Elements of disease in a changing world: modelling feedbacks between infectious disease and ecosystems

Borer, Elizabeth T.; Asik, Lale; Everett, Rebecca A.; Frenken, Thijs; Gonzalez, Andrea F.; Paseka, Rachel E.; Peace, Angela; Seabloom, Eric W.; Strauss, Alexander T.; Waal, Dedmer B. Van de; White, Lauren A.

doi:10.1111/ele.13617

Cited by 16 publications

(42 citation statements)

References 67 publications

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“…Studying these relationships as unidirectional processes is empirically convenient and a prerequisite to a broader perspective that encompasses many processes linking disease and ecosystem function. However, pathogens and nutrient availability can simultaneously impact host stoichiometry, growth rate, and mortality, scaling up to generate dynamic impacts on nutrients as well as host populations and communities (Borer et al, 2021; Vannatta & Minchella, 2018). Thus, these concurrent effects can interact to qualitatively alter the dynamics of hosts, pathogens, and nutrients.…”

Section: Disease‐mediated Nutrient Dynamicsmentioning

confidence: 99%

“…Shifts in infection within hosts can, in turn, lead to impacts on nutrient dynamics, particularly when the hosts are autotrophs, by altering individual host chemistry, physiology, and demographic rates (Borer et al, 2021, Figure 1, arrow 2). Although infection is often associated with elevated mortality, pathogens can alter ecosystem function via both sublethal, trait‐mediated effects or lethal, density‐mediated effects (Fischhoff et al, 2020; Preston et al, 2016), including decoupling elemental flows into and out of infected hosts (Frenken et al, 2021).…”

Section: The Cycle From Nutrient Supply To Host–pathogen Interactions...mentioning

confidence: 99%

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Disease‐mediated nutrient dynamics: Coupling host–pathogen interactions with ecosystem elements and energy

Borer

Paseka

Peace

et al. 2022

Ecological Monographs

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Autotrophs play an essential role in the cycling of carbon and nutrients, yet disease-ecosystem relationships are often overlooked in these dynamics. Importantly, the availability of elemental nutrients like nitrogen and phosphorus impacts infectious disease in autotrophs, and disease can induce reciprocal effects on ecosystem nutrient dynamics. Relationships linking infectious disease with ecosystem nutrient dynamics are bidirectional, though the interdependence of these processes has received little attention. We introduce disease-mediated nutrient dynamics (DND) as a framework to describe the multiple, concurrent pathways linking elemental cycles with infectious disease. We illustrate the impact of disease-ecosystem feedback loops on both disease and ecosystem nutrient dynamics using a simple mathematical model, combining approaches from classical ecological (logistic and Droop growth) and epidemiological (susceptible and infected compartments) theory. Our model incorporates the effects of nutrient availability on the growth rates of susceptible and infected autotroph hosts and tracks the return of nutrients to the environment following host death. While focused on autotroph hosts here, the DND framework is generalizable to higher trophic levels. Our results illustrate the surprisingly complex dynamics of host populations, infection patterns, and ecosystem nutrient cycling that can arise from even a relatively simple feedback between disease and nutrients. Feedback loops in disease-mediated nutrient dynamics arise via effects of infection and nutrient supply on host stoichiometry and population size. Our model illustrates how host growth rate, defense, and tissue chemistry can impact the dynamics of disease-ecosystem relationships. We use the model to motivate a review of empirical examples from autotroph-pathogen systems in aquatic and terrestrial environments, demonstrating the key role of nutrient-disease and disease-nutrient relationships in real systems. By assessing existing evidence and uncovering data gaps and apparent mismatches between model predictions and the dynamics of empirical systems, we highlight priorities for future research intended to narrow

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Section: Disease‐mediated Nutrient Dynamicsmentioning

confidence: 99%

Section: The Cycle From Nutrient Supply To Host–pathogen Interactions...mentioning

confidence: 99%

Disease‐mediated nutrient dynamics: Coupling host–pathogen interactions with ecosystem elements and energy

Borer

Paseka

Peace

et al. 2022

Ecological Monographs

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“…The availability of elements such as C, N and P is essential to all organisms and can strongly affect the interactions between primary producers and their pathogens (Huber and Haneklaus 2007, Dordas 2009, Budria 2017, Borer et al 2021). More specifically, the supply of N and P can induce positive or negative effects on pathogen prevalence and disease severity in primary producers (Bruning and Ringelberg 1987, Lacroix et al 2014, Borer et al 2016).…”

Section: A Framework To Study Impacts Of Changing Elemental Cycles On Primary Producer–pathogen Interactionsmentioning

confidence: 99%

Changing elemental cycles, stoichiometric mismatches, and consequences for pathogens of primary producers

Frenken

Paseka

Gonzalez

et al. 2021

Oikos

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Human‐induced changes in biogeochemical cycles alter the availability of carbon (C), nitrogen (N) and phosphorus (P) in the environment, leading to changes in the elemental stoichiometry of primary producers. These changes in elemental ratios may, in turn, alter the degree of stoichiometric mismatch between primary producer hosts and their pathogens. Here, we outline how ecological stoichiometry could be used as a framework to predict the effects of changing nutrient supply on stoichiometric mismatches in autotroph–pathogen interactions. We discuss empirical evidence linking pathogen performance to stoichiometric mismatches arising from shifts in elemental availability. Our synthesis indicates that fungi may be particularly sensitive to changes in N supply and viruses generally respond strongly to changes in the supply of either of these elements, but it also highlighted the need for additional data, especially for bacteria. Consequently, fungal pathogens may respond more strongly to changes in host C:N stoichiometry, whereas viruses may be highly sensitive to both changes in C:N and C:P of hosts. Additionally, our synthesis suggests that viruses may be more homeostatic than fungi, and therefore respond more strongly to changing elemental supplies. Revealing stoichiometric mismatches may greatly support our understanding of how host–pathogen interactions in primary producers will respond to changes in global biogeochemical cycles, controlling disease incidence in primary producers under scenarios of global change.

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“…For example, N enrichment can modify plantpathogen interactions (Dordas, 2009;Veresoglou et al, 2013) and interactions among different pathogens that co-infect plants (Lacroix et al, 2014;Kendig et al, 2020). The communities of pathogens that rely on plants can in turn impact plant productivity, community composition, and ecosystem processes (Lovett et al, 2010;Paseka et al, 2020;Borer et al, 2021). However, a key component of terrestrial systems-soil microbes-have been neglected in many studies of N enrichment on aboveground plant pathogens.…”

Section: Introductionmentioning

confidence: 99%

Soil microbes mediate the effects of nitrogen supply and co-inoculation on Barley Yellow Dwarf Virus inAvena sativa

Easterday

Kendig

Lacroix

et al. 2021

Preprint

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Nutrient supply rates to hosts can mediate host-pathogen interactions. In terrestrial systems, nutrient supply to plants is mediated by soil microbes, suggesting a potential indirect effect of soil microbes on plant-pathogen interactions. Soil microbes also may affect plant pathogens by inducing plant defenses. We tested the role of soil microbes, nitrogen supply to plant hosts, and co-inoculation on infection by aphid-vectored RNA viruses, Barley Yellow Dwarf Virus (BYDV-PAV) and Cereal Yellow Dwarf Virus (CYDV-RPV), in a grass host grown in soil microbes collected from a long-term nitrogen enrichment experiment. BYDV-PAV incidence declined with high nitrogen supply, co-inoculation, or presence of soil microbes exposed to long-term low nitrogen enrichment. However, when combined, the negative effects of these treatments were sub-additive: nitrogen and co-inoculation did not reduce BYDV-PAV incidence in plants grown with the soil microbes. While soil microbes impacted leaf chlorophyll, they did not alter biomass or CYDV-RPV incidence. Soil microbes mediated the effects of nitrogen supply and co-inoculation on infection incidence and the effects of infection on host symptoms. Thus, soil microbial communities can indirectly control disease dynamics, altering the effects of nitrogen enrichment on plant-pathogen and pathogen-pathogen interactions in terrestrial systems.

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Elements of disease in a changing world: modelling feedbacks between infectious disease and ecosystems

Cited by 16 publications

References 67 publications

Disease‐mediated nutrient dynamics: Coupling host–pathogen interactions with ecosystem elements and energy

Disease‐mediated nutrient dynamics: Coupling host–pathogen interactions with ecosystem elements and energy

Changing elemental cycles, stoichiometric mismatches, and consequences for pathogens of primary producers

Soil microbes mediate the effects of nitrogen supply and co-inoculation on Barley Yellow Dwarf Virus inAvena sativa

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