Epiphyte ecology has been a recurrent topic throughout the preceding chapters but little or nothing has been said about community organization, succession, associated phytotelmata, phorophyte specificity, or influence of epiphytes on supports and other biota. Although documentation of cause and effect is scarce, it is clear that canopy-dwelling flora can help shape forest structure and economy; processes as fundamental as community-wide mineral cycling and productivity are affected. Influence on animals is no less pervasive. Without plant resources beyond those provided by earth-rooted vegetation, much of the immense and diverse fauna characteristic of humid tropical woodlands (Erwin 1983) would not exist. This chapter will emphasize the role of epiphytes as members of communities and substrata for other organisms.

Host specificity

Only the exceptional epiphyte has but one acceptable phorophyte (Table 7.1). Far more commonly, anchorage occurs on several kinds of supports, although usually not with equal frequency. Valdivia (1977) studied the distribution of 153 vascular epiphyte species on 45 different trees in east-central Mexico. Only Acacia cornigera, a myrmecophyte that is aggressively defended against other insects and encroaching vegetation by its ant colonies, hosted no epiphytes. The remaining 44 each supported more than one species; the record was 107, demonstrating that certain trees offer especially suitable crowns. Few phorophytes provide anchorage to every potential colonist, however, nor does occurrence always follow expected patterns. Aechmea bracteata is abundant on several trees in semievergreen forest in the Sian Ka'an Reserve, Mexican Yucatan (Olmsted and Dejean 1987).

All epiphytes photosynthesize, but certain life stages of several taxa are heterotrophic – for example, gametophytes of arboreal Lycopodium, Ophioglossum, Psilotum, and Tmesipteris. Similarly, orchid seedlings remain achlorophyllous for weeks to months, subsisting on substrates provided by symbiotic fungi (Figs. 4.10, 4.12). Flow of fungal metabolites into adult orchids may also occur, but claims for epiparasitism in canopy-based Orchidaceae (e.g., Ruinen 1953; Johansson 1977) need confirmation using labeled nutrients. As for dwarf mistletoes, utilization of host substrates has been great enough to allow considerable leaf reduction; most of the vegetative body is endophytic.

The question now is how autotrophy operates in canopy-adapted vegetation. This chapter will examine (1) photosynthetic pathways among epiphytes, two of which are certain, the third equivocal; (2) accommodation of carbon balance to mineral scarcity and shade; (3) segregation of co-occuring populations along light gradients; (4) photosynthetic phenomena peculiar to certain specialized taxa; (5) ancestral habitats; and (6) the economics of epiphyte foliage versus that of phorophytes. The interrelationship between photosynthesis and water balance is covered more thoroughly in Chapter 3.

Photosynthetic pathways

The reductive pentose phosphate (C3) pathway

Machinery for trapping radiant energy, perfected in plants long before land was colonized, required tailoring as the terrestrial flora developed. Light intensity and quality, supplies of moisture, nitrogen (N), and presumably other key nutritive elements, influenced selection during the subsequent radiation, up to and including colonization of tree crowns.

Aspects of foliage reveal the fact that stress, particularly drought, is a powerful selective force on plants anchored in tree crowns. Whereas phorophytes are usually characterized by mesomorphic leaves and C3 photosynthesis, their epiphytes tend to xeromorphism and unusual mechanisms for procuring, as well as greater capacity for storing, water. Therefore, if accommodations to aridity can be identified, so will many of the epiphytes' most distinguishing features. In this chapter, that challenge is met by first laying some groundwork and then examining the nature of water balance mechanisms and their influence on overall epiphyte biology.

Water use and conservation: defense against drought

All land plants must expend water in order to create biomass. As stomata open for CO2 influx, water vapor exits at a much higher rate. Xerophytic forms manage this unavoidable trade-off with suprising success: Their transpiration ratios (TRs) are in the neighborhood of 100:1, and exceptional performers do considerably better (Table 3.1). But water economy always has its price; productivity is slowed as leaf conductance falls – the lower the TR, the slower it is. In contrast, species native to humid habitats or those arid-land dwellers whose active phase coincides with the rainy season expend as much as 1000 g of water for each gram of dry matter they create. These drought-sensitive taxa serve notice that parsimonious water use is not always the best mechanism and can be decidedly disadvantageous when moisture is plentiful.

This volume represents the proceedings of a Symposium of the Plant Metabolism Group of the Society for Experimental Biology, held at the University of York in April 1987. I am most grateful to the chairman of this Group, Dr Curt Givan and the Chairman of the Publications Committee of the SEB, Professor Ken Bowler, for their encouragement to publish these proceedings. The generous financial support of the SEB is also gratefully acknowledged. Particular thanks are also due to all contributors who not only provided excellent verbal presentations but also produced manuscripts in good time.

The allocation of a Symposium to this area reflects the current interest in the physiology and biochemistry of herbicide action. Workers in the field of photosynthesis have used herbicides such as monuron and diuron as experimental tools for nearly 40 years, and as a consequence have extended our detailed knowledge of the mechanism of action of these compounds. In recent years the discovery of inhibitors of the shikimic acid pathway, of branched chain amino acid biosynthesis and of fatty acid biosynthesis, for example, has focussed much more attention on these areas of plant metabolism than there might otherwise have been.

In spite of the inevitable time lag between the presentation of papers and the publication of this volume, it is hoped that many undergraduates, research students and workers in academia and industry will find this volume of use and interest.

Abbreviations

Standard biochemical nomenclature has been used where appropriate. Trivial names and company numbers have been used to refer to some chemicals. Their structures are given in the chemical glossary, page 261.

1. chlorsulfuron (page 175)

2. sulfometuron methyl

3. imazapyr

4. imazaquin

5. AC 222164

6. N-phthalyl-L-valine anilide

7. 2-nitro-6-methyl sulphonanilide

Introduction

Sulphonylureas (E.I. du Pont de Nemours and Co) and imidazolinones (American Cyanamid Co) are new classes of herbicides characterised by low use rates (as little as 4 g/ha for some sulphonylureas), pre- and post-emergent activity and low toxicity. Variants have been developed to control weeds in a wide range of different crops.

Sulphonylureas, imidazolinones and sulphonanilides (a type of herbicide described in recent patent from Dow Co) kill plants in an identical and distinctive fashion. The symptoms of plant death first appear in the meristematic tissues where growth ceases soon after treatment. Chlorosis and the necrosis of the tissue soon follows with die back to the more mature parts of the plant taking a further 3–4 weeks. In this chapter a review of the current ideas of the mechanism of action of these herbicides will be presented. Some of this work has not been reported elsewhere.

Physiological studies of herbicide mode of action

Studies of the physiological effects of the sulphonylureas on plants provided the first clues to their mode of action. Corn seedlings stopped growing within two hours of a foliar application of chlorsulfuron (Ray, 1982a, b).

Introduction

A number of herbicides have been reported, over the years, to inhibit lipid metabolism. The effects of many of these compounds are believed to be secondary. However, three classes of herbicides may have a more specific effect on fatty acid (and lipid) synthesis. These groups of compounds are the substituted pyridazinones, thiocarbamates and a rather diverse class of graminaceae-selective herbicides which include the oxyphenoxy propionic acids and cyclohexanediones. These three groups form the substance of this brief review.

The overall topic of herbicides and lipid metabolism has been reviewed by several authors (Duke, 1985; Fedtke, 1982; Rivera & Penner, 1979; St John, 1982).

Substituted pyridazinones

The mode of action of pyridazinone herbicides has been reviewed recently and appears to involve several target sites in plants (St John, 1982; Duke, 1985). Depending on the exact structure of the compound, and the plant test species, the effects have been noted to include inhibition of photosynthetic O2 evolution, of pigment synthesis and changes in fatty acid composition.

Two substituted pyridazinones which have excited particular interest with regard to their effects on fatty acid formation are San 9785, (BASF 13 338; 4-chloro-5-(dimethylamino)-2-phenyl-3(2H) pyridazinone) and San 6706 (metflurazon); 4-chloro-5-(dimethylamino)-2-(α,α,α-trifluoro-m-tolyl)-3(2H)-pyridazinone)(Figure 1). It was noted by St John (1976) that San 9785 altered the proportions of linoleic and α linolenic acids in monogalactosyl- and digalactosyldiacylglycerol. In contrast, San 9774 merely reduced the proportion of α-linolenate in monogalactosyldiacyl-glycerol alone.

Introduction

Occurrence and spread of resistance to triazine herbicides

The first incidences of resistance in weed species to triazine herbicides occurred in 1968 in the State of Washington USA. During the 1970s and 1980s, notably in North America and mainly western Europe, and to a lesser extent in Israel in the 1980s there has been an irregular but relatively steady addition to the occurrences of new species becoming resistant mainly to triazine herbicides (but also to some others). Figure 1 gives an indication of the total number of species in different countries which are occurrences of resistance not previously recorded. Worldwide 49 species of 33 genera have become resistant to triazine herbicides (Le Baron pers. comm. 1987) and a further 11 species have evolved resistance to other herbicides.

A record of the occurrence of a herbicide-resistant biotype will often conceal the fact that numerous populations have independently evolved in many different locations over a period of just a few years. For example, in Hungary, Amaranthus retroflexus resistant to-s-triazines occurred in scores of locations and 75% of the maize growing area has become infested by the resistant biotype (Hartmann, 1979). In the USA, evolution of resistance to s-triazines in A. hybridus first occurred in Maryland in 1972 but between 1976 and 1982 there were numerous reports of resistant populations occurring throughout Virginia, New York, Delaware, Pennsylvania, Massachusetts, West Virginia and Illinois (Le Baron & Gressel, 1982; Le Baron pers. comm., 1987).

Introduction

Weed control using organic chemicals commenced just over half a century ago, when in 1932, 4,6-dinitro-o-cresol (DNOC) was first used as a weed-controlling agent. The phenoxyacetic acids such as 2,4-D followed in the 1940s. Chemical weed control was widely accepted when the ureas (1951), the triazines (1955) and the bipyridiniums (1960) became available. The latter three groups of herbicides act via the photosynthetic process. The ureas and triazines effectively block photosynthetic electron transport at the level of the Photosystem II acceptor site. Many reviews are now available on the effects of herbicides on Photosystem II, for example: Van Rensen (1982), Pfister & Urbach (1983), Sandmann & Böger (1986) and Renger (1986).

Research on the action of herbicides inhibiting photosynthesis has yielded much detailed information about their mechanisms of action. Furthermore, our understanding of the photosynthetic process has been greatly enhanced by the use of these chemicals as specific inhibitors. This chapter highlights important events of the research on Photosystem II herbicides and surveys some recent developments.

The photosynthetic electron transport pathway

The light energy conversion processes of photosynthesis are located in the grana of the chloroplasts, while the reduction of carbon dioxide occurs within the stroma. Grana consist of stacks of thylakoids, i.e. vesicle-like structures having an internal space surrounded by a membrane. The grana are interconnected by unappressed stroma thylakoids. The thylakoid membranes contain the electron and proton translocating components (Fig. 1).

Introduction

The observation reported in 1980 by Amrhein and his colleagues (Amrhein, Schab & Steinrücken, 1980; Steinrücken & Amrhein, 1980) that the herbicide glyphosate was a highly specific inhibitor of the shikimate pathway enzyme 5-enolpyruvylshikimate 3-phosphate (EPSP) synthase served to focus the attention of many agricultural scientists on the possibility of finding other herbicides which acted by inhibiting the biosynthesis of macromolecular precursors and especially amino acids. Although knowledge of most pathways of amino acid biosynthesis in higher plants was still fairly primitive the idea that amino acid biosynthetic enzymes were good targets for herbicides was soon reinforced by the recognition that the sulfonyl urea and imidazolinone based herbicides (La Rossa & Schloss, 1984; La Rossa & Falco, 1984; Shaner, Anderson & Stidham, 1984; see Chapter 7) acted by inhibiting acetolactate synthase, a key enzyme in branched chain amino acid biosynthesis, and phosphinothricin (Leason et al., 1982; see Chapter 8) acted by inhibiting glutamine synthetase. All these compounds had resulted from random screening procedures but it is now widely believed in the agrochemical industry that it should be possible to accelerate the development of new herbicides by the judicious application of knowledge of the biochemistry and molecular biology of amino acid biosynthesis.

The principal information required for rational herbicide design is the structure and mechanism of the target enzymes. This immediately highlights a difficulty. There was, and continues to be, a general lack of mechanistic and structural information for plant amino acid biosynthetic enzymes.

Introduction

Most herbicides on entering the target plant undergo some metabolic transformation. This generally results in a loss of biological activity but there are a few instances where the parent molecule becomes activated in the plant.

Although most proherbicides or those which require bioactivation were almost certainly discovered by chance, it may be interesting to consider whether this feature has any significance or is just a scientific curiosity. Possible advantages may be summarised:

1. the proherbicide may have superior physical properties from the point of view of penetration or stability.

2. the bioactivation mechanism may alter the selectivity of the compound in a useful manner.

3. the reactivity of compounds may be toned down by the presence of protecting groups, allowing better distribution, especially if the activating mechanism is located near the site of herbicidal action. An extreme case of this might be a suicide inhibitor of an enzyme, although no herbicides have been reported to have this mechanis.

4. delayed release of the active herbicide may be a desirable feature allowing better distribution and a more prolonged effect.

These are some of the possible advantages of proherbicides, but the knowledge that bioactivation is occurring is essential if the mode of action and structure: activity relationships of an herbicide are to be clearly understood. For example, one explanation for the situation with the imidazolinones where activity against the target enzyme is up to a thousand fold less than that against intact cells could involve some form of bioactivation.