Even in antiquity there was an awareness that plants influence the growth of their neighbors. The earliest reference comes from Theophrastus (called the “father of botany”) who, roughly 2300 years ago, noted that chickpea killed weeds and depleted the soil. He might have been describing what we call “allelopathy”, the phenomenon in which a chemical produced by one plant interferes with the growth of another.
The classic example of allelopathy that is familiar to most gardeners is black walnut (Juglans nigra). Black walnut and its close relatives (butternut, Juglans cinerea, being one of them) release a chemical (juglone) that causes susceptible plants growing near it to yellow, wilt, and die. Juglone is present in all parts of the plant and is the staining, brown pigment in walnut hulls. Solanaceous annuals, such as tomato (Lycopersicon spp.), are especially sensitive to it.
There are good reasons to study allelopathy. One is the search for natural compounds that rival synthetic agrochemicals in efficacy and perhaps trump them for environmental and human safety. Another is breeding allelopathy into crop plants to suppress weeds, as in the case of rice where there is evidence of natural allelopathy.
However, allelopathy is controversial and not well understood. Demonstrating that a plant chemical has a clear biological effect in nature is difficult. Test conditions will strongly influence any experiment designed to investigate allelopathic activity. Also, there are innumerable interactions that can occur in the soil. A compound can be metabolized and inactivated by soil microorganisms. It may be irreversibly bound to soil particles, rendering it null. It will certainly become increasingly dilute the farther it diffuses from its source. All these variables and others need to be explored and controlled.
A further complication is that plants also interact through competition for limited resources, mostly light, water, and soil nutrients. The manifestations of allelopathy and competition are similar. Sometimes they are identical. To demonstrate allelopathy, an isolated plant compound must be toxic to other plants even when interactions such as competition are removed, and any experimental design that separates allelopathy from competition may be unnatural.
A persuasive, but false, instance of allelopathy involves purple sage (Salvia leucophylla), a herbaceous plant that grows in the southern California coastal scrub plant community. Beneath and under purple sage are zones of bare ground (“halos”) where apparently no plants can grow. These halos were theorized to be caused by the allelopathic effect of volatile compounds emitted by purple sage. Laboratory work supported the hypothesis and confirmed that isolated purple sage compounds were biologically active and inhibited seed germination. These results were assumed to apply in nature, and the work was published in Science, the most prestigious scientific journal in the world. A photo of plant-free zones around purple sage highlighted the article on the issue’s cover.
A competing theory postulated that small birds and rodents seeking protection from predators hide beneath purple sage and, feeding on seeds and seedlings, create and maintain the zones of bare ground. Several years after the Science article appeared, a graduate student fenced plots of purple sage to exclude birds and rodents; seeds readily sprouted and grew to fill the bare areas. Thus, science is rarely settled or “QED”.
There is strong evidence, though, that allelopathy or something like it plays a role in the success of invasive plants. Garlic mustard (Alliaria petiolata), which must now be familiar to all North American gardeners, is an example. The plant is native to Europe and was first reported in North America on Long Island, NY, in 1868. It has since spread across most of the USA and much of Canada. It is a threat to native plants, and the animals that depend on them, in forest plant communities wherever it grows.
In a couple of growing seasons, garlic mustard is able to suppress and displace many of the plants that live in the forest understory and at its margin, including seedlings of the dominant canopy trees. It becomes far more abundant here than in its native range in Europe. There it is a weak competitor only and coexists with many of the same plants that it so successfully outcompetes on this continent.
What accounts for this difference? At least two basic possibilities exist to explain the success of invasive species in general: there is weaker opposition from other species in the new range than at home, and the invasive plant has stronger effects in the new range than at home. For garlic mustard, both may play a role, but the second possibility is the key. Garlic mustard has novel compounds that are particularly destructive to mycorrhizal fungi here in its new range.
Most vascular plants form mycorrhizal associations in which fungi grow within or in intimate contact with plant roots. These are mutualistic relationships that involve symbiotic nutrient exchange; fungi “feed” plants minerals and water, and plants provide the fungi photosynthetically derived sugars. Many plants, but not all, are dependent (some highly dependent) on these associations for growth and survival. The herbs and woody perennials found where garlic mustard is so successful are especially dependent on these fungi.
Experiments show that garlic mustard grown in U.S. soils decreases the concentration of resident mycorrhizal fungi. When North American plants are sown to this soil, the mycorrhizae-dependent plants do not germinate. The grasses and sedges that are not so dependent on fungi grow essentially normally. Garlic mustard grown in European soils does not change the concentration of mycorrhizal fungi, and when European varieties of the same plants as those tested in the USA are sown to this soil, germination is normal. Purified extracts of garlic mustard added to soil give the same results.
Garlic mustard’s method of success then is not “direct” allelopathy. Rather, by the chemicals it emits, garlic mustard inhibits mutualistic fungi that many of our native plants rely on for survival, and, so, it is able to outcompete these plants. In Europe, the fungi that coevolved with garlic mustard are not sensitive to these chemicals, and the explosive growth that epitomizes garlic mustard’s invasion of the USA is checked.
Of course, plants are rooted in one spot. Where animals can range far and wide seeking water, food, and companionship, plants cannot. Yet, in their own way, plants are every bit as dynamic as animals, maybe more so. They respond to their environment rapidly and reversibly in ways that could be termed “behavior”. This is seen not only in plants’ ability to sense up and down or where light comes from but also in their capacity to manipulate their environment chemically. Plants use an astonishing array of chemicals to influence their world, from defense against “enemy” plant pathogens and herbivores to acquisition of nutrients. What we call allelopathy is just one facet of this. Our conception of allelopathy—as discrete and unconnected with the numerous other chemical interactions that plants engage in—is artificial and limits our ability to model and clearly understand allelopathy.
To use a current word, allelopathy is more “nuanced” than we thought. It is not a single mechanism or plant function; it’s an expression of many. There is at present active work on allelopathy in many plant science disciplines, ecology and weed science to name two. This is a good thing. The more we regard allelopathy as part of a larger puzzle, the more we will understand it. Theophrastus would probably approve.