Chytrid infections of Daphnia pulicaria: development, ecology, pathology and phylogeny of Polycaryum laeve

Abstract

SUMMARY1. We combined ecological surveys, life table studies, microscopy and molecular sequencing to determine the development, ecology, pathology and phylogeny of Polycaryum laeve, an endoparasite of cladocerans. We report the first records of P. laeve from North America, where we have used a polymerase chain reaction primer and microscopic examination to confirm infections in 14 lakes. Infections are highly pathogenic and caused increased mortality, reduced growth, and reproductive castration in Daphnia pulicaria during life table studies. 2. Biweekly data from Allequash Lake (Wisconsin, U.S.A.) throughout 2003 indicated that fecundity and infection prevalence were inversely correlated. Infection prevalence was highest in late winter and early spring (up to 80%) and lowest during late summer. Epidemics were generally followed by sharp declines in host population density (up to 99%). 3. Within the haemocoel of its host, P. laeve forms thick-walled sporangia, which occur systemically in later stages of infection. Fungal thalli associate closely with muscle fibres and connective tissue, leading to degeneration as the infection becomes advanced. Following death of the host, flagellated zoospores are released through an exit papilla on the sporangium. Based on the infection-induced castration of the host and increases in infection prevalence with Daphnia size, we postulate that transmission is horizontal, but may be indirect through an additional host or free-living stage. 4. Molecular and morphological data clearly indicate that P. laeve belongs in the fungal phylum Chytriodiomycota, order Blastocladiales. Based on ribosomal RNA gene sequences and morphological features, we transfer the genus Polycaryum from the Haplosporidia to the Chytridiomycota, and designate a lectotype and epitype for P. laeve. Considering the high prevalence of P. laeve infection within Daphnia populations, the frequency with which we detected infections among lakes, and the keystone importance of large-bodied Daphnia in aquatic food webs, we suggest that P. laeve may exert a regulatory influence on Daphnia populations in lake ecosystems.

Challenges in modelling complexity of fungal entomopathogens in semi-natural populations of insects

“…These principles were established using models in which, quite deliberately, the host was not influenced by any other form of population regulation, including intraspecific density dependence. The features of the hostpathogen interaction that resulted in population cycles included the density dependent nature of horizontal transmission which is well recorded for fungal entomopathogens (Johnson et al 2006;Thomas et al 1995), and the persistent nature of the external infectious stages (Baverstock et al 2008;Weseloh and Andreadis 1997; Table 1). The density dependence of horizontal transmission ensures that the prevalence of the fungus in susceptible hosts rises as host population density rises, so checking the exponential growth of the host population.…”

“…There is no doubt that such studies have provided fundamental information on the host-fungus relationship. However, there are still profound gaps in our understanding of their ecology particularly in semi-natural or minimally managed systems both in terrestrial and aquatic environments (Johnson et al 2006;Stentiford et al 2001;Roy and Cottrell 2008;Roy et al 2009). The role of pathogens as natural enemies of non-pest insects, including those of conservation value, is seldom considered beyond their context as 'non-targets' of microbial control agents ).…”

Evidence for limited microbial transfer of methane in a planktonic food web

“…Although caveats exist when considering PCR-based techniques, these approaches have been successfully used to characterize parasites of Daphnia (e.g. Johnson et al 2006) and potential MOB symbionts of Chironomus plumosus .…”

“…Although caveats exist when considering PCR-based techniques, these approaches have been successfully used to characterize parasites of Daphnia (e.g. Johnson et al 2006) and potential MOB symbionts of Chironomus plumosus .A CH 4 -oxidizing symbiont is an alternative explanation for the observed depletion of zooplankton δ 13 C relative to their prey (Lennon et al 2006). Strong symbiotic relationships between MOB and invertebrates have been documented at marine hydrocarbon seeps (Childress et al 1986, Schmaljohann et al 1990).…”

Aquatic Fungi

“…The most impressive example for interspecies relationships with high impact for general fungal biodiversity considerations stems from members of Arthropoda. Theoretically, one single animal can simultaneously provide microhabitats for several aquatic fungi (not including saprophytic or coprophagous fungi): host muscle cells as habitat for intracellular parasites of Microsporidia (Ebert, 1995;Messick et al, 2004); in the host tissue yeasts can be found (Ebert et al, 2004); and in the haemocoel occasionally detrimental Chytridiomycetes occur (Johnson et al, 2006). Moreover, an obligate endoparasite of Entomophthorales (Sparrow, 1960) and likely a represantative of Coelomomycetes (Whisler et al, 1975) can be found and the animal's gut hosts yeasts and symbiotic species of Harpellales (trichomycetes; Strongman & White, 2008).…”