Brad S. Ripley

Ecophysiological traits in C3 and C4 grasses: a phylogenetically controlled screening experiment

Experimental evidence demonstrates a higher efficiency of water and nitrogen use in C(4) compared with C(3) plants, which is hypothesized to drive differences in biomass allocation between C(3) and C(4) species. However, recent work shows that contrasts between C(3) and C(4) grasses may be misinterpreted without phylogenetic control. Here, we compared leaf physiology and growth in multiple lineages of C(3) and C(4) grasses sampled from a monophyletic clade, and asked the following question: which ecophysiological traits differ consistently between photosynthetic types, and which vary among lineages? C(4) species had lower stomatal conductance and water potential deficits, and higher water-use efficiency than C(3) species. Photosynthesis and nitrogen-use efficiency were also greater in C(4) species, varying markedly between clades. Contrary to previous studies, leaf nitrogen concentration was similar in C(4) and C(3) types. Canopy mass and area were greater, and root mass smaller, in the tribe Paniceae than in most other lineages. The size of this phylogenetic effect on biomass partitioning was greater in the C(4) NADP-me species than in species of other types. Our results show that the phylogenetic diversity underlying C(4) photosynthesis is critical to understanding its functional consequences. Phylogenetic bias is therefore a crucial factor to be considered when comparing the ecophysiology of C(3) and C(4) species.

Comparing models for predicting species' potential distributions: a case study using correlative and mechanistic predictive modelling techniques

Abstract Models used to predict species’ potential distributions have been described as either correlative or mechanistic. We attempted to determine whether correlative models could perform as well as mechanistic models for predicting species potential distributions, using a case study. We compared potential distribution predictions made for a coastal dune plant ( Scaevola plumieri ) along the coast of South Africa, using a mechanistic model based on summer water balance (SWB), and two correlative models (a profile and a group discrimination technique). The profile technique was based on principal components analysis (PCA) and the group-discrimination technique was based on multiple logistic regression (LR). Kappa ( κ ) statistics were used to objectively assess model performance and model agreement. Model performance was calculated by measuring the levels of agreement (using κ ) between a set of testing localities (distribution records not used for model building) and each of the model predictions. Using published interpretive guidelines for the kappa statistic, model performance was “excellent” for the SWB model ( κ =0.852), perfect for the LR model ( κ =1.000), and “very good” for the PCA model ( κ =0.721). Model agreement was calculated by measuring the level of agreement between the mechanistic model and the two correlative models. There was “good” model agreement between the SWB and PCA models ( κ =0.679) and “very good” agreement between the SWB and LR models ( κ =0.786). The results suggest that correlative models can perform as well as or better than simple mechanistic models. The predictions generated from these three modelling designs are likely to generate different insights into the potential distribution and biology of the target organism and may be appropriate in different situations. The choice of model is likely to be influenced by the aims of the study, the biology of the target organism, the level of knowledge the target organism’s biology, and data quality.

Fire and fire‐adapted vegetation promoted C4 expansion in the late Miocene

Large proportions of the Earths land surface are covered by biomes dominated by C(4) grasses. These C(4)-dominated biomes originated during the late Miocene, 3-8 million years ago (Ma), but there is evidence that C(4) grasses evolved some 20 Ma earlier during the early Miocene/Oligocene. Explanations for this lag between evolution and expansion invoke changes in atmospheric CO(2), seasonality of climate and fire. However, there is still no consensus about which of these factors triggered C(4) grassland expansion. We use a vegetation model, the adaptive dynamic global vegetation model (aDGVM), to test how CO(2), temperature, precipitation, fire and the tolerance of vegetation to fire influence C(4) grassland expansion. Simulations are forced with late Miocene climates generated with the Hadley Centre coupled ocean-atmosphere-vegetation general circulation model. We show that physiological differences between the C(3) and C(4) photosynthetic pathways cannot explain C(4) grass invasion into forests, but that fire is a crucial driver. Fire-promoting plant traits serve to expand the climate space in which C(4)-dominated biomes can persist. We propose that three mechanisms were involved in C(4) expansion: the physiological advantage of C(4) grasses under low atmospheric CO(2) allowed them to invade C(3) grasslands; fire allowed grasses to invade forests; and the evolution of fire-resistant savanna trees expanded the climate space that savannas can invade.

Differences in drought sensitivities and photosynthetic limitations between co-occurring C3 and C4 (NADP-ME) Panicoid grasses

BACKGROUND AND AIMS The success of C4 plants lies in their ability to attain greater efficiencies of light, water and nitrogen use under high temperature, providing an advantage in arid, hot environments. However, C4 grasses are not necessarily less sensitive to drought than C3 grasses and are proposed to respond with greater metabolic limitations, while the C3 response is predominantly stomatal. The aims of this study were to compare the drought and recovery responses of co-occurring C3 and C4 NADP-ME grasses from the subfamily Panicoideae and to determine stomatal and metabolic contributions to the observed response. METHODS Six species of locally co-occurring grasses, C3) species Alloteropsis semialata subsp. eckloniana, Panicum aequinerve and Panicum ecklonii, and C4 (NADP-ME) species Heteropogon contortus, Themeda triandra and Tristachya leucothrix, were established in pots then subjected to a controlled drought followed by re-watering. Water potentials, leaf gas exchange and the response of photosynthetic rate to internal CO2 concentrations were determined on selected occasions during the drought and re-watering treatments and compared between species and photosynthetic types. KEY RESULTS Leaves of C4 species of grasses maintained their photosynthetic advantage until water deficits became severe, but lost their water-use advantage even under conditions of mild drought. Declining C4 photosynthesis with water deficit was mainly a consequence of metabolic limitations to CO2 assimilation, whereas, in the C3 species, stomatal limitations had a prevailing role in the drought-induced decrease in photosynthesis. The drought-sensitive metabolism of the C4 plants could explain the observed slower recovery of photosynthesis on re-watering, in comparison with C3 plants which recovered a greater proportion of photosynthesis through increased stomatal conductance. CONCLUSIONS Within the Panicoid grasses, C4 (NADP-ME) species are metabolically more sensitive to drought than C3 species and recover more slowly from drought.

Drought limitation of photosynthesis differs between C3 and C4 grass species in a comparative experiment

Phylogenetic analyses show that C₄ grasses typically occupy drier habitats than their C₃ relatives, but recent experiments comparing the physiology of closely related C₃ and C₄ species have shown that advantages of C₄ photosynthesis can be lost under drought. We tested the generality of these paradoxical findings in grass species representing the known evolutionary diversity of C₄ NADP-me and C₃ photosynthetic types. Our experiment investigated the effects of drought on leaf photosynthesis, water potential, nitrogen, chlorophyll content and mortality. C₄ grasses in control treatments were characterized by higher CO₂ assimilation rates and water potential, but lower stomatal conductance and nitrogen content. Under drought, stomatal conductance declined more dramatically in C₃ than C₄ species, and photosynthetic water-use and nitrogen-use efficiency advantages held by C₄ species under control conditions were each diminished by 40%. Leaf mortality was slightly higher in C₄ than C₃ grasses, but leaf condition under drought otherwise showed no dependence on photosynthetic-type. This phylogenetically controlled experiment suggested that a drought-induced reduction in the photosynthetic performance advantages of C₄ NADP-me relative to C₃ grasses is a general phenomenon.

The growth responses of coastal dune species are determined by nutrient limitation and sand burial

Past work suggests that burial and low nutrient availability limit the growth and zonal distribution of coastal dune plants. Given the importance of these two factors, there is a surprising lack of field investigations of the interactions between burial and nutrient availability. This study aims to address this issue by measuring the growth responses of four coastal dune plant species to these two factors and their interaction. Species that naturally experience either high or low rates of burial were selected and a factorial burial by nutrient addition experiment was conducted. Growth characteristics were measured in order to determine which characteristics allow a species to respond to burial. Species that naturally experience high rates of burial (Arctotheca populifolia and Scaevola plumieri) displayed increased growth when buried, and this response was nutrient-limited. Stable-dune species had either small (Myrica cordifolia, N-fixer) or negligible responses to burial (Metalasia muricata), and were not nutrient-limited. This interspecific difference in response to burial and/or fertiliser is consistent with the idea that burial maintains the observed zonation of species on coastal dunes. Species that are unable to respond to burial are prevented from occupying the mobile dunes. Species able to cope with high rates of burial had high nitrogen-use efficiencies and low dry mass costs of production, explaining their ability to respond to burial under nutrient limitation. The interaction between burial and nutrient limitation is understudied but vital to understanding the zonation of coastal dune plant species.

A molecular phylogeny of the genus Alloteropsis (Panicoideae, Poaceae) suggests an evolutionary reversion from C4 to C3 photosynthesis.

Background and Aims The grass Alloteropsis semialata is the only plant species with both C3 and C4 subspecies. It therefore offers excellent potential as a model system for investigating the genetics, physiology and ecological significance of the C4 photosynthetic pathway. Here, a molecular phylogeny of the genus Alloteropsis is constructed to: (a) confirm the close relationship between the C3 and C4 subspecies of A. semialata; and (b) infer evolutionary relationships between species within the Alloteropsis genus. Methods The chloroplast gene ndhF was sequenced from 12 individuals, representing both subspecies of A. semialata and all four of the other species in the genus. ndhF sequences were added to those previously sequenced from the Panicoideae, and used to construct a phylogenetic tree. Key Results The phylogeny confirms that the two subspecies of A. semialata are among the most recently diverging lineages of C3 and C4 taxa currently recognized within the Panicoideae. Furthermore, the position of the C3 subspecies of A. semialata within the Alloteropsis genus is consistent with the hypothesis that its physiology represents a reversion from C4 photosynthesis. The data point to a similar evolutionary event in the Panicum stenodes–P. caricoides–P. mertensii clade. The Alloteropsis genus is monophyletic and occurs in a clade with remarkable diversity of photosynthetic biochemistry and leaf anatomy. Conclusions These results confirm the utility of A. semialata as a model system for investigating C3 and C4 physiology, and provide molecular data that are consistent with reversions from C4 to C3 photosynthesis in two separate clades. It is suggested that further phylogenetic and functional investigations of the Alloteropsis genus and closely related taxa are likely to shed new light on the mechanisms and intermediate stages underlying photosynthetic pathway evolution.

Physiological advantages of C4 grasses in the field: a comparative experiment demonstrating the importance of drought

Global climate change is expected to shift regional rainfall patterns, influencing species distributions where they depend on water availability. Comparative studies have demonstrated that C4 grasses inhabit drier habitats than C3 relatives, but that both C3 and C4 photosynthesis are susceptible to drought. However, C4 plants may show advantages in hydraulic performance in dry environments. We investigated the effects of seasonal variation in water availability on leaf physiology, using a common garden experiment in the Eastern Cape of South Africa to compare 12 locally occurring grass species from C4 and C3 sister lineages. Photosynthesis was always higher in the C4 than C3 grasses across every month, but the difference was not statistically significant during the wettest months. Surprisingly, stomatal conductance was typically lower in the C3 than C4 grasses, with the peak monthly average for C3 species being similar to that of C4 leaves. In water-limited, rain-fed plots, the photosynthesis of C4 leaves was between 2.0 and 7.4 μmol m−2 s−1 higher, stomatal conductance almost double, and transpiration 60% higher than for C3 plants. Although C4 average instantaneous water-use efficiencies were higher (2.4–8.1 mmol mol−1) than C3 averages (0.7–6.8 mmol mol−1), differences were not as great as we expected and were statistically significant only as drought became established. Photosynthesis declined earlier during drought among C3 than C4 species, coincident with decreases in stomatal conductance and transpiration. Eventual decreases in photosynthesis among C4 plants were linked with declining midday leaf water potentials. However, during the same phase of drought, C3 species showed significant decreases in hydrodynamic gradients that suggested hydraulic failure. Thus, our results indicate that stomatal and hydraulic behaviour during drought enhances the differences in photosynthesis between C4 and C3 species. We suggest that these drought responses are important for understanding the advantages of C4 photosynthesis under field conditions.

Photosynthetic innovation broadens the niche within a single species.

Adaptation to changing environments often requires novel traits, but how such traits directly affect the ecological niche remains poorly understood. Multiple plant lineages have evolved C4 photosynthesis, a combination of anatomical and biochemical novelties predicted to increase productivity in warm and arid conditions. Here, we infer the dispersal history across geographical and environmental space in the only known species with both C4 and non-C4 genotypes, the grass Alloteropsis semialata. While non-C4 individuals remained confined to a limited geographic area and restricted ecological conditions, C4 individuals dispersed across three continents and into an expanded range of environments, encompassing the ancestral one. This first intraspecific investigation of C4 evolutionary ecology shows that, in otherwise similar plants, C4 photosynthesis does not shift the ecological niche, but broadens it, allowing dispersal into diverse conditions and over long distances. Over macroevolutionary timescales, this immediate effect can be blurred by subsequent specialisation towards more extreme niches.

Determinants of flammability in savanna grass species.

Summary Tropical grasses fuel the majority of fires on Earth. In fire‐prone landscapes, enhanced flammability may be adaptive for grasses via the maintenance of an open canopy and an increase in spatiotemporal opportunities for recruitment and regeneration. In addition, by burning intensely but briefly, high flammability may protect resprouting buds from lethal temperatures. Despite these potential benefits of high flammability to fire‐prone grasses, variation in flammability among grass species, and how trait differences underpin this variation, remains unknown. By burning leaves and plant parts, we experimentally determined how five plant traits (biomass quantity, biomass density, biomass moisture content, leaf surface‐area‐to‐volume ratio and leaf effective heat of combustion) combined to determine the three components of flammability (ignitability, sustainability and combustibility) at the leaf and plant scales in 25 grass species of fire‐prone South African grasslands at a time of peak fire occurrence. The influence of evolutionary history on flammability was assessed based on a phylogeny built here for the study species. Grass species differed significantly in all components of flammability. Accounting for evolutionary history helped to explain patterns in leaf‐scale combustibility and sustainability. The five measured plant traits predicted components of flammability, particularly leaf ignitability and plant combustibility in which 70% and 58% of variation, respectively, could be explained by a combination of the traits. Total above‐ground biomass was a key driver of combustibility and sustainability with high biomass species burning more intensely and for longer, and producing the highest predicted fire spread rates. Moisture content was the main influence on ignitability, where species with higher moisture contents took longer to ignite and once alight burnt at a slower rate. Biomass density, leaf surface‐area‐to‐volume ratio and leaf effective heat of combustion were weaker predictors of flammability components. Synthesis. We demonstrate that grass flammability is predicted from easily measurable plant functional traits and is influenced by evolutionary history with some components showing phylogenetic signal. Grasses are not homogenous fuels to fire. Rather, species differ in functional traits that in turn demonstrably influence flammability. This diversity is consistent with the idea that flammability may be an adaptive trait for grasses of fire‐prone ecosystems.