Temperature Drives Epidemics in a Zooplankton-Fungus Disease System: A Trait-Driven Approach Points to Transmission via Host Foraging

Shocket, Marta S.; Strauss, Alexander T.; Hite, Jessica L.; Šljivar, Maja; Civitello, David J.; Duffy, Meghan A.; Cáceres, Carla E.; Hall, Spencer R.

doi:10.1086/696096

Cited by 62 publications

(100 citation statements)

References 58 publications

(86 reference statements)

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“…Finally, simulations demonstrate that these temperature‐driven changes in transmission rate can explain why epidemics become larger when they start warmer (Shocket et al. ) and wane as lakes cool. The population model predicts that most spores are reared recently (i.e., rearing temperature ≈ exposure/infection temperature) because lakes cool gradually as spores turn over quickly.…”

Section: Discussionmentioning

confidence: 99%

“…, Shocket et al. ). Therefore, any factor inhibiting the start of epidemics, all else equal, should make them smaller via thermal effects describe here.…”

Section: Discussionmentioning

confidence: 99%

“…In this population model, traits of host and parasite (i.e., model parameters) vary as functions of temperature (modified from Shocket et al. to include rearing temperature and omit algal food resources). The model, written without traits as functions of temperatures for visual clarity, is (see also Tables and Appendix : Table ):

\frac{ds}{dt} = b false(1 - c (S + I) false) false(S + I false) - d S - u f S Z

\frac{dI}{dt} = u f S Z - d_{normali} I

\frac{dz}{dt} = d_{normali} I σ - m Z - f false(S + I false) Z

T_{normalEI} false(t false) = \frac{T_{normalmax} - T_{normalmin}}{1 + R^{t - D}} + T_{normalmin}

\frac{d T_{normalR}}{dt} = \frac{d_{normali} I σ false(T_{EI} - T_{R} false)}{z}

…”

Section: Methodsmentioning

confidence: 99%

“…, Shocket et al. ). Therefore, seasonal dynamics of epidemics could depend on a thermal rearing effect coupled with the thermal responses of these other traits.…”

Section: Study Systemmentioning

confidence: 99%

“…, , Shocket et al. ). Furthermore, spore infectivity itself may also depend on temperature at the time of exposure and during the new infection.…”

Section: Introductionmentioning

confidence: 99%

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Parasite rearing and infection temperatures jointly influence disease transmission and shape seasonality of epidemics

Shocket

Vergara

Sickbert

et al. 2018

Ecology

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Seasonal epidemics erupt commonly in nature and are driven by numerous mechanisms. Here, we suggest a new mechanism that could determine the size and timing of seasonal epidemics: rearing environment changes the performance of parasites. This mechanism arises when the environmental conditions in which a parasite is produced impact its performance-independently from the current environment. To illustrate the potential for "rearing effects", we show how temperature influences infection risk (transmission rate) in a Daphnia-fungus disease system through both parasite rearing temperature and infection temperature. During autumnal epidemics, zooplankton hosts contact (eat) fungal parasites (spores) reared in a gradually cooling environment. To delineate the effect of rearing temperature from temperature at exposure and infection, we used lab experiments to parameterize a mechanistic model of transmission rate. We also evaluated the rearing effect using spores collected from epidemics in cooling lakes. We found that fungal spores were more infectious when reared at warmer temperatures (in the lab and in two of three lakes). Additionally, the exposure (foraging) rate of hosts increased with warmer infection temperatures. Thus, both mechanisms cause transmission rate to drop as temperature decreases over the autumnal epidemic season (from summer to winter). Simulations show how these temperature-driven changes in transmission rate can induce waning of epidemics as lakes cool. Furthermore, via thermally dependent transmission, variation in environmental cooling patterns can alter the size and shape of epidemics. Thus, the thermal environment drives seasonal epidemics through effects on hosts (exposure rate) and the infectivity of parasites (a rearing effect). Presently, the generality of parasite rearing effects remains unknown. Our results suggest that they may provide an important but underappreciated mechanism linking temperature to the seasonality of epidemics.

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Section: Discussionmentioning

confidence: 99%

“…, Shocket et al. ). Therefore, any factor inhibiting the start of epidemics, all else equal, should make them smaller via thermal effects describe here.…”

Section: Discussionmentioning

confidence: 99%

\frac{ds}{dt} = b false(1 - c (S + I) false) false(S + I false) - d S - u f S Z

\frac{dI}{dt} = u f S Z - d_{normali} I

\frac{dz}{dt} = d_{normali} I σ - m Z - f false(S + I false) Z

T_{normalEI} false(t false) = \frac{T_{normalmax} - T_{normalmin}}{1 + R^{t - D}} + T_{normalmin}

\frac{d T_{normalR}}{dt} = \frac{d_{normali} I σ false(T_{EI} - T_{R} false)}{z}

…”

Section: Methodsmentioning

confidence: 99%

“…, Shocket et al. ). Therefore, seasonal dynamics of epidemics could depend on a thermal rearing effect coupled with the thermal responses of these other traits.…”

Section: Study Systemmentioning

confidence: 99%

“…, , Shocket et al. ). Furthermore, spore infectivity itself may also depend on temperature at the time of exposure and during the new infection.…”

Section: Introductionmentioning

confidence: 99%

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Parasite rearing and infection temperatures jointly influence disease transmission and shape seasonality of epidemics

Shocket

Vergara

Sickbert

et al. 2018

Ecology

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A high‐throughput method to quantify feeding rates in aquatic organisms: A case study with Daphnia

Hite

Pfenning-Butterworth

Vetter

et al. 2020

Ecology and Evolution

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Food ingestion is one of the most basic features of all organisms. However, obtaining precise—and high‐throughput—estimates of feeding rates remains challenging, particularly for small, aquatic herbivores such as zooplankton, snails, and tadpoles. These animals typically consume low volumes of food that are time‐consuming to accurately measure. We extend a standard high‐throughput fluorometry technique, which uses a microplate reader and 96‐well plates, as a practical tool for studies in ecology, evolution, and disease biology. We outline technical and methodological details to optimize quantification of individual feeding rates, improve accuracy, and minimize sampling error. This high‐throughput assay offers several advantages over previous methods, including i) substantially reduced time allotments per sample to facilitate larger, more efficient experiments; ii) technical replicates; and iii) conversion of in vivo measurements to units (mL‐1 hr‐1 ind‐1) which enables broad‐scale comparisons across an array of taxa and studies. To evaluate the accuracy and feasibility of our approach, we use the zooplankton, Daphnia dentifera, as a case study. Our results indicate that this procedure accurately quantifies feeding rates and highlights differences among seven genotypes. The method detailed here has broad applicability to a diverse array of aquatic taxa, their resources, environmental contaminants (e.g., plastics), and infectious agents. We discuss simple extensions to quantify epidemiologically relevant traits, such as pathogen exposure and transmission rates, for infectious agents with oral or trophic transmission.

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Shedding light on environmentally transmitted parasites: lighter conditions within lakes restrict epidemic size

Shaw

Hall

Overholt

et al. 2020

Ecology

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Parasite fitness depends on a successful journey from one host to another. For parasites that are transmitted environmentally, abiotic conditions might modulate the success of this journey. Here we evaluate how light, a key abiotic factor, influences spatiotemporal patterns of zooplankton disease where light varies seasonally, across lakes, and with depth in a lake. In an in situ experiment using those three sources of variation, we tested sensitivity of spores of two parasites to ambient light. Infectivity of both parasites was lower when exposed to ambient light in comparison to parasites exposed to otherwise similar conditions in the dark. The more sensitive parasite (the fungus, Metschnikowia) was damaged even under lower ambient light during late fall (November). With this differential sensitivity established, we evaluated links between light environment and natural outbreaks in lakes. Consistent with the incubations, epidemics of the less sensitive parasite (the bacterium, Pasteuria) started earlier in the fall (under higher ambient light), and both parasites had smaller outbreaks in more transparent lakes. Overall, light environment may impact the timing and size of disease outbreaks. Outbreaks could thus become exacerbated by human activities that darken waters, including lake browning associated with climate change and eutrophication.

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Temperature Drives Epidemics in a Zooplankton-Fungus Disease System: A Trait-Driven Approach Points to Transmission via Host Foraging

Cited by 62 publications

References 58 publications

Parasite rearing and infection temperatures jointly influence disease transmission and shape seasonality of epidemics

Parasite rearing and infection temperatures jointly influence disease transmission and shape seasonality of epidemics

A high‐throughput method to quantify feeding rates in aquatic organisms: A case study with Daphnia

Shedding light on environmentally transmitted parasites: lighter conditions within lakes restrict epidemic size

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