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Electronic Supplemental Information – Disease ecology meets ecosystem science by D. L.

Preston, J. A. Mischler, A. R. Townsend and P. T. J. Johnson

Methods and Results for Empirical Literature Searches

Figure 1: “The divide between disease ecology and ecosystem science”

We conducted two literature searches using the Web of Science database to quantify 1)

the proportion of disease ecology publication that involve different levels of ecological

organization (that is, host, population, community and ecosystem) and 2) the proportion of

ecosystem ecology publications that involve different types of ecological interactions (that is,

herbivory, predation, competition, parasitism and mutualism). We focused on publications from

1980 to 2013 because we found no ecosystem-disease publications before that date, and we

restricted the search to the Ecology section of the Web of Science database because this produced

the most relevant publications (for example, omitting publications on human medicine). The aims

of our searches were to compare the relative proportion of publications, rather than the absolute

values. Our search strings were established to minimize the numbers of papers that do not fit the

aims of each search, and to avoid biases between different levels of ecological organization or

different types of species interactions. As a result, the number of publications is likely

conservative because it misses papers that do not contain the keywords used. We first conducted

the following title key word search to identify publications in disease ecology: TI=(parasit* OR

disease* OR pathog* OR infect*) AND WC = (ecology). We then combined that search with

each of the following searches that identified publications with title keywords involving different

levels of ecological organization: [TI = (host*) AND WC = (ecology)], [TI = (population*) AND

WC = (ecology)], [TI = (communit*) AND WC = (ecology)], and [TI = (ecosystem*) AND WC

= (ecology)]. To standardize for increases in the number of disease ecology publications over

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time, we then divided the number of publications at each level of ecological organization per year

by the total number disease ecology publications per year. To examine whether the resulting

yearly proportions of disease ecology publications at each level of organization changed over

time (from 1980 to 2013) we used generalized additive models that allowed nonlinear

relationships and accounted for temporal autocorrelation. We used AIC comparisons of multiple

models to determine whether smoothing, autoregressive or moving average terms improved fit

over simple linear models (after Altizer and others 2013). We used the mgcv and nlme packes in

R for the analyses (R Core Team 2013).

For the second literature search we used a similar approach by first identifying

publications that involved ecosystem ecology using the following search string: TI=((ecosystem

AND (function* OR process* OR propert* OR structure OR stability OR dynamic* OR service*

OR engineer* OR disturbance* OR energ* OR change* OR diversity)) OR succession OR

biogeochem* OR ((nutrient* OR nitrogen OR phosphorus OR carbon OR element*) AND (cycl*

OR recycl* OR flux* OR dynamic*)) OR decomposition OR (energ* AND (flow* OR flux* OR

dynamic*)) OR (product* AND (biomass OR primary OR secondary)) OR (change* AND

(global OR environmental))) AND WC = (ecology). We then combined the above search string

with additional searches that identified publications that included specific types of ecological

interactions in their titles: [TI = (predat*) AND WC = (ecology)], [TI = (compet*) AND WC =

(ecology)], [TI = (herbiv* OR graz*) AND WC = (ecology)], [TI = (mutual*) AND WC =

(ecology)], and [TI = (parasit*) AND WC = (ecology)]. To maintain consistency with the disease

ecology search, we restricted the results to publications between 1980 and 2013. We determined

that using a simple search term for each level of ecological organization or type of species

interaction was the most efficient method to ensure there were not major differences in the

efficiency of our search strings. Although this likely makes our total number of publications

conservative, it ensure there is little bias in the results.

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The disease ecology search string returned 8,466 total papers. Publications with the term

‘ecosystem’ were less common than all other levels of ecological organization. We present the

proportion of publications that involved different levels of ecological organization in two ways:

the total proportion from 1980 to 2013 (Figure 1a) and the yearly proportion, which allowed

visualizing trends over time (Figure 1b). For ease of presentation, these data were binned at two-

year intervals in the figure (but not for analyses). For the host, community, and ecosystem level,

simple linear models performed better than generalized additive models in evaluating time trends

in the proportion of publications. The proportion of disease ecology publications between 1980

and 2013 did not change significantly at the host level (GLM, p = 0.141) or the population level

(GAM, p = 0.786). In contrast, the proportion of publications at the community level (GLM, p <

0.001) and the ecosystem level (GLM, p = 0.026) increased significantly from 1980 to 2013

(Figure 1b).

The second search identified 11,680 total ecosystem ecology publications and

reinforced the finding that papers linking ecosystems and disease are uncommon. However, we

note that all of the species interaction terms were relatively uncommon in the titles of ecosystem

ecology publications. Papers that involved herbivory were considerably more common than the

other interaction types, at 2.6% of the total (Figure S1). Parasitism was less common than

herbivory, predation or competition, but was more common than mutualism.

Figure S2: “Patterns in existing ecosystem and disease research”

To examine patterns in published studies linking ecosystem science and disease ecology,

we first identified papers that quantified how parasites affected ecosystems, specifically focusing

on ecosystem structure, biogeochemistry, energy flow, and temporal ecosystem dynamics. We

initially filtered publications that were found with the aforementioned searches used to generate

results shown in Figure 1. This included the Web of Science searches of disease ecology papers at

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the ecosystem level and of ecosystem science papers that involved host/parasite interactions

(described above). We included only primary literature where the authors directly quantified

effects of parasitism and disease. We omitted most publications that focused on community

structure or food webs, as these topics focus on community ecology. We also omitted review

papers that appeared in those searches, but included papers from their literature cited that fit our

criteria. After identifying an initial list of publications, we then searched the literature cited of

those papers to identify additional relevant publications. Lastly, we performed additional focused

searches using Google Scholar to make the dataset more complete (using the search terms

“ecosystem” and “disease” or “parasite”). Among the papers that met our criteria, we extracted

information on six variables: the type of ecosystem (forest, freshwater, marine, grassland or

other), the ecosystem property affected (biogeochemistry, ecosystem structure, energy flow, or

temporal ecosystem dynamics), the approach used in the study (observational, experimental,

modeling, or a combination), the mechanism underlying ecosystem effects of parasites (density-

mediated indirect, trait-mediated indirect or direct effect), and the taxa of hosts and parasites.

We identified a total of 39 publications where the effects of parasites on ecosystem

structure and function were quantified. The full citations and the information extracted are

provided in Table S1. Figure S2 shows the observed patterns in mechanisms, ecosystem types,

ecosystem properties and approaches used. The patterns in host and parasite taxa are shown in

Figure S3.

References

Altizer SA, Ostfeld RS, Johnson PTJ, Kutz S, Harvell CD. 2013. Climate

change and infectious diseases: from evidence to a predictive framework. Science

341: 514-519.

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R Core Team. 2013. R: A language and environment for statistical computing. R

Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-

project.org/.

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http://www.R-

Supplemental Figures and Tables

Figure S1. The percentage of ecosystem ecology publications (1980 to 2013) that include title

keywords for different types of species interactions.

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Figure S2. Patterns in mechanisms, ecosystem properties studied, approaches used and

ecosystem types from 39 publications that quantified how parasites affected some aspect of

ecosystem structure or function.

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Figure S3. Patterns in host and parasite taxa from 39 publications that quantified cases where

parasites affected ecosystem structure or function.

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Table S1. Published Studies Quantifying the Effects of Parasites on Ecosystem Structure and Function

Ecosystem Property

Ecosystem Type

Host/Parasite System

Mechanism Approach Ecosystem Effects

Citation

Ecosystem Structure

Abiotic Structure Intertidal mud flat

Amphipods and trematode worms

Host density regulation

Observational field study

Amphipod declines increase sediment particle sizes and erosion rates.

Mouritsen and others 1998. Journal of the Marine Biological Association of the United Kingdom.

Temperate forest

Chesnut trees and fungal pathogens



Loss of chesnut trees has altered soil properties, including carbon and nitrogen content.

Rhoades 2007. Pedobiologia.

Biotic Structure Temperate forest

Rabbits and myxoma virus



Rabbit declines facilitate shifts from grassland to forest ecosystems.

Sumption and Flowerdew 1985. Mammal Review.

Marine estuary

Marsh plants and hemiparasitic plants



Parasitic plants alter patterns of plant composition, which forms ecosystem structure.

Pennings and Callaway 1996. Ecology.

Intertidal mud flat

Cockles and trematode worms

Alteration of host traits

Observation and experiment

Trematodes impair cockle burrowing ability, altering the role of an ecosystem engineer.

Thomas and others 1998. Proceedings of the Royal Society, B.

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Rocky intertidal shore

Snails and trematode worms


Experiment Trematodes alter rates of snail grazing leading to changes in macroalgae structure.

Wood and others 2007. Proceedings of the National Academy of Sciences.

Alpine forest

White park pine and fungal pathogens



White pine blister rust affects the formation of tree islands at treeline.

Resler and Tomback. 2008. Arctic, Antartic and Alpine Research.

Temperate forest

Oak trees and root fungal pathogens


Observation and modelling

Oak tree declines cause changes in forest structure, including tree size distribution and abudnance of standing dead trees.

Cobb and others 2012. Journal of Ecology.

Temperate forest

Oak trees and root fungal pathogens



Sudden oak death drives course woody debris dynamics within the forest.

Cobb and others 2012. Ecosystems.

Biogeochemistry

Carbon Cycling Grassland Wildebeest and rinderpest virus


Modelling Eradication of rinderpest leads to increases in tree density and net carbon storage.

Holdo and others 2009. PLoS Biology.

Nutrient Cycling Open ocean Marine bacteria and viruses


Experiment Lysis of bacterial cells by viruses releases bioavailable iron used by phytoplankton.

Poorvin and others 2004. Limnology and Oceanography.

Grassland Grassland plants and hemiparasitic plants


Experiment Hemiparasites change soil microbial composition leading to increased rates of nitrogen cycling.

Bardgett and others 2006. Nature.

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River floodplain

Fungal pathogens and alder trees



Reductions in tree density have led to reductions in nitrogen fixation.

Ruess and others 2009. Ecosystems.

Temperate forest

Beech trees and pathogenic fungi



Shifts from beech to other tree species have altered nitrogen cycling.

Lovett and others 2010. Ecosystems.

Tropical

streamAmphibians and chytrid fungi


Experiment The loss of tadpoles reduces rates of nitrogen cycling.

Whiles and others 2013. Ecosystems.

Temperate stream

Snails and trematode worms


Experiment Trematode infection alter rates of host nutrient excretion.

Bernot and others 2013. Freshwater Science.

Decomposition Temperate stream

Chesnut trees and fungal pathogens


Experiment Chestnut leaves were processed at different rates than replacement species, leading to changes in decomposition.

Smock and MacGregor 1988. Journal of the North American Benthological Society.

Sub-arctic heathland

Plants and hemiparasitic plants

Direct effect of parasites


Hemiparasites are enriched in nutrients and accelerate litter decomposition.

Quested and others 2002. Oecologia.

Temperate stream

Isopods and acanthocephalan worms



Acanthocephalan infection reduces rates of litter breakdown by isopods.

Hernandez and Sukhdeo 2008. International Journal for Parasitology.

Temperate forest

Mistletoe and eucalyptus trees



Mistletoe litterfall alters phosphorus and trace element cycling on the forest floor.

March and Watson 2010. Austral Ecology.

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Alpine tundra

Alpine plants and hemiparasitic plants



Hemiparasites accelerate rates of litter decomposition and increase available nitrogen.

Spasojevic and Suding 2011. Oecologia.

Temperate stream

Maple trees and foliar fungal pathogens


Experiment Fungal infection delays decomposition rates of leaves within streams.

Grimmett and others 2012. Freshwater Science.

Temperate forest

Dung beetles and nematodes


Experiment Nematode infection reduces rates of feces consumption by host beetles, leading to changes in decomposition.

Boze and others 2012. Journal of Insect Behavior.

Energy Flow

Primary Production

Open ocean Phytoplankton and viruses


Experiment Viruses reduce primary production by up to 78%.

Suttle and others 1990. Nature.

Temperate stream

Caddisflies and microsporidian parasites



Caddisfly declines result in increases in benthic primary production.

Kohler and Wiley 1997. Ecology.

Grassland Plants and foliar fungal pathogens


Experiment Foliar fungal pathogens strongly reduce grassland primary production.

Mitchell 2003. Ecology Letters.

Marine estuary

Cockles and trematode worms


Experiment Infection causes cockles to alter habitat such that local primary production and secondary production increases.

Mouritsen and Poulin 2006. Journal of the Marine Biological Association of the United Kingdom.

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Tropical stream

Amphibians and chytrid fungi


Experiment Amphibian declines lead to changes in benthic primary production.

Connely and others 2008. Ecosystems.

Grassland Grassland plants and soil fungal pathogens


Experiment Soil pathogens alter relationships between plant species richness and productivity.

Maron and others 2011. Ecology Letters.

Secondary Production

Marine estuary

Multiple hosts and parasites



Parasite biomass equals or exceeds many free-living groups, including birds.

Kuris and others 2008. Nature.

Freshwater pond

Multiple hosts and trematode worms



Trematode biomass equals or exceeds many free-living groups, including most insects.

Preston and others 2013. Journal of Animal Ecology.

Ecosystem Subsidies

Freshwater stream/ temperate forest

Crickets and nematomorph worms



Infected crickets provde a large energetic subsidy to enter streams.

Sato and others 2011. Ecology.

Freshwater stream/ temperate forest

Crickets and nematomorph worms


Experiment Eliminating cricket subsides led to cascading effects on benthic invertebrates, primary production, and decomposition.

Sato and others 2012. Ecology Letters.

Temporal Dynamics

Succession Freshwater lake

Phytoplankton and chytrid fungi



Chytrid infection accelerates phytoplankton succession.

Van Donk and Ringleberger 1983. Freshwater Biology.

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Sand dune Plants and soil pathogens


Experiment Soil pathogens control plant competition and patterns of sucession.

Van der Putten and others 1993. Nature.

Temperate forest

Dougals fir trees and root-rot fungi



A fungal pathogen acellerates sucession by supressing early successional tree species.

Holah and others 1997. Oecologia.

Stability Coral reef Sea urchins and microbial pathogens



Extirpations of urchins facilitates macroalgae and eliminates coral recruitment, lowering reef resilience.

Lessios 1988. Annual Review of Ecology and Systemtics.

Kelp forest Sea urchins and microbial pathogens



Extirpations of urchins leads to shift from urchin barrens to kelp forest.

Scheibling 1986. Oecologia.

Invasibility Grassland Grassland plants and viruses


Modeling The presence of viruses is necessary to allow invasion success of annual grasses in California.

Borer and others 2007. Proceedings of the National Academy of Sciences.

For each publication, we report the ecosystem property that is affected, the type of ecosystem, the host/parasite system, the mechanism through

which parasites exert ecosystem effects (that is, density-mediated indirect effects, trait-mediated indirect effects, or direct effects), the approach

used in the study (observational field study, experiment or modeling), and a description of the effects that were observed.

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Table S2. Traits of the Host, the Parasite, Their Interaction, and the Ecosystem that are Predicted to Affect the Magnitude and Scale of Ecosystem Effects of Disease

Traits Prediction and Rationale

Parasite Pathogenicity and virulence Disease severity is determined in part by parasite traits and can mediate the strength of indirect effects.

Host manipulation Manipulators alter host behavior, morphology, and physiology, increasing the potential for trait-mediated effects.

Host castration Castrators eliminate host reproduction, potentially inducing density-mediated effects.

Introduced vs. native Introduced parasites are most likely to cause epizootics, increasing the potential for density-mediated effects.

Transmission mode Directly transmitted, frequency dependent parasites may increase the potential for density-mediated effects.

Body size and productivity Large and productive parasites can exert direct effects on energy and matter flows.

Host Functional role Unique host functional roles (for example, ability to cycle nutrients) enhance the potential for ecosystem effects.

Abundance Dominant host species with a high density are most likely to facilitate ecosystem roles of parasites.

Physical structure Hosts that are ecosystem engineers (for example, trees and corals) will mediate parasite-driven changes in ecosystem structure.

Interaction strengths Hosts that are keystone species by virtue of their interactions (for example, predation) enhance the potential for ecosystem effects.

Trophic position Hosts that exert top-down or bottom-up effects may enhance the potential for ecosystem roles of parasites.

Introduced vs. native Introduced hosts can strongly alter ecosystems, enhancing the potential for ecosystem effects.

Resistance and tolerance Disease severity is determined in part by host resistance and tolerance, and can mediate the strength of indirect effects.

Interaction

Host outcome Greater host damage or mortality will increase the potential for ecosystem effects.

Infection prevalence and intensity

Increasing prevalence and intensity should increase the potential for ecosystem effects.

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Transmission rate High transmission rates may contribute to ecosystem effects.

Geographic extent of the infection

The larger area over which hosts are affected, the larger the potential scale of ecosystem effects.

Co-evolutionary history A long co-evolutionary history can lead to lower virulence and host adaptation, decreasing the potential for ecosystem effects.

Coinfection Coinfection may increase or decrease ecosystem effects, depending on host responses and parasite interactions.

Ecosystem

Biotic vs. abiotic controls over process rates

Biota must control aspects of ecosystem functioning for parasites to have important roles in ecosystem processes.

Biotic vs. abiotic controls over physical structure

Biota must control aspects of ecosystem structure for parasites to have important roles in ecosystem structure.

Complexity Complex ecosystems with many species interactions can buffer changes due to single species.

Resilience, resistance and robustness

More stable ecosystems may diminish the potential for some ecosystem roles of parasites.

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