Gregory S. Gilbert

Phylogenetic signal in plant pathogen–host range

What determines which plant species are susceptible to a given plant pathogen is poorly understood. Experimental inoculations with fungal pathogens of plant leaves in a tropical rain forest show that most fungal pathogens are polyphagous but that most plant species in a local community are resistant to any given pathogen. The likelihood that a pathogen can infect two plant species decreases continuously with phylogenetic distance between the plants, even to ancient evolutionary distances. This phylogenetic signal in host range allows us to predict the likely host range of plant pathogens in a local community, providing an important tool for plant ecology, design of agronomic systems, quarantine regulations in international trade, and risk analysis of biological control agents. In particular, the results suggest that the rate of spread and ecological impacts of a disease through a natural plant community will depend strongly on the phylogenetic structure of the community itself and that current regulatory approaches strongly underestimate the local risks of global movement of plant pathogens or their hosts.

Fungal endophytes in dicotyledonous neotropical trees: patterns of abundance and diversity

Fungal endophytes have been found in every plant species examined to date and appear to be important, but largely unquantified, components of fungal biodiversity. Endophytes are especially little known in tropical forest trees, where their abundance and diversity are thought to be greatest. Here, we explore the occurrence of endophytes in a broad diversity of woody, angiospermous taxa in a lowland, moist tropical forest in central Panama. We use similarity indices to assess host preference and spatial heterogeneity of endophytes associated with two co-occurring, but distantly related, understorey tree species in two sites of that forest, and assess the utility of indices based on frequencies of morphospecies occurrence (Morisita-Horn index) and on presenceabsence data (Sorensens index). We suggest that our understanding of fungal diversity will be enhanced by exploring ecological patterns underlying endophyte occurrence in host species, and discuss methods for assessing the proportion of fungal biodiversity represented by tropical endophytes.

Direct and Interactive Effects of Enemies and Mutualists on Plant Performance: a Meta-Analysis

Plants engage in multiple, simultaneous interactions with other species; some (enemies) reduce and others (mutualists) enhance plant performance. Moreover, effects of different species may not be independent of one another; for example, enemies may compete, reducing their negative impact on a plant. The magnitudes of positive and negative effects, as well as the frequency of interactive effects and whether they tend to enhance or depress plant performance, have never been comprehensively assessed across the many published studies on plant-enemy and plant-mutualist interactions. We performed a meta-analysis of experiments in which two enemies, two mutualists, or an enemy and a mutualist were manipulated factorially. Specifically, we performed a factorial meta-analysis using the log response ratio. We found that the magnitude of (negative) enemy effects was greater than that of (positive) mutualist effects in isolation, but in the presence of other species, the two effects were of comparable magnitude. Hence studies evaluating single-species effects of mutualists may underestimate the true effects found in natural settings, where multiple interactions are the norm and indirect effects are possible. Enemies did not on average influence the effects on plant performance of other enemies, nor did mutualists influence the effects of mutualists. However, these averages mask significant and large, but positive or negative, interactions in individual studies. In contrast, mutualists ameliorated the negative effects of enemies in a manner that benefited plants; this overall effect was driven by interactions between pathogens and belowground mutualists (bacteria and mycorrhizal fungi). The high frequency of significant interactive effects suggests a widespread potential for diffuse rather than pairwise coevolutionary interactions between plants and their enemies and mutualists. Pollinators and mycorrhizal fungi enhanced plant performance more than did bacterial mutualists. In the greenhouse (but not the field), pathogens reduced plant performance more than did herbivores, pathogens were more damaging to herbaceous than to woody plants, and herbivores were more damaging to crop than to non-crop plants (suggesting evolutionary change in plants or herbivores following crop domestication). We discuss how observed differences in effect size might be confounded with methodological differences among studies.

Density and distance-to-adult effects of a canker disease of trees in a moist tropical forest

We compared the spatial distribution of stem cankers on the canopy tree Ocotea whitei (Lauraceae) in a 20-ha plot on Barro Colorado Island, Panama, with spatial and temporal patterns of mortality in this host over the previous decade. The cankers occur both on adult and juvenile individuals, aothough juveniles are much more likely the adults to show symptoms. Disease incidence is host-density dependent, and both the presence of the disease and host mortality are more likely close to than far from a conspecific adult, which resulted in a net spatial shift of the juvenile population away from conspecific adults through time. Disease incidence is lower than expected among juveniles of O. whitei growing near to adults of the non-susceptible canopy tree Beilschmiedia pendula. The coincidence of spatial patterns of canker incidence and host mortality suggest a role for the disease in regulating host spatial distribution, in agreement with predictions of the Janzen-Connell hypothesis.

WHEN THERE IS NO ESCAPE: THE EFFECTS OF NATURAL ENEMIES ON NATIVE, INVASIVE, AND NONINVASIVE PLANTS

An important question in the study of biological invasions is the degree to which successful invasion can be explained by release from control by natural enemies. Natural enemies dominate explanations of two alternate phenomena: that most introduced plants fail to establish viable populations (biotic resistance hypothesis) and that some introduced plants become noxious invaders (natural enemies hypothesis). We used a suite of 18 phylogenetically related native and nonnative clovers (Trifolium and Medicago) and the foliar pathogens and invertebrate herbivores that attack them to answer two questions. Do native species suffer greater attack by natural enemies relative to introduced species at the same site? Are some introduced species excluded from native plant communities because they are susceptible to local natural enemies? We address these questions using three lines of evidence: (1) the frequency of attack and composition of fungal pathogens and herbivores for each clover species in four years of common garden experiments, as well as susceptibility to inoculation with a common pathogen; (2) the degree of leaf damage suffered by each species in common garden experiments; and (3) fitness effects estimated using correlative approaches and pathogen removal experiments. Introduced species showed no evidence of escape from pathogens, being equivalent to native species as a group in terms of infection levels, susceptibility, disease prevalence, disease severity (with more severe damage on introduced species in one year), the influence of disease on mortality, and the effect of fungicide treatment on mortality and biomass. In contrast, invertebrate herbivores caused more damage on native species in two years, although the influence of herbivore attack on mortality did not differ between native and introduced species. Within introduced species, the predictions of the biotic resistance hypothesis were not supported: the most invasive species showed greater infection, greater prevalence and severity of disease, greater prevalence of herbivory, and greater effects of fungicide on biomass and were indistinguishable from noninvasive introduced species in all other respects. Therefore, although herbivores preferred native over introduced species, escape from pest pressure cannot be used to explain why some introduced clovers are common invaders in coastal prairie while others are not.

Effects of an Introduced Bacterium on Bacterial Communities on Roots

The objective of this work was to determine whether introduction of a bac- terium altered microbial communities associated with roots. We conducted experiments in the field and in a growth chamber to determine whether coating soybean seeds with marked strains derived from the biological control agent Bacillus cereus UW85 affected the bacterial community in the rhizosphere of soybeans. We characterized 2651 individual isolates of bacteria from root-free soil and from soybean seedlings based on 43-50 phys- iological attributes. Discriminant analysis of the bacterial communities according to these attributes showed that the communities of rhizosphere bacteria that developed on non- treated plants and on plants grown from seeds coated with a single strain of bacteria were sometimes dramatically different. This occurred even when the introduced strain did not persist as a common member of the community. In two of four experiments we could as easily differentiate between bacterial communities on roots of UW85-treated and non- treated seedlings as between the communities in the rhizosphere and root-free soil. In the other two experiments we could differentiate only between communities in root-free soil and on roots. In the comparison of bacteria from root-free soil and from the soybean rhizosphere, we found that bacteria from root-free soil were more likely to degrade complex carbon sources than were rhizosphere bacteria, whereas bacteria from roots were resistant to more antimicrobial substances and were able to grow on a wider range of simple carbon sources than were bacteria isolated from root-free soil.

Phylogenetic structure and host abundance drive disease pressure in communities

Pathogens play an important part in shaping the structure and dynamics of natural communities, because species are not affected by them equally. A shared goal of ecology and epidemiology is to predict when a species is most vulnerable to disease. A leading hypothesis asserts that the impact of disease should increase with host abundance, producing a ‘rare-species advantage’. However, the impact of a pathogen may be decoupled from host abundance, because most pathogens infect more than one species, leading to pathogen spillover onto closely related species. Here we show that the phylogenetic and ecological structure of the surrounding community can be important predictors of disease pressure. We found that the amount of tissue lost to disease increased with the relative abundance of a species across a grassland plant community, and that this rare-species advantage had an additional phylogenetic component: disease pressure was stronger on species with many close relatives. We used a global model of pathogen sharing as a function of relatedness between hosts, which provided a robust predictor of relative disease pressure at the local scale. In our grassland, the total amount of disease was most accurately explained not by the abundance of the focal host alone, but by the abundance of all species in the community weighted by their phylogenetic distance to the host. Furthermore, the model strongly predicted observed disease pressure for 44 novel host species we introduced experimentally to our study site, providing evidence for a mechanism to explain why phylogenetically rare species are more likely to become invasive when introduced. Our results demonstrate how the phylogenetic and ecological structure of communities can have a key role in disease dynamics, with implications for the maintenance of biodiversity, biotic resistance against introduced weeds, and the success of managed plants in agriculture and forestry.

Susceptibility of clover species to fungal infection: the interaction of leaf surface traits and environment.

Many foliar pathogens require free water to germinate; therefore, disease pressure should favor plants that are able to repel water. For a suite of 18 sympatric clover species (Trifolium and Medicago, Fabaceae), we evaluated leaf traits affecting leaf wetness and susceptibility to infection by the fungal pathogen Stemphylium sp., causal agent of Stemphylium leaf spot. Spore germination increased with time in free water, and the relative susceptibility of host plants to infection was proportional to the duration of water retention on leaves. Larger leaves captured more water and retained it longer. Unexpectedly, trichomes and leaf wettability did not affect water capture. For clovers planted within natural clover populations at two sites, infection was threefold greater at the wetter site. At the drier site, water retention on the leaf surface was an important predictor of infection rates across host species, but persistent fog and dew at the wetter site reduced the importance of rapid leaf drying. Our results suggest that plant adaptations that reduce water retention on leaves may also reduce disease incidence, but the selective advantage of these traits will vary among habitats.

Polypore fungal diversity and host density in a moist tropical forest

In a moist tropical forest in Panama, the wood-decay polyporefungi comprise many rare species (more than half found only once) andexhibit diversity that exceeds that of the supporting tree community.The most abundant fungal species were non-specialists, each found onseveral host species from multiple plant families. In diverse fungalcommunities, each of many species should infect a given host species ina density-dependent manner, so that the infected proportion of a hostpopulation should increase with host density. Applied across hostspecies, hosts with denser populations should support greater fungaldiversity. For 10 tree species, fungal incidence and diversity increasedwith abundance of the host in the community, consistent withacross-species density-dependent infection. Fungal diversity associatedwith individual trunks did not, however, vary with host-species density.Both host density and persistence of decaying logs may be important indetermining fungal diversity associated with tree species.

Community composition of root-associated fungi in a Quercus-dominated temperate forest: “codominance” of mycorrhizal and root-endophytic fungi

In terrestrial ecosystems, plant roots are colonized by various clades of mycorrhizal and endophytic fungi. Focused on the root systems of an oak-dominated temperate forest in Japan, we used 454 pyrosequencing to explore how phylogenetically diverse fungi constitute an ecological community of multiple ecotypes. In total, 345 operational taxonomic units (OTUs) of fungi were found from 159 terminal-root samples from 12 plant species occurring in the forest. Due to the dominance of an oak species (Quercus serrata), diverse ectomycorrhizal clades such as Russula, Lactarius, Cortinarius, Tomentella, Amanita, Boletus, and Cenococcum were observed. Unexpectedly, the root-associated fungal community was dominated by root-endophytic ascomycetes in Helotiales, Chaetothyriales, and Rhytismatales. Overall, 55.3% of root samples were colonized by both the commonly observed ascomycetes and ectomycorrhizal fungi; 75.0% of the root samples of the dominant Q. serrata were so cocolonized. Overall, this study revealed that root-associated fungal communities of oak-dominated temperate forests were dominated not only by ectomycorrhizal fungi but also by diverse root endophytes and that potential ecological interactions between the two ecotypes may be important to understand the complex assembly processes of belowground fungal communities.