The Flowering of Australia's Rainforests

Pollination Ecology and Plant Evolution

Geoff Williams

• Publisher: CSIRO PUBLISHING
• Year: 2021
• Print ISBN: 9781486314270
• eBook ISBN: 9781486314294
• Edition: 2
• Topic: Biological Sciences
• Subtopic: Ecology
• Index: Biological Sciences

The Flowering of Australia's Rainforests provides a comprehensive introduction to the pollination ecology, evolution and conservation of Australian rainforest plants, with particular emphasis on subtropical rainforests and their associated pollinators. This significantly expanded second edition includes new information on the impact of climate change, fire, fragmentation and invasive species.

Rainforests continue to be a focus of global conservation concern, not only from threats to biodiversity in general, but to pollinators specifically. Within Australia, this has been emphasised by recent cataclysmic fire impacts, ongoing extreme drought events, and the wider consideration of climate change. This second edition strengthens coverage of these issues beyond that of the first edition.

The Flowering of Australia's Rainforests makes timely contributions to our understanding of the nature and function of the world's pollinator fauna, plant-reproduction dependencies, and the evolutionary pathway that has brought them to their current state and function. Illustrated with 150 colour plates of major species and rainforest formations, this reference work will be of value to ecologists and field naturalists, botanists, conservation biologists, ecosystem managers and community groups involved in habitat restoration.

1 Categorising rainforest plants

THE DAWNING OF VASCULAR PLANTS, AND THOSE THAT ARE DEAD

‘The colonisation and radiation of multicellular plants on land that started over 470 million years ago was one of the defining events in the history of this planet.’

(Pires and Dolan 2012)

Originating from aquatic forebears, vascular plants (plants with woody conducting tissue) came to occupy primordial land habitats and are now the dominant plant forms on the Earth’s landmasses (Rensing 2018). Vascular plants probably originated from multicellular green algae (e.g. Charophyaceae [see Nishiyama 2007]) during the Silurian period ~440 million years ago (mya) (Taylor et al. 2009), with perhaps the most rapid evolution unfolding during the broader Silurian-Devonian time interval (Niklas and Crepet 2020). Developments that defined the successful invasion of land by vascular plants included the possession of spores that were protected from drying out, the protection of the plant body from the extremes of evaporation, and the evolution of the phloem and xylem which allowed the efficient conduction of water and nutrients (Brodribb et al. 2010; Raven et al. 1992); with laminate (leaf-like) sporophylls and bracts occurring independently in several distantly related Early Devonian plant lineages (Hao and Xue 2013). Ultimately several lineages developed seeds, an outstanding feature which provided a major element in the dominance of terrestrial vascular plants. The seed protects and nourishes (via the seed-coat or testa, and the nutritive endosperm and perisperm) the embryonic plant in uncertain and sometimes harsh environments, allowing a period of dormancy during conditions not ideal for germination and subsequent growth.

Today more than a quarter of a million species of vascular plants are recognised, divided into four extinct and about eight living groups (authors differ on the number and placement of taxa). The extinct divisions are represented by the Rhyniophyta (e.g. Rhynia [Taylor et al. 2009]), which are known first from Silurian fossils, and the Zosterophyllophyta (Zosterophyllum [Taylor et al. 2009]), which date at least from the Late Silurian and are considered by some palaeobotanists to be the ancestors of the living club mosses (Lycophyta [ = Lycopsida]) (e.g. see Crane 1989). Zosterophyllophyta were diverse by the Late Silurian, and by the Early Devonian are known from Gondwana (Taylor et al. 2009). A third early group of now extinct vascular plants is the Trimerophytophyta (Psilophyton [Taylor et al. 2009]), first recorded from the Lower-Middle Devonian ~360 mya.

Rhyniophyta have traditionally been considered the most ancient and simplest group of vascular plants but more recent information indicates that some taxa are not true Rhyniophyta at all but share characteristics of bryophytes (plants lacking vascular tissue; i.e. liverworts, hornworts, mosses [see Bell et al. 2020]) and vascular plants (Taylor et al. 2009). The Rhyniophyta were dichotomously (in successive dual divisions) branched plants, believed to have inhabited mudflats and marshes. Rhyniophytans were seedless and their bodies did not possess distinguishable roots or leaves. Known Zosterophyllophyta species were also dichotomously branched, and may have been aquatic with the lower branches possibly anchored in mud. This conjecture is based on the restriction of stomata (structures in the leaf surface allowing gaseous exchange during respiration and photosynthesis, and the transpiration of water) to the uppermost branches. The lateral and downward growth of some branches may have provided support within the substrate, consequently allowing further outward growth of the parent. Trimerophytophyta may have been derived from the Rhyniophyta (Taylor et al. 2009) and are possibly the progenitors of the ferns, progymnosperms and horsetails (Sphenopsida). However, the Trimerophytophyta possess a more complex branching pattern and a more massive vascular strand than the Rhyniophyta, which likely permitted the development of a relatively large-sized plant. These three groups of early vascular plants produced only a single kind of spore in their sporangia and so their reproductive systems were like those of nearly all the present-day ferns, in addition to the less-known living groups Psilopsida, Sphenopsida and several of the Lycophyta.

The fourth group of extinct ancient vascular plants, the progymnosperms, stands aside from the Rhyniophyta, Trimerophytophyta and Zosterophyllophyta. The progymnosperms (e.g. Archaeopteris and Triloboxylon [Taylor et al. 2009]) are considered precursors to true gymnosperms, being intermediate in aspects of their development between gymnosperms and the Trimerophytophyta – they reproduced by spores but possessed a more complex branching and vascular system. Known from the Palaeozoic era, some, such as Archaeopteris, resembled tall leafy branched conifers. Archaeopteris is widespread in the fossil record, particularly the Northern Hemisphere, and is also known from Australia. During the Carboniferous period, ~300 mya, the ‘seed ferns’ (e.g. Medullosales, Glossopteridales, Caytoniales, Corystospermales), appeared in the Australian fossil record. Related to the progymnosperms, seed ferns (which are neither a natural nor monophyletic group [Taylor et al. 2009]), became extinct by the end of the Cretaceous. However, amongst their various members is the genus Caytonia, which was originally considered as representing a new group of angiosperms, possessing features showing possible affinity with an angiosperm carpel.

LIVING VASCULAR PLANTS

All living vascular land plants are now grouped within the Equisitopsida (see Angiosperm Phylogeny Group III 2009). Species that occur today within the divisions of the plant world can be grouped into those that are seedless and those that produce seeds of various kinds (Kramer et al. 2013; Kubitzki 2013). Among the former the most numerous are the Filicopsida (true ferns) and the more poorly represented are Psilopsida (fork ferns), Lycophyta (club mosses, quillworts) and Sphenopsida (horsetails) (Niklas and Crepet 2020; Taylor et al. 2009). Only the Sphenopsida do not naturally occur in Australia (although they were present millions of years ago). However, one sphenopsid species (Equisetum arvense) is locally naturalised (Harden 1990) and is regarded as a potential major weed. All four classes lack flowers and reproduce by the production of spores.

In Australia the Psilopsida consist of two genera, Psilotum and Tmesipteris, encountered in rainforest as epiphytes, particularly on the trunks of tree ferns (Harden 1990). Psilotum is sometimes referred to as a ‘living fossil’ as it resembles some of the first terrestrial plants, such as the extinct Cooksonia (however, Cooksonia may represent a separate lineage because the connective tissues are different from vascular plants [Niklas and Crepet 2020; Taylor et al. 2009]). Some modern Psilopsida are also terrestrial in habit, though all are small in size. Psilotum nudum can be found growing on shaded rock overhangs in rainforest, and is even recorded from rock outcrops adjacent to Sydney Harbour. Psilopsida do not possess true roots, rather being differentiated into a creeping rhizome and stems with reduced leaves that resemble scales (as in Psilotum) or more conspicuous leaves (Tmesipteris). But even in Tmesipteris the ‘leaves’ are not true leaves, but outgrowths of the stem epidermis. In the Lycophyta the herbaceous plants comprise true roots, with leaves arranged spirally about the aerial stems or arising in a grass-like manner. The class includes terrestrial and epiphytic species found in rainforest as well as other types of plant communities. Lycophyta fossils are known from the Late Silurian (Taylor et al. 2009), and during the Carboniferous the Lycophyta included tree-like species (lepidodendrids) that reached 25 m in height and dominated much of the part of the Carboniferous that is popularly called the ‘Age of Coal’ (predominantly Northern Hemisphere, as the Australian coal basins are younger). Among the fossil forms recorded from Australia is the enigmatic Upper Silurian-Lower Devonian genus Baragwanathia (see discussion in Taylor et al. 2009 regarding its implication for the early origin of vascular plants). Sphenopsida were widespread during the Carboniferous and Devonian periods, and though still widely distributed now consist of a single living family (Equisetaceae) and a solitary though cosmopolitan genus, Equisetum. Sphenopsidans possess true roots and a rhizome and leafy stems; the extinct Australian flora included Schizoneura, a characteristic element of the Permian flora of Gondwana (Taylor et al. 2009), whose thin stems were branched, with sporangia formed as long cones at the ends of small side branches. The leaves of sphenopsidans are reduced and scale-like, in appearance reminiscent of those of the angiosperm she-oaks (Casuarinaceae). In Gondwanophyton, a taxon known from the Early Permian of India and Australia (McLoughlin 1992), the relatively large kidney-shaped leaves are arranged in paired whorls around a narrow stem. However, the reproductive structures of Gondwanophyton are unknown. Though now greatly impoverished in diversity and of diminished form, during the Carboniferous and Devonian the Sphenopsida once included towering trees (Calamites) over 15 m in height (Taylor et al. 2009). Their greatest development, like that of the tree-like lepidodendrids, took place on the landmasses of the Northern Hemisphere where tropical conditions prevailed during the Carboniferous. The climate of Australia (within the great southern supercontinent of Gondwana, comprising Africa, South America, Antarctica, Australia, India, New Zealand and New Caledonia) was then cold and dry, allowing little opportunity for the development of wet forests.

The Devonian saw the emergence and radiation of the true ferns (Hao and Xue 2013; Pires and Dolan 2012; Rensing 2018). Present-day Filicopsida comprise rainforest-inhabiting species of diverse form. These include the tall trunked tree ferns (Dicksoniaceae and Cyatheaceae) typical of many Australian temperate rainforests at high and intermediate altitudes, in addition to the multitude of herbaceous terrestrial and epiphytic species that festoon tree trunks, boulders, stream lines and moist forest floors. In families such as the Polypodiaceae and Dicksoniaceae the fronds of several species characteristic of rainforests are both conspicuous and robust. Yet in some, such as the Hymenophyllaceae and Adiantaceae, there are ferns of a much more delicate construction (Harden 1990). All Filicopsida possess true roots, stems and leaves.

There are five extant seed-bearing divisions of the plant world; Cycadophyta ( = Cycadopsida), Pinophyta ( = Coniferopsida), Ginkgophyta, Gnetophyta ( = Gnetales) and Magnoliophyta (Magnoliopsida) (see Taylor et al. 2009). The Magnoliophyta comprise the flowering plants (angiosperms) with the remaining four groups characterised as the ‘gymnosperms’ (Kramer et al. 2013). Gymnosperms arose in the Devonian (c. 400–360 mya), much earlier than the flowering seed plants (the angiosperms) (Enright et al. 1995). Several authors have proposed that the Gnetophyta and angiosperms, plus the extinct orders Bennettitales, Pentoxylales and Caytoniales, constitute a closely related group, this hypothesis based on the idea that the angiosperm flower is homologous with the reproductive organ of a gymnosperm (i.e. the ‘pseudanthial’, or ‘anthophyte’ theory [Donoghue and Doyle 2000; Doyle and Donoghue 1992; Friis et al. 2011]). The Cycadophyta (cycads) and Pinophyta (conifers) are seed-bearing, though non-flowering, classes commonly referred to as gymnosperms. Both have true roots, stems and differentiated leaves, reproduce sexually and, as in all gymnosperms, possess seeds that do not develop within an ovary (thus being considered ‘naked’). If we include fossil evidence, living gymnosperms represent only a fraction of the known diversity, though ~750 species of gymnosperms (~550 if cycads are excluded) survive today (Dodd et al. 1999, Enright et al. 1995). The shrubby, palm-like Cycadophyta and the ‘reptilian’ Dinosauria collectively lent their names to the Mesozoic, popularly defining the period as the ‘Age of Dinosaurs and Cycads’. This was a time when both were conspicuous in the landscape.

Cycads, from the Palaeozoic to the present, have never been taxonomically diverse, and though morphologically conservative (Gorelick and Olson 2011), extant cycads are not relictual ‘living fossils’. Cycads are often cited as reaching their greatest diversity during the Jurassic-Cretaceous (~199–65 mya). Extinctions occurred towards the end of the Mesozoic, however, fossil-calibrated molecular phylogenies have shown that cycads underwent an almost synchronous global rediversification beginning about the late Miocene (Nagalingum et al. 2011) followed by a slowdown in diversification towards the Holocene (Recent...

Table of contents

• Cover
• Title Page
• Copyright
• Contents
• Acknowledgments
• Preface
• Introduction
• 1 Categorising rainforest plants
• 2 Rise of the angiosperms, and archaic vascular plants in Australia’s rainforests
• 3 Being a flower
• 4 Introduction to breeding systems
• Colour plates
• 5 Spatial and temporal structure of rainforest: general mechanisms that influence pollination and reproductive ecology
• 6 Australian vegetation history and its influence on plant–pollinator relationships
• 7 Pollination and the Australian flora
• 8 Pollination syndromes: who brings the ‘flower children’ in rainforest?
• 9 Pollination ecology of Australian subtropical rainforests: implications for the conservation of remnant communities
• Appendix 1. Case studies of pollination in the Australian rainforest flora
• Appendix 2. Large insects and their place in the scheme of things
• Appendix 3. Generalised pollen groups based on exine sculpture
• Appendix 4. Captions to photographs
• Appendix 5. Divisions of geologic time
• Glossary
• Bibliography
• Index