Ectomycorrhizal fungi associated with ponderosa pine and Douglas-fir: a comparison of species richness in native western North American forests and Patagonian plantations from Argentina

The putative ectomycorrhizal fungal species registered from sporocarps associated with ponderosa pine and Douglas-fir forests in their natural range distribution (i.e., western Canada, USA, and Mexico) and from plantations in south Argentina and other parts of the world are listed. One hundred and fifty seven taxa are reported for native ponderosa pine forests and 514 taxa for native Douglas-fir forests based on available literature and databases. A small group of genera comprises a high proportion of the species richness for native Douglas-fir (i.e., Cortinarius, Inocybe, and Russula), whereas in native ponderosa pine, the species richness is more evenly distributed among several genera. The comparison between ectomycorrhizal species richness associated with both trees in native forests and in Patagonia (Argentina) shows far fewer species in the latter, with 18 taxa for the ponderosa pine and 15 for the Douglas-fir. Epigeous species richness is clearly dominant in native Douglas-fir, whereas a more balanced relation epigeous/hypogeous richness is observed for native ponderosa pine; a similar trend was observed for Patagonian plantations. Most fungi in Patagonian Douglas-fir plantations have not been recorded in plantations elsewhere, except Suillus lakei and Thelephora terrestris, and only 56% of the fungal taxa recorded in Douglas-fir plantations around the world are known from native forests, the other taxa being new associations for this host, suggesting that new tree + ectomycorrhizal fungal taxa associations are favored in artificial situations as plantations.     

Biological invasions increase the richness of arbuscular mycorrhizal fungi from a Hawaiian subtropical ecosystem

Biological invasions can have various impacts on the diversity of important microbial mutualists such as mycorrhizal fungi, but few studies have tested whether the effects of invasions on mycorrhizal diversity are consistent across spatial gradients. Furthermore, few of these studies have taken place in tropical ecosystems that experience an inordinate rate of invasions into native habitats. Here, we examined the effects of plant invasions dominated by non-native tree species on the diversity of arbuscular mycorrhizal (AM) fungi in Hawaii. To test the hypothesis that invasions result in consistent changes in AM fungal diversity across spatial gradients relative to native forest habitats, we sampled soil in paired native and invaded sites from three watersheds and used amplicon sequencing to characterize AM fungal communities. Whether our analyses considered phylogenetic relatedness or not, we found that invasions consistently increased the richness of AM fungi. However, AM fungal species composition was not related to invasion status of the vegetation nor local environment, but stratified by watershed. Our results suggest that while invasions can lead to an overall increase in the diversity of microbial mutualists, the effects of plant host identity or geographic structuring potentially outweigh those of invasive species in determining the community membership of AM fungi. Thus, host specificity and spatial factors such as dispersal need to be taken into consideration when examining the effects of biological invasions on symbiotic microbes.     

Ectomycorrhizal fungi of exotic pine plantations in relation to native host trees in Iran: evidence of host range expansion by local symbionts to distantly related host taxa

Introduction of exotic plants change soil microbial communities which may have detrimental ecological consequences for ecosystems. In this study, we examined the community structure and species richness of ectomycorrhizal (EcM) fungi associated with exotic pine plantations in relation to adjacent native ectomycorrhizal trees in Iran to elucidate the symbiont exchange between distantly related hosts, i.e. Fagales (Fagaceae and Betulaceae) and Pinaceae. The combination of morphological and molecular identification approaches revealed that 84.6 % of species with more than one occurrence (at least once on pines) were shared with native trees and only 5.9 % were found exclusively on pine root tips. The community diversity of ectomycorrhizal fungi in the pine plantations adjacent to native EcM trees was comparable to their adjacent native trees, but the isolated plantations hosted relatively a species-poor community. Specific mycobionts of conifers were dominant in the isolated plantation while rarely found in the plantations adjacent to native EcM trees. These data demonstrate the importance of habitat isolation and dispersal limitation of EcM fungi in their potential of host range expansion. The great number of shared and possibly compatible symbiotic species between exotic Pinaceae and local Fagales (Fagaceae and Betulaceae) may reflect their evolutionary adaptations and/or ancestral compatibility with one another.     

Exotic Mammals Disperse Exotic Fungi That Promote Invasion by Exotic Trees

Biological invasions are often complex phenomena because many factors influence their outcome. One key aspect is how non-natives interact with the local biota. Interaction with local species may be especially important for exotic species that require an obligatory mutualist, such as Pinaceae species that need ectomycorrhizal (EM) fungi. EM fungi and seeds of Pinaceae disperse independently, so they may use different vectors. We studied the role of exotic mammals as dispersal agents of EM fungi on Isla Victoria, Argentina, where many Pinaceae species have been introduced. Only a few of these tree species have become invasive, and they are found in high densities only near plantations, partly because these Pinaceae trees lack proper EM fungi when their seeds land far from plantations. Native mammals (a dwarf deer and rodents) are rare around plantations and do not appear to play a role in these invasions. With greenhouse experiments using animal feces as inoculum, plus observational and molecular studies, we found that wild boar and deer, both non-native, are dispersing EM fungi. Approximately 30% of the Pinaceae seedlings growing with feces of wild boar and 15% of the seedlings growing with deer feces were colonized by non-native EM fungi. Seedlings growing in control pots were not colonized by EM fungi. We found a low diversity of fungi colonizing the seedlings, with the hypogeous Rhizopogon as the most abundant genus. Wild boar, a recent introduction to the island, appear to be the main animal dispersing the fungi and may be playing a key role in facilitating the invasion of pine trees and even triggering their spread. These results show that interactions among non-natives help explain pine invasions in our study area.     

Native and non-native mammals disperse exotic ectomycorrhizal fungi at long distances from pine plantations

We aimed to evaluate if exotic ectomycorrhizal fungi from exotic pine plantations disperse through non-native, but also native, mammals in a mountain ecosystem devoid of native ECM plants. Among four non-native and three native mammal species, feces of non-native wild boar (Sus scrofa) and brown hare (Lepus europaeus), and native pampa fox (Lycalopex gymnocercus) were selected to inoculate seedlings of Pinus elliottii. These feces came from two transects in an elevation gradient (1350–2250 m asl) and different distances from a pine plantation (100–6000 m). We show that feces of wild boar, brown hare (non-native), and pampa fox (native) were effective as inoculum for establishing ectomycorrhizal pine seedlings. Through molecular analyses, we determined that two species are mostly consumed and successfully form ectomycorrhizas with pine roots: Suillus granulatus and Rhizopogon pseudoroseolus. We provide novel evidence for the long-distance dispersal of exotic ectomycorrhizal fungi by non-native and native animal vectors.     

Spatial distribution of some alien plants across a restricted mountainous area

Plant invasion of natural ecosystems is one of the most serious ecological crises of our time. The invasive plants are one of the causes for native species decline and ecosystem degradation. This study tries to answer the question whether studied mountainous area is relatively free of plant invasions. We also try to provide a clue about the possible causes for the current invasion state of the studied territory. We used direct ordination, correlation and multiple regression techniques coupled with different statistical tests to describe the current invasion pattern of the studied vegetation. We found that the most invaded vegetation types are lowelevational mixed xerophilous and subxerophilous oak forests and pine plantations. The open subalpine communities are relatively uninvaded. Alien species richness is highest in the xeric habitats at low elevations and in the mesic ones at higher elevations. The common beech forests in the mesic habitats at low to middle elevations are almost completely free of invasion. The leading factors, driving invasion processes in the area are thought to be the anthropogenic and natural disturbances, placed in the context of main local environmental gradients like elevation, habitat moisture and slope inclination. Understanding the factors that drive mountain vegetation invasion helps us taking timely actions to prevent further degradation of precious natural habitats around the globe.     

Habitat matters: The role of spore bank fungi in early seedling establishment of Florida slash pines

This study investigated broad patterns in communities of ectomycorrhizal fungi from three Florida habitats (sandhills, scrub, and pine rocklands) and the ability of spore bank fungi to associate with Pinus elliottii (slash pine) and Pinus densa (south Florida slash pine). Efforts to replant pines in the endangered pine rocklands are vital to the persistence of this habitat, yet little is known about the ectomycorrhizal fungi communities or how they may differ from those in other pine-dominated habitats in Florida. We used high-throughput amplicon sequencing (HTS) to assess baseline fungal communities and greenhouse bioassays to bait ectomycorrhizal fungi using seedlings. HTS soil data recovered 188 ectomycorrhizal species but only a few subsequently colonized the bioassay seedlings. We recovered 21 ectomycorrhizal species on pine seedlings including common spore bank fungi such as Cenococcum, Suillus, and Tuber, but Rhizopogon species were dominant across all sites and habitats. Habitat type and site were significant variables influencing the community composition of the total soil fungal community, soil ectomycorrhizal community, and the fungi found on seedling root tips. However, we found no significant differences between the ectomycorrhizal communities on seedling roots from the two Pinus species.     

Pine invasion impacts on plant diversity in Patagonia: invader size and invaded habitat matter

Conifers, which are widely planted as fast growing tree crops, are invading forested and treeless environments across the globe, causing important changes in biodiversity. However, how small-scale impacts on plant diversity differ according to pine size and habitat context remains unclear. We assessed the effects of different stages of pine invasion on plant communities in forest and steppe sites located in southern Chile. In each site, we sampled plant diversity under and outside the canopy of Pinus contorta individuals, using paired plots. We assessed the relative impact of pine invasion on plant species richness and cover. In both sites, richness and cover beneath pine canopy decreased with increasing pine size (i.e. height and canopy area). A significant negative impact of pines on species richness and plant cover was detected for pines over 4 m in height. The impact of pines on plant richness and cover depended on pine size (i.e. canopy area) and habitat type. Larger pines had more negative impacts than smaller pines in both sites, with a greater impact for a given pine size in the Patagonian steppe compared to the A. araucaria forest. Species composition changed between under and outside canopy plots when pines were 4 m or taller. Pine presence reduced cover of most species. The impacts of pine invasions are becoming evident in forested and treeless ecosystems of southern Chile. Our results suggest that the magnitude of pine invasion impacts could be related to how adapted the invaded community is to tree cover, with the treeless environment more impacted by the invasion.     

Co-invading ectomycorrhizal fungal succession in pine-invaded mountain grasslands

Ectomycorrhizal (EM) fungal communities that associate with invading pines (Pinus spp.) are expected to be poor in species diversity. However, long-term successional trajectories and the persistence of dispersal limitations of EM fungi in the exotic range are not well understood. We sampled the roots and surrounding soil of Pinus elliottii and P. taeda trees invading mountain grasslands of Argentina. We also sampled the EM fungal spore bank in grassland soil near (∼150 m) and far (∼850 m) from the original pine plantations. We found 86 different co-invasive EM fungal OTUs. Differential dispersal capacities among EM fungi were detected in the spore bank of grassland soil, but not under mature pines. After thirty years of invasion, the age, but not the degree of spatial isolation of pine individuals affected the EM fungal composition. We showed how EM fungal succession occurs during pine invasions, which may have clear consequences for ecosystem functioning of co-invaded sites.     

In tallgrass prairie restorations,relatedness influences neighborhood-scale plant invasion while resource availability influences site-scale invasion

Attempting to control invasive plant species in tallgrass prairie restorations is time-consuming and costly, making improved approaches for predicting and reducing invasion imperative. Both biotic and abiotic factors mediate plant invasions, and can potentially be used by restoration managers to reduce invasion rates. Biotic factors such as plant species richness and phylogenetic diversity of the native community may impact invasion. Relatedness of invading species to those in recipient communities has also been shown to influence invasion success. However, the direction of this influence is variable, reflecting Darwin’s Naturalization Conundrum. Abiotic factors such as fire regime and soil factors may impact invasion by selecting against invasive species or indicating suitable habitats for them. We surveyed 17 tallgrass prairie restorations in Illinois, USA, to investigate the effects of biotic and abiotic factors on invasion by non-native plant species at two different scales. We predicted we would find support for Darwin’s Naturalization Hypothesis at the plot (neighborhood) scale with invasion by distantly related species, and find support for the Pre-adaptation Hypothesis at the site scale. We hypothesized that biotic factors would exert more influence at the neighborhood scale, while abiotic factors would be more influential at a coarser site scale. Contrary to our expectations, at the neighborhood scale we found that closely related invasive species are more likely to invade, supporting the Pre-adaptation Hypothesis. We found that native species richness and age of restoration were negatively correlated with invasion. At the site scale, soil organic matter [SOM] concentrations and heterogeneity in SOM were positively associated with the number of invasive species while pH heterogeneity was negatively associated. Restoration practitioners may be able to reduce plant invasions by increasing native species richness, and non-native species most closely related to the resident community should potentially be prioritized as those most likely to be highly invasive.     

Impacts of experimental warming and northern light climate on growth and root fungal communities of Scots pine populations

Global warming is driving plant range shifts towards higher latitudes, where plants encounter different light environment (photoperiod and light spectral quality) than that to which they are adapted. Light environment may indirectly influence the belowground part of the plant, where trees associate with ectomycorrhizal (ECM) and other biotrophic fungi. We studied joint impacts of warming and light climate on Scots pine (Pinus sylvestris) and its root-associated fungi in a reciprocal transplantation study, where pine seedlings from southern and northern tree populations were grown under similar experimental temperature in southern (60°N) and northern (69°N) Finland. Based on fungal ITS rDNA, the abundance of Basidiomycota, and ECM fungi in particular, was highest in the roots of southern pines in the south and in northern pines in the north, and seedling biomass was determined by population origin. Our results imply that root-associated fungi may respond differentially in native vs. non-native light environment of the host plant.     

Comparing the influences of ecological and evolutionary factors on the successful invasion of a fungal forest pathogen

The fungal forest pathogen Heterobasidion annosum has been introduced from North America into Italy and is now associated with high mortality of Italian stone pines. Due to the presence of a closely related native H. annosum taxon, this pathosystem presents an unusual opportunity to test specific ecological and evolutionary factors influencing fungal invasions. Comparative inoculation experiments on Scots pine cuttings and on seedlings of European and North American pines failed to identify significant increased pathogenicity of North American genotypes on European hosts congruent with lack of host-pathogen co-evolution. However, spore trappings indicate that while reproductive potential of native H. annosum was significantly reduced in the dry season, that of the invasive taxon was consistently high regardless of season. Ecological differences between the native and exotic taxon may therefore facilitate this invasion. Understanding which factors enhance this emerging forest disease is important both for biotic invasion theory and for disease control.     

Comparison of root-associated communities of native and non-native ectomycorrhizal hosts in an urban landscape

Non-native tree species are often used as ornamentals in urban landscapes. However, their root-associated fungal communities remain yet to be examined in detail. Here, we compared richness, diversity and community composition of ectomycorrhizosphere fungi in general and ectomycorrhizal (EcM) fungi in particular between a non-native Pinus nigra and a native Quercus macrocarpa across a growing season in urban parks using 454-pyrosequencing. Our data show that, while the ectomycorrhizosphere community richness and diversity did not differ between the two host, the EcM communities associated with the native host were often more species rich and included more exclusive members than those of the non-native hosts. In contrast, the ectomycorrhizosphere communities of the two hosts were compositionally clearly distinct in nonmetric multidimensional ordination analyses, whereas the EcM communities were only marginally so. Taken together, our data suggest EcM communities with broad host compatibilities and with a limited numbers of taxa with preference to the non-native host. Furthermore, many common fungi in the non-native Pinus were not EcM taxa, suggesting that the fungal communities of the non-native host may be enriched in non-mycorrhizal fungi at the cost of the EcM taxa. Finally, while our colonization estimates did not suggest a shortage in EcM inoculum for either host in urban parks, the differences in the fungi associated with the two hosts emphasize the importance of using native hosts in urban environments as a tool to conserve endemic fungal diversity and richness in man-made systems.     

Invasive ectomycorrhizal fungi can disperse in the absence of their known vectors

Positive interactions between non-native species can accelerate their invasion rate and exacerbate their impacts. This has been shown for non-native mammals that disperse invasive ectomycorrhizal fungi (EMF), in turn facilitating the invasion of non-native tree species. Mammal-mediated dispersion is assumed to be the main mechanism of EMF long distance dispersal, being particularly critical for truffle-like EMF species. We asked whether the absence of non-native mammals is an obstacle for Pinaceae invasion given the lack of invasive EMF being dispersed. We studied EMF species colonization and Pseudotsuga menziesii (Douglas-fir) trees’ growth in soil from mainland sites where non-native mammals are highly abundant, and lake islets in which they have been historically absent. Contrary to what we expected, we found invasive EMF, including truffle-like species, in sites where invasive mammals have been historically absent. Douglas-fir trees grew equally well and had the same EMF colonization in soil from mainland and islets. Alternative mechanisms of EMF dispersal, such as saltation, bird dispersal, or human dispersal, can be involved in their arrival to native stands. The presence of invasive EMF makes native sites vulnerable to Pinaceae invasion, even in the absence of mammalian dispersers.     

Impact of invasions by alien plants on soil seed bank communities: Emerging patterns

Much of our current understanding of the impact of invasive species on plant communities is based on patterns occurring in the above-ground vegetation, while only few studies have examined changes in soil seed banks associated with plant invasions, despite their important role as determinants of vegetation dynamics. Here, we reviewed the literature on the impact of plant invasions on the seed bank and we provide a quantitative synthesis using a meta-analysis approach. Specifically, (1) we quantified the impact of 18 invasive alien plants on (i) species richness and (ii) density of the seed banks of invaded communities, based on 58 pair-wise invaded-uninvaded comparisons (cases); we identified (2) the invasive taxa that are responsible for the largest changes in the seed bank; and (3) the habitats where substantial changes occur. Our study showed three major findings: (1) species richness (68% of cases) and density (58% of cases) were significantly lower in native seed banks invaded by alien plants; (2) species richness and density of native and alien species were remarkably lower in seed banks invaded by large, perennial herbs compared to uninvaded sites; and (3) invaded seed banks were often associated with a larger richness and/or abundance of alien species. This study indicates a need for additional seed bank data in invasion ecology to characterize species-specific and habitat-specific impacts of plant invasions, and to determine whether changes in the seed banks of native and alien species are a symptom of environmental degradation prior to a plant invasion or whether they are its direct result. The findings of this study help improve our capacity to predict the long-term implications of plant invasions, including limitations in the recruitment of native species from the seed bank and the potential for secondary invasions by seeds of other alien species.     

Fire as a driver of pine invasions in the Southern Hemisphere: a review

Contrasting evidence in the degree of post-fire conifer invasion reported for different regions of the Southern Hemisphere (SH) raises questions about the role of fire as a presumed driver of invasion. We studied the influence of fire on invasion responses (assessing ‘serotiny’ and ‘time’ as key factors to determine invasion) based on a review of case studies performed in natural habitats of the SH. Our work showed that burned environments have no lag time with respect to invasion and are more susceptible to serotinous pine invasion than are unburned environments. Also, serotinous pines reached extremely high densities in burned habitats, exceeding records for the same species in unburned habitats, as well as for non-serotinous pines in any habitat condition. Therefore, burned environments are impacted by conifer invasion earlier and more intensively than unburned ones. Overall, our work indicates that fire is a leading driver of invasion, but only for serotinous pines. This highlights the importance of considering life history traits of introduced species to determine the probability and extent of invasion in relation to disturbance. We discuss the implications of introducing serotinous species in regions of the SH where serotiny is absent from native flora. Lastly, we provide suggestions for prioritizing management and further study.     

Pine invasion decreases density and changes native tree communities in woodland Cerrado

ABSTRACT

Background: Invasive plants can negatively impact native communities, but the majority of the effects of these invasions have been demonstrated only for temperate ecosystems. Tropical ecosystems, including the Cerrado, a biodiversity hotspot, are known to be invaded by numerous non-native species, but studies of their impacts are largely lacking.

Aims: Our research aimed at quantifying how Pinus spp. presence and density affected Cerrado plant communities.

Methods: We sampled areas invaded and non-invaded by Pinus spp. to determine if pine invasion affected native tree richness, diversity, evenness, and density. We also evaluated if community composition differed between invaded and non-invaded sites.

Results: We found invaded plots had lower native tree densities than non-invaded plots and that Pinus spp. invasions changed native tree communities by reducing native species abundances.

Conclusion: Invasive pines had negative impacts on the native Cerrado tree community by reducing native plant density and changing species abundances. Reduced density and abundance at early invasion stages can result in reduction in biodiversity in the long term.     

Landscape characteristics of non‐native pine plantations and invasions in Southern Chile

The spread of non‐native conifers into areas naturally dominated by other vegetation types is a growing problem in South America. This process results in a landscape transformation as the conifers suppress native vegetation leading to reduced biodiversity, lower water availability and altered nutrient dynamics. Previous research highlights the broad spatial extents of land cover change in parts of Chile. However, in Southern Chile, the extent of plantations and the landscape characteristics associated with plantations and ongoing pine invasions are poorly understood. Here, we characterised non‐native pine land cover within one Landsat scene (World Reference System 2 Path 232/Row 92; ~34 000 km²) in Southern Chile. We created training data based on historical high‐resolution imagery, derived land cover predictors from time series of Landsat observations and used a Random Forest classifier to map the distribution of non‐native pines. The overall classification accuracy was 88%, and the accuracy of the non‐native pine class exceeded 90%. Although 71% of non‐native pine patches were within 500 m of other non‐native pine patches, isolated non‐native pine patches were found to occur up to 55 km from the nearest neighbour. These distant plantations could exacerbate invasion risk by creating propagule sources for novel invasion fronts. In relation to landscape characteristics, non‐native pines were found to be more likely to occur in low slope and mid‐elevation areas. Because most of the study area is native forest, most non‐native pine patches border native forest. However, non‐native pine patches were almost three times more likely than random patches to border grass/agriculture. This suggests that grasslands and disturbed sites, which have low resistance to non‐native pine invasion, are disproportionately exposed to pine propagules. Our results indicate that non‐native pine plantations are extensive across Southern Chile, and well poised to cause future invasion.     

Filling in the gaps: modelling native species richness and invasions using spatially incomplete data

Detailed knowledge of patterns of native species richness, an important component of biodiversity, and non-native species invasions is often lacking even though this knowledge is essential to conservation efforts. However, we cannot afford to wait for complete information on the distribution and abundance of native and harmful invasive species. Using information from counties well surveyed for plants across the USA, we developed models to fill data gaps in poorly surveyed areas by estimating the density (number of species km⁻²) of native and non-native plant species. Here, we show that native plant species density is non-random, predictable, and is the best predictor of non-native plant species density. We found that eastern agricultural sites and coastal areas are among the most invaded in terms of non-native plant species densities, and that the central USA appears to have the greatest ratio of non-native to native species. These large-scale models could also be applied to smaller spatial scales or other taxa to set priorities for conservation and invasion mitigation, prevention, and control efforts.     

Assessing the conservation value of a human-dominated island landscape: Plant diversity in Hawaii

The conversion of native habitats to pasture and other working lands, unbuilt lands modified by humans for production, is one of the greatest threats to biodiversity. While some human-dominated landscapes on continents support relatively high native biodiversity, this capacity is little studied in oceanic island systems characterized by high endemism and vulnerability to invasion. Using Hawaii as a case study, we assessed the conservation value of working landscapes on an oceanic island by surveying native and non-native plant diversity in mature native forest and in the three dominant land covers/uses to which it has been converted: native, Acacia koa timber plantations, wooded pasture, and open pasture. As expected, native plant diversity (richness and abundance) was significantly higher and non-native abundance significantly lower in mature native forests than any other site type. A. koa plantations and wooded pasture supported four and three times greater, respectively, species richness of native understory plants than open pasture. Also, A. koa plantations and wooded pasture supported similar species communities with about 75% species in common. Conservation and restoration of mature native forest in Hawaii is essential for the protection of native, rare species and limiting the spread of non-native species. A. koa plantations and wooded pasture, however, may help harmonize production and conservation by supporting livelihoods, more biodiversity than open pasture, and some connectivity between native forest remnants important for sustaining landscape-level conservation value into the future.