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Halliday, F. W.

Publications and source records attributed to Halliday, F. W..

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Loss of a belowground mutualist disrupts a fundamental biodiversity-disease relationship

Diverse ecological communities can reduce pathogen transmission; a phenomenon known as the dilution effect of biodiversity. This effect, in turn, depends on variation in host species' ability to spread disease (i.e., host competence) and which host species persist under biodiversity loss. Mutualistic symbionts can influence host competence and are sensitive to variation in host biodiversity; yet whether mutualists can modify dilution effects is unknown, partially because quantifying host competence during epidemics remains challenging. We experimentally tested whether mutualists could modify dilution effects by establishing gradients of host species richness, community competence, and access to the below-ground arbuscular mycorrhizal fungus (AMF), Rhizoglomus irregulare. Plant hosts were then exposed to the fungal root pathogen, Rhizoctonia solani, and disease spread was monitored over the course of an epidemic. Overall, host richness did not affect epidemic outcomes. Instead, AMF inoculation increased disease risk via species-specific increases in host competence. Moreover, communities containing highly competent host species experienced more disease, but only in the presence of mutualistic AMF. These results underscore the importance of plant community composition in mycorrhiza-mediated disease dynamics and suggest that predicting disease in our changing world might require a deeper understanding of host-symbiont and pathogen-symbiont interactions under global change.

ecology↗

Environment and host infection history jointly predict disease risk in a multi-pathogen system

Forecasting disease epidemics may require considering both abiotic and biotic conditions. Abiotic conditions can influence pathogen dispersal, survival, and infection, while prior infection by one pathogen species can alter host susceptibility to subsequent pathogens, creating historical contingencies. Yet, the relative importance of environmental conditions, within-host pathogen interactions, and their interplay in predicting seasonal disease dynamics remains underexplored. We analyzed approximately 30,000 plant-level observations of three foliar fungal diseases on the grass species tall fescue in a North Carolina old field, and meteorological data, from 2017-2024. Using such datasets to make ecological predictions that are accurate and interpretable may require multiple modeling approaches. Temporally explicit random forest models predicted future disease with over 80% accuracy for two of the three diseases and revealed environmental thresholds for disease prediction in environmental variables including temperature and humidity. Survival analyses showed that pathogen-pathogen interactions rivaled environmental conditions in predicting risk of crown rust, which was strongly facilitated by prior anthracnose infection. Across all pathogens, Bayesian hierarchical models recovered evidence that facilitative interactions between coinfecting pathogens were modulated by effects of environmental conditions, particularly temperature. Together, these complementary approaches show that a host's current disease state can matter as much as its environment in predicting disease, identify key environmental factors associated with disease risk, and show that modulation of environmental drivers by pathogen coinfections can improve predictions of seasonal disease epidemics. Other disease forecasts may be improved by accounting not just for environmental drivers, but also how those drivers propagate through pathogen species interactions.

ecology↗

Disease decreases variation in host community structure in an old-field grassland

Disease may modulate variation in host community structure by modifying the interplay of deterministic and stochastic processes. For instance, deterministic processes like ecological selection can benefit species less impacted by disease. When disease consistently selects for certain host species, this can reduce variation in host community composition. On the other hand, when host communities are less impacted by disease and selection is weaker, stochastic processes (e.g., drift, dispersal) may play a bigger role in host community structure, which can increase variation in structure among communities. While effects of disease on host community structure have been quantified in field experiments, few have addressed the role of disease in modulating variation in structure among host communities. To address this, we conducted a field experiment spanning three years, using a tractable system: foliar fungal pathogens in an old-field grassland community dominated by the grass Lolium arundinaceum, tall fescue. We reduced foliar fungal disease burden in replicate host communities (experimental plots in intact vegetation) in three fungicide regimens that varied in the duration of fungicide exposure and included a fungicide-free control. We measured host diversity, biomass, and variation in community structure among replicate communities. Disease reduction generally decreased plant richness and increased aboveground biomass relative to communities experiencing ambient levels of disease. Despite changes in structure of the plant communities over the experiments three years, the effects of disease reduction on plant richness and biomass were consistent across years. However, disease reduction did not reduce variation in host community structure, providing little evidence for ecological selection by competition or other deterministic processes. Instead, disease reduction tended to amplify variation in host community structure among replicate communities (i.e., within fungicide treatment groups), suggesting that disease diminished the degree to which host communities were structured by stochastic processes. These results of experimental disease reduction both highlight the potential importance of stochastic processes in plant communities and reveal the potential for disease to regulate variation in host community structure.

ecology↗

Global change drivers and the risk of infectious disease

Anthropogenic change is contributing to the rise in emerging infectious diseases, but it remains unclear which global change drivers most increase disease and under what contexts. We amassed a dataset from the literature that includes 1,832 observations of infectious disease responses to global change drivers across 1,202 host-parasite combinations. We found that biodiversity loss, climate change, and introduced species were associated with increases in disease-related endpoints or harm (i.e., enemy release for introduced species), whereas urbanization was associated with decreases in disease endpoints. Natural biodiversity gradients, deforestation, forest fragmentation, and most classes of chemical contaminants had non-significant effects on these endpoints. Overall, these results were consistent across human and non-human diseases. Context-dependent effects of the global change drivers on disease were common and are discussed. These findings will help better target disease management and surveillance efforts towards global change drivers that increase disease. One-Sentence SummaryHere we quantify which global change drivers increase infectious diseases the most to better target global disease management and surveillance efforts.

ecology↗

Effects of abiotic environment on invertebrate herbivory depend on plant community context in a montane grassland

Invertebrate herbivores are important and diverse, and their abundance and impacts are expected to undergo unprecedented shifts under climate change. Yet, past studies of invertebrate herbivory have documented a wide variety of responses to changing temperature, making it challenging to predict the direction and magnitude of these shifts. One explanation for these idiosyncratic responses is that changing environmental conditions may drive concurrent changes in plant communities and herbivore traits. Thus, the impacts of changing temperature on herbivory might depend on how temperature combines and interacts with characteristics of plant communities and the herbivores that occupy them. Here, we test this hypothesis by surveying invertebrate herbivory in 220, 0.5 meter-diameter herbaceous plant communities along a 1101-meter elevational gradient. Our results suggest that increasing temperature can drive community-level herbivory via at least three overlapping mechanisms: increasing temperature directly reduced herbivory, indirectly affected herbivory by reducing phylogenetic diversity of the plant community, and indirectly affected herbivory by altering the effects of functional and phylogenetic diversity on herbivory. Consequently, increasing functional diversity of plant communities had a negative effect on herbivory, but only in colder environments while a positive effect of increasing phylogenetic diversity was observed in warmer environments. Moreover, accounting for differences among herbivore feeding guilds considerably improved model fit, because different herbivore feeding guilds varied in their response to temperature and plant community composition. Together, these results highlight the importance of considering both plant and herbivore community context in order to predict how climate change will alter invertebrate herbivory.

ecology↗

Environmental drivers of disease depend on host community context

Predicting disease risk in an era of unprecedented biodiversity and climate change is more challenging than ever, largely because when and where hosts are at greatest risk of becoming infected depends on complex relationships between hosts, parasites, and the environment. Theory predicts that host species characterized by fast-paced life-history strategies are more susceptible to infection and contribute more to transmission than their slow-paced counterparts. Hence, disease risk should increase as host community structure becomes increasingly dominated by fast-paced hosts. Theory also suggests that environmental gradients can alter disease risk, both directly, due to abiotic constraints on parasite replication and growth, and indirectly, by changing host community structure. What is more poorly understood, however, is whether environmental gradients can also alter the effect of host community structure on disease risk. We addressed these questions using a detailed survey of host communities and infection severity along a 1100m elevational gradient in southeastern Switzerland. Consistent with prior studies, increasing elevation directly reduced infection severity, which we attribute to abiotic constraints, and indirectly reduced infection severity via changes in host richness, which we attribute to encounter reduction. Communities dominated by fast pace-of-life hosts also experienced more disease. Finally, although elevation did not directly influence host community pace-of-life, the relationship between pace-of-life and disease was sensitive to elevation: increasing elevation weakened the relationship between host community pace-of-life and infection severity. This result provides the first field evidence, to our knowledge, that an environmental gradient can alter the effect of host community structure on infection severity.

ecology↗

Contrasting effects of nutrients and consumers on tree colonization and growth during secondary succession

For succession to proceed from herbaceous to woody dominance, trees must colonize herbaceous communities and grow. Success across these two phases of succession might result from different interactions with the herbaceous community. First, colonizing trees must compete against larger, established herbs, while subsequent growth occurs among similarly sized or smaller herbs. This shift from colonization to growth may cause three drivers of secondary succession-- nutrients, consumers, and herbaceous diversity--to differentially affect tree colonization and growth. Initially, these drivers should favor larger, established herbs, reducing colonization. Later, when established trees can better compete with herbs, these drivers should benefit trees and increase their growth. In a four-year study, we added nutrients to, excluded aboveground consumers from, and manipulated initial richness of, the herbaceous community, then allowed trees to naturally colonize these communities (from intact seedbanks or as seed-rain) and grow. Nutrients and consumers had opposing effects on tree colonization and growth: adding nutrients and excluding consumers reduced tree colonization, but later increased established tree growth (height, basal diameter). Together, this shows stage-specific impacts of nutrients and consumers that may improve predictions of the rate and trajectory of succession: factors that initially limited tree colonization later helped established trees to grow.

ecology↗

Biodiversity loss underlies the dilution effect of biodiversity

The dilution effect predicts increasing biodiversity to reduce the risk of infection, but the generality of this effect remains unresolved. Because biodiversity loss generates predictable changes in host community competence, we hypothesized that biodiversity loss might drive the dilution effect. We tested this hypothesis by reanalyzing four previously published meta-analyses that came to contradictory conclusions regarding generality of the dilution effect. In the context of biodiversity loss, our analyses revealed a unifying pattern: dilution effects were inconsistently observed for natural biodiversity gradients, but were commonly observed for biodiversity gradients generated by disturbances causing losses of native biodiversity. Incorporating biodiversity loss into tests of generality of the dilution effect further indicated that scale-dependency may strengthen the dilution effect only when biodiversity gradients are driven by biodiversity loss. Together, these results help to resolve one of the most contentious issues in disease ecology: the generality of the dilution effect.

ecology↗

Parasites as niche modifiers for the microbiome: A field test with multiple parasites

Parasites can affect and be affected by the hosts microbiome, with consequences for host susceptibility, parasite transmission, and host and parasite fitness. Yet, there are two aspects of the relationship between parasite infection and the host microbiome that remain little understood: the nature of the relationship under field conditions, and how the relationship varies among parasite species. To overcome these limitations, we assayed the within-leaf fungal community in a grass population to investigate how diversity and composition of the fungal microbiome are associated with natural infection by fungal parasites with different feeding strategies. We hypothesized that parasites that more strongly modify niches available within a host will thereby alter the microbial taxa that can colonize the community and be associated with greater changes in microbiome diversity and composition. A parasite that creates necrotic tissue to extract resources (necrotrophs) may act as a particularly strong niche modifier whereas one that does not (biotrophs) may not. Barcoded amplicon sequencing of the fungal ITS region revealed that the microbiome of leaf segments that were symptomatic of necrotrophs had lower fungal diversity and distinct composition compared to segments that were asymptomatic or symptomatic of other parasites. There were no clear differences in fungal diversity or composition between leaf segments that were asymptomatic and segments that were symptomatic of other parasite feeding strategies. This supports the hypothesis that within-host niches link infection by parasites to the hosts microbiome. Together, these results highlight the importance of parasite traits in determining parasite impacts on the hosts microbiome.

ecology↗

Facilitative priority effects drive parasite assembly under coinfection

Host individuals are often coinfected with diverse parasite assemblages, resulting in complex interactions among parasites within hosts. Within hosts, priority effects occur when the infection sequence alters the outcome of interactions among parasites. Yet, the role of host immunity in this process remains poorly understood. We hypothesized that the host response to first infection could generate priority effects among parasites, altering the assembly of later arriving strains during epidemics. We tested this by infecting sentinel host genotypes of Plantago lanceolata with strains of the fungal parasite, Podosphaera plantaginis, and measuring susceptibility to subsequent infection during experimental and natural epidemics. In these experiments, prior infection by one strain often increased susceptibility to other strains, and these facilitative priority effects altered the structure of parasite assemblages, but this effect depended on host genotype, host population, and parasite genotype. Thus, host genotype, spatial structure, and priority effects among strains all independently altered parasite assembly. Then, using a fine-scale survey and sampling of infections on wild hosts in several populations, we identified a signal of facilitative priority effects, which altered parasite assembly during natural epidemics. Together, these results provide evidence that within host priority effects by early arriving strains can drive parasite assembly, with implications for how strain diversity is spatially and temporally distributed during epidemics.

ecology↗

Host community assembly modifies the relationship between host and parasite richness

Host and parasite richness are generally positively correlated, but the stability of this relationship during community assembly remains untested. The composition of host communities can alter parasite transmission, and the relationship between host and parasite richness is sensitive to parasite transmission. Thus, changes in composition during host community assembly could strengthen or weaken the relationship between host and parasite richness. Host community assembly, in turn, can be driven by many processes, including resource enrichment. To test the hypothesis that host community assembly can alter the relationship between host and parasite richness, we experimentally crossed host diversity and resource supply to hosts, then allowed communities to assemble. As previously shown, initial host diversity and resource supply determined the trajectory of host community assembly, altering post-assembly host species richness, richness-independent host phylogenetic diversity, and colonization by exotic host species. Throughout community assembly, host richness predicted parasite richness. As predicted, this effect was moderated by exotic abundance: communities dominated by exotic species exhibited a stronger positive relationship between post-assembly host and parasite richness. Ultimately, these results suggest that, by modulating parasite transmission, community assembly can modify the relationship between host and parasite richness, providing a novel mechanism to explain contingencies in this relationship.

ecology↗

Priority effects, consumer pressure, and soil resources independently alter plant diversity and resource strategies during a multi-year successional field experiment

O_LIPlant community succession is structured by priority effects, plant consumer pressure, and soil resource supply. Importantly, these drivers may interact, their effects may vary temporally, and they may influence different facets of plant community diversity by promoting different plant tradeoff strategies.\nC_LIO_LIIn an herbaceous successional system, we manipulated priority effects by altering initial plant richness, consumer pressure via pesticide spraying, and soil resource supply via fertilization. We examined how these processes jointly influenced succession, including taxonomic diversity and functional traits, over four years.\nC_LIO_LIDiversity decreased in different years in response to more diverse priority effects, lower consumer pressure, and increased soil resource supply. Functionally, higher soil resource supply increased community height, SLA, and seed mass; higher consumer pressure decreased intraspecific community height, and increased interspecific SLA; priority effects led to decreased seed mass only when plots were unplanted.\nC_LIO_LIOur results suggest species resource strategies underlie plant diversity responses. Resource addition promoted resource-acquisitive species, consumer pressure disadvantaged resource-conservative species, and diversity of priority effects altered subsequent community composition through persistence of early residents, not via traits. We show that community responses to drivers of succession depend on underlying trait tradeoffs of resident species, and these tradeoffs influence community diversity across succession.\nC_LI

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