Photo: Kochia, southwest Montana. © 2020 Delena Norris-Tull
Novel Weapons Hypothesis: Its role in the success of invasive plants
Summaries of the research and commentary by Dr. Delena Norris-Tull, Professor Emerita of Science Education, University of Montana Western, July 2020.
One problem with the “natural enemies” or EICA hypothesis is that it should apply to all non-native plants that are introduced to a new environment. But it does not. Many non-native plants (including many current and previous agricultural and ornamental crops) grow, either by accident or on purpose, in agricultural fields, gardens, lawns, etc., all over the world. Most of them never become “invaders.”
He, Feng, Ridenour, Thelen, Pollock, Diaconu, and Callaway (April, 2009) reported that spotted knapweed (Centaurea stoebe or C. maculosa) “shows evidence for evolutionary changes towards increased size and competitive ability in the invaded range.” But Callaway and Ridenour (Oct., 2004) challenged the hypothesis that increased size in new environments is what gives non-native species a competitive advantage. They proposed a “novel weapons hypothesis,” suggesting that some invasive species may be successful due to “unique allelopathic, defense, or antimicrobial biochemistry to which naïve native species are not adapted” (He, et al., 2009). Callaway and Ridenour, 2004, suggest that “some exotics transform from native weaklings to invasive bullies by exuding biochemicals that are highly inhibitory [allelopathic] to plants or soil microbes in invaded communities, but relatively ineffective against natural neighbors that may have adapted over time.” They report that over 100,000 different natural products have been identified in plants, many of which are specific to individual plant species. This diversity may be due to “selection pressures for many different jobs, including soil nutrient acquisition, defense against herbivory, root communication, and antimicrobial protection. Alternatively, many biochemicals may be metabolic byproducts without particular functions… There is no reason to think that novel weapons may have originally evolved for the purpose of poisoning other plants. There may be good reason, however, to think that biochemicals, once evolved, can affect other plants, that other plants or microbes may evolve to tolerate the chemicals exuded by their neighbors, and that possession of novel weapons may lead to their proliferation [in the introduced environment].”
Callaway and Ridenour, 2004, point out that little research has been conducted on the role of allelopathy within plant communities, and they summarized that research. “Recent evidence suggests that geographic coevolutionary trajectories based on unique biochemistry may affect plant coexistence and the development of communities,” and that, “disruption of these trajectories by invaders may therefore have profound consequences.” They point to the need for additional research related to the impact of plant biochemical exudates on soil biota, and the subsequent impacts on plant communities.
The novel weapon in spotted knapweed appears to be a root exudate, (±)-catechin, that inhibits growth of neighboring plants. Several studies support the phytotoxicity of (±)-catechin, while other researchers have found no or little phytotoxicity in the exudate. He, et al., 2009, conducted a series of experiments on spotted knapweed, to explore the novel weapons hypothesis. To control for likely geographic genetic differences, they compared knapweed plants from eight European native spotted knapweed populations to plants from nine North American invasive spotted knapweed populations. By growing seeds in pots in greenhouses, they compared the size of the plants from the North American and European populations. And they tested the competitive advantage of the two populations by planting them in pots, paired in competition with four native species from Western Montana, and four native European species. After four months of growth, plants were harvested, dried, and weighed. They found that the biomass of the North American population of knapweed plants was 31% greater than that of the European populations. They found that the mean biomass of all the North American knapweed populations was significantly higher than the mean biomass of all European populations.
Comparing biomass of the various native species with spotted knapweed plants with which they were paired, He, et al., 2009, found that, “European competitors suppressed C. maculosa from both regions much more than North American competitors. North American [native species] competitors were far more inhibited by C. maculosa than were European [native species] competitors.”
The following year, He, et al., 2009, further extended their experiment to examine the effects of spotted knapweed on a wider geographic range of native plant species. They planted knapweed in pots, paired with ten additional Western North American native plant species, and 15 additional European native plant species. However, in order to reduce the number of total test pots, they only included knapweed plants from one of the North American populations they had tested the year before, and plants from one European population. Unfortunately, these experiments had varied results and did not corroborate the findings of the previous year’s experiments.
The following year, He, et al., 2009, tested the direct effects of (±)-catechin phytotoxicity by applying concentrations of the exudate in sand, using known in situ soil concentrations. They found that (±)-catechin had “much stronger effects on native North American species than on native European species… The effect of (±)-catechin on the mortality of North American species was highly variable… (±)-Catechin reduced the biomass of North American natives more than it reduced the biomass of European natives... (±)-Catechin did not have a significant effect on the germination or subsequent mortality of European species, but decreased the germination of North American species by 46% and increased the mortality of germinants from 5% in the control to 50% in the treatment. The effect of (±)-catechin was more consistent across North American species than in experiment 1, with all [native] species showing reduced germination and increased mortality.”
He, et al., 2009, describe various limitations of their first two experiments. They suggest that, while their conflicting results cause their conclusions to be tentative, the larger size of the knapweed plants from the North American populations “may not be as important for competitive domination as possessing a ‘novel weapon.’” In the (±)-catechin experiments, they found variability in the effects of the exudate on different native species. Other authors have found the phytotoxic effects to range from zero to very strong between diverse native species.
He, et al., 2009, suggest that European native species, through coevolutionary processes, may be adapted to the biochemicals in European spotted knapweed root exudates, whereas North American native species are not adapted to the exudate from the non-native spotted knapweed invasive plants. They point out that not enough research has been conducted on the factors that give competitive advantage to non-native plants that become successful invasives.
Ridenour, Vivanco, Feng, Horiuchi, and Callaway (2008) conducted additional greenhouse experimental comparisons of the success of European populations of spotted knapweed compared with North American populations of knapweed. They found that the North American knapweed plants not only grew larger than their European counterparts, but they were more resistant to insect herbivory than the European plants. (This research summary is also included in the chapter on Biocontrol).
Ridenour, et al., 2008, tested two specialist biocontrol insects, the European root boring weevil, Cyphocleonus achates (first released in the US in 1987), and a moth, Agapeta zoegana, that has root boring larvae (first released in the US in 1984). Both species do substantial damage to knapweed roots, and adult Cyphocleonus eat the leaves. Ridenour, et al., 2008, also used some native North American generalist insects in their experiments, insects that are not used for biocontrol.
The results from these experiments are somewhat astonishing. The specialist biocontrol insects produced significantly more damage to the European knapweed plants than to the North American knapweed. While the weevil caused significant damage to both populations of plants, nearly twice as many North American knapweed plants survived than did the European plants. The moth larvae also preferentially attacked the European plants. Each of the generalist insects (native to North America) also caused more severe damage to the European plants.
Ridenour, et al., 2008, found that leaves on the North American spotted knapweed plants “contained approximately two times higher concentrations of the defense compound precursor, phytol, in their leaves than the European populations.” North American knapweed leaves were also much tougher than the European plants. They concluded that North American spotted knapweed plants “were bigger, elicited stronger competitive effects, and demonstrated stronger competitive responses than European populations.” They were able to rule out phenotypic plasticity as a cause of the differences. They concluded that some of their results support the “evolution of increased competitive ability” hypothesis. But they also concluded that, “North American Centaurea genotypes were also consistently better defended against (or avoided by) specialist and generalist consumers, demonstrating both a stronger inhibitory effect on the consumers (resistance) and a better ability to grow in response to herbivory (tolerance), which questions the trade-off based assumptions of EICA as a consistent mechanistic basis for the continental differences between populations.” Ridenour, et al., 2008, suggest that “selection for effective competitive or defense traits may not be easily coupled to resource or energetic trade-offs for a simple reason: different defense or allelopathic chemicals may cost the same energetically or nutritionally, but differ a great deal in effectiveness… Physiological costs of a biochemical may be trivial in an ecological context if the biochemical is exceptionally effective or performs more than one job.”
Ridenour, et al., 2008, also state that “there is evidence that (±)-catechin, and allelopathic chemicals from other Centaurea species, are more toxic to naïve (native) North American species than to European species in their native communities…the novelty of a biochemical may correlate with its superior effectiveness because new and naïve neighbors would not have had the opportunity to evolve tolerance or resistance… If invaders possess traits, such as allelochemical weapons or defense chemicals, that provide greater competitive or defense advantages in their new habitats than in their original ranges, then selection pressure for the traits conferring competitive advantages may be greater on the genotypes in the invaded regions… Individuals that produce larger amounts of unusually effective defense or allelopathic chemicals might grow and reproduce more than individuals that do not, resulting in adaptive evolution driven by selection on specific biochemistry.”
Some results from the experiments by Ridenour, et al., 2008, and by He, et al., 2009, may support the EICA hypothesis. But the novel weapons hypothesis would challenge the idea that greater biomass in spotted knapweed is caused by the lack of natural consumers in the non-native environment. Rather, larger biomass may be a secondary result. If biochemicals in spotted knapweed are able to reduce growth in neighboring native plants, and/or if the biochemicals reduce herbivory on spotted knapweed, the knapweed plants can put more energy into growth.
References:
Next Sections on research on the success of invasive species:
Novel Weapons Hypothesis: Its role in the success of invasive plants
Summaries of the research and commentary by Dr. Delena Norris-Tull, Professor Emerita of Science Education, University of Montana Western, July 2020.
One problem with the “natural enemies” or EICA hypothesis is that it should apply to all non-native plants that are introduced to a new environment. But it does not. Many non-native plants (including many current and previous agricultural and ornamental crops) grow, either by accident or on purpose, in agricultural fields, gardens, lawns, etc., all over the world. Most of them never become “invaders.”
He, Feng, Ridenour, Thelen, Pollock, Diaconu, and Callaway (April, 2009) reported that spotted knapweed (Centaurea stoebe or C. maculosa) “shows evidence for evolutionary changes towards increased size and competitive ability in the invaded range.” But Callaway and Ridenour (Oct., 2004) challenged the hypothesis that increased size in new environments is what gives non-native species a competitive advantage. They proposed a “novel weapons hypothesis,” suggesting that some invasive species may be successful due to “unique allelopathic, defense, or antimicrobial biochemistry to which naïve native species are not adapted” (He, et al., 2009). Callaway and Ridenour, 2004, suggest that “some exotics transform from native weaklings to invasive bullies by exuding biochemicals that are highly inhibitory [allelopathic] to plants or soil microbes in invaded communities, but relatively ineffective against natural neighbors that may have adapted over time.” They report that over 100,000 different natural products have been identified in plants, many of which are specific to individual plant species. This diversity may be due to “selection pressures for many different jobs, including soil nutrient acquisition, defense against herbivory, root communication, and antimicrobial protection. Alternatively, many biochemicals may be metabolic byproducts without particular functions… There is no reason to think that novel weapons may have originally evolved for the purpose of poisoning other plants. There may be good reason, however, to think that biochemicals, once evolved, can affect other plants, that other plants or microbes may evolve to tolerate the chemicals exuded by their neighbors, and that possession of novel weapons may lead to their proliferation [in the introduced environment].”
Callaway and Ridenour, 2004, point out that little research has been conducted on the role of allelopathy within plant communities, and they summarized that research. “Recent evidence suggests that geographic coevolutionary trajectories based on unique biochemistry may affect plant coexistence and the development of communities,” and that, “disruption of these trajectories by invaders may therefore have profound consequences.” They point to the need for additional research related to the impact of plant biochemical exudates on soil biota, and the subsequent impacts on plant communities.
The novel weapon in spotted knapweed appears to be a root exudate, (±)-catechin, that inhibits growth of neighboring plants. Several studies support the phytotoxicity of (±)-catechin, while other researchers have found no or little phytotoxicity in the exudate. He, et al., 2009, conducted a series of experiments on spotted knapweed, to explore the novel weapons hypothesis. To control for likely geographic genetic differences, they compared knapweed plants from eight European native spotted knapweed populations to plants from nine North American invasive spotted knapweed populations. By growing seeds in pots in greenhouses, they compared the size of the plants from the North American and European populations. And they tested the competitive advantage of the two populations by planting them in pots, paired in competition with four native species from Western Montana, and four native European species. After four months of growth, plants were harvested, dried, and weighed. They found that the biomass of the North American population of knapweed plants was 31% greater than that of the European populations. They found that the mean biomass of all the North American knapweed populations was significantly higher than the mean biomass of all European populations.
Comparing biomass of the various native species with spotted knapweed plants with which they were paired, He, et al., 2009, found that, “European competitors suppressed C. maculosa from both regions much more than North American competitors. North American [native species] competitors were far more inhibited by C. maculosa than were European [native species] competitors.”
The following year, He, et al., 2009, further extended their experiment to examine the effects of spotted knapweed on a wider geographic range of native plant species. They planted knapweed in pots, paired with ten additional Western North American native plant species, and 15 additional European native plant species. However, in order to reduce the number of total test pots, they only included knapweed plants from one of the North American populations they had tested the year before, and plants from one European population. Unfortunately, these experiments had varied results and did not corroborate the findings of the previous year’s experiments.
The following year, He, et al., 2009, tested the direct effects of (±)-catechin phytotoxicity by applying concentrations of the exudate in sand, using known in situ soil concentrations. They found that (±)-catechin had “much stronger effects on native North American species than on native European species… The effect of (±)-catechin on the mortality of North American species was highly variable… (±)-Catechin reduced the biomass of North American natives more than it reduced the biomass of European natives... (±)-Catechin did not have a significant effect on the germination or subsequent mortality of European species, but decreased the germination of North American species by 46% and increased the mortality of germinants from 5% in the control to 50% in the treatment. The effect of (±)-catechin was more consistent across North American species than in experiment 1, with all [native] species showing reduced germination and increased mortality.”
He, et al., 2009, describe various limitations of their first two experiments. They suggest that, while their conflicting results cause their conclusions to be tentative, the larger size of the knapweed plants from the North American populations “may not be as important for competitive domination as possessing a ‘novel weapon.’” In the (±)-catechin experiments, they found variability in the effects of the exudate on different native species. Other authors have found the phytotoxic effects to range from zero to very strong between diverse native species.
He, et al., 2009, suggest that European native species, through coevolutionary processes, may be adapted to the biochemicals in European spotted knapweed root exudates, whereas North American native species are not adapted to the exudate from the non-native spotted knapweed invasive plants. They point out that not enough research has been conducted on the factors that give competitive advantage to non-native plants that become successful invasives.
Ridenour, Vivanco, Feng, Horiuchi, and Callaway (2008) conducted additional greenhouse experimental comparisons of the success of European populations of spotted knapweed compared with North American populations of knapweed. They found that the North American knapweed plants not only grew larger than their European counterparts, but they were more resistant to insect herbivory than the European plants. (This research summary is also included in the chapter on Biocontrol).
Ridenour, et al., 2008, tested two specialist biocontrol insects, the European root boring weevil, Cyphocleonus achates (first released in the US in 1987), and a moth, Agapeta zoegana, that has root boring larvae (first released in the US in 1984). Both species do substantial damage to knapweed roots, and adult Cyphocleonus eat the leaves. Ridenour, et al., 2008, also used some native North American generalist insects in their experiments, insects that are not used for biocontrol.
The results from these experiments are somewhat astonishing. The specialist biocontrol insects produced significantly more damage to the European knapweed plants than to the North American knapweed. While the weevil caused significant damage to both populations of plants, nearly twice as many North American knapweed plants survived than did the European plants. The moth larvae also preferentially attacked the European plants. Each of the generalist insects (native to North America) also caused more severe damage to the European plants.
Ridenour, et al., 2008, found that leaves on the North American spotted knapweed plants “contained approximately two times higher concentrations of the defense compound precursor, phytol, in their leaves than the European populations.” North American knapweed leaves were also much tougher than the European plants. They concluded that North American spotted knapweed plants “were bigger, elicited stronger competitive effects, and demonstrated stronger competitive responses than European populations.” They were able to rule out phenotypic plasticity as a cause of the differences. They concluded that some of their results support the “evolution of increased competitive ability” hypothesis. But they also concluded that, “North American Centaurea genotypes were also consistently better defended against (or avoided by) specialist and generalist consumers, demonstrating both a stronger inhibitory effect on the consumers (resistance) and a better ability to grow in response to herbivory (tolerance), which questions the trade-off based assumptions of EICA as a consistent mechanistic basis for the continental differences between populations.” Ridenour, et al., 2008, suggest that “selection for effective competitive or defense traits may not be easily coupled to resource or energetic trade-offs for a simple reason: different defense or allelopathic chemicals may cost the same energetically or nutritionally, but differ a great deal in effectiveness… Physiological costs of a biochemical may be trivial in an ecological context if the biochemical is exceptionally effective or performs more than one job.”
Ridenour, et al., 2008, also state that “there is evidence that (±)-catechin, and allelopathic chemicals from other Centaurea species, are more toxic to naïve (native) North American species than to European species in their native communities…the novelty of a biochemical may correlate with its superior effectiveness because new and naïve neighbors would not have had the opportunity to evolve tolerance or resistance… If invaders possess traits, such as allelochemical weapons or defense chemicals, that provide greater competitive or defense advantages in their new habitats than in their original ranges, then selection pressure for the traits conferring competitive advantages may be greater on the genotypes in the invaded regions… Individuals that produce larger amounts of unusually effective defense or allelopathic chemicals might grow and reproduce more than individuals that do not, resulting in adaptive evolution driven by selection on specific biochemistry.”
Some results from the experiments by Ridenour, et al., 2008, and by He, et al., 2009, may support the EICA hypothesis. But the novel weapons hypothesis would challenge the idea that greater biomass in spotted knapweed is caused by the lack of natural consumers in the non-native environment. Rather, larger biomass may be a secondary result. If biochemicals in spotted knapweed are able to reduce growth in neighboring native plants, and/or if the biochemicals reduce herbivory on spotted knapweed, the knapweed plants can put more energy into growth.
References:
- Callaway, R.M., & Ridenour, W.M. (Oct., 2004). Novel weapons: Invasive success and the evolution of increased competitive ability. Frontiers in Ecology and the Environment, 2 (8), 436-443.
- He, W., Feng, Y., Ridenour, W.M., Thelen, G.C., Pollock, J.L., Diaconu, A., & Callaway, R.M. (April, 2009). Novel weapons and invasion: Biogeographic differences in the competitive effects of Centaurea maculosa and its root exudate – catechin. Oecologia, 159 (4), 803-815.
- Ridenour, W.M., & Callaway, R.M. (Oct., 2004). Novel weapons: Invasion success and the evolution of increased competitive ability. Frontiers in Ecology and the Environment, 2(8): 436- 443.
- Ridenour, W.M., Vivanco, J.M., Feng, Y., Horiuchi, J. & Callaway, R.M. (2008). No evidence for trade-offs: Centaurea plants from America are better competitors and defenders. Ecological Monographs, 78, 369–386.
Next Sections on research on the success of invasive species: