AusTraits, a curated plant trait database for the Australian flora.

We introduce the AusTraits database - a compilation of values of plant traits for taxa in the Australian flora (hereafter AusTraits). AusTraits synthesises data on 448 traits across 28,640 taxa from field campaigns, published literature, taxonomic monographs, and individual taxon descriptions. Traits vary in scope from physiological measures of performance (e.g. photosynthetic gas exchange, water-use efficiency) to morphological attributes (e.g. leaf area, seed mass, plant height) which link to aspects of ecological variation. AusTraits contains curated and harmonised individual- and species-level measurements coupled to, where available, contextual information on site properties and experimental conditions. This article provides information on version 3.0.2 of AusTraits which contains data for 997,808 trait-by-taxon combinations. We envision AusTraits as an ongoing collaborative initiative for easily archiving and sharing trait data, which also provides a template for other national or regional initiatives globally to fill persistent gaps in trait knowledge.

Links between environment and stomatal size through evolutionary time in Proteaceae.

The size of plant stomata (adjustable pores that determine the uptake of CO2 and loss of water from leaves) is considered to be evolutionarily important. This study uses fossils from the major Southern Hemisphere family Proteaceae to test whether stomatal cell size responded to Cenozoic climate change. We measured the length and abundance of guard cells (the cells forming stomata), the area of epidermal pavement cells, stomatal index and maximum stomatal conductance from a comprehensive sample of fossil cuticles of Proteaceae, and extracted published estimates of past temperature and atmospheric CO2. We developed a novel test based on stochastic modelling of trait evolution to test correlations among traits. Guard cell length increased, and stomatal density decreased significantly with decreasing palaeotemperature. However, contrary to expectations, stomata tended to be smaller and more densely packed at higher atmospheric CO2. Thus, associations between stomatal traits and palaeoclimate over the last 70 million years in Proteaceae suggest that stomatal size is significantly affected by environmental factors other than atmospheric CO2. Guard cell length, pavement cell area, stomatal density and stomatal index covaried in ways consistent with coordinated development of leaf tissues.

Fossil evidence for open, Proteaceae-dominated heathlands and fire in the Late Cretaceous of Australia.

PREMISE OF THE STUDY: The origin of biomes is of great interest globally. Molecular phylogenetic and pollen evidence suggest that several plant lineages that now characterize open, burnt habitats of the sclerophyll biome, became established during the Late Cretaceous of Australia. However, whether this biome itself dates to that time is problematic, fundamentally because of the near-absence of relevant, appropriately aged, terrestrial plant macro- or mesofossils. METHODS: We recovered, identified, and interpreted the ecological significance of fossil pollen, foliar and other remains from a section of core drilled in central Australia, which we dated as Late Campanian-Maastrichtian. KEY RESULTS: The sediments contain plant fossils that indicate nutrient-limited, open, sclerophyllous vegetation and abundant charcoal as evidence of fire. Most interestingly, >30 pollen taxa and at least 12 foliage taxa are attributable to the important Gondwanan family Proteaceae, including several minute, amphistomatic, and sclerophyllous foliage forms consistent with subfamily Proteoideae. Microfossils, including an abundance of Sphagnales and other wetland taxa, provided strong evidence of a fenland setting. The local vegetation also included diverse Ericaceae and Liliales, as well as a range of ferns and gymnosperms. CONCLUSIONS: The fossils provide strong evidence in support of hypotheses of great antiquity for fire and open vegetation in Australia, point to extraordinary persistence of Proteaceae that are now emblematic of the Mediterranean-type climate southwestern Australian biodiversity hotspot and raise the profile of open habitats as centers of ancient lineages.

Environmental adaptation in stomatal size independent of the effects of genome size.

Cell sizes are linked across multiple tissues, including stomata, and this variation is closely correlated with genome size. These associations raise the question of whether generic changes in cell size cause suboptimal changes in stomata, requiring subsequent evolution under selection for stomatal size. We tested the relationships among guard cell length, genome size and vegetation type using phylogenetically independent analyses on 67 species of the ecologically and structurally diverse family, Proteaceae. We also compared how genome and stomatal sizes varied at ancient (among genera) and more recent (within genus) levels. The observed 60-fold range in genome size in Proteaceae largely reflected the mean chromosome size. Compared with variation among genera, genome size varied much less within genera (< 6% of total variance) than stomatal size, implying evolution in stomatal size subsequent to changes in genome size. Open vegetation and closed forest had significantly different relationships between stomatal and genome sizes. Ancient changes in genome size clearly influenced stomatal size in Proteaceae, but adaptation to habitat strongly modified the genome-stomatal size relationship. Direct adaptation to the environment in stomatal size argues that new proxies for past concentrations of atmospheric CO2 that incorporate stomatal size are superior to older models based solely on stomatal frequency.

Paleo-Antarctic rainforest into the modern Old World tropics: the rich past and threatened future of the "southern wet forest survivors".

UNLABELLED: • PREMISE OF STUDY: Have Gondwanan rainforest floral associations survived? Where do they occur today? Have they survived continuously in particular locations? How significant is their living floristic signal? We revisit these classic questions in light of significant recent increases in relevant paleobotanical data.• METHODS: We traced the extinction and persistence of lineages and associations through the past across four now separated regions-Australia, New Zealand, Patagonia, and Antarctica-using fossil occurrence data from 63 well-dated Gondwanan rainforest sites and 396 constituent taxa. Fossil sites were allocated to four age groups: Cretaceous, Paleocene-Eocene, Neogene plus Oligocene, and Pleistocene. We compared the modern and ancient distributions of lineages represented in the fossil record to see if dissimilarity increased with time. We quantified similarity-dissimilarity of composition and taxonomic structure among fossil assemblages, and between fossil and modern assemblages.• KEY RESULTS: Strong similarities between ancient Patagonia and Australia confirmed shared Gondwanan rainforest history, but more of the lineages persisted in Australia. Samples of ancient Australia grouped with the extant floras of Australia, New Guinea, New Caledonia, Fiji, and Mt. Kinabalu. Decreasing similarity through time among the regional floras of Antarctica, Patagonia, New Zealand, and southern Australia reflects multiple extinction events.• CONCLUSIONS: Gondwanan rainforest lineages contribute significantly to modern rainforest community assembly and often co-occur in widely separated assemblages far from their early fossil records. Understanding how and where lineages from ancient Gondwanan assemblages co-occur today has implications for the conservation of global rainforest vegetation, including in the Old World tropics.

Early evidence of xeromorphy in angiosperms: stomatal encryption in a new eocene species of Banksia (Proteaceae) from Western Australia.

UNLABELLED: • PREMISE OF THE STUDY: Globally, the origins of xeromorphic traits in modern angiosperm lineages are obscure but are thought to be linked to the early Neogene onset of seasonally arid climates. Stomatal encryption is a xeromorphic trait that is prominent in Banksia, an archetypal genus centered in one of the world's most diverse ecosystems, the ancient infertile landscape of Mediterranean-climate southwestern Australia.• METHODS: We describe Banksia paleocrypta, a sclerophyllous species with encrypted stomata from silcretes of the Walebing and Kojonup regions of southwestern Australia dated as Late Eocene.• KEY RESULTS: Banksia paleocrypta shows evidence of foliar xeromorphy ∼20 Ma before the widely accepted timing for the onset of aridity in Australia. Species of Banksia subgenus Banksia with very similar leaves are extant in southwestern Australia. The conditions required for silcrete formation infer fluctuating water tables and climatic seasonality in southwestern Australia in the Eocene, and seasonality is supported by the paucity of angiosperm closed-forest elements among the fossil taxa preserved with B. paleocrypta. However, climates in the region during the Eocene are unlikely to have experienced seasons as hot and dry as present-day summers.• CONCLUSIONS: The presence of B. paleocrypta within the center of diversity of subgenus Banksia in edaphically ancient southwestern Australia is consistent with the continuous presence of this lineage in the region for ≥40 Ma, a testament to the success of increasingly xeromorphic traits in Banksia over an interval in which numerous other lineages became extinct.

First evidence for Wollemi Pine-type pollen (Dilwynites: Araucariaceae) in South America.

We report the first fossil pollen from South America of the lineage that includes the recently discovered, extremely rare Australian Wollemi Pine, Wollemia nobilis (Araucariaceae). The grains are from the late Paleocene to early middle Eocene Ligorio Márquez Formation of Santa Cruz, Patagonia, Argentina, and are assigned to Dilwynites, the fossil pollen type that closely resembles the pollen of modern Wollemia and some species of its Australasian sister genus, Agathis. Dilwynites was formerly known only from Australia, New Zealand, and East Antarctica. The Patagonian Dilwynites occurs with several taxa of Podocarpaceae and a diverse range of cryptogams and angiosperms, but not Nothofagus. The fossils greatly extend the known geographic range of Dilwynites and provide important new evidence for the Antarctic region as an early Paleogene portal for biotic interchange between Australasia and South America.

Unified changes in cell size permit coordinated leaf evolution.

The processes by which the functions of interdependent tissues are coordinated as lineages diversify are poorly understood. Here, we examine evolutionary coordination of vascular, epidermal and cortical leaf tissues in the anatomically, ecologically and morphologically diverse woody plant family Proteaceae. We found that, across the phylogenetic range of Proteaceae, the sizes of guard, epidermal, palisade and xylem cells were positively correlated with each other but negatively associated with vein and stomatal densities. The link between venation and stomata resulted in a highly efficient match between potential maximum water loss (determined by stomatal conductance) and the leaf vascular system's capacity to replace that water. This important linkage is likely to be driven by stomatal size, because spatial limits in the packing of stomata onto the leaf surface apparently constrain the maximum size and density of stomata. We conclude that unified evolutionary changes in cell sizes of independent tissues, possibly mediated by changes in genome size, provide a means of substantially modifying leaf function while maintaining important functional links between leaf tissues. Our data also imply the presence of alternative evolutionary strategies involving cellular miniaturization during radiation into closed forest, and cell size increase in open habitats.

Testing the impact of calibration on molecular divergence times using a fossil-rich group: the case of Nothofagus (Fagales).

Although temporal calibration is widely recognized as critical for obtaining accurate divergence-time estimates using molecular dating methods, few studies have evaluated the variation resulting from different calibration strategies. Depending on the information available, researchers have often used primary calibrations from the fossil record or secondary calibrations from previous molecular dating studies. In analyses of flowering plants, primary calibration data can be obtained from macro- and mesofossils (e.g., leaves, flowers, and fruits) or microfossils (e.g., pollen). Fossil data can vary substantially in accuracy and precision, presenting a difficult choice when selecting appropriate calibrations. Here, we test the impact of eight plausible calibration scenarios for Nothofagus (Nothofagaceae, Fagales), a plant genus with a particularly rich and well-studied fossil record. To do so, we reviewed the phylogenetic placement and geochronology of 38 fossil taxa of Nothofagus and other Fagales, and we identified minimum age constraints for up to 18 nodes of the phylogeny of Fagales. Molecular dating analyses were conducted for each scenario using maximum likelihood (RAxML + r8s) and Bayesian (BEAST) approaches on sequence data from six regions of the chloroplast and nuclear genomes. Using either ingroup or outgroup constraints, or both, led to similar age estimates, except near strongly influential calibration nodes. Using "early but risky" fossil constraints in addition to "safe but late" constraints, or using assumptions of vicariance instead of fossil constraints, led to older age estimates. In contrast, using secondary calibration points yielded drastically younger age estimates. This empirical study highlights the critical influence of calibration on molecular dating analyses. Even in a best-case situation, with many thoroughly vetted fossils available, substantial uncertainties can remain in the estimates of divergence times. For example, our estimates for the crown group age of Nothofagus varied from 13 to 113 Ma across our full range of calibration scenarios. We suggest that increased background research should be made at all stages of the calibration process to reduce errors wherever possible, from verifying the geochronological data on the fossils to critical reassessment of their phylogenetic position.

Leaf fossils of the ancient Tasmanian relict Microcachrys (Podocarpaceae) from New Zealand.

PREMISE OF THE STUDY: Microcachrys tetragona (Podocarpaceae), endemic to the mountains of Tasmania, represents the only remaining taxon of one of the world's most ancient and widely distributed conifer lineages. Remarkably, however, despite its ∼150 Myr heritage, our understanding of the fossil history of this lineage is based almost entirely on the pollen record. Fossils of Microcachrys are especially important in light of recent molecular phylogenetic and dating evidence. This evidence dates the Microcachrys lineage to the Mesozoic and does not support the traditional placement of Microcachrys as sister to the southeastern Australian genus Pherosphaera. METHODS: We undertook comparative studies of the foliage architecture, cuticle, and paleoecology of newly discovered fossils from the Oligo-Miocene of New Zealand and M. tetragona and discussed the importance of Microcachrys in the context of Podocarpaceae phylogeny. KEY RESULTS: The fossils represent the oldest and first extra-Australian macrofossils of Microcachrys and are described as the new foliage species M. novae-zelandiae. These fossils confirm that the distinctive opposite decussate phyllotaxy of the genus is at least as old as the Oligo-Miocene and contribute to evidence that Microcachrys plants were sometimes important components of oligotrophic swampy habitats. CONCLUSIONS: Leaf fossils of Microcachrys closely comparable with the only extant species confirm that this lineage had a much wider past distribution. The fossil record and recent molecular phylogenetic studies, including that of Microcachrys, also serve to emphasize the important status of Tasmania as a refugium for seed plant lineages.

Leaf fossils of Banksia (Proteaceae) from New Zealand: An Australian abroad.

Fossils can shed new light on plant biogeography and phylogeny. Pinnately lobed leaves from the Oligo-Miocene Newvale lignite mine, South Island, New Zealand are the first extra-Australian leaf fossils of the charismatic genus Banksia (Proteaceae), and they are assigned to a new species, B. novae-zelandiae. Comparison with extant taxa shows that the fossils are best regarded as an extinct stem relative of Banksia because their available features are either plesiomorphic for the genus (notably, the stomata are superficially placed, not sunken in balloon-like pits as in many extant species) or lack evidence of synapomorphies that would enable them to be placed in the crown group. Banksia novae-zelandiae does, however, exhibit two cuticular features that are unique or highly derived for Banksia. These are rugulate subsidiary cell ornamentation and the presence of complex papillae that extensively cover the abaxial leaf surface. The fossils add to the widespread records of the pinnately lobed leaf form in Banksia in Australia beginning in the late Paleocene. This form is now limited to species confined to sclerophyllous heathlands of Mediterranean climate in southwestern Australia. Banksia novae-zelandiae could be part of a lineage that had a long history in New Zealand, perhaps dating to the early Paleogene.

Seed ferns survived the end-Cretaceous mass extinction in Tasmania.

Seed ferns, dominant elements of the vegetation in many parts of the world from the Triassic to Cretaceous, were considered to have disappeared at the end of the Cretaceous together with several other groups that had occupied key positions in terrestrial and marine ecosystems such as dinosaurs, plesiosaurs, and ammonoids. Seed-fern demise is generally correlated with competition from diversifying flowering plants through the Cretaceous and the global environmental crisis related to the Chicxulub impact event in the paleotropics at the end of the period. New fossils from Tasmania show that one seed-fern lineage survived into the Cenozoic by at least 13 million years. These fossils are described here as a new species, Komlopteris cenozoicus. Komlopteris is a genus of seed ferns attributed to Corystospermaceae and until now was not known from sediments younger than the Early Cretaceous. Discovery of this "Lazarus taxon," together with the presence of a range of other relictual fossil and extant organisms in Tasmania, other southern Gondwanan provinces, and some regions of northern North America and Asia, underscores high-latitude regions as biodiversity refugia during global environmental crises and highlights their importance as sources of postextinction radiations.

The evolutionary relations of sunken, covered, and encrypted stomata to dry habitats in Proteaceae.

Sunken, covered, and encrypted stomata have been anecdotally linked with dry climates and reduced transpiration and therefore have been used to infer dry palaeoclimates from fossils. This study assesses the evolutionary and ecological associations of such stomatal protection in a model system-the diverse southern hemisphere family Proteaceae. Analyses were based on the morphology of over 1400 Australian, South African, New Caledonian, New Zealand, and South American species, anatomy of over 300 of these species, and bioclimatic data from all 1109 Australian species. Ancestral state reconstruction revealed that five or six evolutionary transitions explain over 98% of the dry climate species in the family, with a few other, minor invasions of dry climates. Deep encryption, i.e., stomata in deep pits, in grooves, enclosed by tightly revolute margins or strongly overarched by cuticle, evolved at least 11 times in very dry environments. Other forms of stomatal protection (sunken but not closely encrypted stomata, papillae, and layers of hairs covering the stomata) also evolved repeatedly, but had no systematic association with dry climates. These data are evidence for a strong distinction in function, with deep encryption being an adaptation to aridity, whereas broad pits and covered stomata have more complex relations to climate.

Giant cuticular pores in Eidothea zoexylocarya (Proteaceae) leaves.

Ubiquitous, large diameter pores have not previously been adequately demonstrated to occur in leaf cuticles. Here we show conclusively that such structures occur in Eidothea zoexylocarya, a rainforest tree species of Proteaceae restricted to the Australian Wet Tropics. The pores are abundant, large-diameter apertures (∼1 µm), that extend perpendicularly most of the way through the cuticle from the inside. They occur on both sides of the leaf, but are absent from the cuticle associated with stomatal complexes on the abaxial side. No such pores were found in any other species, including the only other species of Eidothea, E. hardeniana from New South Wales, and other species that have previously been purported to possess cuticular pores. To determine whether these pores made the cuticles more leaky to water vapor, we measured astomatous cuticular conductances to water vapor for E. zoexylocarya and seven other Proteaceae species of the Wet Tropics. Cuticular conductance for E. zoexylocarya was relatively low, indicating that the prominent pores do not increase conductance. The function of the pores is currently obscure, but the presence of both pores and an adaxial hypodermis in E. zoexylocarya but not E. hardeniana suggests evolution in response to greater environmental stresses in the tropics.