Photo: Kochia, southwest Montana. © 2020 Delena Norris-Tull
Enemy Release Hypothesis (ERH): Its role in the Success or Failure 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, updated November 2024.
Do invasive species succeed in the new environment because of some traits that are inherent in the species when they arrive in the new habitat, or do they develop/evolve new or enhanced competitive advantages within the new environment?
Research in support of the hypothesis
A number of researchers have posed that plant and animal species become invasive due to the lack of natural predators in their new habitat. When placed in a new environment, the plant or animal species is ‘released’ from its natural enemies, and thus can thrive. Ridenour, Vivanco, Feng, Horiuchi, and Callaway (2008) note that the enemy release hypothesis is based on the idea that “exotic [plant] invaders explode in abundance because they are no longer suppressed by the specialist herbivore consumers they evolved with in their natural environments” (Also see Callaway & Ridenour, 2004).
Ziska and Runion (2007, p. 264) point out that invasive plants have a number of biological similarities that help explain why they become problems. Plants become problems in agriculture because of their superior “colonization of disturbed environments, vigorous growth, prodigious seed production, and seed longevity.” In addition, some invasives are able to spread vegetatively, in other words, without seed production. Non-crop species become a problem if they can successfully compete with crop species.
The Enemy Release hypothesis is based on the following: Plants have a limited amount of energy resources (in the form of carbohydrates) to devote to (1) growth, (2) reproduction, and (3) defense from herbivore predation. Because there are no natural herbivore predators in the new ecological community, Blossey and Nötzold, 1995, proposed that introduced plant species do not have to waste resources defending against predators. Thus, they can redirect resources to growth and reproduction. This would, over time, result in the “evolution of increased competitive ability” (EICA). If this hypothesis is correct, this increased competitive ability could be a major factor in the plant’s success within the new habitat.
Treharne, 1989, found that non-native plants that become invasive have a greater genetic diversity and therefore greater physiological plasticity when compared with many crops. Schierenbeck, et al., 1994, found that invasive plant genotypes can be larger or more reproductive than the same species in its native habitat.
Research that challenges the hypothesis
Research in support of the Enemy Release hypothesis, or the IECA hypothesis, has shown mixed results, and has mainly focused on growth and reproduction and studies of direct defense mechanisms (e.g., mechanical defenses, such as spines and thorns, or biochemical defenses, such as alkaloids, lignins, flavonoids, and tannins). Some studies (Joshi and Vrieling, 2005; Ridenour, et al., 2008) have shown that some invasive plant species have a higher level of chemical defenses in the introduced habitat than in their native habitat, which is the opposite of what one would expect if the IECA hypothesis is correct. Both Centaurea maculosa and Senecio jacobaea appear to have a competitive advantage because they expend more resources on defense in the introduced habitat than in their native habitats.
Parker, Burkepile, & Hay (March 6, 2006) conducted a meta-analysis of 63 field studies that involved experiments in herbivore exclusion. Overall, these studies examined the impact of herbivore removal on more than 100 exotic plant species. 35 of these studies monitored herbivore effects on entire plant communities. They reviewed an additional 28 studies that monitored herbivore effects on specific species of exotic plants. Many diverse environments and many diverse herbivores (from cattle to bison, elk, deer, antelope, waterfowl, rabbits, rodents, fishes, insects, etc.) were included among these studies.
They concluded that enemy release hypothesis fails to explain invasive species success. For example, it does not take into account the fact that the vast majority of non-native plant species brought into the USA do NOT become invasive. They also challenged the effectiveness of biocontrol herbivores. For example, insects who are the natural predators of invasive species have been brought into the USA because it has been believed that they are the best predators to control invasive species. Rather, Parker, et al. concluded that generalist herbivores native to the USA are significantly more effective at controlling invasive species, than are the herbivores from the home environment. This makes sense if you consider that, in their native environment, plants that become invasive in the USA are NOT eliminated by the herbivores that naturally prey upon them at home. Rather, an ecological balance is reached between predator and prey in the home environment.
The meta-analysis revealed that "native herbivores strongly suppressed, whereas exotic herbivores strongly enhanced, the relative abundance of exotic plants... Overall, the relative abundance of exotic plants was 52% higher in communities grazed by exotic herbivores.. than in communities grazed by native herbivores." In addition, "exotic herbivores suppressed the abundance of native plants." They also found that, "Native vertebrate herbivores had a three- to five-fold larger impact on exotic plant survival than did native invertebrate herbivores."
Parker, et al., 2006, propose the biotic resistance hypothesis as a better answer to the problem than enemy release. Natural habitats, composed of many native plant species, are naturally resistant to invasive plant species. It is only when humans remove native species, to replace them with a crop or in grazing or other land use, that invasive species emerge as a problem.
Parker & Gilbert (2007) (not the same Parker) also found that invasive species of clover were more strongly suppressed by herbivores native to the US than by exotic herbivores. And native clover species did not differ from nonnative clovers in the degree of damage caused by exotic herbivores. In contrast to the biotic resistance hypothesis, they found that native plants were not preferentially preyed upon by exotic herbivores. For more detail, refer to the section within this website: Insects as Biocontrol.
Liu, et al. (2007), compared herbivore damage on native Eugenia, introduced invasive Eugenia, and introduced non-invasive Eugenia species in South Florida. Both of the introduced species had less herbivore damage than the native species. But the two introduced species did not differ from each other in herbivore damage.
Dawson, et al. (2014), conducted a multi-species experiment, comparing the response to pesticides of native plants, introduced invasive plants, and introduced non-invasive plants. They found that all plants gained more biomass when treated with pesticides. "However, invasive, non-invasive and native species did not differ in their biomass response to pesticide treatment... The proportion of leaves damaged on invasive species was significantly lower compared to native species, but not when compared to non-invasive species. However, the difference was lost when plant size was accounted for. There were no differences between invasive, non-invasive and native species in herbivore abundance."
Research with mixed results
Zhang, et al. (2018), found evidence both for and against Enemy Release theory. They conducted "a meta-analysis of 61 common garden studies that provide data on resistance and/or tolerance for both introduced and native populations on 32 invasive plant species." They found that "introduced populations, relative to native populations, decreased their resistance against specialists, and increased their resistance against generalists. These differances were significant when resistance was measured in terms of damage caused by the herbivore, but not in terms of performance of that herbivore." In addition, they found that "magnitude of resistance differences between introduced and native populations depended significantly on herbivore origin (i.e.,whether the test herbivore was collected from the native or non-native range of the invasive plant). Finally, tolerance to generalists was found to be higher in introduced populations, while neither tolerance to specialists nor that to simulated herbivory differed between introduced and native plant populations." They conclude that "enemy release from specialist herbivores and biotic resistance from generalist herbivores has contrasting effects on resistance evolution in invasive plants." They believe that these results "provide strong support for the Shifting Defense hypothesis."
Enemy release may only provide part of the answer
Dostál, et al. (2013), examined differences in herbivore and fungal damage on native and exotic plant species in the Czech Republic. Three community characteristics, "habitat fertility, relatedness to the native community and native species diversity, can influence the accumulation of enemies and thus potentially their impact on exotic species. However, these factors have usually been studied in isolation...and their relative importance in influencing enemy accumulation on exotic species remains unclear."
In the first part of their study, Dostál, et al., "scored all above-ground, visible, damage morphotypes (groups based on similar types of damage) caused by herbivores, along with the presence of fungal pathogens, in 72 populations of 12 exotic species invasive to Central Europe. [They] also estimated levels of leaf herbivory and fruit damage."
The study sites "included 12 exotic species represented by 72 populations in total (at least five populations per exotic species. All 12 species are naturalized in the Czech Republic, and 10 of them are considered invasive... In the second part of this study, where [they] tested the ERH and R-ERH hypotheses, [they] included nine exotic species and eight native congeneric species...; exotic species Conyza canadensis (also Erigeron canadense) and Erigeron annuus shared the same native congener Erigeron acer]. Exotic species were represented by 28 populations that were also included in the first part of the study, but here [they] used only those that co-occurred with populations of native congeners....All study populations contained at least 100 individuals per species and were located in central and north-west Bohemia... Some sites had populations of more than one exotic species or of more than one congeneric pair."
They discovered nine types of damage or enemies: powdery mildew, rust fungi, herbivory by mammals, phloem feeding aphids, insect leaf herbivory, leaf mining by larval insects, pre-dispersal fruit damage by insects, stem boring by insects, and stem scraping, likely by molluscs. Between 2008 and 2009, they scored 3920 plant individuals.
Dostál, et al. (2013), found that, "Damage diversity and damage levels on exotic populations increased with habitat fertility... Standing biomass was the most important variable that positively influenced mean damage diversity and mean proportion of leaf herbivory... Ellenberg indicator values for nutrients and moisture were the best predictors of cumulative damage diversity and mean proportion of damaged fruits."
"The other two predictor groups – relatedness and community diversity – were less important but they influenced the presence of damaged fruits and herbivory... Specifically, the presence of closely related native species in the community significantly increased the probability of fruit attack... Herbivory was less likely in communities with a high phylogenetic diversity... However, phylogenetic diversity was an important predictor (in terms of AIC weight) only when inverse relatedness metrics were fitted in the models."
The enemy release hypothesis (ERH) predicts that enemy load on exotic plants is smaller than on native competitors. The resource-enemy release hypothesis (R-ERH) predicts that that relationship is most pronounced in resource-rich habitats. In the second part of their study, Dostál, et al., "tested the ERH and the R-ERH by comparing damage of plants in 28 pairs of co-occurring native and exotic populations, representing nine congeneric pairs of native and exotic species."
"The R-ERH predicts that the difference between native and exotic species in enemy load should increase along a productivity gradient. For the ERH/R-ERH test, [Dostál, et al.] thus included the nine congeneric pairs of exotic and native species occurring in habitats that differed considerably in productivity, as expressed by standing biomass. Whereas some grew in resource-poor sites, such as road verges or scree slopes, with mean habitat productivities of 123 g/m 2 or 154 g/m 2 (the Matricaria pair and the Sedum pair, respectively), the Bidens congeneric pair was confined to very fertile sites: fish pond banks with a productivity of 655 g m of 655 g/m 2."
They found that "plants in fertile habitats had on average more damage morphotypes than those from less fertile habitats... Native and exotic congeners, however, experienced similar levels of mean damage and damage diversity... The mean proportion of damaged fruits was lower in exotic species, but this difference was not statistically significant ... The overall analysis indicated that damage diversity and damage levels were similar for congeneric pairs from unproductive and from productive habitats. However, when [they] regressed the difference between the native and exotic species, in mean and cumulative damage diversity, against productivity, [they] found significantly negative relationships for both variables... This indicates that exotic species tended to have lower damage diversity than native species in unproductive habitats but that the opposite was true in productive habitats. The R-ERH predicts the opposite pattern"....[These] results therefore suggest that the relationship between herbivory and productivity is similar for native and exotic species, although [they] could not definitely identify the mechanism behind this."
Dostál, et al.,"found higher rates of fruit damage on exotics growing with more closely related natives, which suggests that oligophagous herbivores (those that eat few specific types of food) were also likely to play a role in the case of pre-dispersal fruit damage."
"The enemy release hypothesis, which assumes that exotic species leave behind more enemies in their native range than they accumulate in the novel range..., has been a very influential concept in invasion biology. However, here [Dostál, et al.,] found no differences in damage diversity and levels between exotic and native congeners growing in the same communities. Even species introduced as recently as 50 years ago...had similar levels of damage as their native relatives, despite the fact that enemy accumulation by exotic species is assumed to be a slow process... Invasive populations in fertile habitats also had similar levels of damage diversity to their native counterparts, which does not support the R-ERH... and instead suggests that exotic species can be exposed to similar levels of damage as co-occurring native species, irrespective of the habitat productivity."
Genton, et al. (2005), compared the success of ragweed, Ambrosia artemisiifolia, in its native range in Canada and the USA, with its success in its introduced range in France. Ragweed is native to North America, but has expanded its range there dramatically due to human disturbance of other natural habitats. It causes serious illness in allergy and asthma sufferers in the fall. Ragweed was planted in botanical gardens in France in the 1700s, and quickly spread to nearby fields. It has since spread through Europe, to Russia and parts of Asia and Australia.
Genton, et al. (2005), conducted intercontinental reciprocal transplant experiments in four common gardens, to examine the likelihood of evolutionary changes that might improve defence or vigour. They collected seeds from plants in Ontario and South Carolina, and plants from the Rhone-Alpes region of France. They collected seeds from at least ten plants in each site. The seeds were germinated in greenhouses in France and Toronto. The seedlings were then transplanted to four experimental fields, one in Ontario (63 plants), and three locations in France (totaling 191 plants). Size, flowering status, and herbivore damage were recorded for each plant over four weeks. All invertebrate herbivores were collected and identified.
They state that, "surveys of natural enemy damage revealed that natural populations in Canada suffered more damage than those in France. Canadian populations were far more attacked by herbivores than were (the invasive) French populations, whereas no differences were found for pathogen damage. Chewing and perforation were by far the most common forms of damage observed in Canada, greatly exceeding any other type of damage at any location. These types of damage as well as leaf mines were much more common in Canada than in France, while frequencies of other types of damage (scraping, discolouration and white rust) were not significantly different between the two continents. Populations varied for all measures of damage." "A limited variety of insects, mostly aphids and grasshoppers, were found on the plants at the French sites, whereas, at the Canadian site, (they) recorded the presence of many herbivores known to attack ragweed."
Genton, et al. (2005), found that, "As with natural populations, experimental plants suffered far less herbivore damage in France than in Ontario. This difference in herbivory translated into increased growth but not into increased size or vigour. Moreover, (they) found that native genotypes were as damaged as invading ones in all experimental sites, suggesting no evolutionary loss of defence against herbivores."
Improved outcomes over time
Siemann, Rogers, & Dewalt, 2006, carried out a study of long-term changes in the genotype of the Chinese tallow tree, Sapium sebiferum. A native of China and other Asian countries, it is considered invasive in the southeastern USA. This species has been present in various locations in the USA from 100-233 years. In 2003, they grew tallow tree seedlings from seeds collected in its native range (Asia), sites in Georgia (introduced 1772), Florida (approximately 1865), Louisiana (approximately 1900), and Texas (approximately 1900). Genetic analysis suggests that tallow trees in Georgia came from different Asian ecotypes than in the other states.
They planted the seedlings in common gardens that included seedlings of native sweetgum and hackberry trees. They compared the performance of the seedlings for two growing seasons, collecting data on survival, height growth rates and plant size. They conducted short-term insect herbivory bioassays with the seedlings to compare potential herbivore pressure in the various states.
Average survival time for tallow seedings was longer than for the native species. But this varied by genotype. "Tallow trees had a substantial advantage compared to natives in terms of growth rate only in the two locations where it has been more recently introduced" (Texas and Louisiana). But "tallow tree had a lower growth rate than natives in the two locations where it had been present for a longer period of time" (Georgia and Florida).
"Results of herbivory bioassays indicated that pest accumulation likely plays a role in this reversal of tallow tree and native performance in at least the Georgia site." In the bioassays, "tallow tree seedlings suffered less chewing damage on average than did native trees seedlings but damage was higher for tallow trees than for natives in Georgia."
"Both native species had faster growth rates in Georgia and Florida than tallow tree seedlings did and tallow tree seedlings had faster height growth rates in Louisiana and Texas than either native species did... The strong pattern of higher damage on tallow tree seedlings than native seedlings in Georgia held for tallow tree and each native species."
Siemann, Rogers, & Dewalt state that these results indicate "a complex interaction of native herbivores and introduced plants in which low levels of herbivory at first may promote invasion success but then accumulation of herbivores over a period of centuries eventually equalizes invasive and native plant performance."
References:
Next Sections on the research on the success of invasive species:
Enemy Release Hypothesis (ERH): Its role in the Success or Failure 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, updated November 2024.
Do invasive species succeed in the new environment because of some traits that are inherent in the species when they arrive in the new habitat, or do they develop/evolve new or enhanced competitive advantages within the new environment?
Research in support of the hypothesis
A number of researchers have posed that plant and animal species become invasive due to the lack of natural predators in their new habitat. When placed in a new environment, the plant or animal species is ‘released’ from its natural enemies, and thus can thrive. Ridenour, Vivanco, Feng, Horiuchi, and Callaway (2008) note that the enemy release hypothesis is based on the idea that “exotic [plant] invaders explode in abundance because they are no longer suppressed by the specialist herbivore consumers they evolved with in their natural environments” (Also see Callaway & Ridenour, 2004).
Ziska and Runion (2007, p. 264) point out that invasive plants have a number of biological similarities that help explain why they become problems. Plants become problems in agriculture because of their superior “colonization of disturbed environments, vigorous growth, prodigious seed production, and seed longevity.” In addition, some invasives are able to spread vegetatively, in other words, without seed production. Non-crop species become a problem if they can successfully compete with crop species.
The Enemy Release hypothesis is based on the following: Plants have a limited amount of energy resources (in the form of carbohydrates) to devote to (1) growth, (2) reproduction, and (3) defense from herbivore predation. Because there are no natural herbivore predators in the new ecological community, Blossey and Nötzold, 1995, proposed that introduced plant species do not have to waste resources defending against predators. Thus, they can redirect resources to growth and reproduction. This would, over time, result in the “evolution of increased competitive ability” (EICA). If this hypothesis is correct, this increased competitive ability could be a major factor in the plant’s success within the new habitat.
Treharne, 1989, found that non-native plants that become invasive have a greater genetic diversity and therefore greater physiological plasticity when compared with many crops. Schierenbeck, et al., 1994, found that invasive plant genotypes can be larger or more reproductive than the same species in its native habitat.
Research that challenges the hypothesis
Research in support of the Enemy Release hypothesis, or the IECA hypothesis, has shown mixed results, and has mainly focused on growth and reproduction and studies of direct defense mechanisms (e.g., mechanical defenses, such as spines and thorns, or biochemical defenses, such as alkaloids, lignins, flavonoids, and tannins). Some studies (Joshi and Vrieling, 2005; Ridenour, et al., 2008) have shown that some invasive plant species have a higher level of chemical defenses in the introduced habitat than in their native habitat, which is the opposite of what one would expect if the IECA hypothesis is correct. Both Centaurea maculosa and Senecio jacobaea appear to have a competitive advantage because they expend more resources on defense in the introduced habitat than in their native habitats.
Parker, Burkepile, & Hay (March 6, 2006) conducted a meta-analysis of 63 field studies that involved experiments in herbivore exclusion. Overall, these studies examined the impact of herbivore removal on more than 100 exotic plant species. 35 of these studies monitored herbivore effects on entire plant communities. They reviewed an additional 28 studies that monitored herbivore effects on specific species of exotic plants. Many diverse environments and many diverse herbivores (from cattle to bison, elk, deer, antelope, waterfowl, rabbits, rodents, fishes, insects, etc.) were included among these studies.
They concluded that enemy release hypothesis fails to explain invasive species success. For example, it does not take into account the fact that the vast majority of non-native plant species brought into the USA do NOT become invasive. They also challenged the effectiveness of biocontrol herbivores. For example, insects who are the natural predators of invasive species have been brought into the USA because it has been believed that they are the best predators to control invasive species. Rather, Parker, et al. concluded that generalist herbivores native to the USA are significantly more effective at controlling invasive species, than are the herbivores from the home environment. This makes sense if you consider that, in their native environment, plants that become invasive in the USA are NOT eliminated by the herbivores that naturally prey upon them at home. Rather, an ecological balance is reached between predator and prey in the home environment.
The meta-analysis revealed that "native herbivores strongly suppressed, whereas exotic herbivores strongly enhanced, the relative abundance of exotic plants... Overall, the relative abundance of exotic plants was 52% higher in communities grazed by exotic herbivores.. than in communities grazed by native herbivores." In addition, "exotic herbivores suppressed the abundance of native plants." They also found that, "Native vertebrate herbivores had a three- to five-fold larger impact on exotic plant survival than did native invertebrate herbivores."
Parker, et al., 2006, propose the biotic resistance hypothesis as a better answer to the problem than enemy release. Natural habitats, composed of many native plant species, are naturally resistant to invasive plant species. It is only when humans remove native species, to replace them with a crop or in grazing or other land use, that invasive species emerge as a problem.
Parker & Gilbert (2007) (not the same Parker) also found that invasive species of clover were more strongly suppressed by herbivores native to the US than by exotic herbivores. And native clover species did not differ from nonnative clovers in the degree of damage caused by exotic herbivores. In contrast to the biotic resistance hypothesis, they found that native plants were not preferentially preyed upon by exotic herbivores. For more detail, refer to the section within this website: Insects as Biocontrol.
Liu, et al. (2007), compared herbivore damage on native Eugenia, introduced invasive Eugenia, and introduced non-invasive Eugenia species in South Florida. Both of the introduced species had less herbivore damage than the native species. But the two introduced species did not differ from each other in herbivore damage.
Dawson, et al. (2014), conducted a multi-species experiment, comparing the response to pesticides of native plants, introduced invasive plants, and introduced non-invasive plants. They found that all plants gained more biomass when treated with pesticides. "However, invasive, non-invasive and native species did not differ in their biomass response to pesticide treatment... The proportion of leaves damaged on invasive species was significantly lower compared to native species, but not when compared to non-invasive species. However, the difference was lost when plant size was accounted for. There were no differences between invasive, non-invasive and native species in herbivore abundance."
Research with mixed results
Zhang, et al. (2018), found evidence both for and against Enemy Release theory. They conducted "a meta-analysis of 61 common garden studies that provide data on resistance and/or tolerance for both introduced and native populations on 32 invasive plant species." They found that "introduced populations, relative to native populations, decreased their resistance against specialists, and increased their resistance against generalists. These differances were significant when resistance was measured in terms of damage caused by the herbivore, but not in terms of performance of that herbivore." In addition, they found that "magnitude of resistance differences between introduced and native populations depended significantly on herbivore origin (i.e.,whether the test herbivore was collected from the native or non-native range of the invasive plant). Finally, tolerance to generalists was found to be higher in introduced populations, while neither tolerance to specialists nor that to simulated herbivory differed between introduced and native plant populations." They conclude that "enemy release from specialist herbivores and biotic resistance from generalist herbivores has contrasting effects on resistance evolution in invasive plants." They believe that these results "provide strong support for the Shifting Defense hypothesis."
Enemy release may only provide part of the answer
Dostál, et al. (2013), examined differences in herbivore and fungal damage on native and exotic plant species in the Czech Republic. Three community characteristics, "habitat fertility, relatedness to the native community and native species diversity, can influence the accumulation of enemies and thus potentially their impact on exotic species. However, these factors have usually been studied in isolation...and their relative importance in influencing enemy accumulation on exotic species remains unclear."
In the first part of their study, Dostál, et al., "scored all above-ground, visible, damage morphotypes (groups based on similar types of damage) caused by herbivores, along with the presence of fungal pathogens, in 72 populations of 12 exotic species invasive to Central Europe. [They] also estimated levels of leaf herbivory and fruit damage."
The study sites "included 12 exotic species represented by 72 populations in total (at least five populations per exotic species. All 12 species are naturalized in the Czech Republic, and 10 of them are considered invasive... In the second part of this study, where [they] tested the ERH and R-ERH hypotheses, [they] included nine exotic species and eight native congeneric species...; exotic species Conyza canadensis (also Erigeron canadense) and Erigeron annuus shared the same native congener Erigeron acer]. Exotic species were represented by 28 populations that were also included in the first part of the study, but here [they] used only those that co-occurred with populations of native congeners....All study populations contained at least 100 individuals per species and were located in central and north-west Bohemia... Some sites had populations of more than one exotic species or of more than one congeneric pair."
They discovered nine types of damage or enemies: powdery mildew, rust fungi, herbivory by mammals, phloem feeding aphids, insect leaf herbivory, leaf mining by larval insects, pre-dispersal fruit damage by insects, stem boring by insects, and stem scraping, likely by molluscs. Between 2008 and 2009, they scored 3920 plant individuals.
Dostál, et al. (2013), found that, "Damage diversity and damage levels on exotic populations increased with habitat fertility... Standing biomass was the most important variable that positively influenced mean damage diversity and mean proportion of leaf herbivory... Ellenberg indicator values for nutrients and moisture were the best predictors of cumulative damage diversity and mean proportion of damaged fruits."
"The other two predictor groups – relatedness and community diversity – were less important but they influenced the presence of damaged fruits and herbivory... Specifically, the presence of closely related native species in the community significantly increased the probability of fruit attack... Herbivory was less likely in communities with a high phylogenetic diversity... However, phylogenetic diversity was an important predictor (in terms of AIC weight) only when inverse relatedness metrics were fitted in the models."
The enemy release hypothesis (ERH) predicts that enemy load on exotic plants is smaller than on native competitors. The resource-enemy release hypothesis (R-ERH) predicts that that relationship is most pronounced in resource-rich habitats. In the second part of their study, Dostál, et al., "tested the ERH and the R-ERH by comparing damage of plants in 28 pairs of co-occurring native and exotic populations, representing nine congeneric pairs of native and exotic species."
"The R-ERH predicts that the difference between native and exotic species in enemy load should increase along a productivity gradient. For the ERH/R-ERH test, [Dostál, et al.] thus included the nine congeneric pairs of exotic and native species occurring in habitats that differed considerably in productivity, as expressed by standing biomass. Whereas some grew in resource-poor sites, such as road verges or scree slopes, with mean habitat productivities of 123 g/m 2 or 154 g/m 2 (the Matricaria pair and the Sedum pair, respectively), the Bidens congeneric pair was confined to very fertile sites: fish pond banks with a productivity of 655 g m of 655 g/m 2."
They found that "plants in fertile habitats had on average more damage morphotypes than those from less fertile habitats... Native and exotic congeners, however, experienced similar levels of mean damage and damage diversity... The mean proportion of damaged fruits was lower in exotic species, but this difference was not statistically significant ... The overall analysis indicated that damage diversity and damage levels were similar for congeneric pairs from unproductive and from productive habitats. However, when [they] regressed the difference between the native and exotic species, in mean and cumulative damage diversity, against productivity, [they] found significantly negative relationships for both variables... This indicates that exotic species tended to have lower damage diversity than native species in unproductive habitats but that the opposite was true in productive habitats. The R-ERH predicts the opposite pattern"....[These] results therefore suggest that the relationship between herbivory and productivity is similar for native and exotic species, although [they] could not definitely identify the mechanism behind this."
Dostál, et al.,"found higher rates of fruit damage on exotics growing with more closely related natives, which suggests that oligophagous herbivores (those that eat few specific types of food) were also likely to play a role in the case of pre-dispersal fruit damage."
"The enemy release hypothesis, which assumes that exotic species leave behind more enemies in their native range than they accumulate in the novel range..., has been a very influential concept in invasion biology. However, here [Dostál, et al.,] found no differences in damage diversity and levels between exotic and native congeners growing in the same communities. Even species introduced as recently as 50 years ago...had similar levels of damage as their native relatives, despite the fact that enemy accumulation by exotic species is assumed to be a slow process... Invasive populations in fertile habitats also had similar levels of damage diversity to their native counterparts, which does not support the R-ERH... and instead suggests that exotic species can be exposed to similar levels of damage as co-occurring native species, irrespective of the habitat productivity."
Genton, et al. (2005), compared the success of ragweed, Ambrosia artemisiifolia, in its native range in Canada and the USA, with its success in its introduced range in France. Ragweed is native to North America, but has expanded its range there dramatically due to human disturbance of other natural habitats. It causes serious illness in allergy and asthma sufferers in the fall. Ragweed was planted in botanical gardens in France in the 1700s, and quickly spread to nearby fields. It has since spread through Europe, to Russia and parts of Asia and Australia.
Genton, et al. (2005), conducted intercontinental reciprocal transplant experiments in four common gardens, to examine the likelihood of evolutionary changes that might improve defence or vigour. They collected seeds from plants in Ontario and South Carolina, and plants from the Rhone-Alpes region of France. They collected seeds from at least ten plants in each site. The seeds were germinated in greenhouses in France and Toronto. The seedlings were then transplanted to four experimental fields, one in Ontario (63 plants), and three locations in France (totaling 191 plants). Size, flowering status, and herbivore damage were recorded for each plant over four weeks. All invertebrate herbivores were collected and identified.
They state that, "surveys of natural enemy damage revealed that natural populations in Canada suffered more damage than those in France. Canadian populations were far more attacked by herbivores than were (the invasive) French populations, whereas no differences were found for pathogen damage. Chewing and perforation were by far the most common forms of damage observed in Canada, greatly exceeding any other type of damage at any location. These types of damage as well as leaf mines were much more common in Canada than in France, while frequencies of other types of damage (scraping, discolouration and white rust) were not significantly different between the two continents. Populations varied for all measures of damage." "A limited variety of insects, mostly aphids and grasshoppers, were found on the plants at the French sites, whereas, at the Canadian site, (they) recorded the presence of many herbivores known to attack ragweed."
Genton, et al. (2005), found that, "As with natural populations, experimental plants suffered far less herbivore damage in France than in Ontario. This difference in herbivory translated into increased growth but not into increased size or vigour. Moreover, (they) found that native genotypes were as damaged as invading ones in all experimental sites, suggesting no evolutionary loss of defence against herbivores."
Improved outcomes over time
Siemann, Rogers, & Dewalt, 2006, carried out a study of long-term changes in the genotype of the Chinese tallow tree, Sapium sebiferum. A native of China and other Asian countries, it is considered invasive in the southeastern USA. This species has been present in various locations in the USA from 100-233 years. In 2003, they grew tallow tree seedlings from seeds collected in its native range (Asia), sites in Georgia (introduced 1772), Florida (approximately 1865), Louisiana (approximately 1900), and Texas (approximately 1900). Genetic analysis suggests that tallow trees in Georgia came from different Asian ecotypes than in the other states.
They planted the seedlings in common gardens that included seedlings of native sweetgum and hackberry trees. They compared the performance of the seedlings for two growing seasons, collecting data on survival, height growth rates and plant size. They conducted short-term insect herbivory bioassays with the seedlings to compare potential herbivore pressure in the various states.
Average survival time for tallow seedings was longer than for the native species. But this varied by genotype. "Tallow trees had a substantial advantage compared to natives in terms of growth rate only in the two locations where it has been more recently introduced" (Texas and Louisiana). But "tallow tree had a lower growth rate than natives in the two locations where it had been present for a longer period of time" (Georgia and Florida).
"Results of herbivory bioassays indicated that pest accumulation likely plays a role in this reversal of tallow tree and native performance in at least the Georgia site." In the bioassays, "tallow tree seedlings suffered less chewing damage on average than did native trees seedlings but damage was higher for tallow trees than for natives in Georgia."
"Both native species had faster growth rates in Georgia and Florida than tallow tree seedlings did and tallow tree seedlings had faster height growth rates in Louisiana and Texas than either native species did... The strong pattern of higher damage on tallow tree seedlings than native seedlings in Georgia held for tallow tree and each native species."
Siemann, Rogers, & Dewalt state that these results indicate "a complex interaction of native herbivores and introduced plants in which low levels of herbivory at first may promote invasion success but then accumulation of herbivores over a period of centuries eventually equalizes invasive and native plant performance."
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