Soil pathogen communities associated with native and non‐native Phragmites australis populations in freshwater wetlands

Soil pathogens are believed to be major contributors to negative plant–soil feedbacks that regulate plant community dynamics and plant invasions. While the theoretical basis for pathogen regulation of plant communities is well established within the plant–soil feedback framework, direct experimental evidence for pathogen community responses to plants has been limited, often relying largely on indirect evidence based on above‐ground plant responses. As a result, specific soil pathogen responses accompanying above‐ground plant community dynamics are largely unknown. Here, we examine the oomycete pathogens in soils conditioned by established populations of native noninvasive and non‐native invasive haplotypes of Phragmites australis (European common reed). Our aim was to assess whether populations of invasive plants harbor unique communities of pathogens that differ from those associated with noninvasive populations and whether the distribution of taxa within these communities may help to explain invasive success. We compared the composition and abundance of pathogenic and saprobic oomycete species over a 2‐year period. Despite a diversity of oomycete taxa detected in soils from both native and non‐native populations, pathogen communities from both invaded and noninvaded soils were dominated by species of Pythium. Pathogen species that contributed the most to the differences observed between invaded and noninvaded soils were distributed between invaded and noninvaded soils. However, the specific taxa in invaded soils responsible for community differences were distinct from those in noninvaded soils that contributed to community differences. Our results indicate that, despite the phylogenetic relatedness of native and non‐native P. australis haplotypes, pathogen communities associated with the dominant non‐native haplotype are distinct from those of the rare native haplotype. Pathogen taxa that dominate either noninvaded or invaded soils suggest different potential mechanisms of invasion facilitation. These findings are consistent with the hypothesis that non‐native plant species that dominate landscapes may “cultivate” a different soil pathogen community to their rhizosphere than those of rarer native species.     

Virulence of oomycete pathogens from Phragmites australis‐invaded and noninvaded soils to seedlings of wetland plant species

Soil pathogens affect plant community structure and function through negative plant–soil feedbacks that may contribute to the invasiveness of non‐native plant species. Our understanding of these pathogen‐induced soil feedbacks has relied largely on observations of the collective impact of the soil biota on plant populations, with few observations of accompanying changes in populations of specific soil pathogens and their impacts on invasive and noninvasive species. As a result, the roles of specific soil pathogens in plant invasions remain unknown. In this study, we examine the diversity and virulence of soil oomycete pathogens in freshwater wetland soils invaded by non‐native Phragmites australis (European common reed) to better understand the potential for soil pathogen communities to impact a range of native and non‐native species and influence invasiveness. We isolated oomycetes from four sites over a 2‐year period, collecting nearly 500 isolates belonging to 36 different species. These sites were dominated by species of Pythium, many of which decreased seedling survival of a range of native and invasive plants. Despite any clear host specialization, many of the Pythium species were differentially virulent to the native and non‐native plant species tested. Isolates from invaded and noninvaded soils were equally virulent to given individual plant species, and no apparent differences in susceptibility were observed between the collective groups of native and non‐native plant species.     

Bacterial phytopathogen infection disrupts belowground plant indirect defense mediated by tritrophic cascade

Plants can defend themselves against herbivores through activation of defensive pathways and attraction of third‐trophic‐level predators and parasites. Trophic cascades that mediate interactions in the phytobiome are part of a larger dynamic including the pathogens of the plant itself, which are known to greatly influence plant defenses. As such, we investigated the impact of a phloem‐limited bacterial pathogen, Candidatus Liberibacter asiaticus (CLas), in cultivated citrus rootstock on a well‐studied belowground tritrophic interaction involving the attraction of an entomopathogenic nematode (EPN), Steinernema diaprepesi, to their root‐feeding insect hosts, Diaprepes abbreviatus larvae. Using belowground olfactometers, we show how CLas infection interferes with this belowground interaction by similarly inducing the release of a C12 terpene, pregeijerene, and disconnecting the association of the terpene with insect presence. D. abbreviatus larvae that were not feeding but in the presence of a CLas‐infected plant were more likely to be infected by EPN than those near uninfected plants. Furthermore, nonfeeding larvae associated with CLas‐infected plants were just as likely to be infected by EPN as those near noninfected plants with D. abbreviatus larval damage. Larvae of two weevil species, D. abbreviatus and Pachnaeus litus, were also more attracted to plants with infection than to uninfected plants. D. abbreviatus larvae were most active when exposed to pregeijerene at a concentration of 0.1 μg/μl. We attribute this attraction to CLas‐infected plants to the same signal previously thought to be a herbivore‐induced plant volatile specifically induced by root‐feeding insects, pregeijerene, by assessing volatiles collected from the roots of infected plants and uninfected plants with and without feeding D. abbreviatus. Synthesis. Phytopathogens can influence the structuring of soil communities extending to the third trophic level. Field populations of EPN may be less effective at host‐finding using pregeijerene as a cue in citrus grove agroecosystems with high presence of CLas infection.     

Inhibitory effects of Eucalyptus globulus on understorey plant growth and species richness are greater in non‐native regions

Aim

We studied the novel weapons hypothesis in the context of the broadly distributed tree species Eucalyptus globulus. We evaluated the hypothesis that this Australian species would produce stronger inhibitory effects on species from its non‐native range than on species from its native range.

Location

We worked in four countries where this species is exotic (U.S.A., Chile, India, Portugal) and one country where it is native (Australia).

Time period

2009–2012.

Major taxa studied

Plants.

Methods

We compared species composition, richness and height of plant communities in 20 paired plots underneath E. globulus individuals and open areas in two sites within its native range and each non‐native region. We also compared effects of litter leachates of E. globulus on root growth of seedlings in species from Australia, Chile, the U.S.A. and India.

Results

In all sites and countries, the plant community under E. globulus canopies had lower species richness than did the plant community in open areas. However, the reduction was much greater in the non‐native ranges: species richness declined by an average of 51% in the eight non‐native sites versus 8% in the two native Australian sites. The root growth of 15 out of 21 species from the non‐native range were highly suppressed by E. globulus litter leachates, whereas the effect of litter leachate varied from facilitation to suppression for six species native to Australia. The mean reduction in root growth for Australian plants was significantly lower than for plants from the U.S.A., Chile and India.

Main conclusions

Our results show biogeographical differences in the impact of an exotic species on understorey plant communities. Consistent with the novel weapons hypothesis, our findings suggest that different adaptations of species from the native and non‐native ranges to biochemical compounds produced by an exotic species may play a role in these biogeographical differences.     

Effect of plant root symbionts on performance of native woody species in competition with an invasive grass in multispecies microcosms

The majority of terrestrial plants form mutualistic associations with arbuscular mycorrhizal fungi (AMF) and rhizobia (i.e., nitrogen‐fixing bacteria). Understanding these associations has important implications for ecological theory and for restoration practice. Here, we tested whether the presence of AMF and rhizobia influences the performance of native woody plants invaded by a non‐native grass in experimental microcosms. We planted eight plant species (i.e., Acacia acuminata, A. microbotrya, Eucalyptus loxophleba subsp. loxophleba, E. astringens, Calothamnus quadrifidus, Callistemon phoeniceus, Hakea lissocarpha and H. prostrata) in microcosms of field‐conditioned soil with and without addition of AMF and rhizobia in a fully factorial experimental design. After seedling establishment, we seeded half the microcosms with an invasive grass Bromus diandrus. We measured shoot and root biomass of native plants and Bromus, and on roots, the percentage colonization by AMF, number of rhizobia‐forming nodules and number of proteaceous root clusters. We found no effect of plant root symbionts or Bromus addition on performance of myrtaceous, and as predicted, proteaceous species as they rely little or not at all on AMF and rhizobia. Soil treatments with AMF and rhizobia had a strong positive effect (i.e., larger biomass) on native legumes (A. microbotrya and A. acuminata). However, the beneficial effect of root symbionts on legumes became negative (i.e., lower biomass and less nodules) if Bromus was present, especially for one legume, i.e., A. acuminata, suggesting a disruptive effect of the invader on the mutualism. We also found a stimulating effect of Bromus on root nodule production in A. microbotrya and AMF colonization in A. acuminata which could be indicative of legumes’ increased resource acquisition requirement, i.e., for nitrogen and phosphorus, respectively, in response to the Bromus addition. We have demonstrated the importance of measuring belowground effects because the aboveground effects gave limited indication of the effects occurring belowground.     

Soil legacy effects of plants and drought on aboveground insects in native and range-expanding plant communities

Soils contain biotic and abiotic legacies of previous conditions that may influence plant community biomass and associated aboveground biodiversity. However, little is known about the relative strengths and interactions of the various belowground legacies on aboveground plant–insect interactions. We used an outdoor mesocosm experiment to investigate the belowground legacy effects of range-expanding versus native plants, extreme drought and their interactions on plants, aphids and pollinators. We show that plant biomass was influenced more strongly by the previous plant community than by the previous summer drought. Plant communities consisted of four congeneric pairs of natives and range expanders, and their responses were not unanimous. Legacy effects affected the abundance of aphids more strongly than pollinators. We conclude that legacies can be contained as soil ‘memories’ that influence aboveground plant community interactions in the next growing season. These soil-borne ‘memories’ can be altered by climate warming-induced plant range shifts and extreme drought.     

Root volatiles in plant–plant interactions II: Root volatiles alter root chemistry and plant–herbivore interactions of neighbouring plants

Volatile organic compounds (VOCs) emitted by plant roots can influence the germination and growth of neighbouring plants. However, little is known about the effects of root VOCs on plant–herbivore interactions of neighbouring plants. The spotted knapweed (Centaurea stoebe) constitutively releases high amounts of sesquiterpenes into the rhizosphere. Here, we examine the impact of C. stoebe root VOCs on the primary and secondary metabolites of sympatric Taraxacum officinale plants and the resulting plant‐mediated effects on a generalist root herbivore, the white grub Melolontha melolontha. We show that exposure of T. officinale to C.stoebe root VOCs does not affect the accumulation of defensive secondary metabolites but modulates carbohydrate and total protein levels in T. officinale roots. Furthermore, VOC exposure increases M. melolontha growth on T. officinale plants. Exposure of T. officinale to a major C. stoebe root VOC, the sesquiterpene (E)‐β‐caryophyllene, partially mimics the effect of the full root VOC blend on M. melolontha growth. Thus, releasing root VOCs can modify plant–herbivore interactions of neighbouring plants. The release of VOCs to increase the susceptibility of other plants may be a form of plant offense.     

Ingestion by an endemic frugivore enhances seed germination of endemic plant species but decreases seedling survival of exotics

Aim To test whether ingestion by endemic frugivores differentially affects the seed germination time, germination percentage and seedling survival of endemic, native and exotic fleshy fruited plant species, and to identify the principal processes and attributes driving such effects. Location Round Island, Mauritius. Methods We conducted a germination and seedling survival experiment for 3 months to test whether ingestion (gut passage and deposition in faeces) by the endemic Telfair’s skink (Leiolopisma telfairii) had a differential effect on the germination time, germination percentage and seedling survival of two endemic, four native and two exotic fleshy fruited plant species. To assess the importance of factors involved in the ingestion process, we used a factorial design with gut passage (gut‐passed vs. not gut‐passed), depulping (whole fruit vs. manually depulped seed) and the presence of faecal material (faeces vs. without faeces). In addition, the roles of species‐specific traits, seed size and deposition density (average number of seeds per faeces) were examined. Results Exotic species had a higher germination percentage than indigenous (native and endemic) species when not ingested. Following skink ingestion, there was no longer a difference, as ingestion enhanced germination percentage most in endemic species. The exotic species still germinated faster overall than the indigenous species, despite ingestion accelerating the germination time of endemics. However, ingestion strongly reduced seedling survival of the exotic species, while having no negative effect on the survival of indigenous seedlings. Overall, ingested indigenous seeds were more likely to germinate and the seedlings more likely to survive than ingested exotic seeds and seedlings. Seed size, deposition density and the removal of fruit pulp by either manual depulping or gut passage were important predictors of germination time, germination percentage and seedling survival. Main conclusions These endemic frugivores can enhance the competitiveness of endemic compared with exotic fleshy fruited plants at the critical germination and seedling establishment stage. Consequently, conservation and restoration of mutualistic endemic plant–animal interactions may be vital to mitigating the degradation of habitats invaded by exotic plants, which is of particular relevance for island ecosystems in which large numbers of endemics are threatened by exotic invaders.     

Direct effects of warming increase woody plant abundance in a subarctic wetland

Both the direct effects of warming on a species’ vital rates and indirect effects of warming caused by interactions with neighboring species can influence plant populations. Furthermore, herbivory mediates the effects of warming on plant community composition in many systems. Thus, determining the importance of direct and indirect effects of warming, while considering the role of herbivory, can help predict long‐term plant community dynamics. We conducted a field experiment in the coastal wetlands of western Alaska to investigate how warming and herbivory influence the interactions and abundances of two common plant species, a sedge, Carex ramenskii, and a dwarf shrub, Salix ovalifolia. We used results from the experiment to model the equilibrium abundances of the species under different warming and grazing scenarios and to determine the contribution of direct and indirect effects to predict population changes. Consistent with the current composition of the landscape, model predictions suggest that Carex is more abundant than Salix under ambient temperatures with grazing (53% and 27% cover, respectively). However, with warming and grazing, Salix becomes more abundant than Carex (57% and 41% cover, respectively), reflecting both a negative response of Carex and a positive response of Salix to warming. While grazing reduced the cover of both species, herbivory did not prevent a shift in dominance from sedges to the dwarf shrub. Direct effects of climate change explained about 97% of the total predicted change in species cover, whereas indirect effects explained only 3% of the predicted change. Thus, indirect effects, mediated by interactions between Carex and Salix, were negligible, likely due to use of different niches and weak interspecific interactions. Results suggest that a 2°C increase could cause a shift in dominance from sedges to woody plants on the coast of western Alaska over decadal timescales, and this shift was largely a result of the direct effects of warming. Models predict this shift with or without goose herbivory. Our results are consistent with other studies showing an increase in woody plant abundance in the Arctic and suggest that shifts in plant–plant interactions are not driving this change.     

Aboveground competition influences density‐dependent effects of cordgrass on sediment biogeochemistry

Interspecific interactions between plants influence plant phenotype, distribution, abundance, and community structure. Each of these can, in turn, impact sediment biogeochemistry. Although the population and community level impacts of these interactions have been extensively studied, less is known about their effect on sediment biogeochemistry. This is surprising given that many plants are categorized as foundation species that exert strong control on community structure. In southern California salt marshes, we used clipping experiments to manipulate aboveground neighbor presence to study interactions between two dominant plants, Pacific cordgrass (Spartina foliosa) and perennial pickleweed (Sarcocornia pacifica). We also measured how changes in cordgrass stem density influenced sediment biogeochemistry. Pickleweed suppressed cordgrass stem density but had no effect on aboveground biomass. For every cordgrass stem lost per square meter, porewater ammonium increased 0.3–1.0 µM. Thus, aboveground competition with pickleweed weakened the effects of cordgrass on sediment biogeochemistry. Predictions about plant–soil feedbacks, especially under future climate scenarios, will be improved when plant–plant interactions are considered, particularly those containing dominant and foundation species.     

Responses of a native beetle to novel exotic plant species with varying invasion history

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Smells from the desert: Microbial volatiles that affect plant growth and development of native and non‐native plant species

The plant microbiota can affect host fitness via the emission of microbial volatile organic compounds (mVOCs) that influence growth and development. However, evidence of these molecules and their effects in plants from arid ecosystems is limited. We screened the mVOCs produced by 40 core and representative members of the microbiome of agaves and cacti in their interaction with Arabidopsis thaliana and Nicotiana benthamiana. We used SPME‐GC‐MS to characterize the chemical diversity of mVOCs and tested the effects of selected compounds on growth and development of model and host plants. Our study revealed that approximately 90% of the bacterial strains promoted plant growth both in A. thaliana and N. benthamiana. Bacterial VOCs were mainly composed of esters, alcohols, and S‐containing compounds with 25% of them not previously characterized. Remarkably, ethyl isovalerate, isoamyl acetate, 3‐methyl‐1‐butanol, benzyl alcohol, 2‐phenylethyl alcohol, and 3‐(methylthio)‐1‐propanol, and some of their mixtures, displayed beneficial effects in A. thaliana and also improved growth and development of Agave tequilana and Agave salmiana in just 60 days. Volatiles produced by bacteria isolated from agaves and cacti are promising molecules for the sustainable production of crops in arid and semi‐arid regions.     

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.     

Litter mixture effects on tropical tree seedling growth--a greenhouse experiment

Decomposing litter provides critical nutrients for plants, particularly in nutrient-poor ecosystems such as tropical forests. We hypothesised that decomposing litter improves the performance of a variety of tropical tree seedlings, and that this litter effect varies depending on the species of litter present in litter mixtures. We addressed these hypotheses with a large pot experiment manipulating a range of different litter mixtures of contrasting quality and using seedlings of four tree species from the Amazonian forest of French Guiana. In contrast to our initial hypothesis, decomposing litter had either neutral or negative impacts on seedling growth, despite strongly different growth rates, biomass allocation patterns and leaf and root traits among tree species. Tree species varied in their responses to litter additions, which were further modified by species identity of the added litter. Our data show litter species-specific effects on growth, biomass allocation and leaf and root traits of tropical tree seedlings. These results suggest that a net nutrient release from decomposing litter does not necessarily improve tree seedling growth, even under nutrient-limiting conditions. In conclusion, litter layer composition may affect seedling establishment and recruitment success beyond litter-derived plant nutrient availability, which may contribute to tree species composition and dynamics in the studied tropical forest.     

Influence of presence and spatial arrangement of belowground insects on host‐plant selection of aboveground insects: a field study

Abstract 1. Several studies have shown that above‐ and belowground insects can interact by influencing each others growth, development, and survival when they feed on the same host‐plant. In natural systems, however, insects can make choices on which plants to oviposit and feed. A field experiment was carried out to determine if root‐feeding insects can influence feeding and oviposition preferences and decisions of naturally colonising foliar‐feeding insects. 2. Using the wild cruciferous plant Brassica nigra and larvae of the cabbage root fly Delia radicum as the belowground root‐feeding insect, naturally colonising populations of foliar‐feeding insects were monitored over the course of a summer season. 3. Groups of root‐infested and root‐uninfested B. nigra plants were placed in a meadow during June, July, and August of 2006 for periods of 3 days. The root‐infested and the root‐uninfested plants were either dispersed evenly or placed in clusters. Once daily, all leaves of each plant were carefully inspected and insects were removed and collected for identification. 4. The flea beetles Phyllotreta spp. and the aphid Brevicoryne brassicae were significantly more abundant on root‐uninfested (control) than on root‐infested plants. However, for B. brassicae this was only apparent when the plants were placed in clusters. Host‐plant selection by the generalist aphid M. persicae and oviposition preference by the specialist butterfly P. rapae, however, were not significantly influenced by root herbivory. 5. The results of this study show that the presence of root‐feeding insects can affect feeding and oviposition preferences of foliar‐feeding insects, even under natural conditions where many other interactions occur simultaneously. The results suggest that root‐feeding insects play a role in the structuring of aboveground communities of insects, but these effects depend on the insect species as well as on the spatial distribution of the root‐feeding insects.     

Microbial phylotype composition and diversity predicts plant productivity and plant–soil feedbacks

The relationship between ecological variation and microbial genetic composition is critical to understanding microbial influence on community and ecosystem function. In glasshouse trials using nine native legume species and 40 rhizobial strains, we find that bacterial rRNA phylotype accounts for 68% of amoung isolate variability in symbiotic effectiveness and 79% of host specificity in growth response. We also find that rhizobial phylotype diversity and composition of soils collected from a geographical breadth of sites explains the growth responses of two acacia species. Positive soil microbial feedback between the two acacia hosts was largely driven by changes in diversity of rhizobia. Greater rhizobial diversity accumulated in association with the less responsive host species, Acacia salicina, and negatively affected the growth of the more responsive Acacia stenophylla. Together, this work demonstrates correspondence of phylotype with microbial function, and demonstrates that the dynamics of rhizobia on host species can feed back on plant population performance.