Philip K. Groom

The worldwide leaf economics spectrum

Bringing together leaf trait data spanning 2,548 species and 175 sites we describe, for the first time at global scale, a universal spectrum of leaf economics consisting of key chemical, structural and physiological properties. The spectrum runs from quick to slow return on investments of nutrients and dry mass in leaves, and operates largely independently of growth form, plant functional type or biome. Categories along the spectrum would, in general, describe leaf economic variation at the global scale better than plant functional types, because functional types overlap substantially in their leaf traits. Overall, modulation of leaf traits and trait relationships by climate is surprisingly modest, although some striking and significant patterns can be seen. Reliable quantification of the leaf economics spectrum and its interaction with climate will prove valuable for modelling nutrient fluxes and vegetation boundaries under changing land-use and climate.

Phosphorus accumulation in Proteaceae seeds: a synthesis.

The family Proteaceae dominates the nutrient-poor, Mediterranean-climate floristic regions of southwestern Australia (SWA) and the Cape of South Africa. It is well-recognised that mediterranean Proteaceae have comparatively large seeds that are enriched with phosphorus (P), stored mainly as salts of phytic acid in protein globoids. Seed P can contribute up to 48% of the total aboveground P, with the fraction allocated depending on the species fire response. For SWA species, 70–80% of P allocated to fruiting structures is invested in seeds, compared with 30–75% for Cape species, with SWA species storing on average 4.7 times more P per seed at twice the concentration. When soil P is less limiting for growth, seed P reserves may be less important for seedling establishment, and hence plants there tend to produce smaller seeds with less P. For Australian Hakea and Grevillea species the translocation of P from the fruit wall to the seed occurs in the days/weeks before final fruit dry mass is reached, and accounts for 4–36% of seed P. Seed P content increases with the level of serotiny, though it decreases marginally as a fraction of the total reproductive structure. The greater occurrence of serotiny and higher seed P content within the Proteaceae in SWA supports the notion that SWA soils are more P-impoverished than those of the Cape.

SEED AND SEEDLING BIOLOGY OF THE WOODY-FRUITED PROTEACEAE

Within the Proteaceae, 353 species confined to 7 genera in the Grevilleoideae have woody fruits. The majority (> 70%) occur in fire-prone vegetation on nutrient-poor, summer-dry soils of south-western Australia. These species are characterised by large, winged seeds contained within serotinous follicles. Seed release is mediated by desiccation of the follicle walls resulting from fruit death, although wet–dry cycles are required in some genera. After release, germination must take place by the next wet season, as the seeds are not long-lived. Seeds are particularly high in protein (40–60%), P (1–2%) and Fe (10–60‰) compared with other Proteaceae. Seeds are favoured food for pre- and post-dispersal granivores (insects, birds, rodents) and young seedlings are favoured by herbivores (insects, marsupials), with the more serotinous fruits providing extra protection for their seeds. Successful establishment is facilitated by the protective and water retentive role of the testa during germination, and the remobilisation of N and P from the cotyledons to the seedling within 10 weeks of emergence. Drought stress reduces seedling establishment in otherwise favourable postfire microsites and prevents it (assisted by herbivores) in mature vegetation. Typically, < 10% of seeds released after fire become seedlings, and < 50% of these survive the first summer. Among fire-killed species, species that produce few seeds are more likely to have drought-resistant seedlings, often associated with larger seeds and/or needle-shaped leaves. Species that resprout after fire produce a few large viable seeds per plant, whereas fire-killed species produce many smaller seeds. Of all the Proteaceae, the ecology of woody-fruited species is best known, providing great scope for comparative biology studies.

Influence of Leaf Type and Plant Age on Leaf Structure and Sclerophylly in Hakea (Proteaceae)

Hakea Schrader (Proteaceae) species possess one of two contrasting leaf morphologies—broad or terete. Terete leaves are either simple (needle-like) or two- or three-pronged, and are further characterised by their greater thickness (> 1 mm), smaller projected area and mass, higher mass per unit area (a measure of sclerophylly) and lower density than broad leaves. Broad leaves are much more variable in their morphology, ranging from narrow-linear to fan-shaped or ovoid-elliptic, and may be flat, undulate, shell-shaped or spiralled. The greater thickness and sclerophylly of terete leaves can be partially attributed to the presence of a prominent, thick-walled parenchyma core and increased palisade thickness. The core contains a compact conduit of fibre-capped vascular bundles. The sclerophyllous nature of broad leaves is due to their high density, attributable to their thin palisade and large fibre caps surrounding the main vascular bundles. Both leaf types have a thick cuticle (> 20 µm) in mature plants, and sunken stomates, with terete leaves possessing a greater stomatal density than broad leaves. Both leaf types are isolateral and hence amphistomatous. Within a species, adult and seedling leaves having a similar leaf type differ morphologically rather than anatomically, with an overall increase in leaf thickness and higher levels of sclerophylly in adult leaves. Some species produce broad seedling leaves that are eventually replaced by terete adult leaves.

Heat damage in sclerophylls is influenced by their leaf properties and plant environment

Abstract: Mediterranean southwestern Australia experienced two successive days of extreme (> 45 °C) maximum temperatures and hot winds during the summer of 1991, resulting in adult mortality and extensive crown damage in a sclerophyllous mallee-heathland. To investigate the relationship between leaf attributes, plant environment, and heat tolerance in sclerophylls, measurements of plant height, leaf clustering, leaf morphology (thickness, dry density, area, perimeter/area ratio), percentage crown damage, and percentage mortality, and categories of exposure to wind, shade, and bare soils were recorded for 40 heat-damaged and 14 undamaged co-occurring species. Analyzing the entire dataset by principal components analysis showed that undamaged species had thicker leaves (on average 61% thicker) than species with damaged leaves and were more exposed to wind, sun, and bare soil. Thicker leaves are a common response to hot, dry, and more exposed environments and are more heat tolerant than thinner leaves. A separate analysis of the Proteaceae (25 damaged and six undamaged species) showed a similar trend to the overall dataset. An analysis of the Myrtaceae (10 damaged and three undamaged species) showed that wind exposure and level of shading were the most important variables influencing the degree of leaf damage. Percentage leaf damage was significantly correlated with percentage adult mortality, but not with the ability of a species to regrow (percentage of plants producing new shoots). Differences between undamaged and damaged species may be a result of preconditioning, whereby species growing in more exposed habitats were pre-adapted to tolerate periods of heat stress. It is unlikely that the study species were able to reduce leaf temperatures via transpirational cooling during the hottest part of the 2-d heatwave. The ability of a species to tolerate extreme temperature events will be determined by the interaction between leaf heat loads, leaf heat-storing capacity, and the degree of exposure to environmental elements.

Ecogeographical Analysis of Hakea (Proteaceae) in South-Western Australia, With Special Reference to Leaf Morphology and Life Form

The genus Hakea Schrader (Proteaceae) has its world centre of diversity in south-western Australia; the majority (c. 70%) of species are endemic to this region. To examine the distribution of Hakea within south-western Australia, canonical correspondence analysis (CCA) was used on species presence and bioclimatic parameters in 0.5° x0.5° latitude-longitude grid cells. Of the 12 bioclimatic attributes initially applied, annual temperature and rainfall data, and indices of their variation, were best related to species distribution. Clustering of the species (on the CCA ordination) produced five distinct groups (not including species near the origin of the ordination) roughly representing floristic regions of southwestern Australia (Avon, Irwin, Eyre-Roe, southern Darling, northern-central Darling). Species distribution was then related to four morphological groups based on their leaf type (broad, terete) and post-fire life form (non-sprouter, resprouter). The highest percentage of terete-leaved non-sprouters occurred in areas of low-moderate rainfall and large annual temperature ranges (Avon and Eyre-Roe clusters), whereas terete-leaved resprouters displayed a very patchy distribution, accounting for less than 20% of the hakeas present in most of the grid cells. Broad-leaved resprouters dominated areas of strongly seasonal rainfall (Irwin and northern-central Darling clusters), with few species occurring in the drier Avon and Eyre-Roe districts. Broad-leaved non-sprouters were best represented in areas of low annual temperature (southern Darling and Eyre-Roe clusters). The distribution of non-sprouters and resprouters may be due to climatic factors affecting seedling recruitment and/or fire frequencies. Leaf morphology appears to be more directly related to species distribution, as broad leaves are favoured in regions of medium-high, seasonal rainfall (less stressful habitats) while terete leaves are better adapted to tolerate hot, dry environments.

Contrasting morphology and ecophysiology of co-occurring broad and terete leaves in Hakea trifurcata (Proteaceae)

We studied the morphology, anatomy, phyllotaxy and daily seasonal ecophysiology of the two leaf types (broad and terete) of Hakea trifurcata (Smith) R.Br., a widespread shrub in south-western Australia. Both leaf types may be present on the same branchlet, with one or two broad leaves forming first during the annual growth period (late winter) followed by many terete leaves in spring. Terete leaves were more xeromorphic than broad leaves, including greater thickness, denser tissues and fewer veins. Broad leaves fixed more carbon and transpired more water per unit mass than terete leaves, in a well ventilated leaf chamber, and had lower (more negative) xylem pressure potentials. Broad leaf temperatures only exceeded those of terete leaves under hot, dry conditions, with no relationship between transpiration rates and leaf temperature. Terete leaves possessed many structural and physiological characteristics commonly associated with drought-tolerant leaves, whereas broad leaves were characteristic of leaves which keep their stomates open during periods of water and heat stress. Both leaf types appear to increase the fitness of this species in a mediterranean climate, with broad leaves having the potential to supply extra photosynthates and nutrients to the new seasons growth.

Regional and local effects on reproductive allocation in epicormic and lignotuberous populations of Banksia menziesii

Reproductive allocation (RA) is a measure of how resources (biomass, nutrients) are partitioned between reproductive structures and the rest of the plant. For plants that resprout after fire, the percentage of resources allocated to reproduction may vary depending on their resprouting ability. Our study examines the percentage RA (biomass, N, P, K) and nutrient content of current season’s growth in southern (Swan Coastal Plain) epicormic and northern (Eneabba Plain) lignotuberous resprouter populations of Banksia menziesii (Proteaceae), a species endemic to nutrient-impoverished sandplains of southwestern Australia. Within each population, plants along road edges were compared with plants not associated with road edges. There was no difference in total nutrient content of current year’s growth between both resprouting types, except that total K in the shoots of lignotuberous populations was >2 times that in the epicormic populations. Non-road lignotuberous plants allocated twice the biomass, N and P, and 13.5 times the K, to reproduction as non-road epicormic plants. Lignotuberous populations had the highest RA (17–34% of biomass, N, P, K), with non-road epicormic populations the lowest RA (3–15%). This can be viewed as an adaptive (ultimate) response to the poorer postfire survival and recruitment conditions where the lignotuberous populations occur. Total biomass and nutrient content of road-edge plants was 2–3 times that of non-edge plants. Lignotuberous populations in both road positions allocated the same fraction of biomass, N and P to reproduction, whereas road-edge populations allocated 10% less K than non-road. Road-edge epicormic populations allocated 5–10% more biomass, N, P and K to reproduction than non-road populations. This can be viewed as an ecophysiological (proximate) response to the better growing conditions created by the roadways that may also ultimately have an adaptive explanation.

A Trade-off between Fecundity and Drought Susceptibility in Adults and Seedlings of Hakea Species as Influenced by Leaf Morphology

Successful seedling recruitment is vital for the persistence of fire-killed species in a community. Maximising seed and seedling production (fecundity) and the ability of adults and seedlings to survive summer drought are crucial in taking advantage of post-fire recruitment opportunities. In this study, the fecundity (seed and seedling production), mortality and water relations of fire-killed Hakea species with contrasting leaf morphologies (broad and terete) were examined over 2 consecutive years of exceptionally low rainfall at two sites, to investigate possible trade-offs between drought susceptibility (as influenced by leaf morphology) and fecundity of a species. Adult mortality was high in the broad-leaved species (H. smilacifolia Meissn. and H. undulata R.Br.) and low in terete-leaved species (H. erinacea Meissn., H. circumalata Meissn. and H. polyanthema Diels) with high transpiration rates (broad-leaved species) associated with greater plant death. Only H. smilacifolia had proportionally greater fecundity to compensate for high adult mortality. Seedling mortality increased proportionally with higher initial seedling : parent ratios (adult fecundity). Lowest mortality was for the terete-leaved species, apparently achieved by means of a combination of drought avoidance and tolerance mechanisms. Hakea undulata seedlings had the highest mean leaf area, but mortality was highest in H. smilacifolia. Thus, for seedlings, leaf morphology was not as strongly related to drought susceptibility as it was for adults.

Contribution of transition and stabilization processes to speciation is a function of the ancestral trait state and selective environment in Hakea

Currently the origin and trajectories of novel traits are emphasised in evolutionary studies, the role of stabilization is neglected, and interpretations are often post hoc rather than as hypothesised responses to stated agents of selection. Here we evaluated the impact of changing environmental conditions on trait evolution and stabilization and their relative contribution to diversification in a prominent Australian genus, Hakea (Proteaceae). We assembled a time-based phylogeny for Hakea, reconstructed its ancestral traits for six attributes and determined their evolutionary trajectories in response to the advent or increasing presence of fire, seasonality, aridity, nectar-feeding birds and (in)vertebrate herbivores/granivores. The ancestral Hakea arose 18 million years ago (Ma) and was broad-leaved, non-spinescent, insect-pollinated, had medium-sized, serotinous fruits and resprouted after fire. Of the 190 diversification events that yielded the 82 extant species analysed, 8–50% involved evolution, stabilization or re-evolution (reversal) of individual novel traits. Needle leaves appeared 14 Ma and increased through the Neogene/Quaternary coinciding with intensifying seasonality and aridity. Spinescence arose 12 Ma consistent with the advent of vertebrate herbivores. Bird-pollination appeared 14 Ma in response to advent of the Meliphagidae in the early Miocene. Small and large woody fruits evolved from 12 Ma as alternative defenses against granivory. Fire-caused death evolved 14 Ma, accounting for 50% of subsequent events, as fire became less stochastic. Loss of serotiny began in the late Miocene as non-fireprone habitats became available but only contributed 8% of events. Innovation and subsequent stabilization of functional traits promoted the overall species diversification rate in Hakea by 15 times such that only three species now retain the ancestral phenotype. Our approach holds great promise for understanding the processes responsible for speciation of organisms when the ancestral condition can be identified and the likely selective agents are understood.