“Metal hyperaccumulating plants contain very high metal contents. Because of the general toxicity of metals, chemically-mediated biotic interactions involving hyperaccumulating plants may differ greatly from those of non-hyperaccumulators. Recent research has demonstrated a defensive function for hyperaccumulated metals against herbivores and pathogens. We predict that some herbivore/pathogen species have evolved metal tolerance, and suggest that resulting high metal levels in herbivores/pathogens may defend them against their own predators. Little is known regarding interference and commensal interactions involving hyperaccumulating plants. Decreased competition may occur through an interference interaction similar to allelopathy, in which enrichment of metal in the soil under a hyperaccumulator plant’s canopy may inhibit another plant species, thus resulting in “elemental allelopathy”. Metal enrichment of soil under hyperaccumulators also may result in commensalism if another plant species (possibly another hyperaccumulator) derives a benefit from growing in the metal-enriched soil under the canopy of a hyperaccumulating overstory plant. It seems likely that high-metal plant litter will host a specialized microflora of decomposers and may affect nutrient cycling rates. Mutualist biotic interactions also may be affected by the elevated metal contents of hyperaccumulating species. Mycorrhizal fungi may form mutualisms with hyperaccumulators, but the phenomenon is poorly-explored. The few cases investigated to date have not detected mycorrhizae. Pollination and seed dispersal mechanisms may require biotic vectors that might be affected by plant metal content. Hyperaccumulating plants may have solved this dilemma in three ways. First, some may rely on abiotic vectors for pollen or seed dispersal. Second, biotic vectors used by these species may have varied diets and thus dilute metal intake to non-toxic levels. Finally, biotic vectors may have evolved tolerance of elevated dietary levels of metals, and perhaps have become specialists on hyperaccumulator species.”
NOVEL WEAPONS HYPOTHESIS
Allelopathy, Invasiveness and the Novel Weapons Hypothesis
“It is the nature of some plants not to kill, but to injure, by the odour they emit, or by the admixtures of their juices; such is the influenced exercised by the radish and the laurel upon the vine.” —Pliny
“Allelopathy is the production and release of chemicals that harm or otherwise decrease the fitness of other plants (Hierro and Callaway 2003). More simply put, allelopathy is chemical competition between plants (Ricklefs 1990). While the definition is sometimes broadened to include non-antagonistic relationships between organisms (Whittaker and Feeny 1971), I have restricted my definition to chemically-induced antagonism, whether direct, such as the release of a phytotoxin into the soil, or indirect, the facilitation of competition-reducing forest fires by eucalyptus trees rich in highly flammable oils (Much 1970). Allelopathy as a mechanism for plant-plant interactions appears in a 1925 study by A. B. Massey that has been and is considered one of the defining experiments in the history of allelopathy, although one common direct mechanism for allelopathy (phytotoxins exuded into the soil by plant roots) appears in 1832 (De Candolle in Hieero and Callaway 2003, Whittaker and Feeny 1971), and other allelopathic studies were undertaken earlier (Schreiner and Reed 1907, 1908). The Massey study showed that walnut trees release toxins that impeded the growth of other plants, giving it a competitive advantage (Massey 1925 in Ricklefs 1990). It led to many other studies, about walnuts and other potential allelopaths, and the field peaked in the 1960s and 70s (Hierro and Callaway 2003) before growing criticism (e.g. Keeley 1988) began to decrease interest (Hierro and Callaway 2003). Studies of allelochemics never stopped altogether, though, and there have been several important studies in the past decade with more sophisticated and accurate methodology than earlier experiments. Chemical competition in addition to resource competition has implications for population dynamics, in invasive species for example (Hierro and Callaway 2003), which has been the focus of many recent studies, producing very interesting results. Information about the role of allelopathy in some invasive species could contribute to more effective methods of controlling these weeds, as it increases understanding of the mechanisms involved in allelopathy and its role in the overall competitiveness of a plant. Experiments comparing the role of allelopathy in native versus invasive populations also further this understanding. Finally, understanding the function of allelopathy in native habitats also adds to our knowledge of community and ecosystem dynamics. Starting with an analysis of problems in early allelopathic studies, my goal with this paper is to analyze the role of direct and indirect allelopathy in plant communities, the role of allelopathy in invasive plant species and the novel weapons hypothesis, and especially the role of allelopathy in several key invasive plant species, including Centaurea maculosa, C. diffusa and Alliaria petiolata.
Early Studies of Allelopathy
Most studies testing for allelopathy, including those from the 1960s, 70s and into the 80s, used bioassays: a solvent, often water, was run over the roots, stems or both of a potential allelopath, or the plant was crushed, either fresh or dried, and then soaked in water and filtered to create an exudate. There were other methods as well, bu the end result was a solution that was then added to seeds growing in Petri dishes on agar or filter paper, or an aqueous medium. Sometimes specific chemicals were isolated and used alone to identify the active allelochemical. Multiple plants were found to be allelopathic: Centaurea diffusa (Muir and Majak 1983), Eltrygia repens (Le Torneau and Heggenesse 1957; Weston et al. 1987), Parthenium hysterophorus (Kanchan and Jayachandra 1980; Pandey 1994) and Sorghum halepense (Abdul-Wahab and Rice 1967), for example. Certain studies even seemed to find that most plants were allelopathic, directly or indirectly by affecting soil biota, to the point where experiments would find allelopathy in thirteen out of twenty, ten out of twelve and fourteen out of fourteen species (Rice 1964). Suspicious growth habits combined with potentially phytopathic chemicals isolated from an exudate of the plant were considered enough to definitely determine allelopathy in a plant (Muller 1965, 1966). Criticism over these methods began to emerge. Bioassays are insufficient evidence of allelopathy because they do not factor in environmental factors other than the possible presence of allelochemicals, and they do not accurately represent field conditions (Keeley 1988). Chemicals regularly cited as allelopathic might not persist long enough in the soil to have a significant impact on plant growth: phenolic acids (cited as potential allelochemicals in Sorghum halepense (Abdul-Wahab and Rice 1967), Adenostoma fasciculatum (Kaminsky 1981) and Parthenium hysterophorus (Kanchan and Jayachandra 1980)) were found to persist in the soil for only hours: they could only have an important allelochemical effect if they emerged at a very specific point of plant development, for example the peak germination point of a major competitor (Ohno 2001). Another study supports these results, showing that the activity of phenolic acids was only allelopathic on germination paper, and that even greatly exaggerated levels of the chemicals had no effect on plants growing in a soil substrate (Krogmeier and Bremner 1989). Soil itself significantly lowered allelopathic effects to the point of negating them completely in multiple experiments. Euphorbia esula and Bundas orientalis were both shown to be allelopathic in bioassays, but exudates added to plants growing in a soil medium had no allelopathic effects, both because of microbial activity in the soil and because of the soil structure itself: soil binds up allelochemicals much more effectively than an aquatic medium does (Le Tourneau and Heggeness 1957; Dietz et al. 1996). Another plant, Adenostoma fasciculatum, produced phenolic acids but never introduced enough of them into the soil to be phytotoxic (Kaminsky 1981). Allelopathy was clearly not one of the forms of competition for these plants, even if they contained chemicals that were allelopathic when applied in artificial conditions at concentrations that might be impossible to obtain in the field, even under optimal conditions. Bioassays were simply inaccurate: Stowe (1979) found that seven identified allelopaths did not follow the distribution patter that their alleged phytotoxicity should have produced. In contrast to this, Wardle et al. (1996) had opposite results on the relationship between bioassay-determined phytotoxicity and their result on the growth of Carduus nutans. Growth patterns in field conditions, such as apparent inhibition of growth around the potential allelopath, or monospecific stands, are often interpreted as evidence of allelopathy. It can be difficult to differentiate between the different forms of competition (chemical versus resource) by these methods, and there are often more factors that must be accounted for. In one experiment where Eltrygia repens was found to be allelopathic in bioassays (Weston et al. 1987; Le Torneau and Heggeness 1957), a negative correlation between plant competitor biomass and proximity to the allelopath was found; however, the role of limiting resources and resource competition is unspecified (Weston et al. 1987). The most famous example is a series of experiments on the role of allelopathy in the bare zones around certain desert shrubs in California (Salvia leucophylla, Adenostoma fasciculata and Artemisia californica) (Muller 1965; Muller 1966; Bartholomew 1970). Muller (1965) found that chemicals isolated from the shrubs were phytotoxic (although not necessarily under field conditions), and concluded that the bare zones surrounding the shrubs were caused by an allelopathic affect (1965; 1966). Bartholomew (1970) found that grazing and foraging by rabbits, mice, birds and other small animals had a significant effect on plant biomass, and that these animals stayed close to the protective shelter of the shrubs, increasing herbivory in these areas. Furthermore, he found that annual plants would grow in a purportedly allelopathic bare zone if animals were excluded. There were more mechanisms at work than simply allelopathy.
Refinements in Allelopathy Experiments
Higher standards for evidence of allelopathy began to be developed. Choesin and Boerner (1991) developed three criteria that must be met: firstly, the chemical must enter the soil in significant amounts; secondly, it must persist in the soil; and thirdly, it needed a mechanism through which to encounter the other plant. Bioassays did not satisfy these developing standards. An alternative to adding allelochemicals to an aqueous growing medium or agar plates is to add the chemical(s) to soil. This has been used to test the effects of plant extracts on nodulation in legumes (Rice 1964), although this sort of experiment requires determining a concentration of allelochemicals (and translating that to soil concentrations) that resembles that of field conditions (Callaway et al. 2008), often difficult, especially since soil microbes may break down some allelochemicals (Vivanco et al. 2004) and natural concentrations of chemicals may be unknown unless the plant has been very rigorously studies; even then, numbers may be conflicting (Callaway et al. 2008; Bais et al. 2003). Similarly, mulching plants with leaf litter from a potential allelopath, mimicking the decomposition of biomatter from plants in the field showed allelopathy in Cirsium arvense (Stachon and Zimdahl 1980) and Euphorbia esula (Steenhagen and Zimdahl 1979). The decomposing leaf matter specifically of Carduus nutans was found to be allelopathic in field tests (Wardle et al. 1994). In another variation on these types of soil tests, soil samples taken from either wild or cultivated stands of the potential allelopath are mixed with another substrate or used alone, which has shown allelopathy successfully (Steenhagen and Zimdahl 1999; Dietz et al. 1996). Sterile soil or soil inoculated with specific soil biota can also be pre-cultivated with an allelopath and then re-planted with the test plants after the allelopath has been removed (Callaway et al. 2008). One final soil-based method of experimenting on allelopathy is to plant the species to be tested together in a soil medium (He et al. 2009). This can be useful in certain, specific situations, but the obvious problem with it is that, normally, it does not differentiate between chemical and resource-based competition, since a decrease in growth is more likely to be from a plant being out-competed for resources such as light and nutrients than the result of phytotoxins. Activated carbon becomes an effective way to differentiate between these effects. Activated carbon absorbs or removes all or most allelochemicals from soil or other growing mediums (Le Tourneau and Heggenesse 1957; Rice 1964). It does not affect seed germination significantly, and insignificantly reduced seed germination or growth in some field experiments, but did not give any advantage to non-allelopathic plants being tested (Prati and Bossdorf 2004; Ridenour and Callaway 2000; Callaway and Aschehoug 2000), making it an effective way to test for allelopathy. Since the activated carbon will greatly reduce or negate any allelochemicals present, adding it to a pot with both an allelopath and a competitor will show to what extent the effects are caused by phytotoxins, and the carbon can be added to soil to provide a control that has almost identical conditions (Prati and Bossdorf 2004; Callaway and Aschehoug 2000; Ridenour and Callaway 2000; Rice 1964). Finally, the use of a “stairstep apparatus,” or a system of plants growing in sand substrates in pots (that is, the allelopath in one area and the other plant(s) in another, so that there is no root-root contact, to prevent resource competition) connected by a system that flushes water over their roots, spreading any potential allelochemicals throughout the system (Bell and Koeppe 1972; Stevens and Tang 1985). Potential concerns with this method, other than the difficulty in setting it up, is the effectiveness of sand in absorbing allelochemicals when compared to soils found in natural habitats, and the concentrations of the phytotoxins, both because of the substrate and because of the water flow. These new methods of testing for allelopathy have caused large improvements in the results attained, even if they are still imperfect. Despite this, Petri-dish bioassays remain popular because of their relative ease and simplicity (Robers and Anderson 2001), and because they allow for the isolation of specific chemicals (Vaughn and Berhow 1999). Bioassays also continue to be used as a supplement to more sophisticated experiments, or as a precursor to further investigation (Yamamoto 1995).
Direct allelopathy is direct chemical warfare: a phytotoxic chemical is released, often into the soil through the roots but also through other means such as toxins in decomposing leaf matter, that negatively impacts other plants. This is the best-studied form of allelopathy, and many plants have demonstrated it: Acroptilon repens (Alford et al. 2009), Anthoxanthum odoratum (Yamamoto 1995), Bidens pilosa (Stevens and Tang 1985), Centaurea maculosa (Bais et al. 2002, 2003; Ridenour and Callaway 2000), Centaurea diffusa (Vivanco et al. 2004), Cirsium arvense (Stachon and Zimdahl 1980), Euphorbia esula (Steenhagen and Zimdahl 1979), and Setaria faberii (Bell and Koeppe 1972). Many of these do not have isolated allelochemicals identified, but some research has been done on this: (±)-catechin from Centaurea maculosa, especially the (–)-catechin portion (Bais et al. 2002, 2003; Alford et al. 2009; He et al. 2009; Thorpe et al. 2009); coumarin from Anthioxanthum odoratum (Yamamoto 1995); sesquiterpine lactones from Parenthium hysterophorus (Kanchan and Jayachandra 1980) and C. diffusa (Muir and Majak 1983) which also produced 8-hydroxyquinoline (Vivanco et al. 2004); and 7,8benzoflavone from Acroptilon repens (Alford et al. 2009). As previously mentioned, phenolic acids are common potential phytochemicals, although their allelopathic potential under field conditions is unclear (Abdul-Wahab and Rice 1967; Kaminsky 1981; Ohno 2001; Krogmeier and Bremner 1989). Isothiocyanates such as allyl isothiocyanate and benzyl isothiocyanate (Vaughn and Berhow 1999) are tied to Alliaria petiolata and other Brassicaceae (Choesin and Boerner 1991; Vaughn and Berhow 1999). All of these have shown at least some direct allelopathic effect, although many have not been thoroughly tested, especially in conditions approximating those that would be found in the field.
Indirect Allelopathy and Microorganisms in Soil
Indirect allelopathy has been mentioned previously in the form of wild fire encouragement in Eucalyptus species (Mutch 1970). Most recent studies on indirect allelopathy, however, focus on the relationships between allelopaths, soil microbes and other plants. Allelopathic effects on other plants because of interactions with soil microbes has been found in Aristida oligantha (Rice 1964), Adenostoma fasciculatum (Kaminsky 1981), Centaurea diffusa (Vivanco et al. 2004), Alliaria petiolata (Callaway et al. 2008; Roberts and Anderson 2001; Stinson et al. 2006) and C. maculosa (Alford et al. 2009; Carey et al. 2004; Bais et al. 2002, 2003). Adenostoma fasciculatum was found to form associations with microorganisms that produced phytotoxic chemicals instead of being allelopathic in and of itself (Kaminsky 1981), but it seems to be mostly an exception. The relationship is unclear for several species, such as C. diffusa, where sterilizing soil suppressed the allelopath to varying extents depending on the population it was taken from, possibly because of differing abilities of soil biota to process the allelochemicals produced (Vivanco et al. 2004). The presence of a fungal pathogen in the growing medium of C. maculosa caused an increase in the concentration of allelochemicals, although it did not inhibit the growth of the pathogen (Bais et al. 2002). Aristida oligantha reduced nodulization of legumes and inhibited nitrogen-fixing and nitrifying bacteria (Rice 1964). Similarly, legume species were found to be particularly resistant to allelochemical effects caused by Acroptilon repens (Alford et al. 2009). In a more sophisticated, recent series of experiments, the allelochemical (±)-catechin from C. maculosa was found to affect nodulation as well, and to negatively impact the growth of Rhizobia–although some species seem to metabolize the allelochemicals (). To complicate things even further, a study by Carey et al. (2004) found that Centaurea maculosa may use arbuscular mycorrhizal fungi to “steal” carbon from Festuca idahoensis. The interactions between soil biota and allelopaths are clearly complicated. Alliaria petiolata also seems to use indirect allelopathy to increase its competitiveness. It prevents germination and colonization of abruscular mychorrhizal fungi (Roberts and Anderson 2001; Callaway et al. 2008; Stinson et al. 2006), and in the field, high Alliaria densities resulted in a lowered mychorrhizal inoculum potential (Roberts and Anderson 2001). Stinson et al. (2006) found that it was indirectly allelopathic, slowing growth and decreasing germination in trees, by negatively affecting arbuscular mychorrhizal fungal relationships. Further evidence of the effects of this fungal disruption is found in how the allelopathic effects of Alliaria were found to be ineffective or supportive of the growth of non-mycorrhizal plants (Callaway et al. 2008).
Allelopathy and Invasive Plants: The Novel Weapons Hypothesis
The novel weapons hypothesis is that plant communities co-evolve in species- and population-specific ways, so that allelopathy is countered by chemical resistances in the native ranges of a plant. However, when a plant is introduced to a new area, the vegetation is naïve to the chemical weapons of the invaders, granting them a sensitivity not present in species or populations with a history of proximity. This, rather than or in addition to predator release, drives invasiveness in certain species (Callaway et al. 2008). There is strong support for this theory in three primary species: Alliaria petiolata, Centaurea diffusa and C. maculosa. A fourth species, Solidago candensis, shows more complicated patterns of regional differences, involving allelochemicals, the origin of the allelopath, the origin of the affected species and the origin of the soil biota (Abhilasha et al. 2008). Still, biogeography is clearly an important element in its allelopathic effects. North American species (from the invasive range of C. diffusa) are much more sensitive to its allelochemicals (including 8-hydroxyquinoline) and less effective competitors than parallel European species from its native range (Callaway and Aschehoug 2000; Vivanco et al. 2004); there is also evidence that soil biota are better able to metabolize 8-hydroxyquinoline in European soils than in American ones (Vivanco et al. 2004). Centaurea maculosa exhibited very similar results (Thorpe et al. 2009; He et al. 2009; Bais et al. 2003) and Alliaria, although unrelated, showed the same patterns (Callaway et al. 2008; Prati and Bossdorf 2004). Alliaria allelochemicals were also more effective against North American arbuscular fungi, supporting indirect (fungicidal) allelopathy only in North America, further evidence of the novel weapons hypothesis and its role in the associations between allelopaths and soil biota.
While the role of allelopathy has been overstated in the past by inaccurate experiments, recent studies show that allelopathy may play an important role in some invasive plant species due to a chemical naïveté in invaded communities, either in the plants themselves (direct allelopathy) or through their indirect associations with nitrogen fixing bacteria, arbuscular mycorrhizae fungi and other soil biota: the novel weapons hypothesis. Three primary invasive species, Centaurea maculosa, C. diffusa and Alliaria petiolata show strong support for both allelopathy and the novel weapons hypothesis. This has many ramifications for conservation. As all three of the primary species used as examples are extremely invasive, there are many conservation efforts to control or eradicate them underway. If the role of allelopathy and naïve communities in their success as an invader is misunderstood or otherwise unaccounted for, it could impede attempts to control the invasiveness; for example, the introduction of a natural predator may not have as significant effects because its invasiveness is not entirely due to predator release. Many questions remain about the extent of allelopathy both in known species and in other species, especially other invasives. The role of soil biota and allelopathy is also unclear in many cases. Further experimentation should be done to test the novel weapons hypothesis, and the interplay of factors between different populations of soil microorganisms, allelopaths and invaded or native plants.”
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MICROBES as GEOACTIVE AGENTS
HOW PLANTS GOSSIP
ALARM SCENT WARNS OTHER TREES to KILL