The scaling of elemental stoichiometry and growth rate over the course of bamboo ontogeny.

Stoichiometric rules may explain the allometric scaling among biological traits and body size, a fundamental law of nature. However, testing the scaling of elemental stoichiometry and growth to size over the course of plant ontogeny is challenging. Here, we used a fast-growing bamboo species to examine how the concentrations and contents of carbon (C), nitrogen (N) and phosphorus (P), relative growth rate (G), and nutrient productivity scale with whole-plant mass (M) at the culm elongation and maturation stages. The whole-plant C content vs M and N content vs P content scaled isometrically, and the N or P content vs M scaled as a general 3/4 power function across both growth stages. The scaling exponents of G vs M and N (and P) productivity in newly grown mass vs M relationships across the whole growth stages decreased as a -1 power function. These findings reveal the previously undocumented generality of stoichiometric allometries over the course of plant ontogeny and provide new insights for understanding the origin of ubiquitous quarter-power scaling laws in the biosphere.

Comparison between computer recognition and manual measurement methods for the estimation of leaf area.

BACKGROUND AND AIMS: Leaf area (A) is a crucial indicator of the photosynthetic capacity of plants. The Montgomery equation (ME), which hypothesizes that A is proportional to the product of leaf length (L) and width (W), is a valid tool for nondestructively measuring A for many broad-leaved plants. At present, the methods used to compute L and W for ME can be broadly divided into two kinds: using computer recognition, and measuring manually. However, the potential difference in the prediction accuracy using either method has not been thoroughly examined in prior studies. METHODS: In the present study, we measured 540 Alangium chinense leaves, 489 Liquidambar formosana leaves, and 215 Liriodendron × sinoamericanum leaves, utilizing computer recognition and manual measurement methods to determine L and W. ME was used to fit the data determined by the two methods, and the goodness of fits were compared. The prediction errors of A were analyzed by examining the correlations with two leaf symmetry indices (areal ratio of the left side to the right side, and standardized index for bilateral asymmetry), as well as the leaf shape complexity index (the leaf dissection index). KEY RESULTS: The results indicate that there is a neglectable difference in the estimation of A between both methods. This further validates that ME is an effective method for estimating A in broad-leaved tree species, including those with lobes. Additionally, leaf shape complexity significantly influenced the estimation of A. CONCLUSIONS: These results show that the use of computer recognition and manual measurement in the field are both effective and feasible, although the influence of leaf shape complexity should be considered when applying ME to estimate A in the future.

The allocation of anatomical traits determines the trade-off between fine root resource acquisition-transport function.

Cortex radius (CR) and stele radius (SR) are important functional traits associated with the nutrient acquisition and transport functions of fine roots, respectively. However, for developmental and anatomical reasons, the resource acquisition-transport relationship of fine roots is expected to be different for different root orders. To address this issue, critical fine root anatomical traits were examined for the first three orders of roots of 59 subtropical woody plants. Designating the most distal fine roots as order one, SR scaled isometrically with respect to root radius (RR) (i.e., SR ∝ RR1.0) in the three root orders, whereas CR scaled allometrically with respect to RR (i.e., CR ∝ RR>1.0) with the numerical values of scaling exponents increasing significantly with increasing root orders thereby indicating a disproportional increase in CR with increasing root orders. There were also differences between normalized root tissue (CR/RR and SR/RR) and RR in different root orders. A negative isometric relationship (i.e., SR/RR ∝ RR-1.0) existed between SR/RR and RR in three order roots, whereas the allometric exponent between CR/RR and RR increased with root order (from 0.88 to 1.55). Collectively, the data indicate that root anatomical and functional traits change as a function of RR and that these changes need to be considered when modeling fine root resource acquisition-transport functions.

The fern economics spectrum is unaffected by the environment.

The plant economics spectrum describes the trade-off between plant resource acquisition and storage, and sheds light on plant responses to environmental changes. However, the data used to construct the plant economics spectrum comes mainly from seed plants, thereby neglecting vascular non-seed plant lineages such as the ferns. To address this omission, we evaluated whether a fern economics spectrum exists using leaf and root traits of 23 fern species living under three subtropical forest conditions differing in light intensity and nutrient gradients. The fern leaf and root traits were found to be highly correlated and formed a plant economics spectrum. Specific leaf mass and root tissue density were found to be on one side of the spectrum (conservative strategy), whereas photosynthesis rate, specific root area, and specific root length were on the other side of the spectrum (acquisitive strategy). Ferns had higher photosynthesis and respiration rates, and photosynthetic nitrogen-use efficiency under high light conditions and higher specific root area and lower root tissue density in high nutrient environments. However, environmental changes did not significantly affect their resource acquisition strategies. Thus, the plant economics spectrum can be broadened to include ferns, which expands its phylogenetic and ecological implications and utility.

Environmental-biomechanical reciprocity and the evolution of plant material properties.

Abiotic-biotic interactions have shaped organic evolution since life first began. Abiotic factors influence growth, survival, and reproductive success, whereas biotic responses to abiotic factors have changed the physical environment (and indeed created new environments). This reciprocity is well illustrated by land plants who begin and end their existence in the same location while growing in size over the course of years or even millennia, during which environment factors change over many orders of magnitude. A biomechanical, ecological, and evolutionary perspective reveals that plants are (i) composed of materials (cells and tissues) that function as cellular solids (i.e. materials composed of one or more solid and fluid phases); (ii) that have evolved greater rigidity (as a consequence of chemical and structural changes in their solid phases); (iii) allowing for increases in body size and (iv) permitting acclimation to more physiologically and ecologically diverse and challenging habitats; which (v) have profoundly altered biotic as well as abiotic environmental factors (e.g. the creation of soils, carbon sequestration, and water cycles). A critical component of this evolutionary innovation is the extent to which mechanical perturbations have shaped plant form and function and how form and function have shaped ecological dynamics over the course of evolution.

Competitive performance of Pinus massoniana is related to scaling relationships at the individual plant and branch levels.

PREMISE: Competition is an important driver of tree mortality and thus affects forest structure and dynamics. Tree architectural traits, such as height-to-diameter (H-D) and branch length-to-diameter (L-d) relationships are thought to influence species competitiveness by affecting light capture. Unfortunately, little is known about how the H vs. D and L vs. d scaling exponents are related to tree performance (defined in the context of growth vigor) in competition. METHODS: Using data from field surveys of 1547 individuals and destructive sampling of 51 trees with 1086 first-order branches from a high-density Pinus massoniana forest, we explored whether the H vs. D and the L vs. d scaling exponents respectively differed numerically across tree performance and branch vertical position in crowns. RESULTS: The results indicated that (1) the H vs. D scaling exponent decreased as tree performance declined; (2) the L vs. d scaling exponent differed across tree performance classes (i.e., the scaling exponent of "inferior" trees was significantly larger than that of "moderate" and "superior" trees); (3) the L vs. d scaling exponent decreased as branch position approached ground level; and (4) overall, the branch scaling exponent decreased as tree performance improved in each crown layer, but decreased significantly in the intermediate layer. CONCLUSIONS: This study highlights the variation within (and linkage among) length-to-diameter scaling relationships across tree performance at the individual and branch levels. This linkage provides new insights into potential mechanisms of tree growth variation (and even further mortality) under competition in subtropical forests.

Scaling relationships of leaf vein and areole traits versus leaf size for nine Magnoliaceae species differing in venation density.

PREMISE: Across species, main leaf vein density scales inversely with leaf area (A). Yet, minor vein density manifests no clear relationship with respect to A, despite having the potential to provide important insights into the trade-off among the investments in leaf mechanical support, hydraulics, and light interception. METHODS: To examine this phenomenon, the leaves of nine Magnoliaceae leaves were sampled, and the scaling relationships among A and midrib length (ML), total vein length (TVL), total vein area (TVA), total areole area (TAA), and mean areole area (MAA) were determined. The scaling relationships between MAA and areole density (the number of areoles per unit leaf area) and between MAA and A were also analyzed. RESULTS: For five of the nine species, A was proportional to ML2 . For eight of the nine species, TVL and TVA were both proportional to A. The numerical values of the scaling exponents for TAA vs. A were between 1.0 and 1.07 for eight species; i.e., as expected, TAA was isometrically proportional to A. There was no correlation between MAA and A, but MAA scaled inversely with respect to areole density for each species. CONCLUSIONS: The correlation between midrib "density" (i.e., ML/A) and A, and the lack of correlation between total leaf vein density and A result from the A ∝$\propto $ ML2 scaling relationship and the proportional relationship between TVL and A, respectively. Leaves with the same size can have widely varying MAA. Thus, leaf size itself does not directly constrain leaf hydraulic efficiency and redundancy.

Diminishing returns among lamina fresh and dry mass, surface area, and petiole fresh mass among nine Lauraceae species.

PREMISE: The phenomenon called "diminishing returns" refers to a scaling relationship between lamina mass (M) vs. lamina area (A) in many species, i.e., M ∝ Aα>1 , where α is the scaling exponent exceeding unity. Prior studies have focused on the scaling relationships between lamina dry mass (DM) and A, or between fresh mass (FM) and A. However, the scaling between petiole mass and M and A has seldom been investigated. Here, we examine the scaling relationships among FM, DM, A, and petiole fresh mass (PFM). METHODS: For each of 3268 leaves from nine Lauraceae species, FM, DM, A, and PFM were measured, and their scaling relationships were fitted using reduced major axis regression protocols. The bootstrap percentile method was used to test the significance of the difference in α-values between any two species. RESULTS: The phenomenon of diminishing returns was verified between FM vs. A and DM vs. A. The FM vs. A scaling relationship was statistically more robust than the DM vs. A scaling relationship based on bivariate regression r2 -values. Diminishing returns were also observed for the PFM vs. FM and PFM vs. A scaling relationships. The PFM vs. FM scaling relationship was statistically more robust than the PFM vs. A scaling relationship. CONCLUSIONS: "Diminishing returns" was confirmed among the FM, DM, A, and PFM scaling relationships. The data collectively indicate that the petiole scales mechanically more strongly with lamina mass than with area, suggesting that static (self) loading takes precedence over dynamic (wind) loading.

Plant volatiles mediate evolutionary interactions between plants and tephritid flies and are evolutionarily more labile than non-volatile defenses.

Studies show that plant defenses influence the host-use of herbivores and tend to be evolutionarily more labile than herbivore traits (e.g. feeding preferences). However, all previous studies have focused exclusively on non-volatile plant defenses thereby overlooking the roles of plant volatiles. We hypothesized that volatiles are equally important determinants of herbivore host-use and are evolutionarily more labile than herbivore traits. To test these hypotheses, the following experiments were conducted. We identified the volatiles and non-volatiles of 17 Asteraceae species and measured their relative contents. We also used a highly resolved bipartite trophic network of the 17 host species and 20 herbivorous (pre-dispersal seed predator) tephritid fly species to determine the evolutionary interactions between plants and herbivores. The chemical data showed that interspecific similarity in volatiles-but not non-volatiles and phylogenetic distance-significantly accounted for the herbivore community across the plant species; this implies that plant volatiles-but not non-volatile compounds and species identity-dictate plant-tephritid fly interactions. Moreover, we observed phylogenetic signal for non-volatiles but not for volatiles; therefore closely related herbivores do not necessarily use closely related host species with similar non-volatiles, but do tend to attack plants producing similar volatiles. Thus, plant volatiles are evolutionarily more labile than non-volatiles and herbivore traits associate with host use. These results show that the interactions between plants and herbivores are evolutionary asymmetric, shed light on the role of plant volatiles in plant-herbivore interactions, and highlight the need to include data for both volatiles and non-volatiles when investigating plant-animal interactions.

Rare plant species are at a disadvantage when both herbivory and pollination interactions are considered in an alpine meadow.

Rare plant species often suffer less damage than common species because of positive density-dependent herbivory, and it has been suggested that this 'rare species advantage' fosters plant species coexistence. However, it is unknown whether rare species have an advantage when pollination interactions are also considered. We hypothesized that a 'positive density-dependent pollination success' across plant species would result in common plants experiencing higher seed set rates compared to rare species, and that positive density-dependent effects would negate or even override the positive density-dependent damage due to herbivory resulting in higher seed loss rates in common plant species. We tested this hypothesis by concurrently examining a plant-predispersal seed predator system and a plant-pollinator system for 24 Asteraceae species growing in an alpine meadow community (Sichuan Province, China). Having previously reported a positive density-dependent effect on seed loss rates due to seed predators, we here focus on the density-dependent effects on pollination success by investigating pollinator species richness, visitation frequencies and seed set rates for each plant species. We also estimated the seed output rate of each plant species as the product of seed set rate and the rate of surviving seeds (i.e. 1 - the seed loss rate). Consistent with our hypothesis, a positive density-dependent effect was observed for pollinator species richness, visitation frequencies and seed set rates across plant species. Moreover, the positive effect overrode the negative density-dependent effect of herbivores on seed production, such that common species tended to have a higher seed output rate than rare species (i.e. we observed a 'rare species disadvantage'). These results indicate that the low seed output rate of rare species might result from a pollination limitation, and that both mutualistic and antagonistic interactions should be examined simultaneously to fully understand plant species coexistence in local communities.

"Diminishing returns" for leaves of five age-groups of Phyllostachys edulis culms.

PREMISE: Leaf mass (M) and lamina surface area (A) are important functional traits reported to obey a scaling relationship called "diminishing returns" (i.e., M ∝ Aα>1 ). Previous studies have focused primarily on eudicots and ignored whether the age of leaves affects the numerical value of the scaling exponent (i.e., α). METHODS: The effect of age was examined using 1623 Phyllostachys edulis leaves from culms differing in age collected in Nanjing, China. The scaling relationships among leaf A, fresh mass (FM), and dry mass (DM) were evaluated using reduced major axis protocols. The bootstrap percentile method was used to test the significance of differences in α-values. RESULTS: Overall, the numerical values of α exceeded 1.0. The scaling relationship between FM and A was statistically more robust than that between DM and A. The scaling exponents of FM vs. A exhibited a "high-low-high-low-high" numerical trend from the oldest to the youngest age-group. FM increased linearly as culm age decreased; the leaf DM per unit area (LMA) exhibited a parabolic trend across the age-groups. CONCLUSIONS: "Diminishing returns" is confirmed for all but one age-group of an important monocot species. The relationship between FM and A was statistically more robust than that between DM and A for each age-group. The FM per unit A decreased with increasing age-groups, whereas the middle age-groups had a greater LMA than the oldest and youngest age-groups. These data are the first to show that the age of shoots affects the scaling relationship between leaf mass and area.

Linkage between species traits and plant phenology in an alpine meadow.

Plant phenology differs largely among coexisting species within communities that share similar habitat conditions. However, the factors explaining such phenological diversity of plants have not been fully investigated. We hypothesize that species traits, including leaf mass per area (LMA), seed mass, stem tissue mass density (STD), maximum plant height (Hmax), and relative growth rate in height (RGRH), explain variation in plant phenology, and tested this hypothesis in an alpine meadow. Results showed that both LMA and STD were positively correlated with the onset (i.e., beginning) and offset (i.e., ending) times of the four life history events including two reproductive events (flowering and fruiting) and two vegetative events (leafing and senescing). In contrast, RGRH was negatively correlated with the four life phenological events. Moreover, Hmax was positively correlated with reproductive events but not with vegetative events. However, none of the eight phenological events was associated with seed size. In addition, the combination of LMA and STD accounted for 50% of the variation in plant phenologies. Phylogenetic generalized least squares analysis showed plant phylogeny weakened the relationships between species traits vs. phenologies. Phylogeny significantly regulated the variation in the ending but not the beginning of phenologies. Our results indicate that species traits are robust indicators for plant phenologies and can be used to explain the diversity of plant phenologies among co-occurring herbaceous species in grasslands. The findings highlight the important role of the combination of and trade-offs between functional traits in determing plant phenology diversity in the alpine meadow.

A General Model for Seed and Seedling Respiratory Metabolism.

The ontogeny of seed plants usually involves a dormant dehydrated state and the breaking of dormancy and germination, which distinguishes it from that of most organisms. Seed germination and seedling establishment are critical ontogenetic stages in the plant life cycle, and both are fueled by respiratory metabolism. However, the scaling of metabolic rate with respect to individual traits remains poorly understood. Here, we tested metabolic scaling theory during seed germination and early establishment growth using a recently developed model and empirical data collected from 41 species. The results show that (i) the mass-specific respiration rate (Rm) was weakly correlated with body mass, mass-specific N content, and mass-specific C content; (ii) Rm conformed to a single Michaelis-Menten curve as a function of tissue water content; and (iii) the central parameters in the model were highly correlated with DNA content and critical enzyme activities. The model offers new insights and a more integrative scaling theory that quantifies the combined effects of tissue water content and body mass on respiratory metabolism during early plant ontogeny.

Water content quantitatively affects metabolic rates over the course of plant ontogeny.

Plant metabolism determines the structure and dynamics of ecological systems across many different scales. The metabolic theory of ecology quantitatively predicts the scaling of metabolic rate as a function of body size and temperature. However, the role of tissue water content has been neglected even though hydration significantly affects metabolism, and thus ecosystem structure and functioning. Here, we use a general model based on biochemical kinetics to quantify the combined effects of water content, body size and temperature on plant metabolic rates. The model was tested using a comprehensive dataset from 205 species across 10 orders of magnitude in body size from seeds to mature large trees. We show that water content significantly influences mass-specific metabolic rates as predicted by the model. The scaling exponents of whole-plant metabolic rate vs body size numerically converge onto 1.0 after water content is corrected regardless of body size or ontogenetic stage. The model provides novel insights into how water content together with body size and temperature quantitatively influence plant growth and metabolism, community dynamics and ecosystem energetics.

The many roads to and from multicellularity.

The multiple origins of multicellularity had far-reaching consequences ranging from the appearance of phenotypically complex life-forms to their effects on Earth's aquatic and terrestrial ecosystems. Yet, many important questions remain. For example, do all lineages and clades share an ancestral developmental predisposition for multicellularity emerging from genomic and biophysical motifs shared from a last common ancestor, or are the multiple origins of multicellularity truly independent evolutionary events? In this review, we highlight recent developments and pitfalls in understanding the evolution of multicellularity with an emphasis on plants (here defined broadly to include the polyphyletic algae), but also draw upon insights from animals and their holozoan relatives, fungi and amoebozoans. Based on our review, we conclude that the evolution of multicellular organisms requires three phases (origination by disparate cell-cell attachment modalities, followed by integration by lineage-specific physiological mechanisms, and autonomization by natural selection) that have been achieved differently in different lineages.

Morphological (and not anatomical or reproductive) features define early vascular plant phylogenetic relationships.

PREMISE: Perhaps the most rapid period of vascular plant evolution occurred during the Silurian-Devonian time interval. Yet, few quantitative analyses have established the extent to which anatomical, morphological, or reproductive features contributed to this episode of tracheophyte diversification. METHODS: Phylogenetic analyses were performed using a newly revised matrix of 54 characters (with 158 character states) of 37 of the best-preserved Paleozoic (predominantly Devonian) plants. Equisetum was included to determine whether it aligns with fossil sphenopsids or taxa collectively considered "ferns". The topology of the 54-character consensus tree was then compared to the topologies generated using only reproductive features (18 characters; 47 character states), only anatomical features (14 characters; 54 character states), only morphological features (22 characters; 57 character states), and the three pairwise combinations (e.g., anatomical and morphological characters). RESULTS: The new 54-character tree topology continued to identify a trimerophyte-euphyllophyte clade and a zosterophyllophyte-lycophyte clade emerging from a Cooksonia-rhyniophyte plexus. Equisetum aligned with fossil sphenopsids rather than fern-like fossil taxa. Reproductive characters or anatomical characters analyzed in isolation resulted in nearly complete polytomy. Among the various permutations of the three categories, anatomical and morphological characters when combined provided the best restoration of the 54-character tree topology. CONCLUSIONS: The phylogenetic relationships among the canonical fossil taxa used in this analysis predominantly reflect morphological trends. Reproductive and anatomical features taken in isolation appear to be evolutionarily conservative characters, i.e., natural selection "sees" the external phenotype.

Nondestructive estimation of leaf area for 15 species of vines with different leaf shapes.

PREMISE: The nondestructive measurement of leaf area is important for expediting data acquisition in the field. The Montgomery equation (ME) assumes that leaf area (A) is a proportional function of the product of leaf length (L) and width (W), i.e., A = cLW, where c is called the Montgomery parameter. The ME has been successfully applied to calculate the surface area of many broad-leaved species with simple leaf shapes. However, whether this equation is valid for more complex leaf shapes has not been verified. METHODS: Leaf A, L, and W were measured directly for each of 5601 leaves of 15 vine species, and ME and three other models were used to fit the data. All four models were compared based on their root mean square errors (RMSEs) to determine whether ME provided the best fit. RESULTS: The ME was a reliable method for estimating the A of all 15 species. In addition, the numerical values of 13 of the 15 values of c fell within a previously predicted numerical range (i.e., between 1/2 and π/4). The data show that the numerical values of c are largely affected by the value of W/L, the concavity of the leaf base, and the number of lobes on the lamina. CONCLUSIONS: The Montgomery parameter can reflect the influence of leaf shape on leaf-area calculations and can serve as an important tool for nondestructive measurements of leaf area for many broad-leaved species and for the investigation of leaf morphology.

A general review of the biomechanics of root anchorage.

With few exceptions, terrestrial plants are anchored to substrates by roots that experience bending and twisting forces resulting from gravity- and wind-induced forces. Mechanical failure occurs when these forces exceed the flexural or torsional tolerance limits of stems or roots, or when roots are dislodged from their substrate. The emphasis of this review is on the general principles of anchorage, how the mechanical failure of root anchorage can be averted, and recommendations for future research.

The evolutionary origins of cell type diversification and the role of intrinsically disordered proteins.

The evolution of complex multicellular life forms occurred multiple times and was attended by cell type specialization. We review seven lines of evidence indicating that intrinsically disordered/ductile proteins (IDPs) played a significant role in the evolution of multicellularity and cell type specification: (i) most eukaryotic transcription factors (TFs) and multifunctional enzymes contain disproportionately long IDP sequences (≥30 residues in length), whereas highly conserved enzymes are normally IDP region poor; (ii) ~80% of the proteome involved in development are IDPs; (iii) the majority of proteins undergoing alternative splicing (AS) of pre-mRNA contain significant IDP regions; (iv) proteins encoded by DNA regions flanking crossing-over 'hot spots' are significantly enriched in IDP regions; (v) IDP regions are disproportionately subject to combinatorial post-translational modifications (PTMs) as well as AS; (vi) proteins involved in transcription and RNA processing are enriched in IDP regions; and (vii) a strong positive correlation exists between the number of different cell types and the IDP proteome fraction across a broad spectrum of uni- and multicellular algae, plants, and animals. We argue that the multifunctionalities conferred by IDPs and the disproportionate involvement of IDPs with AS and PTMs provided a IDP-AS-PTM 'motif' that significantly contributed to the evolution of multicellularity in all major eukaryotic lineages.