Abstract

Media Summary

Key Words

Introduction

The idea that plants affect neighboring plants by releasing chemicals in the environment has been known since c. 370 BC (Willis 1985, 1997). Greeks and Romans used this knowledge in practising agriculture as early as 64 AD. The antagonistic effects of certain tree species such as walnut tree (Juglan spp.) on understory plants and nearby crops were also known to humans centuries ago (Rizvi and Rizvi 1992; Willis 2000, 2004). Poor yield of repeated cultivation of certain crops and fruits due to so called ‘soil sickness’ has been known and investigated since the beginning of horticulture. Although this form of plant-plant interference has been known for quite some time, it is only recently (1937) that the Austrian plant physiologist, Hans Molisch, gave it a formal name, allelopathy (Molisch 1937; 2001). During its long history, allelopathy was perceived as a donor-receiver phenomenon where one plant releases chemicals that affect the growth of the neighbouring plants mostly in agricultural and horticultural settings. The idea of allelopathy as an ecological phenomenon structuring plant communities is rather recent. Whittaker and Feeny (1970) recognized the role of allelochemicals in plant community organization. In the 1960s and 1970s through a series of field and complimentary laboratory studies by several authors provided data showing that certain plants can influence their neighbouring community of plants directly by releasing allelochemicals and indirectly by affecting the activity of rhizosphere microbes (Muller 1966, 1969; Muller et al. 1964; Whittaker and Feeny 1970; Rice 1964, 1965). However, their assertion was met with skepticism following a demonstration that bare ground created around allopathic shrubs can be invaded by plants after removal of herbivores (Bartholomew 1970) generating the famous criticism from J.L. Harper who described allelopathy as a complex “undeniably natural phenomenon” but “nearly impossible to prove” (Harper 1975). The following four decades experienced a great deal of scepticism by the general plant ecologists in accepting almost any results suggesting the presence of allelopathy as a viable explanation of plant-plant interaction principally on the ground that effects of other factors have not been removed in demonstrating allelopathy. Unreasonable ‘burden of proof’ was imposed on the researchers proposing allelopathy as a plant-plant interference mechanism (Williamson 1990; Willis 1985). By the end of the last century several authors suggested that allelopathy can not only affect neighbouring plants and influence plant community structuring, but it can also induce a broader ecosystem level change when it coincides with disturbance (Zackrisson et al. 1997; Wardle et al. 1997; Mallik 1995). In a well-written review, Wardle et al. (1998) argued that the concept of allelopathy can be applied more effectively at the ecosystem-level rather than at population level of resolution. Recently, several authors published convincing evidence of allelopathy as ecological mechanisms of exotic plant invasion through a series of well designed experiments and sophisticated chemical analyses (Bias et al 2002, 2003; Callaway and Aschehoug 2000; Vivanco et al. 2004). These authors also argued ecosystem-level vegetation change following exotic invasion.

In my address today I would like do three things: first, briefly review the evolution of the concept of allelopathy from individual to population to ecosystem-level perspective, highlight the interplay of ecosystem disturbance and plants reproductive strategy in bringing about ecosystem-level changes; secondly, impress upon the need for fundamental research to discover the mechanisms of allelopathic interactions not only to solidify the scientific basis of the discipline but also use this knowledge to develop new methods for sustainable land management strategy. I shall end my contribution by highlighting some current challenges, opportunities and future directions in allelopathy research.

Evolution of the concept of allelopathy

Early observations and experimentations in allelopathy were based on the concept that allelopathic donor plants release alleochemicals (from root exudates, volatiles from above ground components or decaying plant litter) in the environment that interfere with the growth of nearby plants. From this, the donor plants would gain competitive advantage, out-compete their neighbours and bring about individual and population level changes. Molisch (1937) demonstrated, with simple laboratory experiments, that toxic volatile (ethylene) from plant (apple) can affect the growth (wilting, bud and root inhibition of stem cutting) of other plants. From this he cautiously speculated that chemicals of plant origin (allelochemicals) have potential for bringing about population level change by affecting the growth of neighbouring plants. He named this phenomenon allelopathy and became the father of allelopathy. Unfortunately, we inherited the excessive use of the term ‘potential’ and a habit of using simple experiments to draw far reaching conclusions without giving much thought to the complexity of other ecological interactions in the natural world. The result has been an issue of credibility where most of the early work on allelopathy has failed to withhold the rigour of scientific scrutiny (Willis 1985; Romeo 2000; Mallik 2000).

Disturbance and ecosystem-level change

Type, frequency and intensity of disturbance by interacting with plants’ regeneration strategies and allelopathic properties can dictate the direction of succession following disturbance. For example, forest canopy removal by clearcutting and non-sever fire can stimulate certain ericaceous plants with allelopathic property to dominate the post disturbance landscape and resist tree invasion, transforming forests into ericaceous heath (Mallik 2003; Zackrission and Nilsson 1992). Zackrisson et al. (1996) published field evidence showing that natural fires perform key ecological functions in maintaining conifer forests of northern Sweden by removing competition and allelopathy from the ericaceous plant, Empetrum harmaphroditum, by adsorbing allelochemicals (Batatasin III) in charcoal, removing phenol rich humus by thermal combustion and creating a favourable seedbed for conifers. Fire suppression and clearcutting on the other hand promote understory ericaceous growth causing an ecosystem level vegetation change where Empetrum allelopathy plays a significant role in inhibiting germination and seedling growth of tree species (Nilsson 1992).

In the case of the nutrient poor black spruce-Kalmia ecosystems in eastern Canada the prominent role of competition in structuring plant community following disturbance can be preempted by allelopathy and seedbed limitation (Bloom 2001; Mallik and Roberts 1994). Canopy removal by clearcutting and the absence of high intensity natural fires stimulate vegetative growth of Kalmia, transforming forest into ericaceous heath, which resists tree colonization. High Kalmia cover, in the absence of a canopy tree, produces large amounts of litter rich in polyphenols, which can induce long-term physical and chemical changes in the soil creating an alternate persistent vegetation state (Bloom and Mallik 2003). The ‘afterlife effects’ (Bergelson 1990; Wardle et al. 1997) of the ericaceous litter makes the soil more acidic, their phenolic allelochemicals bind N in protein-phenol complexes and the habitat becomes further deficient in available N (Bending and Read 1996a,b; Mallik, 2001). In the presence of a large array of phenolic acids, metallic cations such as Fe, Al, Ca, Zn, Mn etc. precipitate to the lower soil horizon and form hard iron pans altering the soil-plant-water relation (Inderjit and Mallik 1996). With rapid build up of acidic humus and a high rate of paludification, occupancy of the ericaceous community brings about long-term change in the habitat that is less and less suitable for conifer regeneration (Gimingham 1960; Damman 1971; Meades 1983; Bradshaw and Zackrisson, 1990; Prescott et al. 1996). Following Jones et al (1994) and Lawton and Jones (1995), one can argue that this persistent vegetation state is a result of ecological engineering effects brought about by the combined effect of polyphenol rich Kalmia humus with allelopathic property, as well as competition from its aggressive vegetative regeneration strategy (Mallik 1993, 1994; Zhu and Mallik 1994).

Wardle et al. (1998) reported another example of site preemption by an invading, weed nodding thistle (Carduus nutans) in New Zealand pastures dominated by perennial ryegrass (Lolium perenne) and white clover (Trifolium repens). In this case, through aggressive seed regeneration in small pasture gaps (5 cm diameter) followed by rapid vegetative growth of its rosette leaves the invading species cause expansion of the invaded patch (up to 1 m diameter). The thick rosette leaves of C. nutans undergo very rapid decomposition producing a strong allelopathic effect on T. repens, completely displacing it from the patch. Nodulation and nitrogen fixation of white clover is seriously inhibited by the leaf decomposition product of C nutans leaving the patch relatively nutrient poor compared to the adjacent area. The authors were able to discount other ecological effects such as competition for light, nutrients and herbivory from this interaction to demonstrate the over riding effect of allelopathy in displacing T. repens. Wardle et al. (1998) suggested that by inhibition of nitrogen fixation in the presence of leaf decomposing allelochemicals, C. nutans can induce long-term nitrogen decline in such a pasture ecosystem.

Allelopathy induced ecosystem-level effects of exotic invasive plants have been reported by several authors (Hierro and Callaway 2003; Vivanco et al 2004). Through a series of greenhouse, field and laboratory experiments these authors demonstrated convincingly that root exudates of Centauria diffusa and C. maculosa, natives of Eurasia and exotics noxious to Palouse and intermountain prairies of North America, can not only directly affect the root growth of the North American native plants but also their rhizosphere microbes (Callaway and Aschehoug 2000; Bais et al. 2002, 2003). Not only do these exotic plants bring with them novel allelochemicals that adversely affect germination and growth of native plants, but the chemicals stimulate the synthesis of allelochemicals by their rhizspheric biota (Callaway 2002; Ridenour and Callaway 2001). Extensive use of these exotic chemical weapons, in conjunction with unique seed regenerating strategy and perennial habit of the invasive plants, brings about ecosystem-level changes creating monospecific stands and change the chemistry and biophysical properties of soil (Callaway and Ridenour 2004).

Establishing the scientific basis of allelopathy

This is the theme of the 2005 congress. It is appropriate and timely. By reading the history of allelopathy one can easily conclude that in addition to some useful discoveries, the past was replete with observations, hypotheses, experiments and conclusions that were often simplistic and scientifically unfounded (Willis 1985, 2004). As a result, the main stream ecologists practically ignored research on allelopathy, essentially claiming that the influence of other major factors such as resource competition, soil chemical and biological properties have not been considered and successfully eliminated to demonstrate the effect of allelopathy. The critiques had some valid reasons to be skeptical, but the demand for unequivocal proof often becomes too much of a burden to bear (Willis 1985; Williamson 1990).Unfortunately, the trend of making broad and generalized conclusions unsupported by data continues, despite repeated cautions and explanations of the complexity of the phenomenon that call for careful and logical experiments and responsible data interpretations (Romeo 2000; Inderjit and Callaway 2003). Remarkable progress has been made in the last four decades. Demonstration of allelopathy mechanisms that were once considered impossible (Harper 1975) have been achieved by creative experimentation and use of advanced biomolecular analytical techniques (Bias et al 2003; Vivanco et al. 2004). In order to establish the discipline (allelopathy) on a solid scientific footing we must strive to demonstrate the mechanism of allelopathy in explaining plant to plant interactions and community structuring. Because of its interacting nature, any discovery in allelopathy will require interdisciplinary collaboration involving ecophysiologists, biochemists, molecular biologists, microbiologists, soil scientists and ecosystem ecologists. The nature of the research question will determine the type of collaboration required.

Current status and future direction

Experimental evidence of allelopathy: a nagging preoccupation

I eluded this issue in the earlier section. In general the most important challenge for allelopathy researchers has been to demonstrate the effects of allelopathy separating it from other associated processes under field or experimental conditions. This ‘burden of proof’ placed upon the experimentalists makes them think critically before arriving at conclusions and in general this principle served modern science well. However, because of the interacting nature of allelopathy which readily crosses the boundary of many disciplines,it is often difficult to demonstrate allelopathy. Some suggested that it is so intimately associated with other biotic and abiotic process that it is impossible to separate allelopathic effects from other related processes under field conditions (Inderjit and Del Moral 1997). Indications of the presence of allelopathy are not enough. To be convinced, one has to prove it ‘beyond reasonable doubt’ by eliminating all other possibilities (Williamson 1990). Because of the complexity involved it is ‘nearly impossible’ to demonstrate allelopathy experimentally (Harper 1975). But progress has been made by using innovative experimental designs and sophisticated biochemical and molecular techniques. A recent paper by Bias et al. (2003) has done what thought to be impossible in Harper’s days in the 1970s. The article attracted the attention of critics and sceptics alike generating a headline in Science ‘making allelopathy respectable’ (Fitter 2003). No doubt it was an excellent piece of scientific work, clever and convincing with a detailled investigation where intricate ecophysiological links have been traced and uncovered experimentally. The International Allelopathy Society (IAS) has rightfully awarded this year’s Grodzinski award to the authors for this publication. It is practically unheard of for allelopathy researchers to get editorial praise in Science. However, while giving a full recognition for the work in question the headline also reminds us of the skepticism as if prior to this paper allelopathy research was not respectable. Novel approaches in demonstrating allelopathy or separating allelopathy from competition have been published earlier and one can say that they were pretty respectable (Nilsson 1994; Weidenhamer et al 1989; Callaway and Aschehoug 2000; Mattner and Parbery 2001; Ridenour and Callaway 2001). To be acceptable not all experiments have to demonstrate ‘proof’ by isolating specific allelochemical (s) or discovering allelopathy mechanisms. Arguments can be made by experimentally eliminating associated factors (see for example Mattner and Parbery 2001). Besides, there is also a place for measured speculation based on the data trends and logical deductions.

Methodological challenges

This has been a serious issue for most allelopathy experiments. Doing allelopathy experiments is not a trivial matter. Questions must be clear and logical. To be relevant, experimental design must reflect the ecosystem condition as best as possible (Inderjit and Callaway 2003). Elegance in experiment can come from clever and simple designs (eg Nilsson 1994; Callaway and Aschehoug 2000) as well as complicated design and thorough analyses, which often requires collaboration from several related disciplines (Bais et al. 2003; Vivanco et al. 2004). In either case, clearly identifying good research question(s) is crucial. Since alleochemicals are involved in the process, good knowledge in chemistry or collaboration with natural product chemists is often necessary. Simple bioassay with unrelated plants and artificial media can be of limited use in answering any mechanistic or applied questions. This does not mean that all allelopathy studies require a sophisticated chemistry laboratory. Manipulation experiments can be performed in the field, greenhouse or in lab that can answer both fundamental and applied land management questions (see Mattner and Parbery 2001). But the habit of making generalized process based comments based on quick and unrealistic bioassay must stop. The history of agriculture is replete with examples of ancient traditional biological and cultural methods of crop protection. Hints can be obtained from these traditional cultural practices, some of which can be explained by allelopathy (Anaya 1999). Refinement of many traditional techniques of crop rotation, multiple cropping, mulching, cover cropping, green manuring and microbial inoculation can enhance crop productivity by reducing or in some cases eliminating the use of agrochemicals resulting in improvement of environmental quality. Over the last four decades many allelopathy bioassays have been conducted. The time has come to use these results to demonstrate the application of this knowledge by conducting statistically designed large-scale field trials.

Open-ended definition, seeking boundary of the discipline

There have been concerns expressed as to the limits and bounds of allelopathy. The widely used definition of Rice (1984) ‘any direct and indirect effect by one plant (including microorganisms) on another through production of chemical compounds that escape into the environment’ is viewed as all-encompassing and lacks any boundary. The definition of the IAS, ‘any process involving secondary metabolites produced by plants, algae, bacteria and fungi that influence the growth and development of biological and agricultural systems’ (IAS 1996). This definition also suffers from being too broad and had limited use since its publication. Many secondary metabolites of plants in the rhizosphere include sugar, simple polysascharides, amino acids and other organic acids are not all allelopathic (Bertin et al. 2003). In describing algal allelopathy Inderjit and Dakshini (1994) defined allelopathy as ‘a phenomenon where allomones contributed by the algae can affect: 1) other algae in its vicinity, 2) its own growth, 3) microbes associated with it, 4) higher plants in its vicinity, and 5) accumulation and availability of nutrient iones which influences the distribution, growth and establishment of other algae, microorganisms, and plants’. Unlike others, this is a specific but wordy definition that highlights autotoxicity. Several others have described allelopathy as: i) ‘allelopathy is an interference mechanism by which plants release chemicals that affect other plants’ (Wardle et al. 1998), ii) ‘allelopathy is the negative effect of chemicals released by one plant species on the growth and reproduction of another’ (Inderjit and Callaway 2003), iii) ‘allelopathy is the release of extracellular compounds that inhibit the growth of other microorganisms’ (Suikkanen 2004), vi) ‘suppression of neighboring plant growth by the release of toxic compounds’ (Fitter 2003), vi) ‘release of chemical compounds by an invader that have harmful effects on members of the recipient plant community’ (Hiero and Callaway 2003) and vii) ‘the chemical suppression of competing plant species’ (Vivanco et al. 2004). One thing seems to be common in all these definitions except Rice (1984) is that they all refer allelopathy to negative effects as did the authors writing in the 1950s and 1960s (Muller et al 1964; Muller 1966, 1969; Rice 1974). Examples of stimulatory effect of allelopathy are rare and usually associated with low concentration effects of the compounds (Rice 1984).

The word allelopathy does not appear in popular reference such as the new Oxford Encyclopedic Dictionary, despite many thousands of peer-reviewed publications in the English language. Where it does appear, such as in the Oxford English Dictionary Additions Series, the Webster’s Dictionary and the Encyclopedia Britannica, allelopathy refers to chemicals released by plants having strictly negative effects on neighbouring plants (Willis 2004). Often authors define allelopathy based on their worldview from a very narrow to a very broad perspective. Inderjit (2001) suggested that allelopathy should refer only to the inhibitory effects of allelochemicals. One of the main reasons for having this difficulty with the definition is because the allelopathic phenomenon is linked directly and indirectly with a diversity of physical, chemical and biological processes involving a large array of compounds and their precursors. However, no matter how complicated it is we must have an acceptable definition indicating the limits and boundary of the discipline. With respect to specialization and worldview we must consider the rich disciplinary diversity of the field as strength rather than an obstacle because complicated research questions in allelopathy can only be answered through interdisciplinary research. As the mechanism of allelopathy becomes more and more clear to us it will be easier to define it. I can think of three things requiring attention in redefining allelopathy i) mechanism, ii) evolutionary significance (ie. the need for plants to have this property) and iii) the outcome (effects on neighbours, ecosystems).

Future direction

Self-criticism and good science

In order to think about future directions we must reflect on how we are doing now, what is working and what is not working. In my view, we are doing well and lately research in allelopathy has made quite a breakthrough, at least in the sense that the scientific community is becoming more receptive to the idea that it is worthwhile to pursue research in allelopathy. This has been possible only because of good science published in influential journals. We have to do more of this to make an impact. It is a challenging but necessary field of research that can keep us intrigued because of its complexity and applications in sustainable resource management. What has not worked in the past and will not work in the future is a half-hearted endeavour. Allelopathy research without clear and logical question(s), unjustifiable methodology, poor data and unreasonable conclusions has been counter productive. There is a tremendous opportunity for allelopathy researchers to contribute to the achievement of sustainable management of natural resources be it forestry, agriculture, horticulture, grassland, rangeland, parks, ecological reserves and conservation areas. I have already mentioned that for too long we have been preoccupied to find “proof” of allelopathy. The time has come to take the next step. By working collaboratively with chemists, agronomists, ecologists, hydrologists, bio-statisticians and most of all with the farmers, foresters and aquaculturalists, we must try to solve the ecological problems at hand by using the knowledge of allelopathy. It is only then we can gain respect for our science and our profession.

Allelochemicals as weed control agents, signaling molecules and genetic manipulation

Birkett et al (2001) made a literature review asking the question whether allelopathy offers real promise for practical weed management. There are several different approaches to weed control, most popular being total elimination of weeds by chemical herbicides widely practised in industrial agriculture. There are potent allelochemicals in plants (Nimbal et al. 1996; Czarnota 2001) but the chance of finding allelochemicals that can be used as industrial bioherbicides for successful weed control is not good (Duke et al. 2001). However, microbially synthesized herbicide such as bialophos has been in the market for several years showing success in weed control in agriculture and forestry (Jobidon 1991). The second approach is using allelopathic plants as mulch, cover crop, row crop etc that take advantage of not just the chemicals inhibiting seed germination and growth of crops but its biomass which physically suppress weed growth (Mattice et al. 2000; Moyer et al. 2000). This method does not aim for complete eradication of weeds by chemicals but rather allows coexistence of competing plants with much reduced vigor. The biomass added to the soil in this practice incorporates organic matter to the rhizosphere which influences the soil microbial ecology and nutrient conditions. Traditional agriculture has been using this approach of weed control and there is room for further improvement through research.

Following extensive lab and field trials several allelopthic rice varieties have been selected (Dilday et al 1991) and although it promises to be challenging we are steps closer in transferring allelopathic property in rice by plant breeding (Olofsdotter 2001a,b; Olofsdotter et al. (2002). Genetically modified rice with insect resistance is currently at pre-commercial field trial stage in China (Huang et al. 2005), Golden rice 2 has been genetically engineered by incorporating certain enzymes (psy) from maize. This has resulted in a dramatic increase in Beta-carotine (pro-vitamin A). Use of this rice can reduce vitamin A deficiency, a common and very serious problem encountered in a large population in Asia where rice is the staple food (Paine et al. 2005). Research is underway in identifying the signal compounds in plants that can synthesize chemicals used for defense for insects and pests. If gene transfer for insect resistance, pro-vitamin A or signaling compounds from plant to plant is possible then transfer of allelopathic genes for weed control is also possible. Success in this area will definitely reduce and in some cases eliminate the use of herbicides and pesticides. There are exciting research and development opportunities in these emerging fields. However, as in many GM organisms the risk of long-term adverse effects of such genetic manipulations on the environment and human health must be assessed.

In conclusion I would like to emphasize three points: i) in allelopathy research we must keep a dual focus, a) fundamental mechanistic and b) applied problem solving, ii) we must enhance interdisciplinary collaboration and iii) we must strive for effective communication by publishing results in peer reviewed journals, organizing workshops and conferences where we learn from each other through discussions. The Fourth World Congress on Allelopathy provides such an excellent opportunity and we very much appreciate the hard work of the local organizing committee under the leadership of Professor Jim Pratley.

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