skip to main content

Attention:

The NSF Public Access Repository (NSF-PAR) system and access will be unavailable from 11:00 PM ET on Thursday, October 10 until 2:00 AM ET on Friday, October 11 due to maintenance. We apologize for the inconvenience.


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

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 (R0) 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.

 
more » « less
NSF-PAR ID:
10455902
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Ecology Letters
Volume:
24
Issue:
1
ISSN:
1461-023X
Format(s):
Medium: X Size: p. 6-19
Size(s):
p. 6-19
Sponsoring Org:
National Science Foundation
More Like this
  1. Death is a common outcome of infection, but most disease models do not track hosts after death. Instead, these hosts disappear into a void. This assumption lacks critical realism, because dead hosts can alter host–pathogen dynamics. Here, we develop a theoretical framework of carbon‐based models combining disease and ecosystem perspectives to investigate the consequences of feedbacks between living and dead hosts on disease dynamics and carbon cycling. Because autotrophs (i.e. plants and phytoplankton) are critical regulators of carbon cycling, we developed general model structures and parameter combinations to broadly reflect disease of autotrophic hosts across ecosystems. Analytical model solutions highlight the importance of disease–ecosystem coupling. For example, decomposition rates of dead hosts mediate pathogen spread, and carbon flux between live and dead biomass pools are sensitive to pathogen effects on host growth and death rates. Variation in dynamics arising from biologically realistic parameter combinations largely fell along a single gradient from slow to fast carbon turnover rates, and models predicted higher disease impacts in fast turnover systems (e.g. lakes and oceans) than slow turnover systems (e.g. boreal forests). Our results demonstrate that a unified framework, including the effects of pathogens on carbon cycling, provides novel hypotheses and insights at the nexus of disease and ecosystem ecology.

     
    more » « less
  2. Abstract

    Animals interact with and impact ecosystem biogeochemical cycling—processes known as zoogeochemistry. While the deposition of various animal materials (e.g. carcasses and faeces) has been shown to create nutrient hotspots and alter nutrient cycling and storage, the inputs from parturition (i.e. calving) have yet to be explored. We examine the effects of ungulate parturition, which often occurs synchronously during spring green‐up and therefore aligns with increased plant nitrogen demand in temperate biomes.

    Impacts of zoogeochemical inputs are likely context‐dependent, where differences in material quality, quantity and the system of deposition modulate their impacts. Plant mycorrhizal associations, especially, create different nutrient‐availability contexts, which can modify the effects of nutrient inputs. We, therefore, hypothesize that mycorrhizal associations modulate the consequences of parturition on soil nutrient dynamics and nitrogen pools.

    We established experimental plots that explore the potential of two kinds of zoogeochemical inputs deposited at ungulate parturition (placenta and natal fluid) in forest microsites dominated by either ericoid mycorrhizal (ErM) or ectomycorrhizal (EcM) plants. We assess how these inputs affect rates of nutrient cycling and nitrogen content in various ecosystem pools, using isotope tracers to track the fate of nitrogen inputs into plant and soil pools.

    Parturition treatments accelerate nutrient cycling processes and increase nitrogen contents in the plant leaf, stem and fine root pools. The ecosystem context strongly modulates these effects. Microsites dominated by ErM plants mute parturition treatment impacts on most nutrient cycling processes and plant pools. Both plant–fungal associations are, however, equally efficient at retaining nitrogen, although retention of nitrogen in the parturition treatment plots was more than two times lower than in control plots.

    Our results highlight the potential importance of previously unexamined nitrogen inputs from animal inputs, such as those from parturition, in contributing to fine‐scale heterogeneity in nutrient cycling and availability. Animal inputs should therefore be considered, along with their interactions with plant mycorrhizal associations, in terms of how zoogeochemical dynamics collectively affect nutrient heterogeneity in ecosystems.

     
    more » « less
  3. Abstract

    The spread of many diseases depends on the demography and dispersal of arthropod vectors. Classic epidemiological theory typically ignores vector dynamics and instead makes the simplifying assumption of frequency‐dependent transmission. Yet, vector ecology may be critical for understanding the spread of disease over space and time and how disease dynamics respond to environmental change.

    Here, we ask how environmental change shapes vector demography and dispersal, and how these traits of vectors govern the spatiotemporal spread of disease.

    We developed disease models parameterised by traits of vectors and fit them to experimental epidemics. The experiment featured a viral pathogen (CYDV‐RPV) vectored by aphidsRhopalosiphum padiamong populations of grass hostsAvena sativaunder two rates of environmental resource supply (i.e. fertilisation of the host). We compared anon‐spatialmodel that ignores vector movement, alagged dispersalmodel that emphasises the delay between vector reproduction and dispersal, and atravelling wavemodel that generates waves of infections across space and time.

    Resource supply altered both vector demography and dispersal. Thelagged dispersalmodel fit best, indicating that vectors first reproduced locally and then dispersed globally among hosts in the experiment. Elevated resources decreased vector population growth rates, nearly doubled their carrying capacity per host, increased dispersal rates when vectors carried the virus, and homogenised disease risk across space.

    Together, the models and experiment show how environmental eutrophication can shape spatial disease dynamics—for example, homogenising disease risk across space—by altering the demography and behaviour of vectors.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less
  4. Abstract

    Anthropogenic activities have altered historical disturbance regimes, and understanding the mechanisms by which these shifting perturbations interact is essential to predicting where they may erode ecosystem resilience. Emerging infectious plant diseases, caused by human translocation of nonnative pathogens, can generate ecologically damaging forms of novel biotic disturbance. Further, abiotic disturbances, such as wildfire, may influence the severity and extent of disease‐related perturbations via their effects on the occurrence of hosts, pathogens and microclimates; however, these interactions have rarely been examined.

    The disease ‘sudden oak death’ (SOD), associated with the introduced pathogenPhytophthora ramorum, causes acute, landscape‐scale tree mortality in California's fire‐prone coastal forests. Here, we examined interactions between wildfire and the biotic disturbance impacts of this emerging infectious disease. Leveraging long‐term datasets that describe wildfire occurrence andP. ramorumdynamics across the Big Sur region, we modelled the influence of recent and historical fires on epidemiological parameters, including pathogen presence, infestation intensity, reinvasion, and host mortality.

    Past wildfire altered disease dynamics and reduced SOD‐related mortality, indicating a negative interaction between these abiotic and biotic disturbances. Frequently burned forests were less likely to be invaded byP. ramorum, had lower incidence of host infection, and exhibited decreased disease‐related biotic disturbance, which was associated with reduced occurrence and density of epidemiologically significant hosts. Following a recent wildfire, survival of mature bay laurel, a key sporulating host, was the primary driver ofP. ramoruminfestation and reinvasion, but younger, rapidly regenerating host vegetation capable of sporulation did not measurably influence disease dynamics. Notably, the effect ofP. ramoruminfection on host mortality was reduced in recently burned areas, indicating that the loss of tall, mature host canopies may temporarily dampen pathogen transmission and ‘release’ susceptible species from significant inoculum pressure.

    Synthesis. Cumulatively, our findings indicate that fire history has contributed to heterogeneous patterns of biotic disturbance and disease‐related decline across this landscape, via changes to the both the occurrence of available hosts and the demography of epidemiologically important host populations. These results highlight that human‐altered abiotic disturbances may play a foundational role in structuring infectious disease dynamics, contributing to future outbreak emergence and driving biotic disturbance regimes.

     
    more » « less
  5. Abstract

    Globally, anthropogenic pressures are reducing the abundances of marine species and altering ecosystems through modification of trophic interactions. Yet, consumer declines also disrupt important bottom‐up processes, like nutrient recycling, which are critical for ecosystem functioning. Consumer‐mediated nutrient dynamics (CND) is now considered a major biogeochemical component of most ecosystems, but lacking long‐term studies, it is difficult to predict how CND will respond to accelerating disturbances in the wake of global change. To aid such predictions, we coupled empirical ammonium excretion rates with an 18‐year time series of the standing biomass of common benthic macroinvertebrates in southern California kelp forests. This time series of excretion rates encompassed an extended period of extreme ocean warming, disease outbreaks, and the abolishment of fishing at two of our study sites, allowing us to assess kelp forest CND across a wide range of environmental conditions. At their peak, reef invertebrates supplied an average of 18.3 ± 3.0 µmol NH4+ m−2 hr−1to kelp forests when sea stars were regionally abundant, but dropped to 3.5 ± 1.0 µmol NH4+ m−2 hr−1following their mass mortality due to disease during a prolonged period of extreme warming. However, a coincident increase in the abundance of the California spiny lobster,Palinurus interupptus(Randall, 1840), likely in response to both reduced fishing and a warmer ocean, compensated for much of the recycled ammonium lost to sea star mortality. Both lobsters and sea stars are widely recognized as key predators that can profoundly influence community structure in benthic marine systems. Our study is the first to demonstrate their importance in nutrient cycling, thus expanding their roles in the ecosystem. Climate change is increasing the frequency and severity of warming events, and rising human populations are intensifying fishing pressure in coastal ecosystems worldwide. Our study documents how these projected global changes can drive regime shifts in CND and fundamentally alter a critical ecosystem function.

     
    more » « less