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Bioactive Chemicals and Biological--Biochemical Activities and Their Functions in Rhizospheres of Wetland Plants.

I. Abstract

Wetland soils provide anoxia-tolerant plants with access to ample light, water, and nutrients. Intense competition, involving chemical strategies, ensues among the plants. The roots of wetland plants are prime targets for root-eating pests, and the wetland rhizosphere is an ideal environment for many other organisms and communities because it provides water, oxygen, organic food, and physical protection. Consequently, the rhizosphere of wetland plants is densely populated by many specialized organisms, which considerably influence its biogeochemical functioning. The roots protect themselves against pests and control their rhizosphere organisms by bioactive chemicals, which often also have medicinal properties. Anaerobic metabolites, alkaloids, phenolics, terpenoids, and steroids are bioactive chemicals abundant in roots and rhizospheres in wetlands. Bioactivities include allelopathy, growth regulation, extraorganismal enzymatic activities, metal manipulation by phytosiderophores and phytochelatines, various pest-control effects, and poisoning. Complex biological--biochemical interactions among roots, rhizosphere organisms, and the rhizosphere solution determine the overall biogeochemical processes in the wetland rhizosphere and in the vegetated wetlands. To comprehend how wetlands really function, it is necessary to understand these interactions. Such understanding requires further research.

II. Introduction

The rhizosphere is the volume of soil surrounding the plant root and interacting with it (Curl & Truelove, 1986). Some critical features distinguish the rhizospheres of wetland plants from those of terrestrial plants. The main difference is the water that surrounds the roots in wetland plants, as opposed to the air spaces around the roots of terrestrial plants. Because of the slow rate at which gases diffuse through water, rhizospheres of wetland plants are often limited in oxygen, supplied there almost exclusively by the plant root itself (e.g., Brix & Schierup, 1990; Armstrong et al., 1992). On the other hand, being flooded makes the rhizospheres of wetland plants more accessible to water-carried chemicals and organisms from the bulk soil than are terrestrial rhizospheres.

Flooded anaerobic soils are considered hostile to plants (e.g., Mitsch & Gosselink, 1993). According to this view, plants in flooded soils are constantly stressed. They survive only if they can counteract the suffocation of their roots. Usually, their defenses involve root aeration and detoxification of anaerobic metabolites (reviewed extensively in Crawford, 1987; Blom, 1990; Gopal & Masing, 1990; Crawford & Braendle, 1996). Yet it is apparent that for those plants that can protect their roots from anoxia and its resulting toxins, the wetland soil is a very suitable environment. The flooded soil, cleared of its taller vegetation by the anoxia, provides the plant with its most basic and essential requirements: access to light from above, water and nutrients from below, and room to expand.

In the hostile anaerobic bulk soil the rhizospheres of wetland plants create oxidized oases for various benign and pest microorganisms (e.g., Lee & Baker, 1973; Meyers, 1974) and small animals (e.g., Prejs, 1977; Osenga & Coull, 1983). Some of them could be expected to quickly consume the roots, yet this often happens only after the plant dies (cf. Verhoeven, 1986). Life in such a demanding environment has required the development of a large array of interesting, and often unique, defensive and aggressive chemical and biological-chemical processes in the flooded rhizosphere and around it, to aid in plant--pest and plant--plant competition.

Pest-control chemicals in the root may slow its consumption by pests. These chemicals can have also medicinal properties, which have not always been scientifically studied. However, healers in traditional cultures may have used such medicinal properties.

Thanks to the proximity in the rhizosphere of anaerobic and aerobic zones, and of steep gradients in oxygen (e.g., Andersen & Kristensen, 1988) and nutrients (e.g., Bottomley & Bayly, 1984) perpendicular to the rhizoplane--the external surface of the root--the most interesting and significant biogeochemical processes of the flooded soil, and the densest microbial populations, occur there (see Ogan, 1982, and Laanbroek, 1990; the early literature on this subject is well reviewed in Makulova, 1970; Ulehlova, 1976). Furthermore, the total surface area of the anaerobic-aerobic plane around the rhizospheres in densely vegetated wetlands can be much larger than the area of the horizontal sediment--water or anaerobic--aerobic interfaces (e.g., Smith et al., 1979; Francour & Semroud, 1992). Thus it is likely that the processes occurring in the rhizosphere have quantitatively more influence on the total biogeochemical processes in the wetland than does the horizontal sediment--water interface, although the latter is more conveniently studied. There has therefore been a rising recognition that understanding wetland biogeochemistry requires understanding of rhizosphere processes (e.g., Doyle & Otte, 1997; Havens, 1997; Hsieh & Yang, 1997).

Yet there is a shortage of data on these multidisciplinary issues; wetland processes and functions have typically been studied by specialists. For instance, soil biogeochemists have studied the physical, thermodynamic, and chemical factors that control biogeochemical processes in wetland soils (see Mitsch & Gosselink, 1993). These scientists have often studied the soil--water interfaces of wetlands with soil cores and slurries but have excluded their rooted plants. Similarly, microbiologists have studied microorganisms and the processes they mediate, necessarily often in pure cultures or in sediment slurries, but without plants. Therefore, much is known about the different microbial groups of flooded soils, their requirements, and their activities in cultures (e.g., Laanbroek, 1990) but not in situ. The plants themselves have often been studied by botanists, plant physiologists, and ecologists, who often have not incorporated the soil and microbial disciplines into their research. Frequently, the first stage in preparing a wetland plant for an experiment is brushing and rinsing off the soil from the roots. Therefore, there is much greater understanding of the physiological adaptations that allow plants to live in flooded soils (Blom, 1990; Armstrong et al., 1991) than of their chemical--biochemical interactions with rhizosphere organisms and chemicals (Braendle et al., 1996). It is revealing to note that when wetland soils were studied with the plants in them--for example, in relation to wastewater treatment (see Reddy & Smith, 1987)--the plant-soil complex was considered a "black box." Insufficient attention was often paid to the quantitative details of the chemical-biochemical interactions of the plant, its rhizosphere, and the microbial communities in and around it (Hackney, 1987; de la Cruz et al., 1989). The oxygen regime in wetland rhizospheres (e.g., Armstrong et al., 1991) and root exudates as suppliers of degradable organic carbon to the rhizosphere (e.g., Wetzel, 1992) are favorable exceptions; that is , they are well studied with respect to the overall ecosystem.

There is also a growing body of evidence that the oxygen pumped to the soil by the plants controls many important biogeochemical and biological activities and processes. For instance, it was recently suggested that the overall rate of methane release to the atmosphere in a peatland is controlled by the supply of oxygen to the rhizosphere of the aquatic macrophyte Sparganium eurycarpum (King, 1996). However, we believe that the subject of oxygen supply to wetland rhizospheres is sufficiently dealt with in the literature. Root-pathogen interactions have also been well documented, but primarily in agricultural crops (rice, water hyacinth). Complex chemical and genetic controls were indeed found in many such cases (Dixon & Lamb, 1990). Unfortunately, not enough is known about such interactions in natural wetlands. A study of iron oxide deposition on roots of rice (Oryza sativa; Johnson-Green & Crowder, 1991) and a study of N-cycling in the wetland rhizosphere (Reddy et al., 1989), where root-rhizosphere interact ions were investigated in detail, indeed provided insight into the overall interactions in the rhizosphere. But such studies are scarce. Some of the research that did integrate rhizosphere microbiological processes and interactions has been reviewed in a series of articles by Gunnison and Barko (1988a, 1988b, 1989; Barko et al., 1991) and others (Carpenter & Lodge, 1986; Waisel & Agami, 1996).

Obviously, isolating the components of an ecological system is necessary for understanding how they function. However, the complete ecological picture may become blurred by such practices. Therefore, the application of experimental results to natural systems is often difficult or speculative and leads to unpleasant surprises. For instance, in a study of lacustrine sediments Kepkay (1985) described unexpectedly strong and unexplained inhibition of manganese oxidation and nitrification by roots (see other examples in Burdick et al., 1989, and in Gangawane & Kulkarni, 1985).

The gathering of information available on wetland rhizospheres from as many disciplines as possible will allow a more comprehensive understanding of the functioning of vegetated wetlands. Moreover, pointing out rhizosphere processes and functions that have been documented in nonwetland plants can aid in formulating plans for research on such issues in wetlands. We hope to point out issues for which there are gaps in the scientific knowledge and to stimulate interest in filling them. In the present article, the first in a series (two other publications will describe microbes and animals of wetland rhizospheres and their interactions with the plant root and its environment), we synthesize published evidence on bioactive chemicals and biological-biochemical activities and their influence on the functioning of wetlands. In several cases we believe that similar phenomena are likely to be found in wetlands if looked for, so we have presented the relevant information from nonwetland environments. We then use the ev idence to suggest lines of research necessary to interpret this information in the context of the functioning of a wetland. We hope to complement previous reviews on more specific wetland subjects (such as Hook, 1984; Kozlowski, 1984; Blom, 1990; Armstrong et al., 1991).

III. Biological Activities of Chemicals from Wetland Plants

Bioactive plant chemicals modify the activity of organisms (Rinehart et al., 1990). Plant chemicals that inhibit organisms that damage the plant are considered natural pest-control chemicals. Carpenter and Lodge (1986) expressed the notion that aquatic plants usually lack grazing deterrents. However, as we shall show, this is not true. Even in grasses, not known for their bioactive chemicals, genera with widespread wetland species--Panicum and Phalaris--have been reported to contain effective toxins (Cheeke, 1995). Other rhizosphere organisms in wetlands also produce bioactive chemicals, which can influence the biological-biochemical functioning of the rhizosphere. In this section we shall review the most studied chemical and biological activities that are or can be associated with wetland rhizospheres.


The potential role of plant poisons in the defense of the plants is straightforward. Quite a few wetland plants are poisonous to animals, especially in the Nymphaeaceae, Rannunculaceae, and Umbiliferae (Table I; Muenscher, 1975; for a review of toxic plant proteins, see Tu & Miller, 1992). Moreover, most of the typically "poisonous" plant families have wetland members (Table V). The natural role of these poisons is presumably protection of the whole plant against grazing animals, but often the roots are more toxic than is the rest of the plant (Grainge & Ahmed, 1988). There are also reports of antiplant poisons--natural herbicides--in the roots of several wetland plants (Grainge & Ahmed, 1988).

Unfortunately, studies of plant toxicity and general pest-control activity often do not identify the chemicals. For instance, Ceratophyllum plants protect themselves from herbivores by unidentified repellent substances (Bronmark, 1985), and aquatic plants of several genera--Lyonia, for example--produce effective hemolytic piscicides (Bhatt & Farswan, 1992). Plants in the widespread generaXanthium, Scirpus, Typha, and Phragmites produce unidentified fungicides, bactericides, and larvicides (briefly reviewed by Laksman, 1987). Typha and Eleocharis also produce selective algicides (Aliotta et al., 1990). That aquatic plants have traditionally provided man with poisons against fish and other aquatic animals is indicative of the prevalence of poisons in roots of wetland plants (see Costa-Pierce et al., 1991).


It has often been observed that certain live plants are not attacked by pests and herbivores. As we discuss below, plants have several mechanisms for achieving pest-control results in their rhizospheres. One of them is pest-control chemicals (another common approach in plants is localized hypersensitivity to the pathogens, as described in Smith, 1989). These chemicals can be antimicrobial, insecticidal, or poisonous, as described above. To influence the rhizosphere, these chemicals do not have to be actively exudated, Often significant release rates result from root growth, dying root cells, and sloughing off cells. Furthermore, when pests attack the root tissue, the dead or injured tissues release those chemicals at the attacked point, thus locally protecting the plant from further damage (Smith, 1976).

More than 2,000 plants are known to have pest-control chemicals (Balandrin et al., 1985; Grainge & Ahmed, 1988). Much of the information on pest-control chemicals in wetland and aquatic plants is from economically important rice. The documented cases regarding resistance of rice varieties to insects, for example, include several volatile repellents and phenolic feeding deterrents found in all organs of the plant (reviewed by Smith, 1989). But reports exist for other plant species as well. Exudates of the aquatic fern Salvinia auriculata inhibited the breeding of the mosquito Anopheles albimanus (Hobbs & Molina, 1983), and a petroleum extract from the roots of the mangrove plant Heritiera littoralis was a piscicide (Miles et al., 1989). In a more complex case, the inhibition of microbial organic-matter decomposition in the rhizosphere of Pinus radiata was attributed to exudates not from the root but from its symbiotic mycorrhiza (Gadgil & Gadgil, 1975). The antibacterial activity of root exudates from wetland plants is widespread (Gopal & Goel, 1993). The plant genera involved included Nuphar, Scirpus, Acorus, Juncus, Iris, Mentha, Phragmites, Alnus, Lemna, Nymphaea, Carex, Vallisneria, Potamogeton, Typha, and several aquatic angiosperms.

Smith (1976) described important bioactive chemicals typical of certain plant families. The important bioactive chemicals of plant origin are anaerobic metabolites (organic acids, alcohols), alkaloids, phenolics, terpenoids, steroids, and hydrogen cyanide (HCN). Intuitively, a chemical can have more than one function or bioactivity in the plant and its environment.

1. Anaerobic Metabolites

In the broad sense, anaerobic metabolites can be inhibitory to plants and various other organisms. Elevated [CO.sub.2] concentrations or large pH and ionic shifts created in their rhizosphere or by their roots can make the plants toxic (see Hook, 1984). A well-known example is that of plants from the Sphagnaceae, which by exchanging ions with their surroundings reduce the pH until it becomes detrimental to most other plants and to many microorganisms or animals (Dickinson, 1983; Mason & Standen, 1983; Speight & Blackith, 1983). However, the pH changes can also depend on the chemical form of plant nutrition. For instance, [N.sub.2] fixation and ammonia uptake lead to decreased pH, but nitrate uptake leads to increased pH. There are also interesting interactions among root exudates, rhizosphere pH, and the uptake of such micronutrients as iron and zinc in wetland rice (Kirk & Bajita, 1995).

Plants adapted to waterlogging, such as the willow (Salix alba), mannagrass (Glyceria aquatica), and rice (Oryza sativa), exude glycolytic products to the rhizosphere under waterlogged conditions (Cirkova, 1978; Hook, 1984; Smith et al., 1986). Products such as alcohols and organic acids (lactate, malate) can be toxic to plants, animals, and microorganisms. The roots of the wetland plants themselves have some resistance to them. Such metabolites can be respired in the root itself, when oxygen becomes available, or they can be transported to aerial parts of the plant for detoxification by oxidation (Crawford, 1987).

2. Alkaloids

Alkaloids, the most studied--and useful to man--biologically active plant-produced chemicals, exist in several plant families with wetland or aquatic species (Table III). Clark et al. (1985) extracted several antibacterial and antifungal alkaloids from tissues of the yellow poplar or tulip tree, Liriodendron tulipifera (Magnoliaceae). Alkaloids are also produced by the roots of Cassia fistula (Sinha et al., 1992). Unfortunately, few of the specific wetland members of many of these families have been examined for their alkaloids. For instance, roots in species of the Annonacea family, which include the wetland tree Annona glabra, produce tannins and alkaloids (Lewis & Elvin-Lewis, 1977).

3. Phenolics

Phenolic compounds are widespread in plants, including those from wetlands. They can be rather poisonous to microorganisms and aquatic animals (e.g., Green et al., 1985). Many of the documented plant-produced pest-control effects are caused by chemicals of this family. Sarkar et al. (1988) described an effective pest-control and deterrent phenolic compound from the roots of the wetland plant needle rush, Juncus roemerianus. This explains earlier observations of herbivores' avoidance of this plant. Phenolics extracted from Typha roots have been shown to be algicides (Aliotta et al., 1990). Biologically active phenolics have also been extracted and identified from roots of the widespread Nuphar variegatum (Nishizawa et al., 1990), Urtica dioica (Kraus & Spiteller, 1990), and Myriophyllum verticillatum (Aliotta et al., 1992). Some of the most common wetland plants--the genera Phragmites, Asciepias, Phalaris, Spartina, Sphagnum, and Euphorbia--have been shown to release phenolics to their rhizospheres (cf. Dicki nson, 1983). Various plant genera that contain wetland species have been suggested to inhibit with phenolic compounds nitrifying bacteria--competitors for oxygen and ammonia--in their rhizosphere (reviewed briefly in Cooper, 1986; see also Hedges & Messens, 1990).

Because phenolic compounds are intermediaries in the pathways of several important biochemical processes, some plants and soil microbes can metabolize external phenols as well. Brummet and O'Keefe (1982), following an earlier report by Wolverton and McKown (1976), observed in water hyacinth roots the uptake and translocation of externally administered phenolic compounds to the aboveground parts for metabolism. This activity could be induced, and preexposure of the plants to 25-100 mg/l of phenol doubled their tolerance for the chemical, to up to 400 mg/l. Potential targets of plant-bioactive chemicals, soil microbes have been shown to consume phenolic compounds, thus protecting themselves, neighboring organisms, and plant roots (Gunnison & Barko, 1988a).

Betalains are pigmented nitrogenous phenols found only in the plants of the order Centrospermae (Smith, 1976). They give these plants, such as red beets, their typical color and are also effective insect repellents. Several families in this order have genera of wetland plants, such as the Aizoaceae (Sesuvium), Polygonaceae (Rumex, Polygonum, Brunnichia), Chenopodiaceae (Halimione, Chenopodium, Atriplex, Salicornia, Suaeda), Amaranthaceae (Amaranthus, Acnida), and Portulacaceae (Montia).

Phenolic compounds in the rhizosphere can also be of microbial origin. Certain soil microorganisms release phenolics, perhaps in self-defense (cf. Dickinson, 1983; Laksman, 1987; Gunnison & Barko, 1988a, 1989; Lynn & Chang, 1990). Once in the rhizosphere, such potent chemicals can interfere with any biological activity around and in the roots. Microbial phenolics have been implicated in affecting rhizosphere processes, such as plant-microbe host-symbiont recognition and specificity (Lynn & Chang, 1990). Yet there is little specific information on phenolic compounds in wetland plants and on their role in the functioning of the rhizosphere.

4. Terpenoids and Steroids

Terpenoids and steroids, including the carotenes, rubber, and several plant hormones, are common plant chemicals, which are potent in several bioactivities, in particular antifungal roles (Smith, 1976). Many of these chemicals are grazing repellent, causing a bitter taste and bad physiological reactions in animals and insects. Some terpenoids are water soluble and bind well to soil, thus maintaining their activity there for a long time. Some of them have been associated with allelopathy in the wide sense. Cineole and camphor, in particular, are inhibitors of seed germination. In waterlogged soils, terpenoids and steroids deactivate free soil enzymes (Wetzel, 1991).

Terpenoids have been found in the roots of wetland plants, such as Urtica dioica, whose common name "stinging nettle" perhaps reflects the effect of the chemicals (Kraus & Spiteller, 1991).

5. Other Chemicals

Many bioactive chemicals are less widespread. Beta-ecdysone, for instance, is an insect feeding deterrent that effectively inhibits insect development (Smith, 1976). It has been found only in the Taxaceae and Podocarpaceae of the gymnosperms, some of which inhabit wetlands. Rhizomes of Urtica dioica produce an antifungal lectin (Broekaert et al., 1989). The plants from several families that include wetland species produce nonprotein amino acids, shown to inhibit or kill insects and microbes (Smith, 1976). Plants from the family Annonaceae, which includes the wetland tree Annona glabra, produce derivatives of fatty acids with potent biological activities, some of which have medicinal uses. Documented bioactivities of this source are cytotoxic, antitumor, antimalarial, antimicrobial, immunosuppressant, antifeedant, and pesticidal (cf. Rupprecht et al., 1990). Long-chain fatty acids are biologically active chemicals characteristic of aquatic plants (Gopal & Goel, 1993), and they have been implicated in allelopa thic interactions of Polygonum, Eleocharis, Potamogeton, Najas, Thalassia, Ruppia, and Typha. Elemental sulfur release has been also reported by several aquatic plants, including Ceratophyllum demersum (Gopal & Goel, 1993).

Some plants produce phytoalexines and HCN to fight the invaders (Lynch, 1990; Isaac, 1992). Table IV presents the families in which HCN was been shown to be produced and the typical wetland genera belonging to these families. Apparently, some of the most common wetland plants belong to such families. It seems reasonable to suggest further investigations on the role of HCN in rhizosphere functioning in these plants.

Agriculturally important plant-produced insecticides are also found in wetland plants. Rotenone, a potent and useful pesticide, is found in roots of the genus Pieris (Ericaceae; Grainge & Ahmed, 1988), which includes the wetland plant fetter bush (Pieris floribunda). Pyrethrins are also agriculturally important insecticides that occur in plants of the Pyrethrum genus, which contains wetland species.


1. Extracellular Enzymatic Activity

The rhizosphere of the wetland plant can be considered a "soup" of extracellular enzymes. Although some enzymes are actively secreted, many of them simply exude from cells that are broken in the natural process of root growth and the emergence of adventitious roots. Free enzymes are important in the aquatic environment, especially the rhizosphere (Jandera et al., 1989; Wetzel, 1991, 1992). They can be of plant, microbial, or animal origin, and they have different functions. Their activity can be preserved for some time. Toth and Zlinszky (1989) showed that upon the death of the organism, the enzymes of the electron-transport systems of many flooded-soil organisms can keep functioning and enhancing the breaking down of organic matter for weeks. Live roots of axenically cultured plants released phosphatases, invertases, proteases, and peroxidases, all of which could participate in the biogeochemical cycling of compounds (cf. Wetzel, 1991). Ammerman (1991) and Cotner and Wetzel (1991) reviewed different systems of extracellular enzymes that perform important functions in the regeneration and metabolism of phosphorus in the aquatic environment. Apparently, extracellular enzymes can also carry out significant rates of nitrification in flooded soils (van Cleemput & Patrick, 1974). Rhizosphere microbes, particularly pathogens, produce pectinolytic enzymes and cutinase with a specific role: to penetrate the root. Some roots, in turn, produce glucanase to damage the walls of fungal pathogens.

Enzymatic activity is higher in the rhizosphere of terrestrial plants than elsewhere in the soil (Jandera et al., 1989; Lynch, 1990). In flooded soils enzymes are often inhibited by complexation to humic and fulvic substances (Wetzel, 1991, 1992). Tannins in particular bind proteins into indigestible and often inactive complexes (Mandava, 1985; Wetzel, 1991). The in situ function of extracellular enzymes is responsive to environmental conditions, such as redox potential or pH (Benner et al., 1989). Enzymes in flooded organic soils, even if inactive under anaerobic conditions, accelerate the breakdown of nonhumified organic matter upon oxidation (Mathur & Farnham, 1985). The activities of peat enzymes, either intracellular or extracellular--cellulases, proteases, and polyphenoloxidases--indeed increased dramatically upon soil oxygenation (Lahdesmaki & Piispanen, 1990). Such activity led to the quick release of various nutrients, especially amino acids and ammonia, to the interstitial waters. Because roots of wetland plants modify the pH and increase the redox potential in their rhizosphere, it appears that they influence extracellular enzyme activity there. The evidence of active free enzymes in wetland rhizospheres is particularly intriguing in another sense. As we observed above, free enzymes may be inactivated and preserved by tannins and other chemicals in the bulk anaerobic soil, and reactivation can occur upon oxidation. This raises the possibility that the wetland plant, upon oxygenation of new domains by its expanding root system, practically "releases" bound enzymes, thus enhancing the breakdown of organic matter and supplying itself with remineralized nutrients.

2. Growth Regulators (Hormones)

Plant-growth regulators found in the soil are produced not only by plants but by other organisms as well. Plant hormones can influence various physiological processes in plants even when administered through the water. If a hormone released by one plant interferes with the normal growth of another, it can be interpreted as allelopathy (see below). Solutions of plant hormones, even in low concentrations (0.01 mg/l of abscisic acid), when applied to water hyacinth, caused significant changes in its metabolism (D'Angelo & Reddy, 1987). Earlier such observations led to the use of the floating Lemna in plant-hormone bioassays. The effects of auxins, gibberellins, cytokinins, abscisic acid, ethylene, and salicylic acid on Lemna were reviewed by Cleland et al. (1982) and by Mitsch and Gosselink (1993). Laksman (1987) reviewed reports that Typha and Eleocharis produced and released plant-growth-stimulating hormones. There are also many such reports for the water hyacinth (e.g., Sicar & Chakraverty, 1968).

Ethylene, an important plant-growth hormone that is produced microbially and by roots in flooded soils (Howarth et al., 1988), also influences other rhizosphere processes, such as the inhibition of ammonia oxidation (Porter, 1992). Although ethylene is produced microbially in flooded soils from phenolic acids, it is also bacterially oxidized there (Gunnison & Barko, 1988a). Ethylene is quickly degraded in flooded rice rhizospheres (Yoshida & Suzuki, 1975; Armstrong, 1979). Other hormones, such as salicylic acid (SA), are also released to the rhizosphere from the root. Neori, Kane, and Raskin (unpublished) found that SA release from the seedling roots of several tissue-cultured aquatic plants (Orontium, Pontederia, and Sagittaria) reached tens of micromoles [1.sup.-1] and 1% of plant dry weight within 3-4 weeks. SA, at concentrations as low as 10 micromoles [1.sup.-1], significantly inhibited potassium uptake in roots of terrestrial plants (Putnam, 1985) and is likely to do the same in wetland plants.

Soil microbes also produce and modify other plant hormones to control their environment. Azospirillum brasilense, a nitrogen fixer in the rhizosphere of various grass species--in particular, wetland rice--released indole lactic acid, gibberellin, and other hormones.

3. Phytosiderophores

Insoluble ferric iron ([Fe.sup.3+]) often concentrates as a precipitate in the rhizospheres of wetland plants (Johnson-Green & Crowder, 1991), where it diffuses as soluble ferrous iron ([Fe.sup.2+]) from bulk anaerobic soil. Phytosiderophores are nonproteinogenic amino-acid root exudates that complex and dissolve ferric iron. In the Graminae, which include many wetland species, these molecules complex the ferric iron and are taken up by the root via a highly specific uptake system (Marschner et al., 1986). Other plants, lacking such an uptake system, can then become iron deficient in a phenomenon that appears like allelopathy when the siderophore released by a plant inhibits growth of another plant. Phosphate precipitated with ferric iron becomes available for plant uptake by the siderophore activity. The process is not sensitive to high pH or bicarbonates, and this gives grasses an advantage over other plants in soils with such conditions. This probably explains why the resistance of several rice varieties to alkaline iron deficiency, or "lime chlorosis"--a typical disease of paddy-rice seedlings in alkaline soils--correlated with their ability to release phytosiderophores (Marschner et al., 1986). Tagaki et al. (1984) showed that rice released to the soil solution mugineic and avenic acids, two nonproteigenic amino acids that effectively chelate ferric iron. Mon et al. (1991) showed that deoxymugineic acid is produced in the rice root, secreted to the rhizosphere, chelates ferric iron, and transports it into the cells via a specialized transporter of deoxy mugineic acid-[Fe.sup.3+] If the seedlings were not allowed sufficient time to produce this phytosiderophore, they suffered chlorosis and could not develop properly. Certain phytosiderophores can also aid in the uptake of other metals, such as copper, manganese, and zinc (Romheld, 1991).

Most bacteria need bioavailable iron at concentrations much greater than higher plants need (1 micromolar for bacteria, versus 1 nanomolar for plants; see Hemming, 1986). Flooding and the solubilization of iron following anaerobiosis therefore stimulate the activity of some iron-limited soil bacteria. However, in the oxidized rhizosphere the bacteria may still need siderophores to obtain their iron. Mycorrhiza and other fungi also produce siderophores for this reason. Lynch (1990) described several studies of the complex role of microbially produced siderophores and other ionophores in plant nutrition under flooded conditions. Hydroxamate siderophores exist in certain soils at levels that significantly affect the bioavailability of iron (Hemming, 1986). Some siderophores found in nonflooded soils are produced by microbes, such as the fluorescent Pseudomonas syringae, P. fluorescens, and P. aeruginasa. These fluorescent pseudomonades also inhibit plant pathogens (Hemming, 1986). There is no reason for the sit uation to be different in wetland plants. Indeed, Pseudomonas sp. was also described from the rhizoplane of rice (Asanuma et al., 1980), where it inhibited fungal pathogens (Lee et al., 1990).

4. Heavy-Metal Binders and Phytochelatins

Plant roots exude a variety of organic chemicals, such as organic acids, with strong binding capacities for heavy metals (Smith et al., 1982; van Steveninck et al., 1987, 1990). These chemicals protect all the organisms that share the rhizosphere from heavy-metal toxicity. The result seems to be that rhizoplane microbes are more sensitive to heavy-metal toxicity than are rhizosphere microbes (Smith et al., 1982). Several aquatic and wetland plants, especially floating ones such as Azzola and the water hyacinth, have been shown to have metal-binding peptides (Zolotukhina et al., 1989), to absorb heavy metals from the water, to accumulate them in their roots and upper parts (Wolverton & McDonald, 1978; Sela et al., 1988), and to have some resistance to their toxicity (Nir et al., 1990). Similar observations have been reported for the emergent macrophyte Sparganium androcladum (Balch & Jones, 1991).

Phytochelatins may be the principal heavy-metal complexing peptides of higher plants (Grill et al., 1985; Steffens, 1990). They are metallothionein-like in function but differ in their chemical structure and composition (L-cystein, L-glutamate, and glycine at a ratio of 4:4:1). The synthesis of these peptides can be induced by copper, mercury, lead, and zinc. Their chemical formula seems similar for all metals and for all plants examined. Phytochelatins have been reported from several aquatic and wetland plants as well. Salt et al. (1989) and Robinson and Thurman (1986) found such copper-binding peptides in Mimulus guttatus, and water hyacinth contained peptides that bound cadmium (Fujita & Kawanishi, 1986; Fujita & Nakano, 1988).

Other organic compounds of plant origin also bind heavy metals in the aquatic environment. Wetzel (1991) discussed the role of plant-derived humic substances in detoxifying heavy metals in wetland and aquatic environments. Thurman and Rankin (1982) reported on the role of organic acids in zinc tolerance by Deschampsia caespitosa. Neori, Bitton, Kane, and Clark (unpublished) have observed significant detoxification of copper by as-yet-unidentified root exudates from axenic arrowhead (Sagittaria sp.) seedlings.

Chelating substances may have other effects in the rhizosphere, which deserve further research. The chelating chemical EDTA is toxic to plants because it complexes essential metals and makes them unavailable (Karataglis, 1978).

5. Allelopathy

Allelopathy is the inhibition of one plant species through chemical means by another plant (Szczepanski, 1977; Rice, 1984; Friedman & Waller, 1985; Putnam, 1985). The issue of allelopathy may be controversial, particularly with aquatic plants (cf. Inderjit & de Moral, 1997). However, the authors of two excellent reviews have evaluated and discussed it in detail and have shown the ecological relevance of allelopathy in wetlands (Gopal & Goel, 1993; Hootsmans & Blindow, 1994). In the present discussion, we have tried to avoid semantics and consider allelopathy in its widest functional connotation, including even plant-inhibiting chemicals produced by microbial modification of the plant exudates or released from decaying plants.

Allelopathy between wetland plants has been observed often, both experimentally and in the field (e.g., Cheng & Riemer, 1988; see the comprehensive review in Gopal & Goel, 1993). In a recent study, Hizkiahoo-Shak (1996) reported on numerous experimental instances of specific apparent allelopathic interactions among aquatic macrophytes. Some of the most widespread wetland plants have been reported to be involved in allelopathic interactions. According to Elakovich and Wooten (1987b, 1989), Gopal and Goel (1993), and Szczepanski (1977), allelopathic chemicals and interactions occur in many wetland genera, including the widespread Acer, Carex, Cyperus, Eleocharis, Hydrilla, Myriophyllum, Panicum, Peltandra, Phragmites, Potamogeton, Polygonum, Sagittaria, Smilax, and Typha (Table I). Agami and Waisel (1985) described specific allelopathic bilateral inhibition of growth between Najas marina and Myriophyllum spicatum. They also reviewed other such cases involving Ceratophyllum, Hydrilla, Typha, and Vallisneria. Pl ants of the genera Ambrosia, Peltandra, Bidens, and Typha were shown to produce plant-growth inhibitors (Thompson, 1985; briefly reviewed in Laksman, 1987). Plants in the genera Cyperus, Digitaria, and Euphorbia, all of which include aquatic species, show widespread allelopathic activity (Elmore, 1985). The water shield (Brasenia schreberi) produced strongly allelopathic chemicals (Elakovich & Wooten, 1987a). Both it and the spikerush (Eleocharis spp.) often keep other plants and algae out of their neighborhood. Eleocharis coloradoensis showed effective allelopathy toward Potamogeton sp. and Elodea sp. (Frank & Dechoretz, 1980). It is therefore obvious that allelopathy is a driving force in the creation of a wetland plant community.

Unfortunately, the chemicals involved have not been identified in many functional studies and observations of allelopathy between wetland plants (Gopal & Goel, 1993). However, there is a growing body of identified allelopathic chemicals from wetland plants and their roots (cf. Gopal & Goel, 1993). Allelopathic chemicals belong to several chemical groups, particularly phenolics (Hagland & Williams, 1985), organic acids (Rao & Mikkelsen, 1977), plant hormones and metabolites of plant-aromatic amino acids (Gunnison & Barko, 1988a, 1989), alkaloids, flavonids, terpenoids, steroids (McClure, 1970), long-chain fatty acids, alomones, and elemental sulfur (cf. Gopal & Goel, 1993).

Eleocharis is perhaps the most studied wetland genus concerning chemicals and mechanisms involved with its allelopathic capability (Elakovich & Wooten, 1987b). Anderson (1985) and Stevens and Merrill (1980) reported on dihydroactinodiolide (DAD) from Eleocharis sp. and on the inhibitory effects of this compound on other aquatic plants, such as Potamogeton nodos. The allelopathic chemicals are released either actively to the rhizosphere in soluble or volatile forms or only as cells die, slough off, or are attacked by pathogens (Putnam, 1985).

Several bioactive chemicals produced by plants and soil microbes persist longer in anaerobic soils than in aerated ones. For instance, humic and fulvic acids, anaerobic metabolites that persist in wetland soils and rice paddies, inhibited growth of other plants through inhibition of nodulation (Hagland & Williams, 1985). Because the same process may occur with other allelopathic chemicals, allelopathy may be more effective in wetlands than in terrestrial ecosystems (cf. Gunnison & Barko, 1988a), even though the root-to-shoot ratio in aquatic plants is much lower than is that of terrestrial plants.

The exact mechanism of allelopathic inhibition in the soil is usually not identified unequivocally, but seedlings of sweetgum (Liquidambar styraciflua) had their mineral compositions changed upon exposure to rhizosphere exudates of the fescue Festuca arundinacea (Walters & Gilmore, 1976). DAD from Eleocharis sp., mentioned above, at concentrations above 5 mg/l, inhibited seed germination and seedling growth in other aquatic plant species (Ashton et al., 1985).

Allelochemicals often have medicinal properties. Members of the Asteraceae family, including such wetland genera as Baccharis, Bidens, Callilepsis, Erigeron, Franseria, and Parthenium, often produce an effective allelochemical, sesquiterpene lactone (Stevens & Merrill, 1985). In a case discussed in the section on chemicals with medicinal properties, a macrocyclic trichothecene mycotoxin with a phytotoxic activity is produced by the rhizosphere fungus Myrothecium spp. Baccharis megapotamica, which is not sensitive to the toxin, slightly metabolizes the chemical, making it more phytotoxic and also, incidentally, anticancerous (Jarvis et al., 1985). Nicollier et al. (1985) found phytotoxic chemicals in plants of the wetland genera Erigeron, Euphorbia, Polygonum, and Smilax. Their allelopathic compounds--coumarin, o-coumaric acid, and melilotic acid--are also antibacterial.

Macrophyte--algal antagonism is widespread and has often been shown to be chemically based. Van Aller et al. (1985) reported on the inhibition of algae--and zooplankton--by chemicals extracted from Potamogeton foliosus and Anacharis canadensis. Oxygenated fatty acids present in water extracts of Eleocharis microcarpa strongly inhibited many bloomforming algal species, especially cyanobacteria. Similar compounds were also found in extracts from other aquatic species of the genera Potamogeton, Najas, Thalassia, Ruppia, numerous algae, and water from several natural ponds, especially one with dense stands of Eleocharis microcarpa.

Apparently, allelopathic chemicals are released to the environment under natural conditions. Leon (1992) examined the literature on allelopathy in the marsh plants Spartina patens, Distichlis spicata, Juncus roemerianus, and Scirpus olneyi. Chemical competition in the soil, between the underground parts of the plants, was considered prominent in determining the density and distribution of the four species. Saxena and Kulshreshtha (1992) reported that decomposing roots of Lantana sp. inhibited and killed water hyacinth. The latter weed, however, was shown to be able to protect itself from allelopathic interference: It could effectively metabolize certain phenolic compounds with allelopathic activity, particularly phenol itself. Rates of up to 0.4 g/l could be tolerated and metabolized (Brummet & O'Keefe, 1982). Because phenols are common products of plants, including wetland plants (Hagland & Williams, 1985), this capability gives the water hyacinth an advantage in allelopathic conflicts and may play a role i n its competitiveness. Conversely, some aquatic plants are sensitive to allelopathic chemicals. The aquatic plant Lemna minor has been even used in assessing allelopathic effects (Anderson, 1985; Einhellig et al., 1985).

IV. Medicinal Properties of Wetland Plants

Because wetland plants often contain highly bioactive chemicals, it is no surprise that these plants are often of use to humankind. Numerous reports on traditional uses of aquatic plants as sources of poisons against fish and other aquatic animals appear in Costa-Pierce et al. (1991), and several reports on the medicinal uses of wetland plants appear below. Yet most plant species in the world have not been surveyed in modem times for their chemical or biologically active constituents (Balandrin et al., 1985; Cox & Balick, 1994). Such information on plants that have been surveyed can be found in the literature of modern medicine and of ethnomedicine, the science that preserves medical knowledge of traditional cultures. There is substantial knowledge about the medicinal properties and value of plants (Table II; Taylor, 1940; Millspaugh, 1974; Lewis & Elvin-Lewis, 1977; Balandrin et al., 1985; Duke, 1986; Cox & Balick, 1994). Bioactive plant chemicals from wetlands have been widely used in both "primitive" and "modern" cultures. A large fraction of plants traditionally cultivated for medicinal purposes came from wetlands or had closely related wetland species (e.g., Stockberger, 1927).


The use of wetland plants in medicine reflects the importance of wetland plant chemicals to humankind. Over the millennia, traditional cultures have collected much practical knowledge about the medicinal properties of plants. Much of this information is now being lost, but the medicines of several peoples have been documented. The experience of these peoples may teach us to identify plants with bioactive ingredients that modern scientists have not yet discovered (Cox & Balick, 1994).

Native Americans used approximately 25% of plants in the United States as medicines, and about 10% of all plants in the world have medicinal value (Duke, 1986). Although not all of the plants in use are effective, it has been estimated that nearly 40% of the plants used actually contain chemicals with the desired medical influence. One of the best-known cases is the willow, Salix, used by Native Americans for the same purposes for which modem medicine uses its active compound, salicylic acid, or aspirin. The roots of many other wetland plants served to poison, disinfect, prevent infection, and prevent inflammation.

Weenen et al. (1990) examined the antimalarial activity of root extracts from several plants used in traditional Tanzanian medicine. Of the three most effective extracts, one came from the common wetland plant Cyperus rotundata. Another common wetland plant, Acorus calamus (sweet flag), was widely used for medicinal purposes in North America, as well as in India (Sivarajan, 1994).

Of the 55 genera typical and prevalent in Florida wetlands (R. Best, pers. comm.), at least the following 26 genera were medically used by Native Americans (compiled from data in Lewis & Elvin-Lewis, 1977; Duke, 1986): Acer, Cephalanthus, Cornus, Fraxinus, Hypericum, Ilex, Lachnanthus, Lemna, Liquidambar, Magnolia, Myrica, Nuphar, Nymphaea, Nyssa, Orontium, Persea, Poligala, Pontederia, Rhexia, Sabatia, Sagittaria, Salix, Sarracenia, Saururus, Typha, and Xyris. Only nine of these 26 genera do not appear in the lists of plants with scientifically proved medical activity in Tables I, I, III, IV, and V (Liquidambar, Nyssa, Orontium, Poligala, Pontederia, Rhexia, Sabatia, Saururus, and Xyris).


It is beyond our expertise to provide a thorough review of wetland plants in medicine. Therefore, we cite only a few cases of medically active or useful chemicals from the roots of wetland plants to illustrate our point. Laksman (1987) reviewed evidence for the medicinal properties of chemicals from wetland plants. Antitumor activity was found in Spartina alterniflora, S. patens, Juncus roemerianus, Sagittaria falcata, and Phragmites australis, and polysaccharides extracted from Typha were shown to coagulate blood. Jarvis et al. (1985) described an allelopathic and poisonous chemical originating from roots of Baccharis megapotamica that also had anticancerous properties. The chemical was a macrocyclic trichothecene, a mycotoxin without anticancerous properties, produced by the fungus Myrothecium spp. Apparently, the fungus lives on the plant roots and produces the nonanticancerous toxin, which is very phytotoxic, but not to Baccharis. The species B. megapotamica slightly metabolizes the chemical, making it a nticancerous too. This seems like a case of symbiotic association that confers on the plant not only a medicinal value but also, possibly, a chemical antimicrobial or antiviral defense. Other plant species that harbor this fungus possess the chemical in its original form, which is toxic but not anticancerous. Urtica dioica, reported above to contain quite a few phenolic and terpenoid compounds, has been used to treat prostatahyperplasia (Kraus & Spiteller, 1990). Several chemicals that had confirmed activity against standard antitcancer tests of the National Cancer Institute have been extracted from the common salt-marsh plants Juncus roemerianus (needle rush) (Miles et al., 1981).

V. Discussion

A picture of the "typical" wetland plant can be drawn from the extensive literature reviewed here. This wetland plant not only is well adapted to its harsh environment but also controls the chemical and biological environment of its rhizosphere. To do so it is involved in a complex array of chemical interactions, most of which occur at the rhizosphere. These include employing allelopathic chemicals in competition for soil space with other plants, employing pest-control chemicals for the control of microbial and animal pests, and chemical inhibition and resource competition with microbial competitors, such as nitrifiers. The "typical" plant can also chemically extract precipitated nutrients, such as iron and phosphate, from the soil, detoxify heavy metals, and detoxify metabolites of anaerobic metabolism from the neighboring bulk soil.

For these activities the wetland plant utilizes either by-products of its own metabolism or "made-to-order" chemicals. The wetland plant is also affected by metabolites and chemicals, such as enzymes, released to the soil by its dead and damaged tissues or produced in or near its rhizosphere by other organisms.

Concerted scientific effort is required to fill the many gaps in our knowledge of chemical and biochemical interactions in the rhizospheres of wetland plants and of how they influence wetland functions. Convincing evidence is sparse on chemical activities in such rhizospheres, probably because most of the available information on bioactive chemicals has been produced in disciplines such as agriculture, entomology, toxicology, medicine, chemistry, and phytopathology, not typically involved yet in wetland research. However, we have found many "leads" that require further investigation. Such leads encompass obscure publications, evidence of bioactive chemicals from "upland" relatives of wetland plants, and chemicals whose bioactivity in the laboratory has not been confirmed in situ. We are aware of examples in which species of the same genera differ chemically. However, the probability is higher than random that an unstudied wetland species has bioactive chemicals if other species in its genus, family, or order are already known to have them (Cox & Balick, 1994). For example, the salt marsh species Suaeda monoica (Chenopodiaceae) belongs to the order Centrospermae. As presented above, many plants in this order contain bioactive betalains. Such a chemical is therefore more likely to be found in the root of this species than in the root of species from other orders.

A tantalizing question remains: What is the role of each root bioactive chemical or poison in controlling rhizosphere pests, on one hand, and in modifying rhizosphere biogeochemical processes, on the other hand? Specific reports of a chemical bioactivity in a wetland plant can probably be generalized: For instance, it is possible that wetland plants with poisonous above-ground parts also have poisonous roots.

Plant hormones have been shown here to exist in wetland soils and rhizospheres in relatively high concentrations. Obviously, a hormone that appears out of the natural rhythm can detrimentally influence a plant. Because organic compounds degrade slowly in flooded soils, one would expect water-soluble growth regulators to persist there longer and thus to be more effective than they are in dry soils (cf. Gunnison & Barko, 1989). It is therefore intriguing to imagine what the production and release of a hormone into the flooded soil, by either a plant or a microorganism, do to the plant community, to the inhabitants of its rhizosphere, and to the functioning of a wetland.

Plant and microbial siderophores and phytochelatines occur in roots of several wetland plants and significantly influence iron mobilization and heavy-metal detoxification in wetland rhizospheres. The evidence provided here suggests that such chemicals can provide the plants that produce them with the quadruple functions of metal nutrition, metal detoxification, pest control, and allelopathy.

Allelopathy is difficult and controversial to define in a way that satisfies everyone. Even so, we have reviewed many documented cases of apparent allelopathy in wetland plants and allelopathic chemicals in root systems of wetland plants. The existence of so many reports on allelopathic chemicals and their effects in wetland plants confirms that competition for space in wetlands is intense. This certainly disagrees with the notion (Crawford, 1987; Crawford & Braendle, 1996) that wetland plants live under constant acute stresses ("comparable to life under a prolonged heart attack"; Crawford, pers. comm.) that result from anaerobiosis of the soil. Plants under such severe stress, each one for itself, would have been constantly trying to just survive the environmental attacks on their physiology. The survivors would have been few and far between. Under such difficult conditions, plants are not able and do not have to compete with each other, so they do not need allelopathy. Acute heart patients in a hospital ra rely compete with each other when they are fighting for survival, and they leave many empty beds between them. The contention that the existence of an effective phytotoxin in the root and rhizosphere of a plant from a densely vegetated, multispecies wetland can be inconsequential to the success of this plant is, in our opinion, questionable. At this time we can only speculate about whether plant-plant competition for soil space--which is often competition for sunlight, because nutrients and water are abundant in flooded soils--is fiercer in wetlands than in dry-soil environments.

The limited evidence presented here about the medicinal properties of wetland plants, from both ethnomedicine and modem medicine, should be extended. We are not qualified to evaluate the validity of each report on the medical potency of a wetland plant, so we have not tried to review such reports comprehensively. It is plausible, however, that, upon further study, interesting and ecologically significant chemical-biological interactions will be found in rhizospheres of medicinal wetland plants. It is only logical that medicinal chemicals perform for the plants that produce them tasks other than providing medicines. For instance, the chemicals that cause a paste made by a shaman from Typha roots to coagulate human blood most probably also coagulate the blood of root borers and kill them.

VI. Conclusion

The initial information collected and synthesized here clearly demonstrates the widespread nature of bioactive chemicals and chemical-biological interactions in wetland rhizospheres. Evaluation of the information in this review and educated predictions about the possible prevalence of plant bioactive chemicals in wetland rhizospheres can be greatly facilitated by the study of Grainge and Ahmed (1988), a comprehensive collection of information on pest-control chemicals and poisons from plants. From the 3,400 plants they cataloged as containing pest-control and poisonous chemicals, many--at least 170, or about 5%--were wetland or aquatic macrophytes. Many more cataloged plant species were not aquatic but belonged to genera that contain typical and widespread wetland species. The latter species had not been studied with respect to bioactive chemicals. At the moment, we can extrapolate using the existing data. A little over 1% of the world's plants are included in the catalog of Grainge and Ahmed (1988). However , strikingly, of the 55 plant species that are considered most typical of wetlands in the well-studied region of Florida (R. Best, pers. comm.), 36--65%--have documented pest-control chemicals (Grainge & Ahmed, 1988), activity that is poisonous to large animals (Muenscher, 1975; Grainge & Ahmed, 1988; Turner & Szczawinski, 1991), and/or medicinal action (Taylor, 1940; Duke, 1986). Furthermore, 47--85%--of the 55 plant genera in that Florida group include species that possess activity in at least one category of bioactivity. On a larger scale, of the 279 species of Florida wetland plants that appear in the popular manual Wetland Plant Species of Florida (Dressler et al., 1987), at least 26%--40% of the genera--were found to have bioactivity in one of the three categories. Assuming that wetland plants in Florida are no different from those in the rest of the world in this respect, we can confidently predict that, upon further examination, at least similar proportions of the world's common wetland and aquatic pl ants will be found to have bioactive chemicals. It is beyond the scope of this review to assess whether wetland plants in Florida--or elsewhere--have more frequently bioactive chemicals than do upland plants in Florida--or elsewhere--but the percentage comparison with the Grainge and Ahmed catalog speaks for itself. If found to be so, one could even interpret such evidence to imply that the families of terrestrial plants with the genetic disposition to produce defensive chemicals were more successful in colonizing the harsh but competitive wetland environments.

It is an outstanding additional finding, from one of the most intensely studied wetland regions in the world, that Native Americans in Florida used as medicines more than half of the most typical and common Florida wetland plants, 65% of them for a scientifically proved reason. This suggests that, with more detailed studies, such a situation is likely to be found in the rest of the world's wetlands.

We conclude that a large fraction, perhaps more than half, of the plants in the world's wetlands contain various bioactive chemicals, even though we do not yet know how much each of these chemicals affects wetland processes in quantitative terms, how the chemicals interact, or even how far from the roots they diffuse and have an influence. Such difficult questions call for novel ideas and techniques, such as the procedure of Tippkotter et al. (1986) for soil thin sections for biological studies and the high-resolution pore-water gel sampler of Krom et al. (1994). We can confidently assume, however, that such chemicals are involved to significant degrees in pest control, allelopathy, and other chemical interactions within the rhizospheres of the plants that produce them. These activities probably play more significant roles than is currently believed in determining the bioecological functioning of wetlands.

VII. Acknowledgments

Most of the literature on which this article is based was collected and synthesized during a sabbatical year that A. N. spent at the Department of Soil and Water Sciences, University of Florida. We thank Karen Brown and the Aquatic Plant Information Center, the Center for Aquatic Plants, and the staff of the Marston Science Library of the University of Florida for their aid in assembling the literature. A. N. thanks J. Doucha and the staff at the Academy of Sciences of the Czech Republic, Institute of Microbiology, Department of Autotrophic Microorganisms at Trebon, where the manuscript was completed. We are especially grateful to J. Kvet for reviewing the manuscript and for fruitful discussions and many useful suggestions, to N. Rea for critical reading of an early draft of the article, and to R. Tadmor for technical assistance. The present article owes much also to several anonymous reviewers.

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