Feeding the fever: Complex host-pathogen dynamics along continuous resource gradients.

Food has long been known to perform dual functions of nutrition and medicine, but mounting evidence suggests that complex host-pathogen dynamics can emerge along continuous resource gradients. Empirical examples of nonmonotonic responses of infection with increasing host resources (e.g., low prevalence at low and high resource supply but high prevalence at intermediate resources) have been documented across the tree of life, but these dynamics, when observed, often are interpreted as nonintuitive, idiosyncratic features of pathogen and host biology. Here, by developing generalized versions of existing models of resource dependence for within- and among-host infection dynamics, we provide a synthetic view of nonmonotonic infection dynamics. We demonstrate that where resources jointly impact two (or more) processes (e.g., growth, defense, transmission, mortality, predation), nonmonotonic infection dynamics, including alternative states, can emerge across a continuous resource supply gradient. We review the few empirical examples that concurrently measured resource effects on multiple rates and pair this with a wide range of examples in which resource dependence of multiple rates could generate nonmonotonic infection outcomes under realistic conditions. This review and generalized framework highlight the likely generality of such resource effects in natural systems and point to opportunities ripe for future empirical and theoretical work.

Litter, Plant Competition, and Ecosystem Dynamics: A Theoretical Perspective.

AbstractCommunity structure depends jointly on species' responses to, and effects on, environmental factors. Many such factors, including detritus, are studied in ecosystem ecology. Detritus in terrestrial ecosystems is dominated by plant litter (nonliving organic material), which, in addition to its role in material cycling, can act as a niche factor modulating interactions among plants. Litter thus links traditional community and ecosystem processes, which are often studied separately. We explore this connection using population dynamics models of two plant species and a litter pool. We first find conditions determining the outcome of interactions between these species, highlighting the role that litter plays and the role of broader ecosystem parameters, such as decomposition rate. Species trade-offs in tolerance to direct competition and litter-based interference competition allow for coexistence, provided the litter-tolerant species produces more litter at the population level; otherwise, priority effects may result. When species coexist, litter-mediated interactions between plants disrupt the traditional relationship between biomass accumulation and decomposition. Increasing decomposition rate may have no effect on standing litter density and, in some cases, may even increase litter load. These results illustrate how ecosystem variables can influence community outcomes that then feed back to influence the ecosystem.

Long-term nitrogen enrichment mediates the effects of nitrogen supply and co-inoculation on a viral pathogen.

Host nutrient supply can mediate host-pathogen and pathogen-pathogen interactions. In terrestrial systems, plant nutrient supply is mediated by soil microbes, suggesting a potential role of soil microbes in plant diseases beyond soil-borne pathogens and induced plant defenses. Long-term nitrogen (N) enrichment can shift pathogenic and nonpathogenic soil microbial community composition and function, but it is unclear if these shifts affect plant-pathogen and pathogen-pathogen interactions. In a growth chamber experiment, we tested the effect of long-term N enrichment on infection by Barley Yellow Dwarf Virus (BYDV-PAV) and Cereal Yellow Dwarf Virus (CYDV-RPV), aphid-vectored RNA viruses, in a grass host. We inoculated sterilized growing medium with soil collected from a long-term N enrichment experiment (ambient, low, and high N soil treatments) to isolate effects mediated by the soil microbial community. We crossed soil treatments with a N supply treatment (low, high) and virus inoculation treatment (mock-, singly-, and co-inoculated) to evaluate the effects of long-term N enrichment on plant-pathogen and pathogen-pathogen interactions, as mediated by N availability. We measured the proportion of plants infected (i.e., incidence), plant biomass, and leaf chlorophyll content. BYDV-PAV incidence (0.96) declined with low N soil (to 0.46), high N supply (to 0.61), and co-inoculation (to 0.32). Low N soil mediated the effect of N supply on BYDV-PAV: instead of N supply reducing BYDV-PAV incidence, the incidence increased. Additionally, ambient and low N soil ameliorated the negative effect of co-inoculation on BYDV-PAV incidence. BYDV-PAV infection only reduced chlorophyll when plants were grown with low N supply and ambient N soil. There were no significant effects of long-term N soil on CYDV-RPV incidence. Soil inoculant with different levels of long-term N enrichment had different effects on host-pathogen and pathogen-pathogen interactions, suggesting that shifts in soil microbial communities with long-term N enrichment may mediate disease dynamics.

Native perennial and non-native annual grasses shape pathogen community composition and disease severity in a California grassland.

The densities of highly competent plant hosts (i.e. those that are susceptible to and successfully transmit a pathogen) may shape pathogen community composition and disease severity, altering disease risk and impacts. Life history and evolutionary history can influence host competence; longer lived species tend to be better defended than shorter lived species and pathogens adapt to infect species with which they have longer evolutionary histories. It is unclear, however, how the densities of species that differ in competence due to life and evolutionary histories affect plant pathogen community composition and disease severity.We examined foliar fungal pathogens of two host groups in a California grassland: native perennial and non-native annual grasses. We first characterized pathogen community composition and disease severity of the two host groups to approximate differences in competence. We then used observational and manipulated gradients of native perennial and non-native annual grass densities to assess the effects of each host group on pathogen community composition and disease severity in 1-m2 plots.Native perennial and non-native annual grasses hosted distinct pathogen communities but shared generalist pathogens. Native perennial grasses experienced 26% higher disease severity than non-native annuals. Only the observational gradient of native perennial grass density affected disease severity; there were no other significant relationships between host group density and either disease severity or pathogen community composition.Synthesis. The life and evolutionary histories of grasses likely influence their competence for different pathogen species, exemplified by distinct pathogen communities and differences in disease severity. However, there was limited evidence that the density of either host group affected pathogen community composition or disease severity. Therefore, competence for different pathogens likely shapes pathogen community composition and disease severity but may not interact with host density to alter disease risk and impacts at small scales.

Water availability modifies productivity response to biodiversity and nitrogen in long-term grassland experiments.

Diversity and nitrogen addition have positive relationships with plant productivity, yet climate-induced changes in water availability threaten to upend these established relationships. Using long-term data from three experiments in a mesic grassland (ranging from 17 to 34 yr of data), we tested how the effects of species richness and nitrogen addition on community-level plant productivity changed as a function of annual fluctuations in water availability using growing season precipitation and the Standardized Precipitation-Evapotranspiration Index (SPEI). While results varied across experiments, our findings demonstrate that water availability can magnify the positive effects of both biodiversity and nitrogen addition on productivity. These results suggest that productivity responses to anthropogenic species diversity loss and increasing nitrogen deposition could depend on precipitation regimes, highlighting the importance of testing interactions between multiple global change drivers.

Emerging fungal pathogen of an invasive grass: Implications for competition with native plant species.

Infectious diseases and invasive species can be strong drivers of biological systems that may interact to shift plant community composition. For example, disease can modify resource competition between invasive and native species. Invasive species tend to interact with a diversity of native species, and it is unclear how native species differ in response to disease-mediated competition with invasive species. Here, we quantified the biomass responses of three native North American grass species (Dichanthelium clandestinum, Elymus virginicus, and Eragrostis spectabilis) to disease-mediated competition with the non-native invasive grass Microstegium vimineum. The foliar fungal pathogen Bipolaris gigantea has recently emerged in Microstegium populations, causing a leaf spot disease that reduces Microstegium biomass and seed production. In a greenhouse experiment, we examined the effects of B. gigantea inoculation on two components of competitive ability for each native species: growth in the absence of competition and biomass responses to increasing densities of Microstegium. Bipolaris gigantea inoculation affected each of the three native species in unique ways, by increasing (Dichanthelium), decreasing (Elymus), or not changing (Eragrostis) their growth in the absence of competition relative to mock inoculation. Bipolaris gigantea inoculation did not, however, affect Microstegium biomass or mediate the effect of Microstegium density on native plant biomass. Thus, B. gigantea had species-specific effects on native plant competition with Microstegium through species-specific biomass responses to B. gigantea inoculation, but not through modified responses to Microstegium density. Our results suggest that disease may uniquely modify competitive interactions between invasive and native plants for different native plant species.

Host nutrition mediates interactions between plant viruses, altering transmission and predicted disease spread.

Interactions among co-infecting pathogens are common across host taxa and can affect infectious disease dynamics. Host nutrition can mediate these among-pathogen interactions, altering the establishment and growth of pathogens within hosts. It is unclear, however, how nutrition-mediated among-pathogen interactions affect transmission and the spread of disease through populations. We manipulated the nitrogen (N) and phosphorus (P) supplies to oat plants in growth chambers and evaluated interactions between two aphid-vectored Barley and Cereal Yellow Dwarf Viruses: PAV and RPV. We quantified the effect of each virus on the other's establishment, within-plant density, and transmission. Co-inoculation significantly increased PAV density when N and P supplies were low and tended to increase RPV density when N supply was high. Co-infection increased PAV transmission when N and P supplies were low and tended to increase RPV transmission when N supply was high. Despite the parallels between the effects of among-pathogen interactions on density and transmission, changes in virus density only partially explained changes in transmission, suggesting that virus density-independent processes contribute to transmission. A mathematical model describing the spread of two viruses through a plant population, parameterized with empirically derived transmission values, demonstrated that nutrition-mediated among-pathogen interactions could affect disease spread. Interactions that altered transmission through virus density-independent processes determined overall disease dynamics. Our work suggests that host nutrition alters disease spread through among-pathogen interactions that modify transmission.

Disease in Invasive Plant Populations.

Non-native invasive plants can establish in natural areas, where they can be ecologically damaging and costly to manage. Like cultivated plants, invasive plants can experience a relatively disease-free period upon introduction and accumulate pathogens over time. Diseases of invasive plant populations are infrequently studied compared to diseases of agriculture, forestry, and even native plant populations. We evaluated similarities and differences in the processes that are likely to affect pathogen accumulation and disease in invasive plants compared to cultivated plants, which are the dominant focus of the field of plant pathology. Invasive plants experience more genetic, biotic, and abiotic variation across space and over time than cultivated plants, which is expected to stabilize the ecological and evolutionary dynamics of interactions with pathogens and possibly weaken the efficacy of infectious disease in their control. Although disease is expected to be context dependent, the widespread distribution of invasive plants makes them important pathogen reservoirs. Research on invasive plant diseases can both protect crops and help manage invasive plant populations.

Modeling nutrient and disease dynamics in a plant-pathogen system.

Human activities alter elemental nutrient cycling, which can have profound impacts on agriculture, grasslands, lakes, and other systems. It is becoming increasingly clear that enhanced nitrogen and phosphorus levels can affect disease dynamics across a range of taxa. However, there are few mathematical models that explicitly incorporate nutrients into host-pathogen interactions. Using viral load and plant mass data from an experiment with cereal yellow dwarf virus and its host plant, Avena sativa, we propose and compare two models describing the overall infection dynamics. However, the first model considers nutrient-limited virus production while the other considers a nutrient-induced viral production delay. A virus reproduction number is derived for this nutrient model, which depends on environmental and physiological attributes. Results suggest that including nutrient mediated viral production mechanisms can give rise to robust models that can be used to untangle how nutrients impact pathogen dynamics.

The community ecology of pathogens: coinfection, coexistence and community composition.

Disease and community ecology share conceptual and theoretical lineages, and there has been a resurgence of interest in strengthening links between these fields. Building on recent syntheses focused on the effects of host community composition on single pathogen systems, we examine pathogen (microparasite) communities using a stochastic metacommunity model as a starting point to bridge community and disease ecology perspectives. Such models incorporate the effects of core community processes, such as ecological drift, selection and dispersal, but have not been extended to incorporate host-pathogen interactions, such as immunosuppression or synergistic mortality, that are central to disease ecology. We use a two-pathogen susceptible-infected (SI) model to fill these gaps in the metacommunity approach; however, SI models can be intractable for examining species-diverse, spatially structured systems. By placing disease into a framework developed for community ecology, our synthesis highlights areas ripe for progress, including a theoretical framework that incorporates host dynamics, spatial structuring and evolutionary processes, as well as the data needed to test the predictions of such a model. Our synthesis points the way for this framework and demonstrates that a deeper understanding of pathogen community dynamics will emerge from approaches working at the interface of disease and community ecology.