Disease-mediated ecosystem services: Pathogens, plants, and people

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

doi:10.1016/j.tree.2020.04.003

Cited by 55 publications

(32 citation statements)

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“…For example, fungal infection can induce large reductions in biomass accumulation in forests and grasslands (Seabloom et al ., 2017; Fei et al ., 2019). These effects are not likely to remain constant with global change; increasing elemental nutrient supply to ecosystems (Steffen et al ., 2015), for example, can lead to increasing, decreasing or nonlinear changes in infection severity, pathogen spread and host mortality in plants (Dordas, 2008; Fones and Gurr, 2017; Paseka et al ., 2020). These impacts of infection can persist beyond host death as legacy effects of disease by inducing changes in plant nutrient and defensive chemistry that either speed up or slow down nutrient recycling (Jackrel et al ., 2019; Pazianoto et al ., 2019).…”

Section: An Integrated Modelling Approachmentioning

confidence: 99%

“…Currently, models in disease ecology rarely track organisms past death, yet death from infection can alter elemental recycling and nutrient supply to living hosts (Ruardij et al ., 2005; Suttle, 2007). Thus, both disease and ecosystem ecology stand to grow as fields by exploring questions that arise at their intersection, including disease impacts on the cycling of carbon (C) and elemental nutrients (Preston et al ., 2016; Fischhoff et al ., 2020; Paseka et al ., 2020), and the role of death and nutrient recycling in disease dynamics.…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2020

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An overlooked effect of ecosystem eutrophication is the potential to alter disease dynamics in primary producers, inducing disease-mediated feedbacks that alter net primary productivity and elemental recycling. Models in disease ecology rarely track organisms past death, yet death from infection can alter important ecosystem processes including elemental recycling rates and nutrient supply to living hosts. In contrast, models in ecosystem ecology rarely track disease dynamics, yet elemental nutrient pools (e.g. nitrogen, phosphorus) can regulate important disease processes including pathogen reproduction and transmission. Thus, both disease and ecosystem ecology stand to grow as fields by exploring questions that arise at their intersection. However, we currently lack a framework explicitly linking these disciplines. We developed a stoichiometric model using elemental currencies to track primary producer biomass (carbon) in vegetation and soil pools, and to track prevalence and the basic reproduction number (R 0) of a directly transmitted pathogen. This model, parameterised for a deciduous forest, demonstrates that anthropogenic nutrient supply can interact with disease to qualitatively alter both ecosystem and disease dynamics. Using this element-focused approach, we identify knowledge gaps and generate predictions about the impact of anthropogenic nutrient supply rates on infectious disease and feedbacks to ecosystem carbon and nutrient cycling.

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Section: An Integrated Modelling Approachmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

et al. 2020

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“…Parasites, which are supposed to account for half of the species richness, could make up the unseen majority of species extinctions (Carlson et al ., 2017). Majority of parasites have essential ecological roles by contributing to the resilience of ecosystems, limiting the invasion and emerging of infectious diseases, and being critical to the biomass transfer between trophic levels (Johnson et al ., 2013; Dougherty et al ., 2016; Paseka et al ., 2020). In marine ecosystems, parasites have a predominant role in the planktonic protists interactome inferred by sequence-based correlation networks (Lima-Mendez et al ., 2015) and can represent up to 18% of interactions (Bjorbækmo et al ., 2020).…”

Section: Introductionmentioning

confidence: 99%

Dinophyceae use exudates as weapons against the parasiteAmoebophryasp. (Syndiniales)

Long

Marie

Szymczak

et al. 2021

Preprint

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SummaryParasites of the genus Amoebophrya sp. are important contributors to marine ecosystems and can be determining factors in the demise of blooms of Dinophyceae, including microalgae commonly responsible for toxic red tides. Yet they rarely lead to the total collapse of Dinophyceae blooms. The addition of resistant Dinophyceae (Alexandrium minutum or Scrippsiella donghaienis) or their exudate into a well-established host-parasite culture (Scrippsiella acuminata-Amoebophrya sp.) mitigated the success of the parasite and increased the survival of the sensitive host. Effect were mediated via water-borne molecules without the need of a physical contact. Severity of the anti-parasitic defenses fluctuated depending on the species, the strain and its concentration, but never totally prevented the parasite transmission. The survival time of Amoebophrya sp. free-living stages (dinospores) decreased in presence of A. minutum but not of S. donghaienis. The progeny drastically decreased with both species. Integrity of the membrane of dinospores was altered by A. minutum which provided a first indication on the mode of action of these anti-parasitic molecules. These results demonstrate that extracellular defenses are an effective strategy against parasites that does not only protect the resistant cells but also have the potential to affect the whole surrounding community.

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“…Because within-host parasite accumulation is often directly or indirectly linked to between-host transmission [23,38], microbial mutualists may be important drivers of epidemiological dynamics, which can have impacts on ecosystem function [39,40]. Yet, our understanding of how microbial mutualists impact disease dynamics is mostly based on investigations of pairwise interactions.…”

Section: Introductionmentioning

confidence: 99%

Higher-order interactions among coinfecting parasites and a microbial mutualist impact disease progression

Simha

Mitchell

2021

Preprint

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Interactions among parasites and other microbes within hosts can impact disease progression, yet study of such interactions has been mostly limited to pairwise combinations of microbes. Given the diversity of microbes within hosts, higher-order interactions among more than two microbial species may also impact disease. To test this hypothesis, we performed inoculation experiments that investigated interactions among two fungal parasites, Rhizoctonia solani and Colletotrichum cereale, and a systemic fungal endophyte, Epichloê coenophiala, within a grass host. Both pairwise and higher-order interactions impacted disease progression. While the endophyte did not directly influence R. solani growth or C. cereale symptom development, the endophyte modified the interaction between the two parasites. The magnitude of the facilitative effect of C. cereale on the growth of R. solani tended to be greater when the endophyte was present. Moreover, this interaction modification strongly affected leaf mortality. For plants lacking the endophyte, parasite co-inoculation did not increase leaf mortality compared to single-parasite inoculations. In contrast, for endophyte-infected plants, parasite co-inoculation increased leaf mortality compared to inoculation with R. solani or C. cereale alone by 1.9 or 4.9 times, respectively. Together, these results show that disease progression can be strongly impacted by higher-order interactions among microbial symbionts.

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Disease-mediated ecosystem services: Pathogens, plants, and people

Cited by 55 publications

References 100 publications

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

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

Dinophyceae use exudates as weapons against the parasiteAmoebophryasp. (Syndiniales)

Higher-order interactions among coinfecting parasites and a microbial mutualist impact disease progression

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