Introduction

Tropical dry forests constitute over 40% of all tropical forests (Murphy & Lugo 1986), yet their dynamics have been poorly studied relative to tropical moist forests (Bullock et al. 1995). Major ecological factors influencing the dynamics of tropical dry forests include high variability in climate, herbivory by wild mammals and domestic livestock (Skarpe 1991; Sukumar et al. 1998), natural and human-induced fires (Swain 1992; Goldammer 1993) and human extraction of a variety of products (Chopra 1993; Narendran et al. 2001). There has been much thinking on the issue of stability of tropical forests; some of this follows from or is related to the broader issue of the stability–diversity debate (e.g. Connell 1978; Pimm 1984; Lawton 1994; Johnson et al. 1996) or that of the turnover rate of tropical forests (Philips et al. 1994; Sheil 1995). These have been discussed mostly in the context of tropical moist forests.

It is being increasingly recognized that environmental variability is a major influence in shaping the structure, functioning and evolution of communities. In particular, we can expect that environmental variability would influence the evolution of life-history traits of species that constitute a particular community (e.g. Murphy 1968; Gadgil & Bossert 1970; Stearns 1977, 1992; Boyce & Daley 1980). Interannual variation in climate (e.g. precipitation) is usually taken as the most important measure of environmental variability that shapes life-history traits in a species. At the same time, the role of disturbances (e.g. hurricanes, fire) in eliciting short-term ecological responses should also be considered.

Introduction

The roots of almost all species of tropical rainforest trees contain mycorrhizal fungi (Alexander 1989a). Our aim here is to demonstrate that not only are these fungi central to ecosystem processes such as carbon- and nutrient-cycling, but that they also have the potential to influence biotic interactions between species, and so help to shape the structure and composition of forest communities. As such, they should be of interest to all ecologists, not just those who are primarily concerned with nutrient dynamics.

Mycorrhizas have continued to be the subject of intensive research in the 15 years since we last reviewed their role in tropical rain forest (Alexander 1989a). The processes by which mycorrhizal fungi access mineral nutrients in natural substrates are more fully understood, and important functional differences between types of mycorrhiza have been recognized (Read & Perez-Moreno 2003). There have been major advances in our understanding of the role of mycorrhizal fungi in forest carbon cycles. In boreal forest, for example, 20%–30% of current assimilate is consumed by mycorrhizal fungi (Söderström 2002), over 50% of CO2 released from soils is accounted for by the respiration of tree roots and their associated mycorrhizal fungi (Högberg et al. 2001) and 30% of the soil microbial biomass is the extraradical hyphae of mycorrhizal fungi (Högberg & Högberg 2002). There is also growing evidence that mycorrhizal associations are multifunctional, and that benefit to the host may not accrue solely or entirely through enhanced capture of mineral nutrients (Newsham et al. 1995a).

Introduction

Fungal endophytes are defined as those fungi that live inside plant tissues (e.g. roots, stems, leaves) without causing apparent harm to their host (see Wilson 1995). Although we will also mention stem-associated endophytes (see Evans et al. 2003) and endophytes associated with roots (mycorrhizae; see Herre et al., this volume), throughout this chapter, we will focus primarily on the implications of recent studies of the endophytic fungi that live inside plant leaf tissue. These foliar endophytes are extremely diverse phylogenetically and have been documented in nearly all plants sampled (e.g. mosses, liverworts, ferns, conifers and angiosperms; Carroll 1988; Clay 1988; Petrini 1991; Schultess & Faeth 1998; Frohlich & Hyde 1999; Stone et al. 2000; Arnold et al. 2000; Arnold 2002; Arnold et al. 2003; Davis et al. 2003). Despite the growing recognition of their wide distribution across plant taxa, basic attributes of their biology are still poorly understood. Specifically, endophyte diversity, distributions, life cycles, interactions with hosts and other fungi, and their net chemical, physiological and ecological influences are only beginning to be appreciated and studied. This is particularly true in the extremely diverse tropics.

The best-studied endophytes are ascomycetes belonging to the family Clavicipitaceae. These fungi grow throughout the aboveground tissues of some temperate grass species (e.g. Festuca arundinacea, see Clay & Schardl 2002). Typically, in infected individuals, a single fungal genotype infects a single plant individual.

Introduction

Understanding seed dispersal is critical to understanding plant population and community dynamics (Nathan & Muller-Landau 2000), especially in tropical forests where seed rain of virtually all plant species is sparse and patchy (Hubbell et al. 1999; Muller-Landau et al. 2002). Seed rain determines potential population growth rates and spatial patterns, as well as the relative influences of post-dispersal processes such as seed predation (e.g. Wright et al. 2000), microhabitat requirements for establishment (e.g. Svenning 1999) and density-dependent survival (e.g. Harms et al. 2000). Despite its importance, we know very little about seed dispersal of tropical trees, because it has been studied in only a tiny proportion of the many tropical tree species and seed dispersers, and because the patterns that have been observed have largely eluded easy generalization.

Just as there is a greater diversity of plant species and animal species in the tropics than in other regions, there is also a greater diversity of seed-dispersal strategies and patterns. Seed dispersal by animals predominates – it is the main strategy of 70%–90% of tropical forest plant species (Willson et al. 1989) – and involves a tremendous diversity of animal species and behaviours. Birds, bats, arboreal and terrestrial mammals (everything from mice to elephants), ants, dung beetles, even fish can disperse seeds (Levey et al. 1994). Animals may consume fruit and drop, spit or defecate the seeds, carry seeds in their coats or scatter-hoard seeds for later consumption.

Introduction

Understanding the processes underpinning high biodiversity in tropical rain forests is a major goal for ecologists. There has been a long-standing interest in the role of herbivory in the tropics, in part because it has been proposed as a mechanism contributing to the maintenance of this diversity for tree species (Janzen 1970; Connell 1971; Marquis, Chapter 13, this volume). The Janzen–Connell hypothesis predicts that herbivore damage may act in a density-, distance- or frequency-dependent manner and, if the amounts of damage are sufficient to cause changes in growth rates or mortality of seedlings (or seeds), then this could lead to the distancing of conspecifics and hence promote species diversity. In areas of high conspecific density, increased herbivory could kill or reduce the growth of more common species, allowing rarer species to persist. This hypothesis relies on the ability of herbivory to significantly affect seedling growth or mortality, and although many studies have found variation in damage levels between species (Coley 1983; Coley & Barone 1996; Blundell & Peart 1998; Howlett & Davidson 2001), few studies have found conclusive effects on seedling growth, much less on mortality (Aide & Zimmerman 1990; Webb & Peart 1999; Howlett & Davidson 2001; Horvitz & Schemske 2002; Hyatt et al. 2003; Pearson et al. 2003b). Of the studies that have demonstrated differences in growth rates or mortality between species caused by herbivory (Marquis 1984; Coley 1986; Bazzaz et al. 1987; Sork 1987; Osunkoya et al. 1993; Terborgh & Wright 1994; Sagers & Coley 1995; Whitmore & Brown 1996; Ickes et al. 2001; Wallin & Raffa 2001), the majority are attributable to mammalian herbivores and seed predators (Sork 1987; Osunkoya et al. 1993; Terborgh & Wright 1994; Ickes et al. 2001).

Plant invasions pose a current and increasing threat to species diversity and composition of forests worldwide. Biological invasions are natural ecological processes and the movement of plants across geographic barriers has always occurred (Sauer 1988), but humans have greatly accelerated the rate of introductions and moved plants across barriers that probably would not have been spanned naturally. Many of these plant introductions, whether deliberate or accidental, have had negative effects in the areas of introduction. Plant invasions have led to native species loss, altered ecosystem-level processes and caused enormous economic and environmental damage in various ecosystems, including tropical forests (Vitousek et al. 1987; Gordon 1998; Parker et al. 1999; Mack et al. 2000). Remote tropical islands and fragmented landscapes are particularly vulnerable to invasion by non-native plants (Laurance et al. 2002; Denslow 2003), but continental species-rich tropical rainforests also are invasible (Usher 1991; Rejmánek 1996a), particularly following natural or human disturbance (Whitmore 1991). Because of such negative impacts, species invasions are seen as one of the primary agents of global change (Vitousek et al. 1996), and tropical forests are unlikely to be immune (Fine 2002).

This chapter explores how biotic interactions, particularly herbivory and pathogen attack, may affect the abundance and distribution of invasive woody species in tropical rainforests. Specifically, I examine whether herbivores and fungal pathogens (natural enemies) are important determinants of species' abundance and distribution in their native ranges and whether the absence or reduced impact of these natural enemies may explain why certain introduced woody plants are successful invaders in tropical rainforests.

Introduction

At a symposium 44 years ago, J. B. Gillett proposed the Theory of Pest Pressure, whereby plant pathogens and pests were responsible for the genesis and maintenance of high plant diversity in tropical forests and other high-diversity systems. In his conclusion to the paper produced from that talk he hoped that this ‘new theory may be useful in stimulating discussion and research’ on the roles of pests and pathogens as a force in plant diversity. Apparently his theory has been useful, as much has happened in the last four decades to explore and expand on his idea. My aim is to review key research on the effects of plant pathogens in tropical forests since Gillett's seminal paper with emphasis on the special case of his Theory of Pest Pressure known as the Janzen–Connell Hypothesis. I will also suggest critical areas that need to be explored as we continue to discuss and research the role of pathogens in the maintenance of species diversity in tropical forests.

‘Parcere subiectis et debellare superbos’

Gillett (1962) paraphrased Virgil's famous formula for the greatness of Rome, ‘Spare the lowly and conquer the haughty’ (AeneidVI: 853), when he first introduced the idea that if plant pests have a greater impact on more common species than on rare species, the rare species should then increase in relative frequency, providing a mechanism for the maintenance of diversity in species-rich communities.

Introduction

Disturbance is integral to a forest's ecology, and selective logging is a form of disturbance. Whether disturbance is natural or anthropogenic, it is likely that the biotic interactions within the system are influenced by it. This volume attests to the importance of biotic interactions to tropical forest function and diversity. And while there are still many unknowns in how interactions change with perturbation, particularly when the impacts are as variable as those associated with timber management, an understanding of these changes is important to inform the development of management interventions that are ecologically sustainable, i.e. where the manipulations stay within the limits of natural disturbance patterns for the forests (e.g. ecological forestry, sensu Seymour & Hunter 1999) and where ecosystem functions are maintained (Forest Stewardship Council (FSC) 2000).

Generally, approaches to the study of impacts of logging and other silvicultural interventions are based on comparisons, for example control versus impact designs where unlogged, old-growth forests are used as the control (Johns 1983; Lambert 1992; Silva et al. 1995), or various treatments are compared, for example different logging systems (Johns et al. 1996; Pinard & Putz 1996), different harvest intensities (Kasenene 1987; Panfil & Gullison 1998; van der Hout 1999), or different stand-improvement treatments (Fox & Chai 1982; de Graaf et al. 1999; Gerwing 2001). But as with other forms of anthropogenic impacts, detecting change is difficult because of the complexity and variability (temporal and spatial) of natural systems (Underwood 1991, 1993).

Introduction

As described in Chapter 8, plant growth results from a combination of cell division, elongation and differentiation, initiated from groups of cells known as meristems. During embryogenesis two meristems are formed – the shoot apical meristem which gives rise to the shoot system, and the root apical meristem which forms the root system. As these primary meristems develop, they give rise to more apical meristems which will form side branches or lateral roots, and lateral meristems which result in an increase in girth (Fig. 9.1).

Together, environmental and internal signals control the rate of growth, the activation of new meristems, and the differentiation of cells and tissues, producing the plant body within the framework of the basic ‘body plan’ of the plant. Meristem activity must be under precise control to generate the specific structures of the plant, but at the same time must be flexible enough to respond to environmental signals. Some of the controlling signals, and the genetic systems on which they act, are discussed below, with reference to the formation of the vegetative organs of the plant. The formation of reproductive structures is covered in Chapter 11.

The structure and activity of the shoot apical meristem

Organ initiation

During the vegetative phase of growth, the shoot apical meristem (SAM) produces stem, leaves and axillary buds in units known as phytomers.

Introduction

A mature plant is a complex organism made of many different organs, tissue types and cell types. The plant develops from a single cell, the zygote (fertilized egg) which first divides to form an embryo within a seed. By the time the embryo is mature, it already contains distinct meristems, from which the entire plant will develop upon germination. The meristems remain potentially capable of producing new cells throughout the life of the plant, and all of the complex organized structures of the plant develop from these apparently simple meristems by a combination of cell division, cell expansion and cell differentiation, as well as programmed cell death in some cases. Plant cells being immobile, migration of cells, as occurs in animal embryos, plays no part. This is the process of morphogenesis (morpho = form, genesis = origin) briefly touched on in Chapter 6. It is now necessary to consider in depth the manner in which meristems give rise to vegetative and reproductive structures.

The first stage in the formation of any plant structure is production of new cells by cell division. Determination of the position, direction, number and timing of the divisions is the first control stage in the morphogenetic process. Once the cells are formed, the morphogenetic process continues with expansion in a determined direction and to a controlled size. This is accompanied by cellular differentiation.

The history of this book dates back to the late 1960s, when the publishers Edward Arnold launched a series of student textbooks as the Contemporary Biology series, designed to provide up-to-date texts at elementary university and final-year school level. One of the first authors who was asked to contribute, on the topic of flowering plant physiology, was Professor H. E. Street, then Professor of Botany at the University of Wales, Swansea. He asked one of us (H.Ö.) to collaborate, and the first edition was duly published by Edward Arnold in 1970 under the authorship of H. E. Street and Helgi Öpik, and entitled The Physiology of Flowering Plants: Their Growth and Development. The emphasis of the text was on the ‘whole plant’ aspects of physiology. The second edition followed in 1976 and the third in 1984, although Professor Street sadly deceased in 1977.

While the second and third editions were still very much revisions of the original text, the longer time interval since the last edition, and the rapid pace at which biological knowledge has grown in the last few decades, have now necessitated a very thorough rewriting of large sections of the book, and the task has been quite challenging in the face of an accumulation of facts that on occasion has seemed quite overwhelming. It is not possible now to interpret many aspects of plant physiology without reference to molecular biology, even when one is basically interested in functioning at the organismal level.

Introduction

Light is critically important to plants. The majority of them are photosynthetic and light provides the energy source required for growth. However, light is equally important for the normal development of plants as an information medium. In the environment light is a very complex and dynamic signal. It varies in quantity, quality (colour) and direction over timescales ranging from seconds to months (Fig. 10.1). These different variables can indicate the passing of the seasons, the availability of new habitats for growth or the presence of neighbouring vegetation which may compete for resources. Therefore it is not surprising that many aspects of plant growth and development are strongly influenced by light. The plant, too, is a complicated and ever-changing system, and the response of a plant to a given set of environmental conditions will depend upon its developmental state. As discussed in Chapter 9, plants pass through a juvenile state where their response to environmental signals differs from that of mature plants. Likewise, signals which stimulate a mature plant to flower may cause the seed of the same species to germinate – radically different developmental pathways. Similarly, plant responses are species-specific. Whilst a fast-growing weed such as Chenopodium album will respond to shaded conditions (i.e. low light) by elongating rapidly, rainforest tree seedlings can persist under a vegetation canopy for many years and commence rapid growth only when a gap opens in the forest canopy.

Introduction

Although it is a general perception that plants do not move very much, or very quickly, this is true only when seen from a human perspective. If we view the world using time-lapse photography we quickly become aware that all plants are, more or less, in continuous motion. This should not come as a surprise when one considers that plants cannot uproot themselves and relocate to a new environment to maintain suitable conditions; they must orientate their organs, largely by growth, to optimize their interactions with the non-uniform environment which surrounds them. We tend to take it for granted that shoots (usually) grow upwards into the air and roots grow down into the ground; leaves spread out and turn to the light; flowers take up specific orientations. All this positioning is the result of differential growth, growth movements, in precise and complex responses to environmental stimuli, especially light and gravity. Mutants which lack some of these responses are unable to grow normally; e.g. mutant shoots unable to respond to gravity lie on the ground and in the field would be overgrown and perish. Growth movements, imperceptible as they are to instantaneous observation, are vital to the plant. In addition to the relatively slow growth movements, more rapid, visible movements are exhibited by specialized plant organs.

Introduction

Reproductive development of flowering plants has been studied for many hundreds, if not thousands, of years. This is not surprising, given the importance of flowering, fruiting and seed setting in agriculture. Society also has a fascination with producing ever more diverse flowers for horticultural purposes. The rose is the oldest known domesticated flower and its popularity endures today; over 103 million roses are sent for Valentine's day in the USA alone, with the global trade in all cut flowers exceeding $4 billion annually. Moreover, since cut flowers are desired at all seasons, control of the time of flowering has great commercial value. Hence a study of the reproductive processes of flowering plants is of great economic importance as well as enabling us to understand the functioning of plants in their natural ecosystems.

Juvenility and ‘ripeness to flower’

Vegetative growth eventually leads to a transition to reproductive development. However, plants will not flower, nor respond to environmental stimuli which ensure subsequent flowering, until they have completed a certain period of vegetative growth and reached ‘ripeness to flower’. A plant can therefore be considered to pass through three growth phases:

1. juvenile – in which it will not flower

2. mature – in which appropriate environmental stimuli will evoke flowering

3. reproductive – in which flowering actually takes place

Introduction

Any factor that acts on an organism so as to impair its functions can be termed a stress. Plants growing in the field are habitually exposed to a number of environmental stresses, e.g. drought and frost. Being sessile organisms, plants cannot move away from a stressful situation. The ability to withstand environmental stresses therefore frequently becomes the limiting factor for plant growth, survival and geographical distribution. Plants in fact may possess remarkable powers of endurance. The vegetation of arctic regions can experience winter temperatures of − 70 ℃, whilst in hot deserts over 50 ℃ may be encountered, and even greater temperature extremes have been survived in the laboratory. On the other hand, some plants are killed by chilling at 10 ℃: species vary tremendously in their resistance towards a particular stress. Studies of the reactions of plants under stress, and mechanisms of stress resistance, are of great practical importance, since agricultural yield is only too often drastically reduced by stressful external factors. The demands of an expanding human population have stimulated research into improving the stress resistance of crop species in order to extend the geographical range of a crop, or with a view to utilizing land areas previously regarded as too ‘extreme’ for cultivation, such as semi-deserts.

Terminology and concepts

Stress is a very wide concept, and while the general idea is easily conveyed it is not so easy to decide where the limits should be drawn. Stress was briefly defined above as ‘impairing function’.

Introduction

Growth is one of the most fundamental and conspicuous characteristics of living organisms, being the consequence of increase in the amount of living protoplasm. Externally this is manifested by the growing system getting bigger, and growth is therefore often defined as an irreversible increase in the mass, weight or volume of a living system. The size increase must be permanent; the swelling of a cell in water is not growth, being easily reversed by returning the cell to a solution of lower Ψ. It is, however, possible to consider as growth developmental changes not immediately involving an increase in size. An amphibian embryo, or a Selaginella female gametophyte, for a long time utilizes the nutrient store with which it was released from the parent, to produce many new cells without any increase in overall size, yet growing in the sense that living protoplasm is increasing at the expense of stored nutrients. Again, if dry mass is measured, a flowering plant seedling loses dry mass while utilizing reserves and growing.

Growth is an exceedingly complex process. Every reaction associated with the synthesis and maintenance of living protoplasm is associated with it, which makes it complicated enough at the cellular level. At the organismal level, it means the coordinated multiplication, size increase and specialization of millions of cells, all arranged in precise positions. Growth processes are also synchronized with seasonal changes, plants responding to appropriate environmental stimuli to achieve this synchronization.