Introduction

The goal of this chapter is to review seedling morphology and evolution within a broad phylogenetic perspective. Its contents, therefore, are derivative of numerous and widely scattered publications.

Traditionally, seedling refers to the juvenile seed plant sporophyte after its emergence from the seed coat, which immediately evokes the concept of the seed itself, that is, an indehiscent, integumented megasporangium (Bierhorst, 1971; Gifford & Foster, 1988). Within this limited phylogenetic framework, a review of the morphology and evolution of the seedling is necessarily restricted to the seed plant lineages (i.e. spermatophytes) represented in contemporary floras by Ginkgo biloba, cycads, gnetophytes, conifers, and angiosperms.

However, the thesis advocated in this chapter is that a much broader phylogenetic perspective is required to understand seedling morphology and evolution fully because many of the features that characterize the seedling sensu stricto evolved well before the appearance of the first seed plants. Perhaps the most important of these features is the physical retention and physiological nurturing of the developing sporophyte within gametophytic tissues. This feature is characteristic of all land plants (i.e. embryophytes) by virtue of their (1) diplobiontic life cycle, in which a multicellular diploid sporophyte alternates with a multicellular haploid gametophyte to complete the sexual reproductive life cycle, and (2) their archegoniate condition, in which the developing diploid embryo is retained, protected, and nurtured within an archegonium (or its presumed vestigial remnants, e.g. synergids).

Introduction

Over the past two decades, ecological restoration has progressed to rely on more refined techniques, to include a greater array of ecosystems, and to attempt larger and more complex problems. Despite this progress, the outcome of many restorations fails to result in ecosystems that are similar to their natural counterparts. Restored ecosystems typically have fewer species and do not accumulate species over time, as expected. A lack of available seeds or suitable microsites for seedling establishment can hinder community development. Not surprisingly, seed availability is more often reported to be the key limitation to higher richness (e.g. Pywell et al., 2002; Martin & Wilsey, 2006; Kettenring, 2006). Most restorations introduce a small subset of the species expected and often at much lower abundances than exist in unaltered sites. To do otherwise seldom has been considered necessary because dispersal has the potential to add species over time. Unfortunately, habitat fragmentation has diminished native species propagule pressure and hinders dispersal in many landscapes (Galatowitsch & van der Valk, 1996; Honnay et al., 2002; Young et al., 2005) leading to increased recognition of the importance of adequate seed introductions for restorations.

When the investment in acquiring native seed for restoration is significant, there needs to be a reasonable likelihood that conditions are suitable for seedling emergence and growth. This can be especially challenging considering that site conditions at the start of a restoration project can be radically different than what might have ever existed in an unaltered community, even after natural disturbances.

Introduction

Flowering plants – angiosperms – are presently the most ecologically significant lineage on the green-plant tree of life. With the exception of high latitude and some upland regions, angiosperms dominate both the species number and biomass of the world's major biomes. Furthermore, the chemistry, productivity, and structure of angiosperms are the foundation of ecological webs of biotic interactions that generate and sustain terrestrial biodiversity.

Yet, despite their entrenched and manifold roles in today's ecosystems, angiosperms represent the youngest major group of terrestrial plants (Wing & Boucher, 1998; Boyce, 2005). Compared to other major lineages of plant evolution that appear in the fossil record during the mid-to late Paleozoic, angiosperms are relative newcomers with the first undisputed fossils appearing nearly 100 Ma later during the Early Cretaceous. This pattern raises the question: How did angiosperms achieve such tremendous diversity and nearly singular ecological dominance over a relatively brief geological interval (≈100–60 million years ago; Wing & Boucher, 1998; Lupia et al., 1999; Nagalingum et al., 2002)? Answering this question is difficult because the deep time phases of angiosperm evolution, preeminently their early biology and causes of initial success, remain uncertain (Wing & Boucher, 1998). Ultimately, the early angiosperm enigma clouds the resolution of the biological and environmental mechanisms sparking the rise of the modern day angiosperm epoch and diverse biotas that co-evolved with them.

Introduction

To understand the role of seedlings in the dynamics of dryland ecosystems, I consider functions seedlings fulfill in population and community dynamics of desert plants and how these functions affect ecosystem and landscape processes. My main focus is to explore the interactions of seedlings with the structure and function of dryland ecosystems. These include not only the responses of seedlings to changes in their environment, but especially their roles in formation and maintenance of spatial heterogeneity and its degradation. These interactions are also involved in sustainable management of arid and semiarid rangeland and in restoration of landscapes degraded by unsustainable human land use. Understanding the roles that plants in general, and seedlings in particular, play in dryland ecosystem and landscape processes may help in formulating appropriate management and restoration methods for sustainable dryland land use under changing climatic conditions.

Interactions involving seedlings are complex and diverse, concerning both pure ecosystem processes, such as resource dynamics of energy, water, nutrients, and gas flows and fluxes, foodweb relations, and the dynamics of the substrate within which the processes occur, that is, the landscape. Part of the complexity arises from the interrelations between ecosystem functions and landscape structure at various spatial and temporal scales. This is strikingly illustrated by the nature of dryland ecosystems, which are characterized by the temporal variability of resources due to scarce pulses of rainfall and by the spatial heterogeneity of the landscape. Both vary from modest in semiarid areas to extreme in hyperarid zones.

Introduction

Many plant ecophysiological issues, such as trade-offs associated with resource acquisition strategies, are shared between seedlings and larger plants. Yet, seedlings face several unique challenges in their struggle to achieve positive net carbon balance necessary for growth and survival. First, seedlings go through dynamic physiological changes from complete dependency on seed reserves to dependency on light and external nutrients. Second, because seedlings are small, modest changes in carbon allocation patterns will have large consequences on whole plant carbon balance and survival. Third, seedlings experience intense mortality from a wide range of abiotic and biotic factors, including strong asymmetric competition from larger neighbors, herbivory, disease, and disturbance (Moles & Westoby; 2004c; Fenner & Thompson, 2005; Kitajima, 2007; Chapter 10). Finally, phylogeny exerts a particularly strong influence on seed size (Moles et al., 2005b) and morphological traits (Saverimuttu & Westoby, 1996b; Ibarra-Manréquez et al., 2001; Zanne et al., 2005) of young seedlings. These unique aspects undoubtedly influence the evolution of resource allocation strategies in relation to the regeneration niches of species (Grubb, 1977).

In this chapter, we discuss both theoretical and technical issues important in evaluating carbon allocation strategies of seedlings. We place a large emphasis on inter- and intraspecific trade-offs due to constraints in resource allocation. Presumably, such trade-offs reflect specializations in ecological space defined by spatial and temporal heterogeneity, and ultimately restrict the range of environments in which seedlings establish (Chapters 3, 10). We explore key concepts pertaining to carbon balance strategies.

Introduction

This chapter considers the internal and external processes that affect seedling communities. Internal or endogenous drivers include the density dependence of seedling populations, as well as the relationship of parent to offspring and the competitive relationships affecting seedling populations. There are many external or exogenous drivers, but we will focus on climate, predation, and fire. We will integrate these internal and external drivers of community composition to address the questions: To what extent do seedling recruitment strategies relate to community assembly rules and do these rules dictate the potential combinations of regeneration niches to be found in any given community? This chapter will focus on long-lived woody species because the differences in life history stages and factors affecting them appear much more prominent than in some other growth forms.

Internal drivers

Communities of regeneration niches

Plant recruitment strategies have received a great deal of attention generally to determine the environmental conditions that favor one strategy over another (Chapter 11). Although communities comprise an assemblage of different seedling strategies, relatively little attention has been paid to the community combinations or rules that limit possible combinations. A useful concept for understanding seedling communities is that of safe sites (Harper, 1977), which is a species-specific phenomenon driven by unique aspects of ecology and phylogeny. It is important to recognize the diversity of potential safe sites and how they are distributed in space and time. Also of importance is how species reach safe sites and the role of metapopulations.

The properties of seedlings are potentially important to all plant ecologists, whether they be interested chiefly in understanding seminatural indigenous vegetation, invasive plants, or the problems of restoration. In seminatural vegetation, seedling properties may determine the climatic regions occupied on a continental scale and the habitats occupied within a landscape, the ability of one species to coexist with another in a community, and the abundance of one species relative to another at a given time and place. The requirements of seedlings often determine the sites in which potentially invasive species can succeed and whether a given approach to restoration of seminatural vegetation is effective.

During the last 40 years, there has been a steady increase in the amount of research by ecologists on the properties of seedlings as opposed to those of mature plants. Great pioneers such as F. E. Clements and E. J. Salisbury appreciated the importance of studying seedlings, although papers on experimental studies on seedlings were uncommon before the 1960s. Several factors have driven the increase in work on seedlings. Here I emphasize seven.

First, there has been a desire to seek generalizations about seed-lings. For example, how does relative growth rate vary with the mass of reserves in the seed, and how does it differ at a given seed-reserve mass between plants of different growth forms (such as tree vs. herb), or species from different kinds of habitat (where the vegetation shows high and low productivity, respectively)?

Lichens are the dominant life forms in about 8% of the land surface of the Earth (Ahmadjian 1995), mainly in polar regions and on the tops of mountains. These places are characterized by severe abiotic stresses such as desiccation, temperature extremes, and high light intensities. Arguably, what really makes lichens special, and what separates them from most other eukaryotic organisms, is their ability to tolerate extreme stresses. For this reason, some have called lichens “extremophiles,” organisms that can thrive in conditions that would kill other, less specialized organisms. Scientists have found that hardy lichens can survive a trip into space, and now the list of natural astronauts includes lichens. During a recent experiment by the European Space Agency, lichen astronauts were placed on board a rocket and launched into space, where they were exposed to vacuum, extreme temperatures, and ultraviolet radiation for two weeks. Upon analysis, it appeared that the lichens handled their spaceflight just fine (Young 2005)!

In the typical environments that many lichens inhabit, stresses such as low thallus water content and temperature extremes can develop within just a few minutes. However, others, such as a nutrient deficiency, can take months to develop. The stressfulness of a particular habitat is the result of the interaction of climate and substrate. It plays a major role in determining lichen distribution. Understanding the physiological processes that lie behind stress injury, and how lichens tolerate environmental stress, is therefore of great importance in lichen biology.

Although earlier literatures provided an insight into the uniqueness of lichens, it gave little hint of the major role these apparently insignificant organisms play in the shaping of the physical and biological environment of our planet and their importance in maintaining its equilibrium. Their role as biological weathering agents in the development of soils, for example, was formerly considered in a geological context only, but recent research has shown that these organisms are capable of biodeteriorating stone substrates within a relatively short timescale. Information is now available to demonstrate that lichens can often contribute substantial biomass and support a high biodiversity of micro- and macroorganisms, creating complex food webs and adding significantly to energy flow (Chapter 10) and mineral cycling (Chapter 12).

The disappearance of lichens, due to many aspects of human interference in the natural world, has therefore led inexorably to environmental impoverishment. Lichens are natural sensors of our changing environment: the sensitivity of particular lichen species and assemblages to a very broad spectrum of environmental conditions, both natural and unnatural, is widely appreciated. Lichens are therefore used increasingly in evaluating threatened habitats, in environmental impact assessments, and in monitoring environmental perturbations, particularly those resulting from a disturbingly large and growing number of chemical pollutants (Chapter 15). Nevertheless, lichens undoubtedly represent one of the most successful forms of symbiosis in nature.

Photosynthesis is used by autotrophic organisms to convert light energy into chemical energy for maintenance, growth, and reproduction. Heterotrophs have shown considerable agility in forming symbiotic relationships with autotrophs so that they obtain a reliable carbon source. The endosymbiont theory proposes that the chloroplast of eukaryotic cells evolved from photosynthetic cyanobacterium-like organisms which were engulfed by nonphotosynthetic cells, leading eventually to the evolution of algae and plants. Fungi have also developed symbioses, one being the lichen, an extrasymbiosis with photosynthetic algae and/or cyanobacteria, which, in many respects, appears to function like a single autotrophic “organism.” Its photosynthesis and respiration are complex biophysical and biochemical processes that will not be discussed here in any detail. We shall restrict our analysis to those aspects that are of ecological relevance, in particular carbon dioxide (CO2) exchange, which is the subject of this chapter.

On average, approximately 40 to 50% of a lichen's dry mass consists of carbon which is almost exclusively fixed by photobiont photosynthesis. Photosynthetic processes are vital for the existence, survival, and growth of the lichen. Energy-producing respiratory processes that release CO2 occur in both the mycobiont and photobiont, although the individual contributions of the symbionts to the respiration of the whole lichen thallus are not yet known. However, it is most probable that total thallus respiration mainly reflects the metabolic activity of the fungal partner (Quispel 1960).

Historically, lichen fungi have through most of the nineteenth and twentieth centuries been arranged in its own class, Lichenes, based on their symbiotic life form as expressed by their composite thalli. By convenience, the name of the lichen fungus is usually but inaccurately applied to the feature referred to as a lichen, as if that was an organism. Actually, lichens are small ecosystems (Section 1.6), comprising associations with two or more components, an algal producer and a fungal consumer. The components are individual organisms; lichens are not. Consequently, lichens per se cannot be classified into natural systems because they have no phylogeny. Today lichen fungi are classified together with other chitinous fungi and incorporated into a common fungal system.

Systematics

Systematics – the science of studying the diversity and hierarchy of nature – is not only the oldest natural science, but is also a science where the modern development is progressing at a dramatic pace. Systematics is built up by four major parts: taxonomy (the delimitation and description of taxa), nomenclature (the formal naming of taxa), phylogeny (the natural relationships among taxa), and classification (the organization of taxa into a hierarchical system). In the present treatment, we focus on the phylogeny and classification of lichen fungi. Taxonomic methods and nomenclatural rules and principles are beyond the scope of the present book.

Lichens have been recognized as being very sensitive to air pollution for many years (Hawksworth 1971; Nimis et al. 2002). In the 1800s independent observations in England, Munich, and Paris documented that lichens were already disappearing from urban areas. By the early 1900s this “city” effect was a widely recognized phenomenon in Europe and was first attributed to coal dust, which was emitted by most homes as well as many industries. Only later did the colorless gas, sulfur dioxide, become recognized as a principal phytotoxic agent. Today the list of air pollutants is much longer and includes oxidants, hydrogen fluoride, some metals (Section 12.7), acid rain, and organics. Certainly the list of potentially toxic substances is not yet fully circumscribed.

The high sensitivity of lichens is related to their biology. Most species live for decades or hundreds of years and a few longer; thus, as perennials, they are subject to the cumulative effect of pollutants. Lichens have no vascular system for conducting water or nutrients; as a consequence, they have developed efficient mechanisms for taking up water and nutrients from atmospheric sources. Fog and dew, major water sources for lichens, often have much higher pollutant concentrations than precipitation, and the lichens' nutrient concentration mechanisms also will concentrate pollutants. Unlike many vascular plants, lichens have no deciduous parts, and hence cannot avoid pollutant exposure by shedding such parts.

The symbiosis

Lichens are by definition symbiotic organisms, usually composed of a fungal partner, the mycobiont (Chapter 3), and one or more photosynthetic partners, the photobiont (Chapter 2), which is most often either a green alga or cyanobacterium. Although the dual nature of most lichens is now widely recognized, it is less commonly known that some lichens are symbioses involving three (tripartite lichens) or more partners. The potential relationships of mycobionts and photobionts may in fact be quite complex (Chapter 4), and a rigorous classification of many types of relationships was developed by Rambold and Triebel (1992). In general, lichens exist as discrete thalli and are implicitly treated as individuals in many studies (but see Chapter 13), even though they may be a symbiotic entity involving three kingdoms! From a genetic and evolutionary perspective, lichens can certainly not be regarded as individuals and this fact has major implications for many areas of investigation, such as developmental and reproductive studies (Chapter 5).

The nature of the lichen symbiosis is widely debated and deserves further investigation. Most general textbooks and many researchers refer to lichens as a classical case of mutualism, where all the partners gain benefits from the association. Alternatively, lichens are regarded as an example of controlled parasitism, because the fungus seems to obtain most of the benefits and the photobiont may grow more slowly in the lichenized state than when free-living (Ahmadjian 1993).