Allelopathic Impact of Plants
Introduction
"Allelopathy" is the term used to refer to certain biochemical interactions between all types of plants, including micro-organisms. chemical exudates or leachates which are released from leaves, stems or roots (living or dead) can have an inhibitory or a stimulatory effect on other species or on the same species. The word does not refer to direct competition for water, minerals, food or light (Molisch, 1937). "A rapidly growing body of data suggests that allelopathy is often important in the survival and growth of trees in both plantations and natural stands. An awareness of this phenomenon, and its potential effects on regeneration and site productivity, is essential in the practice of intensive silviculture". (Fisher, 1980 ). "The evidence is obviously accumulating rapidly indicating that many important forest tree species exert allelopathic effects against either herbaceous species or woody species or both. Such effects can no longer be ignored in forestry. The word allelopathy was first used by Hans Molisch in 1937 when describing the beneficial and deleterious chemical interactions of plants and microorganisms (Willis 1985). Today, the more accepted definition is any direct or indirect effect (commonly negative) of one plant on another mediated through the production of chemical compounds that escape into the environment (Rice 1974). While the term is relatively new, the concept of allelopathy is quite old.
Allelopathic Impact
Allelopathic impact may be both negative and positive. But most of the cases the negative impacts are discussed. Here various allelopathic effects are given
Allelopathy as a mechanism
Does it matter if allelopathy or resource competition (or some combination of the two) drives particular exotic invasions? From a perspective of what invasions can teach us about theory and plant communities– certainly. From the perspective of how invasions might be controlled – probably. There are several theoretical implications to the scenario of invaders succeeding by employing allelochemicals (also see Callaway and Aschehoug, 2000). First, disruption of native communities by chemicals exuded by an exotic would suggest that natural plant communities might be more tightly knit entities than generally thought and that invasion disrupts inherent, co-evolved interactions among long-associated native species. Invasive success due to an ability to out-compete locals has no new bearing on the nature of plant communities. Second, unusually strong allelopathic effects of an invader against species in recipient communities suggest that plant–plant interactions may be somewhat species-specific. This may not be the case if invaders simply out-compete locals for resources. Finally, if allelopathy is more important in exotic invasion than in natural communities the possibility is raised that interactions among plant species may drive natural selection in communities, in turn implying that natural biological communities may evolve in some way as functionally organized units (see Goodnight, 1990; Wilson, 1997). From an applied perspective, if exotics succeed because of an unusual capacity for resource competition then control is a matter of keeping them from acquiring resources. Herbicide, biocontrols, grazing, or any other method of reducing the mass of invaders should help. If allelopathy is involved, the effect of reducing the mass of invasive species may be much less predictable. In fact, induction of herbivore defenses may actually increase allelopathic effects
General Observation
(a) Nature of the Phytotoxins
The study of allelopathy is by no means limited to observing the phenomenon in the laboratory and in the field. A large number of phytotoxins have been isolated, and for many of theim their mode of action is known or suspected.
(b) Most Toxic Part of a Plant
Del Moral and Gates (1971) analysed 40 plrnt species and concluded that chemicals leached from intact, living dicot leaves were, on the average, considerably miore inhibitory than those leached from either conifers or ferns. In nearly every individual case, litter extracts were substantially more inhibitory than leaf extracts of the same species. Matveev (1980) supports this finding.
(c) Environmental Degradation
Rice (1979) says that it is abundantly clear that if allelopathic compounds which are released into the environment were not decomposed, probably no plants could survive. Jameson (1970) says that "frequently inhibitors do not have any apparent ecological effect. If a small amount of material is deposited, or if the natural organic-matter breakdown processes proceed normally, little toxic material is accumulated. In some cases, however, material is deposited more rapidly than it is broken down, and species sensitive to these toxins are thereby influenced". Rice (1979) continues: "although many species produce and release substances with potential growth regulating properties, few seem to have phytotoxic effects on other plants. The substances often do not persist long enough to accumulate to toxic concentrations . Under well-aerated and well-drained conditions may phytotoxins resulting from both plant excretion and residue decomposition are rapidly metabolised by micro-organisms into non-toxic forms". This would certainly explain Whyte's findings that poor growth in some second rotation radiata pine forests occurred on the ridge tops and generally worse sites.Whyte also found that ploughing the affected areas removed the problem, and in any case the effect disappeared given time (Whyte, 1982, pers. comm.). If allelopathy is discovered to be a problem in two-tier farming, then this line of reasoning might act as a caution against restricting it to poor hill-country sites, rather than to the best soils. Where drainage is poor the evidence is clear that phytotoxins accumulate. Del Moral and Muller (1970) say that "anaerobic conditions are not favourable to the metabolism of those microorganisms responsible for the detoxification of phenolic compounds". Fisher (1978) confirms this by reporting that "on excessively drained sites, Pinus resinosa seemed unaffected by Juglans nigra, while on imperfectly drained sites walnuts sup pressed or even killed the pines". In laboratory studies, he showed that juglone and its inhibitory activity readily disappeared under a "dry moisture regime" but remained under a "wet moisture regime". Howard (1925) showed that aeration of thp soil stopped fruit trees dying of "grass poisoning". De Bell (1970) says that "in most cases where phytotoxins have been shown to be associated with decreased germination or growth, soils are characterised by heavy texture, poor aeration, excessive moisture and often cool temperatures. However, these are generalizations and certainly do not apply in all cases. Recent work by Muller has shown that different classes of phytotoxins persist optimally in different soil types."
(d) Synergistic Effects
Watanabe et al. (1961) discovered a 20-fold increase in scopolin in leaves of tobacco plants that grew in a boron-free solution for 38 days. Dear and Aronoff (1965) found a pronounced increase in caffeic and chlorogenic acids in leaves and growing points of boron-deficient sunflower plants. This illustrates a certain point: it may be naive to attribute poor growth in the Nelson district, for example, to either boron deficiency or to allelopathy. The latter could be caused by the former. It is nonetheless important to pinpoint the precise mechanism involved: applications of boron may be ineffective if the damage has already been done by allowing the accumulation of toxins in the soil. Del Moral (1972) discovered that increasing water-stress in sunflower plants increased total chlorogenic acid in the roots, stems and leaves. But the greatest increase in chlorogenic acid resulted from a combination of drought stress and nitrogen deficiency: this gave a 15-fold increase. This finding makes one suspect that competition and allelopathy cannot be considered in isolation
Inhibitory Effects:
Leaf of some species have inhibitory effect, they inhibits germination and growth behavior of some popular agricultural crops. For example Albizia lebbeck the different concentration of leaf extract inhibits the germination of crop seeds to a certain extent which in some cases found to causes complete inhibition of the species. Overall growth rate of seedlings was also reduced in almost all the treatments compared to control. The survivors exhibited varying degree of necrosis and chlorosis, thin and grayish in color. Many seedlings lost their ability to develop normally as a result of reduced radicle elongation and root necrosis. So, it was inferred that, the inhibition of seed germination and seedling growth is dependent on the concentration i.e. inhibition was more as the concentration increased. These findings coincided with the report of Daniel (1999), who reported that Allelopathy includes both promoting and inhibitory activities and is a concentration-dependent phenomenon. Mortality of the seedlings and reduced vigor under laboratory conditions indicated the accumulation of toxic substances (allelopathic potential) of the donor plant is harmful to the growth of seedlings of receptor plants. These findings correlated with the report of Chou (1992), Waller (1987), Rice (1984), Chou and Kuo (1984) and Chou and Waller (1980), who found that many species within the Leguminosae family contain secondary plant products that have allelopathic potential. Response of the bioassay species to the aqueous extracts varied among the five species. Considering the overall treatment among the five bioassay species the C. sativus was the least sensitive to the aqueous extract followed by P. mungo and V. unguiculata while R. sativus and B. juncea was the most sensitive. Marked reduction in root length was noticed in most of the seedlings compared to shoot length and germination. This result also coincided with the result of Swami Rao and Reddy (1984) who found the inhibitory effect of leaf extracts of Eucalyptus (hybrid) on the germination of certain food crops. Zackrisson and Nilsson (1992) supported higher sensitivity of root growth than seed germination. So, it may be concluded that the water soluble leachates from the fresh leaves of A. lebbeck has the allelopathic potential that reduce the germination as well as suppress the growth and development of agricultural crops. Allelopathics are often due to synergistic activity of allelochemicals rather than to single compounds (Williamson 1990). Under field conditions, additive or synergistic effects become significant even at low concentrations (Einhelliing and Rasmussen 1978). However, while the potential of an allelopathic influence exist, it exists as a part of ecological but not so prominent as to be singled out as the most important factor affecting stand characteristics as in the case of some other system (Rice 1984). Though laboratory bioassays in allelopathic research are of great importance, long-term field studies must be recommended to carry out before incorporating A. lebbeck in any agroforestry system.
ESTABLISHMENT PROBLEMS DUE TO "COMPETITION
Auto-inhibition as noted above appears to be less common, not surprisingly, than inhibition between species. Researched examples of the latter are too numerous to relate, but a few examples will suffice. Brown (1967) found that leaf extracts of nine species inhibited jackpine out of fifty-six species tested. Del Moral and Cates (1971) found allelopathic agents in nine of forty species investigated. Matveev (1977) found allelopathy in most of 47 species examined. Timofeev (1979) found that most of the above-ground plant parts of 12 species of ground flora inhibited germination and seedling development of Dahurian larch. Horsley (1977a,b) examined regeneration failure in black cherry and ruled out the effects of browsing, macroclimate and competition for light and nutrients. He deduced that allelopathic inhibition by fern, grass, goldenrod and aster was the main cause.
(a) Grass "Competition"
Radiata pine planted directly into' pasture does not succeed well (Tustin et al., 1979). This is normally attributed to competition, for moisture. But Pickering (1903) concluded that the pernicious effects of grass on apple trees were due to in a direct poisoning effect on apple roots, Spurr and Barnes (1973) report that grass extracts inhibit hybrid poplar growth. Naturally, we must specify which species of grasses we are discussing. It cannot be assumed that all grass species share the same allelopathic properties. Not all the research favours allelopathy. Webb and von Althen (1979) report that couch-grass affected sugar maple seedlings by competition and not by allelopathy. The word "competition" is used very loosely in forestry circles. For example, the NZFS handbook (1982) on forest farming research at Tikitere declares (on p. 3) that "the trees and pasture compete for moisture, nutrients and light.
(b) Bracken "Competition
Torkildsen (1950) prepared an extract of bracken roots with cold, distilled water and found that it killed or dwarfed Norway spruce seedlings. Del Moral and Gates (1971) showed that bracken litter chemically inhibited Douglas fir. On the other hand, Stewart (1975) found that extracts of senescent bracken reduced germination in two species of Rubus but not in Douglas fir! Also Brown (1967) found that the best germination of jack pine occurred with bracken extract, from 56 plants tested. Giessman and Muller (1972) showed that the phytotoxin was leached from dead fronds, but not from living ones. They suggest that allelopathy is often the limiting factor on the growth of associated plants, rather than competition as is commonly supposed. Bohm and Tryon (1966) identified some toxins in bracken and in many other common ferns.
(c) Heather "Competition"
Calluna vulgaris is a common exotic weed of the Central Volcanic Plateau (Healy 1973), and colonises a site very rapidly after a fire. Is this to the detriment of radiata seedlings planted in a heather matrix? For Calluna vulgaris is known to inhibit mycorrhizae of various tree species (Harley, 1952, Handley, 1963; Robinson, 1972; Mantilla et al, 1975).
(e) Effects of Lichen
New Zealand has many species of lichens that grow on bare ground, often beneath a manuka canopy. It is a rare forester that takes an interest in such small, seemingly insignificant plants. And yet Brown and Mikola (1974) and Fisher (1979) found that reindeer lichen has a very toxic effect on key mycorrhizae of jack pine. New Zealand shares three species of lichen with those researched overseas: Cladonia alpestris, Cetraria islandica and Cladonia pleurota. These are known to cause inhibition, but the former two are not likely to be found in places where exotic planting would be undertaken (Martin and Child, 1972).
(f) Sphagnum moss
We do not plant radiata in places where sphagnum moss grows: the soil is too badly drained. We do, however, collect this plant and export it. This is a rapidly developing industry on the West Coast of the South Island, and the NZFS is involved as it controls much of the suitable land. Brown (1967) observed that Sphagnum capillaceum contained phytotoxins. The significance of this becomes obvious when we consider that the main use of sphagnum is a plant growing or packing medium. The moss is of proven worth for general purposes, but perhaps certain species of commercial plant may be especially sensitive to any phytotoxins present.
Impacts on Ecosystems
Allelopathy influences vegetational associations and patterns, succession, invasion of exotic plant species, nitrogen fixation, seed preservation, the extent of disease and other dynamics of natural plant communities. Although terrestrial ecosystems have been the focus of most of the investigations, allelopathy occurs in aquatic ecosystems as well. Occasionally the role of allelochemicals dominates, but more often it is a subtle, difficult to measure component of community relationships. The case studies chosen to illustrate the capacity of plant chemicals to influence community relationships not only show the direct action of allelochemicals on higher plants, they also illustrate effects on that subsequently impact the vegetational community. Vegetational patterns the most visual evidences of allelopathy in natural communities are instances of bare-looking areas, a "halo" zone, around a plant or stand of one type of vegetation. This effect has been intensely scrutinized in the chaparral of southern California and in the sand pine scrub community of Florida's central ridge and costal dunes. The classic studies on the zonation of vegetation in the chaparral showed Saliva leucophylla, Artemisia californica, and other aromatic shrubs release a variety of volatile terpenes that solubilize into the leaf cuticle of associated species or adsorb on soil particles from which they may later transfer into root tissue of seedling that will try to establish in proximity to the shrub (53,112). Water-soluble phenolic acids are leached from leaves of these and other shrubs, adding to the complex of inhibitory allochemicals that will be encountered by the associated herb and grassland vegetation. Annual grasses are sensitive to these allelochemicals and the net result is a border zone of sparse vegetation near that may wax and wane to some degree with seasonal precipitation. As pointed out by Halligan (113), the situation is complicated by moisture conditions, mammals, and other factors interacting with the chemical environment to create the vegetational pattern. In Florida, sharp ecotones often marked by persistent bare zones exist between the sandhill and pine scrub communities, and there is little ground cover under the scrubs. Both allelopathy and fire cycles appear to contribute to vegetational patterns associated with the scrubs (114-117). Grasses are excluded from the immediate vicinity of Polygonella myriophylla (118). Ceratiola ericoides and several of the other early scrub colonizers also inhibit grasses. A variety of allelochemicals have been implicated in this activity. For C. eriocoides, these include mono-, di-, and triterpenes and several flavonoids (115-117). Ceratiolin, a novel flavonoid, may be among the more important compounds since it degrades by photochemical action to produce the very toxic hydrocinnamic acid. It appears that allelopathy interacts with other environmental stresses to generate some Agricultural Ecosystems Productivity of agricultural fields, including pasture land and agroforestry environments, is routinely influenced by allelopathy. The source of may be the crop, weeds, or microorganisms of the decomposition processes (62,128). Alternately, any of these groups could be the affected species and allele-chemical transformations in the soil always complicate our insights. Even though a variety of scenarios are possible, it is the net effect on crop yield that has been a primary concern. As shown in this book and other literature (6), agricultural allelopathy issues have drawn the attention of scientists from many regions of the world. A few specific examples will be used to illustrate the range of allelopathic impact on the agricultural economy. Interference Since weeds are a major cause of yield losses, the aggressive growth habits of some of the most tenacious species have come in for scrutiny. Putnam and Weston (129) listed 90 species that show allelopathic potential and have been reported since then. The data implicate some of the world's worst weeds in allelopathy, including ragweed parthenium (Parthenium hysterophorus) (130), quackgrass [Elytrigia repens (L.) Nevski (Agropyron repens)](129,131), Johnsongrass (Sorghum halepense (42,119), Canada thistle Cirsium arvense)(132) and giant foxtail (Setaria faberi)(133). The most complete investigations on weeds have tied field-based evidence with a search for allelochemicals. Parthenium hysterophorus, a tropical weed endemic to America, has done great damage since arriving as an exotic to the India landscape and other places. Numerous reports of the last two decades document the phytotoxicity of its living and decomposing tissue, leachates, and root exudates (134-137). Effects on the receiving crop plants and other weeds include reductions in chlorophyll, water uptake, nutrient uptake, and legume nodulation. Several sesquiterpene lactones, phenolic acids, and organic acids have been identified as the responsible agents. Quackgrass is a second example where multiple investigations spread over many years have elucidated toxicity problems. Decomposing residues and foliage and rhizomes of living plants all reduce crop growth. Putnam and Weston (129) found quackgrass residues left on the surface in no-till systems reduced the biomass of eight crop species tested by at least 50%, with alfalfa (Medicago sativa) and carrot (Daucus carota) reduced more than 90%. Quackgrass inhibited legume nodulation, crops associated with living quackgrass exhibited symptoms of mineral deficiency, and added fertilizer did not solve the problem. These examples show there is a need for awareness of allelochemical toxicity in residue management practices The phenomenon of allelopathy encompasses all types of chemical interactions among plants and microorganisms. Several hundred different organic compounds (allelochemicals) released from plants and microbes are known to affect the growth or aspects of function of the receiving species. Many new allelochemicals have been identified in recent years and it has become clear that the actions of allelochemicals are important features characterizing the interrelationships among organisms. These compounds influence patterns in vegetational communities, plant succession, and seed preservation, germination of fungal spores, the nitrogen cycle, mutualistic associations, crop productivity, and plant defense. Allelopathy is tightly coupled with competition for resources and stress from disease, temperature extremes, moisture deficit, and herbicides. Such stresses often increase allele-chemical production and accentuate their action. Allelopathic inhibition typically results from a combination of allele-chemicals which interfere with several physiological processes in the receiving plant or microorganism. Other than the autecological study of specific species, there are persistent challenges in allelopathy to determine the mechanism of action of compounds, isolate new compounds, evaluate environmental interactions, and understand activity in the soil. New frontiers will focus on ways to capitalize on allelopathy to enhance crop production and develop a more sustainable agriculture, including weed and pest control through crop rotations, residue management, and a variety of approaches in biocontrol. Other goals are to adapt allelochemicals as herbicides, pesticides, and growth stimulants, modify crop genomes to manipulate allelochemical production, and better elucidate chemical communications that generate associations between microorganisms and higher plants.
Allelopathy in Botanical Invasions
While new techniques in allelopathic research have given greater credibility to the field, the role of allelopathy as a ‘novel defense’ in plant invasions has garnered the most attention. Most of the work on the role of allelopathy in invasions has been done on the invasive Centaurea species. Native to Eastern Europe and Asia Minor, C. maculosa and C. diffusa have spread throughout rangeland in the United States and Canada (Roche and Roche 1991). These aggressive plants can form monospecific stands, which negatively affect livestock and wildlife forage (Watson and Renney 1974). Centaurea species were suspected of being allelopathic 40 years ago (Fletcher and Renney 1963), but it was not until the past five years that this idea drew significant attention. In a groundbreaking paper, Callaway and Aschehoug (2000) reported that C. diffusa had stronger negative effects on grass species from its introduced range (North America) than its native range (Europe). North American grasses were reduced 85% when grown with C. diffusa, compared to only a reduction of 50% for closely related Eurasian species. This was the first paper to indicate that allelopathy may aid in invasions, and it led the authors to suggest that “some exotic invasive plants may use competitive mechanisms that are not present in the natural communities that they invade to disrupt inherent, coevolved interactions among longassociated native species.” In a follow-up study, a native bunchgrass, Festuca idahoensis, was grown with C. maculosa with and without activated carbon, which ameliorates the effects of the allelochemical (Ridenour and Callaway 2001). It was found that Festuca plants were 50% smaller when grown with Centaurea than with conspecifics, yet when Festuca was grown with Centaurea and activated carbon, Festuca was 85% larger than when grown with Centaurea alone. These results led the authors to conclude that allelopathy accounts for a substantial portion of the total interference on Festuca. Shortly after it was shown that Centaurea species negatively affect native species through the purported action of allelopathy, the putative chemical was found (Bais et al. 2002). Bais et al. identified (-)-catechin as a phytotoxic compound produced in the roots of C. maculosa. To look at the toxicity of (-)-catechin, eight plants were grown in the presence of root exudates of C. maculosa. All of the plants showed mortality after two weeks of the addition of the exudate. This led the authors to conclude that (-)-catechin has broad-spectrum herbicidal activity and likely plays a role in spotted knapweed’s allelochemistry and successful invasion. In a complementary study, it was shown that the (-)-catechin triggers a wave of reactive
Allelopathy and exotic plant invasion
To our knowledge, no other studies have compared the relative allelopathic effects of an invader on species from ‘origin’ versus ‘recipient’ communities; however chemical allelopathy has long been suspected as a mechanism by which invasive plant species eliminate natives. The observation that non-native plants often form dense, virtually mono-specific stands, whereas natural monospecific stands of any species are rare, has been one of the rationales for proposing mechanisms other than resource. The literature linking allelopathy to exotic invasion includes some of the best known plant invaders in the world, including Eltrygia repens (ex. Agropyron, Korhammer and Haslinger, 1994; Osvald, 1948; Welbank, ; Weston et al., 1987), Bromus tectorum (Rice, 1964), several Centaurea species (Fletcher and Renney, 1963; Muir and Majak, 1983; Ridenour and Callaway, 2001; Stevens, 1986), Cirsium arvense (Stachon and Zimdahl, 1980), Cyperus rotundus (Agarwal et al., 2002; Komai and Tang, 1989; Komai et al., 1991; Quayyum et al., 2000; Tang et al., 1995), Euphorbia esula (Letourneau and Heggeness, 1957; Selleck, 1972; Steenhagen and Zimdhal, 1979), Parthenium hysterophorus (Kanchan and Jayachandra, 1979, 1980; Pandey, 1994), Setaria faberii (Bell and Koeppe, 1972), and Sorghum halepense (Abdul-Wahab and Rice, 1967; Elmore, 1985). Although the number of studies suggesting allelopathic effects of exotic plants is impressive, research on allelopathy and exotic invasion is less convincing than the argument for allelopathy in general. This may be due to gaps in research approaches rather than the biological effects of allelopathy. Indeed, there is reason to hypothesize that allelopathy may be much more important as a mechanism in recipient than in origin communities. A strong argument against allelopathy as an important mechanism in natural plant communities is that plants appear to evolve tolerance to chemicals rapidly (Williamson, 1990). For allelopathy to be effective, the argument goes, plants must evolve new weapons more rapidly than their neighbors evolve defenses. This is thought to rarely happen, as it appears that even Monsanto cannot keep the defense in front. In invasions, however, members of recipient communities may be much more likely to be naïve to the chemicals possessed by newly arrived species. The argument for allelopathy in exotic invasion has been enervated primarily by two issues. First, questionable methodological approaches, particularly the use of petri dish bioassays, have been overemphasized as assessments for allelopathy, and warrant the skepticism many express for allelopathy in general (Harper, 1977; Keeley, 1988; Stowe, 1979). Second, target species used to evaluate the potential allelopathic effects of invaders have been predominantly crop species and other exotic weeds rather than the native species that are actually excluded. However, during the last 15 years, apparently in response to surging concern about exotic invasion in natural systems, the allelopathic effects of a number of exotic invasive plants has been tested on natives. Zoysia-dominated seminatural grasslands of Japan have been heavily invaded by a pasture plant introduced from Europe, Anthoxanthum odoratum,
Conclusion
This review has tried to demonstrate that a knowledge of allelopathy may be essential to all who seek to study the growth of plants. Perhaps only a fraction of foresters have even heard the word "allelopathy". This is not necessarily because the subject is unimportant, but is because the bulk of the research has occurred only in the last decade, and the principles have not yet filtered down to the applied sciences. In particular, changes in our understanding of the "replant problem", competition between plants, and in the ecology of natural forests are postulated. It is suggested that allelopathy may be of vital significance in two-tier farming, especially if new species of tree or grass are considered.
it was shown that competition occurring between trees and grass did not explain the reduction in grass growth. In fact the reduction could be explained wholly or largely in terms of allelopathy. Competition may well be the correct explanation, but trials should be established to settle the point. potential (Putnam and Duke, 1974; Fay and Duke, 1977). Rice (1979) says "we are on the threshold of breeding crop plants that will inhibit the chief weeds in a given area through allelopathic action, and thus decrease the need for synthetic weed killers. Alternatively, we may be able to breed strains devoid of any allelopathic action, and thus achieve the maximum potential for two-tier farming. The situation, however, is by no means simple. There is evidence, as we shall see, that competition and allelopathy interact in subtle and complicated ways.
