Raymond J. Carpenter

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 systems 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.

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.

LEAF CUTICULAR MORPHOLOGY LINKS PLATANACEAE AND PROTEACEAE

The leaf cuticular morphology of extant species of Platanus was investigated using light and scanning electron microscopy. All species are shown to possess trichome bases of the same type as those commonly found in Proteaceae. Of particular significance are compound forms that consist of an annular surface scar associated with more than one underlying epidermal cell. These are found on the adaxial leaf surfaces of all species of Platanus and are also clearly evident on the abaxial surface of Platanus orientalis. This type of trichome base is therefore interpreted as the first detected nonreproductive morphological synapomorphy linking Proteaceae and Platanaceae. Also, the laterocytic, sometimes paracytic, or anomocytic arrangement of subsidiary cells in Platanus is distinct from the general state in Proteaceae, which is brachyparacytic and presumably derived. In Bellendena, possibly the most basal genus of extant Proteaceae, subsidiary cell arrangements resemble those of Platanus. These results are discussed with respect to leaf fossil records of Proteales, where it is concluded that the combination of brachyparacytic stomata and compound trichome bases is strong evidence for Proteaceae.

Ptilophyllum muelleri (Ettingsh.) comb. nov. from the Oligocene of Australia: Last of the Bennettitales?

Several small pinnate leaves of early Oligocene age from Cethana, Tasmania, are newly described and found to be conspecific with Anomozamites muelleri Ettingsh. recorded from coeval strata at Emmaville, northern New South Wales. These fossils are most probably referable to the Bennettitales on the basis of leaf size, leaflet shape, and venation patterns, in the absence of diagnostic cuticular details. They are transferred to Ptilophyllum on the basis of leaflet morphology and represent the youngest putative bennettitalean remains yet documented. Their occurrence reinforces previous arguments that the highest-paleolatitude fragments of southeastern Gondwana provided moist temperate refugia for the survival of Mesozoic gymnosperm taxa well into the Cenozoic.

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.

No snow in the mountains: Early Eocene plant fossils from Hotham Heights, Victoria, Australia

An Early Eocene plant assemblage from near the summit of Mt Hotham, Victoria, is described, using a combination of macro- and microfossils, especially cuticles. This is important since no other Australian macrofossil sites from this time, when environmental conditions are believed to have been the warmest of the Cenozoic, have been described in detail. The nature of the flora and vegetation supports geological evidence that the site was upland (approximately 800 m above sea level) at this time, with climatic conditions similar to those now experienced in regions such as the Atherton Tablelands in Queensland and mid-montane Papua New Guinea. The vegetation was probably a form of rainforest dominated by mesotherm elements, with abundant ferns including Gleicheniaceae and the tree ferns Cnemidaria, Cyathea and Dicksonia. Gymnosperms included Araucariaceae (Agathis) and Podocarpaceae (at least Acmopyle and Dacrydium). Angiosperms were diverse in Lauraceae (at least nine species including probably Cryptocarya, Endiandra and Litsea) and Proteaceae (at least nine species including probably Musgravea and Darlingia). Other angiosperms included Cunoniaceae, Gymnostoma (Casuarinaceae), Diospyros-like Ebenaceae, and the vine Cissocarpus (Vitaceae). Nothofagus was rare or absent from the Mt Hotham region at this time, as no macrofossil evidence was found, and pollen percentages were very low.

Near-tropical early eocene terrestrial temperatures at the Australo-Antarctic margin, western Tasmania

A worldwide greenhouse warm climate prevailed in the Early Eocene, and nowhere was warming more dramatic than at high latitudes. Sea-surface temperatures of ∼34 °C have been estimated for a site at paleolatitude 65°S on the East Tasman Plateau of the southwest Pacific Ocean, but these estimates require independent validation, including from terrestrial proxies. Here we determine a near-tropical terrestrial mean annual temperature estimate of ∼24 °C at sea level for an Early Eocene site in Tasmania, Australia, using three proxies based on well-dated estuarine plant fossils. This estimate is lower than the nearby sea estimates to the east, but similarly suggests that, as in the southwest Pacific, Early Eocene climates in the eastern Australo-Antarctic region were warmer than inferred elsewhere at high latitudes, including on the Antarctic Peninsula. Such data are essential for improving our understanding of climatic and biotic evolution in the Southern Hemisphere.

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.

Early Tertiary Macrofossils of Proteaceae from Tasmania

Proteaceous leaves from two Early Tertiary sites in Tasmania are described and discussed. Based on gross leaf morphological and cuticular characters, 15 species are recognised from Oligocene lacustrine sediments at Cethana. Specimens of two taxa are not distinguishable from the extant species Telopea truncata from Tasmania and Lomatia fraxinifolia from north-eastern Queensland, and are therefore assigned to these species. Two new species of Banksieaephyllum are recognised. Ten other taxa are difficult to identify to existing genera, and are therefore referred to a new genus Proteaciphyllum. They all possess features typical of subfamily Grevilleoideae. Other, less well preserved, but probable Proteaceae from Cethana are also described. Specimens from the Leven River deposit, probably also of Oligocene age, are assigned to a new species of Orites, O. excelsoides. This species is closely related to extant O. excelsa from rainforests of north-eastern New South Wales and north-eastern Queensland. Cethana has by far the highest diversity of Proteaceae of any fossil flora described to date. The fossils also demonstrate the past association of now geographically remote taxa, and the prevalence of sclero- and xero-morphy in the family by the Oligocene.

Banksieaephyllum taylorii (Proteaceae) from the Late Paleocene of New South Wales and its relevance to the origin of Australia's scleromorphic flora

Leaf specimens from Late Paleocene sediments in New South Wales are assigned to a new species of Banksieaephyllum, B. taylorii. In gross morphology the leaves are indistinguishable from those of extant Dryandra formosa, and similar to a few other species of Dryandra and Banksia. These species have pinnately lobed leaves and are now confined to south-western Australia. In cuticular morphology, B. taylorii is most similar to Banksia species from subgenus Banksia, section Oncostylis. One species in this section, B. dryandroides, also has pinnately lobed leaves. The fossil specimens demonstrate that subtribe Banksiinae had differentiated by the Late Paleocene and represent the earliest record of angiosperm scleromorphy in Australia to date. The superficial placement of the stomates compared with most modem Banksiinae supports the hypothesis that xeromorphy in this group generally increased in response to the development of less mesic climates in the Late Tertiary.