Abstract
Fungal diseases threaten natural and man‐made ecosystems. Chytridiomycota (chytrids) infect a wide host range, including phytoplankton species that form the basis of aquatic food webs and produce roughly half of Earth's oxygen. However, blooms of large or toxic phytoplankton form trophic bottlenecks, as they are inedible to zooplankton. Chytrids infecting inedible phytoplankton provide a trophic link to zooplankton by producing edible zoospores of high nutritional quality. By grazing chytrid zoospores, zooplankton may induce a trophic cascade, as a decreased zoospore density will reduce new infections. Conversely, fewer infections will not produce enough zoospores to sustain long‐term zooplankton growth and reproduction. This intricate balance between zoospore density necessary for zooplankton energetic demands (growth/survival), and the loss in new infections (and thus new zoospores) because of grazing was tested empirically. To this end, we exposed a cyanobacterial host (Planktothrix rubescens) infected by a chytrid (Rizophydium megarrhizum) to a grazer density gradient (the rotifer Keratella cf. cochlearis). Rotifers survived and reproduced on a zoospore diet, but the Keratella population growth was limited by the amount of zoospores provided by chytrid infections, resulting in a situation where zooplankton survived but were restricted in their ability to control disease in the cyanobacterial host. We subsequently developed and parameterized a dynamical food‐chain model using an allometric relationship for clearance rate to assess theoretically the potential of different‐sized zooplankton groups to restrict disease in phytoplankton hosts. Our model suggests that smaller‐sized zooplankton may have a high potential to reduce chytrid infections on inedible phytoplankton. Together, our results point out the complexity of three‐way interactions between hosts, parasites, and grazers and highlight that trophic cascades are not always sustainable and may depend on the grazer's energetic demand.
Highlights
Fungal parasites are among the most virulent emerging diseases and are expected to threaten both naturalManuscript received 22 February 2019; revised 18 July 2019; accepted 26 August 2019
We developed a dynamical food-chain model to test the maximum potential of Keratella to suppress the level of chytrid infection on an inedible phytoplankton host
We hypothesized that increasing zooplankton grazing intensity will lower chytrid zoospore density, resulting in a decreased prevalence of infection
Summary
Fungal parasites are among the most virulent emerging diseases and are expected to threaten both naturalManuscript received 22 February 2019; revised 18 July 2019; accepted 26 August 2019. Many bloom-forming phytoplankton species are large-sized and filamentous; they may be toxin producers, which makes them less suitable food for zooplankton (Lampert 1987, Turner and Tester 1997). Chytrids that infect these inedible phytoplankton species, make organic compounds available to zooplankton by producing edible transmission stages (zoospores). Chytrid zoospores can reach densities of over 1,000/mL and are of a high nutritional quality, as they contain essential fatty acids and sterols (Kagami et al 2007b, 2014, Jobard et al 2010, Gerphagnon et al 2018). The mycoloop has been tested with various zooplankton species, including rotifers, cladocerans, and copepods, and feeding on zoospores has been shown to facilitate zooplankton survival or even allow population growth (Kagami et al 2007b, 2011, Searle et al 2013, Schmeller et al 2014, Agha et al 2016, Frenken et al 2016, 2018)
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