Abundance,origin, and phylogeny of plants do not predict community‐level patterns of pathogen diversity and infection

Pathogens have the potential to shape plant community structure, and thus, it is important to understand the factors that determine pathogen diversity and infection in communities. The abundance, origin, and evolutionary relationships of plant hosts are all known to influence pathogen patterns and are typically studied separately. We present an observational study that examined the influence of all three factors and their interactions on the diversity of and infection of several broad taxonomic groups of foliar, floral, and stem pathogens across three sites in a temperate grassland in the central United States. Despite that pathogens are known to respond positively to increases in their host abundances in other systems, we found no relationship between host abundance and either pathogen diversity or infection. Native and exotic plants did not differ in their infection levels, but exotic plants hosted a more generalist pathogen community compared to native plants. There was no phylogenetic signal across plants in pathogen diversity or infection. The lack of evidence for a role of abundance, origin, and evolutionary relationships in shaping patterns of pathogens in our study might be explained by the high generalization and global distributions of our focal pathogen community, as well as the high diversity of our plant host community. In general, the community‐level patterns of aboveground pathogen infections have received less attention than belowground pathogens, and our results suggest that their patterns might not be explained by the same drivers.     

Social immunity modulates competition between coinfecting pathogens

Coinfections with multiple pathogens can result in complex within‐host dynamics affecting virulence and transmission. While multiple infections are intensively studied in solitary hosts, it is so far unresolved how social host interactions interfere with pathogen competition, and if this depends on coinfection diversity. We studied how the collective disease defences of ants – their social immunity – influence pathogen competition in coinfections of same or different fungal pathogen species. Social immunity reduced virulence for all pathogen combinations, but interfered with spore production only in different‐species coinfections. Here, it decreased overall pathogen sporulation success while increasing co‐sporulation on individual cadavers and maintaining a higher pathogen diversity at the community level. Mathematical modelling revealed that host sanitary care alone can modulate competitive outcomes between pathogens, giving advantage to fast‐germinating, thus less grooming‐sensitive ones. Host social interactions can hence modulate infection dynamics in coinfected group members, thereby altering pathogen communities at the host level and population level.     

Root pathogen diversity and composition varies with climate in undisturbed grasslands,but less so in anthropogenically disturbed grasslands

Soil-borne pathogens structure plant communities, shaping their diversity, and through these effects may mediate plant responses to climate change and disturbance. Little is known, however, about the environmental determinants of plant pathogen communities. Therefore, we explored the impact of climate gradients and anthropogenic disturbance on root-associated pathogens in grasslands. We examined the community structure of two pathogenic groups—fungal pathogens and oomycetes—in undisturbed and anthropogenically disturbed grasslands across a natural precipitation and temperature gradient in the Midwestern USA. In undisturbed grasslands, precipitation and temperature gradients were important predictors of pathogen community richness and composition. Oomycete richness increased with precipitation, while fungal pathogen richness depended on an interaction of precipitation and temperature, with precipitation increasing richness most with higher temperatures. Disturbance altered plant pathogen composition and precipitation and temperature had a reduced effect on pathogen richness and composition in disturbed grasslands. Because pathogens can mediate plant community diversity and structure, the sensitivity of pathogens to disturbance and climate suggests that degradation of the pathogen community may mediate loss, or limit restoration of, native plant diversity in disturbed grasslands, and may modify plant community response to climate change.Subject terms: Fungal ecology, Soil microbiology, Grassland ecology     

Effects of elevated CO2, nitrogen deposition, and decreased species diversity on foliar fungal plant disease

Three components of global change, elevated CO₂, nitrogen addition, and decreased plant species richness (‘diversity’), increased the percent leaf area infected by fungi (pathogen load) for much to all of the plant community in one year of a factorial grassland experiment. Decreased plant diversity had the broadest effect, increasing pathogen load across the plant community. Decreased diversity increased pathogen load primarily by allowing remaining plant species to increase in abundance, facilitating spread of foliar fungal pathogens specific to each plant species. Changes in plant species composition also strongly influenced community pathogen load, with communities that lost less disease prone plant species increasing more in pathogen load. Elevated CO₂ increased pathogen load of C₃ grasses, perhaps by decreasing water stress, increasing leaf longevity, and increasing photosynthetic rate, all of which can promote foliar fungal disease. Decreased plant diversity further magnified the increase in C₃ grass pathogen load under elevated CO₂. Nitrogen addition increased pathogen load of C₄ grasses by increasing foliar nitrogen concentration, which can enhance pathogen infection, growth, and reproduction. Because changes in foliar fungal pathogen load can strongly influence grassland ecosystem processes, our study suggests that increased pathogen load can be an important mechanism by which global change affects grassland ecosystems.     

Divergent phenologies may facilitate the coexistence of arbuscular mycorrhizal fungi in a North Carolina grassland

Interest in the diversity of arbuscular mycorrhizal (AM) fungal communities has been stimulated by recent data that demonstrate that fungal communities influence the competitive hierarchies, productivity, diversity, and successional patterns of plant communities. Although natural communities of AM fungi are diverse, we have a poor understanding of the mechanisms that promote and maintain that diversity. Plants may coexist by inhabiting disparate temporal niches; plants of many grasslands are either warm or cool season specialists. We hypothesized that AM fungi might be similarly seasonal. To test our hypothesis, we tracked the sporulation of individual AM fungal species growing within a North Carolina grassland. Data were collected in 1996 and 1997; in 1997, sampling focused on two common species. We found that AM fungi, especially Acaulospora colossica and Gigaspora gigantea, maintained different and contrasting seasonalities. Acaulospora colossica sporulated more frequently in the warm season, but Gi. gigantea sporulated more frequently in the cool season. Moreover, AM fungal species were spatially aggregated at a fine scale. Contrasting seasonal and spatial niches may facilitate the maintenance of a diverse community of AM fungi. Furthermore, these data may illuminate our understanding of the AM fungal influence on plant communities: various fungal species may preferentially associate with different plant species and thereby promote diversity in the plant community.     

Erosion of community diversity and stability by herbivore removal under warming

Climate change has the potential to influence the persistence of ecological communities by altering their stability properties. One of the major drivers of community stability is species diversity, which is itself expected to be altered by climate change in many systems. The extent to which climatic effects on community stability may be buffered by the influence of species interactions on diversity is, however, poorly understood because of a paucity of studies incorporating interactions between abiotic and biotic factors. Here, I report results of a 10-year field experiment, the past 7 years of which have focused on effects of ongoing warming and herbivore removal on diversity and stability within the plant community, where competitive species interactions are mediated by exploitation through herbivory. Across the entire plant community, stability increased with diversity, but both stability and diversity were reduced by herbivore removal, warming and their interaction. Within the most species-rich functional group in the community, forbs, warming reduced species diversity, and both warming and herbivore removal reduced the strength of the relationship between diversity and stability. Species interactions, such as exploitation, may thus buffer communities against destabilizing influences of climate change, and intact populations of large herbivores, in particular, may prove important in maintaining and promoting plant community diversity and stability in a changing climate.     

Sick plants in grassland communities: a growth‐defense trade‐off is the main driver of fungal pathogen abundance

Aboveground fungal pathogens can substantially reduce biomass production in grasslands. However, we lack a mechanistic understanding of the drivers of fungal pathogen infection and impact. Using a grassland global change and biodiversity experiment we show that the trade‐off between plant growth and defense is the main determinant of infection incidence. In contrast, nitrogen addition only indirectly increased incidence via shifting plant communities towards faster growing species. Plant diversity did not decrease incidence, likely because spillover of generalist pathogens or dominance of susceptible plants counteracted negative diversity effects. A fungicide treatment increased plant biomass production and high levels of infection incidence were associated with reduced biomass. However, pathogen impact was context dependent and infection incidence reduced biomass more strongly in diverse communities. Our results show that a growth‐defense trade‐off is the key driver of pathogen incidence, but pathogen impact is determined by several mechanisms and may depend on pathogen community composition.     

Plant‐driven changes in soil microbial communities influence seed germination through negative feedbacks

相似文献   

Using direct amplification and next-generation sequencing technology to explore foliar endophyte communities in experimentally inoculated western white pines

Fungal endophytes can influence survivability and disease severity of trees. Here we characterized the endophyte community in Pinus monticola (western white pine), an important species in the northwest USA, largely decimated by pathogenic fungi. We also assessed the ability to successfully inoculate seedlings with desirable endophytes, with the long-term goal of providing a protective microbiome and added defense from pathogens. P. monticola seedlings were inoculated in the field with potential pathogen antagonists and fungi isolated from healthy mature trees. Following inoculations direct amplification and next generation sequencing were used to characterize fungal endophyte communities, and explore interspecific competition, diversity, and co-occurrence patterns in needle tissues. Negative co-occurrence patterns between inoculated fungi and potential pathogens, as well as many other species, suggest early competitive interactions. Our study explores early endophyte community assemblage and shows that fungal inoculations may influence tree growth.     

Limited contributions of plant pathogens to density‐dependent seedling mortality of mast fruiting Bornean trees

Fungal pathogens are implicated in driving tropical plant diversity by facilitating strong, negative density‐dependent mortality of conspecific seedlings (C‐NDD). Assessment of the role of fungal pathogens in mediating coexistence derives from relatively few tree species and predominantly the Neotropics, limiting our understanding of their role in maintaining hyper‐diversity in many tropical forests. A key question is whether fungal pathogen‐mediated C‐NDD seedling mortality is ubiquitous across diverse plant communities. Using a manipulative shadehouse experiment, we tested the role of fungal pathogens in mediating C‐NDD seedling mortality of eight mast fruiting Bornean trees, typical of the species‐rich forests of South East Asia. We demonstrate species‐specific responses of seedlings to fungicide and density treatments, generating weak negative density‐dependent mortality. Overall seedling mortality was low and likely insufficient to promote overall community diversity. Although conducted in the same way as previous studies, we find little evidence that fungal pathogens play a substantial role in determining patterns of seedling mortality in a SE Asian mast fruiting forest, questioning our understanding of how Janzen‐Connell mechanisms structure the plant communities of this globally important forest type.     

Pathogen impacts on plant diversity in variable environments

Environmental variability can promote species diversity when species respond differently to environmental conditions, via the storage effect. Pathogens, predators and other shared consumers can also facilitate coexistence when they differentially limit common species. However, it remains unclear how environmental variation and consumers interact to determine species diversity. Here, I use a model based on California annual grassland plants to show that a generalist pathogen with no host specificity can enhance the positive effect of environmental variability on diversity. The model predicts that pathogens can promote diversity by increasing the covariance between the environment and competition, enhancing the storage effect. However, pathogen impacts depend on life history. Pathogens that infect germinating seeds or plants tend to increase the storage effect, whereas those that infect dormant seeds can undermine the storage effect by eliminating population buffering during unfavorable years. These results suggest that pathogens may mediate plant responses to environmental variability and change, and in doing so may maintain diversity.     

Species coexistence and pathogens with frequency-dependent transmission

Pathogens that infect multiple hosts are commonly transmitted by vectors, and their transmission rate is often thought to depend on the proportion of hosts or vectors infected (i.e., frequency dependence). A model of a two-host, one-pathogen system with frequency-dependent transmission is used to investigate how sharing a pathogen with an alternative host influences pathogen-mediated extinction. The results show that if there is frequency-dependent transmission, a host can be rescued from pathogen-mediated extinction by the presence of a second host with which it shares a pathogen. The study provides an important conceptual counterexample to the idea that shared pathogens necessarily result in apparent competition by showing that shared pathogens can mediate apparent mutualism. We distinguish two types of dilution effect (pathogen reduction with increasing host diversity), each resulting from different underlying pathogen transmission processes and host density effects. These results have important consequences for understanding the role of pathogens in species interactions and in maintaining host species diversity.     

The negative effects of pathogen‐infected prey on predators: a meta‐analysis

Intra‐guild predation (IGP) – where a top predator (IG_Pred) consumes both a basal resource and a competitor for that resource (IG_Prey) – has become a fundamental part of understanding species interactions and community dynamics. IGP communities composed of intraguild predators and prey have been well studied; however, we know less about IGP communities composed of predators, pathogens, and resources. Resource quality plays an important role in community dynamics and may influence IGP dynamics as well. We conducted a meta‐analysis on predator–pathogen–resource communities to determine whether resource quality mediated by the pathogen affected predator life‐history traits and if these effects met the theoretical constraints of IGP communities. To do this, we summarized results from studies that investigated the use of predators and pathogens to control insect pests. In these systems, the predators are the IG_Pred and pathogens are the IG_Prey. We found that consumer longevity, fecundity, and survival decreased by 26%, 31% and 13% respectively, when predators consumed pathogen‐infected prey, making the infected prey a low quality resource. Predators also significantly preferred healthy prey over infected prey. When we divided consumers by enemy type, strict predators (e.g. wolf spiders) had no preference while parasitoids preferred healthy prey. Our results suggest that communities containing parasitoids and pathogens may rarely exhibit intraguild predation; whereas, communities composed of strict predators and pathogens are more likely dominated by IGP dynamics. In these latter communities, the consumption of low and high quality resources suggests that IGP communities composed of strict predators, pathogens and prey should naturally persist, supporting IGP theory. Synthesis We investigated how consuming pathogen‐infected prey influence important life‐history parameters of insect predators. Pathogens are used in a variety of biocontrol programs, especially to control crop pests. We found that true predators (i.e. wolf spiders) have no preference for healthy or infected prey and have reduced fecundity, survival and longevity consuming infected prey. However, parasitoids avoided infected prey when possible. In biocontrol programs with multiple control agents, parasitoids and pathogens would do a better job controlling pests as predators would reduce the amount of pathogen available and have reduced fitness from consuming infected prey. However, theory suggests that true predators, prey and pathogens may coexist long term.     

The interaction between plant competition and disease

It is well documented that pathogens can affect the survival, reproduction, and growth of individual plants. Drawing together insights from diverse studies in ecology and agriculture, we evaluate the evidence for pathogens affecting competitive interactions between plants of both the same and different species. Our objective is to explore the potential ecological and evolutionary consequences of such interactions. First, we address how disease interacts with intraspecific competition and present a simple graphical model suggesting that diverse outcomes should be expected. We conclude that the presence of pathogens may have either large or minimal effects on population dynamics depending on many factors including the density-dependent compensatory ability of healthy plants and spatial patterns of infection. Second, we consider how disease can alter competitive abilities of genotypes, and thus may affect the genetic composition of populations. These genetic processes feed back on population dynamics given trade-offs between disease resistance and other fitness components. Third, we examine how the effect of disease on interspecific plant interactions may have potentially far-reaching effects on community composition. A host-specific pathogen, for example, may alter a competitive hierarchy that exists between host and non-host species. Generalist pathogens can also induce indirect competitive interactions between host species. We conclude by highlighting lacunae in our current understanding and suggest that future studies should (1) examine a broader taxonomic range of pathogens since work to date has largely focused on fungal pathogens; (2) increase the use of field competition studies; (3) follow interactions for multiple generations; (4) characterize density-dependent processes; and (5) quantify pathogen, as well as plant, population and community dynamics.     

Emergence and accumulation of novel pathogens suppress an invasive species

Emerging pathogens are a growing threat to human health, agriculture and the diversity of ecological communities but may also help control problematic species. Here we investigated the diversity, distribution and consequences of emerging fungal pathogens infecting an aggressive invasive grass that is rapidly colonising habitats throughout the eastern USA. We document the recent emergence and accumulation over time of diverse pathogens that are members of a single fungal genus and represent multiple, recently described or undescribed species. We also show that experimental suppression of these pathogens increased host performance in the field, demonstrating the negative effects of emerging pathogens on invasive plants. Our results suggest that invasive species can facilitate pathogen emergence and amplification, raising concerns about movement of pathogens among agricultural, horticultural, and wild grasses. However, one possible benefit of pathogen accumulation is suppression of aggressive invaders over the long term, potentially abating their negative impacts on native communities.     

Effect of different root endophytic fungi on plant community structure in experimental microcosms

Understanding the effects of root‐associated microbes in explaining plant community patterns represents a challenge in community ecology. Although typically overlooked, several lines of evidence point out that nonmycorrhizal, root endophytic fungi in the Ascomycota may have the potential to drive changes in plant community ecology given their ubiquitous presence, wide host ranges, and plant species‐specific fitness effects. Thus, we experimentally manipulated the presence of root endophytic fungal species in microcosms and measured its effects on plant communities. Specifically, we tested whether (1) three different root endophyte species can modify plant community structure; (2) those changes can also modified the way plant respond to different soil types; and (3) the effects are modified when all the fungi are present. As a model system, we used plant and fungal species that naturally co‐occur in a temperate grassland. Further, the soil types used in our experiment reflected a strong gradient in soil texture that has been shown to drive changes in plant and fungal community structure in the field. Results showed that each plant species responded differently to infection, resulting in distinct patterns of plant community structure depending on the identity of the fungus present. Those effects depended on the soil type. For example, large positive effects due to presence of the fungi were able to compensate for less nutrients levels in one soil type. Further, host responses when all three fungi were present were different from the ones observed in single fungal inoculations, suggesting that endophyte–endophyte interactions may be important in structuring plant communities. Overall, these results indicate that plant responses to changes in the species identity of nonmycorrhizal fungal community species and their interactions can modify plant community structure.     

Phylogenetic congruence between subtropical trees and their associated fungi

Recent studies have detected phylogenetic signals in pathogen–host networks for both soil‐borne and leaf‐infecting fungi, suggesting that pathogenic fungi may track or coevolve with their preferred hosts. However, a phylogenetically concordant relationship between multiple hosts and multiple fungi in has rarely been investigated. Using next‐generation high‐throughput DNA sequencing techniques, we analyzed fungal taxa associated with diseased leaves, rotten seeds, and infected seedlings of subtropical trees. We compared the topologies of the phylogenetic trees of the soil and foliar fungi based on the internal transcribed spacer (ITS) region with the phylogeny of host tree species based on matK, rbcL, atpB, and 5.8S genes. We identified 37 foliar and 103 soil pathogenic fungi belonging to the Ascomycota and Basidiomycota phyla and detected significantly nonrandom host–fungus combinations, which clustered on both the fungus phylogeny and the host phylogeny. The explicit evidence of congruent phylogenies between tree hosts and their potential fungal pathogens suggests either diffuse coevolution among the plant–fungal interaction networks or that the distribution of fungal species tracked spatially associated hosts with phylogenetically conserved traits and habitat preferences. Phylogenetic conservatism in plant–fungal interactions within a local community promotes host and parasite specificity, which is integral to the important role of fungi in promoting species coexistence and maintaining biodiversity of forest communities.     

Virulence and community dynamics of fungal species with vertical and horizontal transmission on a plant with multiple infections

The virulence evolution of multiple infections of parasites from the same species has been modeled widely in evolution theory. However, experimental studies on this topic remain scarce, particularly regarding multiple infections by different parasite species. Here, we characterized the virulence and community dynamics of fungal pathogens on the invasive plant Ageratina adenophora to verify the predictions made by the model. We observed that A. adenophora was highly susceptible to diverse foliar pathogens with mixed vertical and horizontal transmission within leaf spots. The transmission mode mainly determined the pathogen community structure at the leaf spot level. Over time, the pathogen community within a leaf spot showed decreased Shannon diversity; moreover, the vertically transmitted pathogens exhibited decreased virulence to the host A. adenophora, but the horizontally transmitted pathogens exhibited increased virulence to the host. Our results demonstrate that the predictions of classical models for the virulence evolution of multiple infections are still valid in a complex realistic environment and highlight the impact of transmission mode on disease epidemics of foliar fungal pathogens. We also propose that seedborne fungi play an important role in structuring the foliar pathogen community from multiple infections within a leaf spot.     

Strong coupling of plant and fungal community structure across western Amazonian rainforests

The Amazon basin harbors a diverse ecological community that has a critical role in the maintenance of the biosphere. Although plant and animal communities have received much attention, basic information is lacking for fungal or prokaryotic communities. This is despite the fact that recent ecological studies have suggested a prominent role for interactions with soil fungi in structuring the diversity and abundance of tropical rainforest trees. In this study, we characterize soil fungal communities across three major tropical forest types in the western Amazon basin (terra firme, seasonally flooded and white sand) using 454 pyrosequencing. Using these data, we examine the relationship between fungal diversity and tree species richness, and between fungal community composition and tree species composition, soil environment and spatial proximity. We find that the fungal community in these ecosystems is diverse, with high degrees of spatial variability related to forest type. We also find strong correlations between α- and β-diversity of soil fungi and trees. Both fungal and plant community β-diversity were also correlated with differences in environmental conditions. The correlation between plant and fungal richness was stronger in fungal lineages known for biotrophic strategies (for example, pathogens, mycorrhizas) compared with a lineage known primarily for saprotrophy (yeasts), suggesting that this coupling is, at least in part, due to direct plant–fungal interactions. These data provide a much-needed look at an understudied dimension of the biota in an important ecosystem and supports the hypothesis that fungal communities are involved in the regulation of tropical tree diversity.     

Herbivore and pathogen effects on tree growth are additive,but mediated by tree diversity and plant traits

Herbivores and fungal pathogens are key drivers of plant community composition and functioning. The effects of herbivores and pathogens are mediated by the diversity and functional characteristics of their host plants. However, the combined effects of herbivory and pathogen damage, and their consequences for plant performance, have not yet been addressed in the context of biodiversity–ecosystem functioning research. We analyzed the relationships between herbivory, fungal pathogen damage and their effects on tree growth in a large‐scale forest‐biodiversity experiment. Moreover, we tested whether variation in leaf trait and climatic niche characteristics among tree species influenced these relationships. We found significant positive effects of herbivory on pathogen damage, and vice versa. These effects were attenuated by tree species richness—because herbivory increased and pathogen damage decreased with increasing richness—and were most pronounced for species with soft leaves and narrow climatic niches. However, herbivory and pathogens had contrasting, independent effects on tree growth, with pathogens decreasing and herbivory increasing growth. The positive herbivory effects indicate that trees might be able to (over‐)compensate for local damage at the level of the whole tree. Nevertheless, we found a dependence of these effects on richness, leaf traits and climatic niche characteristics of the tree species. This could mean that the ability for compensation is influenced by both biodiversity loss and tree species identity—including effects of larger‐scale climatic adaptations that have been rarely considered in this context. Our results suggest that herbivory and pathogens have additive but contrasting effects on tree growth. Considering effects of both herbivory and pathogens may thus help to better understand the net effects of damage on tree performance in communities differing in diversity. Moreover, our study shows how species richness and species characteristics (leaf traits and climatic niches) can modify tree growth responses to leaf damage under real‐world conditions.