Belowground Enemies Research Articles

Does introduced European Phragmites australis experience belowground microbial enemy release in North America?

AbstractEscape from native range enemies can give invasive species a competitive edge according to the enemy‐release hypothesis. While more commonly associated with predators and herbivores, release from belowground microbial antagonists has been recently demonstrated to benefit invasive plants. Biogeographic variation in dominance and comparisons of soil communities suggest that invasive European Phragmites australis may have also benefitted from belowground enemy release in North America (NA). Here we examine the effects of native range (Europe) versus introduced range (NA) soil communities on European and North American P. australis using a reciprocal inoculation seedling growth experiment. Contrary to the enemy‐release hypothesis, we found that North American P. australis was sensitive to soil community origin in that the seedlings grown in European soil communities had higher total biomass than seedlings grown in North American soil communities. This pattern was not observed in the European P. australis seedlings which had similar biomass when grown with North American or European soil communities. Notably, North American P. australis had higher biomass than European P. australis regardless of which soil community it was grown in, suggesting a growth–defense tradeoff. Though the relative abundance of mutualists and pathogens composition did not differ between the two ranges, an indicator analysis revealed that mutualistic fungi and bacteria were key components of European soil communities but not in North American communities. Interestingly, North American soil communities had lower β diversity than European communities suggesting higher levels of community conservation among North American populations. This research represents the first evidence of growth–defense trade‐offs in North American P. australis and offers a novel mechanism in understanding the invasion of P. australis in NA.

Soil Biota in a Nonnative Range has a Net Positive Effect on the Perennial Herb Lupinus polyphyllus

Invasive species can have detrimental effects on the health of local ecosystems. Lupinus polyphyllus is an herb native to western and northeast North America, but the species has become invasive worldwide. In northeastern Ohio, United States, the species is nonnative, but not invasive and not spreading rapidly. Because physical distance is not a barrier, there are other reasons behind the inability of the species to become locally invasive. Here, the net effect of the local soil biota on the range expansion of the species was tested to explore 2 alternative, non-mutually exclusive, hypotheses. First, if belowground enemies limit this species range, thenet effect of the soil biota would be negative. Alternatively, soil mutualists might have a relatively greater net effect on plant fitness. A greenhouse experiment was conducted with 3 populations of seeds from the invasive range across 2 experimental treatments: a general fungicide (ZeroTol®) treatment and a water-control treatment. Fungicide treatment reduced total biomass in 2 out of 3 populations, consistent with limitations by the abundance of belowground mutualists. Fungicide treatment also changed root structure by reducing the number of nodules, root length, and diameter, while increasing root tissue density. Although the fungicidetreatment hindered the growth of lupines overall, the changes in root structure indicate that the treated individuals were able to partially compensate by shifting to more of an outsourcing method of resource acquisition. The results suggest that in addition to belowground mutualistic interactions, phenotypic plasticity and intraspecific genetic variation may also contribute to the success of L. polyphyllus in its nonnative ranges.

Plant population and soil origin effects on rhizosphere nematode community composition of a range-expanding plant species and a native congener

Climate change causes species range expansions to higher latitudes and altitudes. It is expected that, due to differences in dispersal abilities between plants and soil biota, range-expanding plant species will become associated with a partly new belowground community in their expanded range. Theory on biological invasions predicts that outside their native range, range-expanding plant species may be released from specialist natural enemies, leading to the evolution of enhanced defence against generalist enemies. Here we tested the hypothesis that expanded range populations of the range-expanding plant species Centaurea stoebe accumulate fewer root-feeding nematodes than populations from the original range. Moreover, we examined whether Centaurea stoebe accumulates fewer root-feeding nematodes in expanded range soil than in original range soil. We grew plants from three expanded range and three original range populations of C. stoebe in soil from the original and from the new range. We compared nematode communities of C. stoebe with those of C. jacea, a congeneric species native to both ranges. Our results show that expanded range populations of C. stoebe did not accumulate fewer root-feeding nematodes than populations from the original range, but that C. stoebe, unlike C. jacea, accumulated fewest root-feeding nematodes in expanded range soil. Moreover, when we examined other nematode feeding groups, we found intra-specific plant population effects on all these groups. We conclude that range-expanding plant populations from the expanded range were not better defended against root-feeding nematodes than populations from the original range, but that C. stoebe might experience partial belowground enemy release.

Release from below- and aboveground natural enemies contributes to invasion success of a temperate invader

Efforts to concurrently test for enemy release of both above- and belowground enemies for invasive plants in non-native range are limited. Moreover, direct evidence for the causal link between enemy release and performance is rare for invasive plants. Thus, we sought to investigate if above- and/or belowground enemies are involved in the enemy release mechanisms at various life stages of a temperate invader and their consequences on plant community properties. We conducted field surveys of enemy damage and plant performance, and plant-soil feedback experiments in the glasshouses using Ambrosia trifida in both its non-native and native ranges across the seed, seedling, and adult life stages. Field surveys showed that seeds of A. trifida were more severely damaged by aboveground enemies in the native relative to the non-native range, while the difference in leaf damage between ranges was small. Plant-soil feedback experiments showed that release from belowground enemies was also important, as seed germination and plant growth were significantly reduced in soils from the native range compared with soils from the non-native range. Consistent with the above results, A. trifida was larger, produced more seeds, had higher density, and exerted stronger impacts on co-occurring native plants in the non-native relative to the native range. Our results demonstrated that release from both above- and belowground enemies at various life stages contributed to the invasion success of A. trifida in its non-native range and highlighted the importance of considering both above- and belowground enemy release when studying plant invasions.

Relatedness with plant species in native community influences ecological consequences of range expansions

Global warming is enabling many plant species to expand their range to higher latitudes and altitudes, where they may suffer less from natural aboveground and belowground enemies. Reduced control by natural enemies can enable climate warming‐induced range expanders to gain an advantage in competition with natives and become disproportionally abundant in their new range. However, so far studies have only examined individual growth of range expanders, which have common congeneric plant species in their new range. Thus it is not known how general is this reduced effect of above‐ and belowground enemies and how it operates in communities, where multiple plant species also interact with each other. Here we show that range‐expanding plant species with and without congenerics in the invaded habitats differ in their ecological interactions in the new range. In a community‐level experiment, range‐expanding plant species, both with and without congenerics, suppressed the growth of a herbivore. However, only range expanders without congenerics reduced biomass production of the native plant species. In the present study, range expanders without congenerics allocated more biomass aboveground compared to native plant species, which can explain their competitive advantage. Competitive interaction and also biomass allocation of native plants and their congeneric range expanders were similar. Our results highlight that information about species phylogenetic relatedness with native flora can be crucial for improving predictions about the consequences of climate warming‐induced range expansions.

Biogeographic differences in soil biota promote invasive grass response to nutrient addition relative to co-occurring species despite lack of belowground enemy release.

Multiple plant species invasions and increases in nutrient availability are pervasive drivers of global environmental change that often co-occur. Many plant invasion studies, however, focus on single-species or single-mechanism invasions, risking an oversimplification of a multifaceted process. Here, we test how biogeographic differences in soil biota, such as belowground enemy release, interact with increases in nutrient availability to influence invasive plant growth. We conducted a greenhouse experiment using three co-occurring invasive grasses and one native grass. We grew species in live and sterilized soil from the invader's native (United Kingdom) and introduced (New Zealand) ranges with a nutrient addition treatment. We found no evidence for belowground enemy release. However, species' responses to nutrients varied, and this depended on soil origin and sterilization. In live soil from the introduced range, the invasive species Lolium perenne L. responded more positively to nutrient addition than co-occurring invasive and native species. In contrast, in live soil from the native range and in sterilized soils, there were no differences in species' responses to nutrients. This suggests that the presence of soil biota from the introduced range allowed L. perenne to capture additional nutrients better than co-occurring species. Considering the globally widespread nature of anthropogenic nutrient additions to ecosystems, this effect could be contributing to a global homogenization of flora and the associated losses in native species diversity.

Comparative impacts of aboveground and belowground enemies on an invasive thistle.

Most research examining how herbivores and pathogens affect performance of invasive plants focuses on aboveground interactions. Although important, the role of belowground communities remains poorly understood, and the relative impact of aboveground and belowground interactions is still debated. As well, most studies of belowground interactions have been carried out in controlled environments, so little is known about the role of these interactions under natural conditions or how these relationships may change across a plant's range. Using the invasive plant Cirsium arvense, we performed a reciprocal transplant experiment to test the relative impacts of above‐ and belowground interactions at three sites across a 509‐km latitudinal gradient in its invaded range in Ontario, Canada. At each site, C. arvense seedlings were protected with above‐ and/or belowground exclosures in a factorial design. Plant performance (biomass, height, stem thickness, number of leaves, length of longest leaf, maximum rhizome length) was greatest when both above‐ and belowground exclosures were applied and lowest when no exclosures were applied. When only one type of exclosure was applied, biomass generally improved more with belowground exclosures than with aboveground exclosures. Despite site‐to‐site differences in foliar damage, root damage, and mesofaunal populations, belowground interactions generally had a greater negative impact on performance than aboveground herbivory alone. These results stress the importance of including both aboveground enemy interactions and plant–soil interactions in studies of plant community dynamics and invader performance.

Phylogeny Explains Variation in The Root Chemistry of Eucalyptus Species.

Plants are dependent on their root systems for survival, and thus are defended from belowground enemies by a range of strategies, including plant secondary metabolites (PSMs). These compounds vary among species, and an understanding of this variation may provide generality in predicting the susceptibility of forest trees to belowground enemies and the quality of their organic matter input to soil. Here, we investigated phylogenetic patterns in the root chemistry of species within the genus Eucalyptus. Given the known diversity of PSMs in eucalypt foliage, we hypothesized that (i) the range and concentrations of PSMs and carbohydrates in roots vary among Eucalyptus species, and (ii) that phylogenetic relationships explain a significant component of this variation. To test for interspecific variation in root chemistry and the influence of tree phylogeny, we grew 24 Eucalyptus species representing two subgenera (Eucalyptus and Symphyomyrtus) in a common garden for two years. Fine root samples were collected from each species and analyzed for total phenolics, condensed tannins, carbohydrates, terpenes, and formylated phloroglucinol compounds. Compounds displaying significant interspecific variation were mapped onto a molecular phylogeny and tested for phylogenetic signal. Although all targeted groups of compounds were present, we found that phenolics dominated root defenses and that all phenolic traits displayed significant interspecific variation. Further, these compounds displayed a significant phylogenetic signal. Overall, our results suggest that within these representatives of genus Eucalyptus, more closely related species have more similar root chemistry, which may influence their susceptibility to belowground enemies and soil organic matter accrual.

Release from belowground enemies and shifts in root traits as interrelated drivers of alien plant invasion success: a hypothesis.

Our understanding of the interrelated mechanisms driving plant invasions, such as the interplay between enemy release and resource-acquisition traits, is biased by an aboveground perspective. To address this bias, I hypothesize that plant release from belowground enemies (especially fungal pathogens) will give invasive plant species a fitness advantage in the alien range, via shifts in root traits (e.g., increased specific root length and branching intensity) that increase resource uptake and competitive ability compared to native species in the alien range, and compared to plants of the invader in its native range. Such root-trait changes could be ecological or evolutionary in nature. I explain how shifts in root traits could occur as a consequence of enemy release and contribute to invasion success of alien plants, and how they could be interrelated with other potential belowground drivers of invasion success (allelopathy, mutualist enhancement). Finally, I outline the approaches that could be taken to test whether belowground enemy release results in increased competitive ability and nutrient uptake by invasive alien plants, via changes in root traits in the alien range.

Top-down control of root-feeding nematodes in range-expanding and congeneric native plant species

Climate warming may result in range expansion of species towards previously colder environments, and it has been demonstrated that in the new range successfully range-expanding plant species can be less attacked by aboveground and belowground enemies than congeneric natives. Plant enemies may be controlled naturally by complex bottom-up and top-down interactions with their hosts, however, little is known about how these interactions may operate in the new range. Here, we examine how root-feeding nematodes are controlled in the root zone of successfully range-expanding plant species in comparison with congeneric plant species native to the new range. As range-expanding plant species can have less negative soil feedback than congeneric natives, we tested the hypothesis that top-down control of root-feeding nematodes may be strongest on range-expanding plant species. To test this, we grew four pairs of range-expanding plant species and their native congeners in field soil, to which we added soil microbes, nematodes, or microarthropods from the new habitat. Addition of soil microorganisms and microarthropods reduced the numbers of root-feeding nematodes, being strongest when microorganisms were added. Opposite to our expectation, nematode control was not more effective in the root zone of range-expanding than native plant species. We conclude that top-down control of root-feeding nematodes is highly plant species-specific and that top-down control of these nematodes in the root zone of range-expanding plant species can be as effective as in the root zone of congeneric natives.

Increased compensatory ability of an invasive plant to above- and below-ground enemies in monocultures

Above- and below-ground enemies have prominent influence on plant invasions, and increasing evidence has shown that plant invasions are also affected by inter- or intraspecific interactions between individual plants. However, how these two factors interactively affect plant invasions has rarely been tested. Here, we examined the response of the invasive plant Alternanthera philoxeroides (Mart.) Griseb. to above- and below-ground enemies at varying plant densities in a greenhouse experiment in Wuhan, China. We found that both above- and below-ground enemies decreased the plant total and root mass at individual and population levels, but that of the two, below-ground enemies had a greater effect than above-ground enemies, and that the two guilds of enemies acted additively on the plant. However, their impacts decreased as the plant density increased, due to enhanced plant tolerance to both guilds of enemies. The increased plant tolerance may result from changes in plant resource allocation patterns, corresponding to a positive linear relationship between the ratio of fine root mass to total root mass and plant density. Given that forming dense monocultures in their new ranges is one of the most important characteristics of invasive plants, we propose that the high compensatory ability at dense monocultures may be an important mechanism underlying exotic species invasion.

Additive effects of aboveground polyphagous herbivores and soil feedback in native and range‐expanding exotic plants

Plant biomass and plant abundance can be controlled by aboveground and belowground natural enemies. However, little is known about how the aboveground and belowground enemy effects may add up. We exposed 15 plant species to aboveground polyphagous insect herbivores and feedback effects from the soil community alone, as well as in combination. We envisaged three possibilities: additive, synergistic, or antagonistic effects of the aboveground and belowground enemies on plant biomass. In our analysis, we included native and phylogenetically related range-expanding exotic plant species, because exotic plants on average are less sensitive to aboveground herbivores and soil feedback than related natives. Thus, we examined if lower sensitivity of exotic plant species to enemies also alters aboveground-belowground interactions. In a greenhouse experiment, we exposed six exotic and nine native plant species to feedback from their own soil communities, aboveground herbivory by polyphagous insects, or a combination of soil feedback and aboveground insects and compared shoot and root biomass to control plants without aboveground and belowground enemies. We observed that for both native and range-expanding exotic plant species effects of insect herbivory aboveground and soil feedback added up linearly, instead of enforcing or counteracting each other. However, there was no correlation between the strength of aboveground herbivory and soil feedback. We conclude that effects of polyphagous aboveground herbivorous insects and soil feedback add up both in the case of native and related range-expanding exotic plant species, but that aboveground herbivory effects may not necessarily predict the strengths of soil feedback effects.

Range-expanding populations of a globally introduced weed experience negative plant-soil feedbacks.

BackgroundBiological invasions are fundamentally biogeographic processes that occur over large spatial scales. Interactions with soil microbes can have strong impacts on plant invasions, but how these interactions vary among areas where introduced species are highly invasive vs. naturalized is still unknown. In this study, we examined biogeographic variation in plant-soil microbe interactions of a globally invasive weed, Centaurea solstitialis (yellow starthistle). We addressed the following questions (1) Is Centaurea released from natural enemy pressure from soil microbes in introduced regions? and (2) Is variation in plant-soil feedbacks associated with variation in Centaurea's invasive success?Methodology/Principal FindingsWe conducted greenhouse experiments using soils and seeds collected from native Eurasian populations and introduced populations spanning North and South America where Centaurea is highly invasive and noninvasive. Soil microbes had pervasive negative effects in all regions, although the magnitude of their effect varied among regions. These patterns were not unequivocally congruent with the enemy release hypothesis. Surprisingly, we also found that Centaurea generated strong negative feedbacks in regions where it is the most invasive, while it generated neutral plant-soil feedbacks where it is noninvasive.Conclusions/SignificanceRecent studies have found reduced below-ground enemy attack and more positive plant-soil feedbacks in range-expanding plant populations, but we found increased negative effects of soil microbes in range-expanding Centaurea populations. While such negative feedbacks may limit the long-term persistence of invasive plants, such feedbacks may also contribute to the success of invasions, either by having disproportionately negative impacts on competing species, or by yielding relatively better growth in uncolonized areas that would encourage lateral spread. Enemy release from soil-borne pathogens is not sufficient to explain the success of this weed in such different regions. The biogeographic variation in soil-microbe effects indicates that different mechanisms may operate on this species in different regions, thus establishing geographic mosaics of species interactions that contribute to variation in invasion success.

Climate change and invasion by intracontinental range-expanding exotic plants: the role of biotic interactions.

In this Botanical Briefing we describe how the interactions between plants and their biotic environment can change during range-expansion within a continent and how this may influence plant invasiveness. We address how mechanisms explaining intercontinental plant invasions by exotics (such as release from enemies) may also apply to climate-warming-induced range-expanding exotics within the same continent. We focus on above-ground and below-ground interactions of plants, enemies and symbionts, on plant defences, and on nutrient cycling. Range-expansion by plants may result in above-ground and below-ground enemy release. This enemy release can be due to the higher dispersal capacity of plants than of natural enemies. Moreover, lower-latitudinal plants can have higher defence levels than plants from temperate regions, making them better defended against herbivory. In a world that contains fewer enemies, exotic plants will experience less selection pressure to maintain high levels of defensive secondary metabolites. Range-expanders potentially affect ecosystem processes, such as nutrient cycling. These features are quite comparable with what is known of intercontinental invasive exotic plants. However, intracontinental range-expanding plants will have ongoing gene-flow between the newly established populations and the populations in the native range. This is a major difference from intercontinental invasive exotic plants, which become more severely disconnected from their source populations.

Successful range-expanding plants experience less above-ground and below-ground enemy impact

Many species are currently moving to higher latitudes and altitudes. However, little is known about the factors that influence the future performance of range-expanding species in their new habitats. Here we show that range-expanding plant species from a riverine area were better defended against shoot and root enemies than were related native plant species growing in the same area. We grew fifteen plant species with and without non-coevolved polyphagous locusts and cosmopolitan, polyphagous aphids. Contrary to our expectations, the locusts performed more poorly on the range-expanding plant species than on the congeneric native plant species, whereas the aphids showed no difference. The shoot herbivores reduced the biomass of the native plants more than they did that of the congeneric range expanders. Also, the range-expanding plants developed fewer pathogenic effects in their root-zone soil than did the related native species. Current predictions forecast biodiversity loss due to limitations in the ability of species to adjust to climate warming conditions in their range. Our results strongly suggest that the plants that shift ranges towards higher latitudes and altitudes may include potential invaders, as the successful range expanders may experience less control by above-ground or below-ground enemies than the natives.

Local escape of an invasive plant, common ragweed (Ambrosia artemisiifolia L.), from above‐ground and below‐ground enemies in its native area

Summary 1. The Enemy Release Hypothesis proposes that exotic species gain an advantage in new regions because their natural enemies are lost during invasion; however, enemy release could also occur as a result of much smaller scale movements within an invasive plant’s native range, i.e. if it escapes enemies while colonizing new sites. Few studies have considered this possibility, and none has compared escape from multiple guilds of enemies. 2. We studied an invasive North American weed, Ambrosia artemisiifolia (common ragweed), to determine whether it escapes above-ground or below-ground enemies at a local scale in its native range. Exotic populations of this plant are known to have escaped above-ground enemies in Europe. 3. Experimental populations of ragweed isolated from existing populations by just 100 m experienced reduced levels of damage by invertebrate folivores and seed predators; however, there was no clear evidence that this escape led to improved performance. 4. Plants inoculated with unsterilized soil grew better than plants in sterile soil, likely reflecting a need for mycorrhizal colonization. Inoculum from ragweed populations was as beneficial as inoculum from nearby ragweed-free sites, suggesting only a small initial role for site-specific pathogens. 5. Performance declined over time when plants were serially inoculated with non-sterile soil, indicating negative feedback with the soil biota. This feedback was stronger for inocula derived from ragweed populations vs. those from nearby ragweed-free sites. 6. Seeds buried in ragweed populations were less likely to germinate subsequently than seeds buried in nearby ragweed-free sites. This difference was not reduced by treatment with fungicide; consequently, the mechanism is unclear. 7. Synthesis . These results indicate that ragweed can escape both above-ground and below-ground enemies by dispersing to new sites, resulting in reduced levels of folivory, seed predation, soil feedback and perhaps losses to seed pathogens. Although consequences often may be small, this demonstrates that enemy release can occur for native as well as exotic populations of this species, linking possible mechanisms of local spread with long-distance invasion.

Invasive plants and their escape from root herbivory: a worldwide comparison of the root-feeding nematode communities of the dune grass Ammophila arenaria in natural and introduced ranges

Invasive plants generally have fewer aboveground pathogens and viruses in their introduced range than in their natural range, and they also have fewer pathogens than do similar plant species native to the introduced range. However, although plant abundance is strongly controlled by root herbivores and soil pathogens, there is very little knowledge on how invasive plants escape from belowground enemies. We therefore investigated if the general pattern for aboveground pathogens also applies to root-feeding nematodes and used the natural foredune grass Ammophila arenariaas a model. In the late 1800s, the European A. arenariawas introduced into southeast Australia (Tasmania), New Zealand, South Africa, and the west coast of the USA to be used for sand stabilization. In most of these regions, it has become a threat to native vegetation, because its excessive capacity to stabilize wind-blown sand has changed the geomorphology of coastal dunes. In stable dunes of most introduced regions, A. arenaria is more abundant and persists longer than in stabilized dunes of the natural range. We collected soil and root samples and used additional literature data to quantify the taxon richness of root-feeding nematodes on A.␣arenaria in its natural range and collected samples from the four major regions where it has been introduced. In most introduced regions A. arenaria did not have fewer root-feeding nematode taxa than the average number in its natural range, and native plant species did not have more nematode taxa than the introduced species. However, in the introduced range native plants had more feeding-specialist nematode taxa than A. arenaria and major feeding specialists (the sedentary endoparasitic cyst and root knot nematodes) were not found on A. arenaria in the southern hemisphere. We conclude that invasiveness of A. arenaria correlates with escape from feeding specialist nematodes, so that the pattern of escape from root-feeding nematodes is more alike escape from aboveground insect herbivores than escape from aboveground pathogens and viruses. In the natural range of A. arenaria, the number of specialist-feeding nematode taxa declines towards the margins. Growth experiments are needed to determine the relationship between nematode taxon diversity, abundance, and invasiveness of A. arenaria.