Chytrid infections and diatom spring blooms: paradoxical effects of climate warming on fungal epidemics in lakes

Abstract

1. We describe the dynamics of host-parasite interactions over a period of more than 30 years between the freshwater diatom Asterionella formosa and two highly virulent chytrid parasites (Rhizophydium planktonicum and Zygorhizidium planktonicum) in Lake Maarsseveen, The Netherlands. This period is characterised by a significant warming trend which is strongest in spring. 2. The key spring event in lakes, the diatom bloom, was in many years dominated by Asterionella. We examine whether and how climate warming has affected the prevalence of infection in Asterionella by chytrids. 3. In years with cold winters/early springs, a dense Asterionella bloom is followed by epidemic development of disease as high Asterionella densities greatly facilitate transmission of chytrid zoospores. This sequence of events is absent in milder winters. 4. Earlier experimental studies have shown that the parasite is almost non-infective at water temperatures below 3 degrees C, offering a disease-free window of opportunity for growth of Asterionella. Climate warming has reduced periods in which water temperature remains < 3 degrees C, narrowing the window of opportunity for uninfected growth. Consequently, Asterionella continuously suffers from infection, albeit at low levels. 5. Population reduction as a result of low level infection allows other diatoms to take over as dominant species, possibly through priority effects. 6. In mild winters, chytrid infections no longer reach epidemic levels, but remain at low prevalence since transmission is impaired at low host densities. Climate warming thus affects both host and parasite in intricate ways, with the host denied a bloom and consequently the parasite denied an epidemic. 7. A shift from Asterionella to a mixed diatom community in years with mild winters may benefit the food web, because of the poor edibility of Asterionella, unless the numerous chytrid zoospores produced during epidemics significantly contribute to zooplankton nutrition. 8. Our study demonstrates the potential complexity of climate change impacts on disease. A reduction in the likelihood of epidemic development of a virulent parasite would seem to be of great benefit to the host, but this was not the case. Unexpected, sometimes paradoxical consequences of climate change can be expected and suggest that the view of a 'warmer hence sicker world' may not always apply

Parasitic infection of the diatom Guinardia delicatula, a recurrent and ecologically important phenomenon on the New England Shelf

“…2 & 5). Interestingly, this conclusion is similar to findings of Ibelings et al (2011), who studied chytrid parasites of the diatom Asterionella formosa in a freshwater lake; in that system, they observed almost no infection at water temperatures < 3°C, and corresponding evidence for boom− bust cycles of host and parasite only in years with cold winters or early spring periods. Diatom blooms are expected to be influenced by a variety of processes, notably those that control availability of light and nutrients as they impact growth physiology and those that control interactions with predators of different types.…”

“…Parasitic interactions in the phytoplankton may be common and varied (Van Donk 1989, Coats & Park 2002, Park et al 2004, Montagnes et al 2008, Gachon et al 2010, Ibelings et al 2011), but they have been difficult to study in a quantitative manner in natural systems. We have taken advantage of a cabled observatory facility (MVCO) to carry out extended time series observations with IFCB of a particular parasite− host relationship in waters of the New England Shelf.…”

“…Parasites and pathogens that are known to impact a wide variety of phytoplankton hosts include viruses documented to restrict or terminate Phaeocystis blooms (Brussaard et al 2005), fungi that can influence bloom dynamics and succession in dia toms (Ibelings et al 2011, Sime-Ngando 2012, dinoflagellates that infect other dinoflagellates (Coats & Park 2002, and bacteria that infect dinoflagellates and may be useful for toxic bloom control (Kim et al 2008). Most knowledge of ABSTRACT: Plankton images collected by Imaging FlowCytobot from 2006 to 2013 at the Martha's Vineyard Coastal Observatory (Massachusetts, USA) were used to identify and quantify the occurrence of the diatom Guinardia delicatula and of a parasite that seems specific to this host.…”

Chytrid epidemics may increase genetic diversity of a diatom spring-bloom

“…Asterionella was present in low numbers (maximum 14 cells ml À 1 ) and parasitized at low levels (maximum prevalence 15%). The 2009 and 2010 spring-blooms (Figures 1b and c) showed more typical population maxima (2009: 530 cells ml À 1 ; and 2010: 264 cells ml À 1 ) and were followed by high prevalence epidemics (maximum prevalence 2009: 77% and 2010: 80%) (Ibelings et al, 2011). The AFLP analysis yielded on average 32.0 ± 2.2 marker bands per primer pair (128 marker bands; 87.5% polymorphism).…”

“…In Lake Maarsseveen (The Netherlands), the diatom Asterionella formosa Hassall regularly forms springblooms, which are followed by high prevalence parasite epidemics of its fungal parasite, the chytrid Zygorhizidium planktonicum Canter (Van Donk and Ringelberg, 1983;Ibelings et al, 2011). The Asterionella population is genetically very diverse (De Bruin et al, 2004) even though it is presumed to reproduce (predominantly) clonally.…”