The alternate role of direct and environmental transmission in fungal infectious disease in wildlife: threats for biodiversity conservation

Abstract

Emerging fungal pathogens have substantial consequences for infected hosts, as revealed by the global decline of amphibian species from the chytrid fungus. According to the “curse of the Pharaoh” hypothesis, free-living infectious stages typical of fungal pathogens lengthen the timespan of transmission. Free-living infectious stages whose lifespan exceeds the infection time of their hosts are not constrained by virulence, enabling them to persist at high levels and continue transmitting to further sensitive hosts. Using the only Mesomycetozoea fungal species that can be cultured, Sphaerothecum destruens, we obtained tractable data on infectivity and pathogen life cycle for the first time. Here, based on the outcomes of a set of infectious trials and combined with an epidemiological model, we show a high level of dependence on direct transmission in crowded, confined environments and establish that incubation rate and length of infection dictate the epidemic dynamics of fungal disease. The spread of Mesomycetozoea in the wild raise ecological concerns for a range of susceptible species including birds, amphibians and mammals. Our results shed light on the risks associated with farming conditions and highlight the additional risk posed by invasive species that are highly abundant and can act as infectious reservoir hosts.

The rise of the rosette agent in Europe: An epidemiological enigma

“…The bimodal transmission of S. destruens (i.e. environmental/direct) has been shown using a Susceptible‐exposed‐infectious‐recovered model (SEIR) to increase its risk of emergence and persistence (Al‐Shorbaji, Gozlan, Roche, Britton, & Andreou, ; Al‐Shorbaji et al., , ). After the introduction of S. destruens in the wild, the predicted pattern of mortality suggests an initial rapid decline in local fish communities as empirically observed at site level by Gozlan et al.…”

“…In natural communities, it is expected that shoaling species (e.g., sunbleak Leucaspius delineatus ) would experience higher levels of mortality compared to solitary species (e.g., carp Cyprinus carpio ), as hosts would be closely grouped in large numbers, allowing both direct and environmental transmission to take place. Solitary species and those at low densities would more likely demonstrate chronic decline from environmental transmission (Al‐Shorbaji et al., ). This shows that to fully understand S. destruens ’ emergence, it is important to take into account a whole range of site specific parameters such as local environmental conditions, fish community structure, competitive interactions between species and fish species resistance to infection.…”

Impact of the invasive alien topmouth gudgeon (Pseudorasbora parva) and its associated parasite Sphaerothecum destruens on native fish species

“…Sphaerothecum destruens lives as intracellular spores within its host that are released into the water via the host's urine, bile or gut epithelium. Here it forms active, uniflagellate zoospores that can infect other hosts (Arkush et al 2003;Andreou 2010;Al-Shorbaji et al 2015). Sphaerothecum destruens tolerates a wide range of temperatures (Andreou et al 2009) and can survive up to 26 days as a zoospore at 4°C.…”

“…An increasing number of studies showed that S. destruens negatively impacts local native fish populations in Europe (Gozlan et al 2009;Andreou 2010;Peeler et al 2011;Andreou et al 2012;Ercan et al 2015). Abramis brama, Rutilus rutilus and L. delineatus, all species native to Western Europe, are highly susceptible to infection by S. destruens (Al-Shorbaji et al 2015). However, the impact of P. parva or S. destruens on abundance, body condition and reproduction of native fish in situ are poorly known.…”

First report of the intracellular fish parasite Sphaerothecum destruens associated with the invasive topmouth gudgeon (Pseudorasbora parva) in France

“…More recent studies have also reported infections in cyprinids (sunbleak, Leucaspius delineatus; bream, Abramis brama; carp, Cyprinus carpio; roach, Rutilus rutilus) (Gozlan et al, 2009). Given its potential to infect diverse other species, S. destruens has become a major worldwide threat for fish biodiversity (Arkush et al, 2003;Al-Shorbaji et al, 2015). Although many cyprinids are highly susceptible to S. destruens infection, the topmouth gudgeon (Pseudorasbora parva) is a healthy carrier of the parasite.…”