately 0.25 m² of each species was collected from sites in the North Carolina Coastal Plain and in New York State (nomenclature follows Anderson, 1990). Brown material, determined visually, was removed from the stem base, and samples were returned to Union College for common garden and laboratory studies.

Plants were grown hydroponically in 21 cm diameter, 7.5 cm high cylindrical containers with white vinyl walls, and a 1 x 1 cm plastic mesh bottom. Plants were trimmed to 3 cm and arranged at natural densities (measured in the field) in the mesh with the capitula resting on the container base. Containers were placed on the tops of buckets of the same diameter so that the stems dangled into the bucket and surplus water drained from the plants. Three replicates from each species were prepared. Containers were randomly placed on a bench surrounded by clear plastic sheeting and covered with 40% shade cloth in a temperature-controlled greenhouse (16°–27°C range) at Union College beginning on 16 November 2004. Samples were watered with an automatic sprinkler five times per 24 h with deionized water and sprayed with Gamborg’s B-5 basal medium with minimal organics (0.32 M, G5893, Sigma-Aldrich, St. Louis, Missouri, USA) every 2 weeks. Natural sunlight was supplemented with 1000 W multivapor lamps achieving a maximum of 300 µmol•m^–2•s^–1 photosynthetic photon flux density (PPFD; light intensity over a range of 400–700 nm) for 16 h•d^–1. Sample positions were randomized three times during the growth period. At 7 weeks, two 7.5 cm diameter, 1–2 cm high PVC rings were fastened around portions of each canopy and anchored to the mesh. These became the samples measured for physiological properties. Analyses began on 25 February 2005. Plant growth form appeared similar to natural populations throughout the study.

Plant traits
Plant characteristics were measured on new tissue produced during the growth period. Tissue traits included: water content (g H₂O•g dry mass^–1), shoot mass per area (SMA g•dry mass•cm^–2 ground surface area), chlorophyll (chl) concentration (chls a + b, µg chl•g dry mass^–1), carotenoid concentration (µg carotenoids, g•dry mass^–1), and nitrogen content on mass (N_mass, %) and area (N_area, g•m^–2 ground surface area) bases. Water content was determined during photosynthesis measurements and represents the water content under common-garden conditions and is not a measure of maximal water holding capacity. Pigment, SMA, and nitrogen analyses were vertically stratified. Plants were divided into three layers: (1) the capitulum, (2) the uppermost 3 cm of plant stem plus branches below the capitulum (hereafter referred to as the stem), and (3) the plant portion below 3 cm (hereafter referred to as the base). Biomass from each layer of physiological samples (three per species as described later) was determined following oven drying (24 h at 65°C), and when divided by ground surface area, their sum represents SMA. Concentrations of nitrogen were determined separately for each layer in each sample. Dried and ground (#20 screen on Wiley Mill) tissue was analyzed following combustion on a ThermoQuest CE Instruments NC2100 Elemental Analyzer (ThermoQuest Italia S.P.A., Rodano, Italy) at the Biology Annex Analytical Laboratories, University of New Mexico. For whole canopies, N_mass and N_area were calculated. Given that up to 80% of net carbon gain occurs in the capitulum (Wallén et al., 1988), N_mass and N_area were also calculated for the capitulum only (Cap-N_mass, Cap-N_area). For pigment analyses, three individuals were collected from each sample, divided into the three sections, frozen, and stored at –70°C prior to analysis. Pigment concentrations were measured following low pressure drying to constant mass (16 h) in a lyophilizer (Labconco Centrivap 78100–00, Kansas City, Missouri, USA), and extraction in 80% acetone following procedures outlined in Rice (1995). Calculations for chlorophylls a and b and carotenoids follow Lichtenthaler and Wellburn (1983). Concentrations of chlorophyll a and b and carotenoids for each canopy segment were multiplied by biomass within each layer of photosynthesis samples. The sums of these were divided by biomass of the photosynthesis samples to calculate whole canopy chlorophyll and carotenoid concentrations.

Plant shoot and canopy traits were also evaluated and included fascicle density (i.e., clusters of branches on stem), volume of leaf hyaline cells (i.e., water-holding cells that lack plasma membranes and organelles at maturity), capitulum density (number per cm² ground surface area), canopy height (cm), the ratio of capitulum to stem biomass, and light attenuation. Fascicle density was derived by counting the number of fascicles on three 3-cm portions of the upper stem for each sample. Mean values per plant were expressed on a per cm basis. Assuming that the fraction of the leaf cell cross-sectional area is invariant along the leaf length, the relative volume of hyaline cells is equal to their relative cross-sectional area within the leaf. The relative hyaline cell volume was measured on leaf cross-sections taken from the middle third of mature spreading branch leaves. Cross-sections were digitally photographed at 400x (Zeiss Axioskope microscope with an Infinity 2 camera and software; Lumenera Scientific, Ottawa, Ontario, Canada). The areas of five hyaline and five photosynthetic cells from two leaves per sample were measured using the area tool in the program Image J (W.S. Rasband, ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA). Relative hyaline cell volume was expressed as the percent of total leaf volume; mean values from each sample were used.

Capitulum density was measured by counting capitula in the photosynthesis samples and dividing by ground surface area. Plant height was measured in the greenhouse at the end of the growth period. The ratio of biomass between the capitulum and top 3 cm of the stem was used to characterize differences in its vertical distribution in the canopy (M_cap/M_stem).

Light attenuation was measured as the absorbance of light by the upper 3 cm of the canopy. In S. teres, there was insufficient material to conduct this analysis, so only nine species were evaluated. For this analysis, 7.5 cm diameter samples were trimmed to 3 cm in depth, and the light intensity at the base of this section was measured relative to that at the surface. Light was supplied at 110 µmol•m^–2•s^–1 PPFD from a light array containing 120 2-mm diameter white LED lamps. Light levels were assessed at six evenly distributed locations in the base of the canopy using a 2 mm diameter light probe (Walz Leaf-Clip 2060-B interfaced with the MINIPAM chlorophyll fluorometer; Effeltrich, Germany). Light absorbance was calculated as the ratio of light intensity at 3 cm depth relative to the canopy surface subtracted from unity and expressed on a percentage basis.

Photosynthetic characteristics
Maximum net CO₂ assimilation rates (A), apparent quantum yield (), the light intensity where 95% of A is achieved (PPFD_95%, µmol•m^–2•s^–1), and the light compensation point (LCP) were estimated from light response curves conducted on three samples per species. Assimilation was expressed relative to biomass (A_mass) and area (A_area).

To measure photosynthesis, we removed samples in the 7.5 cm diameter mesh-bottomed PVC rings and trimmed all stem material beneath the mesh, leaving only plant tissue that formed during the greenhouse growth period. Following induction under 100 µmol•m^–2•s^–1 PPFD, cylinders were placed in a closed 1.8 L photosynthesis chamber. A fan circulated chamber air through the sample and chamber from below. This chamber was interfaced with an IRGA based photosynthesis system (LiCor 6200, Lincoln, Nebraska, USA). Measurements of net rates of CO₂ exchange followed a 6-min equilibration at each light level. Chamber conditions were 420 ppm CO₂ (initial), 24 ± 2°C branch temperature and 90 ± 4% relative humidity. Change in CO₂ over two sequential 20 s periods was averaged and used to calculate net photosynthetic rates. Light curves were generated by conducting seven measurements over light intensities from 35 to 900 µmol•m^–2•s^–1 PPFD. Samples were weighed initially and rewetted following measurement at each light level to maintain constant water content. Light was supplied with a 10 cm x 11 cm array providing 900 µmol•m^–2•s^–1 maximal PPFD from 445 and 617 nm LED lights (Photon Systems Instruments, Brno, Czech Republic). Rates of dark respiration expressed per unit mass (R_mass) were measured following a 20-min equilibration in the dark.

Photosynthetic parameters were derived by fitting light response curves to the Mitscherlich model: net photosynthesis = A [1 – exp^{– (PPFD – LCP)}], where A is maximum assimilation, is apparent quantum efficiency, PPFD is light intensity, and LCP, is light compensation point (Peek et al., 2002). Models were fit using nonlinear Levenberg-Marquardt estimation procedures.

Carbon isotope fractionation that occurs during CO₂ exchange due to physiochemical (e.g., diffusion) and physiological (e.g., fixation at rubisco) processes was measured using tissue ¹³C values (Farquhar et al., 1989). ¹³C values vary as a function of chloroplastic CO₂ concentrations, which are influenced by rates of carbon fixation and diffusive resistance, the latter controlled by the thickness of water films in Sphagnum (Rice and Giles, 1996; Williams and Flanagan, 1996; Rice, 2000). The ¹³C values were measured on 1–2 mg capitulum samples using a Delta S SIRMS with Conflo interface (Finnigan MAT, Bremen, Germany) in continuous flow mode after combustion in a Carlo Erba 1500 Series 1 (Carlo Erba Strumentazione, Milan, Italy) at the Carnegie Institute, Palo Alto, California, USA.

Statistical analyses
The correlation structure among plant traits was explored with principal components analysis (PCA) employing a correlation matrix with samples as data points (N = 30). N_area was not used in this analysis because it is the product of SMA and N_mass, which were both included. N_area was used in regressions (described later). Correlation analysis was used to compare physiological characteristics and their association with PCA axis scores. Linear regression was applied to compare individual plant traits, including N_area, with A_mass and A_area. In addition, the distribution of nitrogen in the capitulum only (Cap-N_mass, Cap-N_area) was used in this analysis. Distributions of all traits were not significantly different from normal (P > 0.05, K-S test). Statistical tests were carried out using the program SPSS 13.0 for Windows (SPSS, Chicago, Illinois, USA).

RESULTS

Plant traits
Variation in plant traits among species was highly structured. In the PCA analysis, the first three axes combined to account for 72% of variation in the data with the first axis representing the majority of that variation (43%). That axis showed a spectrum of variation in species values. Although S. tenerum appeared as an outlier on the first axis due to its having the highest or lowest value for 11 of 12 traits (Tables 1, 2), it was left in the analysis because the structure of the PCA was very similar with or without it as evidenced by a high correlation among the two first axis scores and the two second axis scores in those analyses (r = 0.97 and 0.91 for first and second axes correlations). Species with low first axis scores had elevated values for M_cap/M_stem, plant height, and chl a/b ratio, which were positively correlated with one another. Variation in these characteristics was inversely related to those with high first axis loadings: high carotenoid and nitrogen concentrations, canopy light absorbance, water content, and capitulum and fascicle densities (Fig. 1). Thus, the first PCA axis showed high correlation structure among traits at the tissue, shoot, and canopy levels and distinguished densely packed species with high concentrations of pigments and nitrogen (high first axis scores) from those with low concentrations of those that distribute biomass in the upper portions of the canopy and grow rapidly in height. The second PCA axis (16% of variation) separated species by hyaline cell volume and water content.

View larger version (11K): [in this window] [in a new window]   Fig. 1. Plant trait factor loadings from a principal component analysis (PCA) of Sphagnum plant tissue and canopy traits. Data are from Tables 2 and 3 and the PCA employed a correlation matrix. The length of vectors represents the correlation (r value) of each variable with the PCA axes.

View larger version (21K): [in this window] [in a new window]   Fig. 2. Distribution of nitrogen in Sphagnum shoots. Mean (N = 3) nitrogen contents of the capitulum, stem (top 3 cm) and base (below 3 cm) are shown and expressed on a mass basis (Nmass; error bars represent standard errors). Species differ in their allocation of nitrogen within the canopy with the highest Nmass occurring in the capitulum, stem or base, depending on the species. Species names are provided in Table 1.

Functional relationships
Physiological characteristics associated closely with the primary variation in tissue, shoot, and canopy traits as summarized by the PCA. Physiological parameters differed in their association with the PCA axis scores and in their relationships with plant traits individually. A_mass and R_mass, but not A_area, had a strong negative association with the first PCA axis and ¹³C had a positive relationship. The LCP was negatively associated with the third PCA axis. Neither PPFD_95% nor were associated with the first three PCA axes (Table 4).

There was no association between A_mass and N_mass or between A_area and N_area (Fig. 3A, B). However, when considering only nitrogen in the capitulum, A_area and Cap-N_area, but not A_mass and Cap-N_mass, associated strongly (R² > 0.64, P < 0.001; Fig. 3C, D). The positive A_area–Cap-N_area relationship was not due to differences in nitrogen concentration within capitulum (Cap-N_mass), which did not correlate with Cap-N_area. A_mass and A_area were also associated with plant traits that had high or low factor loadings on the first PCA axis. Positive associations included plant height and M_cap.:M_stem ratio, whereas water content and carotenoid concentration were inversely related (Fig. 4).

View larger version (18K): [in this window] [in a new window]   Fig. 3. Assimilation–nitrogen relationships in Sphagnum. Light saturated rates of (A, C) net CO2 exchange expressed on mass (Amass) or (B, D) area (Aarea) bases are expressed relative to shoot system nitrogen (Nmass and Narea) or to nitrogen in the capitulum only (Cap-Nmass, Cap-Narea). Only the relationship Aarea–Cap-Narea is significant (P < 0.001). Species names are provided in Table 1.

View larger version (15K): [in this window] [in a new window]   Fig. 4. Relationships between CO2 assimilation and selected traits in Sphagnum. Regression relationships are shown between plant traits and expression of light saturated rates of net CO2 uptake on mass (Amass) and area (Aarea) bases. Lines indicate significant relationships (P < 0.05). Species designations are shown in Fig. 3.

Assimilation–nitrogen relationships
Although functional traits in Sphagnum have a strong primary dimension of variation, as do vascular plant leaves, the specific relationships in these two groups differ dramatically and suggest that Sphagnum shoot systems do not function as vascular plant leaf analogues. For example, in broad surveys of vascular plants, A_mass and A_area have strong positive relationships with N_mass and N_area (Hikosaka, 2004; Wright et al., 2004a, b). Leaves with elevated tissue nitrogen have increased allocation to photosystems and Calvin cycle enzymes relative to structural or other nonphotosynthetic biochemistry or cells, thereby increasing rates of carbon uptake. In Sphagnum, neither A_mass nor A_area was significantly associated with nitrogen contents of whole canopies (Fig. 3).

In vascular plant leaves, species differ in their allocation of nitrogen to carbon gain; species with thick leaves and high investment in cell wall compounds, which contribute to longer leaf life span, reduce light availability within the leaf (Hikosaka, 2004; Shipley et al., 2006), and lower area-based carbon assimilation. Such trade-offs in nitrogen allocated to either photosynthetic metabolism or nonphotosynthetic structural or metabolic compounds underlie the positive relationship between A and nitrogen. In Sphagnum, differences in the distribution of nitrogen within shoot systems may affect the efficiency of carbon uptake relative to nitrogen and dissociate carbon assimilation from nitrogen content. In all Sphagnum species, nitrogen concentrations remain high in lower stems (70–126% of capitulum nitrogen concentrations in stems and leaves below 3 cm, Fig. 2), even though light levels in this region are below those required for positive carbon gain for most species. Sequestering nitrogen and other nutrient ions in stems is an effective competitive strategy in Sphagnum (Rydin and Jeglum, 2006) and reduces rates of decomposition, thereby contributing to peat formation (Vitt et al., 2003). To assist with this, up to 30% of plant biomass may be allocated to polyuronic acids that participate in this process (Clymo, 1963; van Breemen and Finzi, 1998; Popper and Fry, 2003; Kremer et al., 2004; Ballance et al., 2007). In addition, Sphagnum species store nitrogen in amino acids in the stem, particularly asparagine, which can account for up to 21% of stem nitrogen content (Limpens and Berendse, 2003). Although plants may translocate nitrogen from the stem to growing tissues in the capitulum, this transport accounts for less than 12% percent of the annual requirement in the capitulum (Aldous, 2002), and nitrogen concentrations in the stem remain high. Consequently on an area basis, species retain high concentrations of nitrogen in shoot tissues that are not involved in photosynthesis.

In Sphagnum, the pool of nitrogen in shoot regions not subject to sufficient light may be over two-thirds of shoot system nitrogen, but much lower in species that position nitrogen more effectively in the capitulum (see Fig. 2). Thus, the nitrogen content in the capitulum rather than in the entire shoot system is a better predictor of carbon assimilation, at least on an area basis (Fig. 3D). This results from some species, but not others, concentrating nitrogen and biomass in the capitulum at the top of the plant where light levels are high. Because A_mass for the capitulum alone was not measured, we could not determine if a similar relationship was found when considering A_mass and N_mass of the capitulum (Fig. 3C). We suspect that if the only the capitulum was considered, the A_mass–N_mass relationship would be positive. In terms of its functional relationships, the surface of the capitulum, but not the whole shoot system, may function similarly to a vascular plant leaf. Because this dynamic photosynthetic surface can be modified by the growth conditions, it is physiologically and morphologically plastic and allows acclimation to changing environmental conditions. Differences in the rate of vertical plant growth may control the rate of this acclimation process as it influences the formation of new capitulum tissues (discussed later).

Due to sequestering and storing nitrogen in lower stems, Sphagnum shoot systems do not function similarly to vascular plant canopies either. In Sphagnum, all branches originate in the capitulum where light levels are high. Branches are moved to the canopy interior during growth and do not develop in low light where they may become optimized for those conditions as are leaves in woody vascular plant canopies (Terashima and Hikosaka, 1995; Kull and Niinemets, 1998; Hikosaka, 2004). In herbaceous plant canopies, nitrogen is translocated from senescing leaves in the canopy interior to leaves in higher light, which also increases carbon exchange relative to plant nitrogen (Gastal and Lemaire, 2002; Shiratsuchi et al., 2006). Although nitrogen also moves vertically in Sphagnum shoot systems (Aldous, 2002), most nitrogen remains sequestered within the canopy interior.

Instead of translocating nitrogen to keep it within high light regions of the canopy, Sphagnum species differentially concentrate mass and its associated nitrogen in the capitulum, allowing the shoot of some species to use nitrogen within the canopy effectively for net carbon uptake. This character is associated with rapid stem elongation, leading to the strong correlation between plant height and A_mass/A_area (Fig. 4). Ligrone and Duckett (1998) describe the pattern of secondary growth in Sphagnum stems responsible for capitulum formation and stem elongation. A set of subapical cells undergo secondary cell division and elongation forming internodes between fascicles, the length of which determines the rate of stem elongation. Variation in the initiation, duration, and width of this region of secondary growth will control the distribution of biomass and correlated tissue composition within the canopy. Tall plants elongate rapidly in this region, a pattern of development that leads to biomass, nitrogen, and photosynthetic pigments becoming concentrated in the upper canopy (i.e., high M_cap/M_stem), and ultimately to high efficiency of light and carbon capture. Given the strong association between these canopy-level characteristics and photosynthetic function in the genus, variation in secondary growth should be under strong selective pressure and may represent a key adaptive feature that controls plant performance in Sphagnum. This character and its relationship to plant function deserve much more attention.

Water content and distribution
A_mass and A_area had strong associations with water content (Fig. 4), which is a complex trait influenced by biomass distribution (M_cap/M_stem), hyaline cell volume, and morphological factors that affect extracellular water holding. In Sphagnum, variation in plant traits that affect water storage, transport, and loss exert strong influence on the distribution of species across gradients of water availability within and among wetlands (Andrus et al., 1983; Titus and Wagner, 1984; Rydin and McDonald, 1985). Sphagnum leaves are differentiated into photosynthetic and hyaline cells, the latter of which serve in water storage as they lack membranes and organelles, contain only cell walls, and can cover over 75% of the leaf surface. Species with large hyaline cells avoid desiccation and have high plant water contents. Increasing water content, however, reduces rates of carbon assimilation as shown by its strong negative association with A_mass and A_area (Fig. 4). The relationship between water content and C uptake has two potential underlying causes. First, shoots with greater allocation to hyaline relative to photosynthetic cells achieve lower rates of assimilation on a mass basis as leaves have proportionally fewer photosynthetic cells and possess lower efficiency of CO₂ uptake. In aquatic sphagna, higher relative volumes of hyaline cells are associated with lower relative growth rates (Rice and Schuepp, 1995). However, on an area basis, a species can compensate for low tissue level photosynthetic efficiency by having high SMA as shown by S. tenerum, which has a relatively high A_mass for its water content (Fig. 4).

Second, increased water-holding capacity may impede CO₂ uptake through its direct impact on diffusion resistance. Diffusion through external water films is an important component of resistance to CO₂ uptake in bryophytes (Proctor, 1981; Rice and Giles, 1996; Williams and Flanagan, 1996; Proctor, 2000). Relatively larger hyaline cells result in thicker average external water films because they serve as a reservoir to buffer periods of low water availability, maintaining saturated cell walls and capillary spaces. In addition, species differ in their ability to hold extracellular water and water within cell walls (Hájek and Beckett, 2008). In the current study, variation in hyaline cell volume only contributed to 13% of the variation in water content (based on regression, results not shown), and consequently, differences in water content are primarily due to differences in extracellular water holding capacity. Larger hyaline cells may also increase the amount of photosynthetic cell surface exposed to hyaline cell water, increasing diffusion resistance. Increases in these resistances should cause a decrease in fractionation of ¹³CO₂ during photosynthesis as the discrimination would reflect fractionation that occurs during diffusion rather than the large fractionation caused by rubisco during carbon fixation. This relationship is clearly expressed when water contents are varied in single species studies during photosynthesis (Rice and Giles, 1996; Williams and Flanagan, 1996) and should lead to a less negative ¹³C value when diffusional resistance is higher (Rice, 2000), a pattern observed in the positive ¹³C–water content relationship in this study. Also, ¹³C values were negatively associated with A_mass, indicating that species with higher rates of mass specific CO₂ uptake experience lower resistance to CO₂ uptake, which leads to higher chloroplastic concentrations of CO₂ and greater carbon fractionation. A similar result was found in the relationship between ¹³C and relative growth rates in greenhouse studies of Sphagnum (Rice, 2000). These results suggest that enhanced rates of CO₂ uptake are achieved, in part, by reduced diffusional resistance to CO₂ uptake. Unfortunately, there is no clear relationship between particular morphological or anatomical features and water film thickness as that characteristic is a complex function that varies with leaf size, shape, density, and other morphological features that influence the size, abundance, and location of capillary spaces.

Carotenoid function
A_mass and A_area also associate closely with carotenoid concentrations, a relationship that was strongly negative (Fig. 4). These associations suggest that carotenoids are involved in photoprotection expressed through xanthophyll cycle interconversions (Demmig-Adams and Adams, 1992, 1996) or shading, both of which lead to greater dissipation of light energy. Under light intensities of 800 µmol•m^–2•s^–1, Sphagnum undergoes photoinhibition that reduces rates of growth and photosynthesis (Harley et al., 1989; Murray et al., 1993). Species that persist in open habitats like S. contortum, S. lescurii, S. teres, and S. tenerum have the highest carotenoid concentrations. For S. teres across a range of water contents, Van Gaalen et al. (2007) have recently demonstrated that short-term shifts in xanthophyll cycle pigments are associated with nonphotochemical quenching. In other bryophytes, such patterns are linked to changes in pool sizes of xanthophyll cycle pigments (Deltoro et al., 1998; Lovelock and Robinson, 2002), and it is likely that under conditions of high light, carotenoids are functioning to dissipate excess light energy, a process expressed most strongly in species with higher total carotenoid concentrations. For vascular plants, Demmig-Adams and Adams (2006) argue that an array of xanthophyll cycle-mediated photoprotective mechanisms exist, with some having short-term, rapid responses and others having intermediate or long-term effects; the latter are characteristic of slow-growing evergreen species. The negative relationship between carotenoid concentrations and A_mass/A_area may be caused by similar differences in allocation to pigments engaged in long-term or permanent energy dissipation, a characteristic that may benefit plants that inhabit open bog habitats where light may be damaging.

Conclusions
Tissue, shoot, and canopy traits associate with one another and with photosynthetic characteristics, forming a strong primary axis of variation in Sphagnum. Fascicle and capitulum density; carotenoid, chlorophyll and nitrogen concentrations; water content; and SMA were positively associated with each other and negatively related to plant height and ratios of M_cap to M_stem and chl a to b (Fig. 1). These relationships define a principal trade-off between Sphagnum species with high metabolic cost (e.g., high sequestration of nitrogen, high carotenoid concentrations, high investment in water holding capacity) that allow plants to tolerate environmental stress (e.g., low water and nutrients, high light) and species with metabolically inexpensive tissue that photosynthesize and elongate rapidly forming tall active canopies that concentrate biomass, photosynthetic pigments, and nitrogen in their capitula, but that allow deep light penetration and have greater vertical distribution of photosynthesis. Given the important role of the canopy interior branches in water storage and nutrient sequestration, these trade-offs observed in Sphagnum shoot systems differ from those in either vascular plant leaves or canopies. Consequently, the canopies of bryophytes represent a unique functional type and mechanistic models of their function should account for growth and developmental processes that cause variation in the organization of the upper-canopy surface.

FOOTNOTES

¹ The authors thank B. Shaw, J. Shaw, R. Andrus, L. Smith, G. Smith, and T. Fitzgerald for assistance identifying collecting localities or for access to collection sites. L. Giles, L. Fleishman, and J. Kelbeck provided help with laboratory equipment or analyses. The manuscript was improved by comments from three anonymous reviewers. Financial support was received from Union College’s Internal Education Foundation and Faculty Research Fund Grants and from the University of New Mexico.

² Author for correspondence (e-mail: rices{at}union.edu)

LITERATURE CITED

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